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Title Page 1 

Manuscript title: 2 

Best practice perioperative strategies and surgical techniques for preventing 3 

caesarean section surgical site infections: a systematic review. 4 

5 

Authors: 6 

Elizabeth K MARTIN (M Hlth Econ)1 7 

Michael M BECKMANN (MBBS FRANZCOG)2 8 

Louise N BARNSBEE (B Hlth Sci)1 9 

Kate A HALTON (PhD)1 10 

Katharina M D MEROLLINI (PhD)3 11 

Nicholas GRAVES (PhD)1 12 

13 

1Institute of Health and Biomedical Innovation, Queensland University of 14 

Technology, Brisbane, Queensland, Australia 15 

2Mater Health Services, Brisbane, Queensland, Australia 16 

3Faculty of Science, Health, Education and Engineering, University of the Sunshine 17 

Coast, Maroochydore, Queensland, Australia 18 

19 

Corresponding author: 20 

Elizabeth Martin 21 

School of Public Health and Social Work, Queensland University of Technology 22 

60 Musk Ave, Kelvin Grove, Qld, Australia, 4059 23 

+61 731386119 24 

+61 422809021 25 

elizabethkate.martin@qut.edu.au 26 

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27 

Abstract word count: 226 28 

Main text word count: 2976 29 

30 

Shortened running title: Preventing caesarean SSIs. 31 

  3

Abstract 32 

Background: Surgical site infection (SSI) following caesarean section is a problem 33 

for women and health services. Caesarean section is a high volume procedure and 34 

the estimated incidence of SSI may be as high as 9%. 35 

Objectives: The objective of this study was to identify a suite of perioperative 36 

strategies and surgical techniques that reduce the risk of SSI following caesarean 37 

section. 38 

Search strategy: 39 

Six electronic databases were searched to systematically review literature reviews, 40 

systematic reviews and meta-analyses published from 2006 to 2016. Search terms 41 

included: endometritis, SSI, caesarean section, meta-analysis, review, systematic. 42 

Selection criteria: Studies were sought in which competing perioperative strategies 43 

and surgical techniques relevant for caesarean section were identified and 44 

quantifiable infection outcomes were reported. General surgical infection control 45 

techniques were excluded. 46 

Data collection and analysis: Data on study characteristics and clinical effectiveness 47 

were extracted. Quality, including bias within individual studies, was examined using 48 

a modified A Measurement Tool to Assess Systematic Reviews (AMSTAR) checklist. 49 

Recommendations for SSI risk reducing strategies were developed using the 50 

Grading of Recommendations Assessment, Development and Evaluation (GRADE) 51 

approach. 52 

Main results: Of 466 records retrieved, 44 studies were selected for the evidence 53 

synthesis. Recommended strategies were: administer pre-incision antibiotic 54 

prophylaxis, prepare the vagina with iodine-povidone solution and spontaneous 55 

placenta removal. 56 

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Conclusions: We recommend clinicians implement pre-incision antibiotic prophylaxis, 57 

vaginal preparation and spontaneous placenta removal as an infection control 58 

bundle for caesarean section. 59 

60 

Tweetable abstract: Infection control for caesarean: pre-incision AB prophylaxis, 61 

vaginal prep, spontaneous placenta removal. 62 

63 

Key words: 64 

Best practice 65 

Caesarean section 66 

Clinical guidelines 67 

Evidence synthesis 68 

SSI 69 

Systematic review 70 

71 

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Introduction 72 

Surgical site infection (SSI) following caesarean section is a problem for women and 73 

health services. Infection rates vary between 4.9% and 9.8%.1-3 The consequences 74 

of SSI following caesarean section for women include pain and delay returning to 75 

normal activities,4 chronic pelvic pain,5 persistent seroma,6 and depression,7 as well 76 

as out of pocket costs.8, 9 Costs for a health system include additional staff time, use 77 

of pharmaceutical and healthcare supplies, and increased length of stay or re-78 

admission to hospital – potentially occupying a hospital bed that could be used by 79 

another.10 80 

81 

Evidence for perioperative strategies and surgical techniques has not been 82 

adequately synthesised for nurses and physicians (hereafter referred to as 83 

‘clinicians’) and may not always be accessible, as evidenced by large variation in 84 

practice.11-13 Available evidence mostly reports effectiveness of individual risk 85 

reducing strategies, which means up-to-date evidence for all potential strategies is 86 

not available in a single document. Furthermore, SSI is not always a primary 87 

outcome and publications need to be read in depth to identify the impact of each 88 

strategy on SSI. A systematic review published in 2013 that examined a range of 89 

interventions14 quickly became outdated due to new evidence.6, 15-26 In a more recent 90 

systematic review27 the authors did not make clear recommendations for clinical 91 

practice, while the quality of a third review28 is questionable because its methods are 92 

not clear. 93 

94 

A transparent and structured synthesis of systematic reviews, meta-analyses and 95 

other types of reviews has value in informing clinical decision makers of best practice 96 

  6

and remaining gaps.29, 30 The large number of caesarean section review studies on 97 

individual strategies and techniques are difficult for decision makers to decipher. 98 

Evidence syntheses cut through the wealth of evidence while assessing consistency 99 

and quality, and providing definitive summaries to inform clinical practice.29, 30 100 

Cochrane Collaboration acknowledged that this is the case and introduced evidence 101 

synthesis methods in their handbook.31 102 

103 

The objective of this study was to identify a suite of perioperative strategies and 104 

surgical techniques that reduce SSI risk following caesarean section. This paper will 105 

be helpful for clinical teams who seek guidance on reducing the risk of SSI following 106 

caesarean section, as the information is presented with the needs of clinical decision 107 

makers in mind. Making evidence-informed infection prevention decisions when 108 

caring for women having a caesarean section will reduce excess healthcare costs 109 

and improve maternal quality of life. 110 

111 

Methods 112 

A systematic review of literature reviews, systematic reviews and meta-analyses was 113 

conducted using the PRISMA guidelines32 to identify the most effective perioperative 114 

strategies and surgical techniques for reducing the risk of SSI following caesarean 115 

section. A protocol is available33 and the review registered with Prospero (number 116 

CRD42016041366).34 The study was exempt from Institutional Review Board 117 

approval because the research was not conducted with humans or animals and used 118 

publically available data. 119 

120 

  7

Two researchers (EM and LB) independently searched electronic databases 121 

PubMed, CINAHL, Cochrane Library, Science Direct, Scopus and Embase for review 122 

studies published in the English language between January 2006 and June 2016. 123 

Only review studies were chosen, and no clinical trials, as this study seeks to 124 

synthesise the key strategies with as large a volume of effectiveness evidence as 125 

possible. The 10-year timeframe corresponds to the extensive research activity that 126 

commenced after the rate of caesarean sections began to increase in the late 1990s. 127 

128 

The search strategy sought studies that synthesised SSI outcomes for women who 129 

had an emergency or elective caesarean section and were any age, parity and risk 130 

category. Any type of perioperative or surgical intervention and appropriate 131 

comparator relevant to caesarean section was of interest. The primary outcome was 132 

SSI, defined according to the US Centers for Disease Control and Prevention (CDC) 133 

classifications of superficial or deep incisional and organ/space infection, including 134 

endometritis.35 The term ‘wound infection’ was accepted as an alternative outcome 135 

description but aggregate measures of infection such as “total infectious morbidity” 136 

was not used. Caesarean section wound infection is part of the recommended 137 

maternity care core outcomes set within the CROWN initiative.36 S1 shows the 138 

PubMed search strategy for this review that can be replicated to verify or update the 139 

results. 140 

141 

This systematic review is specifically designed to inform providers of maternity care 142 

rather than broader hospital practice. The evidence has already been established for 143 

the importance of infection prevention strategies common to most surgeries at a 144 

general healthcare and surgical healthcare level such as hand hygiene, hemostasis 145 

  8

and antibiotic prophylaxis but – importantly – not the timing of prophylaxis. As such, 146 

inclusion and exclusion criteria were developed to reflect the focus of this review and 147 

shown in Table 1. Titles, then abstracts, were independently scanned and full text 148 

studies were retrieved if the inclusion/exclusion criteria were met. 149 

150 

Insert Table 1 151 

152 

Data was extracted and bias within each review assessed independently by two 153 

researchers (EM and LB). Data identifying the review, key study characteristics and 154 

effectiveness of perioperative strategies and surgical techniques on SSI (usually 155 

relative risk as the summary measure) were entered into a data extraction template. 156 

Bias was examined using a modified A Measurement Tool to Assess Systematic 157 

Reviews (AMSTAR) checklist and categorisation method developed by McKibben 158 

and colleagues.27 The quality of individual studies was reported as ‘good’, ‘fair’ or 159 

‘poor’ using the McKibben method.27 To qualify as a ‘good’ quality study, two or more 160 

of the four major criteria must have been met, as well as four or more of the 23 minor 161 

assessment quality criteria. The method for assigning a quality rank to individual 162 

studies is summarised in Table 2 and we direct readers to the original paper for more 163 

detail.27 164 

165 

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Insert Table 2 166 

167 

A list of perioperative strategies and surgical techniques, and their effectiveness in 168 

reducing SSI risk, was created. Recommendations were made for each strategy 169 

using the GRADE approach of assessing the four determinants of the strength of a 170 

recommendation: effect; quality of evidence; value and preferences; and costs.37 171 

Effectiveness data from the most recent ‘good’ quality studies were examined to 172 

avoid overstating the strength of the recommendation for each strategy however, the 173 

effect size was checked against other studies for consistency. This meant 174 

randomised controlled trials included in multiple meta-analyses were not counted 175 

twice, but important and relevant evidence was still captured. Quality of evidence as 176 

determined by the original authors of the most recent good quality study selected for 177 

each strategy or surgical technique in this synthesis, was used to inform the strength 178 

of each recommendation. A suite of infection control strategies was chosen from 179 

those with strong recommendations and the highest evidence quality. 180 

181 

Other adverse outcomes reported in the included studies such as blood loss, 182 

unintended uterine extensions and including wasted health service resources were 183 

noted in the data extraction process. It was important to identify strategies that had 184 

potential maternal or perinatal morbidity despite their effectiveness in reducing 185 

infection risk. The relative importance of non-infection outcomes was considered 186 

against infection outcomes when developing the suite of infection control strategies. 187 

188 

A health consumer representative from the organisation Maternity Choices, was 189 

involved in the interpretation of the findings as part of their contribution to the 190 

  10

broader research that this study is part of. The health consumer commented on the 191 

appropriateness of the results and the focus of the research on the maternal, rather 192 

than infant, perspective 193 

194 

Funding for this study was provided by the Centre of Research Excellence in 195 

Reducing Healthcare Associated Infections. This was not an awarded grant and did 196 

not include an external peer review for scientific quality. The Centre of Research 197 

Excellence had no role in conducting the research or writing the paper. 198 

199 

Results 200 

In the systematic review and development of the suite of infection control strategies, 201 

67 full text studies were assessed for eligibility. From these, 44 studies were 202 

included for data extraction and synthesis (see Figure 1). Thirty-two studies were 203 

meta-analyses, one was a systematic review and 11 were non-systematic literature 204 

reviews. Excluded studies following abstract screening and full-text assessment for 205 

eligibility with reasons are in S2. 206 

207 

Insert Figure 1. 208 

209 

Amongst the systematic reviews and meta-analyses, 33 were categorised as good 210 

quality and one study was given a ‘fair’ quality rating (see S3). The ‘fair’ quality study 211 

only met one of the four major quality assessment criteria and did not conduct 212 

duplicate data extraction, only searched one database and did not rate and 213 

document the quality of included studies. Non-systematic reviews were all assessed 214 

  11

as ‘poor’ quality as they did not provide enough information on the criteria required in 215 

the McKibben assessment method.27 216 

217 

Seventeen different types of perioperative strategies and surgical techniques for 218 

caesarean section were identified as having been evaluated for their effectiveness in 219 

reducing the risk of SSI (see Table 3). The groups of strategies with the largest 220 

number of studies assessing effectiveness were antibiotic prophylaxis and skin 221 

closure. 222 

223 

Insert Table 3 224 

225 

There was much variation regarding the specific interventions and comparators 226 

examined within each type of strategy. Seventeen studies evaluated three different 227 

aspects of antibiotic prophylaxis: timing, antibiotic class and route of administration. 228 

The effectiveness of 22 different combinations of antibiotic classes was reported 229 

across one meta-analysis23 and one systematic review.38 Similarly, multiple 230 

intervention comparator pairs were also evaluated for skin incision, uterine closure, 231 

peritoneum closure, wound drainage and skin closure (see S4). In total, 82 232 

intervention comparator pairs were identified in this study as having been evaluated 233 

for their effectiveness in reducing the risk of caesarean section SSI. All included 234 

studies that informed the list of perioperative strategies and surgical techniques are 235 

provided in Table 3, while the single most recent good quality studies that influenced 236 

the recommendations are in the text below. 237 

238 

  12

The effectiveness of the 82 intervention comparator pairs was examined. From 239 

these, three perioperative strategies and surgical techniques with strong evidence for 240 

reducing the risk of SSI following caesarean section were identified for the suite of 241 

infection control strategies. The strategies were: administer prophylactic antibiotics 242 

15 to 60 minutes before incision; prepare the vagina with iodine-povidone solution; 243 

and remove the placenta spontaneously with gentle cord traction (see Table 3). Pre-244 

incision antibiotic prophylaxis reduced the risk of endometritis by 46% and wound 245 

infection by 41%.20 Vaginal preparation reduced the risk of endometritis by 55%, but 246 

did not have an effect on wound infection.6 The risk of endometritis was increased by 247 

64% with manual removal of the placenta.39 The three strategies had clear evidence 248 

of reducing the risk of caesarean section SSI and the associated recommendations 249 

were all strong based on an assessment of the four determinants of recommendation 250 

strength used in the GRADE approach (see Table 3). 251 

252 

Two strategies received strong recommendations for providing other surgical 253 

benefits despite little evidence for their effect in reducing SSI risk (see Table 3). 254 

Significantly fewer unintended uterine extensions and a trend towards less blood 255 

loss was observed with blunt cephalad-caudad uterine expansion.21 Closing the skin 256 

with subcuticular sutures has a significantly lower risk of wound complication such as 257 

wound dehiscence.18 258 

259 

Three strategies were strongly not recommended for implementation, because of the 260 

potential to waste scarce healthcare resources (see Table 3). Supplemental 261 

oxygen,40 mechanical dilatation of the cervix,41 and using a subcutaneous drain 262 

(even in obese women or women with subcutaneous tissue greater than 2cm)42 263 

  13

resulted in no beneficial health outcomes and unnecessarily lengthened surgery time 264 

occupying theatres that could be freed for another use. 265 

266 

Intra-abdominal irrigation received a strong recommendation to not implement 267 

because no additional health benefit was reported and it is significantly associated 268 

with intraoperative nausea (see Table 3).17 269 

270 

Discussion 271 

Main Findings 272 

Three perioperative caesarean section strategies and surgical techniques to reduce 273 

SSI risk have been identified as having strong evidence for universal 274 

implementation: pre-incision antibiotic prophylaxis, vaginal preparation with an 275 

iodine-povidone solution and spontaneous placenta removal. We recommend these 276 

strategies to clinicians as an infection control bundle that should be trialled in 277 

practice. This infection control bundle meets the Institute for Healthcare 278 

Improvement definition43 as it consists of three evidence-based interventions 279 

specifically for caesarean section, and we hypothesise that when implemented 280 

together, the bundle will reduce SSI risk more than adhoc implementation of the 281 

individual elements. 282 

283 

Strengths 284 

The strength of this study is that a rigorous synthesis of all caesarean section 285 

perioperative strategies and surgical techniques that have been examined for their 286 

impact on SSI has been conducted. The GRADE approach used, infection control 287 

bundle developed and additional recommendations have resulted clearly outlined 288 

  14

best practice guidelines for clinicians. We did not assess evidence quality in this 289 

study, but extracted original authors’ assessments of evidence quality and used the 290 

data to inform the strength of recommendations made. By examing the four factors 291 

that determine the strength of a GRADE recommendation: effects, quality of 292 

evidence, values and preferences, and costs, we offer clinical practice guidance that 293 

a systematic review alone can not provide. 294 

295 

The focus on infection prevention opportunities perioperatively and during surgery at 296 

caesarean section is a unique aspect of this study. Alternative foci for identifying SSI 297 

risk reducing strategies were general surgical or healthcare approaches; or 298 

addressing intrinsic patient-related risk factors. However the evidence for general 299 

infection control strategies to prevent healthcare associated infections is well 300 

established, and addressing risk factors instrisic to the patient was beyond the scope 301 

this study. Clinicians mostly understand risk factors for SSI that are intrinsic to the 302 

patient, but variation in caesarean section techniques11-13 suggests there is more 303 

uncertainty regarding best practice from a perioperative and surgical perspective. 304 

305 

Limitations 306 

In this study, we synthesised evidence from reviews, systematic reviews and meta-307 

analyses given the prominence placed on the type of evidence generated by the 308 

latter two for clinical end users. As such, a limitation is that there may be strategies 309 

that have been trialled and demonstrate an effect in reducing SSI risk such as 310 

chlorhexidine-gluconate for skin preparation,44 but not captured in this study because 311 

the small volume of evidence has not warranted a review by other researchers. A 312 

synthesis of reviews, systematic reviews and meta-analyses is not an appropriate 313 

  15

method for the development of a full clinicial guideline for caesarean section. There 314 

is potential for bias in this approach if other researchers were unable to publish or 315 

have not conducted systematic reviews of strategies and techniques that may 316 

reduce SSI risk and further inform this study. We have not attempted to write an 317 

authoritative source for all recommended practice at caesarean section, but provide 318 

a targetted suite of infection control strategies that are potentially under utilised 319 

despite the evidence for their effectiveness. 320 

321 

An additional limitation is that the infection control bundle has not been trialled in 322 

practice. Our recommendation to clinicians that the bundle be implemented for every 323 

caesarean section is based on an hypothesis that the evidence for each individual 324 

strategy is strong and, when consistently implemented together, infection outcomes 325 

would improve further. However, it is not clear what the relative contribution optimal 326 

perioperative and surgical technique has to overall healthcare associated infection 327 

prevention measures. Perhaps in practice, the infection control bundle will have little 328 

impact while general surgical infection control practices are substandard and/or risk 329 

factors intrinsic to the patient remain present. A study that evaluates the infection 330 

control bundle while measuring general infection control practice and intrinsic risk 331 

factors is needed. 332 

333 

The primary outcome for this study was maternal SSI, and long term infant outcomes 334 

were not considered. This limitation is relevant for the recommendation to administer 335 

prophylactic antibiotics before skin incision rather than post-cord clamping because 336 

the infant is potentially exposed to antibiotics with pre-incision administration. While 337 

there is no evidence of masked neonatal sepsis in the short term,20 there is emerging 338 

  16

evidence of an infant gut microbiota imbalance45 and little understanding of the long-339 

term outcomes such as development of chronic disease following fetal exposure to 340 

antibiotics.46 341 

342 

There is a noteable limitation to the recommendation favouring one-layer uterine 343 

closure as two-layer closure is considered by many obstetricians to be associated 344 

with a lower risk of uterine rupture in subsequent pregnancies. The conflicting results 345 

regarding risk of uterine rupture between the randomised controlled trials analysed 346 

by the two studies included in our systematic review24, 47 and good quality 347 

observational studies48, 49 are an important issue to resolve with further research. 348 

One-layer uterine closure has no apparent effect on SSI and its only benefit is a 349 

shorter duration of surgery by six minutes.47 With other evidence raising concerns 350 

about one-layer uterine closure, we cannot make a strong recommendation for this 351 

technique. 352 

353 

Interpretation 354 

The results of this study are generally paralleled in other studies. We identified 82 355 

perioperative strategies and surgical techniques that have been evaluated for their 356 

impact on reducing SSI risk, while 77 strategies were found in the McKibben study.27 357 

There was agreement between ours and the McKibben study for 17 out of 18 quality 358 

ratings given to each of the included studies using the modfied AMSTAR method.27 359 

The strategies recommended in this paper also align with some of those identified in 360 

the McKibben paper.27 However, we disagree that the Joel-Cohen skin incision and 361 

that suturing thick (≥ 2cm) subcutaneous tissue is definitively superior to their 362 

alternatives in reducing SSI risk. For skin incision,50 we examined outcomes for 363 

  17

wound infection only, and it appears McKibben used a broader infection outcome.27 364 

For suturing of subcutaneous tissue, we selected an updated study for inclusion42 365 

which was different to that used by McKibben.27 Updated evidence for vaginal 366 

preparation has been sythesied in this study, allowing a stronger recommendation to 367 

be made since a study by Dahlke and colleagues was published.14 However as the 368 

quality of evidence included in a meta-analysis selected for our study was assessed 369 

as low,6 more research for vaginal preparation is warranted, particulary as the effect 370 

sizes may not be seen across all sub-populations. Our results otherwise corroborate 371 

with the Dahlke study. 372 

373 

Conclusion 374 

A perioperative and surgical infection control bundle specifically for caesarean 375 

section has been developed through a comprehensive synthesis of the key 376 

evidence. The infection control bundle is: pre-incision administration of prophylactic 377 

antibiotics, vaginal preparation with iodine-povidone solution and spontaneous 378 

removal of the placenta. 379 

380 

381 

Disclosure statement: 382 

The authors report no conflict of interest. 383 

384 

Author Contributions: 385 

EM conceived the study, NG, MB, KH and KM guided the planning of the study with 386 

EM, EM and LB collected the data and EM analysed the results. The manuscript was 387 

prepared by EM with assistance from LB, NG, MB, KH and KM. 388 

389 

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Ethics details: 390 

Prospero (number CRD42016041366).34 The study was exempt from Institutional 391 

Review Board approval because the research was not conducted with humans or 392 

animals and used publically available data. 393 

394 

Funding: 395 

Funding for Louise Barnsbee’s salary to conduct duplicate searching, quality 396 

assessment and data extraction was provided by the Centre of Research Excellence 397 

in Reducing Healthcare Associated Infections. The Centre of Research Excellence 398 

had no involvement in the study design, collection, analysis and interpretation of 399 

data, writing of the report and the decision to submit the article for publication. 400 

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References 401 

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