Surgical site infection after hysterectomyAeuMuro Gashaw Lake, MD; Alexandra M. McPencow, MD; Madeline A. Dick-BiasDeanna K. Martin, MPH; Elisabeth A. Erekson, MD, MPH

OBJECTIVE: Our objective was to estimate the occurrence of surgi-cal site infections (SSI) after hysterectomy and the associated riskfactors.

STUDY DESIGN:We conducted a cross-sectional analysis of the 2005-2009 American College of Surgeons National Surgical QualityImprovement Program participant use data files to analyze hysterec-tomies. Different routes of hysterectomy were compared. The primaryoutcome was to identify the occurrence of 30-day superficial SSI

ohyx

ey

(n 221 women). Riswere route of hysterecto(95% confidence intervawith the vaginal approa1.84; 95% CI, 1.40e2.4(AOR, 1.79; 95% CI, 1.32.65; 95% CI, 1.85e3.81.06e2.24) The occurr(n 154 women) after

dippas

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de

mdmp

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Inr

ro

SGS Papers www.AJOG.orgwent hysterectomies performed by gy-necologic services. The ACS NSQIP isa national program for surgical qualityimprovement that collects uniform dataon patients who undergo surgical pro-cedures. Hospital participation in theACS NSQIP program is voluntary andcondential. This information is col-

participating in the American College of Surgeons National Surgical Quality Improvement Programare the source of the data used herein. They have not veried and are not responsible for the statisticalvalidity of the data analysis or the conclusions derived by the authors.

The authors report no conict of interest.

Presented in oral format at the 39th annual meeting of the Society of Gynecologic Surgeons,Charleston, SC, April 8-10, 2013.

Reprints not available from the authors.in improving patient safety. EffectiveJanuary 2012, CMS required allMedicare-certied hospitals to publically reportclinical data and outcome measures in aSystematic Clinical Database Registry forGeneral Surgery in theHospital Inpatient

Over the last 2advancements havechoice of hysterectothe occurrence anSSI after total abdo(TAH) has been re

From the Department of Obstetrics, Gynecology, andReproductive Scienceof Medicine, New Haven, CT.

Received Jan. 8, 2013; revised May 16, 2013; accepted June 10, 2013.

Supported in part by a grant from the Claude D. Pepper Older Americansat Yale University School of Medicine (P30AG021342 NIH/NIA) and an awaInstitutes on Aging (R03AG042363-01).

The AmericanCollege of Surgeons National Surgical Quality Improvement P0002-9378/$36.00 2013 Mosby, Inc. All rights reserved. http://dx.doi.org/10.1

490.e1 American Journal of Obstetrics& Gynecology NOVEMBER 2013cades, remarkablebeen made in they routes. Althoughrisk factors of

inal hysterectomyorted,2 neither the

hysterectomy can lead to better riskstratication in the reporting of qualityoutcomes. Our objective was to estimatethe occurrence of 30-day postoperativeSSI after all routes of hysterectomy andto identify associated risk factors.

MATERIALS AND METHODSWe conducted a secondary databaseanalysis of the 2005-2009 AmericanCollege of Surgeons National SurgicalQuality Improvement Program (ACSNSQIP) participant-use data les toanalyze the data of women who under-

Yale University School

dependence Centerd from the National

gram and the hospitalszationshave targeted preventable hospital-acquired infections, such as postoperativesurgical site infections (SSI), as a priority

in this recentmandate for public reportingof postoperative SSI are colon surgeryand hysterectomy.

the reduction of modiable risks toprevent infections. Additionally, under-standing risk factors for SSI after(CMS) and the Joint Commission onthe Accreditation of Healthcare Organi-(cellulitis) after hysterectomy. Secondary outcrence of deep and organ-space SSI afterregression models were conducted to further eof risks factors with SSI after hysterectomy.

RESULTS: A total of 13,822 women were includThe occurrence of postoperative cellulitis after h

Cite this article as: Lake AG, McPencow AM, Dick-Bia

R ecently, United States healthcareinitiatives sponsored by the Cen-ters for Medicare and Medicaid Servicesmes were the occur-sterectomy. Logisticplore the associations

d in our final analysis.sterectomy was 1.6%

CONCLUSION: Our finSSI after the vaginal avaginal hysterectomy

Key words: hysterectsurgical site infection

oechea MA, et al. Surgical site infection after hystere

Quality Reporting Program.1 The conse-quence for an institution or hospital notreporting will be a payment penaltyas of October 2013. The 2 surgicalprocedures that were identied by CMS016/j.ajog.2013.06.018coechea, MD;

k factors that were associated with cellulitismy with an adjusted odds ratio (AOR) of 3.74l [CI], 2.26e6.22) for laparotomy comparedch, operative time >75th percentile (AOR,4), American Society of Anesthesia class 31e2.43), body mass index40 kg/m2 (AOR,0), and diabetes mellitus (AOR, 1.54; 95% CI,ence of deep and organ-space SSI was 1.1%hysterectomy.

ng of the decreased occurrence of superficialroach for hysterectomy reaffirms the role forthe route of choice for hysterectomy.

y, outcome, postoperative complication,

my. Am J Obstet Gynecol 2013;209:490.e1-9.

occurrence nor the risk factors of post-hysterectomy SSI have been reported byhysterectomy route.2-4 Better under-standing of risk factors for SSI afterhysterectomy can help target efforts atlected by a formal chart review process

www.AJOG.org SGS PapersTABLE 1in addition to a 30-day postopera-tive follow-up evaluation of patients.5

Variables that are collected include

Demographic and clinical characterisuperficial surgical site infection aftwomen)

Variable

Age, n (%)

data le of the ACS NSQIP.12 Thesedenitions were also based on criteriaset by the Centers for Disease Controland Prevention (CDC).13 The primaryoutcome was the occurrence of 30-daysupercial SSI (cellulitis) after hys-terectomy. Cellulitis was dened as aninfection that involved only skin orsubcutaneous tissue of the surgical inci-sion. Secondary outcomes were theoccurrence of deep and organ-space SSIand urinary tract infection (UTI) afterhysterectomy. Deep and organ-space SSIincluded infections that involved deepsoft tissues (fascia and muscle) at andaround the surgical incision and in-fections in any part of the body thatwas opened or manipulated duringthe operative procedure. This includesvaginal cuff cellulitis and vaginal cuffabscess, peritonitis, and pelvic abscess.Deep and organ-space SSI were consid-

Descriptive statistics, Student t test,Pearson c2, and Fisher exact test(2-sided) were performed for bivariateanalysis. Three logistic regressionmodelswere conducted to further explore theassociations of risks factors for cellulitis,deep and organ-space SSI, and post-operative UTI after hysterectomy.8,9

Variables that were associated with SSIwere identied for potential inclusionin the nal model based on bivariateanalysis (P < .1). Variables were addedto the model in a stepwise fashionwith the use of forward selection (P .05). Adjusted odds ratios (AORs) and95% condence intervals (CIs) werecalculated. Statistical analysis was per-formed with STATA statistical software(version 11.0; Stata Corporation, CollegeStation, TX) and SAS statistical software(version 9.2; SAS Institute Inc, Cary, NC).

iaA

1

3

1

1

1

1

1

2

1

upic

SGS Papers www.AJOG.orgMedical diagnoses that were consideredincluded diabetes mellitus, a history ofcerebrovascular accidents (CVA) withneurologic decit, ascites, preoperativecorticosteroid use, and obesity. Obesitywas classied based on body mass index(BMI). Women were categorized as hav-ing normal weight (BMI, 75thpercentile is arisk factor for SSI. For hysterectomies inthe ACS NSQIP dataset, the operativetimeof>75thpercentilewas 149minutes.SSI categories were dened by thecriteria found in the participant use

490.e3 American Journal of Obstetrics& Gynecolered as 1 category, because these 2 cate-gories were difcult to distinguish whenhysterectomy is considered to be theprimary procedure. Finally, we exam-ined postoperative UTI, which wasdened byCDC criteria for symptomaticUTI and asymptomatic bacteriuria,which take into account the recent useof indwelling catheters and the age ofthe patient.13

TABLE 2Logistic regression model for assocVariable

Route of hysterectomy

Total vaginal hysterectomy (referent)

Laparotomya

Laparoscopic incisionsb

Operative time >75th percentile duration

American Society of Anesthesiologistsclass 3Body mass index, kg/m2

ri or

n

www.AJOG.org SGS PapersTABLE 3Demographic and clinical characteafter hysterectomy (n[ 13,822)

Variablebefore hysterectomy (n 185), (4) CPT-4 code inconsistent with hysterectomy(n 8943), (5) CPT-4 code that indi-cated pelvic exenteration procedure atthe time of hysterectomy (n 10), and(6) women with diagnosis of preop-erative infection that included sepsis,systemic inammatory response syn-drome, and septic shock immediately

Age, n (%)

(AOR, 2.37; 95% CI, 1.14e4.90), andoperative time >75th percentile (AOR,1.86; 95% CI, 1.52e2.29; Table 6).

Occurrence of SSI by route ofhysterectomyWhen we examined 6 different routesof hysterectomy (TAH, SCH, TLH,LASCH, LAVH, and TVH), we noticedsimilarities in the occurrence of SSIby abdominal incision type (Table 7).Weexamined routes of hysterectomy solelybased on abdominal incisions (laparot-omy, laparoscopic incisions, and noabdominal incisions) and noted that theroute of hysterectomy was associatedwith supercial SSI, but not deep/organ-space SSI or postoperative UTI. Finally,we examined the association of post-hysterectomy SSI by the presence orabsence of vaginal cuff incisions (SCH vsvaginal colpotomy) and found no asso-

obesity category (BMI, 40 kg/m2). Wedid not nd smoking status or hysterec-tomy for gynecologic cancer to be inde-pendent risk factors for postoperativecellulitis.Our nding of the decreased occur-

rence of supercial SSI after the vaginalapproach for hysterectomy reafrms thelong-appreciated role for vaginal hyster-ectomy as the route of choice for hyster-ectomy.14-16 Laparotomy independentlyincreased the risk of supercial SSI afterhysterectomy. A trend was seen forincreased SSI with trocar incisions(minimally invasive hysterectomies), butthis was not statistically signicant.Our ndings add to previous work

with National Healthcare Safety Network(NHSN) data to examine SSI.2,17 TheNHSN is an internet-based surveillancesystem that is usedby theCDC tomonitorhospital-acquired infections that include

ict

ste

SGS Papers www.AJOG.orghysterectomy for cancer (P < .001), ASAclass 3 (P < .001), work relative valueunit (P< .001), use of general anesthesia(P .001), and an operative time >75thpercentile (P < .001; Table 1).Variables that were associated with

30-day postoperative cellulitis on mul-tivariate logistic regressionwere the routeof hysterectomy with an AOR of 3.74(95% CI, 2.26e6.22) for laparotomy in-cisions compared with vaginal approach,operative time >75th percentile (AOR,1.84; 95% CI, 1.40e2.44), ASA class 3(AOR, 1.79; 95%CI, 1.31e2.43),morbidobesity (BMI, 40 kg/m2; AOR, 2.65;95% CI, 1.85e3.80), and diabetes mel-litus (AOR, 1.54; 95% CI, 1.06e2.24;Table 2).

Deep and organ-space SSIThe occurrence of deep and organ-spaceSSI was 1.1% (n/N 154/13,822) afterhysterectomy. No women were catego-rized as having both a deep space SSI andan organ-space SSI. Twenty-one women(0.1%) were diagnosed with both post-operative deep/organ-space SSI andUTI.Variables that were associated with deepand organ-space SSI on bivariate analysisincluded race (P .001), diabetes mel-litus (P < .01), history of CVA withneurologic decit (P < .01), currentsmoking (P .001), obesity category(P .11), preoperative ascites (P .04),preoperative anemia (P < .01), ASAclass 3 (P < .001), and an operativetime>75th percentile (P .03; Table 3).Variables that were associated with

deep and organ-space SSI onmultivariatelogistic regression included ASA class3(AOR, 1.81; 95%CI, 1.25e2.62), currentsmoking (AOR, 1.99; 95% CI,1.40e2.83), history of CVA with neuro-logic decit (AOR, 4.41; 95% CI,1.54e12.65), preoperative anemia (AOR,1.72; 95% CI, 1.21e2.43), and morbidobesity (AOR, 2.23; 95% CI, 1.43e3.49;Table 4). When we examined hysterec-tomy route, both by abdominal incisionsand by vaginal cuff incisions, with deepand organ-space SSI, we did not nd anysignicant associations.

UTIPostoperative UTI occurred in 2.7% of

women (n/N 370/13,822) after

490.e5 American Journal of Obstetrics& Gynecolhysterectomy. Variables that were asso-ciated with postoperative UTI on bivar-iate analysis included history of CVAwith neurologic decit (P .01), ASAclass3 (P< .01), and an operative time>75th percentile (P < .001; Table 5).Variables that were associated with post-operative UTI on multivariate logisticregression were a history of CVA withneurologic decit (AOR, 3.29; 95% CI,1.41e7.70), current corticosteroid use

TABLE 4Logistic regression model for assocsurgical site infection after hystere

Variable

American Society of Anesthesiologistsclass 3Current smoker

History of cerebrovascular accidentwith neurologic deficit

Preoperative anemia (hematocrit,

ri ra

www.AJOG.org SGS PapersTABLE 5Demographic and clinical characte(n[ 13,822)

Variable

Age, n (%)adjustment for all SSI was based on thepredictive model of Culver et al11 thatincorporated wound classication, ASAclassication, and operative time. Usingthese risk factors, Edwards et al2 analyzednearly 7000 hysterectomies that werereported to the NHSN. The occurrenceof all postoperative SSI (supercial, deep

ia

ste

SGS Papers www.AJOG.orgcase-controlled study with approxi-mately 800 patients after TAH and TVH.The cases and control subjects werecollected with the use of the InternationalClassication of Diseases, Ninth Revi-sion, Clinical Modication procedurecodes for hysterectomy from 4 partici-pating CDC Prevention Epicenter Pro-gram hospitals from 2003-2005. BothBMI>35 kg/m2 and intra-/postoperativeblood transfusion were identied asindependent risk factors for supercialSSI after hysterectomy with laparotomy.Similarly, a single institution chart reviewalso found obesity (BMI, 30 kg/m2)and blood transfusion (pre-, intra-,and postoperative) to be associated withall SSI after abdominal hysterectomy.4

However, others have found obesity notto be a risk factor for postoperativecomplications after gynecologic sur-gery.19 We found that, by consideringBMI>30 kg/m2, BMI was identied as arisk-factor for supercial SSI (cellulitis).In our larger multicenter analysis, we

TABLE 6Logistic regression model for assochysterectomy

Variable

History of cerebrovascular accidentwith neurologic deficit

Current corticosteroid use

Operative time >75th percentile duration

CI, confidence interval.

Lake. Surgical site infections after hysterectomy. Am J Obdid not nd an association between pre-operative transfusion and SSI. Althoughintraoperative transfusion was identiedin our bivariate analysis to be associatedwith cellulitis and deep/organ-space SSI,we did not nd a statistically signicantassociation between intraoperative trans-fusion and SSI after adjusting for othervariables. The differences in our ndingsand previous reports regarding trans-fusion (both pre- and intraoperative) asa risk factor for SSI after hysterectomylikely are related to the robust sample sizeof our study.We identied risk factors that were

associated with deep and organ-space

490.e7 American Journal of Obstetrics& GynecolSSI after hysterectomy that includedpreoperative anemia and history of CVA,which may be reective of chronic pre-operative systemic disease. These riskfactors are in addition to risk factors ofASA class 3, current smoking status,and morbid obesity (BMI, 40 kg/m2).We did not nd a statistically signicantdifference in deep and organ-space SSIbetween different hysterectomy routes.We hypothesize that our ndings ofincreased association of both preopera-tive anemia and history of CVA withdeep and organ-space SSI may reect adecrease of the bodys ability to respondto stressors of surgery and to combatpostoperative infection. We found anassociation between preoperative CVAwith residual neurologic decit and therisk of deep and organ-space SSI. CVAhas been noted to be associated signi-cantly with any adverse postoperativeevent.20 We believe that we may haveobserved this relationship because CVAwith residual neurologic decit is a risk

tion of urinary tract infection after

Adjustedodds ratio 95% CI P value

3.29 1.41e7.70 < .01

2.37 1.14e4.90 .02

1.86 1.52e2.29 < .001

t Gynecol 2013.factor for functional dependence.21 Chenet al22 found functional dependence tobe an independent risk factor for post-operative SSI, specically methicillin-resistant Staphylococcus aureus SSI, inolder adults.We did not nd differences in risk

factors for deep and organ-space SSIwhen we examined these infections sep-arately. We ultimately chose to combinethese 2 categories when examiningSSI after hysterectomy. We believe thatdeep and organ-space SSI, althoughdened distinctly by the ACS NSQIPand CDC criteria, are functionally thesame event after hysterectomy because

ogy NOVEMBER 2013of the incision at the vaginal cuff. Aftera hysterectomy, an example of a deepSSI would be considered a vaginal cuffabscess. We believe that a pelvic abscessthat drains through the vaginal cuff,which would be considered as a deepspace SSI draining through the surgicalincision, is essentially similar to a pelvicabscess that requires drainage throughinterventional radiology, which alter-natively would be categorized as anorgan-space SSI. Because of the overlapbetween these terms, we elected tocombine deep and organ-space SSI.The risk factors associated with post-

operative UTI after hysterectomy were ahistory of CVA with neurologic decit,chronic steroid use, and operativetime >75th percentile. We found theoccurrence of 30-day postoperative UTIwas 3.0% (n 402 women) after hys-terectomy. Unfortunately, we did nothave information on catheter use orduration because of limits of the dataset.One hundred forty-two women were

identied as having preoperative sys-temic infection that included sepsis,septic shock, and systemic inammatoryresponse syndrome and were excludedbecause of the inherent difference inthese cases from women who undergoscheduled elective surgery. Althoughthese conditions may be associated witha greater risk of postoperative SSI, thesmall numbers and the various differentcauses of systemic infection made itdifcult to draw conclusions in the cur-rent study.Our study has many limitations. The

rst is that our analysis was limited tothe variables that existed in the database.For example, we were limited by theACS NSQIP denition of deep andorgan-space SSI; therefore, we were alsounable to distinguish between pelvic ab-scesses, vaginal cuff cellulitis, or fasciitis.Second, specic variables were not

collected in the general ACS-NSQIPdataset that would have enhanced ourstudy ndings. For example, the typeand timing of preoperative prophylacticantibiotic administration, which is afactor linked to postoperative infec-tion,23,24 were not available in the data-base. Another limitation of this dataset

was the lack of information about the

route, operative time, diabetes mellitus,

TABLE

7All30

-day

postop

erativesu

rgical

site

infections

andurinarytrac

tinfections

byhy

sterectomyroute(n[

13,822

)

Type

ofsu

rgical

site

infection

n

Totala

bdom

inal

hysterectomy,

n(%

)

Sup

racervical

hysterectomy,

n(%

)

Totalva

gina

lhy

sterectomy,

n(%

)

Lapa

roscop

ic-assisted

vagina

lhy

sterectomy,

n(%

)

Totallap

aros

copic

hysterectomy,

n(%

)

Lapa

roscop

icsu

prac

ervica

lhy

sterectomy,

n(%

)

None

13,081

(94.6)

5069

(93.8)

688(94.0)

2921

(95.3)

2094

(94.3)

837(95.2)

1472

(96.7)

Cellulitis

217(1.6)

141(2.6)

17(2.3)

17(0.6)

17(0.8)

5(0.6)

20(1.3)

Deep/organ-space

154(1.1)

67(1.2)

8(1.1)

32(1.0)

33(1.5)

4(0.5)

10(0.7)

Urinary

tract

infection

370(2.7)

128(2.4)

19(2.6)

94(3.1)

76(3.4)

33(3.8)

20(1.3)

Lake.S

urgicalsiteinfections

afterhysterectomy.Am

JObstetGyn

ecol

2013.

www.AJOG.org SGS Papersindication for hysterectomy. Surgicalprocedures were categorized by CPTcodes alone. The occurrence of post-operative UTI after prolapse or anti-incontinence surgery has been reportedto be higher than that found in ourstudy.25 Because the women wereselected for inclusion in this study basedon hysterectomy and not prolapse orincontinence procedures, we were notable to determine the occurrence ofUTI after prolapse or incontinence pro-cedures in our current analysis.We did not nd an association with

hysterectomies that were performed forgynecologic cancer and SSI based onCPT-4 codes. This nding may also bedue to the lack of specic information inthe dataset regarding cancer stage, grade,and pathologic condition in the ACSNSQIP dataset. We were limited to theidentication of procedures for gyneco-logic cancer based on CPT-4 codes thatindicated radical dissection and lympha-denectomies. Additionally, some hyster-ectomies for cancer that required bowelresection may have been coded primarilyas colon surgery and therefore notincluded in our analysis. We did examineall cancer variables that were availablein the ACS NSQIP dataset (includingknown disseminated tumor, chemo-therapy, or radiation therapy within30 days before procedure and knowncentral nervous system tumor) bothindividually and as a composite groupand did not nd a statistically signicantassociation with SSI. This, again, likelyreects the limitation of the datasetbecause it does not include cancer stage,grade, and disease.Last, hospital participation in the

ACS NSQIP is voluntary and conden-tial, which may introduce selection bias;however, as of 2009,>320 hospitals wereparticipating in the ACS NSQIP pro-gram, which included a wide-range ofcommunity hospitals and tertiary carecenters. The ACS NSQIP participant-usedata les do not allow for identicationof participating hospitals within thedataset; therefore, we were not able toaccount for the effect of clustering ofobservations within centers. However,previous investigators have demon-

strated that the clustering effect from the

NOVEMBER 2013 AmeriASA class 3, BMI, smoking status, pre-operative anemia, CVA with neurologicdecit, and corticosteroid use are associ-ated with SSI after hysterectomy. Devel-opment of a predictivemodel for SSI afterall types of hysterectomy is needed.Unfortunately, we cannot develop a pre-dictive model with this current workbecause of a lack of a validation cohort.Decreasing preventable hospital-

acquired infections is important forthe sake of quality patient care. In light ofthe recent national CMS mandate thatrequires all Medicare-certied hospitalsto report data and outcome measurespublicly, the prevention of SSI will soonbecome important for a hospitalsnancial stability as well.1 The ACSNSQIP program to improve quality andpatient safety has succeeded by pro-viding timely, consistent, condential,risk-adjusted feedback to participatinginstitutions on the institutional occur-rence of a wide range of postoperativecomplications.5 Institutions immedi-ately can identify systems and strategiesto improve patient outcomes in outlyingareas.5 This condential risk-adjustedprogram has begun to improve surgicaloutcomes. Knowledge of the baselineoccurrence of postoperative SSI afterdifferent routes of hysterectomy andassociated risk factors is important toimprove patient safety after hysterec-tomy by helping to identify modiablefactors to prevent SSI. Because CMSenforces mandatory public reportingof postoperative SSI after hysterec-tomy without risk adjustment specicto hysterectomy, careful monitoringmust be used to identify unintendedconsequences. -

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Surgical site infection after hysterectomyMaterials and MethodsResultsCellulitisDeep and organ-space SSIUTIOccurrence of SSI by route of hysterectomy

CommentReferences