article

American Journal of Infection Control 48 (2020) 1216−1219

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American Journal of Infection Control

journal homepage: www.aj ic journal .org

Major Article

Chlorhexidine impregnated surgical scrubs and whole-body wash for reducing colonization of health care personnel

Karina Salazar-Vargas MD a, Magaly Padilla-Orozco MDb, Elvira Garza-Gonz�alez PhD c, Adri�an Camacho-Ortiz MD b,* a Department of Internal Medicine, Hospital Universitario Dr. Jos�e Eleuterio Gonz�alez, Facultad de Medicina, Universidad Aut�onoma de Nuevo Le�on, Monterrey, Nuevo Le�on, M�exico b Department of Hospital Epidemiology and Infectious Disease Service, Hospital Universitario Dr. Jos�e Eleuterio Gonz�alez, Facultad de Medicina, Universidad Aut�onoma de Nuevo Le�on, Monterrey, Nuevo Le�on, M�exico c Gastroenterology service, Hospital Universitario Dr. Jos�e Eleuterio Gonz�alez, Facultad de Medicina, Universidad Aut�onoma de Nuevo Le�on, Monterrey, Nuevo Le�on, M�exico

Key Words:

* Address correspondence to Adri�an Camacho-Ortiz, M Hospital Universitario Dr. Jos�e Eleuterio Gonz�alez, Univ Le�on, Madero y Gonzalitos s/n, Colonia Mitras Centro, M M�exico.

E-mail address: [email protected] (A. Camac Conflicts of interest: None to report.

https://doi.org/10.1016/j.ajic.2020.01.004 0196-6553/© 2020 Association for Professionals in Infect

Background: The use of chlorhexidine as a strategy to reduce nosocomial infections in patients has been proven useful. Bacterial contamination of health care worker’s uniforms during routine patient care has been demonstrated to have potential for horizontal transmission of pathogens. Methods: We performed a prospective, open comparative trial. We included nurses who were in direct patient care and evaluated clothing microbial growth during 3 interventions: (1) participants were given a sterile surgical scrub (SSS) to put on the beginning of the shift, (2) they were instructed to take a chlorhexi- dine bath (CHG-B) before putting on the SSS, and (3) participants were given a chlorhexidine impregnated SSS (CI-SSS). Cultures were obtained from 3 areas (chest pocket, chest, and abdominal) at hour 0, 6, and 12 hours after the start of the shift. Results: A total of 306 cultures processed with 17 bacterial groups. The uniform area with the highest num- ber of CFU was the abdomen (818 CFU), followed by the thorax (654 CFU). Over 50% of the bacterial load occurred at 12 hours (1,092 CFU at 12 hours, 766 CFU at 6 hours, and 184 CFU at 0 hour). There was a signifi- cant reduction in CFU when SSS was compared to CHG-B (CFU mean = 12.5 [0-118] vs CFU mean = 3.5 [0-22], P = .003); and SSS versus CI-SSS (CFU mean = 12.5 [0-118] vs CFU mean = 3 [0-39], P = .007). No severe adverse events were reported. Conclusions: Bacterial load in uniforms decreased when chlorhexidine was used (bathing of personnel or impregnation) when compared to the use of a sterile uniform. © 2020 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All

rights reserved.

Hospital aquired infections Bacterial count Infection control Gram positive cocci Gram negative bacili

D, Infectious Diseases Service, ersidad Aut�onoma de Nuevo onterrey 64460, Nuevo Le�on,

ho-Ortiz).

ion Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.

Pathogenic microorganisms transmitted within the hospital envi- ronment are a serious threat; because they considerably increase the incidence of health care-associated infections (HCAI), having a nega- tive impact on morbidity and mortality of patients, and hospital care costs.1-3

The patient's endogenous microbiota, the hospital environment, and transmission of pathogens by health care workers (HCWs) are the main factors related to HCAI.4

Standardized practices for infection control, including hand hygiene compliance, patient’s isolation, and contact precautions in patients infected or colonized with drug-resistant pathogens, are rec- ommended for the reduction of HCAI, especially in intensive care units (ICU).5-7 Furthermore, the use of chlorhexidine baths as a strat- egy to reduce the incidence of HCAI in patients in the ICU has been proven to be useful.2,4-7

Bacterial contamination of HCWs uniforms and clothing during routine patient care activities throughout a work shift has been demonstrated to have potential for horizontal transmission of pathogens.6,8-11 There is no evidence of the impact that chlorhexi- dine could have on HCW clothes or skin to decrease bacterial coloni- zation of uniforms; therefore, we aimed to determine the effect of the use of chlorhexidine on HCWs uniforms to reduce the bacterial load.

K. Salazar-Vargas et al. / American Journal of Infection Control 48 (2020) 1216−1219 1217

METHODS

Setting and study design

We performed a prospective, open comparative trial. The study was carried out at the Hospital Universitario “Dr. Jose Eleuterio Gon- zalez,” a 650-bed tertiary care hospital in Monterrey, Mexico.

Participants

The study outline was explained in detail to staff nurses, after which they were invited to participate voluntarily in the study. Writ- ten informed consent was obtained from those who agreed to partici- pate before any study procedures were done.

We included nurses who were in direct patient care in the 3 inter- nal medicine wards: 1 (30 beds), 2 (35 beds), and 3 (19 beds) with at least one 12-hour shift per week. The nursing staff activities included mobilization of patients, bathing, assessing vital signs, and adminis- tering medication. This 2-month study was performed in January and February 2019.

All participants with a history of hypersensitivity to chlorhexidine were excluded. We eliminated from the study participants who used additional garments such as a white coat, winter coat, sweaters, and others over the sterile uniform provided for the study.

Definitions and interventions

A sterile uniform consisted of a packed 2-piece sterilized surgical scrub (SSS) by dynamic-air-removal steam sterilization (Belimed, North Charleston, SC).

Chlorhexidine bathing (CHG-B) consisted of a whole-body bathing using 2% chlorhexidine impregnated wipes (Clorhexi wipes, PISA, Mex- ico) without water rinsing before putting on the SSS. A chlorhexidine impregnated-SSS (CI-SSS) refers to a sterile surgical scrub submerged in 0.12% chlorhexidine and left to dry in a sterile environment.

Three interventions were performed on the same study partici- pant during separate 12-hour shift on 3 different days (1 week apart each).

In the first intervention, participants were given a SSS to put on the beginning of the shift. In the second intervention, they were instructed to take a CHG-B before putting on the SSS, and in the third intervention, participants were given a CI-SSS without a CHG-B.

For all 3 interventions, participants were asked to take a regular shower at home before they begin the work shift, and they were asked not to use any additional garments during the 12-hour shift. Partici- pants were questioned regarding adverse events at every intervention.

Microbiological assays

For each intervention, bacterial loads in Colony Forming Units (CFU) were determined by culture taken from surgical scrubs. Cul- tures were obtained from 3 areas of surgical scrubs (chest pocket, chest, and abdominal area) at beginning of the shift (hour 0) and at hours 6 and 12 after the nursing staff started their shift.

Cultures were individually taken from different sites of the surgi- cal scrub using a 1 square inch sterile stainless steel plate designed for this study.

Using sterile gloves, the sterile steel plate was gently pressed from the inside of de surgical scrub to outside of the scrub onto a 5% sheep blood agar plate (Becton Dickinson, Cuautitl�an, Mexico) by 10 sec- onds. After, plates were incubated by 24-48 hours at 35°C-37°C and then examined for total colony count. Bacterial identification was performed by matrix-assisted laser desorption-ionization-time of flight mass spectrometry (MALDI-TOF MS) (Microflex LT system, Bruker Daltonics, Bremen, Germany).

Ethics approval

The study was reviewed and approved by the local ethics commit- tee with the code MI18-00022.

Statistical analysis

The Kolmogorov-Smirnov test was used to assess the normality of distribution. Student's t-test was used for continuous variables, and the chi-square test was used independent samples. A value of P ≤ .05 was considered as statistically significant. The SPSS program, version 22 was used for analysis.

RESULTS

Subjects included and species detected

A total of 10 nurses agreed to participate in the study, with a total of 306 cultures processed: 108 for the first intervention, 108 for sec- ond intervention, and 90 for the third intervention.

A total of 17 bacterial species or bacterial groups were detected, which were classified as skin microbiota, transient microbiota, and potential pathogens.

Species or groups detected as skin microbiota were: Coagulase- negative Staphylococcus, Bacillus spp., Micrococcus spp., and Strepto- coccus viridans. Species detected as transient microbiota were: Chrys- eobacterium spp., Corynebacterium spp., Rothia aeria, Brevibacterium casei, Aerococcus viridans, Macrococcus caseolyticus, Moraxella osloen- sis, Arthrobacter sulfonivorans, Neisseria subflava, and species detected as potential pathogens were: Staphylococcus aureus, gram-negative bacilli (including Acinetobacter spp.), and Enterococcus spp.

Bacterial loads

The distribution of CFU was counted according to classification through the study (Table 1). The uniform area with the highest num- ber of CFU was the abdomen region (818 CFU), followed by the thorax (654 CFU).

For the 3 interventions combined, more than 50% of the bacterial load occurred at 12 hours of using the surgical scrub (1,092 CFU at 12 hours, 766 CFU at 6 hours, and 184 CFU at 0 hour).

There was a significant reduction in CFU when first intervention (SSS) was compared to second intervention (CHG-B) (CFU mean = 12.5, range 0-118 vs CFU mean = 3.5, range 0-22, P = .0038); and when first and third (CI-SSS) interventions were compared (CFU mean = 12.5, range 0-118 vs CFU mean = 3, range 0-39, P = .0079). However, when comparing second and third interventions, no signif- icant reduction in the CFU was observed (P = .0671; Table 2).

In results of this study, 90% of the isolated bacterial species were classified as skin microbiota, and when only this classification was analyzed, bacterial loads were higher in first than in the second inter- vention group (P < .001) and no difference was detected between second and third interventions.

Interestingly, lower bacterial loads were found in chlorhexidine groups (second and third interventions) when compared to the non- chlorhexidine group (fist intervention; P < .001; Table 2).

Specific reduction for Staphylococcus spp. was detected between the first and the second interventions and the first and the third interventions (P < .001 for both).

Gram-negative bacilli were more frequently found in the first intervention group (30 total CFU, average 0.27, range 0-7) when com- pared to second intervention (9 total CFU, average 0.10, range 0-3) and the third intervention (14 total CFU, average 0.12, range 0-3), but the difference was not significant (P = .335).

Table 1 Bacterial loads in total of colony-forming units (CFU) in all 3 interventions

First intervention: SSS Second intervention: CHX-B Third intervention: CI-SSS

Time of culture (h) Area Mean CFU count (range) CFU % Mean CFU count (range) CFU % Mean CFU count (range) CFU %

0 Chest 4.83 (0-26) 4 0.4 (0-2) 1 0.5 (0-3) 1 Chest pocket 1.91(0-10) 2 0.8 (0-7) 3 0 (0-0) 0 Abdominal area 4.0 (0-18) 4 2.6 (0-22) 8 1.2 (0-7) 3 Subtotal 3.58 (0-26) 10 1.26 (0-22) 12 0.56 (0-7) 4

6 Chest 7.41(0-17) 7 3.3 (0-7) 10 3.8 (0-8) 10 Chest pocket 17.16 (2-124) 15 3.1 (0-7) 10 3.3 (1-11) 9 Abdominal area 16.5 (2-57) 15 5.4 (1-12) 17 8.4 (0-39) 22 Subtotal 13.69 (0-104) 37 3.93 (0-12) 37 5.16 (0-39) 41

12 Chest 26.75 (5-118) 24 6.3 (1-16) 20 4.3 (0-9) 11 Chest pocket 16.0 (0-42) 14 4 (0-10) 13 3.7(0-12) 10 Abdominal area 17.91(3-55) 16 5.8 (0-18) 18 12.3 (0-102) 33 Subtotal 20.22 (0-118) 54 5.36 (0-18) 51 6.7 (0-102) 54

Total Mean 12.5 (0-118) 100 2.93 (0-22) 100 3.47 (0-102) 100 Number of CFU 1350 317 375

CHX-B, chlorhexidine bath; CI-SSS, chlorhexidine impregnated-sterile surgical scrub; SSS, sterile surgical scrub.

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Adverse events

During the study, one of the participants presented general pruri- tus after the bathing with 2% chlorhexidine impregnated wipes; no skin lesions were noted on physical examination. The participant received an oral dose of chlorpheniramine (8 mg), and pruritus disap- peared almost instantaneously. The participant had used chlorhexi- dine for regular hand washing previously on multiple occasions and had no history of adverse events. Participant was excluded from con- tinuing in the study. No other adverse events were reported.

DISCUSSION

Health personnel uniforms can be reservoirs of potential micro- bial pathogens, and their contamination frequently occurs in the first hours after use.8,12,13 In this study, we aimed to determine the effect of 3 interventions on HCW uniforms to reduce the bacterial load and detected that the use of chlorhexidine in HCWs (both by bathing of personnel and by the use of chlorhexidine in the uniforms) decreases the bacterial load of species considered as skin microbiota during a 12-hour work shift (P < .001), when compared to a sterile uniform. This is interesting because the postantiseptic effect of chlorhexidine is described to be 6 hours,4,20,21 and the reduction of CFU was still sig- nificant at 12 hours.

It should be noted that no significant reduction in the number of bacterial colonies of gram-negatives species considered as potential pathogens was observed, and although the number of CFU in all the

Table 2 Distribution of group of isolates recovered during the 3 interventions of the study

Microbiota

Intervention Culture area Skin Opportunistic Transient

First (SSS) Thorax 461 5 2 Chest pocket 371 15 35 Abdomen 392 13 56 Total 1224 33 93

Second (CHX-B) Thorax 89 3 8 Chest pocket 74 1 4 Abdomen 131 5 2 Total 294 9 14

Third (CI-SSS) Thorax 80 4 2 Chest pocket 67 3 0 Abdomen 212 7 0 Total 359 14 2

P value SSS vs CHX-B .0006 .070 .171 P value SSS vs CI-SSS .0058 .125 .126

interventions was low, the use of chlorhexidine interventions described in this work should not be considered protective against these bacterial species.

Resistance to CHG is a concern every time you expose microorgan- isms to sublethal concentrations of CHG,22 although concentrations used in the study protocol are well above the MICs of common noso- comial bacterial pathogens, we favor caution when CHG is use for pro- longed periods of time.

There is growing evidence supporting the use of short-sleeved uniforms compared to the traditional white coats and long sleeve coats commonly used in the hospital setting.5,10,12,15,16 In this study, all uniforms were short sleeve and although high touch areas such as the chest pocket and abdomen were studied we cannot assure that the same pathogens might colonize sleeves of other medical attire.

Well-documented studies demonstrate the positive effects achieved by using chlorhexidine bathing on patients,14,17-19 and before this study, there was no evidence of those effects bathing HCW in order to reduce bacterial growth in garments or the use of chlorhexidine directly on hospital attire for those purposes. Our results support that in specific conditions, this alternative may be useful in reducing the bacterial loads in HCWs, especially of bacterial species considered as skin microbiota.

The direct impact of pathogens in HCWs attire on the incidence of HCAI remains unknown thus, the impact of HCW attire bioburden reduction on clinical outcomes is unknown and debatable. The feasi- bility of sustained CHG SSS implementation as well as cost/benefit scaled across a health care system remains untested. Further studies are warranted to assess the efficacy of CHG-SSS as an infection pre- vention strategy although the current study gives way to test other forms of CHG in surgical and medical attire.

In our hospital, there is less than 1% of HCW have reported hyper- sensitivity reactions to CHG among those who use CHG soap for hand washing (unpublished data), and although there are reports of mod- erate and severe dermatitis associated with CHG use23 all of the reac- tions in our experience have been classified as mild; we observed the same pattern when CHG was used in whole body bath and in attire in this study.

We acknowledge some limitations of the study, mainly that the data were obtained from a single teaching hospital, and only the nursing staff of the department of internal medicine were studied, also the long-term effects and tolerability of chlorhexidine baths among HCW was not explored in the study since the effects were analyzed only during a 2-month span; thus, we cannot generalize these results for other types of institutions, other staff, or other services.

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CONCLUSIONS

The bacterial load in personnel uniforms decreased when chlor- hexidine was used (both by bathing of personnel or by cloths impreg- nation) when compared to the use of a sterile uniform. No difference was observed in bacterial load of potential pathogens, thus not justi- fying the effort of chlorhexidine using in HCW.

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