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Epidemiology and Prevention

Complications and Route of Delivery in a Large Cohort Study of HIV-1–Infected Women—IMPAACT P1025

Livingston, Elizabeth G. MD*; Huo, Yanling MS; Patel, Kunjal DSc, MPH†,‡; Tuomala, Ruth E. MD§; Scott, Gwendolyn B. MD; Stek, Alice MD; for the P1025 Team of the International Maternal Pediatric Adolescent AIDS Clinical Trials (IMPAACT) Group

Author Information
JAIDS Journal of Acquired Immune Deficiency Syndromes: September 1, 2016 - Volume 73 - Issue 1 - p 74-82
doi: 10.1097/QAI.0000000000001021

INTRODUCTION

The US Preventive Health Services Task Force (USPTF) and American College of Gynecologists recommend cesarean delivery before labor and before ruptured membranes for HIV-1–infected pregnant women with elevated or unknown HIV-1 plasma viral loads to prevent mother-to-child HIV-1 transmission.1,2 Despite use of highly effective and better-tolerated combination antiretroviral therapy (cART) (≥3 antiretroviral drugs from ≥2 classes) to prevent transmission and improve the health of the mother, cesarean delivery rates remain high among HIV-infected women in the United States. Additionally, there are concerns regarding increased rates of maternal morbidity and mortality of cesarean delivery in this patient population.3–5

Because of these multiple concerns for the HIV-1–infected mother and fetus, planning a delivery route that optimizes outcomes for both patients can be challenging. Our current knowledge of the maternal morbidities and complications associated with delivery route in the effective cART era is limited and provides conflicting data regarding risk.4–10 The Women Infant Transmission Study in HIV-infected women in the United States reported increased rates of morbidity from cesarean delivery.5 A later study from New Orleans suggested that morbidity in HIV-infected women undergoing cesarean was due to other comorbidities aside from HIV.9 Likewise, data from a Latin American HIV-infected pregnant cohort suggested low rates of morbidity.7 European data also reports conflicting results regarding morbidity.4,8,10 A 2005 Cochrane meta-analysis of 6 studies suggested a higher rate of postpartum morbidity in HIV-infected women but acknowledged that the risk was dropping over time.6 This reported decline may reflect improved medical care of these HIV-positive women resulting in better outcomes similar to their HIV negative peers.11–13 Differences between these studies may reflect varying definitions of morbidity or other changes in general obstetric practice such as earlier and broader use of prophylactic antibiotics. Updated information regarding cesarean morbidity with widespread use of cART will be valuable for HIV1-infected women and their clinicians considering the risks and benefits of cesarean vs vaginal deliveries when making decisions regarding the mode of delivery.

We therefore aimed to compare maternal intrapartum and postpartum complications by mode of delivery in a large cohort of HIV-infected pregnant women enrolled across the United States and Puerto Rico. Additionally, we aimed to describe the primary indications for cesarean by calendar year of delivery.

METHODS

Study Population

IMPAACT Protocol 1025 is a prospective cohort study and was designed to “assess maternal and infant safety, and the effectiveness of new and existing interventions prescribed for prevention of mother-to-child transmission of HIV and/or women's health.”14 Beginning in 2002, mothers were enrolled during pregnancy at ≥14 weeks of gestation, ≥8 weeks beginning in 2007, or postpartum within 2 weeks after delivery. Study participant follow-up continued for at least 6 months after delivery. Institutional review boards approved the protocol at all 56 clinical sites located in the United States and Puerto Rico, and written informed consent was obtained from women who had enrolled in P1025. The population eligible for this analysis included women (with at least 1 visit at or after 2 weeks postpartum as of February 1, 2013) with singleton or multiple gestation and live birth or intrauterine fetal demise ≥20 weeks of gestation. Only the most recent pregnancy with complete information on mode of delivery and intrapartum and postpartum complications was included in analyses.

Exposure of Interest

The mode of delivery was classified as “elective cesarean” (ECS), “non-elective cesarean” (NECS), or “vaginal.” For study purposes, ECS was defined as a scheduled cesarean before the onset of labor and before rupture of membranes or rupture of membranes ≤5 minutes before delivery. NECS was defined as a cesarean performed after the onset of labor or ruptured membranes ≥5 minutes before delivery. P1025 also collected information about the planned mode of delivery.

Outcomes of Interest

During maternal study visits, sites were asked to report laboratory abnormalities and diagnoses that met clinical definitions set in an Appendix of Diagnoses by the IMPAACT network. Maternal medical events were ascertained through review of study visit forms for additional visit diagnoses, laboratory abnormalities, and adverse events. Those reported during intrapartum (defined as the time from admission for delivery until delivery) and postpartum periods (defined as the time between delivery and 6 weeks after delivery) were reviewed by 2 obstetricians (E.G.L. and A.S.) and classified into 6 different morbidity outcomes: (1) Surgery plus delivery wound complications: including wound infection with erythema/induration, wound infection with pus, wound separation with blood, wound dehiscence, wound abscess, perineal cellulitis, episiotomy/laceration abscess, and other complications related to episiotomy, cesarean section, laceration or postpartum tubal ligation, (2) Infections: including endomyometritis, bacteremia/sepsis, pyelonephritis, pneumonia, mastitis, breast abscess, and perineal cellulitis (not related to an episiotomy), (3) Thromboembolic events: including septic pelvic thrombophlebitis, ovarian vein thrombophlebitis, pulmonary embolus, and deep vein thrombosis, (4) Gastrointestinal complications: including ileus, antibiotic-associated colitis, and obstruction, (5) Hemorrhagic events: including postpartum hemorrhage with hemodynamic instability, postpartum hemorrhage requiring surgery, and postpartum hemorrhage requiring blood transfusion, (6) Other complications: including febrile morbidity, retained products of conception, postpartum hemolytic uremic syndrome, vulvovaginal hematoma, congestive heart failure, postpartum depression, and postpartum cardiomyopathy.

Extended hospital stay was defined by the clinical sites. The majority of US insurance carriers and prenatal care providers however use greater than 4 days postoperatively from cesarean delivery and greater than 2 days postpartum from vaginal delivery as the standard.

Covariates of Interest

Maternal demographic and clinical covariates of interest included race, ethnicity, age at delivery, prenatal care, number of prior pregnancies, body mass index close to delivery, smoking and alcohol use during pregnancy, last CD4 count and viral load before or at delivery, last Centers for Disease Control and Prevention (CDC) classification during pregnancy, and cART use during pregnancy. Diagnoses, abnormal laboratory events, and signs/symptoms during pregnancy identified by 2 obstetricians as potential risk factors for the outcomes were also considered covariates of interest.

Statistical Analysis

Descriptive statistics for maternal demographic and clinical characteristics were calculated both overall and by the actual mode of delivery. Maternal morbidity outcomes were summarized by delivery mode. Chi-square tests and Kruskal–Wallis tests were used, as appropriate, to compare characteristics by modes of delivery. The distribution of primary indications for cesarean by year of birth was also summarized.

Associations between the mode of delivery and the maternal morbidity outcomes of interest were estimated using logistic regression models. Only the morbidity outcomes with ≥10% prevalence were evaluated in multivariable analyses. Analysis on a combined outcome defined as “any intrapartum/postpartum morbidity” was also performed. For each morbidity outcome, including “any morbidity,” a crude logistic model (including only mode of delivery) was first built; each covariate of interest was then individually added to evaluate whether it was a confounder of the mode of delivery and morbidity association; any covariate changing the effect estimate (odds ratio) for the association between mode of delivery and the morbidity outcome by 10% or more was retained as a potential confounder in the final multivariable regression model. In fitting the final multivariable models, a missing indicator was created for covariates with >5% missing data, covariates with ≥20% missing data were excluded from multivariable analyses. Based on previous studies of mode of delivery and maternal morbidity, maternal disease severity measures including the last CD4 count, viral load, CDC classification during pregnancy, and clinical diagnoses during pregnancy were forced in all final multiple regression models to adjust for potential confounding by indication.4–6,9,10 Odds ratios and 95% confidence intervals were obtained from the final regression models as estimates of the adjusted association between the mode of delivery and each maternal morbidity outcome. Statistical significance was defined as 2-sided P value < 0.05.

RESULTS

As shown in Figure 1, there were a total of 2980 maternal enrollments in P1025 as of February 1, 2013; 2725 had completed a study visit at or after 2 weeks postpartum, 2719 had live births or intrauterine fetal demise at ≥20 weeks of gestation, and 2540 had complete information on mode of delivery and intrapartum and postpartum complications. After limiting the analytic population to the most recent pregnancy enrolled in P1025, there were a total of 2297 women included in our final study population.

F1
FIGURE 1.:
Study population derivation.

Table 1 summarizes the distribution of demographic and clinical characteristics by mode of delivery. Forty-six percent of our study population (n = 1055) delivered vaginally, 35% (n = 798) had an ECS, and 19% (n = 444) had an NECS. Hispanic women, women whose last viral load during pregnancy was >400 copies per milliliter, and women with body mass index ≥40 kg/m2 during pregnancy were more likely to deliver by ECS; women with a lower CD4 count during pregnancy were more likely to have a NECS; and women who had a prior birth were more likely to have a vaginal delivery. In this analytic subset of IMPAACT P1025, there were 13 instances of mother-to-child transmission of HIV. Table 1 shows the distribution of these cases by mode of delivery stratified by last viral load during pregnancy. The small number of cases limited our ability to make statistical inferences about the association between mode of delivery and mother-to-child transmission.

T1
TABLE 1.:
Distribution of Maternal Background Characteristics by Mode of Delivery
table1-a
TABLE 1-A.:
Distribution of Maternal Background Characteristics by Mode of Delivery

Serious morbidity was considered to be need for extended/or additional care. Women with cesarean section delivery (elective or nonelective) were more likely to have their hospitalization extended, be readmitted to a hospital, or go to an Emergency Department/outpatient clinic for postpartum complication evaluation (Table 1).

Of the 2297 women in the study population, 2219 (97%) had available information on planned mode of delivery. Of the 1361 women who planned a vaginal delivery, 27% delivered by either ECS section (n = 141, 10%) or nonelective cesarean section (NECS) (n = 222, 16%). Of the 858 women who planned a cesarean section, 632 (74%) delivered as planned (ie, ECS) and 202 (24%) underwent a cesarean section after the onset of labor or ruptured membranes (ie, NECS). There were no maternal deaths in this IMPAACT 1025 analysis.

Table 2 summarizes the primary indications for cesarean by year of delivery (2002–2013). The most common primary indication for women delivered by cesarean section was a history of a cesarean section (33%). Other primary indications included interruption of HIV transmission (26%), a nonreassuring fetal heart rate (9%), arrest disorder (7%), and failed induction (6%). Over time, there was a decreasing trend of having cesarean section delivery for interrupting HIV transmission (see Supplemental Digital Content 1, https://links.lww.com/QAI/A814).

T2
TABLE 2.:
Delivery Outcome and Distribution of Maternal Intrapartum/Postpartum Morbidities

Table 3 presents data on the complications by delivery mode. Overall, 19% of the women had one or more complications after delivery, with the highest incidence for cesarean surgical wound/vaginal delivery laceration/wound complications (14%), followed by infections (11%) and other complications (7%). The frequency of all types of morbidities was highest for women who delivered by NECS, followed by ECS, and lowest for vaginal delivery. The morbidities with ≥10% frequency, surgical wound/vaginal delivery laceration/wound complications, and infections were included in the further multivariable analyses along with the overall outcome of any complications.

T3
TABLE 3.:
Distribution of the Primary Indications for Cesarean Delivery by 3-Year Intervals

Table 4 shows that after adjusting for the last CD4 count, viral load and CDC classification during pregnancy and clinical diagnoses during pregnancy, ECS, and NECS remained significantly associated with higher odds of any maternal morbidity, surgical wound/vaginal delivery laceration/wound complications, and infections, as compared with vaginal delivery.

T4
TABLE 4.:
Associations Between Mode of Delivery and Intrapartum/Postpartum Morbidities

DISCUSSION

In IMPAACT P1025, 19% of participants experienced at least 1 intrapartum or postpartum morbidity. The most common were wound complications and infectious complications. Other cohorts and case series of HIV-1–infected pregnant women have produced mixed results when evaluating delivery morbidity.4–10,15–20 The morbidity rate in IMPAACT P1025 population is higher than that reported in a Latin American/Caribbean NICHD International Site Development Initiative (NISDI) cohort of 5% complications overall.7 The difference cannot be accounted for by viral load suppression variations because IMPAACT P1025 had an 84% rate of viral load ≤400 copies per milliliter and the NISDI population had a 70% rate. As in the NISDI cohort, IMPAACT P1025 maternal delivery morbidity was more common in women delivering by NECS than by ECS and lowest with vaginal delivery. A low morbidity rate was also reported in a study of 97 HIV-infected women undergoing cesarean at Emory, from 1992 to 2000 that used HIV-uninfected controls.18 The HIV-infected women at Emory had more minor complications, but no difference in major postoperative morbidity. The Swiss Mother and Child HIV Cohort Study reported in 2006 on postpartum complications in 53 matched HIV-infected and uninfected pairs of women undergoing ECS delivery.10 Minor complications were 8-fold more frequent in the HIV-infected Swiss women. All HIV-infected Swiss women received cART, and >60% had undetectable viral load at delivery.

Older studies of HIV-infected pregnant women in the pre-cART era generally report higher rates of delivery-related morbidity.3–5 The European HIV in Obstetrics Group found that HIV-infected women were at higher risk of postpartum complications regardless of the mode of delivery than uninfected women (29% vs 19% overall complications).4 Fifty-two percent of European HIV-infected women delivering by cesarean had complications (complications were 5-fold higher with cesarean vs vaginal delivery). In 2000, the WITS study of 1200 HIV-1 infected pregnant women reported that both scheduled and nonscheduled cesareans were associated with increased postpartum morbidity, mostly postpartum fever.5 In 2000, the ACTG 185 team reported on 497 pregnant women, 132 of whom delivered by cesarean from 1993 to 1997.19 These women were not on cART, and median viral load at delivery was >6000 copies per milliliter. They found an increased risk of postpartum morbidity such as endometritis and wound infection associated with cesarean delivery. Marcollet et al20 reported on their experience with 401 HIV-infected women at a single center in Paris from 1989 to 1999. Similar to P1025, Parisian women delivering by NECS had a higher rate of complications than women delivering by ECS. Women delivering vaginally had the lowest rate of complications. NICHD's Maternal–Fetal Medicine Units Network reported maternal morbidity among 378 HIV-infected and 54,281 uninfected women undergoing cesarean delivery from 1999 to 2002.17 This study found an increased risk of overall maternal perioperative morbidity among HIV-infected vs HIV-uninfected women. Rates of common complications, including endometritis (12% vs 6%), transfusion (4% vs 2%), sepsis or pneumonia, were higher among HIV-infected vs HIV-uninfected women. A 2005 Cochrane review of safety and efficacy of cesarean delivery and HIV compiled the results of several studies between 1999 and 2004.6 Similar to our findings, the Cochrane review concluded that postpartum morbidity was highest in NECS, followed by ECS and lowest in vaginal delivery. Factors in the Cochrane review associated with risk of postpartum morbidity were advanced HIV disease stage and comorbid medical conditions.6 In P1025, the NECS group had a lower rate of HIV viral load detection ≥400, but also higher rate of depressed CD4 counts <350, suggesting the common finding of a delay in immune reconstitution.21 It is unclear how this lower CD4 count/immune reconstitution delay affected the NECS cesarean complication rate.

In our IMPAACT P1025 study population, repeat cesarean was the most common indication for cesarean, similar to a 2013 French study.16 We found HIV interruption as the second most common indication, whereas the French study had obstetric indications followed by HIV interruption.16 IMPAACT P1025 did not record indications for the first cesarean so it is possible that the first was done for HIV interruption leading up to a repeat cesarean. In the 1990s, during early use of nonsuppressive antiretroviral therapy in pregnancy, a US cohort reported increasing cesarean section rates.3 In the IMPAACT 1025 cohort, the decreasing trend of HIV interruption as an indication for cesarean over time parallels the development of more effective and better-tolerated combination antiretroviral regimens in pregnancy leading to improved HIV-1 viral load suppression.11–13

Mother-to-child transmission rates were low in IMPAACT 1025, therefore we are unable to draw clinical conclusions regarding the impact of route of delivery. There were no direct obstetric maternal deaths in this IMPAACT 1025 analysis. This differs from a report from the Maternal–Fetal Medicine Network units of HIV-1 infected women delivering from 1999 to 2002 in which 3 maternal deaths were noted.17

A limitation of our study is that the women were cared for at centers of expertise in HIV and obstetric care so may have experienced more optimal care and lower complication rates than many HIV-infected pregnant women. Our results may not be generalizable to other populations. Additionally, the IMPAACT P1025 database relied on medical diagnoses, adverse events, and concomitant medications forms completed by the sites so events may be underreported. IMPAACT P1025 also allowed women to enroll postpartum which may have led to selection of participants into the study by experience of morbidity. However, only 17% of subjects were enrolled in the postpartum period. Another limitation is that we limited our evaluation of morbidity to a single gestation. Since a cesarean delivery, frequently leads to repeat cesareans, morbidity may occur in a future pregnancy not accounted for in a single gestation study.22

Per USPTF guidelines, most obstetricians recommend cesarean delivery to HIV-1–infected patients who have a viral load >1000 copies per milliliter to prevent mother-to-child transmission. For an individual patient, many factors may influence the final choice of mode of delivery including perceived safety of the surgery. This report suggests that rates of cesarean for the indication of interruption of HIV infection are declining. Vaginal delivery provides the least maternal morbidity, followed by elective and NECS. Rates of cesarean morbidity are lower in IMPAACT 1025 than in reports before use of combined antiretroviral therapy.

ACKNOWLEDGMENTS

P1025 Team: G.B.S., University of Miami School of Medicine, Miami, FL; Elizabeth Smith, MD, National Institute of Allergy and Infectious Diseases Division of AIDS, Pediatric Medicine Branch, Bethesda, MD; Heather Watts, MD, National Institute of Child Health and Human Development, Pediatric, Adolescent, and Maternal AIDS (PAMA) Branch, Bethesda, MD; KaSaundra M. Oden, MHS, International Maternal Pediatric Adolescent AIDS Clinical Trials Group, Silver Spring, MD; Y.H., Harvard School of Public Health, Boston, MA; K.P., Harvard School of Public Health, Boston, MA; Emily A. Barr, CPNP, CNM, MSN, University of Colorado Denver, The Children's Hospital, Denver, CO; Diane W. Wara, MD, University of California at San Francisco, San Francisco, CA; Sandra K. Burchett, MD, MSc, Harvard Medical School, Boston, MA; Jenny Gutierrez, MD, Bronx-Lebanon Hospital, Bronx, NY; Kathleen Malee, PhD, Ann and Robert H. Lurie Children's Hospital of Chicago, Chicago, IL; Patricia Tanjutco, MD, Washington Hospital Center, Washington, DC; Yvonne Bryson, MD, David Geffen School of Medicine, University of California, Los Angeles, CA; Michael T. Basar, BS, Frontier Science & Technology Research Foundation, Inc., Amherst, NY; Adriane Hernandez, MA, Frontier Science & Technology Research Foundation, Inc., Amherst, NY; Amy Jennings, BS, Frontier Science & Technology Research Foundation, Inc., Amherst, NY; Tim R. Cressey, PhD, BSc, Program for HIV Prevention & Treatment, Chang Mai, Thailand; Jennifer Bryant, MPA, Westat, Rockville, MD.

Participating sites and site personnel include: 5041 Children's Hospital of Michigan NICHD CRS (Theodore B. Jones, MD; Ernestine Brown, RN; Natalie Woods, RD); 5052 University of Colorado Denver NICHD CRS (Alisa Katai, MHA; Tara Kennedy, FNP-BC; Kay Kinzie, MSN, FNP-BC; Jenna Wallace, MSW; CTSI Grant Number UL1 TR000154); 5031 San Juan City Hospital PR NICHD CRS (Rodrigo Diaz-Velasco, MD, FACOG, AAHIVS; Midnela Acevedo-Flores, MD, MT; Elvia Pérez-Hernández, BS, MEd, MA, MPH; Antonio Rodriguez-Mimoso, MD; FACOG); 5048 USC LA NICHD CRS (Françoise Kramer, MD; LaShonda Spencer, MD; James Homans, MD; Andrea Kovacs, MD); 4601 UCSD Maternal, Child, and Adolescent HIV CRS (Andrew Hull, MD; Mary Caffery, RN, MSN; Jean M. Manning RN, BSN; Stephen A. Spector, MD); 4101 Columbia IMPAACT CRS; 4201 University of Miami Pediatric Perinatal HIV/AIDS CRS (Charles D. Mitchell, MD; Salih Yasin, MD; Safia Khan, MD); 5083 Rush University Cook County Hospital Chicago NICHD CRS (Mariam Aziz, MD; Latania Logan, MD; Julie Schmidt, MD; Helen Cejtin, MD); 5096 University of Alabama Birmingham NICHD CRS (Marilyn Crain, MPH, MD; Sharan Robbins, BA; Mickey Parks, CRNP; Yvonne Gamble Duke, MA); 6901 Bronx-Lebanon Hospital IMPAACT CRS (Murli Purswani, MD; Stefan Hagmann, MD, MSc, FAAP; Mary Vachon, LMSW, MPH); 5012 NYU School of Medicine NICHD CRS (William Borkowsky, MD; Maryam Minter, RN; Aditya Kaul, MD; Nagamah Deygoo, MS); 3801 Texas Children's Hospital CRS (Shelley Buschur, RN, NMV; Kathleen Pitts, CPNP; Chivon McMullen-Jackson, BSN, RN; Theresa Aldape, LMSW; Grant Number AI069441); 4001 Chicago Children's CRS (Donna McGregor, RN); 5009 Children's Hospital of Boston NICHD CRS (Arlene Buck, RN; Catherine Kneut, RN, CPNP); 5018 USF—Tampa NICHD CRS (Patricia Emmanuel, MD; Karen Bruder, MD; Gail Lewis, RN); 6501 St. Jude/UTHSC CRS (Katherine Knapp, MD; Edwin Thorpe, MD; Nina Sublette, FNP, PhD; Pam Finnie, MSN); 2802 NJ Medical School CRS (Charmane Calilap-Bernardo, RN; Linda Bettica, RN); 3601 UCLA-Los Angeles/Brazil AIDS Consortium (LABAC) CRS (Jaime G. Deville, MD; Karin Nielsen-Saines, MD; Nicole Falgout, RN; Michele Carter, RN); 4005 Mt Sinai Hospital Med Center, Women's & Children's HIV Program (Brenda Wolfe, APN; Molly Hartrich, MPH); 5017 Seattle Children's Hospital CRS; 5023 Washington Hospital Center NICHD CRS (Steven Zeichner, MD, PhD; Sara R. Parker, MD; Vanessa Emmanuel, BA); 5028 University of Illinois College of Medicine at Chicago, Department of Pediatrics (Kenneth Rich, MD; Karen Hayani, MD; Julia Camacho, RN); 5051 University of Florida College of Medicine, Jacksonville (Mobeen Rathore, MD; Ayesha Mirza, MD; Nizar Maraqa, MD; Kathleen Thoma, MA, CCRP); 5094 University of Maryland Baltimore NICHD CRS (Douglas Watson, MD; Corinda Hilyard); 6601 University of Puerto Rico Pediatric HIV/AIDS Research Program CRS (Irma L. Febo, MD; Vivian Tamayo, MD; Ruth Santos, RN, MPH; Maritza Cruz-Rodriguez); 5003 Metropolitan Hospital NICHD CRS; 5013 Jacobi Medical Center Bronx NICHD CRS (Susan Gross, MD; Michael Moore, MD; Carmen Caines, RN); 5038 Yale University School of Medicine; 5045 Harbor UCLA Medical Center NICHD CRS (Margaret Keller, MD; Spring Wettgen, RN, PNP; Judy Hayes, RN; Yolanda Gonzalez, RN); 5095 Tulane University New Orleans NICHD CRS (Yvette Luster, RN; Robert Maupin, MD; Chi Dola, MD; Margarita Silio, MD); 6701 The Children's Hospital of Philadelphia IMPAACT CRS (Steven D. Douglas, MD; Richard M. Rutstein, MD; Carol A. Vincent, CRNP, MSN).

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Keywords:

cesarean section; HIV-1; pregnancy; surgical morbidity

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