Infection

RESEARCH ARTICLE

Adherence to evidence-based

recommendations for surgical site infection

prevention: Results among Italian surgical

ward nurses

Rossella Zucco 1 , Francesco Lavano

1 , Carmelo G. A. Nobile

2 , Rosa Papadopoli

1 ,

Aida BiancoID 1*

1 Department of Health Sciences, University of Catanzaro "Magna Græcia", Catanzaro, Italy, 2 Department

of Pharmacy, Health and Nutritional Sciences, University of Calabria, Cosenza, Italy

* [email protected]

Abstract

Background

The aims of the study were to assess the level of knowledge, the attitudes and the adher-

ence to evidence-based recommendations for surgical site infection (SSI) prevention and to

describe any influences that may motivate nurses to adopt evidence-based practices for

SSI prevention.

Methods

The present study was a national cross-sectional survey conducted from June to November

2017. For each hospital that agreed to participate, 30 nurses were randomly selected. The

questionnaire was aimed at exploring socio-demographic and practice characteristics,

knowledge of, attitudes toward, and reported practices regarding evidence-based proce-

dures for SSI prevention.

Results

Out of 55 hospitals that were contacted, 36 agreed to participate (a response rate of 65%).

Of the original sample of 1313 nurses, a total of 1305 returned the questionnaire, a response

rate of 99.4%. Regarding knowledge, only 53.8% knew that preoperative hair removal, if

necessary, should take place shortly before surgery, and 28.9% of the sample did not know

the right definition of “bundle”. Over three quarters of participants stated that they always

perform hand antisepsis before and after biological sample collection while 9.7% considered

that wearing gloves during this practice is sufficient to prevent SSI. Furthermore, 91% of

nurses reported that they always performed hand antisepsis before and after invasive

procedures.

PLOS ONE | https://doi.org/10.1371/journal.pone.0222825 September 26, 2019 1 / 13

a1111111111

a1111111111

a1111111111

a1111111111

a1111111111

OPEN ACCESS

Citation: Zucco R, Lavano F, Nobile CGA,

Papadopoli R, Bianco A (2019) Adherence to

evidence-based recommendations for surgical site

infection prevention: Results among Italian surgical

ward nurses. PLoS ONE 14(9): e0222825. https://

doi.org/10.1371/journal.pone.0222825

Editor: Italo Francesco Angelillo, University of

Campania, ITALY

Received: July 5, 2019

Accepted: September 9, 2019

Published: September 26, 2019

Copyright: © 2019 Zucco et al. This is an open access article distributed under the terms of the

Creative Commons Attribution License, which

permits unrestricted use, distribution, and

reproduction in any medium, provided the original

author and source are credited.

Data Availability Statement: All relevant data are

within the manuscript and its Supporting

Information files.

Funding: The authors received no specific funding

for this work.

Competing interests: The authors have declared

that no competing interests exist.

Conclusion

The study findings highlight the areas that were most lacking in nurses’ training and for

which targeted activities are needed. These data could support healthcare managers to

implement interventions focused at enabling adherence to effective prevention practices to

reduce risk to all patients.

Introduction

Healthcare-associated infections (HAIs) represent a major threat to patient safety, leading to

significant morbidity, mortality and financial losses for health systems worldwide [1]. In high-

income countries, 7 out of every 100 hospitalized patients develop at least one HAI [1].

A prevalence study found that surgical site infections (SSIs) account for 31% of all HAIs

among hospitalized patients [2]. In the United States, SSIs occur in 2–5% of patients undergo-

ing surgery [3], ranging from 160,000 to 300,000 cases per year [4]. In Europe, the incidence of

SSIs can reach about 20%, depending on the surgical procedure and the quality of the data col-

lected [5]. SSIs are associated with prolonged duration of hospitalization, readmissions, re-

interventions, permanent disability or even death [6,7]. Moreover, data from the USA show

that between 38.7% and 50.9% of pathogens isolated from infected surgical wounds have anti-

biotic resistance patterns [8].

It has been estimated that approximately half of SSIs are preventable by application of evi-

dence-based strategies [9]. Several risk factors for SSIs have been identified and prevention

requires the integration of a range of measures performed before, during, and after surgery

[10]. Various evidence-based recommendations have been published for the prevention of

SSIs [11], such as those of the National Institute for Clinical Excellence (NICE) in the UK [12]

and the surgical care improvement project (SCIP) of the USA [13] which have identified a

number of practices that healthcare workers (HCWs) should adopt. More recently, the World

Health Organization (WHO) set out 29 recommendations for the prevention of SSIs [14].

Accordingly, an expert consensus provided the best available scientific evidence to ensure

high-quality care for every patient, irrespective of the available resources [15,16]. Despite the

widespread availability of evidence-based guidelines, SSI rates have not measurably fallen. This

is probably due to poor knowledge of and/or non-compliance with correct practices [17], espe-

cially among the nurses that can play a leading role in initiatives that aim to minimize the risk

of SSIs [18]. The aims of this study were, therefore, to assess the level of knowledge, the atti-

tudes and adherence to evidence-based recommendations for SSI prevention and to describe

any influences that may motivate nurses to adopt evidence-based practices for SSI prevention.

Methods

The national cross-sectional survey was conducted from June to November 2017, using multi-

stage sampling. First, we stratified our population by region, for each of the 20 Italian regions.

Then, within each stratum, we selected by simple random sampling one regional general hos-

pital and one district general hospital. Regional hospitals have an autonomous direction/man-

agement and provide highly specialized healthcare, whereas district hospitals, which are

directed by Local Health Units, provide a high-standard but a lower complex level of care. The

aims of the study were delineated to members of the management staff of the selected hospitals

by telephone, and at the same time verbal consent was obtained from them in order for the

Surgical site infections prevention among nurses

PLOS ONE | https://doi.org/10.1371/journal.pone.0222825 September 26, 2019 2 / 13

study to be carried out at their institution. In case permission was refused, we randomly chose

a similar type of hospital setting within the same region, with the methodology described

above, and so forth, until consent was given. Non-responder hospitals were contacted every

week by phone and by two e-mail reminders. For each hospital that agreed to participate, 30

questionnaires were mailed along with a numbered roster of nurses working in general or spe-

cialist surgical wards, operating rooms and critical care units and instructions for randomly

selecting 30 nurses. Potential participants were informed of the purpose of the study, its volun-

tary nature together with the stipulation that they could terminate their participation at any

stage of the survey. Subsequently, we obtained their verbal consent which was confirmed by

their participation.

The first version of the questionnaire was given to a convenience sample of 50 nurses and

was pilot-tested a month before the start of the study, to evaluate item clarity and to estimate

comprehensibility; it was subsequently modified to improve the issues noted.

The questionnaire was divided into five sections: (I) socio-demographic and practice char-

acteristics (age, gender, ward, number of years in practice, numbers of years from graduation);

(II) knowledge about risk factors and evidence-based practices for SSI prevention; (III) atti-

tudes toward prevention of infectious risk and evidence-based practices on SSI prevention;

(IV) reported practices regarding evidence-based procedures for SSI prevention; (V) main

sources of information about SSI prevention. The questionnaire was anonymous and confi-

dentiality of the collected data was assured.

The items of the structured questionnaire used in this study were developed in accordance

with WHO guidelines for SSI prevention [14] and after an extensive review of the literature

[10,15,16].

Knowledge was tested through five statements allowing responses on a five-point Likert

scale (‘strongly agree’, ‘agree’, ‘uncertain’, disagree’ and ‘strongly disagree’). To assess the atti-

tudes, nurses were asked to rate the effectiveness of 9 procedures in preventing SSIs on a scale

from 1 to 10 (1 = ineffective and 10 = very effective). The practices adopted by the nurses for

preventing SSIs were investigated through questions in closed-ended format and on a 5-point

Likert scale (never, rarely, sometimes, often, always). Finally, nurses were asked to judge their

knowledge level through a 4-point scale ("insufficient", “sufficient”, "good", “excellent”), and to

indicate the sources of information they used to update their knowledge about prevention of

SSIs and to state whether they felt the need to acquire further information on prevention of

SSIs. The study protocol and the consent process were approved by the Ethical Committee of

the Calabria Region–Central area (27 April 2017).

Statistical analysis

Descriptive analyses were performed to present socio-demographic and practice characteris-

tics of participants. Chi-square and student’s t-test were used to test the association between

the outcome of interest and the independent variables. All independent variables with a p-

value less than or equal to 0.25 were considered eligible for inclusion into the multivariate

regression analysis. Multivariate stepwise logistic regression analysis was performed to deter-

mine the potential predictors of the proper hand antisepsis (no = 0, yes = 1). The proper hand

antisepsis was defined as the reduction or inhibition of the growth of microorganisms by the

application of an antiseptic hand rub or by performing an antiseptic handwash. The following

explanatory variables were included in the model: gender (male = 0 female = 1); hospital wards

(general surgery = 0, specialist surgery = 1, critical area = 2); numbers of years from graduation

(1–15 = 0, 16–30 = 1, >31 = 2); numbers of years in practice as a nurse (<6 = 0, 6–10 = 1,

>10 = 2); knowledge about smoking as a risk factor for the onset of SSIs (disagree/strongly

Surgical site infections prevention among nurses

PLOS ONE | https://doi.org/10.1371/journal.pone.0222825 September 26, 2019 3 / 13

disagree/uncertain = 0, agree/strongly agree = 1); knowledge that a care bundle is a set of 3–5

evidence-based practices that has been proven to improve patient outcomes (disagree/strongly

disagree/uncertain = 0, agree/strongly agree = 1); knowledge that the preoperative hair

removal, if necessary, should take place shortly before surgery (agree/strongly agree/uncer-

tain = 0, strongly disagree/disagree = 1); epidemiological surveillance system of SSIs in place in

the hospital (no = 0, yes = 1); protocol for SSI prevention in place in the hospital (no = 0,

yes = 1); attitudes toward preoperative checklist signaling patients with systemic infection

(poorly effective = 0, mildly effective = 1, highly effective = 2); attitudes toward change of

soiled surgical gowns (poorly effective = 0, mildly effective = 1, highly effective = 2); and utili-

zation of triclosan-coated sutures (poorly effective = 0, mildly effective = 1, highly effective = 2),

attitudes toward effectiveness of minimize the utilization of immediate-use steam sterilization

(poorly effective = 0, mildly effective = 1, highly effective = 2); utilization of adhesive drapes

for surgical incision (never, rarely, sometimes = 0; often, always = 1) and the need to improve

their own knowledge about SSI prevention (no/not sure = 0, yes = 1).

Stata version 14 statistical software package was used in conducting all data analysis [19].

Results

Study population

Out of 55 hospitals that were contacted, 36 agreed to participate and were included in the

study (response rate of 65%). Of the original sample of 1313 nurses, a total of 1305 returned

the questionnaire, for a response rate of 99.4%. The mean age of participants was 44.9 (± 9.9 SD) years, 74.8% were females and the majority of nurses had graduated more than 20 years

previously. The mean number of years in hospital practice was 12.5 (± 10.4 SD) and 22.8% of the sample had a master’s degree.

Knowledge of and attitudes toward evidence-based practices for SSI prevention.

Table 1 reports the nurses’ level of knowledge of and attitude toward evidence-based practices

for SSI prevention. Almost all (90.7%) correctly identified obesity as a risk factor for the onset

of SSIs and 74.2% also recognized the role of smoking as a risk factor for the onset of SSIs.

When assessing knowledge on strategies for SSI prevention, more than two thirds (73%) of the

participants knew that the appropriate time for shower or bath with an antiseptic agent is the

day before surgery, but only 53.8% knew that preoperative hair removal, if necessary, should

take place shortly before surgery. Moreover, 28.9% of the sample did not know the right defini-

tion of “bundle”. When nurses were asked to rate the effectiveness of some interventions for

SSI prevention, dressing change if it is visibly soiled received the highest score (8.9). The belief

that the utilization of immediate-use steam sterilization in the operating room should be mini-

mized received the lowest score (4.7).

Self-reported evidence-based practices for SSI prevention. Over three quarters (75.2%)

of participants stated that they always perform hand antisepsis before and after biological sam-

ple collection (Table 2), while 9.7% considered that wearing gloves during this practice is suffi-

cient to prevent SSIs. Furthermore, 91% of nurses reported to always perform hand antisepsis

before and after invasive procedures (e.g. peripheral intravenous catheter insertion, urethral

catheterization, etc.). A vast majority of respondents (93.2%) “always/often” reported the utili-

zation of single-use protective equipment in patients with an infectious disease. Only 14.1% of

respondents reported the proper duration of antibiotic prophylaxis (<24 hours after surgery)

in their unit. 77% of the sample self-reported that a wound culture was performed in case of

SSI signs and/or symptoms. When investigating the replacement of the wound dressing, only

55.1% of the sample reported the correct frequency for changing of the dressing, and 61.9% of

nurses reported the utilization of adhesive drapes.

Surgical site infections prevention among nurses

PLOS ONE | https://doi.org/10.1371/journal.pone.0222825 September 26, 2019 4 / 13

The results of bivariate and multivariate analyses are reported in Table 3. These data show

that proper hand antisepsis was significantly less likely in nurses who had graduated 16–30

years previously (OR = 0.60, 95% IC = 0.42–0.84), compared with those who had graduated

within the last 15 years and also in those who believed that minimize the utilization of immedi-

ate-use steam sterilization is mildly effective for the reduction of SSI incidence (OR = 0.63,

95% IC = 0.40–0.99), compared with those who considered it poorly effective. However, it was

more likely in respondents with correct knowledge about smoking as a risk factor for SSIs

(OR = 1.57, 95% IC = 1.10–2.23), and about the care bundle (OR = 1.59, 95% IC = 1.14–2.22),

and in those who reported the utilization of adhesive drapes for surgical incision (OR = 1.41,

95% IC = 1.02–1.95).

Questions concerning sources of information indicated that respondents learned about evi-

dence-based practices for SSI prevention mainly from guidelines (73.6%) and continuing edu-

cation courses (51.6%). Nearly three quarters (74.2%) of respondents reported that a

surveillance system of HAIs was in place in their hospital and 43.3% of the sample attended

prevention and control audits. An interesting result was that 97.8% of the nurses reported an

interest in more education to improve their knowledge about SSI prevention.

Discussion

To our knowledge, this study represents one of the first attempts to explore the knowledge,

attitudes and evidence-based practices related to the prevention of SSIs among Italian nurses.

The nursing staff plays a pivotal role in the prevention of the SSIs [18] and they need to be

aware of the relevance of related complications.

The results of the study showed some knowledge gaps among nursing staff. Indeed, about

half of the sample had inadequate knowledge about the correct timing of preoperative hair

Table 1. Nurses’ knowledge of and mean score of attitudes toward SSIs.

Knowledge Correct answer

N (1305)� %

Obesity is a risk factor for the onset of SSIs 1178

(1299)

90.7

Smoking is a risk factor for the onset of SSIs 960 (1293) 74.2

The recommended time for antiseptic shower is the day before surgery 937 (1284) 73

A bundle is a set of 3–5 evidence-based practices that have been proven to improve patient

outcomes

845 (1188) 71.1

Preoperative hair removal, if necessary, should take place shortly before surgery 688 (1258) 53.8

Attitudes Mean

Score

(± SD)

Extraordinary operating room cleaning procedures after contaminated or dirty infected

surgery

8.9 2.0

Dressing change, if it is visibly soiled 8.9 2.2

Preoperative checklist, signaling patients with a preexisting infection at sites remote from the

surgical area

8.4 2.4

Clipping hair removal 8.0 2.5

Pre-operative shower with aseptic agents 7.5 2.8

Hair removal 7.4 3.0

Triclosan-coated suture utilization 6.9 2.8

Minimize the utilization of immediate-use steam sterilization 4.7 3.3

SSIs: Surgical site infections

� Total may not always sum to N because of missing data.

https://doi.org/10.1371/journal.pone.0222825.t001

Surgical site infections prevention among nurses

PLOS ONE | https://doi.org/10.1371/journal.pone.0222825 September 26, 2019 5 / 13

removal. Moreover, about 30% of the sample did not know what a bundle is, which is of con-

cern since “care bundles” are evidence-based practices and have been introduced for the pre-

vention of SSIs. In addition to optimizing care and minimizing the risk of SSIs, the care

bundle is also an actual demonstration of the quality of surgical patient care in the wards [10].

Although a vast majority of the sample recognized the effectiveness of some evidence-based

practices in the reduction of the occurrence of SSIs as recently updated by the WHO guidelines

[14], a lower score was achieved for other evidence-based practices, such as preoperative show-

ering with aseptic agents, recommended the day of the operation or the day before, and the

use of triclosan-containing sutures. To date, several controlled trials [20–22] and meta-analy-

ses [23,24] showed a clinically and statistically significant effect of triclosan-containing sutures

in the reduction of SSIs, although the strength of recommendation regarding their use was

considered conditional by WHO [16]. Moreover, the finding that to minimize the utilization

of immediate-use steam sterilization in the operating room received a low score of effective-

ness deserves a comment. This is an important topic that requires the attention of operating

Table 2. Self-reported evidence-based practices on SSI prevention.

N %

Hand antisepsis procedures (1288)

Before and after dressing replacement at the insertion of CVC 1188 92.4

Before and after invasive procedures 1172 91

Before and after intravenous therapy 1105 86.1

Before and after intramuscular therapy 1099 85.9

Before and after biological sample collection 969 75.6

Frequency of sterile gauze dressing replacement after surgery (1175)

�48 hours 392 32.9

>48 hours 643 55.1

Not sure 140 12

Single-use protective equipment utilization in patients with an infectious disease (1273)

Never/Rarely 35 2.8

Sometimes 34 2.7

Always/Often 1187 93.2

Not sure 17 1.3

Using of impermeable gowns during surgical procedure (1187)

Never/Rarely 74 6.3

Sometimes 48 4

Always/Often 646 54.4

Not sure 419 35.3

Performing wound culture in case of SSI signs and/or symptoms (1264)

Never/Rarely 66 5.2

Sometimes 186 14.7

Always/Often 973 77

Not sure 39 3.1

Adhesive drapes for surgical incision (1218)

Never/Rarely 58 4.8

Sometimes 66 5.4

Always/Often 754 61.9

Not sure 340 27.9

SSIs: Surgical site infections, CVC: Central vascular catheter.

https://doi.org/10.1371/journal.pone.0222825.t002

Surgical site infections prevention among nurses

PLOS ONE | https://doi.org/10.1371/journal.pone.0222825 September 26, 2019 6 / 13

Table 3. Results of the bivariate and multivariate analyses.

Proper hand antisepsis

Bivariate Multivariate

Log likelihood = -470.38 χ2

= 51.8, 17 df, p<0.00001

Variable N % OR 95% CI

Gender

Male 192 60 1.00

Female 623 65.7 1.21 0.85–1.72

χ2 = 3.40, 1 df, p = 0.06

Hospital wards:

General surgery 240 68.8 † †

Other surgery 514 62.5

Critical area 55 63.2

χ2 = 4.20, 2 df, p = 0.12

Numbers of years in practice as a nurse

<6 283 68.4 1.00

6–10 137 65.9 1.23 0.81–1.87

>10 359 60.7 † †

χ2 = 6.4, 2 df, p = 0.04

Numbers of years from graduation

<15 284 69.4 1.00

16–30 332 58.9 0.60 0.42–0.85

> = 31 151 67.4 0.76 0.47–1.24

χ2 = 12.8, 2 df, p = 0.002

Knowledge

-smoking is a risk factor for the onset of SSIs

Disagree/strongly disagree/uncertain

Agree / strongly agree 187 56.2 1.00

645 67.2 1.57 1.11–2.23

χ2 = 13.1, 1 df p<0.001

-obesity is a risk factor for the onset of SSIs

Disagree/strongly disagree/uncertain 69 57 � �

Agree / strongly agree 765 64.9

χ2 = 2.99, 1 df, p = 0.08

-preoperative hair removal should take place shortly before surgery

Agree / strongly agree/uncertain 358 60.7 1.00

Disagree/strongly disagree 224 32.6 1.32 0.95–1.84

χ2 = 6.33, 1 df, p = 0.01

-a bundle is a set of 3–5 evidence-based practices that have been proven to improve patient outcomes

Disagree/strongly disagree/uncertain 203 59.2 1.00

Agree / strongly agree 561 64.4 1.59 1.14–2.22

χ2 = 5.52, 1 df, p = 0.01

Epidemiological surveillance system of SSIs in place in the hospital

No/ uncertain 205 61 † †

Yes 315 34.1

χ2 = 2.58, 1 df, p = 0.10

Protocol for SSI prevention in place in the hospital

No/ uncertain 191 58.9 † †

(Continued)

Surgical site infections prevention among nurses

PLOS ONE | https://doi.org/10.1371/journal.pone.0222825 September 26, 2019 7 / 13

room personnel. This process was initially intended for a single instrument, and when per-

formed correctly and when deemed appropriate, immediate-use steam sterilization is an effec-

tive and safe way to sterilize critical devices. However, it has become routine in some

operating rooms, which is beyond the original intent of the process. The risk of serious

Table 3. (Continued )

Proper hand antisepsis

Bivariate Multivariate

Log likelihood = -470.38 χ2

= 51.8, 17 df, p<0.00001

Variable N % OR 95% CI

Yes 615 66.2

χ2 = 5.50, 1 df, p = 0.01

Written policy about hand antisepsis in place in the hospital

No/ uncertain 48 57.1 1.00

Yes 412 34.6 1.39 0.74–2.61

χ2 = 2.33, 1 df, p = 0.12

Need to improve nurses’ own knowledge about SSs prevention

No/ uncertain 11 39.3 1.00

Yes 797 65.2 1.85 0.66–5.20

χ2 = 8.01, 1 df, p = 0.005

Attitudes

-preoperative checklist signaling patients with systemic infection

Poorly effective (1–5) 82 56.2 1.00

Mildly effective (6–7) 84 63.2 1.85 0.98–3.48

Highly effective (8–10) 655 66.2 1.38 0.84–2.27

χ2 = 5.72, 2 df, p = 0.05

-minimize the utilization of immediate-use steam sterilization

Poorly effective (1–5) 486 67.2 1.00

Mildly effective (6–7) 101 58.7 0.63 0.40–0.99

Highly effective (8–10) 200 61.9 0.66 0.45–0.98

χ2 = 5.78, 2 df, p = 0.05

-change of soiled surgical gowns

Poorly effective (1–5) 64 57.7 1.00

Mildly effective (6–7) 40 57.1 † †

Highly effective (8–10) 372 33.9 1.67 1.05–2.68

χ2 = 5.72, 2 df, p = 0.05

-triclosan-coated sutures utilization

Poorly effective (1–5) 241 63.9 1.00

Mildly effective (6–7) 131 60.9 † †

Highly effective (8–10) 390 66.9 1.21 0.86–1.72

χ2 = 2.77, 2 df, p = 0.25

Adhesive drapes for surgical incision

Never/rarely/sometimes/uncertain 286 61.6 1.00

Often/always 497 65.9 1.41 1.02–1.95

χ2 = 2.28; 1df, p = 0.130

SSIs: Surgical site infections.

�not included in the model.

† removed by the model.

https://doi.org/10.1371/journal.pone.0222825.t003

Surgical site infections prevention among nurses

PLOS ONE | https://doi.org/10.1371/journal.pone.0222825 September 26, 2019 8 / 13

consequences, including SSIs, necessitates that all operating rooms reduce their reliance and

use of this process.These data highlight the areas that were most lacking in the nurses’ training

for which targeted activities are needed. Indeed, knowledge and attitudes were found to be the

strongest predictors of the investigated evidence-based practices. These findings, that are com-

parable with results across the literature [25–27], highlight how an update in knowledge

regarding SSI prevention performed through educational programs could positively affect atti-

tudes and, ultimately, tendency to perform current evidence-based practices [28,29].

The finding that more than half of nurses reported the utilization of adhesive drapes

deserves a comment, considering the lack of evidence that plastic adhesive incise drapes (with

or without antimicrobial properties) prevent SSI. It is alarming given the moderate/very low

quality of the available evidence supporting that practice. Another important study finding to

highlight is that even standard operating procedures, such as hand antisepsis, were often not

performed accurately (by the application of an antiseptic hand rub or by performing an anti-

septic handwash), and similar results were found in a previous study performed to evaluate

handwashing compliance amongst Italian HCWs [25]. It is well-known that hand antisepsis is

meant to eliminate the transient microorganisms and to inhibit the growth of resident micro-

organisms and, ideally, to maintain the microbial release from the hands below baseline until

the end of the procedure [30]. However, some nurses considered that wearing gloves during

this practice is sufficient to prevent SSIs. This finding is also worrying since glove use may

result in missed opportunities for hand hygiene, and gloves reduce transmission of pathogens

only if they are used appropriately and timely hand hygiene is performed [31].

The study findings provide an opportunity to highlight the need of a wound culture in case

of SSI signs and/or symptoms. It may be argued that the diagnosis of a SSI could be left to the

physician clinical judgment as wound swabs take days to produce results. Any suspected surgi-

cal site infection should have wound swabs taken for culture at the site, also for epidemiologi-

cal reasons. Indeed, surveillance of SSI with feedback of appropriate data has been shown to be

an important component of strategies to reduce SSI risk [11].

We found a statistically significant association between the number of years in practice and

the investigated outcome of interest. As the number of years in practice increases, HCWs

become more experienced about infection prevention through working with senior medical

staff. Moreover, with increasing work experience in clinical settings, their motivation for fur-

ther learning and respecting updated guidelines will increase [32].

The finding that a tiny percentage (14.1%) of respondents reported the proper duration of

antibiotic prophylaxis (<24 hours after surgery) in their unit is unacceptable, and we are of the

opinion that physicians tend to overuse antibiotics i.e. prescribing prophylaxis when not indi-

cated, rather than underuse them i.e. not prescribing prophylaxis when indicated, in agree-

ment with previously published observations [33,34]. It is probable that physicians are more

concerned about the risk of SSIs than the risks related to an excess or inappropriate use of anti-

biotics, such as the emergence of resistant microorganisms.

HAI surveillance systems and SSI prevention protocols are in place in only about two-thirds

of the hospitals involved in the study. This is of concern, since the value of HAI surveillance

together with appropriate infection control activities was established almost four decades ago

in the Study on the Efficacy of Nosocomial Infection Control where it was demonstrated that

hospitals without surveillance systems had increased HAI rates [35]. Routine surveillance of

SSI with feedback of appropriate data has been shown to be an important component of strate-

gies to reduce HAI and SSI risk. Almost half of the sample reported attending audits or

rehearsals of care practices and almost all nurses think they need to improve their knowledge.

Routine surveillance of HAIs should become an integral part of infection prevention and

Surgical site infections prevention among nurses

PLOS ONE | https://doi.org/10.1371/journal.pone.0222825 September 26, 2019 9 / 13

quality assurance in hospitals [36] together with a need to implement activities aimed at shar-

ing and standardizing welfare practices in the surgical unit.

Strengths and limitations

The study achieved a very satisfactory response rate (99.4%) which is high enough to limit one

of the main potential source of bias in the results. Furthermore, it emphasizes the quality of the

study as a result of the time and effort devoted to improving it, as well as the important subject

matter involved. Another strength of this study is that the selected sample is representative of

the Italian nurses working in surgical departments, and, therefore, the study results may be

readily generalized to this population.

However, there are some potential limitations in the design and measurements of this study

that should be considered when interpreting the results. As always, self-reporting is subject to

bias as one cannot overrule the possibility of intentional deception on the part of the respon-

dent or incorrect responses due to a poor memory or a misunderstanding of the questions, all

of which can result in erroneous reporting of actual behavior. To undertake direct observation

is not feasible due to the expense involved and may also influence behavior. However, the

assurances given to the respondents regarding anonymity ensures that the responses given

were a true reflection of their knowledge and behavior. Whist there was a small number of

non-responders whose characteristics would be difficult to determine, there is no reason to

suspect that they were any different from the responders.

Conclusion

Despite these limitations, this survey resulted in important findings with respect to knowledge,

attitudes, and evidence-based practices associated with SSI prevention. Although changing

behavior is a very complex process, providing education regarding the outcomes associated

with SSIs, risks for SSIs, and methods focused at enabling adherence to effective prevention

practices to reduce risk to all patients, appears to lead to changes in attitudes and contribute to

improvement in practice. Behavior changes should also be aimed at abandoning outdated

practices and adopting and maintaining evidence-based practices.

Supporting information

S1 File. Appendix. Questionnaire (translated into English).

(DOC)

S2 File. Appendix. Questionnaire (original).

(DOC)

Acknowledgments

We extend our sincere thanks to the Collaborative Working Group, who are as follows: Laura

Bertola MD and Maurizio Salvatico MD (ASL Cn1), Giacomo Scaioli MD (AOU “Città della salute e della scienza di Torino”), Roberto Novati MD (USL Valle d’Aosta), Mariavalentina

Giordano MD (ASST Sette Laghi), Claudio Casella MD (Casa di cura Ambrosiana), Peter

Santa MD (Azienda Sanitaria dell’Alto Adige), Lorenzo Tognon MD (ULSS 1 Dolomiti), Fran-

cesca Malacarne MD (Università degli studi di Udine), Cristiano Alicino MD (ASL 2 Savo- nese), Maria De Martini MD (ASL 3 Liguria), Sandra Serra MD (AUSL Bologna), Laura

Cavazzuti MD (AUSL Reggio Emilia), Silvana Pilia MD and Corrado Tonelli MD (USL

Toscana sud-est), Klaus Beermann MD (AOU“Meyer”), Gioia Calagreti MD (USL Umbria 1),

Surgical site infections prevention among nurses

PLOS ONE | https://doi.org/10.1371/journal.pone.0222825 September 26, 2019 10 / 13

Marilena Spadafora MD (USL Umbria 2), Remo Appignanesi MD (ASUR zona 12 Marche),

Patrizia Alori MD (AOU Ancona), Carolina Marzuillo MD and Domenico Barbato MD (AOU

“Umberto I”) Maria Antonietta Pompeo MD (ASL 2 Abruzzo), Francesco D’Aloisio MD (Uni-

versità degli Studi dell’Aquila), Gabriella Ruzzi MD (ASREM), Silvia Presta MD (ASL Salerno), Gabriella Di Giuseppe MD, Ferdinando Russo MD and Francesco Napolitano MD (AOU “Uni-

versità degli Studi della Campania Luigi Vanvitelli”), Giovanni Merlo MD (Ospedale Casa sol- lievo della sofferenza San Giovanni Rotondo), Giuseppe Perrone MD (ASL Lecce), Gaetano

Annese MD (ASM Matera), Bruno Masino MD (AOR “San Carlo”), Rita Marasco MD and

Antonio Gallucci MD (ASP Catanzaro), Caterina De Filippo MD, Francesca Lotito MD and

Ilario Lazzaro MD (AOU “Mater Domini” Catanzaro), Giacoma Di Martino MD (ASP Cata-

nia), Rosa Mancuso MD and Ziina Picciuca MD (ARNAS “Civico-Di Cristina”), Elena Melis

MD and Olga Porcu MD (ASSL Oristano), Antonietta Dettori MD (ASSL Cagliari).

Author Contributions

Conceptualization: Carmelo G. A. Nobile, Aida Bianco.

Data curation: Rossella Zucco, Francesco Lavano, Rosa Papadopoli.

Methodology: Rossella Zucco, Francesco Lavano, Rosa Papadopoli.

Supervision: Carmelo G. A. Nobile, Aida Bianco.

Validation: Aida Bianco.

Writing – original draft: Rossella Zucco.

Writing – review & editing: Aida Bianco.

References

1. World Health Organization. Healthcare-associated infections: fact sheet, 2014. Available at: http://

www.who.int/gpsc/country_work/gpsc_ccisc_fact_sheet_en.pdf. Accessed 12 February 2019.

2. Magill S, Hellinger W, Cohen J, Kay R, Bailey C, Boland B, et al. Prevalence of healthcare-associated

infections in acute care hospitals in Jacksonville, Florida. Infect Control Hosp Epidemiol. 2012; 33:283–

91. https://doi.org/10.1086/664048 PMID: 22314066

3. Graves EJ. National Hospital Discharge Survey. Vital Health Stat 13. 1989:1–60.

4. Agency for Healthcare Research and Quality.Healthcare Cost and Utilization Project—statistics on hos-

pital stays.2013.http://hcupnet.ahrq.gov/. Accessed February 15, 2019.

5. European centre for disease prevention and control surveillance report: point prevalence survey of

healthcare-associated infections and antimicrobial use in european hospitals 2011–2012. 2013 ECDC-

Stockholm. Avaiable at: http://ecdc.europa.eu/en/publications/Publications/healthcare-associated-

infections-antimicrobial-use-PPS.pdf. Accessed March 12, 2018.

6. O’Keeffe AB, Lawrence T, Bojanic S. Oxford craniotomy infections database: a cost analysis of craniot-

omy infection. Br J Neurosurg. 2012; 26:265–9. https://doi.org/10.3109/02688697.2011.626878 PMID:

22081956

7. Broex EC, van Asselt AD, Bruggeman CA, van Tiel FH. Surgical site infections: how high are the costs?

J Hosp Infect. 2009; 72:193–201. https://doi.org/10.1016/j.jhin.2009.03.020 PMID: 19482375

8. Teillant A, Gandra S, Barter D, Morgan DJ, Laxminarayan R. Potential burden of antibiotic resistance

on surgery and cancer chemotherapy antibiotic prophylaxis in the USA: a literature review and model-

ling study. Lancet Infect Dis. 2015; 15:1429–1437. https://doi.org/10.1016/S1473-3099(15)00270-4

PMID: 26482597

9. Umscheid CA, Mitchell MD, Doshi JA, Agarwal R, Williams K, Brennan PJ. Estimating the proportion of

healthcare-associated infections that are reasonably preventable and the related mortality and costs.

Infect Control Hosp Epidemiol. 2011; 32(2):101–114. https://doi.org/10.1086/657912 PMID: 21460463

10. Anderson DJ, Podgorny K, Berrı́os-Torres SI, Bratzler DW, Dellinger EP, Greene L, et al. Strategies to

prevent surgical site infections in acute care hospitals: 2014 update. Infect Control Hosp Epidemiol.

2014; 35:605–27. https://doi.org/10.1086/676022 PMID: 24799638

Surgical site infections prevention among nurses

PLOS ONE | https://doi.org/10.1371/journal.pone.0222825 September 26, 2019 11 / 13

11. Berrı́os-Torres SI, Umscheid CA, Bratzler DW, Leas B, Stone EC, Kelz RR, et al. Centers for Disease

Control and Prevention Guideline for the Prevention of Surgical Site Infection, 2017. JAMA Surg. 2017;

152(8):784–791. https://doi.org/10.1001/jamasurg.2017.0904 PMID: 28467526

12. National institute for health and clinical excellence (NICE). Surgical site infection: Prevention and treat-

ment of surgical site infection. London: NICE, 2008. http://www.nice.org.uk/nicemedia/pdf/

CG74NICEGuideline.pdf. Accessed January 02, 2019.

13. Bratzler DW, Hunt DR. The surgical infection prevention and surgical care improvement projects:

national initiatives to improve outcomes for patients having surgery. Clin Infect Dis. 2006; 43:322–30.

https://doi.org/10.1086/505220 PMID: 16804848

14. Global guidelines on the prevention of surgical site infection. World Health Organization 2016. Avaible

at: http://apps.who.int/iris/bitstream/10665/250680/1/9789241549882-eng.pdf. Accessed March12,

2019.

15. Allegranzi B, Bischoff P, de Jonge S, Kubilay NZ, Zayed B, Gomes SM et al. New WHO recommenda-

tions on preoperative measures for surgical site infection prevention: an evidence-based global per-

spective. Lancet Infect Dis. 2016; 16:e276–e287. https://doi.org/10.1016/S1473-3099(16)30398-X

PMID: 27816413

16. Allegranzi B, Bischoff P, de Jonge S, Kubilay NZ, Zayed B, Gomes SM, et al. New WHO recommenda-

tions on intraoperative and postoperative measures for surgical site infection prevention: an evidence-

based global perspective. Lancet Infect Dis. 2016; 16:e288–e303. https://doi.org/10.1016/S1473-3099

(16)30402-9 PMID: 27816414

17. Leaper DJ, Tanner J, Kiernan M, Assadian O, Edmiston CE Jr, et al. Surgical site infection: poor compli-

ance with guidelines and care bundles. Int Wound J. 2015; 12:357–62. https://doi.org/10.1111/iwj.

12243 PMID: 24612792

18. Labeau SO, Witdouck SS, Vandijck DM, Claes B, Rello J, Vandewoude KH, et al. Executive board of

the flemish society for critical care nurses. Nurses’ knowledge of evidence-based guidelines for the pre-

vention of surgical site infection. Worldviews Evid Based Nurs. 2010; 7:16–24. https://doi.org/10.1111/j.

1741-6787.2009.00177.x PMID: 19919658

19. Stata Corporation: Stata reference manual. Release 14. College Station TX; 2009.

20. Diener MK, Knebel P, Kieser M, Schüler P, Schiergens TS, Atanassov V, et al. Effectiveness of triclo-

san-coated PDS Plus versus uncoated PDS II sutures for prevention of surgical site infection after

abdominal wall closure: the randomised controlled PROUD trial. Lancet. 2014; 384:142–52. https://doi.

org/10.1016/S0140-6736(14)60238-5 PMID: 24718270

21. Thimour-Bergström L, Roman-Emanuel C, Scherstén H, Friberg Ö, Gudbjartsson T, Jeppsson A. Tri-

closan-coated sutures reduce surgical site infection after open vein harvesting in coronary artery

bypass grafting patients: a randomized controlled trial. Eur J Cardiothorac Surg. 2013; 44:931–8.

https://doi.org/10.1093/ejcts/ezt063 PMID: 23435526

22. Justinger C, Slotta JE, Ningel S, Gräber S, Kollmar O, Schilling MK, et al. Surgical-site infection after

abdominal wall closure with triclosan-impregnated polydioxanone sutures: results of a randomized clini-

cal pathway facilitated trial (NCT00998907). Surgery. 2013; 154:589–95. https://doi.org/10.1016/j.surg.

2013.04.011 PMID: 23859304

23. Edmiston C, Daoud FC, Leaper D. Is there an evidence-based argument for embracing an antimicrobial

(triclosan)-coated suture technology to reduce the risk for surgical-site infections?: A meta-analysis.

Surgery. 2013; 154:89–100. https://doi.org/10.1016/j.surg.2013.03.008 PMID: 23809487

24. Daoud FC, Edmiston CE Jr, Leaper D. Meta-analysis of prevention of surgical site infections following

incision closure with triclosan-coated sutures: robustness to new evidence. Surg Infect (Larchmt). 2014;

15:165–81. https://doi.org/10.1089/sur.2013.177 PMID: 24738988

25. Sessa A, Di Giuseppe G, Albano L, Angelillo IF; Collaborative Working Group. An investigation of

nurses’ knowledge, attitudes, and practices regarding disinfection procedures in Italy. BMC Infect Dis.

2011; 11:148. https://doi.org/10.1186/1471-2334-11-148 PMID: 21612613

26. Bianco A, Bova F, Nobile CG, Pileggi C, Pavia M; Collaborative Working Group. Healthcare workers

and prevention of hepatitis C virus transmission: exploring knowledge, attitudes and evidence-based

practices in hemodialysis units in Italy. BMC Infect Dis. 2013; 13:76. https://doi.org/10.1186/1471-2334-

13-76 PMID: 23391009

27. Bianco A, Coscarelli P, Nobile CG, Pileggi C, Pavia M. The reduction of risk in central line-associated

bloodstream infections: knowledge, attitudes, and evidence-based practices in health care workers.

Clin Microbiol Infect. 2012; 18:1212–8. https://doi.org/10.1111/j.1469-0691.2011.03735.x

28. Turenne J, Héon M, Aita M, Faessler J, Doddridge C. Educational Intervention for an Evidence-Based

Nursing Practice of Skin-to-Skin Contact at Birth. J Perinat Educ. 2016; 25:116–28. https://doi.org/10.

1891/1058-1243.25.2.116 PMID: 27445449

Surgical site infections prevention among nurses

PLOS ONE | https://doi.org/10.1371/journal.pone.0222825 September 26, 2019 12 / 13

29. Owens P, McHugh S, Clarke-Moloney M, Healy D, Fitzpatrick F, McCormick P, et al. Improving surgical

site infection prevention practices through a multifaceted educational intervention. Ir Med J. 2015;

108:78–81. PMID: 25876299

30. WHO Guidelines on hand hygiene in Healthcare. First global patient safety challenge clean care is safer

care. Avaiable at: https://apps.who.int/iris/bitstream/handle/10665/44102/9789241597906_eng.pdf.

Accessed February 21, 2019.

31. WHO Glove Use Information Leaflet. Avaiable at: https://www.who.int/gpsc/5may/Glove_Use_

Information_Leaflet.pdf. Accessed February 20, 2019.

32. Asadollahi M, Arshadi Bostanabad M, Jebraili M, Mahallei M, Seyyed Rasooli A, Abdolalipour M, et al.

Nurses’ knowledge regarding hand hygiene and its individual and organizational predictors. J Caring

Sci. 2015; 4:45–53. https://doi.org/10.5681/jcs.2015.005 PMID: 25821758

33. Giordano M, Squillace L, Pavia M. Appropriateness of Surgical Antibiotic Prophylaxis in Pediatric

Patients in Italy. Infect Control Hosp Epidemiol. 2017; 38:823–31. https://doi.org/10.1017/ice.2017.79

PMID: 28580893

34. Napolitano F, Izzo MT, Di Giuseppe G, Angelillo IF, Collaborative Working Group. Frequency of inap-

propriate medication prescription in hospitalized elderly patients in Italy. PLoS One. 2013; 8:e82359.

https://doi.org/10.1371/journal.pone.0082359 PMID: 24349262

35. Hughes JM. Study on the efficacy of nosocomial infection control (SENIC Project): results and implica-

tions for the future. Chemotherapy. 1988; 34:553–61. https://doi.org/10.1159/000238624 PMID:

3243099

36. Bianco A, Capano MS, Mascaro V, Pileggi C, Pavia M. Prospective surveillance of healthcare-associ-

ated infections and patterns of antimicrobial resistance of pathogens in an Italian intensive care unit.

Antimicrob Resist Infect Control. 2018; 7:48. https://doi.org/10.1186/s13756-018-0337-x PMID:

29636910

Surgical site infections prevention among nurses

PLOS ONE | https://doi.org/10.1371/journal.pone.0222825 September 26, 2019 13 / 13

Copyright of PLoS ONE is the property of Public Library of Science and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.