Root Cause Analysis
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*Corresponding author: Dr. Riffat Mehboob, Department of Biomedical Sciences, King Edward Medical University, Lahore, Pakistan.
E-mail: [email protected] Peer review under responsibility of Hainan Medical University. a Present address: Neurobiology sector, SISSA, Trieste, Italy.
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Nosocomial infections and their control strategies
Hassan Ahmed Khan1, Aftab Ahmad2, Riffat Mehboob3,4,a*
1University of Lahore, Lahore, Pakistan
2National Academy of Young Scientists (NAYS), University of the Punjab, Lahore, Pakistan
3Department of Biomedical Sciences, King Edward Medical University, Lahore, Pakistan
4Department of Neuroscience, SISSA, Trieste, Italy
ARTICLE INFO
Article history: Received 9 Mar 2015 Received in revised form 30 Mar 2015 Accepted 26 Apr 2015 Available online 16 June 2015
Keywords: Hospital-acquired infection Antibiotics Control strategies Surveillance
A B S T R A C T
Nosocomial infections are also known as hospital-acquired/associated infections. Na- tional Healthcare Safety Network along with Centers for Disease Control for surveillance has classified nosocomial infection sites into 13 types with 50 infection sites, which are specific on the basis of biological and clinical criteria. The agents that are usually involved in hospital-acquired infections include Streptococcus spp., Acinetobacter spp., enterococci, Pseudomonas aeruginosa, coagulase-negative staphylococci, Staphylo- coccus aureus, Bacillus cereus, Legionella and Enterobacteriaceae family members, namely, Proteus mirablis, Klebsiella pneumonia, Escherichia coli, Serratia marcescens. Nosocomial pathogens can be transmitted through person to person, environment or contaminated water and food, infected individuals, contaminated healthcare personnel's skin or contact via shared items and surfaces. Mainly, multi-drug-resistant nosocomial organisms include methicillin-resistant Staphylococcus aureus, vancomycin-resistant enterococci, Pseudomonas aeruginosa and Klebsiella pneumonia, whereas Clostridium difficile shows natural resistance. Excessive and improper use of broad-spectrum anti- biotics, especially in healthcare settings, is elevating nosocomial infections, which not only becomes a big health care problem but also causes great economic and production loss in the community. Nosocomial infections can be controlled by measuring and comparing the infection rates within healthcare settings and sticking to the best healthcare practices. Centers for Disease Control and Prevention provides the methodology for surveillance of nosocomial infections along with investigation of major outbreaks. By means of this surveillance, hospitals can devise a strategy comprising of infection control practices.
1. Introduction
“Nosocomial” term is used for any disease acquired by pa- tient under medical care [1]. It is an infection acquired by patient during hospital stay. Recently, a new term, “healthcare associated infections” is used for the type of infections caused by prolonged hospital stay and it accounts for a major risk factor for serious health issues leading to death [2]. About 75% of the burden of these infections is present in developing
countries [3]. Asymptomatic patients may be considered infected if these pathogens are found in the body fluids or at a sterile body site, such as blood or cerebrospinal fluid [4]. Infections that are acquired by hospital staff, visitors or other healthcare personnel may also be considered as nosocomial [5].
The situations in which infections are not believed as noso- comial are: (1) The infections that were present at the time of admission and become complicated, nevertheless pathogens or symptoms change resulting to a new infection; (2) The in- fections that are acquired trans-placentally due to some diseases like toxoplasmosis, rubella, syphilis or cytomegalovirus and appear 48 h after birth [6].
Hospital-acquired infections appeared before the origination of hospitals and became a health problem during the miraculous antibiotic era. Due to these infections, not only the costs but also
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Hassan Ahmed Khan et al./Asian Pac J Trop Biomed 2015; 5(7): 509–514510
the use of antibiotics increased with an extended hospitalization. This resulted in elevated morbidity and mortality. Studies con- ducted in different parts of the world show that in North America and Europe 5%–10% of all hospitalizations result in nosocomial infections, while Latin America, Sub-Saharan Africa and Asia show more than 40% hospitalizations with nosocomial infections [7].
Nosocomial infections can be caused by any organisms but few organisms are particularly responsible for hospital-acquired infections. In this review article, a brief overview on different aspects of nosocomial infections, particularly sites of infections, common nosocomial bacterial agents, selected antibiotic- resistant pathogens along with their modes of transmission and control measures will be discussed.
2. Types of nosocomial infections
National Healthcare Safety Network with Center for Disease Control (CDC) for surveillance has classified nosocomial infec- tion sites into 13 types, with 50 infection sites, which are specific on the basis of biological a nd clinical criteria. The sites which are common include urinary tract infections (UTI), surgical and soft tissue infections, gastroenteritis, meningitis and respiratory in- fections [8]. A change regarding nosocomial infection sites can be easily detected with time due to the elevated use of cancer chemotherapy, advancement in organ transplantation, immunotherapy and invasive techniques for diagnostic and therapeutic purposes. The perfect example of this can be seen in the case of pneumonia as prevalence of nosocomial pneumonia increased from 17% to 30% during five years [9].
3. Agents of nosocomial infections
Nosocomial infections are caused by many microbes and each one can cause infection in healthcare settings. Bacteria are responsible for about ninety percent infections, whereas pro- tozoans, fungi, viruses and mycobacteria are less contributing compared to bacterial infections [10]. The agents that are usually involved in hospital-acquired infections include Streptococcus spp., Acinetobacter spp., enterococci, Pseudomonas aeruginosa (P. aeruginosa), coagulase-negative staphylococci, Staphylo- coccus aureus (S. aureus), Bacillus cereus (B. cereus), Legionella and Enterobacteriaceae family members including Proteus mira- blis, Klebsiella pneumonia (K. pneumonia), Escherichia coli (E. coli), Serratia marcescens. Out of these enterococci, P. aeruginosa, S. aureus and E. coli have a major role [11]. UTI usually contain E. coli, while it is uncommon in other infection sites. Contrarily, S. aureus is frequent at other body sites and rarely causes UTI. In blood-borne infections, coagulase-negative S. aureus is the main causative agent. Surgical-site infections contain Enterococcus spp. which is less prevalent at respiratory tract. One tenth of all infections are caused by P. aeruginosa, which is evenly distributed to the entire body sites [4].
Excessive and improper use of broad-spectrum antibiotics, especially in healthcare settings, are elevating nosocomial in- fections. Penicillin-resistant pneumococci, multi-drug-resistant tuberculosis, methicillin-resistant S. aureus (MRSA), vancomycin-resistant S. aureus are common examples of drug- resistant bacteria. The distribution of bacteria in nosocomial infections is changing over time. For example, Proteus spp., Klebsiella spp. and Escherichia spp. were responsible for
nosocomial infections in the 1960s, but from 1975 to 1980s, Acinetobacter spp. with P. aeruginosa created clinical diffi- culties [12]. During the recent years, streptococci along with coagulase-negative staphylococci and coagulase-positive staph- ylococci reemerged and incidence level of K. pneumonia and E. coli declined from 7% to 5% and 23%–16%, respectively [13].
4. Bacteriology of commonly isolated nosocomial pathogens
A multicenter study was conducted in Japan to isolate bac- teria from surgical infections during 2011–2012. About 785 strains including 31 of Candida spp. were isolated from 204 out of 259 surgical patients. About 523 strains were isolated from primary infections and 231 from surgical site infection. From primary infections, anaerobic Gram-negative bacteria were prevalent. Enterococcus spp. was the highest among Gram- positive aerobic bacteria followed by Streptococcus and Staph- ylococcus spp. E. coli was the predominant form among the Gram-negative aerobic bacteria followed by K. pneumonia, P. aeruginosa and Enterobacter cloacae [14].
4.1. S. aureus
Out of many species of Staphylococcus genus, S. aureus is considered one of the most important pathogens, responsible for nosocomial infections. It is Gram-positive cocci, non-spore forming, catalase- and coagulase-positive, immotile, faculta- tively anaerobe [15]. It is not only a disease-causing organism but also plays its role as commensal. It mainly colonizes in nasal passages. About 20% individuals have persistent colonization of S. aureus, whereas 30% are intermittent. Hospitalized patients with decreased immunity and immunocompetent people in community are more prone to S. aureus infections. S. aureus infects not only the superficial but also the deep tissues and local abscess lesion. Toxin-mediated diseases of S. aureus include food poisoning, due to ingestion of enterotoxins, while toxic shock syndrome toxin 1 is responsible for toxic shock syndrome [16] and exfoliative toxins cause staphylococcal scalded skin syndrome. Virulence mechanisms of S. aureus include toxins, enzymes and immune modulators [15].
4.2. E. coli
E. coli is an emerging nosocomial pathogen causing prob- lems in health care settings [17]. E. coli is Gram-negative and oxidase-negative facultative anaerobe bacteria. It can colonize in gastrointestinal tract of human beings and other animals. E. coli is responsible for a number of diseases including UTI, septi- cemia, pneumonia, neonatal meningitis, peritonitis and gastro- enteritis. Virulence factors meant for its pathogenicity are endotoxins, capsule, adhesions and type 3 secretion systems [18]. Specialized virulence factors are seen in case of UTI and gastroenteritis.
4.3. Vancomycin-resistant enterococci
Enterococci is the second leading cause of hospital acquired infections worldwide and the main leading cause in United States contributing 20%–30% of infections. These are facultative anaerobic Gram-positive enteric microbes [19]. They are a part of
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normal microbiota in female genital tract and gastrointestinal tract as well. Enterococci are involved in the blood-borne in- fections; UTI and wound infections consort to surgical pro- cedures [20]. Virulence factors include extracellular surface proteins, cytolysin, adhesions, hemolysins, gelatinase, extracellular superoxide and aggregation substances [21].
4.4. K. pneumonia
Three to seven percent of hospital-acquired bacterial in- fections are related to K. pneumonia, which is the eighth sig- nificant pathogen in healthcare settings. It is a Gram-positive bacillus and an opportunistic bacterium, which is a part of Enterobacteriaceae family. It usually colonizes gastrointestinal tract, pharynx and skin. It gets involved in diseases such as neonatal septicaemia, pneumonia, wound infections and septi- cemia. Its virulence factors include endotoxins, cell wall re- ceptors and capsular polysaccharide [22].
4.5. P. aeruginosa
P. aeruginosa contributes to 11% of all nosocomial in- fections, which result in high mortality and morbidity rates. It is non-fermenter Gram-negative organism causing diseases espe- cially among immune-compromised people. The sites of colo- nization are kidney, urinary tract and upper respiratory tract. It is a cause of surgical and wound infections, UTI, pneumonia, cystic fibrosis and bacteremia. Some of important virulence factors are adhesions, hemolysins, exotoxins, proteases and siderophores [23].
4.6. Clostridium difficile (C. difficile)
C. difficile is an important nosocomial pathogen which mainly causes diarrhea. Several cases of C. difficile are reported in Europe, U.S. and Canada. It is a Gram-positive bacillus. It is anaerobic and spore-forming bacteria. It usually colonizes in intestinal tract and serves as part of normal microbiota [24]. Diseases caused by toxins produced by C. difficile are colitis and it is responsible for 15%–25% cases of diarrhea. Major virulence factors for C. difficile are toxins, fimbriae, capsule and hydrolytic enzymes [25].
5. Modes of transmission
5.1. S. aureus
Transmission of S. aureus is through infected individuals’ skin or contact via shared items and surfaces like door handles, benches, towels and taps.
5.2. E. coli
E. coli can be transmitted through person to person, envi- ronment or contaminated water and food [17].
5.3. Vancomycin-resistant enterococci
Patients with diarrhea are common means of transmission. Their room items such as surfaces and equipments act as res- ervoirs. This bacterium can survive on theses surfaces for days
or weeks and become a source of contamination for healthcare individuals and other patients [21].
5.4. K. pneumonia
In hospital settings, K. pneumonia can be transmitted by person-to-person contact and especially when healthcare pro- fessionals do not wash or clean hands after checking a contaminated patient. Respiratory machines, catheters or exposed wounds can be the source of its transmission. K. pneumoniae is reported to be transmitted through stool (77%), patients’ hands (42%) and pharynx (19%) [22].
5.5. P. aeruginosa
Common reservoirs for its contamination include breast pumps, incubators [26], sinks and hands of hospital staff and hand soaps [27].
5.6. C. difficile
Spores of C. difficile can hold for months and become a problem for disinfectants and cleaning agents. Inanimate objects and infected intestinal patients are major sites acted as reser- voirs. Hospital staff along with hospital settings are also playing their part to a greater extent [28].
6. Selected antibiotic-resistant nosocomial pathogens
Multi-drug-resistant nosocomial organisms include MRSA, vancomycin-resistant enterococci, P. aeruginosa and K. pneumonia, whereas C. difficile shows natural resistance. In the 1940s, the problem of drug resistance came into light and in the past few years, a rapid increase of multi-drug-resistant pathogens was seen.
Fifty to sixty percent of hospital-acquired infections are caused by resistant pathogens in the United States. Improper use of antibiotics is thought to be the major cause of this drug resistance.
6.1. MRSA
b-Lactamase antibiotics including penicillin along with other antimicrobials became resistant in the 1940s. Resistance of penicillin slowly prevails from hospitals to community due to its improper use. This resistance results are due to the Staphylo- coccal species having penicillinase enzyme which was later solved by the introduction of penicillinase-resistant antibiotics, cephalosporins. In the 1960s, methicillin-resistant species of S. aureus were reported. This resistance was due to the modi- fication of penicillin-binding proteins. This modification made all b-lactam antibiotics along with their derivatives ineffective. Aminoglycosides resistance was another addition to methicillin resistance [29].
6.2. Vancomycin-resistant enterococci
Vancomycin resistance is seen in the enterococcal species due to the vanA and vanB genes. These genes are a part of plasmid and would spread resistance to other microbes as well. Enterococci are resistant to different classes of antibiotics which
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include penicillin, ampicillin, aminoglycosides, tetracyclines, carbapenems, fluoroquinolones and macrolides [30].
6.3. P. aeruginosa
P. aeruginosa is becoming resistant due to different mecha- nisms working against antibiotics. These mechanisms include the restricted uptake of drug, drug modification and altered targets for antibiotics. Due to this increasing resistance, com- plications are seen in the treatment of P. aeruginosa infections. The drugs that are now ineffective due to increasing resistance include cephalosporins, trimethoprim, macrolides, chloram- phenicol, tetracyclines and fluoroquinolones [23].
6.4. K. pneumonia
Resistance to b-lactam antibiotics is a major cause of com- plications in nosocomial infections. K. pneumonia is one of the microbes experiencing resistance of b-lactamase antibiotics along with E. coli. Cephalosporins of third and fourth generation show resistance for K. pneumonia [22].
6.5. C. difficile
Increased use of broad-spectrum antibiotics against C. difficile-associated diseases makes it resistant. Cephalospo- rins, fluoroquinolones, clindamycins and ampicillins are those antimicrobials that are usually employed for C. difficile-associ- ated diseases. Recent studies reported that the improper antibi- otic use was the cause of increasing infections of C. difficile [28].
Figure 1. Measurement and comparison of infection rates.
7. Control of nosocomial infections
There is a lack of actual statistics regarding the causes and antimicrobial susceptibility in developing countries. Pathogens with resistant organisms make it extremely difficult to devise a proper plan and its implementation for control [3].
7.1. Measurement and comparison of infection rates
It is difficult to measure the infection rates in different healthcare settings. For the measurement of infection rates, it is important to know the types of microorganism involved and its correct location inside the body of individual. Infectious or- ganisms are heterogeneous in nature, which makes them different from one another. It is possible that in a hospital, the rates of infection show similarity while the location and het- erogeneity of organisms greatly differ.
To compare the infection rates, one must know the type of healthcare settings, which may be public or private, because the infection rates vary in both types of hospitals. In addition, in these hospitals, the management of infections differs greatly. The types of services that a hospital provides to patients must be taken into account (Figure 1).
7.2. Development of infection control programs
Guidelines for the sterilization and disinfection of invasive devices and medical instruments used for surgeries were developed as the infection rates tend to raise [31,32]. Moreover, guidelines for the prevention of catheter-associated UTI were
Figure 2. Suggested integrated team work for surveillance of nosocomial infections in any hospital.
Hassan Ahmed Khan et al./Asian Pac J Trop Biomed 2015; 5(7): 509–514 513
also devised in 2009 [33]. Lack of compliance with the guidelines, leads to the transmission of nosocomial infections. CDC provides the methodology for surveillance of nosocomial infections along with investigation of major outbreaks. Infection prevention and control guidelines have been developed but the implementation is not yet much known [34]. Training of healthcare professionals, especially nurses, is extremely important for the control and prevention of infection [2,35]. A large gap is present between the existence of guidelines and their actual implementation [36].
7.3. Surveillance of nosocomial infections
Surveillance can be interpreted as “the ongoing, systematic collection, analysis, and interpretation of health data essential to the planning, implementation and evaluation of public health practice, closely integrated with the timely dissemination of these data to those who need to know” [37]. As a part of infection control program, surveillance obliges the data related to infected individuals with their infection sites. Hospitals can work on this data to control the infections by evaluating the efficacy of treatment. By means of this surveillance
(Figure 2), hospitals can devise a strategy comprising of infection control practices [29].
8. Conclusions
In the age of antibiotics, nosocomial infections are still un- controllable. The control of organisms responsible for nosoco- mial infections is much needed as they cause great economic as well as production loss. The transmission of these infections in the hospital settings through healthcare workers can be avoided by the use of infection control practices. Improper and frequent use of antibiotics is an important cause of drug-resistant or- ganisms that are difficult to treat. Hospitals should devise the infection control programs through which infection rates can be compared and controlled. A well-managed surveillance meth- odology is required in the light of CDC guidelines. In addition, there is also great need that the best practice should be shared among hospitals to stop the spread of nosocomial infections.
Conflict of interest
We declare no conflict of interest.
Hassan Ahmed Khan et al./Asian Pac J Trop Biomed 2015; 5(7): 509–514514
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- Nosocomial infections and their control strategies
- 1. Introduction
- 2. Types of nosocomial infections
- 3. Agents of nosocomial infections
- 4. Bacteriology of commonly isolated nosocomial pathogens
- 4.1. S. aureus
- 4.2. E. coli
- 4.3. Vancomycin-resistant enterococci
- 4.4. K. pneumonia
- 4.5. P. aeruginosa
- 4.6. Clostridium difficile (C. difficile)
- 5. Modes of transmission
- 5.1. S. aureus
- 5.2. E. coli
- 5.3. Vancomycin-resistant enterococci
- 5.4. K. pneumonia
- 5.5. P. aeruginosa
- 5.6. C. difficile
- 6. Selected antibiotic-resistant nosocomial pathogens
- 6.1. MRSA
- 6.2. Vancomycin-resistant enterococci
- 6.3. P. aeruginosa
- 6.4. K. pneumonia
- 6.5. C. difficile
- 7. Control of nosocomial infections
- 7.1. Measurement and comparison of infection rates
- 7.2. Development of infection control programs
- 7.3. Surveillance of nosocomial infections
- 8. Conclusions
- Conflict of interest
- References
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Review article http://dx.doi.org/10.1016/j.apjtb.2017.01.019
*Corresponding author: Riffat Mehboob, Biomedical Sciences, King Edward Medical University, Lahore, Pakistan.
E-mail: [email protected] Peer review under responsibility of Hainan Medical University. The journal
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Nosocomial infections: Epidemiology, prevention, control and surveillance
Hassan Ahmed Khan1, Fatima Kanwal Baig2, Riffat Mehboob3*
1Abbottabad University of Science and Technology (AUST), Abbottabad, Pakistan
2National University of Science and Technology (NUST), Islamabad, Pakistan
3Biomedical Sciences, King Edward Medical University, Lahore, Pakistan
ARTICLE INFO
Article history: Received 13 Oct 2016 Accepted 31 Dec 2016 Available online 7 Jan 2017
Keywords: Nosocomial infections Control strategies Hospital acquired infections Pathogens Healthcare
A B S T R A C T
Nosocomial infections or healthcare associated infections occur in patients under medical care. These infections occur worldwide both in developed and developing countries. Nosocomial infections accounts for 7% in developed and 10% in developing countries. As these infections occur during hospital stay, they cause prolonged stay, disability, and economic burden. Frequently prevalent infections include central line-associated blood- stream infections, catheter-associated urinary tract infections, surgical site infections and ventilator-associated pneumonia. Nosocomial pathogens include bacteria, viruses and fungal parasites. According to WHO estimates, approximately 15% of all hospitalized patients suffer from these infections. During hospitalization, patient is exposed to path- ogens through different sources environment, healthcare staff, and other infected patients. Transmission of these infections should be restricted for prevention. Hospital waste serves as potential source of pathogens and about 20%–25% of hospital waste is termed as hazardous. Nosocomial infections can be controlled by practicing infection control programs, keep check on antimicrobial use and its resistance, adopting antibiotic control policy. Efficient surveillance system can play its part at national and international level. Efforts are required by all stakeholders to prevent and control nosocomial infections.
1. Introduction
‘Nosocomial’ or ‘healthcare associated infections’ (HCAI) appear in a patient under medical care in the hospital or other health care facility which was absent at the time of admission. These infections can occur during healthcare delivery for other diseases and even after the discharge of the patients. Addition- ally, they comprise occupational infections among the medical staff [1]. Invasive devices such as catheters and ventilators employed in modern health care are associated to these infections [2].
Of every hundred hospitalized patients, seven in developed and ten in developing countries can acquire one of the healthcare associated infections [3]. Populations at stake are patients in Intensive Care Units (ICUs), burn units, undergoing organ transplant and neonates. According to Extended Prevalence of
Infection in Intensive Care (EPIC II) study, the proportion of infected patients within the ICU are often as high as 51% [4]. Based on extensive studies in USA and Europe shows that HCAI incidence density ranged from 13.0 to 20.3 episodes per thousand patient-days [5].
With increasing infections, there is an increase in prolonged hospital stay, long term disability, increased antimicrobial resistance, increase in socio-economic disturbance, and increased mortality rate. Spare information exists on burden of nosocomial infections because of poorly developed surveillance systems and inexistent control methods. For instance, while getting care for other diseases many patients probably get res- piratory infections and it becomes troublesome to spot the prevalence of any nosocomial infection in continuation of a primary care facility [5]. These infections get noticed only when they become epidemic, yet there is no institution or a country that may claim to have resolved this endemic problem [6].
We have discussed the control strategies of nosocomial in- fections in our previous study [7]. In this review article a brief description about the distribution of these infections across the
nder the CC BY-NC-ND license (http://
Hassan Ahmed Khan et al./Asian Pac J Trop Biomed 2017; 7(5): 478–482 479
globe, emerging causes, brief control methods but more focus on current surveillance will be discussed.
2. Types of nosocomial infections
The most frequent types of infections include central line- associated bloodstream infections, catheter-associated urinary tract infections, surgical site infections and ventilator-associated pneumonia. A brief detail of these is given below:
2.1. Central line-associated bloodstream infections (CLABSI)
CLABSIs are deadly nosocomial infections with the death incidence rate of 12%–25% [8]. Catheters are placed in central line to provide fluid and medicines but prolonged use can cause serious bloodstream infections resulting in compromised health and increase in care cost [9]. Although there is a decrease of 46% in CLABSI from 2008 to 2013 in US hospitals yet an estimated 30,100 CLABSI still occur in ICU and acute facilities wards in US each year [10].
2.2. Catheter associated urinary tract infections (CAUTI)
CAUTI is the most usual type of nosocomial infection glob- ally [11]. According to acute care hospital stats in 2011, UTIs account for more than 12% of reported infections [12]. CAUTIs are caused by endogenous native microflora of the patients. Catheters placed inside serves as a conduit for entry of bacteria whereas the imperfect drainage from catheter retains some volume of urine in the bladder providing stability to bacterial residence [11]. CAUTI can develop to complications such as, orchitis, epididymitis and prostatitis in males, and pyelonephritis, cystitis and meningitis in all patients [12].
2.3. Surgical site infections (SSI)
SSIs are nosocomial infections be fall in 2%–5% of patients subjected to surgery. These are the second most common type of nosocomial infections mainly caused by Staphylococcus aureus resulting in prolonged hospitalization and risk of death [13]. The pathogens causing SSI arise from endogenous microflora of the patient. The incidence may be as high as 20% depending upon procedure and surveillance criteria used [14].
2.4. Ventilator associated pneumonia (VAP)
VAP is nosocomial pneumonia found in 9–27% of patients on mechanically assisted ventilator. It usually occurs within 48 h after tracheal incubation [15]. 86% of nosocomial pneumonia is associated with ventilation [16]. Fever, leucopenia, and bronchial sounds are common symptoms of VAP [17].
3. Nosocomial pathogens
Pathogens responsible for nosocomial infections are bacteria, viruses and fungal parasites. These microorganisms vary depending upon different patient populations, medical facilities and even difference in the environment in which the care is given.
3.1. Bacteria
Bacteria are the most common pathogens responsible for noso- comial infections. Some belong to natural flora of the patient and causeinfectiononlywhentheimmunesystemofthepatientbecomes prone to infections. Acinetobacter is the genre of pathogenic bacteria responsible for infections occurring in ICUs. It is embedded in soil and water and accounts for 80% of reported infections [18]. Bacteroides fragilis is a commensal bacteria found in intestinal tract and colon. It causes infections when combined with other bacteria [19]. Clostridium difficile cause inflammation of colon leading to antibiotic-associated diarrhea and colitis, mainly due to eliminationofbeneficialbacteriawiththatofpathogenic.C.difficileis transmittedfromaninfectedpatienttoothersthroughhealthcarestaff via improper cleansed hands [19]. Enterobacteriaceae (carbapenem- resistance) cause infections if travel to other body parts from gut; where it is usually found. Enterobacteriaceae constitute Klebsiella species and Escherichia coli. Their high resistance towards carbapenem causes the defense against them more difficult [20]. Methicillin-resistant S. aureus (MRSA) transmit through direct contact, open wounds and contaminated hands. It causes sepsis, pneumonia and SSI by travelling from organs or bloodstream. It is highly resistant towards antibiotics called beta-lactams [20].
3.2. Viruses
Besides bacteria, viruses are also an important cause of noso- comial infection. Usual monitoring revealed that 5% of all the nosocomial infections are because of viruses [21]. They can be transmitted through hand-mouth, respiratory route and fecal-oral route [22]. Hepatitis is the chronic disease caused by viruses. Healthcare delivery can transmit hepatitis viruses to both patients and workers. Hepatitis B and C are commonly transmitted through unsafe injection practices [20]. Other viruses include influenza, HIV, rotavirus, and herpes-simplex virus [22].
3.3. Fungal parasites
Fungal parasites act as opportunistic pathogens causing noso- comial infections in immune-compromised individuals. Aspergillus spp. can cause infections through environmental contamination. Candida albicans, Cryptococcus neoformans are also responsible for infection during hospital stay [22]. Candida infections arise from patient's endogenous microflora while Aspergillus infections are caused by inhalation of fungal spores from contaminated air during construction or renovation of health care facility [23].
4. Epidemiology of nosocomial infections
Nosocomial infection affects huge number of patients glob- ally, elevating mortality rate and financial losses significantly. According to estimate reported of WHO, approximately 15% of all hospitalized patients suffer from these infections [23]. These infections are responsible for 4%–56% of all death causes in neonates, with incidence rate of 75% in South-East Asia and Sub-Saharan Africa [1]. The incidence is high enough in high income countries i.e. between 3.5% and 12% whereas it varies between 5.7% and 19.1% in middle and low income countries. The frequency of overall infections in low income countries is three times higher than in high income countries whereas this incidence is 3–20 times higher in neonates [24].
Hand hygiene
Waste mangement
Contact precautions Droplet precautions Airborne precautions
Standard precautions
Immunization/vaccination
Education and training of healthcare staff
Transmission based precautions
Respiratory hygiene Personal protective equipment Injection safety Medication storage and handling
Cleaning and disifection (devices, environmental surfaces)
Figure 1. Infection control program.
Hassan Ahmed Khan et al./Asian Pac J Trop Biomed 2017; 7(5): 478–482480
5. Determinants
Risk factors determining nosocomial infections depends upon the environment in which care is delivered, the suscepti- bility and condition of the patient, and the lack of awareness of such prevailing infections among staff and health care providers.
5.1. Environment
Poor hygienic conditions and inadequate waste disposal from health care settings.
5.2. Susceptibility
Immunosupression in the patients, prolonged stay in inten- sive care unit, and prolonged use of antibiotics.
5.3. Unawareness
Improper use of injection techniques, poor knowledge of basic infection control measures, inappropriate use of invasive devices (catheters) and lack of control policies [25]. In low income countries these risk factors are associated with poverty, lack of financial support, understaffed health care settings and inadequate supply of equipments [5].
6. Reservoirs and transmission
6.1. Microflora of patient
Bacteria belonging to the endogenous flora of the patient can cause infections if they are transferred to tissue wound or sur- gical site. Gram negative bacteria in the digestive tract cause SSI after abdominal surgery.
6.2. Patient and staff
Transmission of pathogens during the treatment through direct contacts with the patients (hands, saliva, other body fluids etc.) and by the staff through direct contact or other environ- mental sources (water, food, other body fluids).
6.3. Environment
Pathogens living in the healthcare environment i.e. water, food, and equipments can be a source of transmission. Transmission to other patient makes one more reservoir for uninfected patient [22].
7. Prevention of nosocomial infection
Being a significant cause of illness and death, nosocomial infections need to be prevented from the base line so that their spread can be controlled.
7.1. Transmission from environment
Unhygienic environment serves as the best source for the pathogenic organism to prevail. Air, water and food can get contaminated and transmitted to the patients under healthcare delivery. There must be policies to ensure the cleaning and use of cleaning agents on walls, floor, windows, beds, baths, toilets
and other medical devices. Proper ventilated and fresh filtered air can eliminate airborne bacterial contamination. Regular check of filters and ventilation systems of general wards, operating the- atres and ICUs must be maintained and documented. Infections attributed to water are due to failure of healthcare institutions to meet the standard criteria. Microbiological monitoring methods should be used for water analysis. Infected patients must be given separate baths. Improper food handling may cause food borne infections. The area should be cleaned and the quality of food should meet standard criteria [22].
7.2. Transmission from staff
Infections can be transferred from healthcare staff. It is the duty of healthcare professionalstotakerole ininfection control. Personal hygiene is necessary for everyone so staff should maintain it. Hand decontamination is required with proper hand disinfectants after being in contact with infected patients. Safe injection practices and sterilized equipments should be used. Use of masks, gloves, head covers or a proper uniform is essential for healthcare delivery [22].
7.3. Hospital waste management
Waste from hospitals can act as a potential reservoir for path- ogens that needs proper handling. 10–25% of the waste generated by healthcare facility is termed as hazardous. Infectious healthcare waste should be stored in the area with restricted approach. Waste containing high content of heavy metals and waste from surgeries, infected individuals, contaminated with blood and sputum and that of diagnostic laboratories must be disposed off separately. Healthcare staff and cleaners should be informed about hazards of the waste and it's proper management [22].
8. Control of nosocomial infections
Despite of significant efforts made to prevent nosocomial infections, there is more work required to control these in- fections. In a day, one out of 25 hospital patients can acquire at least a single type of nosocomial infection [26].
8.1. Infection control programs
Healthcare Institutes should devise control programs against these infections. Administration, workers and individuals admitted or visiting hospital must take into account such pro- grams to play their role in prevention of infections. An efficient infection control program is shown in Figure 1 [22].
Identify Infected Patients
Collecting Risk Factor Data
Attack Rate
Infection Rate
Incidence Rate
Lab Based Results
Priority Oriented
Unit Oriented
Site Oriented
Incidence
Prevalence
Active
Targeted Hight Risk Unit Assessment
Specific lssue of Concem
Host Protection
Agent Destruction
Infection Prevention
Risk Adjusted Rates for Comparisons
Appropriately Trained Investigators
Figure 2. Organization for efficient surveillance [21].
Hassan Ahmed Khan et al./Asian Pac J Trop Biomed 2017; 7(5): 478–482 481
9. Antimicrobial use and resistance
Microbes are the organisms too small to be seen with the eyes, yet they are found everywhere on earth. Antimicrobial drugs are used against the microbes which are pathogenic to- wards living organisms. Antimicrobial resistance occurs when the microbes develop the ability to resist the effects of drugs; they are not killed and their growth does not stop.
9.1. Appropriate antimicrobial use
Antibiotics are greatly used to cure illness. Antimicrobial use should justify the proper clinical diagnosis or an infection causing microorganism. The Centers for Disease Control and Prevention (CDC) estimates that each year about 100 million courses of antibiotics are prescribed by office-based physicians, while approximately 50% of those are unnecessary [27]. The selection of antimicrobials should be based upon the patient's tolerance in addition to the nature of disease and pathogen. The aim of antimicrobial therapy is to use a drug that is selectively active against most likely pathogen and least likely to cause resistance and adverse effects [22]. Antimicrobial prophylaxis should be used when it is appropriate i.e. prior to surgery, to reduce postoperative incidence of surgical site infections. In case of immunocompromised patients, prolonged prophylaxis is used until immune markers are reinstate [28].
9.2. Antibiotic resistance
Antibiotic resistance is responsible for the death of a child every five minutes in South-East Asia region. Drugs that were used to treat deadly diseases are now losing their impact due to emerging drug resistant microorganisms [29]. Self medication with antibiotics, incorrect dosage, prolonged use, lack of standards for healthcare workers and misuse in animal husbandry are the main factors responsible for increase in resistance. This resistance threatens the effective control against bacteria that causes UTI, pneumonia and bloodstream infections. Highly resistant bacteria such as MRSA or multidrug-resistant Gram-negative bacteria are the cause of high incidence rates of nosocomial infections worldwide [30]. South-East Asian region reports reveal that there a high resis- tance in E. coli and K. pneumoniae for third generation cepha- losporin and more than quarter of S. aureus infections are methicillin resistant [31]. “Immediate action is needed to stop the world from heading towards pre-antibiotic era in which all achievements made in prevention and control of communicable diseases will be reversed”, said Dr Poonam Khetrapal Singh, Regional Director of WHO South-East Asia Region [32].
9.3. Antibiotic control policy
The worldwide pandemic of antibiotic resistance shows that it is driven by overuse and misuse of antibiotics, which is a threat to prevent and cure the diseases. WHO's global report on antibiotic resistance, preventing the infection from happening by better hygiene, clean water, and vaccination to reduce the need of antibiotics. The development of new diagnostics and other tools is required in healthcare institutes to stay ahead of evolving resistance. Pharmacists should play their role of prescribing the
right antibiotic when truly needed and policymakers should foster cooperation and information among all stakeholders [31].
10. Surveillance of nosocomial infection
Although the aim of infection prevention and control pro- gram is to eradicate nosocomial infections but epidemiological surveillance for demonstration of performance improvement is still required to accomplish the aim. The efficient surveillance methods include data collection from multiple sources of in- formation by trained data collectors; information should include administrative data, demographic risk factors, patients' history, diagnostic tests, and validation of data. Following the data extraction, analysis of the collected information should be done which includes description of determinants, distribution of in- fections, and comparison of incidence rates. Feedback and re- ports after analysis should be disseminated by infection control committees, management, and laboratories keeping the confi- dentiality of individuals. The evaluation of credibility of sur- veillance systems is required for effective implementations of interventions and its continuity. Finally the undertaking of data at regular intervals for maintenance of efficiency of surveillance systems should be made compulsory [22]. Efficient methodology for appropriate surveillance approach is given in Figure 2.
11. Conclusion
With increased burden of nosocomial infections and antimi- crobial resistance, it has become difficult for healthcare adminis- trations and infection control committees to reach the goal for elimination of intervals. However, by practicing sound and healthy ways for care delivery designed by infection control committees, controlling transmission of these infections using appropriate methods for antimicrobial use, the resistance in emerging patho- gens against antimicrobials can be reduced easily. An efficient surveillance method guided by WHO can help healthcare institutes to devise infection control programs. Proper training of hospital staff for biosafety, proper waste management and healthcare re- forms and making general public aware of these endemic in- fections can also help in reduction of nosocomial infections.
Hassan Ahmed Khan et al./Asian Pac J Trop Biomed 2017; 7(5): 478–482482
Conflict of interest statement
We declare that we have no conflict of interest.
References
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- Nosocomial infections: Epidemiology, prevention, control and surveillance
- 1. Introduction
- 2. Types of nosocomial infections
- 2.1. Central line-associated bloodstream infections (CLABSI)
- 2.2. Catheter associated urinary tract infections (CAUTI)
- 2.3. Surgical site infections (SSI)
- 2.4. Ventilator associated pneumonia (VAP)
- 3. Nosocomial pathogens
- 3.1. Bacteria
- 3.2. Viruses
- 3.3. Fungal parasites
- 4. Epidemiology of nosocomial infections
- 5. Determinants
- 5.1. Environment
- 5.2. Susceptibility
- 5.3. Unawareness
- 6. Reservoirs and transmission
- 6.1. Microflora of patient
- 6.2. Patient and staff
- 6.3. Environment
- 7. Prevention of nosocomial infection
- 7.1. Transmission from environment
- 7.2. Transmission from staff
- 7.3. Hospital waste management
- 8. Control of nosocomial infections
- 8.1. Infection control programs
- 9. Antimicrobial use and resistance
- 9.1. Appropriate antimicrobial use
- 9.2. Antibiotic resistance
- 9.3. Antibiotic control policy
- 10. Surveillance of nosocomial infection
- 11. Conclusion
- Conflict of interest statement
- References
RCA Article 1.pdf
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Open Access Full Text Article
http://dx.doi.org/10.2147/IDR.S177247
Health care-associated infections – an overview
Mainul Haque1
Massimo Sartelli2 Judy McKimm3 Muhamad Abu Bakar1
1Faculty of Medicine and Defence Health, Universiti Pertahanan Nasional Malaysia (National Defence University of Malaysia), Kem Sungai Besi, 57000 Kuala Lumpur, Malaysia; 2Department of Surgery, Macerata Hospital, via Santa Lucia 2, 62100 Macerata, Italy; 3Swansea University School of Medicine, Swansea University, Singleton Park, Swansea, wales SA2 8PP, UK
Abstract: Health care-associated infections (HCAIs) are infections that occur while receiving health care, developed in a hospital or other health care facility that first appear 48 hours or more
after hospital admission, or within 30 days after having received health care. Multiple studies
indicate that the common types of adverse events affecting hospitalized patients are adverse
drug events, HCAIs, and surgical complications. The US Center for Disease Control and Pre-
vention identifies that nearly 1.7 million hospitalized patients annually acquire HCAIs while
being treated for other health issues and that more than 98,000 patients (one in 17) die due to
these. Several studies suggest that simple infection-control procedures such as cleaning hands
with an alcohol-based hand rub can help prevent HCAIs and save lives, reduce morbidity, and
minimize health care costs. Routine educational interventions for health care professionals can
help change their hand-washing practices to prevent the spread of infection. In support of this,
the WHO has produced guidelines to promote hand-washing practices among member countries.
Keywords: health care-associated infections, central line-associated bloodstream infections, sur- gical site infections, catheter-associated urinary tract infections, ventilator-associated pneumonia
Background Health care-associated infections (HCAIs) are those infections that patients acquire
while receiving health care.1 The term HCAIs initially referred to those infections linked
with admission to an acute-care hospital (earlier called nosocomial infections), but
the term now includes infections developed in various settings where patients obtain
health care (eg, long-term care, family medicine clinics, home care, and ambulatory
care). HCAIs are infections that first appear 48 hours or more after hospitalization or
within 30 days after having received health care.2 Multiple studies indicate that the
most common types of adverse events affecting hospitalized patients are adverse drug
events, HCAIs, and surgical complications.3–7 The US Center for Disease Control and
Prevention identifies that nearly 1.7 million hospitalized patients annually acquire
HCAIs while being treated for other health issues and that more than 98,000 of these
patients (one in 17) die due to HCAIs.8 The Agency for Health care Research and
Quality reported that HCAIs are the most common complications of hospital care and
one of the top 10 leading causes of death in the USA.9 Out of every 100 hospitalized
patients, seven patients in advanced countries and ten patients in emerging countries
acquire an HCAI.10 Other studies conducted in high-income countries found that
5%–15% of the hospitalized patients acquire HCAIs which can affect from 9% to
37% of those admitted to intensive care units (ICUs).11,12 Multiple research studies
Correspondence: Mainul Haque Faculty of Medicine and Defence Health, Universiti Pertahanan Nasional Malaysia (National Defence University of Malaysia), Kem Sungai Besi, 57000 Kuala Lumpur, Malaysia Mobile +60 10 926 5543 email [email protected]
Journal name: Infection and Drug Resistance Article Designation: Review Year: 2018 Volume: 11 Running head verso: Haque et al Running head recto: Health care-associated infections and prevention strategy DOI: http://dx.doi.org/10.2147/IDR.S177247
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Haque et al
report that in Europe hospital-wide prevalence rates of HCAIs
range from 4.6% to 9.3%.13–21 The WHO reports however that
HCAIs usually receive public attention only when there are
epidemics.22 HCAIs also have impact on critically ill patients
with around 0.5 million episodes of HCAIs being diagnosed
every year in ICUs alone.7,14,23 ICU patients are often in a very
critically ill, immuno-compromised status which increases
their susceptibility to HCAIs.24,25
Brief history There has been long-standing awareness that the practice of
medicine can do harm as well as good. For example, Hip-
pocrates, the father of modern medicine, stated more than
2,500 years ago that “I will use treatments for the benefit of
the ill in accordance with my ability and my judgment, but
from what is to their harm and injustice I will keep them.”26
It was also recognized (eg, by Semmelweis discussing puer-
peral fever) many years ago that coming into hospitals (in
particular) can be dangerous.27 In this century, the idea that
medicine could cause harm, including death is described as
“unintended physical injury resulting from or contributed to
by medical care, including … [its] absence … that requires
additional monitoring, treatment or hospitalization, or …
results in death.”28,29 Offering another perspective, an Ameri-
can natural sciences writer noted that HCAIs are now killing
around 100,000 people, many more than HIV/AIDS, cancer,
or road traffic accidents.30
The Hungarian obstetrician Professor (Dr) Ignaz Phillip
Semmelweis is largely considered as the medical doctor
who realized that health care providers could communicate
disease. His work identified the mode of communication
and spread of puerperal sepsis while working at the Mater-
nity Hospital in Vienna. In 1847, he observed higher rates
of maternal mortality among patients treated by obstetri-
cians and medical students than among those cared for by
midwives. At that time, he also found that a pathologist had
died of sepsis after wounding himself with a scalpel while
carrying out an autopsy on a patient with puerperal sepsis.
The pathologist’s illness mirrored that of women with puer-
peral sepsis, and Semmelweis wrote that both a scalpel and
a physicians’ contaminated hands could transmit organisms
to mothers during labor. He introduced chlorinated lime
hand washing to the obstetric hospital staff, resulting in
large improvements in maternal mortality rates.31 However,
Semmelweis’ theories were dismissed by most of the medi-
cal establishment because of a lack of appropriate statistical
analysis of the data. Nevertheless, after Koch’s postulates
were published in 1890, the germ theory of disease and
Semmelweis’ theory of transmission of disease from doctor
to patient were found to be valid. Semmelweis was therefore
the first to describe an HCAI and provide an intervention to
avert its spread through hand hygiene.32
Prevalence and brief outline of HCAIs A survey conducted in 183 US hospitals with 11,282 patients
reported that 4% of patients had at least one HCAI with the
most common microorganism being Clostridium difficile.
Most infections were surgical site infections (SSIs), pneumo-
nia, and gastrointestinal infections.33 A study 2 years earlier
by the same group found that 6% (51) of patients had suffered
from HCAIs with the top 75.8% acquiring SSIs, urinary tract
infections (UTIs), pneumonia, and bloodstream infections.
Staphylococcus aureus was the most frequently detected
microorganism.34 The group conducted a comparative study
between 2011 and 2015 and found a statistically significant
(P<0.05) reduction of HCAIs in SSIs, UTIs, and central line infections, probably due to a national initiative.35
HCAIs are also problematic elsewhere in the world. For
example, a study in Singapore reported 11.9% (646) patients
with HCAIs, primarily undetermined clinical sepsis, and
pneumonia caused mainly by S. aureus and Pseudomonas
aeruginosa.36 This study also reported that the Acinetobacter
species and P. aeruginosa were extremely resistant to car-
bapenem.36 A recent European study found that 2,609,911
new patients were identified as having HCAIs annually in
the European Union and European Economic Area.37 This
study revealed that for every 20 patients hospitalized, at least
one acquired an HCAI which was preventable.37 Klebsiella
pneumoniae and the Acinetobacter species were exceedingly
resistant to multiple antimicrobials, and the lack of new anti-
microbials increases the huge burden in Europe.37 In Greece,
the HCAI prevalence rate was 9.1%. The frequent types
of HCAIs were lower respiratory tract infections (LRTIs),
bloodstream infections, UTIs, SSIs, and systemic infections.38
One systematic review and meta-analysis regarding HCAIs in
Southeast Asian countries (Brunei, Myanmar, Cambodia, East
Timor, Indonesia, Laos, Malaysia, the Philippines, Singapore,
Thailand, and Vietnam) found an overall prevalence rate of
9.1% with the most common microorganisms being P. aerugi-
nosa, the Klebsiella species, and Acinetobacter baumannii.39
A study conducted in eight university hospitals of Iran
(ranging from 60 to 700 beds) reported an overall HCAI
frequency of 9.4%, the most common HCAIs were blood-
stream infections, SSIs, UTIs, and pneumonia.40 A logistic
regression analysis showed that the odds ratio (OR) for males
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as opposed to females acquiring infections was 1.56 (95%
confidence interval [CI] 1.21–2.02). Additional risk factors
for HCAIs include a central intravascular catheter, adjusted
OR of 3.86 (95% CI 2.38–6.26), and with a urinary catheter,
adjusted OR of 3.06 (95% CI 2.19–4.28). Being admitted to
an ICU is not in itself a self-determining HCAI risk factor.
The OR for all HCAIs of acquiring an infection was 3.24
(95% CI 2.34–4.47) in patients with hospital stays longer
than 8 days.33 Seventy-one percentage (71%) of the studied
patients received antimicrobials, but 9.4% had at least one
evidence of infection.33 Another study revealed that the
average number of microbes ranged from on (9.67×1011), working surfaces (1.64×1012), door handles (1.71×1012), and highest in taps (2.08×1012).41 The highest number (23) of pathogens were isolated from door handles, and the peak
variance of pathogens were on hospital floors (7). Among
those microbes, those that were disease-producing were
46.14%, 53.86% were nonpathogenic, the most common was
S. aureus at 14.42% and 45.2% of the total bacterial isolates
comprised Bacillus subtilis. A study conducted in Ghana
reported that gentamicin was the most effective antibiotic
(100%) on both Gram-positive and Gram-negative organisms,
but of the 12 antibiotics tested (ampicillin, cefuroxime, cotri-
moxazole, cefotaxime, tetracycline, amikacin, gentamicin,
chloramphenicol, cefixime, cloxacillin, and erythromycin),
six were resistant to either Gram-positive or Gram-negative
organisms.41 Most of the HCAIs in the US are triggered by
the ESKAPE group, comprising the antimicrobial-resistant
Gram-negative microorganisms (K. pneumoniae, A. bauman-
nii, P. aeruginosa, and Enterobacter spp.) and the Gram-
positive species, Enterococcus faecium and S. aureus.42–44
Multiple studies report that Gram-negative organisms are
responsible for 10%,45 20%–40%,46 of HCAIs and that anti-
microbial resistance places a significant burden on the global
health care system, particularly in low resource countries.47,48
This problem is exacerbated as research and development
into new antimicrobials targeting Gram-negative organisms
has rapidly decreased in recent years.48
Among the newer aminoglycosides, plazomicin has
been found to be active against the extended-spectrum beta-
lactamase (ESBL) generating strains of Enterobacter spp.,
Escherichia coli, and K. pneumoniae49 and more effective
in laboratory experiments against A. baumannii than genta-
micin, tobramycin, and amikacin.50 Plazomicin has a better
safety profile than other drugs, with no report of damage
to the cochlea, auditory nerve, vestibular, and renal system
in healthy volunteers, even with high and multiple doses.51
Another study found that, in a comparison between HCAIs
due to methicillin-sensitive S. aureus and methicillin-resistant
S. aureus (MRSA), isolates were statistically significantly
(P<0.005) more resistant to ciprofloxacin, clindamycin, trimethoprim/sulfamethoxazole, erythromycin, gentamicin,
and tetracycline.52 Hospital waste, especially contaminated
surgical waste, often acts as a reservoir for pathogenic viru-
lent microorganisms, and it suggested that 20%–25% of the
waste produced by health care outlets is considered to have
high potential to cause HCAIs, it therefore needs appropriate
handling and disposal.53,54
Causative organisms Around 12–17 microorganisms cause 80%–87% of HCAIs:
S. aureus, Enterococcus species (eg, faecalis, faecium), E.
coli, coagulase-negative Staphylococci, Candida species
(eg, albicans, glabrata), K. pneumoniae and Klebsiella
oxytoca, P. aeruginosa, A. baumannii, Enterobacter spe-
cies, Proteus species, Yeast NOS, Bacteroides species, and
other pathogens.45,55,56 Among these pathogens, 16%–20%
include multidrug-resistant (MDR) phenotypes: MRSA,
vancomycin-resistant E. faecium, carbapenem-resistant
P. aeruginosa, extended-spectrum cephalosporin-resistant
K. pneumoniae, K. oxytoca, E. coli, and Enterobacter spe-
cies, and carbapenem-resistant P. aeruginosa, K. pneumoniae/
K. oxytoca, E. coli, Enterobacter species, and A. bauman-
nii.45,55 Some of these Gram-negative microorganisms have
a much higher rate (20%–40%) of resistance than others45
with the organisms isolated from device-associated HCAIs
having the highest antimicrobial resistance phenotypes.56 In
the latter study, although similar to the percentage resistance
for most phenotypes was that in an earlier research study,45 an
upsurge in the scale of the resistance fractions against E. coli
pathogens was observed, especially with fluoroquinolones.56
Acinetobacter, Burkholderia spp. and Pseudomonas spp.
isolates were 100% were 92% resistant to cephalosporins
respectively. Burkholderia spp. was again totally resistant to
fluoroquinolones and Acinetobacter spp. and Pseudomonas
spp. were 94.2% and 95.8% resistant, respectively. The same
study reported that 86.4% Acinetobacter spp. and 62.5%
Pseudomonas spp. showed a high resistance to carbapenems,
the preferred drug regime in ICUs. Carbapenems were found
more effective against Burkholderia spp. with 20% resistance.57
In another study, Enterobacteriaceae community were found
to be completely resistant to third-generation cephalosporins.58
Over 80% of the Klebsiella spp. community were resistant
to ciprofloxacin, gentamicin, piperacillin, tazobactam, and
imipenem showing 48.6% resistance. E. coli was equally
resistant although carbapenems were effective in almost
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80% cases. Although Citrobacter spp.-related HCAIs are a
relatively minor proportion, they also show resistance toward
cephalosporins, fluoroquinolones, and aminoglycosides.58
Another study reported that although the Acinetobacter spp.
were 76.99%–92.01%, resistant to most antimicrobials, only
30% of Acinetobacter spp. isolated were susceptible.59 It can
be seen therefore that the causative pathogenic microorganisms
differ from country to country as does patterns of resistance.
Types of HCAIs Alongside infections due to cross-contamination between
patients and health workers, patients being susceptible to
common infections due to diminished immune responses,
and infections at surgery sites (SSIs), many HCAIs are due
to implants and prostheses. These include central line-associ-
ated bloodstream infections (CLABSIs), catheter-associated
UTIs, and ventilator-associated pneumonia (VAP).57,60,61
CLABSIs CLABSIs substantially increase morbidity, mortality, and
health care costs, and great attention has been paid to
addressing these.62,63 As a consequence, in 2009, 25,000
fewer CLABSIs occurred in the ICUs of US hospitals than
in 2001, a 58% reduction, with about 6,000 lives saved and
estimated financial savings of US$414 million in potential
excess health care costs, although the costs of reducing such
infections is very high.64 It is estimated that it costs ~$1.8 billion between 2001 and 2009 to save an additional 27,000
lives.64 Despite this investment, a considerable number of
CLABSIs still occur, especially in outpatient hemodialysis
centers and inpatient wards.64 Another study also reported
the link between CLABSIs and considerable morbidity and
mortality, although there is a wide variation in reported infec-
tion rates (from 20% to 62.5%) in emerging economies.65
A study conducted in Taiwan reported the occurrence of
CLABSIs as 3.93 per 1,000 central-catheter days.66 The most
common causative pathogens were Gram-negative (39.2%),
Gram-positive (33.2%), and Candida spp. microorganisms
(27.6%).66 In this study, patients developed CLABSIs 8 days
from the time of insertion of the central line catheter.66 Mul-
tivariate analysis showed that a higher Pitt bacteremia score
(OR 1.41; 95% Cl=1.18–1.68) and the prolonged interval between the onset of CLABSIs and catheter removal (OR
1.10; 95% CI=1.02–1.20) were associated with higher death rates.66 Another similar study identified prolonged catheter
in situ, pediatric ICU stay, and intravenous nutrition were
significant prognosticators of peripherally inserted central
catheter-related CLABSIs among hospitalized children.67
SSIs SSIs (formerly termed “wound infections”) are still one of
the most common adverse events that occur in hospitalized
patients undergoing surgery or in outpatient surgical mea-
sures, regardless of the advances in preventive procedures.68
SSI is the most common complication in postoperative surgi-
cal patients, associated with significant morbidity, high death
rates, and financial stress on national budgets and individual
patients.69–71 SSIs are defined as infections arising up to 30–90
days after surgery in patients receiving an organ, group of
cells, or device and affecting both the incisional site and
deeper tissues around the surgery location.72,73
The type of surgery determines the proportion of SSIs.
Between 2% and 36% of patients may develop SSIs, with
the highest risk for orthopedic followed by cardiac and intra-
abdominal surgery.14,72,74,75 The length of hospital stay for
patients with SSIs increases from 4 to 32 days as compared
with patients with no post-surgical infections.76–78 Approxi-
mately 25% of patients with SSIs develop severe sepsis and
shock and are moved to an ICU.65 SSIs cause statistically
significant morbidity, mortality, and financial burdens for
individuals and for communities.69–71,78
HCAIs are common following cardiac surgery, with a
reported incidence rate of between 5.0% and 21.7%,79,80
often accompanied with multiple organ failure and prolonged
hospital stays, leading to increased mortality rates.79,80 The
three most common locations for HCAIs after cardiac surgery
are lungs, central venous catheters, and surgical sites.69 SSIs
followed by cardiac surgery classically present with local-
ized cellulitis (erythema, warmth, and tenderness), purulent
discharge, sternal instability, chest pain, and systemic upset
with deep infections.81–83 SSIs are devastating for orthopedic
patients as it is very difficult to rid the bones and joints of the
infection.83 One Saudi Arabian study reported an incidence of
SSIs in orthopedic patients of 2.55% (79 of 3,096 patients)
with the most common pathogens being Staphylococcus
species including MRSA (29.11%); Acinetobacter species
(21.5%); Pseudomonas species (18.9%), and Enterococcus
species (17.7%).84 Surgical wound contamination potentials,
patients’ clinical conditions, type of surgery, and length of
surgery were variables statistically significantly associated
with SSIs and should be viewed as risk factors.85 The move-
ment and number of staff and the structural features of the
operating theater also affect the incidence of SSIs.85,86 One
study found that 73.33% cases of SSIs following orthopedic
surgery were culture positive, and a total of 35 bacterial
strains were isolated, among which 65.72% were Gram-
positive isolates and 34.28% were Gram-negative bacteria.87
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About 68.6% of all bacterial isolates were resistant to cefu-
roxime used in the management of orthopedic SSIs. This
study also found that diabetes mellitus, smoking, operations
lasting more than 3 hours, the absence of antibiotic prophy-
laxis, and a history of previous surgery were positive risk
factors associated with a significant upsurge in SSIs.87
SSIs comprise at least 14%–22.2% of all HCAIs for
abdominal surgery88–90 and often lead to extended hospital-
ization and higher antimicrobial costs.71 The microorganisms
generally involved in such SSIs include S. aureus, coagulase-
negative Staphylococci and Enterococcus spp., and E. coli.71
S. aureus has been known to be a major cause of HCAIs for
over 100 years.91 When first introduced, nearly all strains were
susceptible to penicillin, but since its wide and often irratio-
nal use, S. aureus started to become resistant by producing
β-lactamase enzyme.91 By 1960, 95% hospital variants of S. aureus were resistant.91,92 To help combat resistance, several
new penicillins were developed to resist Staphylococcal
β-lactamase, such as methicillin, oxacillin, cloxacillin, and flucloxacillin.91 However, within 1 year of methicillin being
marketed in 1960, the first MRSA strain of S. aureus was
reported in England.93 The MRSA strain represents 50% of
HCAIs in the US and Europe and causes infections that are
very difficult to manage because of their potential resistance
to multiple antimicrobials.94–96 In one study, the incidence
of SSIs was after gastrectomy in 11.3%, after colorectal
surgery in 15.5%, after hepatectomy in 11.3%, and after
pancreaticoduodenectomy in 36.9%.97 While the incidence
of SSIs was higher in the absorbable stitching material than
the silk group for all surgical procedures, the difference was
not statistically significant. 97A Japanese study on abdominal
surgery reported an overall SSI rate of 14.4%. The SSI rates
in the suture-less, Vicryl, and silk groups were 4.8%, 14.8%,
and 16.4%,88 respectively, again with no statistically signifi-
cant differences between the groups. In colorectal surgery,
the SSI rate in the polyglactin 910 (absorbable, synthetic,
usually braided suture; VicrylTM) group was 13.9%, which
was statistically significantly lower than that of the silk
group (22.4%; P=0.034). The incidence of deeper SSIs in the Vicryl group, including deep incisional SSIs (ISSIs) and
organ/space SSIs (OSIs), was statistically significantly lower
than that in the silk group (P=0.04).88 The SSI rates did not differ among the suture types overall in gastric surgery or in
appendectomy.98 A US study of pediatric patients found that
while this was only 2.5% of the caseload, colorectal surgery
contributed to 7.1% of the SSIs.98 The SSI rates of all types
of colorectal surgery were 5.9% (ISSIs: 3.2%; OSIs: 2.7%)
with the uppermost being total abdominal colectomy (11.4%)
trailed by partial colectomy (8.3%) and colostomy closure
(5.0%).98 Inflammatory bowel diseases caused the topmost
health problems in a comparison of all colorectal diagnosed
diseases (24.9%; ISSIs: 22%; OSIs: 28.6%). Hirschsprung’s
disease (14.2%; ISSIs: 15.4%; OSIs: 12.8%) and anorectal
malformations (12.4%; ISSIs: 17.6%; OSIs: 6.4%) were the
next major group in colorectal diseases.98 Finally, a study uti-
lizing univariate analysis defined 13 statistically significantly
variables related to SSIs. Those were patients aged over 60
years, lower functional status, diabetes mellitus, congestive
heart failure, immunocompromising disease, anticancer
medications, immunosuppressive agents, impaired immune
system, open cholecystectomy, laparotomy, an American
Society of Anesthesiologists score above 2, drain insertion,
and dirty wound.99 Using multivariate regression analysis,
this study also found that immunosuppressive agents (OR
=2.5, 95%, CI =1.099–143.443), open cholecystectomy (OR =2.25, 95% CI =2.242–40.109), and contaminated wound (OR =2.179, 95% CI =3.80–20.551) were statistically sig- nificantly linked with SSIs.99
Catheter-associated urinary tract infections (CAUTIs) Internationally, UTIs are the most common HCAIs and one
of the top ranking microbial infections, representing around
40% of HCAIs, with significant consequences for morbidity
and mortality and substantial financial implications.14,99,100
Although CAUTIs are typically benign, some patients have
potentially pathogenic virulent bacteria but are asymptom-
atic, and these patients were associated with a three-times
higher mortality than in non-bacteriuric patients.101,102 Multi-
variate analysis indicates the risk factors for CAUTIs includ-
ing prolonging the duration of the catheter, female sex, older
age, diabetes mellitus, the absence of systemic antibiotics,
catheter insertion outside the operating room, and a breach in
the closed system of catheter drainage.101,103 The rate of CAU-
TIs has been estimated to be about 5% per day, regardless of
the duration of the indwelling catheter, with E. coli being the
main infecting pathogenic microorganism, although a wide
spectrum of other microorganisms were identified, including
eukaryotic fungus.104,105 The repetitive inappropriate admin-
istration of antimicrobials often leads to greater bacterial
resistance. CAUTIs habitually lead to biofilm formation on
both the extraluminal and intraluminal portal catheter surface,
largely from extraluminal microorganisms.106–108 The biofilm
defends microbes from both antimicrobials and host defense
mechanisms.109 Although morbidity from CAUTIs with short-
term catheter use is limited if catheters are appropriately
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inserted and cleaned, in patients with long-term indwelling
catheters, fever from CAUTIs is common with a frequency
fluctuating from one per 100 to one per 1,000 catheter days.105
Patients in institutional care with long-term indwelling
catheters have a greater risk for the presence of pathogenic
microorganisms and other urinary tract diseases than those
without catheters.105 One meta-analysis found that CAUTIs
were linked with statistically significantly higher death rates
(OR =1.99; 95% CI =1.72–2.31; P<0.00001; I2=54%; eight studies; 62,063 patients) and days in the ICU (weighted mean
difference of +12 days; 95% CI =9–15; P<0.00001; I2=96%; seven studies; 13,011 patients) and hospital (mean difference
+21 days; 95% CI =11–32; P<0.0001; I2=98%; five studies; 10,183 patients).110 An Australian health care-associated
urinary tract infection (HCAUTI) non-concurrent cohort
study carried out for 4 consecutive years found that patients
had an extra 4 days (95% CI =3.1–5.0 days) of hospitaliza- tion.111 This study further reported that the infection rate was
statistically significantly minimized utilizing a Cox regres-
sion model (HR =0.78; 95% CI =0.73–0.83) when patients were released from the hospital.111 HCAUTIs very rarely
cause death (HR =0.71; 95%CI =0.66–0.75), especially in large hospitals when compared to other health care institutes,
even when compared with age and sex (HR =0.74; 95% CI =0.69–0.78), although elderly patients more often died (HR =1.40; 95% CI =1.38–1.43).111
vAP The death risk for patients in the ICU is not only because
of their original illness but often because of HCAIs.2,54,112
Pneumonia is the second commonest HCAI in ICUs,
affecting more than one-quarter of patients.113,114 Around
86% of HCAIs are associated with motorized automatic
ventilation and VAP.113 Between 9% and 27% of patients
with assisted ventilation develop this kind of pneumonia,
and VAP has been identified internationally as a potential
major cause of death.114 The average critical time to develop
VAP following endotracheal intubation and mechanical
ventilation was 2–3 days.115 Patients usually develop a
fever, altered bronchial sounds, white blood cell counts
reduced, changes in sputum, and causative organisms are
often identified.116–121 A US study found a range of VAP of
between 1.2 and 8.5 per 1,000 ventilator days122 although an
international group reported a much higher occurrence of
VAP of 13.6/1,000 ventilator days.123 In Asian countries, a
different picture of 3.5–46 infections/1,000 ventilator days
emerges,124 with a very high incidence rate in India of 40.1
per 1,000 ventilator days.125 The initial 5 days of mechanical
ventilation is the most critical time for the development of
VAP, with a mean duration of 3.3 days between intubation
and the development of VAP.119–126 Another recent Indian
study reported that non-fermentative Gram-negative
bacilli127 were the predominant organisms, followed by
Pseudomonas and Klebsiella genus. In this study, S. aureus
reduced in prevalence from 50% to 34.9% between 2011
and 2013, but between 2012 and 2013 vancomycin-resistant
Enterococci increased from 4.3% to 8.3%, while methicil-
lin resistance among S. aureus exceeded 50% in 2013. In
addition, an upwavard trend in resistance by Pseudomonas
genus was observed for piperacillin-tazobactam, amikacin,
and imipenem. The incidence of non-fermenters’ resis-
tance continued to be very high except for amikacin and
imipenem (33.1%) and polymyxin-B (2.4%).127 A study at
Chonnam National University Hospital in South Korea of
the transtracheal aspirates or bronchoalveolar lavage of
patients suffering from VAP found that S. aureus (44%)
was the most frequently detected causative microorganism
followed by A. baumannii (30%), P. aeruginosa (12%),
Stenotrophomonas maltophilia (7%), K. pneumoniae (6%),
and Serratia marcescens (2%).128 In addition, S. aureus was
found as MRSA and 69% of Acinetobacter baumannii were
imipenem-resistant.128 No statistically significant variance
was observed in the imipenem-resistant A. baumannii128
between the earlier and late VAP-related study groups (73%
[8/11] vs 67% [14/21], P=1.000).128 In this study, 67% of K. pneumoniae was ESBL-positive.128 VAP was frequently
linked with substantially increased morbidity, including
prolonged ICU and hospitalization, and higher ventilator
days and health care costs.129
In the UK and the Republic of Ireland, a European
study of HCAIs connected with respiratory infection found
a prevalence rate of 7.59%. Among these HCAIs, 15.7%
were pneumonia, and 7% were lower respiratory tract infec-
tions other than pneumonia (LRTIOP).130 Around 21% of
patients in both the groups were having artificial ventila-
tion, which was much higher when compared to the rest of
the patients with HCAIs. MRSA was the principal invading
microorganism for both pneumonia and LRTIOP. Although
the patients with LRTIOP suffered more from C. difficile-
induced diarrhea than pneumonia, this was not statistically
significant.130 A recent Chinese study reported that 14.94%
(895) of inpatients acquired a LRTI which prolonged their
hospital stay and increased the costs per individual case by
US$2,853.93.131 Another study revealed that 9.6% of patients
developed HCAIs, of which respiratory tract infections
were the highest at 65.8%.132 The most frequently identified
respiratory pathogen was Gram-negative Acinetobacter spe-
cies (40.4%), and among these 21% were MDR.132
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A significant number of patients develop pneumonia after
surgery which includes both hospital-acquired pneumonia
(pneumonia developing 48–72 hours after admission) and (as
discussed above) VAP (pneumonia developing 48–72 hours
after endotracheal intubation).133 Postoperative pneumonia
has been described as one of the leading consequences of
all types of surgery with a high incidence of morbidity and
mortality.134 It increases hospital stays on an average of 7–9
days and increases health care costs from US$12,000 to
US$40,000.114,135,136
HCAIs HCAIs are a major safety concern for both health care pro-
viders and patients. They continue to escalate at an alarm-
ing rate, especially in emerging economies, with infection
rates 3–20 times higher than in high-income countries.1,2,137
HCAIs increase morbidity, mortality, length of hospital
stays, and costs;138–140 therefore, more research and changes
in practice are needed to ensure hospital safety and prevent
HCAIs.32,141–143 The annual costs for HCAIs alone in the
USA are between US$28 and US$45 billion, but with even
this amount of spending, 90,000 lives are still lost per year:
HCAIs are among the top five killers in the USA.14,144–147 The
WHO advocates that effective hand hygiene is the single
most important practice to prevent and control HCAIs, which
form colonies with MDR microbes.1,2,148,149 Several studies
report that a simple and straightforward process, taking only
a few seconds to clean hands with an alcohol-based hand rub
helps prevent HCAIs and save lives, reduce morbidity, and
minimize health care costs.150,151 However, factors such as
the availability of alcohol-based hand rubs and up-to-date
knowledge of the importance of hand washing hinder good
practice in hand hygiene. For example, an Australian observa-
tional study of community nurses highlighted poor practices
of hand hygiene in comparison with a standard protocol.152
The WHO promotes and advocates that all health care
workers (HCWs) must wash their hands before touching a
patient, before clean/aseptic procedures, after body fluid
exposure/risk, after touching a patient, and after touching
patient surroundings.153 The Center for Disease Control
and Prevention has developed a comprehensive plan and
guidelines for the prevention of HCAIs which covers basic
infection prevention and control (IPC); antibiotic resistance;
device- and procedure-associated infections; disease/
organism-specific infections; and guidance for health work-
ers working in specific settings.154 This guidance, like that
of the WHO and the UK Royal College of Nursing (RCN)
also emphasizes the importance of hand washing.153–155 The
RCN also promotes and advocates that all health care profes-
sionals must receive compulsory “infection control training
as part of their induction and on an ongoing annual basis.
It is particularly important that knowledge and skills are
continually updated.”155 Multiple research studies indicate
that policy changes and the adoption of novel multifactorial,
multimodal, multidisciplinary strategies offer the greatest
possibility of success in terms of hand hygiene improvement
and the reduction of HCAIs.156–167
Instigating best practice in health care stems “from
a response to factors that are outside a purely scientific
understanding of infection and not simply understood as a
deficit in knowledge.”168,169 Good practice for infection pre-
vention among HCWs can be ensured through compliance
to IPC guidelines.168 Specific individuals acting as “change
champions” can act as arbitrators or negotiators, contribut-
ing to changing behaviors and implementing best practice
to ensure patient safety.168–171 This calls for educational
interventions that reflect the philosophies, principles, and
community understanding of dirt and infection.169 An edu-
cational intervention involving 4,345 health professionals
in three public hospitals in the USA successfully improved
hand hygiene immensely with the use of alcohol hand rub.
Nurses, physicians, and allied HCWs improved from 14% to
34%, 4.3% to 51%, and 12% to 44%, respectively.172 Other
studies also highlight how behavior change around hand
washing can result from educational interventions.149,151,172
Health professionals must protect themselves with barriers
for example, gloves, gowns, face masks, protective eyewear,
and face shields,173 to decrease the work-related transmis-
sion of microorganisms. Regular use of personal protective
equipment (PPE)173 devices protects both the professional
and the patient from potentially infectious body fluids.173
Nevertheless, the use of PPE does not confirm 100% pro-
tection,174 for example, needlestick injury can breach PPE,
and, in many occasions, issues might go unrecognized
which might cause a dangerous health hazard including
hepatitis B or HIV.175
Respiratory microorganisms, for example, influenza
virus, Bordetella pertussis, Haemophilus influenzae, Neis-
seria meningitidis, and Mycoplasma pneumoniae, severe
acute respiratory syndrome-associated coronavirus, Group
A Streptococcus, adenovirus and rhinovirus, and tubercular
bacilli176 are easily dispersed through droplets (particles ≤5 µm in size) in closed health care settings and often cause
endemics and epidemics.176 PPE, vaccines, and drugs are
the main measures to prevent and control such infections.177
This includes national annual campaigns such as requiring all
health professionals to have a flu vaccine. Multiple research
studies have found that poor cleaning of hospital surfaces is a
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major source of HCAIs because of the transmission of many
dangerous microorganisms such as MRSA, vancomycin-
resistant Enterococcus spp. (VRE), C. difficile, Acinetobacter
spp., and norovirus.178–182 Meticulous cleaning of hospital
surfaces is therefore vital to maintain standards and reduce
the risk of HCAIs.183 Several studies conclude that ultraviolet
devices and hydrogen peroxide vapor technologies success-
fully eradicate potentially dangerous hospital microorgan-
isms adhering to the surfaces in ward or patient rooms.183–186
Furthermore, hydrogen peroxide vapor efficiently sterilizes
and sanitizes all clinical areas where potentially dangerous
microbial MDR microorganisms and spores were suspected
to be present.187
Conclusion In the early to mid-19th centuries in both Europe and USA,
thousands of young women died from puerperal sepsis and
fever, the diseases rampant in the charity maternity clinics
of the time188 and, due to the efforts of (among others) Dr
Ignaz Phillip Semmelweis and Dr Oliver Wendell Holmes, the
fight against puerperal fever was won and it was confirmed
that HCAIs were transmitted via the hands of HCWs.188–192
Despite the development of many hi-tech methods, hand
washing with soap and water or alcohol rub is still the
most important means of maintaining personal hygiene and
preventing HCAIs.192 However, due to the rise of antibiotic-
resistant bacteria and a reluctance of some HCWs to imple-
ment best practice infection control, HCAIs remain one of
the biggest causes of death in most countries. Therefore, it
is essential that strategic, policy, and education initiatives
continue to focus on managing and controlling such (pre-
dominantly needless) infections.
Limitations of the study The topic of HCAIs is a very broad issue, and it has therefore
not been possible to cover all aspects of HCAIs in one paper;
hence, we have been selective in selecting key aspects of the
current debate.
Acknowledgments The authors are grateful to Dr Zakirul Islam, Associate
Professor and Head of The Department, Pharmacology and
Therapeutics, Eastern Medical College, Comilla, Bangladesh
for his cooperation in converting the video abstract from a
PowerPoint file to video format.
Disclosure The authors report no conflicts of interest in this work.
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Infection Prevention in Practice 3 (2021) 100169
Available online at w
Infection Prevention in Practice
journal homepage: www.elsevier.com/locate/ipip
Barriers and facilitators on hand hygiene and hydro- alcoholic solutions’ use: representations of health professionals and prevention perspectives
Nicolas Calcagni a,*, Anne-Gaëlle Venier b, Raymond Nasso c, Guillaume Broc d, Eva Ardichen b, Bruno Jarrige c, Pierre Parneix b, Bruno Quintard a
a INSERM U1219 équipe Handicap, Activité, Cognition, Santé, Université de Bordeaux, Bordeaux, F-33000, France b Centre d’appui pour la prévention des Infections Associées aux Soins, CPias Nouvelle-Aquitaine, CHU de Bordeaux, Bordeaux, F- 33000, France c Centre d’appui pour la prévention des Infections Associées aux Soins, CPias Iles de Guadeloupe, Pointe à Pitre, F-97100, France d Unité Dynamique des capacités humaines et des conduites de santé, Université Paul-Valéry Montpellier 3, Montpellier, F-34000, France
A R T I C L E I N F O
Article history: Received 31 March 2021 Accepted 10 August 2021 Available online 14 August 2021
Keywords: Healthcare-associated infections Hand hygiene Hydro-alcoholic solution Prevention Perceptions Hand rub
* Corresponding author. Address: INSERM, B rue Léo Saignat, BORDEAUX Cedex, 33076, Fr
E-mail address: nicolas.calcagni@u-borde
https://doi.org/10.1016/j.infpip.2021.100169 2590-0889/ª 2021 The Authors. Published by under the CC BY-NC-ND license (http://creat
S U M M A R Y
Background: Healthcare-associated infections pose a serious problem in terms of health and mortality. Their prevention is a necessity, and healthcare professionals are one of their main vectors. Thus, they must be at the centre of preventative strategies. As hydro- alcoholic solutions (alcohol-based hand rub) represent the most effective means of pre- venting these infections, it is necessary to identify the representations, barriers, and facilitators of their use. Method: Forty-six healthcare professionals from two areas in France, New Aquitaine and Guadeloupe, were questioned about their practices through semi-structured registered interviews and four focus groups. Each interview and focus group were transcribed then analysed through lexicometric and thematic content analyses. Results: The interviewed identified several barriers and facilitators related to the com- position and characteristics of hydro-alcoholic solutions (unpleasantness, harmfulness, personal preferences for other hand hygiene products), personal factors (work habits, cognitive bias, lack of knowledge and communication) and organizational (professional constraints, product accessibility, financial resources). Conclusion: Strategies to prevent healthcare-associated infections should be constructed with consideration of psychosocial facilitators and barriers for healthcare professionals in using hydro-alcoholic solutions. These strategies should also ensure that they are well informed about the effectiveness of alcohol-based solutions, through prevention cam- paigns and scientific articles. This awareness should equally be conveyed with educational tools that involve healthcare professionals and use the social dynamics of their work environment.
PHdUMR 1219, Team : Handicap Activity Cognition Health (HACH), F-33000, Bordeaux, France, 146 ance. Tel.: þ33 6 10 03 18 62. aux.fr (N. Calcagni).
Elsevier Ltd on behalf of The Healthcare Infection Society. This is an open access article ivecommons.org/licenses/by-nc-nd/4.0/).
N. Calcagni et al. / Infection Prevention in Practice 3 (2021) 1001692
1 Mission d’Appui Transversal à la prévention aux Soins.
ª 2021 The Authors. Published by Elsevier Ltd on behalf of The Healthcare Infection Society. This is an open access article
under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Background
More than ever, in the context of the COVID-19 pandemic, hand hygiene (HH) is crucial in the fight against the spread of infection. It is repeatedly stated in numerous government messages calling for hand disinfection with hydro-alcoholic solution, alcohol-based hand rub (ABHR), as often as possible [1]. As easy as this example may be, HH is equally relevant in the prevention of healthcare-associated infections (HCAIs) [2,3].
The most common HCAIs include catheter-associated uri- nary tract infections, surgical site infections, ventilator- associated pneumonia and central line-associated blood- stream infection [4]. The numbers involved are overwhelming. In the United States, HCAIs affect 1.7 million people, making them one of the top 10 causes of death in the USA [3]. In France, nearly one patient in 20 is affected by HCAIs (4,000 deaths per year) [5]. At international level, the prevalence varies from 5 to 15% of hospitalized patients depending on the country concerned [3]. In addition to their prevalence and lethality, these infections are particularly costly and stressful for the patients [6e11]. Moreover, the rise of antimicrobial resistance is leading to the increased risk of facing untreatable HCAIs [12].
Caregivers are among the main vectors of HCAIs, as negli- gence of health professionals combined with failure to observe hygiene protocols, overwork, understaffing and the increasing number of patients may all contribute to the development of HCAIs [13e15]. Poor HH is the most common vehicle for the transmission of HCAIs [16]. Compliance with HH standards is the simplest and most important way of preventing and con- trolling HCAIs. There are two ways of performing HH: rubbing hands with an ABHR or washing them with soap and water. When hands are visually clean and dry, ABHR is preferable as it is microbiologically more effective [17]. Most important ABHR allows a better compliance as it is easier and faster to perform [18]. Yet the adherence of healthcare professionals to HH or their knowledge of HCAIs and related good practices are not optimal [3,19e24].
To contain the problem of HCAIs, a preventative, effective and cost-effective approach is necessary [13,25,26]. Health psychology provides useful theoretical insights and socio- cognitive models (such as Reasoned Action Theories and Plan- ned Behaviour Theories), which expose the processes under- lying the establishment and maintenance of health behaviours. These stipulate that to induce an individual to develop such behaviours, it is essential to look at the attitudes, repre- sentations, intentions, barriers, facilitators, and the perceived social norms that one identifies about the behaviour in question [27,28]. Studies to identify these elements in the context of HCAIs and HH are not lacking in the international literature [29e33]. However, those studies focus only on general
des Infections associées
perceptions of hygiene among healthcare professionals, while studies taking a deeper look into the ABHR are scarce [34].
The national Transversal Support Mission for the Prevention of Healthcare-Associated Infections (MATIS)1, led by the Sup- port Centres for the Prevention of Healthcare-Associated Infections (CPIAS)2 of New Aquitaine and Guadeloupe in France, aims to create tools for assessment, training, and communication in terms of infection prevention and control. As part of its mission (2018e2023), qualitative research was con- ducted. The main objective was to explore the representations of hand hygiene among health professionals, and the psycho- social barriers and facilitators associated to the use of ABHR, to obtain a better understanding of ABHR, HCAIs, HH issues, and to develop adapted educational tools to promote HH.
Method
To meet this objective, individual or grouped interviews were proposed to healthcare professionals to make them reflect on their own practices related to HH and ABHR. These interviews were achieved through an open, interpretative, exploratory approach allowing abstracting and generalizing data (inductive approach) [35].
Participants
Forty-six healthcare professionals (22 individual interviews þ 24 participants divided into four focus groups), with different professions and hierarchical status (and prac- ticing in the French regions of New Aquitaine and Guadeloupe) were selected on a voluntary basis and included in the study. We first identified facilities and private practices that could be representative enough of the population of healthcare work- ers. In those facilities, we asked targeted professionals for participation based on our representativeness needs. Only one auxiliary nurse in a nursing home declined because of a lack of time. Healthcare workers were progressively included in this study until thematic saturation was reached [36]. The focus- group participants were recruited by email or by registering on CPIAS Guadeloupe website.
The average age was 44.1 years (25e74), and the average length of service was 11.8 years (6 months-36 years). The samples included 12 men and 34 women, including six manag- ers (health executive, director, head of the department) and 40 caregivers (see Table I below).
Measures
An interview grid was developed for both the individual and focus-grouped interviews with the aim of identifying barriers and facilitator of the use of ABHR, in order to improve com- pliance with HH. This grid was used during telephone
2 Centre d’appui pour la Prévention des Infections Associées aux Soins.
Table I
Participants’ sociodemographic data
Variables New Aquitaine
Guadeloupe Total
Sex
M 10 4 14 F 12 20 32
Statut
Manager 3 3 6 Caregiver 19 21 40 Patient 2 2 4
Profession
Doctor 7 1 8 Dentist 2 0 2 Nurse 3 8 11 Nursing auxiliary 0 6 6 Midwife 1 1 2 Intern 2 0 2 Occupational therapist 0 1 1 Radiographer 0 2 2 Speech/language therapist 1 0 1 Health Executive 1 3 4 Director 2 0 2 Physiotherapist 1 1 2 Surgeon 1 0 1 Head of Department 1 0 1 Hospital Service Agent 0 1 1 Patient 2 2 4
Structure
Hospital 7 3 10 Clinic 1 1 2 Nursing home/Retirement home
0 4 4
Private practitioners 14 2 16 Unknown 0 14 14
Note. M ¼ Male; F ¼ Female.
N. Calcagni et al. / Infection Prevention in Practice 3 (2021) 100169 3
interviews and focus groups for both regions. It was organized around two main themes using open-ended, non-inductive questions:
� Representations concerning ABHR: assessing the use of ABHR in practice, information needs, individual and group barriers and facilitators for its use: “How do you explain the fact that some caregivers do not always use ABHR?” “What could motivate healthcare professionals to use ABHR?”
� Ways to improve hand hygiene in general: give professionals the opportunity to propose awareness techniques adapted for the field: “What would you need in practice to improve your hand hygiene practices?”
Procedure
Semi-directed individual interviews were conducted by telephone. The participants were contacted by email, with an explanation of the objectives of the study and the interview procedures. The interviews were conducted by a psychologist with no prior relationships with the included healthcare
professionals (HCPs), and no previous history with the selected facilities. Interviews happened between September 17 and November 3, 2018, lasted between 20 and 50 minutes and were recorded using a Dictaphone.
A written and oral explanation of the research objectives was given. The focus groups took place between 4 and 26 October 2018 and lasted between 63 and 86 minutes. Three were conducted in Guadeloupe (14 participants divided into three focus groups) and one in New Aquitaine (10 participants). The same interview grid was used for all the focus groups. The discussions were recorded with the permission of the participants.
Ethical considerations
This research has been declared to the Commission Natio- nale de l’Informatique et des Libertés (CNIL; the French National Agency regulating Data Protection) under the number 2207056. An information note and a consent form were sent to each participant. They were notified that they had the possi- bility of withdrawing at any time during the study and that they could obtain any additional information. The data were stored and processed anonymously and confidentially.
Data analysis
Each recording was transcribed verbatim and the whole corpus of the interviews was then prepared for textual analy- sis. The data from the interviews were processed from November 2018 to March 2019. Thematic content analysis was performed with Nvivo software on each transcription until thematic saturation was reached, that is when no new themes emerged in the last five transcriptions analysed. While the- matic content analysis allows to interpret the corpus of texts, we also performed lexicographical analysis to get a better understanding of what our participants talked about [37,38]. This approach allows observation of the frequency and the proximity or distance between words, by drawing up a lexicon of the words used in the corpus, and dividing them into units which will be the subject of a matrix (presence/absence of words in each unit). This matrix is then subjected to multi- dimensional analyses of the distance between words based on Chi2. Those analyses highlight how the discourse can be divided into different classes that regroup words close to each other (Descending Hierarchical Analysis), and how those different classes are opposed or mutually close on a graphic repre- sentation (Factorial Correspondence Analysis). Those are use- ful for assisting the reading of qualitative content, but still rely on subjective interpretation from the researcher. Two psy- chologists (EA and NC) performed the analyses using IRaMuTeQ [39,40].
Results
Barriers of the use of ABHR
When participants were asked what would prevent care- givers from using the hydro-alcoholic solution, the Descending Hierarchical Analysis (DHA) carried out on their answers divi- ded the discourse into three classes (Table II below). Class 1 (14.7% of the discourse) seems to refer to a terminology of
Table II
Classes of discourse elaborated by DHA classification (Alceste Method) about barriers to the use of ABHR and profiles associated with the classes
Classes Words related
Class 3 (48,4%) Hand, Wash, Put on, Gel, Hydro-alcoholic, Use, Clean, Alcohol, ABHR, Smell, Skin, Leave, Friction, Times
Profile Country New Aquitaine Sex Female þþ Lenght of service 32,5e40,5 years þþ, 24,5e32,5 years þ Statut Manager Profession Speech/language therapist þþ, Surgeon þ, Dentist, Intern Structure Private þþ, Clinic Class 1 (14,7%) Question, Habit, Returning, Forgetting, Handing over, Posing,
Practical, Professional, Continuation, Serious, Medical, Work
Profile Age 25e37years old þþ Statut Caregiver Profession Nursing Auxiliary þþþ, Director þ, Physiotherapist Structure Hospital þþ Classe 2 (36,9 %) Hygiene, Doctor, People, Asking, Seeing, Service, Missing, Working,
Training, Establishment, Nurse, Technical
Profile Sex Male þþ Age 64e76years old þþ Statut Patient þþ Profession Hospital Service Agent þþ, Head of Department
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individual responsibility and personal factors (“question”, “habit”, “realize”, “forget”, “practice”, “consequence”, “obligation”). Class 2 (36.9% of the discourse) refers to organizational factors (“hygiene”, “doctor”, “service”, “lack”, “training”, “establishment”, “equipment”). Class 3 (48.4% of the speech) refers to ABHR products and their effect on hands (“hand”, “wash”, “gel”, “hydro-alcoholic”, “alcohol”, “ABHR”, “skin”, “friction”).
The thematic analysis strengthens this classification, as it highlights three types of barriers mentioned by the partic- ipants. The first relates to the composition of the product and its use, which is mainly a barrier of unpleasantness and harm- fulness. First, ABHR hinders the comfort of the caregiver (unpleasant sensation, stickiness, unpleasant smell). It also raises the question of health. In case of wounds or cracks on the hands, ABHR gives a painful burning sensation. Thus, some healthcare professionals might perceive ABHR use as toxic and harmful for the skin in the long run. Some caregivers prefer wearing gloves. Others will prefer washing with soap, which is perceived as less aggressive and more efficient, while ABHR leaves a “false” impression of clean skin.
Representative verbatim sample: “Well, I don’t know if you’ve had
the opportunity to use a lot of it, but it’s something that will burn
your skin. And for some... In winter time, with the cold, you have
dry skin, we’ve all been exposed to that... You have cracks forming
in your hands because I use it... I don’t even know how many times a
day I use it... We exceed almost 100 washes per day and so...”
The second type of barrier relates to intra- and inter- personal factors. These include, for example, the habits and automatisms associated with their practice. The automatic aspect of hand-washing leads to a drop in interest and vigi- lance, conducive to the occasional forgetfulness of using it. Those are also habits that the least experienced caregivers
have yet to adopt, or routines that are rooted too deep in older caregivers’ practices and that are difficult to change.
This category also features cognitive biases, such as beliefs and rumors circulating around ABHR. Participants mentioned the lack of conclusive studies on the effectiveness of ABHR, the long-term health consequences of repeated use of ABHR, or the supposed harm of ABHR on the destruction of the bacterial flora. It is also a question of poor risk assessment, or even risk minimization, as some respondents do not feel that the use of ABHR is relevant to their practices.
Representative verbatim sample: ‘As a result, it’s going to be very,
very violent for the flora of the skin... which is going to degrade...
Moreover, because of the American studies that have come out on
the use of this hydroalcoholic solution... They did a study saying
that they didn’t yet have enough data to know where we were
going... we still don’t know in the long term if daily dose can be
harmful to the skin. It was kind of imposed on us a few years ago.
We were told that it was the solution to all our problem. But
then... in the end, it can have repercussions on the caregivers.’
The last category of hindrance relates to organizational factors. It includes the perceived lack of time, mainly due to the high workload or the lack of staff, which lead to for- getfulness. This category also includes the issue of accessibility and availability of the product, as respondents evoked that sometimes no products were available at all, that they are not visible or not highlighted enough, and that they are not always practical to carry around.
Facilitators of the use of ABHR
A DHA classification divided the discourse into three classes. The first (39.3% of the discourse) relates to the incitement to use ABHR (‘hand’, ‘ABHR’, ‘washing’, ‘time’, ‘think’,
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‘explain’, ‘poster’, ‘effective’, ‘buy’, ‘use’). The second (45.1% of the discourse) relates to the collective involvement of caregivers (‘work’, ‘take’, ‘awareness’, ‘staff’, ‘care- givers’, ‘understand’, ‘transmit’, ‘involve’). The third and last (15.5%) of the discourse refers to the accessibility of the product (’disposal, “door”, “level”, “mark”, ’hallway, ‘pub- lic’, ‘entry’, ‘room’).
A Factorial Correspondence Analysis opposes its classes on an interesting orthogonal axis (Figure 1 below). The vertical axis opposes class 1 (black words) to class 2 (underlined and italic words), on a continuum that seems to distribute the words evoked, from top to bottom, between individual and collective facilitators. The horizontal axis opposes class 3 (grey words) to class 2, and seems to trace a continuum, from left to right, which distributes the words between ABHR products-centred facilitators and prevention/ communication-centred facilitators.
Regarding thematic interpretation, the participants dis- tinguished three types of facilitators to promote the use of ABHR (Table III below). These are firstly related to the product itself, which availability should be improved through better logistical management (small bottles, highlighting, sufficient replenishment), but also by highlighting the advantages in terms of time and efficiency compared to washing with soap.
The second type of identified facilitator is to encourage changes in the professional practices of healthcare givers. These feature reminding people that the use of ABHR is a
Figure 1. Factorial Correspondence Analysis of the discourse related t by Descending Hierarchical Analysis.
matter of patient safety and well-being, but also developing good habits of taking one’s time, so that the use of ABHR does not remain a simple automatism, but a conscious and thoughtful gesture.
Representative verbatim sample: ‘Sometimes we think that the
risk is less direct and so we pay less attention to hand washing, we
forget about it or do it too quickly, and that’s where it happens.
So... So there you go... That’s why, you have to be vigilant all the
time, and be mindful of what you’re doing.’
Finally, the participants stressed the need for prevention around ABHR. To help them to engage in sustainable use of ABHR, live field demonstrations of the transmission of germs through educational tools and the effectiveness of hydro alcoholic solution (HAS) should be carried out. Caregivers should also be convinced of the effectiveness and non-toxicity of ABHR, but also of the risks of not respecting hygiene standards by promoting scientific articles free of conflicts of interest.
Representative verbatim sample: ‘I hope that future studies will be
done over the next few years that would demonstrate that there is
no notable repercussions on daily use, that there is no risk of
causing degenerative diseases. Depending on who decides to do the
study and who actually conducts it, if it’s the lab that asks for it,
they’re bound to hire someone who won’t invalidate the use of the
product or who won’t say that it’s very harmful in the long term for
the professionals who use it. So... It has to come from a private
o the facilitators of ABHR use, carried out on the classes obtained
Table III
List of facilitators for the use of ABHR
Categories Sub-categories Details
Promoting access to the ABHR product
Improving accessibility Small, easily transportable flasks, highlight ABHR presence in the services and in the rooms, regularly replenishing the common containers
Diversity of textures and compositions
To offer different choices of solutions and change for the preference of caregivers
Emphasis on practicality To present the advantages of HAS compared to soap washing, in terms of time and efficiency.
Encouraging change in professional practices
Focusing on the patient’s well-being
To focus the use of ABHR on the well- being and health of the patient, which are undermined by HCAIS
Reminding the basics of hygiene
Clean clothes, remove jewelry, clean nails thoroughly.
Setting targets Standardized Hydro-Alcoholic Solutions Consumption Indicator levels to be achieved
Taking the time To develop good habits, to take one’s time and become aware of the washing gesture and avoid forgetting.
Convincing and preventing
Showing and demonstrating
To demonstrate the transmission of germs in the field during treatment and the eradication of bacteria by ABHR.
Convincing and arguing To prove efficacy, relevance, risks, non-toxicity and health effects on the basis of sound scientific studies and without conflicts of interest.
Communicating and involving
To inform, explain, question caregivers to raise their awareness and promote their interest and action.
Raising awareness among patients and visitors
By means of welcome booklets, posters, communication by the caregivers
N. Calcagni et al. / Infection Prevention in Practice 3 (2021) 1001696
organization... that makes the request alone and that this request
is not made by the laboratory that supplies it. There must not be
any conflict of interest and we must not feel that we are being
cheated in the results.’
Faced with these facilitators, the participants proposed the skeleton of prevention and training interventions (Figure 2 below). The content of these training courses should, in their opinion, include the same content they mentioned in the pre- viously identified facilitators. Finally, these interventions should be based on different support, each with a different purpose.
Discussion
Summary of results
When asked about ABHR, study participants show a clear and solid understanding of its disinfectant role, but they rec- ognize that they use it only at times when there is a perceived
high risk of exposure. These results echo the recurrent problem found in the scientific literature: sufficient knowledge related to HCAIs, but insufficient adherence to hygiene protocols [19e24].
Thus, they identify a series of obstacles, related to the composition of the product or organizational factors in terms of lack of time and product availability which hinder them in the use of ABHR. They also acknowledge their own individual responsibility (underestimation of the risks involved, lack of knowledge, work habits that lead to omission). Incriminating the products, or one’s own respon- sibility in the transmission of germs, is an innovative result, as the available literature so far shows that professionals mostly blame organizational and occupational aspects, such as insufficient cleaning of the work environment [41]. Seen through the prism of popular behaviour frameworks (such as the Behaviour Change Wheel (BCW)), respondents mainly identify the lack psychological capability, physical oppor- tunity, reflective and automatic motivation in the promotion of HH and AHBR [42].
Figure 2. Prevention intervention around ABHR proposed by the study participants.
N. Calcagni et al. / Infection Prevention in Practice 3 (2021) 100169 7
It is therefore natural that they evoke facilitators in response to these barriers that can feed into interventions function according to BCW [42]. For example, they suggest to promote access to ABHR products (BCW: environmental restructuring) by restocking them in a satisfactory manner, by highlighting them in services, by offering small, easily trans- portable bottles, or by highlighting their superiority over soap. Any institutional effort to facilitate access to HH products, or at least a reminder to use them, would be appreciated by health workers. Following BCW, they also suggest strengthen- ing their automatic motivation by developing the mindset of taking one’s time in hand-washing, and to develop more thoughtful and mindful habits (BCW: enablement). Some also suggest focusing the core of prevention around patients’ health, threatening the patient’s safety if they do not hand- wash correctly (BCW: Coercion).
Comparison to literature
It is interesting to note that in recent research, the care- givers interviewed were in favour of an electronic hand hygiene
reminder device, as they perceived a lack of feedback and support from the hospital organization about HH [43]. How- ever, it would also be helpful to encourage people to change their professional practice by establishing more ‘healthy’ habits. As use of ABHR can be perceived as a ‘mindless’ automatism, raising awareness and encouraging caregivers to take their time could bring the gesture at a more reflexive level and prevent omission of its use. Refocusing ABHR onpatient safety and well-being would also improve adherence to good hygiene protocols, as it is the main lever for motivating care- givers to reduce HCAIs [31]. The effort must also be a collective one, by making available an educational arsenal (including scientific articles demonstrating the effectiveness of ABHR), tools for directly observing the transmission of germs, and preventative interventions to explain and involve healthcare workers. This would make it possible to cancel out certain irrational beliefs, according to which ABHR have no scientifi- cally proven effectiveness. These facilitators for adherence to HH have already been identified in other studies [32,44].
Interestingly, participants indicate that informing and sen- sitizing patients and families about HH and ABHR would be an
N. Calcagni et al. / Infection Prevention in Practice 3 (2021) 1001698
important facilitator. This would empower patients and involve them in prevention. However, a study shows that most patients would be uncomfortable with the idea of questioning doctors about their HH unless they are explicitly invited to talk about it [45]. Thus, being proactive with patients and inviting them to talk about HH would encourage dialogue with them and would even prevent unwanted situations where patients directly confront caregivers on their HH [32].
Participants outlined relevant preventative measures based on the themes of informing, demonstrating, involving and using social dynamics, which can be linked to BCW [42]. Our partic- ipants suggested that prevention on HH should revolve around informing caregivers through communications, posters, pre- vention campaigns and scientific articles; giving them access to intellectual knowledge, enabling them to be aware of the processes of transmission and infection control (BCW: educa- tion function, to strengthen psychological capability). Also, demonstrating transmission (through Petri dishes, UV light or dyes) would allow them to experience their own individual action in the fight against infection (BCW: Persuasion, to improve reflective motivation). Involving caregivers through facility reports, team challenges, based on tangible indicators of bacterial infections or consumption of ABHR rates could strengthen their motivation and help them to visualize the impact of ABHR (BCW: Incentivisation). Finally, using social dynamics would allow the caregivers to adjust their norms to the ones of influential colleagues and to perceive the effective opinions and judgments in their environment (BCW: Modelling, to mobilize social opportunity). All these strategies would directly influence caregivers’ representations of HH, integrate norms in their environment, and increase their perception of control over it. Such interventions would thus incorporate all the ingredients favourable to good health behaviour and its implementation, according to Reasoned Action Theories and Planned Behaviour Theories [46]. Moreover, perceived control and subjective norms are the most important factors con- tributing to higher levels of self-reported HH performance [29].
Limitations
Although the number of participants in this study is con- sistent, and despite data saturation being reached, there is an imbalance in the participants’ profession (few clinic staff, prevalence of medical professionals in New Aquitaine and prevalence of paramedics in Guadeloupe). It is therefore pos- sible that the identification of representations, barriers and facilitators is incomplete. Moreover, all the results have been treated from a general point of view, without comparing pos- sible cultural and professional differences between the dif- ferent professions included, or between mainlanders and islanders. It should also be highlighted that data collection happened before the start of the current COVID-19 pandemic. This can be considered strength, as we explored COVID 19-free representations, more genuine to the context of HCAIs. One could argue that those results may be outdated, as it is safe to hypothesize that the pandemic impacted the representations on HH. Nevertheless, the four main barriers declared by care- givers in 2019 and 2020 via the national audit ‘pulpe’ friction’ in France were still the same [47]. But what would happen to those representations in a post-COVID-19 era? It might prove useful to evaluate the impact of COVID-19 on those repre- sentations once the crisis is over. Finally, our study used an
inductive approach. It yielded interesting results and identified the most immediate barriers and facilitators evoked by our participants. It is important to note that the design of this study, which aimed to keep interviews in balance with the precious time include HCPs had to share with us, may have yielded incomplete results. Further qualitative studies, based on deductive approach, may complete this point of view, and should be based on strong behaviour theories or exhaustive frameworks, such as BCW or the Theorical Domains Framework [42,48]. Such studies would be an asset in identifying all the determinants of the use of ABHR, but would require longer and more exhaustive interviews, which can be difficult to obtain given the workload and the lack of time of HCPs.
Implication for practice
Identifying barriers and facilitators is not enough in itself, and future studies could also develop and test intervention programs based on those results. Accordingly, the CPIAS Nouvelle-Aquitaine and Guadeloupe, in the framework of MATIS, developed an intervention: the HH national toolbox. It includes an innovative tool named ‘Pulpe’friction’, a web application that allows an interviewer to question in a short way (less than ten questions) HCPs on their HH practices at different key times and also on the obstacles to hydro- alcoholicsolution. This tool also provides a team diagnosis (compliance declared at different stages of care, majority of obstacles, and stage of change in the team) and proposes a personalized action plan. It allows an institution to monitor the evolution of compliance over time by repeating the audits. The toolbox includes a serious game named ‘I. Control’ (existing in English version) that challenges HCPs and patients on hundreds of clinical situations involving HH and HCAI. Furthermore, several communication tools are featured (video, quiz, edu- cational posters). All those elements and more details are available on the RéPias website [49].
Conclusion
Negative aspects and representations of ABHR, work habits as well as organizational and accessibility constraints prevent compliance with standard precautions on HH. Prevention strategies should rely on promotion of access to ABHR products by improving its accessibility to healthcare professionals, pro- posing diversity of textures and compositions, and by empha- sizing its effectiveness and practicality. Encouraging changes in professional practices are required to focus the messages on patient safety, reminding staff on basics of HH, setting clear objectives, and developing the habit of taking the time for HH. Finally, convincing healthcare workers could be done by dem- onstrating direct effects of HH by the means of ludic tools, reassuring healthcare professionals with the help of scientific efficacy studies of ABHR, and even including patients and vis- itors in hand hygiene-related prevention.
Authors’ contributions
BQ, GB, EA, AGV, RN, BJ and PP designed the protocol of the study. AGV and RN identified the people to be interviewed and organized the focus groups. EA led the interviews, focus groups, and was in charge of the transcript of the verbatim and
N. Calcagni et al. / Infection Prevention in Practice 3 (2021) 100169 9
extraction of the data. EA, AGV and NC performed qualitative analyses and interpreted the results. NC redacted the draft. BQ, AGV, RN, BJ and PP participated in the modification and correction of the draft.
Funding
This study and MATIS mission are funded by Santé Publique France.
Conflict of interest statement
The Author(s) declare(s) that there is no conflict of interest.
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- Barriers and facilitators on hand hygiene and hydro-alcoholic solutions' use: representations of health professionals and p ...
- Background
- Method
- Participants
- Measures
- Procedure
- Ethical considerations
- Data analysis
- Results
- Barriers of the use of ABHR
- Facilitators of the use of ABHR
- Discussion
- Summary of results
- Comparison to literature
- Limitations
- Implication for practice
- Conclusion
- Authors' contributions
- Funding
- Conflict of interest statement
- References
RCA article 3.pdf
RESEARCH ARTICLE Open Access
Risk factors of health care–associated infection in elderly patients: a retrospective cohort study performed at a tertiary hospital in China Xia Zhao1, Lihong Wang1* , Nan Wei2, Jingli Zhang1, Wenhui Ma1, Huijie Zhao1 and Xu Han1
Abstract
Background: The elderly inpatients are in high risk of suffering health-care associated infection (HAI). The study aimed to analyze the risk factors of health-care associated infection (HAI) in elderly hospitalized patients to prevent it and improve the recovery rate of elderly patients.
Methods: The study was a Retrospective Cohort Study based on a 3-year surveillance in elderly inpatients in a large tertiary hospital in China. A retrospective review of the elderly inpatients ≥60 years with or without HAI were conducted. Binary multivariable logistic regression was used to evaluate the potential association between HAI and risk factors.
Results: We investigated a total of 60,332 subjects aged 60 years old or above. The incidence of HAI in elderly was 2.62%. With adjustment for some factors, advanced age, hospital days before HAI, intensive care unit (ICU) admission, use of ventilator, central line catheter or urinary catheter and cerebral hemorrhage, cerebral infarction, brain neoplasms, diabetes mellitus, coronary artery disease, malignant tumor and malignant hematonosis had significantly increased odds ratios (OR) of suffering from HAI compared with the control group but body weight and operation decreased OR.
Conclusion: Our findings suggested that advanced age, accompanied by some neurological and chronic noncommunicable diseases, hospital days before HAI, ICU admission, and use of devices were risk factors of suffering HAI in the elderly but the body weight and operation were the potential protective factors in this sample.
Keywords: Health-care associated infection, Elderly, Risk factors, Retrospective cohort study
Background Health-care associated infections (HAIs) which occur in patients under medical care in hospital or other health care facility is a notable public health concern. They place an enormous burden on poor prognosis, increased mortality, prolong hospitalization, and increased health- care costs. Every day, roughly one in 25 patients in the USA contracts at least one infection during their hos- pital care—an alarming statistic that is unacceptable in view of the fact that health care-associated infections
(HAIs) are mostly preventable [1]. However, HAIs are preventable with adoption of recognized preventive mea- sures. Over the past decade, a downward trend in health care-associated infections has occurred. A Survey of a total 12,299 patients in 199 hospitals showed that fewer patients had health care-associated infections in 2015 (394 patients [3.2%; 95% confidence interval {CI}, 2.9 to 3.5]) than in 2011 (452 [4.0%; 95% CI, 3.7 to 4.4]) (P < 0.001), largely owing to reductions in the prevalence of surgical-site and urinary tract infections [2]. The risk factors of HAI concluded extrinsic factors
such as invasive procedures, medication and stays in risk units and the conditions of the patient’s own condition such as age, sex, body weight, intrinsic comorbidities
© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
* Correspondence: [email protected] 1Hospital Infection Management Division, Xuanwu Hospital, Capital Medical University, No.45 Changchun Street, Xicheng District, Beijing 100053, China Full list of author information is available at the end of the article
Zhao et al. BMC Geriatrics (2019) 19:193 https://doi.org/10.1186/s12877-019-1208-x
and immunological factors on the basis of some previous reports and clinical experience of senior doctors. A sys- tematic review and meta-analysis about risk factors for HAI in hospitalized adults showed that the major risk factors independently associated with HAIs were dia- betes mellitus, immunosuppression, body temperature, surgery time in minutes, reoperation, cephalosporin ex- posure, days of exposure to central venous catheter, in- tensive care unit (ICU) admission, ICU stay in days, and mechanical ventilation [3]. The elderly are vulnerable to infections due to their
reduced immunological competence and complication of chronic illness [4–7]. China is one of the most advanced aging society and aging societies have increased the number of elderly inpatients. In order to take effective intervention to prevent HAIs in elderly, the first step is to find risk factors and identify patients at higher risk of HAI. Published research papers revealed some risk fac- tors for some special sites of HAIs such as surgical site infection (SSI), urinary tract infections, HAIs occured frequently in neurological ICU, etc. [8–11]. But there were few research focused on risk factors of HAIs in eld- erly. This study aimed to identify risk factors (RFs) present on admission and acquired during inpatient stay which could be associated with higher risk of acquiring HAI in elderly. Then we can formulate intervention strategies in the light of high-risk patients and risk fac- tors to reduce the incidence of HAIs and improve the recovery rate of elderly patients.
Methods Study design and data collection The study was a Retrospective Cohort Study based on a 3-year surveillance in elderly inpatients in a large tertiary hospital with 1147 beds in Beijing, China. A retrospect- ive review of the elderly inpatients ≥60 years old with or without HAI were conducted and there was a cohort de- sign. A total of 60,332 subjects (≥60 years old) who had been hospitalized from January 1, 2015 to December 31, 2017 were admitted and the subjects with less than 2 days or more than 60 days of hospitalization were excluded. HAIs were defined as infections occurred 48 h after
admission in inpatients. All HAIs that occurred in their hospitalized stay were identified by infection control practitioners and doctors according to the definitions published by Ministry of Health, the People’s Republic of China in 2001 [12]. We collected 5 categories including 22 kinds of infor-
mation of each participant including demographic char- acteristics, hospitalization days, diagnoses, operations, and specific device days using an automatic online HAI surveillance system named real-time nosocomial infec- tion surveillance system (RT-NISS, VERSION:12.8.2.1).
The RT-NISS is an integrated online HAI surveillance system which automatically download data from other information systems including the Hospital Information System (HIS), Electronic Medical Record (EMR), La- boratory Information System (LIS), Picture Archiving and Communication System (PACS), Mobile Nursing Information System (MNIS) and Anesthesia Operation System (AOS) to record clinical information of the inpa- tients. And then the RT-NISS screen the potential HAIs according to the Chinese NI diagnosis criterion pub- lished by the Ministry of Public Health in 2001 automat- ically which pre-input to the system by the algorithm of microbiological reports, radiology information, sero- logical and molecular testing, antibiotic usage and fever history of the patients [13]. All collected data was checked by the infection control
team and removed invalid data. Then All the potential HAIs were identified by infection control practitioners and doctors according to the definitions published by Ministry of Health, the People’s Republic of China in 2001. So the data we collected was validity and reliability.
Statistical analysis The data was consisted of measurement data and nu- meration data and was analyzed using the software SPSS 13.0. All the continuous variables were presented as means ± standard deviation (M ± s.d.) and the signifi- cance of the difference between the two groups was ana- lyzed by using Independent-Samples t test. The category variables were analyzed by using Chi-square or Fisher’s exact test. Binary multivariable logistic regression was performed to evaluate the potential association between the variables and HAI and the odds ratio (OR) and 95% confidence interval (CI) were calculated at the same time. Statistical testing was performed at the conven- tional 2-tailed α = 0.05.
Results The characteristics of the study elderly inpatients with and without HAI There were 60,332 subjects, including 1580(2.62%) subjects with HAIs. The median age is 69 (range from 60 to 104) and there were 33280(55.16%) males and 27052(44.84%) females. Table 1 and Table 2 show the characteristics of the study elderly inpatients with and withoutHAI in univariate analysis.
The potential association between risk factors and HAI The results of the multivariable logistic regression ana- lysis suggest a significant association between HAI and some relevant factors. With adjustment for some factors, age, hospital days before HAI, ICU admission, use of ventilator, central line catheter or urinary catheter and
Zhao et al. BMC Geriatrics (2019) 19:193 Page 2 of 6
some neurological and chronic noncommunicable dis- eases including cerebral hemorrhage, cerebral infarction, brain neoplasms, diabetes mellitus, coronary artery dis- ease, malignant tumor and malignant hematonosis had significantly increased odds ratios (OR) of suffering from HAI compared with the control group but body weight and operation decreased OR (Table 3).
Discussion This survey based on the retrospective cohort data showed that the incidence of HAI in elderly sample aged 60+ was 2.62% which was lower than many other reports but consistent with our previous study and some similar studies in the same region. Our study about the charac- ters of HAI in venerable elderly hospitalized patients which indicated the incidence of HAI in venerable eld- erly (aged 70+) were significantly higher than those under 70 years old (3.38% vs 1.45%, P<0.05) [14]. The in- vestigation of the HAIs incidence in elderly hospitalized patients at another hospital in Beijing, China, reported that the HAI incidence in patients aged ≥60y was signifi- cant higher than that in all inpatients (2.57% vs 1.84%, χ2 = 70.493, P < 0.05) [15]. A survey of the prevalence of HAIs in older people in acute care hospitals in Scotland found a linear relationship between prevalence of HAI and increasing age which described a pooled prevalence of HAIs in patients less than 65y and more than 65y (7.37% vs 11.13%, P < 0.05) [16]. The low incidence of HAI in this sample probably due to the effective preven- tion or specific diseases in the hospital. This hospital is excellent at diagnosis and therapy of neuroscience and geriatrics, so the nursing care of elderly patients is pro- fessional and the average length of hospital stay is shorten which contribute to the low incidence of HAI. On the other hand, the surveillance definition of HAIs is not entirely consistent in different research which lead to the difference in the result of the incidence of HAI. The present binary multivariable logistic regression
with adjustment for some factors showed that age, hos- pital days before HAI, intensive care unit (ICU) admis- sion, use of ventilator, central line catheter or urinary catheter and cerebral hemorrhage, cerebral infarction, brain neoplasms, diabetes mellitus, coronary artery dis- ease, malignant tumor and malignant hematonosis were
the dependent risk factors of suffering from HAIs based on this elderly sample. These results were similar to the reported conclusion based on adults about the risk fac- tors of HAIs. Length of ICU stay, diabetes and COPD were risk factors in a study of risk factors and epidemiology of HAI from an intensive care unit in Northern India [17]. Published studies observed some intrinsic risk factors such as age > 65 years, terminal incurable disease, gastrointestinal diseases and the pres- ence of > 2 underlying diseases [18, 19]. Other reports showed some extrinsic risk factors such as ICU admis- sion, previous antibiotic use, invasive mechanical ventila- tion, hospitalization time [20, 21]. So for elderly patients, the unnecessary hospital day and device using should be cut off to prevent HAIs. And for the elderly patients ac- companied by some neurological and chronic noncom- municable diseases, we should enhance the intervention to reduce the risk of suffering from HAIs. On the opposite side of the above results, body weight
exhibited a protective effect for elderly inpatients to pre- vent HAIs. Published studies suggested that weight loss should be added to the list of risk factors for some spe- cial infections such as invasive aspergillosis, tuberculosis and other chronic infection [22, 23]. Weight loss reflects a failure of dietary intake to maintain an adequate nutri- tional status and results in immuno-compromised to be vulnerable to infections. So the elderly inpatients should achieve weight maintenance and have a healthier body mass and composition to prevent HAIs. Another result of this study was that operation signifi-
cantly decreased the OR of suffering from HAIs in this elderly population. Operations play an important role in SSIs which is one critical category of HAIs and there were many studies on risk factors for SSIs occurring dif- ferent kinds of surgical procedures. The relationship be- tween patient age and the risk of SSI is not consistently reported in the literature, with numerous studies that implicating advanced age as a risk factor for SSI, and nu- merous studies finding no such association. Although SSI is one of the complications causing poor prognosis postoperative patients, the incidence is reported to vary from 0.1 to 50% [24, 25]. But general incidence of SSI of the most operations is lower than the common HAIs such as pneumonia, urinary tract infection and blood
Table 1 Hospital days and body weight of the subjects with and without HAI in univariate analysis, continuous variables, aged 60+, in Beijing, China
Control group N = 58752
HAI group N = 1580
t P
M ± s.d M ± s.d
Total hospital days (days) 9.16 ± 5.84 21.81 ± 10.45 47.93 < 0.001
Hospital days before HAI (days) 9.16 ± 5.84 10.31 ± 6.95 6.37 < 0.001
Body weight (km) 66.92 ± 11.69 64.46 ± 11.59 6.21 < 0.001
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Table 2 Age, sex, operations, ICU admission, using devices and chronic diseases of the subjects with and without HAI in univariate analysis, category variables, aged 60+, in Beijing, China (As a retrospetive study, there were some missing values about chronic diseases)
Variables No. of subjects No. of HAIs Incidence (%) χ2 P
Age 60~69y 32156 637 1.98 241.76 < 0.001
70~79y 18203 462 2.54
≥80y 9973 481 4.82
Sex Male 33280 909 2.73 3.69 0.06
Female 27052 671 2.48
Operation No 32627 947 2.90 22.42 < 0.001
Yes 27705 633 2.28
ICU days d = 0 51980 911 1.75 3625.18 < 0.001
d < 2 1742 46 2.64
2 ≤ d < 7 4120 159 3.86
7 ≤ d < 14 1472 154 10.46
d ≥ 14 1018 310 30.45
Using ventilator No 58478 1191 2.04 2529.06 < 0.001
Yes 1854 389 2.10
Using central line catheter No 56338 1015 1.80 2228.59 < 0.001
Yes 3994 565 14.15
Using urinary catheter No 43956 626 1.42 906.33 < 0.001
Yes 16376 954 5.82
Cerebral hemorrhage No 56866 1359 2.39 122.02 < 0.001
Yes 2770 160 5.78
Cerebral infarction No 39857 871 2.19 63.38 < 0.001
Yes 19779 648 3.28
Brain neoplasms No 59192 1496 2.53 12.49 < 0.001
Yes 444 23 5.18
Hypertension No 25586 590 2.31 10.50 < 0.001
Yes 34050 929 2.73
Hyperlipidemia No 51189 1330 2.60 3.84 0.05
Yes 8453 189 2.23
Diabetes mellitus No 40751 985 2.42 8.76 < 0.001
Yes 18885 534 2.83
Coronary artery disease No 41284 825 2.00 162.76 < 0.001
Yes 18352 694 3.78
COPD No 57510 1438 2.50 14.16 < 0.001
Yes 2126 81 3.81
Malignant tumor No 49227 1203 2.44 12.13 < 0.001
Yes 10409 316 3.04
Malignant hematonosis No 57123 1229 2.15 854.76 < 0.001
Yes 2513 290 11.53
Osteoarthropathy No 56429 1435 2.54 0.07 0.79
Yes 3207 84 2.62
Gynecological diseases No 58860 1510 2.56 6.10 0.020
Yes 776 9 1.16
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stream infection, especially in elderly. Our previous study showed that the top 3 sites of HAIs in elderly were lower respiratory tract infections, urinary system infec- tions and blood stream infections and the ratio was 41.62, 15.44 and 9.60% respectively, but the ratio of SSIs was only 2.26% [14]. Furthermore, the physical condi- tions of the elderly inpatients for the purpose of surgical treatment maybe were better than those suffering from many kinds of medical diseases, so they would not likely to be infected. This is probably the potential reason to explain this result in the present real world elderly population. There were some limitations in the present study in-
cluding the lack of analysis of special risk factors of spe- cial infections such as pneumonia, urinary infection, bloodstream infection and SSI in elderly. There are probably some special risk factors in a special infection attribute to the characteristics of different infection sites. We will think highly of this limitations and make an ef- fort to reveal in our following study.
Conclusion Our findings suggested that the risk factors of HAI in elderly included extrinsic factors such as advanced age, accompanied by some neurological and chronic non- communicable diseases and intrinsic factors such as hos- pital days before HAI, ICU admission, and use of devices. But body weight indicated a potential protective
effect on elderly population to prevent HAI. On the other hand, operation was not the risk factor of HAI and the operative elderly patients take lower risk of suf- fering HAI in this elderly population.
Abbreviations CAUTI: Catheter-associated urinary tract infection; CI: Confidence intervals; CLABSI: Central line-associated bloodstream infections; HAI: Healthcare associated infections; ICU: Intensive care unit; NISS: Infection surveillance system; VAP: Ventilator-associated pneumonia
Acknowledgements We thank the many health care professionals who assisted with the conduct of surveillance and the infection control team in our hospital.
Authors’ contributions XZ contributed to the specific implementation of the investigation, data analysis and the drafting of the paper; LHW designed and organized the study. NW helped for assistance with data analysis; JLZ reviewed of the manuscript. WHM, HJZ, and XH contributed to data collection. And all the authors were included in the infection control team that has collected the infections´ data. All authors read and approved the final version of the manuscript.
Funding This study was funded by the Scientific Research and Cultivation Program Foundation in Beijing China (No. PG2019018) grants from Beijing Hospitals Authority and Xuanwu Hospital, Capital Medical University. The correspondence author and the foundation would pay for the costs fees of open access publishing. The funding bodies had no role in the design of the study; collection, analysis, interpretation of data; and in writing the manuscript.
Table 3 Adjusted odds ratios for the association between HAI and risk factors among inpatients aged 60+, Beijing, China
β Wals χ2 OR 95% CI. P
Lower limit Upper limit
Age .204 16.168 1.226 1.110 1.355 < 0.001
Body weight −.015 21.077 .985 .979 .991 < 0.001
Hospital days before HAI −.026 16.718 1.138 1.131 1.145 < 0.001
Operation −.370 14.642 .691 .572 .835 < 0.001
ICU admission .388 11.606 1.474 1.179 1.842 .001
Using ventilator .624 16.419 1.867 1.380 2.525 < 0.001
Using central line catheter 1.350 159.015 3.856 3.126 4.755 < 0.001
Using urinary catheter 1.047 102.414 2.848 2.325 3.488 < 0.001
Cerebral hemorrhage .329 5.662 1.389 1.060 1.821 .017
Cerebral infarction .370 20.308 1.448 1.233 1.701 < 0.001
Brain neoplasms .359 12.419 1.432 1.173 1.748 < 0.001
Diabetes mellitus .181 5.196 1.198 1.026 1.400 .023
Coronary artery disease .166 3.968 1.180 1.003 1.389 .046
Malignant tumor .162 5.946 1.176 1.032 1.339 .015
Malignant hematonosis 1.613 244.942 5.018 4.100 6.141 < 0.001
Notes: Binary multivariable logistic regression was performed. Statistical testing was performed at the conventional 2-tailed α = 0.05.OR Odds ratio CI confidence interval Only significant predictors are presented. Variables adjusted in the model include age, body weight, hospital days before HAI, operation, ICU admission, use of ventilator, central line catheter and urinary catheter and some neurological and chronic noncommunicable diseases (including cerebral hemorrhage, cerebral infarction, brain neoplasms, hypertension, diabetes mellitus, coronary artery disease, COPD, malignant tumor, malignant hematonosis and gynecological diseases)
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Availability of data and materials The datasets generated and/or analyzed during the current study are not publicly available due the data copyright protection of the author’s institute, but are available from the corresponding author on reasonable request.
Ethics approval and consent to participate The study design was approved by the ethics review board of Xuanwu Hospital, Capital Medical University. The director of Hospital Infection Management Division and the director of information center of Xuanwu Hospital, Capital Medical University, grant permission for access the raw data of the study.
Consent for publication Not applicable.
Competing interests The authors declare that they have no competing interests.
Author details 1Hospital Infection Management Division, Xuanwu Hospital, Capital Medical University, No.45 Changchun Street, Xicheng District, Beijing 100053, China. 2School of Health Management and Education, Capital Medical University, Beijing, China.
Received: 19 April 2019 Accepted: 10 July 2019
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Zhao et al. BMC Geriatrics (2019) 19:193 Page 6 of 6
- Abstract
- Background
- Methods
- Results
- Conclusion
- Background
- Methods
- Study design and data collection
- Statistical analysis
- Results
- The characteristics of the study elderly inpatients with and without HAI
- The potential association between risk factors and HAI
- Discussion
- Conclusion
- Abbreviations
- Acknowledgements
- Authors’ contributions
- Funding
- Availability of data and materials
- Ethics approval and consent to participate
- Consent for publication
- Competing interests
- Author details
- References
- Publisher’s Note