b r a z j i n f e c t d i s . 2 0 1 5;1 9(2):113117

w ww.elsev ier .com/ locate /b j id

The Brazilian Journal of

INFECTIOUS DISEASES

Original article

Risk factors for surgical site infection followingcesarea case

Tlio CCezar Va Departmenb Departmenc Faculty of d Departmen

a r t i c

Article histor

Received 31

Accepted 30

Available on

Keywords:

Surgical site

Cesarean se

Postpartum

CorresponPorto Alegre

E-mail ahttp://dx.do1413-8670/an section in a Brazilian Womens Hospital:control study

cero Franco Farreta, Jessica Dallb, Vincius da Silva Monteiroc,incius Wrdig Riched, Vicente Sperb Antonellob,

t of Gynecology and Obstetrics, Hospital Fmina, Porto Alegre, RS, Brazilt of Prevention and Infection Control, Hospital Fmina, Porto Alegre, RS, Brazil

Medicine, Universidade do Extremo Sul Catarinense, Cricima, SC, Brazilt of Prevention and Infection Control, Hospital Nossa Senhora da Conceico, Porto Alegre, RS, Brazil

l e i n f o

y:

May 2014

September 2014

line 19 December 2014

infection

ction

complications

a b s t r a c t

The present study evaluated patients with diagnosis of surgical site infection (SSI) following

cesarean section and their controls to determinate risk factors and impact of antibiotic

prophylaxis on this condition.

Methods: All cesareans performed from January 2009 to December 2012 were evaluated for

SSI, based on criteria established by CDC/NHSN. Control patients were determined after

inclusion of case patients. Medical records of case and control patients were reviewed and

compared regarding sociodemographic and clinical characteristics.

Results: Our study demonstrated an association following univariate analysis between post-

cesarean SSI and number of internal vaginal examinations, time of membrane rupture,

emergency cesarean and improper use of antibiotic prophylaxis. This same situation did

not repeat itself in multivariate analysis with adjustment for risk factors, especially with

regard to antibiotic prophylaxis, considering the emergency cesarean factor only.

Conclusion: The authors of the present study not only question surgical antimicrobial pro-

phylaxis use based on data presented here and in literature, but suggest that the prophylaxis

is perhaps indicated primarily in selected groups of patients undergoing cesarean section.

Further research with greater number of patients and evaluated risk factors are fundamental

for better understanding of the causes and evolution of surgical site infection after cesarean

delivery.

2014 Published by Elsevier Editora Ltda.

ding author at: Hospital Fmina, Servico de Controle de Infecco, Rua Mostardeiro, 17, Bairro: Moinhos de Vento CEP 91430-001,, Brazil.ddress: vicente antonello@hotmail.com (V.S. Antonello).i.org/10.1016/j.bjid.2014.09.009

2014 Published by Elsevier Editora Ltda.

114 b r a z j i n f e c t d i s . 2 0 1 5;1 9(2):113117

Introduction

Surgical sitmajor causduration ofrates after to the poputor and ideprophylaxi

Among are prolongvaginal mapremature mia and gerates of pinfection.12

The benoccurrencecesarean setutions theumbilical cimpact of aphylaxis rewhen admiits real implimitations

The precesarean ssurgery witthe impact

Subjects

The presenvational stspecializedAlegre, Bracontrol of ties perform(supercialorgan/spacCenters forcare Safety

The inccase were tion and hobstetric prtion and incesarean spatients weand adhereyears), cesaday as thetious compCDC/NHSNmeeting thif patient re

The medical records of the case and control patients werereviewed with respect to sociodemographic characteristics,

e oruse nournalpproistertistic

witles aTheor co

testated cancc regres ted.

med softwerfoial S

studHosp012

ts

l of 8 oveiagne pag tots (33ed wients

(12.6spac

chats ar, the

mogrody ifferealysil exaitali

ophyer fnciecant tion y.

moed folaxired e. Ape infection (SSI) following cesarean delivery is ae of morbidity and mortality, increasing both the

patient hospitalization and hospital costs.14 SSIcesarean range from 3% to 5%, varying accordinglation being studied, the methods used to moni-ntify cases, and the use of appropriate antibiotics.57

the risk factors described for post-cesarean SSIed labor, premature rupture of membranes, excessnipulation, manual extraction of the placenta, andbirth.811 Comorbidities such as HIV, severe ane-stational diabetes are also associated with higheruerperal infection, particularly surgical wound,13

ecial effect of antibiotic prophylaxis in reducings of infection associated with elective or emergencyction is already well established.14,15 In many insti-

antibiotic administration is performed after theord has been clamped, justied by the neonatalntimicrobial use.15,16 Although antimicrobial pro-duces the risk of endometritis and incisional SSInistered correctly, much has been discussed aboutact due to the small number of studies and their.15,17,18

sent study evaluated patients who underwent aection and presented with and without SSI afterh the aim of determining risk factors and assessing

of antibiotic prophylaxis on this condition.

and methods

t manuscript is a retrospective case-control obser-udy performed at the Hospital Fmina, a hospital

in womens health located in the city of Portozil. The department of prevention and infectionhe Hospital Fmina evaluated all cesarean deliver-ed from January 2009 to December 2012 for SSI

incisional infection, deep incisional infection, ande infection), based on criteria established by the

Disease Control and Preventions National Health- Network (CDC/NHSN).19

lusion criteria for enrollment on the study as apregnant patients who underwent cesarean sec-aving a diagnosis of SSI within 30 days of theocedure. The routine of the department of preven-fection control is to evaluate all patients who hadection up till day 30 from the procedure. Controlre determined after the inclusion of case patientsd to the following inclusion criteria: similar age (2rean section, procedure performed on the same

case patient, no history of post-cesarean infec-lication up to the 13th day, taking into account the

criteria.19 Cases were excluded if a control patiente inclusion requirements could not be identied orcords were not available.

electivlabor, intraveof intetion. Aadmin

Stauationvariabables. used fsquareassocisignilogistioutcomcalculaperforExcel were pfor Soc

Theof the 27th, 2

Resul

A totaFminawere d79 casforminpatienmatchsix patSSI, 10organ/

Thepatiencriteriailar deage, bthat date anvaginaof hospotic pr

Othpregnasigniextracdeliver

Therecordprophycompaferenc emergency cesarean, comorbidities, duration ofof appropriate antibiotic prophylaxis with 2 g ofs cefazolin, duration of membrane rupture, number

vaginal examinations, and length of hospitaliza-priate prophylaxis was dened as the antibioticed 3060 min before the procedure.20

al analysis was performed using descriptive eval-h the mean standard deviation for continuousnd frequency and percentage for categorical vari-

Students t-test for independent samples wasmparing the means between groups and a chi-

to compare categorical variables. Those variableswith the outcome in univariate analysis with ae level below 0.2 were included in a multivariateession model. The odds ratios between factors and

of their respective 95% condence intervals were Also, stepwise backward multiple regression wasto reveal the best set of predictors of SSI. Microsoftare was used for the data storing and analyses

rmed using SPSS for Windows (Statistical Packageciences), version 18 (IBM, Armonk, NY, USA).y was approved by the Research Ethics Committee

ital Conceico Group, Porto Alegre, Brazil, on Augustunder registration number 04189412.3.0000.5530.

180 patients underwent cesarean at the Hospitalr the four-year study period, of which 118 (1.44%)osed with SSI after cesarean delivery. Ultimately,tients with an SSI and 79 control patients con-

the inclusion criteria were identied. Thirty-nine%) were excluded as control patients could not beith them in accordance with the study design. Fifty-

(70.9%) of the 79 cases had a supercial incisional%) had a deep incisional SSI, and 14 (17.7%) had ane SSI.racteristics of the 79 case patients and 79 controle described in Table 1. In addition to the inclusion

patients from both groups had comparatively sim-aphic characteristics, such as age, race, gestationalmass index (BMI) and comorbidities. The factorsntiated case from control patients in the univari-s were emergency cesarean, number of internalminations, time of membrane rupture, durationzation, and inappropriate administration of antibi-laxis (Table 1).actors such as ethnicity, education, number ofs, preeclampsia, and illicit drugs use showed nodifference between cases and controls. Manualof the placenta was not reported in any cesarean

ment when antibiotic prophylaxis was given wasr 72 (91%) cases and 70 (88%) controls. Antibiotics was not administered in 8 (11%) case patientsto 3 (4.3%) control patients, with no statistical dif-propriate provision of the antimicrobial prior to

b r a z j i n f e c t d i s . 2 0 1 5;1 9(2):113117 115

Table 1 Characteristics of patients undergoing cesarean section in Hospital Fmina from January 2009 to December2012.

Characteristics Case patients(n = 79)

Control p(n = 7

Age (years) 25.9 + 6.2 25.3 + 5Caucasian 69 (87.3%) 69 (87.3Obesity 22 (45.8%) 20 (35.7Total duration of hospitalization (days) 5.5 + 5.3 3.5 + 1.9Hospitalization before cesarean (days) 0.5 + 0.91 0.6 + 1.3Time of previous hospitalization (days) 10 (12.5%) 11 (13.9Number of prenatal visits 6.6 + 3.6 7.19 + 3Hemoglobin previous to cesarean (g/dL) 11.3 + 1.6 11.7 + 1Leukocyte count previous to cesarean (cells/L) 12,563 + 3434 11,341 +Interval between RM and delivery (min) 302.2 + 348.8 120.5 + Number of vaginal examinations 3.2 + 2.5 2.55 + 1Patients with prolonged labor 8 (10.1%) 3 (3.8%)Premature RM 27 (34.1%) 21 (26.9Gestational age (weeks) 38.2 + 3.4 38.3 + 2Duration of labor (min) 65.5 + 15.9 64.3 + 1Diabetes 4 (5.1%) 7 (8.8%)Arterial hy (18.9HIV (5%) Cigarette s (8.8%)Indwelling (70.3Adequate a (38.6Emergency (54.4

RM, ruptur

cesarean ocontrol pat

Antibiotassociated [OR 0.46 (0.adjusted oprophylaxiwith the ris

Multivarassociated ables that hof membrator for SSI. Tand leukocber of inteantibiotic p

Table 2 risk facto

Characteris

Hemoglobipreviouscesarean

Leukocyte previouscesarean

Time of merupture (

Number ofexamina

Adequate aprophyla

ng baaluativar

anaroprergets haot rpertension 14 (17.9%) 153 (3.8%) 4

moking 12 (15.2%) 7 urethral catheter 51 (66.2%) 52ntibiotic prophylaxis 16 (22.2%) 27

cesarean 63 (79.8%) 43

e of membranes; min, minutes.

ccurred in 16 (22.2%) case patients and 27 (38.6%)ients.ic prophylaxis administered on a timely basis waswith a lower risk of SSI in univariate analysis220.95), p = 0.049]. However, when a multivariate-dds ratio analysis was performed the use ofs at the recommended time was not associatedk of developing an SSI after cesarean delivery.

Usitors evto mulvariate

App106 empatienhave niate analysis to identify independent risk factorswith SSI (Table 2) was carried out including vari-ad p < 0.20 in the univariate analysis. Only durationne rupture was considered an independent risk fac-he remaining risk factors such as hemoglobin levelyte count prior to the obstetric procedure, num-rnal vaginal examinations and the correct use ofrophylaxis were not associated with SSI.

Multivariate analysis to identify independentrs associated with surgical site infection.

tics OR (95% CI) p value

n to

0.82 (0.531.26) 0.373

count to

1.02 (1.011.03) 0.920

mbranemin)

1.02 (1.011.04) 0.044

vaginaltions

1.15 (0.891.48) 0.277

ntibioticxis

0.63 (0.221.78) 0.388

(56.1%) hadference (p =(36.5%) of tthese, 5/19 was not givSSI. There w

No signsubgroups organ/spacalready notof the ruptu

Discussio

Independenin the scienare young amellitus, chnatal visitscesarean, eantibiotic ptwins.3,14,6,

It can beantibiotic patients9)

OR (95% CI) p value

.4 1.02 (0.971.08) 0.500%) 1.00 (0.392.56) 1.000%) 1.52 (0.693.35) 0.396

1.23 (1.071.40) 0.0020.92 (0.701.23) 0.580

%) 0.90 (0.362.25) 0.999.1 0.95 (0.871.05) 0.320.1 0.82 (0.611.10) 0.180

3582 1.02 (1.011.03) 0.080222.7 1.02 (1.011.04) 0.003.9 1.15 (1.001.33) 0.049

2.85 (0.7311.2) 0.211%) 1.41 (0.712.79) 0.416.9 0.99 (0.901.09) 0.8006.4 1.01 (0.991.03) 0.640

0.55 (0.151.95) 0.532%) 0.93 (0.422.09) 0.999

0.74 (0.163.42) 0.999 1.84 (0.694.96) 0.328%) 0.83 (0.421.65) 0.721%) 0.46 (0.220.95) 0.049%) 3.30 (1.636.67) 0.001

ckward stepwise regression analysis to all risk fac-ted for SSI showed no new result when comparediate analysis of risk factors with p < 0.20 in the uni-lysis.iate prophylaxis was given in 24 (22.6%) of thency cesarean deliveries and of these, 11/24 (45.8%)d an SSI. The remaining 82 patients from this groupeceived suitable prophylaxis and of these, 46/82 an SSI. There was no statistically signicant dif- 0.099). Appropriate prophylaxis was given in 19he 52 elective cesarean delivery patients and of(26.3%) patients had an SSI. Adequate prophylaxisen to 33 patients and of these, 10/33 (30.3%) had anas no statistically signicant difference (p = 0.899).

icant difference was found when evaluating theaccording to type of SSI (supercial, deep ande) for the risk factors assessed, except for thoseed in the group as a whole, especially the durationre of membranes.

n

t risk factors for post-cesarean SSI, as describedtic literature that included multivariate analysis,ge, obesity, hypertension or preeclampsia, diabetesorioamnionitis, nulliparity, less than seven pre-

, extended time from rupture of membranes untilmergency cesarean delivery, lack of appropriaterophylaxis, increased surgical time, and birth of

21

quite difcult to estimate the protective effect ofrophylaxis correctly administered 3060 min prior

116 b r a z j i n f e c t d i s . 2 0 1 5;1 9(2):113117

to the cesarean incision, as antimicrobials are used bothprophylactically and therapeutically, with many patients con-tinuing anttried to elistudy by inwith no hisday postpapatients, 14istered withrecords. Unof antibiotirence of SSof SSI, a other handtrue in the suggestingresult, suchany comorb

The strparticipatinresentativeFmina is a large propoand its met

The evale to the Bcesarean dewhich is co(1.46%).24

Limitatiuation of temergencysuch as thetration andstudy is towhich the rlaxis only abefore the

It is imemergencycompared was found laxis and Scesarean n

The prevariate anainternal vaemergencylaxis. Howthe multivators. Many antibiotic pthe motherquately powpost-cesareauthors of tphylactic aliterature, bindicated insection. We

emergency cesarean, duration of ruptured membranes, dura-tion of surgery, excessive vaginal manipulation, obesity, and

l risinarys.ther nal ng oy, anreve

icts

thor

r e n

eiraowinluati4;38:per Nnomlicattion.en MRisk arean8;29:Kibbeortinommctice5;26:t P, Lowintdisctrol neid

wounaecooe Dser Verg Inbot Tphylndellctiou9.sensction

Assters ct Ceiraccos Colkinsosareamonreaseareantet Gimicrobial therapy after cesarean delivery.3,15 Weminate this bias to the maximum in the presentcluding in the control group only those patientstory of infection or antibiotics use until the 30thrtum, other than the prophylaxis. Of the 158 study6 (89%) at the time of prophylaxis had been admin-

2 g of intravenous cefazolin noted in their medicalivariate analysis showed that the appropriate usec prophylaxis was a protective factor for the occur-I (Table 1), reducing the risk by 54% for any typending consistent with the literature.22,23 On the, this same protective effect situation did not holdmultivariate-adjusted odds ratio analysis (Table 2),

that other variables may have contributed to this as the extended time for ruptured membranes oridities.ength of this study includes the number ofg patients, the evaluated risk factors, and the rep-

nature of the studied group, given that the Hospitalfree and unrestricted tertiary care center serving artion of female patients of the city of Porto Alegreropolitan regions.luated patients also had a similar demographic pro-razilian pregnant population. The rate of SSI afterlivery during the four-year study period was 1.44%,nsistent with the data published by the CDC/NHSN

ons of the present research include the lack of eval-he indication for a cesarean delivery (elective or) and the absence of data in some medical records,

exact time of antimicrobial prophylaxis adminis- BMI values. Another important limitation of the

have evaluated the patient records in a period inecommendation was to perform antibiotic prophy-t the time of cord clamping, rather than 3060 mincesarean section incision.portant to highlight that patients who had an

cesarean had a 3.3-fold greater risk of SSI whenwith the controls. Additionally, no associationbetween the administration of antibiotic prophy-SI neither in patients who underwent emergencyor in those with elective cesarean.sent study demonstrated an association on uni-lysis between post-cesarean SSI and number ofginal examinations, time of membrane rupture,

cesarean and improper use of antibiotic prophy-ever, this same situation did not hold true inriate analysis that adjusts for the other risk fac-publications have questioned the use of antenatalrophylaxis and the risks it could possibly carry to

and fetus, due to both the limited number of ade-ered consistent studies and the small number ofan complications in specic situations.15,18,25 Thehe present study not only question its use as a pro-gent based on the data presented here and in theut also suggest that prophylaxis perhaps must be

selected groups of patients undergoing cesareanll documented risk factors in the literature, such as

surgicaprelimstudie

Furadditiostandideliverin its p

Con

The au

r e f e

1. Olivfolleva200

2. Cooecoappsec

3. OlsVJ. ces200

4. McreprecPra200

5. MitfollposCon

6. SchforGyn

7. YokFraEm

8. TalproMainfe200

9. ConinfeTheCenInfe

10. OlivinfeBra

11. Wilcae

12. DiaInccesObsk must form a part of this decision.18,25 This is a conclusion and must be reinforced by subsequent

research with bigger sample sizes and evaluatingrisk factors are fundamental for a better under-f the causes and evolution of SSI after cesareand in particular the role of antibiotic prophylaxisntion.

of interest

s declare no conicts of interest

c e s

CO, Ciosak SI. Infection of surgical site in theg postdischarge: impact in the incidence andon of the used methods. Rev Esc Enferm USP.37985.J, Sutton AJ, Abrams KR. Decision analytical

ic modeling within a Bayesian framework:ion to prophylactic antibiotics use for caesarean

Stat Methods Med Res. 2002;11:491512.A, Butler AM, Willers DM, Devkota P, Gross GA, Fraserfactors for surgical site infection after low transverse

section. Infect Control Hosp Epidemiol.47784.n L, Horan TC, Tokars JI, et al. Guidance on publicg of healthcare-associated infections:endations of the Healthcare Infection Controls Advisory Committee. Infect Control Hosp Epidemiol.5807.ang K, Peri A, Maimets M. Surgical-site infectionsg cesarean section in an Estonian university hospital:harge surveillance and analysis of risk factors. InfectHosp Epidemiol. 2005;26:44954.-Kofman N, Sheiner E, Levy A, Holcberg G. Risk factorsd infection following cesarean deliveries. Int Jl Obstet. 2005;90:105.S, Noskin GA, Cunningham SM, Zuccotti G, Plaskett T,J. Enhanced identication of postoperative infections.fect Dis. 2004;10:192430.R. Surgical site infections and antimicrobialaxis. In: Mandell GL, Bennett JE, Dolin R, editors., Douglas and Bennetts principles and practice ofs diseases. 7th ed. New York: Churchill Livingstone;

us paper on the surveillance of surgical wounds. The Society for Hospital Epidemiology of America;

ociation for Practitioners in Infection Control; Thefor Disease Control; The Surgical Infection Society.ontrol Hosp Epidemiol. 1992;13:599605.

JCC, Blank N, Damerau EF. Fatores de risco para de stio cirrgico em cirurgia colorretal eletiva. Revoproct. 2001;21:7583.n C, Enkin MW. Manual removal of placenta atn section. CDS Rev. 2000:CD000130.d MP, Entman SS, Salyer SL, Vaughn WK, Boehm FH.d risk of endometritis and wound infection after

section in insulin-dependent diabetic women. Am Jynecol. 1986;155:297300.

b r a z j i n f e c t d i s . 2 0 1 5;1 9(2):113117 117

13. Bjrklund K, Mutyaba T, Nabunya E, Mirembe F. Incidence ofpostcesarean infections in relation to HIV status in a settingwith limited resources. Acta Obstet Gynecol Scand.2005;84:96771.

14. Petter EC, Farret TCF, Scherer JS, Antonello VS. Fatoresrelacionados a infecces de stio cirrgico apsprocedimentos obsttricos. Scientia Medica (Porto Alegre).2013;23:2833.

15. Baaqeel H, Baaqeel R. Timing of administration ofprophylactic antibiotics for caesarean section: a systematicreview and meta-analysis. BJOG. 2013;120:6619.

16. Srun S, Sinath Y, Seng AT, et al. Surveillance of post-caesareansurgical site infections in a hospital with limited resources,Cambodia. J Infect Dev Ctries. 2013;7:57985.

17. Owens SM, Brozanski BS, Meyn LA, Wiesenfeld HC.Antimicrobial prophylaxis for cesarean delivery before skinincision. Obstet Gynecol. 2009;114:5739.

18. Ledger WJ, Blaser MJ. Are we using too many antibioticsduring pregnancy? BJOG. 2013;120:14502.

19. Horan TC, Andrus M, Dudeck MA. CDC/NHSN surveillancedenition of health care-associated infection and criteria for

specic types of infections in the acute care setting. Am JInfect Control. 2008;36:30932.

20. Weber WP, Marti WR, Zwahlen M, et al. The timing of surgicalantimicrobial prophylaxis. Ann Surg. 2008;247:91826.

21. Tran TS, Jamulitrat S, Chongsuvivatwong V, Geater A. Riskfactors for postcesarean surgical site infection. ObstetGynecol. 2000;95:36771.

22. Smaill FM, Gyte GM. Antibiotic prophylaxis versus noprophylaxis for preventing infection after cesarean section.CDS Rev. 2010;(1):CD007482.

23. Dinsmoor MJ, Gilbert S, Landon MB, et al. Perioperativeantibiotic prophylaxis for nonlaboring cesarean delivery.Obstet Gynecol. 2009;114:7526.

24. Edwards JR, Peterson KD, Mu Y, et al. National HealthcareSafety Network (NHSN) report: data summary for 2006through 2008, issued December 2009. Am J Infect Control.2009;37:783805.

25. Turrentine MA. Antenatal antibiotics: too much, too little, orjust right? BJOG. 2013;120:14535.

Risk factors for surgical site infection following cesarean section in a Brazilian Women's Hospital: a casecontrol studyIntroductionSubjects and methodsResultsDiscussionConflicts of interestReferences