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Drdathe.deRates of Postoperative Complicationsamong Human Immunodeficiency Virus–Infected Women Who Have UndergoneObstetric and Gynecologic Surgical Procedures Thomas A. Grubert,1 Daniela Reindell,1 Ralph Ka¨stner,1 Bernd H. Belohradsky,2 Lutz Gu¨rtler,3,a Manfred Stauber,1
and Olaf Dathe1
Departments of 1Gynecology and Obstetrics and 2Pediatrics, and 3Pettenkofer Institute of Hygiene and Medical Microbiology,Ludwig-Maximilians-University of Munich, Germany Clinical observations indicate that human immunodeficiency virus (HIV)–positive women experience more
postoperative problems than do HIV-negative women. To obtain a better estimate of the individual risk of
postoperative morbidity among HIV-infected women, and to determine which procedures pose the greatest
risk, we performed a retrospective case-control study in which we assessed the outcomes after 235 obstetric
and gynecologic surgical procedures. For purposes of comparison, an HIV-negative control patient was matched
for each of the 235 surgical procedures performed, on the basis of the type of procedure and patient age. We
found a significantly greater number of postoperative complications among the HIV-positive women. Higher
complication rates occurred after abdominal surgery (odds ratio [OR], 3.6; P p .001) and curettage (OR, 7.7;
Among HIV-infected women, the risk of complications was associated with immune status. Anti-
retroviral therapy and standard perioperative antibiotic prophylaxis did not decrease the risk of complications.
Indications for performing abdominal surgery and curettage on HIV-infected women should be carefully
weighed against the potential risk of postoperative complications.
In the Northern Hemisphere, the proportion of women of HIV-infected patients. Combination antiretroviral among HIV-infected individuals has been steadily in- therapy (ART) has significantly improved patient sur- creasing during the past 10 years, and, worldwide, it is vival rates, even among patients with advanced-stage estimated that 47% of HIV-infected individuals are women . In the United States and Europe, estimates Because of improved patient survival rates, the num- of the proportion of women among HIV-infected in- ber of operations performed on HIV-infected women dividuals range from 20% to 30% [1, 2]. Meanwhile, will probably increase in the future. Among HIV-in- significant progress has been achieved in the treatment fected women, cervical neoplasia is highly prevalent. Asthe life expectancy of these patients increases, so, too,will their chance of undergoing gynecologic surgery at Received 8 June 2001; revised 18 October 2001; electronically published 11 some point for treatment of this condition. Further- more, the improved outlook for survival often leads a Present affiliation: Loeffler Institute of Medical Microbiology, University of HIV-infected women to have a more positive attitude toward reproduction, which, in turn, leads to increased Reprints or correspondence: Dr. Thomas A. Grubert, I. Frauenklinik der Ludwig- Maximilians-Universita¨t, Maistrasse 11, D-80337 Mu¨nchen, Germany (Thomas pregnancy rates for this group. Because recent reports have shown that delivery of infants by cesarean section Clinical Infectious Diseases
independently reduces the rate of vertical transmission 2002 by the Infectious Diseases Society of America. All rights reserved.
of HIV [6, 7], we will also see an increase in the number 822 • CID 2002:34 (15 March) • HIV/AIDS
of pregnant HIV-infected women who undergo cesarean Data on virus loads were available for 51 (22%) of 235 pro- HIV-infected individuals have a higher risk of developing Lymphocyte immunophenotyping was performed on pe- infectious complications after surgery [8, 9], even after minor ripheral blood mononuclear cells isolated from whole blood procedures . Published data on this topic mainly have fo- by Lymphoprep density centrifugation (Nycomed). After un- cused on HIV-infected males. Only a few studies of HIV-in- dergoing 2 washing steps, the cells were immediately stained fected females and, in particular, HIV-infected females under- with the following fluorochrome-labeled antibodies (Becton going obstetric or gynecologic surgery have been published.
Dickinson): anti-CD3, anti-CD4, anti-CD8, anti-CD19, anti- These studies have also suggested a markedly elevated risk of CD56, and anti-CD25. Fluorescence-activated cell sorter postoperative morbidity in this group [11–14].
(FACS) analysis was performed with CellQuest FACScan re- To obtain further information about the risks faced by HIV- search software (BD Immunocytometry Systems). The absolute infected women who undergo obstetric and gynecologic sur- number of each T cell subpopulation (presented as the number gical procedures, we conducted a case-control study of 235 of cells per microliter) was calculated by multiplying the frac- surgical procedures performed on 173 HIV-positive women.
tion of cells for which staining revealed positive findings by Our objective was to determine which procedures pose the the absolute lymphocyte count, which was derived from the greatest risk for postoperative complications and to identify specific postoperative problems. This information would then All the obstetric and gynecologic surgical procedures that we enable us to better estimate individual risk and develop strat- performed were standard procedures at our teaching hospital.
egies to minimize postoperative morbidity in these patients in The surgical techniques did not undergo significant changes during the 10 years reviewed in our study. Fifty-six of the 62cesarean sections that were performed were elective procedures PATIENTS AND METHODS
done to prevent vertical transmission of HIV [6, 7]. Periop-erative antibiotic prophylaxis involved standard regimens of We have been treating HIV-infected women at our specialized cephalosporins or aminopenicillins combined with b-lactamase outpatient clinic (I. Department of Gynecology and Obstetrics, inhibitors. Such prophylaxis was administered during 68 Ludwig-Maximilians University of Munich) since 1989. As of (28.9%) of 235 procedures in the HIV-positive group and dur- June 1999, we had performed 235 obstetric and gynecologic ing 6 (2.6%) of 235 procedures in the HIV-negative control surgical procedures on 173 women. To compare the clinical outcomes of HIV-infected patients with those of control pa- None of the patients in the present study died, and life- tients, we matched an HIV-negative patient to each surgical threatening complications occurred in only 1 patient. For clas- procedure performed on an HIV-positive patient by selecting sification of the severity of the complications observed, we from our surgical records the first eligible case after the index defined the following postoperative problems as “major com- case. Patient age and the type of surgical procedure performed plications”: fever (temperature, 138ЊC for 148 h) requiring antibiotic therapy during the postoperative clinical period; the For our evaluation, the 235 surgical procedures were clas- need to perform additional surgical procedures; severe anemia sified into 6 categories: abdominal surgery (n p 72; e.g., ab- requiring blood transfusions; and disseminated intravascular dominal hysterectomy, ovariectomy, tubectomy, and cesarean coagulation. Each of these complications was associated with section); endoscopic procedures (n p 10); minor procedures prolonged patient hospitalization. The “minor complications” with an intrauterine component (n p 72; e.g., abortion and included transient fever not requiring antibiotics; impaired curettage); cervical surgery (n p 55; e.g., cervical biopsy, Loop wound healing not requiring surgical revision; anemia not re- electrosurgical excision of the transformation zone, cold-knifecone biopsy, laser vaporization, and cerclage); vulvar surgery quiring blood transfusions; urinary tract infection; and devel- opment of endometritis and lochiostasis after obstetric pro- p 1] and episiotomy [n p 22]); and p 3). A detailed analysis of the subset of cesarean sections included in the “abdominal surgery” category The statistical significance of the differences between the mean values was calculated by Student’s t test. Differences be- Diagnosis of HIV infection in the study group patients was tween proportions were calculated by use of either the 2 done by means of anti–HIV-1 ELISA and was confirmed by or, where applicable, Fisher’s exact test. A multivariate logistic Western blot analysis. Since 1995, measurement of virus loads regression model was used to identify possible independent risk has been performed on a regular basis, parallel to determination factors for postoperative complications. All statistical analyses of CD4 counts, by use of reverse-transcriptase–PCR (Roche).
were performed by use of SPSS software, version 10.0 (SPSS).
HIV/AIDS • CID 2002:34 (15 March) • 823
same frequency in HIV-positive women and HIV-negativewomen (11 complications [4.7%] per 235 procedures vs. 8 Complication rates according to HIV status.
complications [3.4%] per 235 procedures).
tively evaluated and compared the incidence of postoperative Obstetric surgery.
complications among HIV-positive patients with that among occurring among HIV-infected women after childbirth are a HIV-negative control patients. The mean patient age on the major topic of interest, we evaluated patient outcomes after day of surgery was 29.7 years for the HIV-positive women and vaginal deliveries that involved surgical procedures. It has been 30.9 years for HIV-negative women. Because the number of shown elsewhere that cesarean section is associated with a induced abortions in HIV-positive women was larger than the higher rate of postoperative maternal morbidity among HIV- number of induced abortions in available control patients, HIV- infected women, compared with that noted among HIV-neg- negative women who had undergone curettage for incomplete ative women [11, 13]. In contrast to these findings of a higher or missed abortions were included in this control group. For rate of maternal morbidity after cesarean section, we did not 84 (36%) of 235 procedures, the HIV-infected patients were see a worse outcome for HIV-infected mothers following episi- taking antiretroviral drugs at the time of the operation. The otomy performed during spontaneous vaginal delivery. The rate mean duration of HIV infection was ∼4 years. The modes of of complications after this procedure was equal in the group HIV infection were as follows: history of injection drug use (in of HIV-infected women and the control group.
50 [28.9%] of 173 patients), transmission through heterosexual Perioperative antibiotic prophylaxis.
sexual activity (50 [28.9%]), exposure to HIV in an area of phylaxis with different standard antibiotic regimens was pro- endemicity (primarily sub-Saharan Africa; 34 [19.6%]), history vided to HIV-positive patients during 68 of 235 operations.
of injection drug use plus exposure through heterosexual sexual Fifty-three of these 68 surgical interventions were abdominal activity (20 [11.6%]), and other or unknown sources (19 surgeries. Prophylactic antibiotics were provided during 6 of [11%]). Most of the treated patients with HIV infection were 235 surgical procedures (all of which were abdominal opera- asymptomatic. At the time of surgical intervention, HIV disease tions) performed on HIV-negative patients. These HIV-negative stage was determined according to Centers for Disease Control patients were presumed to have an elevated risk of infection.
and Prevention (CDC; Atlanta) classification ; 148 patients None of the 6 HIV-negative patients developed postoperative (63%) had CDC stage 1 HIV disease, 50 (21.3%) had CDC complications, but 24 of the 68 HIV-infected patients who were stage 2 disease, and 21 (8.9%) had CDC stage 3 disease. For receiving antibiotic therapy had complications. Among HIV- 16 patients (6.8%), CDC HIV disease stage was not exactly infected patients, CD4 cell counts were almost equal for patients The overall rate of complications following surgery was sub- with and without complications (mean CD4 cell count, 428 stantially increased for HIV-infected patients, compared with cells/mL vs. 440 cells/mL, respectively). The patterns of com- patients in the control group (44 complications [18.7%] per plications were also similar for the group of HIV-positive pa- 235 procedures vs. 16 complications [6.8%] per 235 proce- tients who were receiving antibiotic therapy and the group that dures). For HIV-positive patients, the majority of complications were associated with more-extensive abdominal operations, Complication rates according to immunologic status.
such as abdominal hysterectomy and cesarean section (figure also investigated how the occurrence of postoperative compli- 1). This difference is statistically significant (OR, 3.2; 95% CI, cations, examined both by type and collectively, correlated with 1.7–5.8; P ! .0001). The general complication rate was higher patient immune status at the time of surgical intervention.
in association with curettage procedures (table 1); it was more Absolute CD4 cell counts or CD4 cell percentages, as well as or less equal in all other categories of surgical procedures.
CD4/CD8 ratios, were used as surrogate markers and were Major complications occurred after 33 (14%) of 235 surgical available for 164 of 235 surgical procedures. Parallel data on interventions performed for HIV-positive patients, compared virus loads were only available for 51 procedures, because we with 8 (3.4%) of 235 interventions performed for matched did not begin measuring this parameter until 1995.
control patients. The difference between frequencies of com- As a general rule, after stratification of patients on the basis plications in the HIV-positive group and those in the HIV- of the surgical procedures performed, we found lower CD4 cell negative control group was also statistically significant (OR, counts and decreased CD4/CD8 ratios among patients who had 4.6; 95% CI, 2.1–10.3; P ! .0001). Again, the complication rate complications. However, most of these differences failed to was highest in association with abdominal surgery (OR, 5.9; reach statistical significance. A statistically significant correla- 95% CI, 2.2–15.4; P ! .0001) and curettage (OR, 3.8; 95% CI, tion between the complication rate and the CD4 cell count was seen only for patients who underwent abdominal surgery. Pa- Figure 1 shows that most complications were major. Minor tients who had general complications after abdominal surgery postoperative complications occurred with approximately the had lower CD4 cell percentages in total lymphocyte counts than 824 • CID 2002:34 (15 March) • HIV/AIDS
Postoperative complications (major and minor) among HIV-positive women (HIV-pos.) versus HIV-negative women (HIV-neg.), by type of did patients who underwent other types of surgery (mean, given zidovudine monotherapy, which was the standard treat- ment at that time. The remainder received a fairly wide range A similar trend was found with regard to the patient virus of drug combinations, including highly active ART (HAART) load at the time of surgery. The mean virus load was 10,200 regimens. The small numbers of patients studied precluded a copies/mL at the time of surgery for the 16 patients with com- meaningful statistical analysis of specific drug combinations.
plications, whereas it was 4700 copies/mL for the 35 patients Multivariate analysis for identification of independent risk
without postoperative problems. For the patients who under- factors for postoperative complications.
went abdominal procedures, the virus load at the time of sur- operations associated with the most complications (abdominal gery was 10,200 copies/mL for the 16 patients who had com- surgery and minor procedures with an intrauterine component plications versus 5000 copies/mL for the 29 patients who did multivariate analysis was performed to assess the not. Again, this difference between the means was not statis- effect of possible confounders that could have influenced pa- tient outcome. We used a logistic regression model that in- Complication rates and current ART.
cluded data on either CDC stage or CD4 cell count (variables the postoperative outcome for patients who were receiving ART, were not independent), antibiotic prophylaxis, and ART. Virus compared with those who were not receiving ART. We were load data was not included in the model, because such data surprised that the 84 patients who were receiving ART tended were available for only 46 of the patients in this subset. Other to have more complications than those who were not. The possible confounding variables that did not show a correlation overall rate of complications for the treated patients was 26.2%, in univariate analyses were not included in the regression compared with 14.6% for the untreated patients (OR, 2.08; 95% CI, 1.07–4.04; P p .036). For major complications, the CD4 cell counts of !200/mL (OR 4.29; 95% CI, 1.21–15.21) rate was 21.4% versus 9.9%, respectively (OR, 2.47; 95% CI, and advanced stages of HIV infection (OR for CDC stage 2, 9 Both differences were statistically signif- 2.87; 95%, CI 1.13–7.29) were identified as independent risk icant. The rates of minor complications in the 2 patient groups factors for postoperative complications. Perioperative antibiotic were nearly equal (4.8% for treated patients vs. 4.6% for un- prophylaxis was identified by univariate analysis as a significant treated patients). The majority of the 84 treated patients were risk factor for postoperative complications, but this finding was HIV/AIDS • CID 2002:34 (15 March) • 825
Rates of postoperative complications among HIV-positive patients and HIV-negative control patients who underwent obstetric
and gynecologic surgical procedures.
Fever for 148 h requiring antibiotic treatment Major, with fever for 148 h requiring antibiotic treatment Minor, with an intrauterine componentb (n p a Patients with 11 complication are counted only once; therefore, the total value of data provided for individual complications may not be the actual value.
b Data for patients who had both major and minor complications are included only in the entries for major complications.
not confirmed by the multivariate model. ART was not asso- plications was successful. They were considered life-threatening ciated with the rate of postoperative complications in this subset Matching of HIV-negative control patients to HIV-positive patients was done on the basis of the surgical procedure per-formed and patient age. Additional matching by the surgeon DISCUSSION
who performed the procedure would have been desirable but Our clinical observations indicate that HIV-positive women was not feasible. During analysis, we did not note any obvious experience more postoperative problems than do HIV-negative accumulations of complications attributable to particular sur- women. The number of operations performed on HIV-positive geons either in our data set or in the general statistics regarding women—in particular, elective cesarean section and cervical complications at our hospital. Therefore, even though we can- surgery—has been increasing noticeably during the past 5 years.
not rule out surgeon-dependent selection bias in the present Therefore, these complications should be kept in mind by ob- study, we believe that it was not significant.
stetricians and gynecologists who treat HIV-infected women.
When we analyzed the total number of postoperative com- To systematically investigate the incidence of complications plications for all types of procedures, we found a 13-fold greater among HIV-infected women following obstetric and gyneco- risk for HIV-infected women, compared with HIV-negative logic surgery, we retrospectively evaluated patient outcomes control patients. For major complications, the risk was in- associated with a total of 235 major and minor surgical pro- creased 14-fold for HIV-infected patients. When we analyzed cedures. The postoperative phase was often characterized by the data in more detail, we found an 8-fold greater risk for complications that had a fairly undramatic onset, a creeping fever requiring antibiotic treatment and a 14-fold greater risk clinical course, and slow clinical development. Protracted treat- for minor, transient fever. Procedures that required opening ment was often necessary, and, overall, treatment of the com- the abdominal cavity appeared to have the highest risk for HIV- 826 • CID 2002:34 (15 March) • HIV/AIDS
CD4 and CD8 cell values for patients with or without postoperative complications, by surgical procedure performed.
Class of surgical procedure, postoperative complication status Patient CD4 and CD4 values,by complication severity a Includes data for all procedures for which patient CD4 and CD8 cell counts were available.
b With intrauterine component.
c In total lymphocyte count.
d Statistically significant at P p Findings of logistic regression analysis of risk factors for postoperative complications.
AZT, azidothymidine; CDC, Centers for Disease Control and Prevention; HAART, highly active antiretroviral therapy. Included in this analysis is a subset of 144 operations performed on HIV-infected women, in which most postoperative complications occurred (abdominalsurgery and minor procedures with an intrauterine component).
infected women. Such procedures were associated with an al- during pregnancy, delivery, or both, such recommendations most 6-fold greater risk for major complications and a 19-fold greater risk for severe postoperative fever. Although postop- The high rate of infectious complications among HIV-pos- erative morbidity did not reach statistical significance, it oc- itive patients, despite the widespread use of standard antibiotic curred more frequently in HIV-positive women than in HIV- prophylaxis, was striking. Although the present study was not negative women after curettage and comparable operations.
powered to prove the efficacy of perioperative antibiotic pro- All other procedures, apparently, were not associated with phylaxis, this previously unreported observation was unex- an elevated risk of postoperative complications. This obser- pected. In the data for the subset of operations for which we vation is of particular importance with regard to HIV-infected performed multivariate analysis, the unadjusted OR for com- women who undergo surgical procedures during childbirth. It plications among patients receiving perioperative antibiotic recently has been shown that scheduled cesarean sections in- prophylaxis was 2.9 (95% CI, 1.38–6.28). One possible expla- dependently reduce the risk of vertical transmission of HIV nation for this finding could be that the proportion of patients [6, 7]. Official recommendations now suggest that HIV-in- with advanced-stage HIV infection (CDC stages 2 and 3) was fected mothers deliver their infants by means of this proce- significantly higher among patients who received perioperative dure [16, 17]. However, as reported elsewhere, HIV-positive antibiotics (OR 2.3; 95% CI, 1.06–4.98), thereby indicating a women who undergo cesarean section have a 3–4-fold in- higher baseline risk for postoperative complications.
creased risk of severe postoperative complications [11, 13, Even though perioperative antibiotic prophylaxis was not 14]. In countries in which hygiene practices are poor and confirmed to be an independent risk factor in our logistic re- access to antibiotic therapy is difficult, this risk could be much gression model, this lack of confirmation should be carefully higher—and eventually fatal—for such mothers . On the evaluated. It could indicate that standard antibiotic prophylax- other hand, HIV-positive women did not have a worse outcome is regimens used widely in general surgical and gynecologic than HIV-negative women following minor obstetric proce- procedures might not be sufficient to prevent infectious com- dures, such as suturing of perineal tears or episiotomies. If, in plications in HIV-infected women who have advanced stages the future, the rate of vertical transmission of HIV could be of HIV infection. Further studies should investigate this ques- substantially reduced even further by use of combination ART tion in more depth to define appropriate prophylactic antibiotic 828 • CID 2002:34 (15 March) • HIV/AIDS
regimens for HIV-infected women who undergo surgical who undergo obstetric and gynecologic surgical procedures.
The procedures associated with the highest risk of postoperative Overall, our data on patient immunologic status at the time morbidity include both abdominal surgery and such relatively of the operation, as measured by CD4 and CD8 cell counts minor interventions as intrauterine curettage. We were able to and virus load, showed some association, although not a sta- demonstrate a correlation between the immune status of the tistically significant correlation, with the incidence and severity patient, as measured by standard surrogate markers, and the of postoperative problems. Patients with CD4 cell counts of occurrence of postoperative complications. Other independent !200/mL or with CD4 cells comprising !25% of the total lym- risk factors could not be identified from a set of possible con- phocyte count seemed to be at a high risk for complications, founders for postoperative morbidity. We conclude that, for particularly after undergoing abdominal surgery. Patients with HIV-infected women, every indication for such surgical pro- high virus loads also seemed to be predisposed to postoperative cedures—in particular, for those that are elective—should be thoroughly balanced against the considerably elevated risk for The results of multivariate analysis of the subset of surgical postoperative morbidity. Because the significance of this study procedures associated with the most postoperative complica- is limited by its retrospective design, a prospective and mul- tions (abdominal surgery and minor procedures with an in- ticentric study could better evaluate the incidence and the se- trauterine component) provided a clearer picture. CD4 cell verity of postoperative complications among HIV-infected counts of !200/mL and advanced-stage HIV infection (CDC women. The need to perform obstetric and gynecologic pro- stage 2), respectively, were confirmed to be independent risk cedures on HIV-positive women is likely to increase in the factors in this model. Patients who belonged to these categories future, and the aforementioned type of study should be in- had 14-fold and nearly 3-fold increased risks of postoperative augurated to develop risk-reduction strategies for these patients.
complications, respectively. It would have been desirable toinclude data on virus load in the logistic regression model as Acknowledgments
well. However, virus load data were available for only one-thirdof the patients in this subset analysis.
We thank Melinda Morgan and Paul Castle, for critical read- Another objective of our study was to evaluate the impact ing of the manuscript, and Irene Krienke, for expert technical of current ART on postoperative complications. At first it was surprising that the 84 patients who received ART tended tohave more complications than the patients who were not re- References
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2011 Lasker~DeBakey Clinical Medical Research Award Tu Youyou For the discovery of artemisinin, a drug therapy for malaria that has saved mil ions of lives across the globe, especial y in the developing world. The 2011 Lasker~DeBakey Clinical Medical Research Award honors a scientist who discovered artemisinin and its utility for treating malaria. Tu Youyou (China Academy of Ch