Journal of Hospital Infection (2008) 70, 166e173 Available online at www.sciencedirect.com www.elsevierhealth.com/journals/jhinEnhanced surgical site infection surveillancefollowing caesarean section: experience ofa multicentre collaborative post-discharge systemV.P. Ward a,*, A. Charlett a, J. Fagan b, S.C. Crawshaw ca Health Protection Agency, London, UKb Nottingham City Hospital, Nottingham, UKc NHS East Midlands, UKReceived 29 November 2007; accepted 2 June 2008Available online 23 August 2008 KEYWORDS Summary The caesarean section rate in the UK has more than doubled Caesarean section; during the last two decades and is continuing to rise. The majority of stud- Antibiotic prescribing; ies carried out to determine the incidence of infection associated with this Surgical site infection; procedure have been restricted to the inpatient stay, which may give mis- Risk factors leading results. Women undergoing caesarean section have routine contact with a community midwife after discharge. This provided an opportunity to assess whether a collaborative surveillance approach between hospital and community staff was feasible using routinely available information. Follow- ing a successful pilot study, 11 maternity units in the East Midlands partici- pated in an extended study. Complete records were available for 5563 (88%) women. Overall, 758 (13.6%) wound problems were reported, 84% of which developed after discharge. Of these, 488 (8.9%) met national def- initions for surgical site infection (SSI); however, there was a marked inter- unit difference in incidence, ranging from 2.9% to 17.9%. Statistical models were used to examine these differences using 12 possible risk factors. Five risk factors were found to be signiﬁcantly associated with the development of a surgical site infection: body mass index, age, blood loss, method of wound closure and emergency procedures. These results suggest that caesarean section is associated with high infectious morbidity, the extent of which would have been considerably underestimated without post- discharge monitoring. Almost all women with wound problems were treated with antibiotics, regardless of how minor the problem, with 97% * Corresponding author. Address: Laboratory of Healthcare Associated Infection, Health Protection Agency, 61 Colindale Avenue,London NW9 5HT, UK. Tel.: þ44 208 327 7332. E-mail address: firstname.lastname@example.org/$ - see front matter ª 2008 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved.doi:10.1016/j.jhin.2008.06.002
SSI surveillance following caesarean section 167 being prescribed in the community. This indicates a requirement for local review of antibiotic prescribing practice. ª 2008 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved.Introduction a multicentre prospective study carried out by the US Centers for Disease Control (CDC).8In the past 15 years, the proportion of caesarean Of the 1029 women who had caesarean de-section births has been increasing steadily in liveries, inpatient and community records wereEngland, and now accounts for 24% of all births.1 available for 896 (87%). Using the criteria of theMore than 150 000 women were delivered in this study hospital, SSIs were classiﬁed as major ifway in 2005, making this procedure one of the wounds were discharging pus or inﬂamed andmost commonly performed major operations.2 required antibiotic therapy; or there was spreadingAlthough it has undoubtedly reduced infant and cellulitis and fever (>38 C), complete or partialmaternal mortality, studies have shown that the (50%) dehiscence, or required surgical revision/procedure is associated with signiﬁcant infectious debridement. Wound problems that did not meetmorbidity involving the operative site. Wound in- these deﬁnitions were classiﬁed as minor. A totalfection rates ranging between 7% and 41.1% have of 213 (23.7%) wound infections were identiﬁedbeen reported.3,4 Although this wide variation from the records, 111 of which were classiﬁed asmay be due to differences in the criteria used to major. The majority of infections (89%) werediagnose infection, case-ﬁnding, and the use of identiﬁed after discharge. All patients had beenantibiotic prophylaxis, the majority of studies routinely prescribed antibiotic prophylaxis. Thesehave been restricted to the inpatient stay. Under- results conﬁrmed that wound infection was a signif-estimation of the incidence of infection ranging icant problem following caesarean section and thatfrom 20% to 70% has been reported in general a combined hospital/community monitoring ap-surgery if patients are not monitored after they proach was feasible.leave hospital.5 A National Audit Ofﬁce report On the basis of these results, it was decided toconsidered that post-discharge surveillance was extend the study to other maternity units in theimportant if National Health Service (NHS) Trusts same region. The primary objective of the mainwere to understand the full extent of hospital- study was to prospectively study the occurrenceacquired infection, yet it had been attempted in of surgical wound and uterine infections followingonly a quarter.6 Their recommendation, subse- caesarean section in maternity units throughoutquently endorsed by the Committee of Public the East Midlands region using a standardisedAccounts, was that post-discharge surveillance approach with common case-deﬁnitions andshould be considered.7 case-ﬁnding methods. Factors associated with It was decided to investigate the incidence of post-delivery infectious morbidity would also besurgical site infection (SSI) in a one-year study that identiﬁed and, because it had been ascertainedincluded post-discharge surveillance at a single that all units routinely gave antibiotic prophy-maternity unit in the East Midlands during laxis, compliance with policies would be assessed.2001e2002. This study used the fact that womenundergoing caesarean section have routine contact Study settingwith a community midwife for a minimum of 10days after discharge, or longer if there are any Eleven maternity units within the East Midlandswound or other obstetric-related problems. This region participated in the surveillance betweenprovided an opportunity to assess whether a col- July 2003 and March 2005, collecting data forlaborative surveillance approach between infec- varying periods of between three and 18 months.tion control teams, and hospital and community Initially, seven units undertook to collect data formidwives was feasible; and whether the incidence 12 months, although two units in one Trust had toof infection following caesarean section and in- stop after six months due to stafﬁng issues.formation on potential risk factors could be de- Towards the end of the study period, four of thetermined from routine records. Included in the risk remaining ﬁve units within the region opted tofactor data to be collected were factors shown to take part, and the study period was extended forbe independently important in predicting SSI in another six months.
168 V.P. Ward et al.Methods criteria. In order to reduce inter-observer varia- tion in the application of these deﬁnitions, all signsStudy design and symptoms of infection were recorded. This information was then used to assess whether theThis was a prospective multicentre study. Each diagnostic criteria for incisional and uterine infec-unit nominated maternity and infection control tions were met.staff to co-ordinate the study. Data collectionStudy population The surveillance protocol was discussed and agreed with collaborating obstetricians, hospital and com-All women who underwent caesarean section at any munity midwives, and infection control and auditof the participating units during the study period staff. Clinical, risk factor, and infection data itemswere included in the surveillance. Patients were to be collected were based on results from thefollowed up from the day of surgery until the date of preliminary study, a brief review of the literature,last contact with the community midwife. and discussions with local experts in the ﬁeld. Close collaboration between hospital and com-Deﬁnitions of infection munity midwifery staff was necessary for effective study of this patient group. The required demo-Based on the experience of the CDC, deep in- graphic and inpatient information was routinelycisional infections involving the fascial and muscle recorded in a variety of sources, including maternitylayers rarely occur after caesarean section unit databases, theatre records, and patient ante-(T. Horan, personal communication). Therefore, natal records. In the UK, postnatal follow-up care isfor the purposes of this study, infections of the entered on to a patient-held record. Communitysurgical site were classiﬁed as either incisional midwives were asked to ensure that any signs and(wound) or uterine (endometritis). The deﬁnitions symptoms that could suggest the presence of in-of incisional infection used were those adopted by fection were clearly and consistently recorded,the Health Protection Agency (HPA) for the na- together with details of action taken. Once care oftional Surgical Site Infection Surveillance Service the patient had been handed over to the health(SSISS) and can be found at http://www.hpa. visitor, the community midwife returned the recordorg.uk/infections/topics_az/hai/SSI_Protocol.pdf. to the hospital, where the required data wereAs the SSISS does not currently include caesarean abstracted by the study co-ordinators.sections, the CDC deﬁnitions for uterine infections Participating units could choose to enter thewere used.9 The criteria for deﬁning incisional and data directly into a local database, or use a caseuterine infections are shown in Table I. These record form that was designed to be read usingdeﬁnitions are based on a number of separate optical mark recognition (OMR) software. Units Table I Criteria for deﬁning incisional and uterine infections Incisional infections 1 Purulent drainage. 2 Culture from wound swab, or aseptically aspirated ﬂuid or tissue, yields organisms and pus cells present on microscopy. 3 At least two of the following symptoms and signs of inﬂammation: pain or tenderness, localised swelling, redness or heat, and (a) incision deliberately opened by surgeon to manage the infection, unless incision culture-negative, or (b) clinician’s diagnosis of incisional infection. 4 Wound spontaneously dehisces, or deliberately opened by surgeon, and at least one of the following symptoms and signs of inﬂammation: localised pain or tenderness, fever (38 C), unless incision culture-negative. 5 Abscess or other evidence of infection found during reoperation, or by histopathological/radiological examination. Uterine infections 1 At least two of the following symptoms and signs of infection: fever (38 C), abdominal pain, uterine tenderness, purulent drainage from uterus. 2 Organisms cultured from ﬂuid or endometrial tissue obtained during operation, needle aspiration, or brush biopsy.
SSI surveillance following caesarean section 169that were able to collect much of the required analysis included a random term for maternity unitinformation electronically from databases within in order to allow for any inter-unit variation in thethe hospital opted to use the Excel database incidence of infection. The factors analysed wereprovided to ensure that the data were in the age, body mass index (BMI), ruptured membranes,agreed format, and data ﬁelds correctly labelled. in labour at the time of surgery, preoperativeInformation on wound problems that occurred stay, American Society of Anesthesiologists (ASA)after discharge were manually retrieved from score, prophylactic antibiotics, emergency pro-community records and transferred either to the cedure, grade of surgeon, duration of caesareanelectronic or paper record. section, blood loss, and method of wound closure. Regardless of the preferred method of collec- Those factors where there was no evidence of antion, all data were forwarded to the regional association were sequentially removed from theco-ordinating centre at the East Midlands Health regression model provided the regression coefﬁ-Protection Agency for collation before being down- cients of the other factors in the model did notloaded to the HPA Centre for Infections for consis- change markedly. All factors removed from thetency checking and statistical analysis. All patient regression model were included in the ﬁnal modelidentiﬁers were removed, and a unique number to ensure that they were not associated.allocated to each record. Data transfer was pass-word-protected and information was held securely Resultsat both sites according to Caldicott principles. Although inpatient information was available forStatistical methods the 6297 caesarean section procedures carried out during the study period, inclusion was dependentThe variation in incisional and uterine infection on the return of the community follow-up recordsrates between maternity units was assessed using to the hospital by the community midwives. Bothc2-tests of association. The assessment of the hospital and community information was availablelength of follow-up was performed using a non- for 5563 (88%) of the patients.parametric test for the equality of medians. The strength of association between potential Length of follow-uprisk factors and the development of an infectionthat met the study deﬁnitions was measured using Overall the median length of follow-up was 15 daysa random effects logistic regression analysis. This (Figure 1). For hospital stay, the median was 3 days, 20 18 16 14 12 Days 10 8 6 4 2 0 1 2 3 4 5 6 7 8 9 10 11 Maternity unitFigure 1 Length of inpatient stay and community follow-up by unit. Grey bars: mean length of hospital stay; blackbars: mean community follow-up.
170 V.P. Ward et al.quartiles 3, 4. For community follow-up, the median two of the signs and symptoms associated withwas 11 days, quartiles 8, 17. There was marked endometritis; 95 (82.6%) of these included puru-inter-unit variation in the length of follow-up, this lent drainage.variation being highly signiﬁcant (P 0.0001). Antibiotic usageIncidence of infection All the maternity units routinely gave antibioticA total of 745 surgical wound problems and/or prophylaxis. Apart from 34 women who wereuterine infections were recorded in 738 (13.3%) of already on antibiotics for other reasons, 5493the 5563 women (Figure 2). Of these, 488 (65.5%) met received prophylaxis, with 97% given as per thethe study deﬁnitions. For 370 incisional infections hospital policy.that met the criteria, the mean was 6.7% (range: Of the 478 women who developed incisional2.9e12.4). For uterine infections, 118 met the study and/or uterine infections, 459 (96%) were treateddeﬁnitions (mean: 2.1%, range: 0e5.5%). There was with antibiotics. A further 22 women receivedwide inter-hospital variation for the two types of in- antibiotics despite there being little or no evi-fection, both of which were highly signiﬁcant dence to support their use. Almost all of the 257(P 0.0001). Only 78 of the 488 SSIs (16%) were diag- women (99%) with wound problems that did notnosed during the inpatient stay, with the remainder meet the study deﬁnitions were also treated withbeing identiﬁed after discharge from hospital. antibiotics. Almost all (98%) incisional infections met one oftwo of the ﬁve possible criteria for infection. Of Risk factorsthe 370 identiﬁed, 204 (55.1%) had purulentdrainage from the incision, and 158 (42.7%) had Since 98% of women had received prophylactictwo or more signs and symptoms of infection plus antibiotics, this factor was not included in theclinician’s diagnosis. Many surgeons consider pus analysis. Univariable analysis indicated that sevento be the most important criterion for infection. of the remaining 11 variables were signiﬁcantlyThere were marked inter-unit differences between associated with infection: BMI (P 0.0001), emer-the proportions of infections associated with puru- gency procedures (P ¼ 0.002), ruptured mem-lent drainage, ranging from 0 to 91%. branes (P ¼ 0.01), in labour at the time of surgery For the 118 uterine infections reported that met (P 0.001), duration of procedure (P ¼ 0.002) andthe study deﬁnitions, 115 were based on at least wound closure method (P ¼ 0.003). 20 928 18 16 Incidence per 100 operations 14 444 12 10 848 8 360 858 256 6 440 257 281 823 4 68 2 0 1 2 3 4 5 6 7 8 9 10 11 Maternity unitFigure 2 Incidence of incisional and uterine infections that met the study deﬁnitions by unit. Numbers above barsindicate numbers of patients. Grey bars: incisional infection; black bars: uterine infection.
SSI surveillance following caesarean section 171 A total of 2328 women had elective surgery, 128 increased by 70% (P 0.0001) for each 10-unit(5.5%) of whom developed an incisional wound increase in BMI. Maternal age was associated withinfection. The corresponding number for the 3234 subsequent development of an infection, with olderwomen who had emergency procedures was 242 women being less likely to develop infection. This(7.5%). This difference was statistically signiﬁcant ﬁnding was also observed by Myles et al., although(P ¼ 0.003). Conversely, there was no signiﬁcant dif- it was not signiﬁcant in their multivariable model.10ference for uterine infections, with 1.9% of women There was an estimated 3% increase in the odds ofwho had elective surgery developing an infection developing an infection for each additional 100 mLcompared to 2.3% who had emergency procedures. of blood loss and a 25% increase for women undergo- With regard to wound closure methods, a num- ing emergency procedures. For wound closure, theber of consultant obstetricians had requested that risk was 39% higher when staples were used. Otherthis information be collected at the protocol de- methods were associated with a ﬁve-fold increase,velopment stage. The majority (70%) of women although this only involved nine women.had continuous sutures, 23% of wounds had beenstapled and 2% had intermittent/other methods of Discussionclosure. For infections that met the study deﬁni-tions, the incidence was signiﬁcantly higher when This study has demonstrated the feasibility andstaples were used, being 12.2% compared to 7.5% usefulness of post-discharge surveillance in a groupwith continuous sutures (P 0.0001). of patients undergoing one of the most com- The other factor of interest to obstetricians was monly performed operative procedures. Hospital-grade of surgeon. Registrars performed 75% of acquired infections delay recovery, may increasecaesarean sections, consultants 14%, and senior the duration of hospital stay, and have economichouse ofﬁcers (SHOs) 12%. There was only weak consequences for the primary and secondaryevidence that consultants had a lower infection healthcare sectors.11e13 In a Department of Healthrate than registrars. SHOs had a slightly higher (DH)-commissioned study undertaken in 1994eincidence of infection. However, most (71%) of the 1995, it was estimated that the average additionalcaesarean sections performed by SHOs were un- inpatient cost of surgical wound infections follow-dertaken at two of the 11 maternity units. Of the ing caesarean section was £524.11 Inevitably this72 infections that developed in the women oper- cost will have risen over the ensuing decade.ated on by an SHO, only 12 occurred in the other In the 5563 patients followed up during theirnine maternity units, which limited the ability of hospital stay and after discharge, there was an 8.9%this study to assess whether this observed excess incidence of SSI that met the study deﬁnitions. Thiswas real or due to other hospital-related factors. incidence is broadly similar to results reported in The risk factors were then assessed using a mul- recent studies that used CDC deﬁnitions of infec-tivariable logistic regression model (Table II). Five tion.14e17 Without post-discharge surveillance therefactors remained statistically signiﬁcant after would have been a considerable underestimate ofcontrolling for any potential confounding effects the incidence of infection at all units, since 84%of the other factors. BMI remained strongly associ- were identiﬁed after discharge. This is consistentated with the subsequent development of a surgical with a recently published UK study showing thatsite infection. The odds of developing an infection 71% of infections were diagnosed in the community.14 Table II Multivariable analysis of all infections meeting study deﬁnitions Factor Category N (%) Estimated OR 95% CI P-value BMI (per 10 units) e 4897 (88.0) 1.70 1.47e1.97 0.0001 Age (per 10 years) e 5558 (99.9) 0.82 0.69e0.99 0.04 Blood loss (per 100 mL) e 5525 (99.3) 1.03 1.01e1.05 0.009 Type of surgery Elective 2328 (41.8) Referent Emergency 3234 (58.1) 1.25 1.00e1.56 0.05 Unknown 1 (0.1) e Type of closure Continuous 3906 (70.2) Referent Intermittent 102 (1.8) 0.73 0.27e1.96 Staples 1273 (22.9) 1.39 1.08e1.79 Other 9 (0.2) 5.35 1.00e28.61 0.01 Unknown 273 (4.9) e OR, odds ratio; CI, conﬁdence interval; BMI, body mass index (kg/m2).
172 V.P. Ward et al. Effective surveillance following caesarean sec- consensus regarding the choice of drug, regimen,tion requires a multidisciplinary approach between or method of administration, and whether pro-infection control nurses, hospital and community phylaxis should be restricted to high-risk pa-midwives and other healthcare personnel. The tients.20 Several different regimens were used byprinciples of clinical governance apply to all who the 11 maternity units that took part in the study.provide or manage patient care services in the NHS, Further analysis is being done to compare theseand require them to work in partnerships to provide regimens and to assess whether these impact onintegrated care to promote quality and improve the the incidence of infection.patient experience of healthcare.18 By using the With regard to the treatment of wound prob-fact that women undergoing caesarean section lems, 96% of women who developed SSI that methave routine contact with a community midwife the study deﬁnitions received antibiotics. How-for a minimum of 10 days, this study demonstrates ever, it should be noted that almost all of the 257the feasibility of a collaborative approach to post- women (99%) with wound problems that did notdischarge surveillance. meet the study deﬁnitions were also treated with Strategies to prevent, or at least decrease, the antibiotics. In line with good antibiotic steward-risk of infection are needed. There is evidence to ship there is a need for reviewing and monitoringsuggest that infection rates can be reduced when antibiotic prescribing locally.routine surveillance with feedback of rates to staff In the course of this study, data on a number ofis included in infection control programmes.19 For risk factors for the development of infection werethe duration of the study, midwives and infection collected. BMI, age, blood loss, method of woundcontrol staff from participating units met with closure, and emergency surgery were found to bethe project team at bi-monthly intervals. As signiﬁcantly associated with the development ofwell as feeding back results, various issues identi- SSI. Work is ongoing to further examine the factorsﬁed during the study were discussed and possible that comprise risk indices developed speciﬁcally bysolutions offered. Several positive outcomes were CDC for uterine and incisional wound infections andreported. The beneﬁts of cross-departmental/ to assess the utility of these indices in a UK setting.multiprofessional working were being realised and Both midwives and infection control nurses af-staff were more receptive to the need for infection ﬁrmed the need to carry out surveillance in thiscontrol measures in view of the unexpectedly high group of patients, but there are clearly workloadincidence of wound problems reported. As well as implications. Standardisation of maternity records,hand hygiene campaigns, theatre audits had particularly those used in the community, andbeen carried out when one unit reported a very electronic linkage of data are high priorities ifhigh number of staff and students present during routine surveillance following caesarean section iscaesarean sections. As a result, new procedures to be incorporated into quality improvement pro-had been instituted to limit the number of staff grammes locally, regionally and nationally.in theatre during a delivery. The choice of woundclosure method varied, and may be inﬂuenced byindividual preference, speed of insertion and sur- Acknowledgementsgeon experience. However, some obstetriciansbegan to review their practice after issues with We thank the staff of participating hospitals andwound closure methods were highlighted. Issues the East Midlands Health Protection Unit for theiraround the standards of record-keeping, unifor- help and support.mity of information in the maternity records anddelays in returning postnatal records to the hospi- Conﬂict of interest statementtal were also addressed. A marked improvement None declared.was reported as the study progressed. When ex-amining infection trends over the period of the Funding sourcesstudy, the decrease in the incidence of infection None.was statistically signiﬁcant over time (P ¼ 0.003),with the decrease being more marked for theunits who had participated for longer. References Prophylactic antibiotics were administered to 1. NHS Institute for Innovation and Improvement. Delivering98% of patients and compliance with prescribing quality and value. Focus on: Caesarean section. Coventry:policy was good. Antibiotics are now routinely NHS Institute for Innovation and Improvement; 2006.prescribed for this group of patients in many 2. Ofﬁce of Health Economics. Compendium of health statis-healthcare facilities, although there is no tics. 18th edn. London: Radcliffe Publishing; 2007.
SSI surveillance following caesarean section 173 3. Hillan EM. Postoperative morbidity following Caesarean 11. Reilly J, Allardice G, Bruce J, et al. An economic analysis of delivery. J Adv Nurs 1995;22:1035e1042. surgical wound infection. J Hosp Infect 2001;49:245e249. 4. Henderson E, Love EJ. Incidence of hospital-acquired infec- 12. Smyth ETM, Emmerson AM. Surgical site infection surveil- tions associated with caesarean section. J Hosp Infect 1995; lance. J Hosp Infect 2000;45:173e174. 29:245e255. 13. Plowman R, Graves N, Grifﬁn MAS, et al. The socio- 5. Holtz TH, Wenzel RP. Postdischarge surveillance for nosoco- economic burden of hospital-acquired infection. London: mial wound infection: a brief commentary. Am J Infect Public Health Laboratory Service; 1999. Control 1992;20:206e213. 14. Johnson A, Young D, Reilly J. Caesarean section surgical site 6. Report by the Comptroller and Auditor General e HC 230 infection. J Hosp Infect 2006;64:30e35. Session 1999e2000. The management and control of 15. Killian CA, Graffunder EM, Vinciguerra TJ, et al. Risk factors hospital acquired infection in acute NHS Trusts in England. for surgical-site infections following caesarean section. London: Stationery Ofﬁce; 2000. Infect Control Hosp Epidemiol 2001;22:613e617. 7. House of Commons. Forty-second report from the commit- 16. Opoien HK, Valbo A, Grinde-Anderson A, et al. Post-cesar- tee on public accounts. The management and control of ean surgical site infections according to CDC standards: hospital acquired infection in acute NHS Trusts in England. rates and risk factors. A prospective cohort study. Acta London: Stationery Ofﬁce; 2000. Obstet Gynecol Scand 2007;86:1097e1102. 8. Horan T, Culver D, Gaynes R. Results of a multicenter study 17. Tran TS, Jamulitrat S, Chongsuvivatwong V, et al. Risk fac- on risk factors for surgical site infections (SSI) following tors for postcesarean surgical site infection. Obstet Gynecol C-section (CSEC). Am J Infect 1996;24:84. 2000;95:67e71. 9. Horan TC, Gaynes RP. Surveillance of nosocomial infections. 18. Report of the Expert Maternity Group. Changing childbirth In: Mayhall CG, editor. Hospital Epidemiology and Infection (Part 1). London: Stationery Ofﬁce; 1995. Control. 3rd edn. Philadelphia: Lippincott Williams 19. Haley RW, White JW, Culver DH, et al. The efﬁcacy of infec- Wilkins; 2004. p. 1659e1702. tion surveillance and control programmes in preventing10. Myles TD, Gooch J, Santolaya J. Obesity as an indepen- nosocomial infection in US hospitals. Am J Epidemiol 1985; dent risk factor for infectious morbidity in patients who 121:182e205. undergo cesarean delivery. Obstet Gynecol 2002;100: 20. Smaill F, Hofmeyr GJ. Antibiotic prophylaxis for cesarean 959e964. section. Cochrane Database Syst Rev 1999;(2). CD000933.