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Pregnancy outcomes in young women with perinatally acquired human immunodeficiency virus-1

Published:November 03, 2008DOI:https://doi.org/10.1016/j.ajog.2008.08.020

      Objective

      The objective of the study was to review pregnancy and neonatal outcomes among perinatally infected pregnant patients at our institution.

      Study Design

      A retrospective review of maternal and neonatal records for all 10 perinatally infected adolescents between 1997 and 2007 was performed. Demographics, CD4 and viral load, antiretroviral treatment, medical comorbidities, pregnancy outcomes, and neonatal human immunodeficiency virus (HIV) status were abstracted.

      Results

      The median age at first pregnancy was 18.5 years and 70% were African American. The most common comorbidities were hematologic abnormalities (70%) and cervical dysplasia/sexually transmitted infections (STIs) (80%). Initial median CD4 and viral load were 317 cells/mm3 and 8780 copies/mL, respectively. The median gestational age at delivery was 38 weeks. The most common obstetrical complications were preeclampsia (23%) and premature rupture of membranes/preterm delivery (31%). The cesarean delivery (CD) rate was 62%, with HIV as the indication in 75%. All infants were born alive; 1 was HIV infected.

      Conclusion

      Despite high rates of STIs, CD, preterm delivery, and hypertensive disorders, perinatal outcomes were favorable.

      Key words

      Adolescent pregnancies account for more than 400,000 deliveries/year in the United States and have been associated with preterm labor, anemia, hypertensive disorders of pregnancy, low birthweight, and a higher neonatal death rate.
      • Fraser A.M.
      • Brockert J.E.
      • Ward R.H.
      Association of young maternal age with adverse reproductive outcomes.
      • Jolly M.C.
      • Sebire N.
      • Harris J.
      • Robinson S.
      • Regan L.
      Obstetric risks of pregnancy in women less than 18 years old.
      • Saftlas A.F.
      • Olson D.R.
      • Franks A.L.
      • Atrash H.K.
      • Pokras R.
      Epidemiology of preeclampsia and eclampsia in the United States, 1979-1986.
      Preterm birth rates as high as 13-18% have been reported among adolescents 10-17 years of age, and the rates of preeclampsia have been as high as 17-19% in a high school–aged cohort.
      • Chen X.K.
      • Wen S.W.
      • Fleming N.
      • Demissie K.
      • Rhoads G.G.
      • Walker M.
      Teenage pregnancy and adverse birth outcomes: a large population based retrospective cohort study.
      • Satin A.J.
      • Leveno K.J.
      • Sherman M.L.
      • Reedy N.J.
      • Lowe T.W.
      • McIntire D.D.
      Maternal youth and pregnancy outcomes: middle school versus high school age groups compared with women beyond the teen years.
      For Editors' Commentary, see Table of Contents
      Currently there are 5678 adolescents, aged 13-19 years, with human immunodeficiency virus (HIV)/acquired immunodeficiency syndrome (AIDS) living in the United States. This group is comprised of both patients infected perinatally and those who acquired the disease during adolescence. As of June 2006, more than 1300 cumulative pediatric HIV/AIDS cases have been reported in New Jersey, and about a third of them are now in their teen years. The majority of these children acquired HIV-1 by perinatal transmission.
      New Jersey Department of Health and Senior Services
      New Jersey HIV/AIDS report.
      With the introduction of combination therapy with protease inhibitors in 1996, the mortality of perinatally infected patients has decreased.
      • Abrams E.J.
      • Weedon J.
      • Bertolli J.
      • et al.
      Aging cohort of perinatally human immunodeficiency virus-infected children in New York City.
      • Grubman S.
      • Gross E.
      • Lerner-Weiss N.
      • et al.
      Older children and adolescents living with perinatally acquired human immunodeficiency virus infection.
      Reduction in disease progression and improved survival with earlier initiation of combination antiretroviral therapy in children has been reported by US as well as international investigators. The European Collaborative Study documented a lower rate of progression to category C (severe symptoms) by 1 year of age among children born from 1995 to 1999 compared with those born from 1985 to 1988 (5% compared with 25%).
      The European Collaborative Study
      Fluctuations in symptoms in human immunodeficiency virus-infected children: the first 10 years of life.
      In the United States, the Pediatrics AIDS Clinical Trials (PACTG) protocol 219 cohort showed that of children and adolescents who received combination therapy, there was a decrease in mortality from 5.3% to 0.7% from 1996 to 1999.
      • Gortmaker S.L.
      • Hughes M.
      • Cervia J.
      • et al.
      Effect of combination therapy including protease inhibitors on mortality among children and adolescents infected with HIV-1.
      Our knowledge of the sexual behaviors, reproductive choices, and pregnancy outcomes of HIV-infected adolescents and young adulthood is limited. In 1998 a case of a 14 year old adolescent who delivered a term, HIV-negative infant was reported by Crane et al.
      • Crane S.
      • Sullivan M.
      • Feingold M.
      • Kaufman G.E.
      Successful pregnancy in an adolescent with perinatally acquired human immunodeficiency virus.
      More recently Zorrilla et al
      • Zorrilla C.
      • Febo I.
      • Ortiz I.
      • et al.
      Pregnancy in perinatally HIV-infected adolescents and young adults—Puerto Rico, 2002.
      have described mother-to-child transmission (MTCT) rates and characteristics of perinatally infected pregnant adolescents. Although there were no cases of MTCT in this cohort, no details were provided regarding obstetrical or medical complications.
      • Zorrilla C.
      • Febo I.
      • Ortiz I.
      • et al.
      Pregnancy in perinatally HIV-infected adolescents and young adults—Puerto Rico, 2002.
      Pregnancy rates and issues of reproductive health in the PACTG 219C cohort have also been described, revealing sexually transmitted infection rates up to 12% and abnormal cervical cytology in 47.5% of tested adolescents.
      • Brogly S.B.
      • Watts D.H.
      • Ylitalo N.
      • et al.
      Reproductive health of adolescent girls perinatally infected with HIV.
      Therefore, given the significant uncertainties regarding pregnancy outcomes among perinatally infected patients, our objective was to describe the medical and obstetric complications of this group over the past decade at our institution. This can provide information to be utilized for assessment of the resources required to optimize maternal and neonatal outcomes for this unique population.

      Materials and Methods

      This study was approved by the Institutional Review Board at University of Medicine and Dentistry of New Jersey–New Jersey Medical School. Perinatally infected patients were included if referred to the high-risk obstetric clinic at University Hospital in Newark, NJ, and delivered between November 1997 and March 2007. Their exposure route was documented by the Francois-Xavier Bagnoud (FXB) Pediatric Infectious Disease Clinic at birth or upon entry into care in infancy or early childhood.
      A retrospective review of pediatric and prenatal charts was performed. Data abstracted included demographics (age, race/ethnicity); medical history including HIV-related complications; reproductive history (number of pregnancies, births, or abortions); gestational age at initiation of care and at delivery; prepregnancy medical, social, and surgical history; mode of delivery; and pregnancy, postpartum, and gynecologic complications. HIV-related data abstracted included treatment regimens prior to and during pregnancy, HIV-1 viral load, and absolute CD4 counts at initial prenatal visit and throughout pregnancy.
      Sex, birthweight, Apgar scores at 5 and 10 minutes, and HIV status of the infants were abstracted. HIV deoxyribonucleic acid (DNA) polymerase chain reaction (PCR) testing for the evaluation of infant status was performed within 48 hours of birth and at 1 and 4 months. If HIV DNA PCR was negative, HIV antibody testing was performed at 12 and 18 months of age. If all tests were negative, the infant was deemed HIV negative. If HIV DNA PCR was positive at any point, a confirmatory test was repeated as soon as possible. An infant was considered to have in utero transmission if there were 2 positive HIV DNA PCR tests within 2 weeks of birth. Neonatal status was documented in pediatric charts of the FXB clinic and reviewed by 2 of the authors (A.D., L.B.).

      Results

      Ten patients were seen during the study period. Three patients had 2 deliveries each for a total of 13 pregnancies. The median age at time of first pregnancy was 18.5 years (range, 16-21 years). Seven patients were African American, 2 were Hispanic, and 1 patient was white.
      All patients had a diagnosis of a medical comorbidity or a sexually transmitted infection, either before or during pregnancy, as listed in Table 1. Hematologic abnormalities, defined as anemia or history of thrombocytopenia, were present in 7 patients. One patient had severe thrombocytopenia, with a platelet nadir of 7000/mm3 during pregnancy requiring WinRho, corticosteroids during pregnancy, and platelet transfusion at delivery. Six patients had a history of pulmonary disease, with asthma or reactive airway disease being the most common. One patient had a history of cardiomyopathy prior to pregnancy with normal cardiac function during pregnancy.
      TABLE 1Medical history and sexually transmitted infections
      Pulmonary6
       Asthma/reactive airway disease6
       Bronchiectasis1
       Lymphoid interstitial pneumonitis1
      Hematologic7
       Anemia
      Hemoglobin < 10.5 g/dL;
      5
       Thrombocytopenia
      Platelets < 150,000/mm3.
      3
      AIDS-related illnesses4
       Esophageal candidiasis3
       Wasting syndrome3
       Lymphoid interstitial pneumonitis1
      Sexually transmitted infections8
       Chlamydia4
       Gonorrhea1
       Condyloma2
       Genital herpes simplex virus3
       Trichomonas2
      Williams. Pregnancy outcomes in young women with perinatally acquired HIV-1. Am J Obstet Gynecol 2009.
      a Hemoglobin < 10.5 g/dL;
      b Platelets < 150,000/mm3.
      Obstetric complications included preeclampsia (n = 3), gestational diabetes controlled with insulin (n = 1), and oligohydramnios (n = 1) (Table 2). The median gestational age at delivery was 38 weeks (range, 33-41 weeks) and 4 patients delivered preterm. Eight of the 13 infants (62%) were delivered by cesarean delivery (CD): 6 for HIV indication, 1 for previous CD, and 1 for active genital herpes outbreak.
      TABLE 2Delivery data, medical/obstetric complications, and neonatal outcomes
      CaseGestational age at deliveryInitial CD4 (cells/mm3)Initial viral load (copies/mL)Viral load at delivery (copies/mL)Adherence (%)
      Percent of visits with documentation of self-reported adherence to antiretroviral regimen.
      Medical historyHospitalizations and postpartum complicationsObstetric complicationsDelivery mode and indication for CDNeonatal status
      1332821,00017,00050Bronchiectasis/RAD, candidiasis, anemiaDeath from pulmonary complications (2000)Preterm labor, low birthweight/small for gestational ageNSVDHIV negative, CMV positive
      2a39324878041000AsthmaNoneOligohydramniosNSVDPositive
      2b339847,000< 40090Asthma, anemia, severe thrombocytopenia, wasting syndrome, candidiasisHospitalizations for thrombocytopenia, gestational diabetes, pneumonia, vomiting, postpartum endometritisPPROM, GDM, preeclampsia, low birthweightCD: HSVNegative
      33855866,83721,500100Herpes zosterNonePreeclampsia, low birthweight/small for gestational ageCD: HIVNegative
      4a3927575786467CardiomyopathyNoneNoneCD: HIVNegative
      4b4117712,4005792CardiomyopathyNoneNoneCD: repeat CDNegative
      53832185825,232100LIP, asthma, wasting syndrome, thrombocytopeniaPeriventricular multifocal leukomalacia (2006)NoneCD: HIVNegative
      6373417407220488NoneNoneGestational hypertensionCD: HIVNegative
      7a3985881< 115100Thrombocytopenia, asthmaNoneNoneNSVDNegative
      7b385905050100Thrombocytopenia, asthmaNoneLow birthweight/small for gestational ageNSVDNegative
      8352> 750,0005240100Asthma, anemia, wasting syndrome, candidiasisNonePreeclampsiaCD: HIVNegative
      936197< 40048,04282AnemiaNonePPROM, low birthweight/small for gestational ageCD: HIVNegative
      104031715,200< 400100Asthma, anemia, neuropathyHospitalized for neuropathyNoneNSVDNegative
      NSVD, normal spontaneous vaginal delivery; CMV, cytomegalovirus; GDM, gestational diabetes; HSV, herpes simplex virus; LIP, lymphoid interstitial pneumonitis; PPROM, preterm premature rupture of membranes; RAD, reactive airway disease.
      Williams. Pregnancy outcomes in young women with perinatally acquired HIV-1. Am J Obstet Gynecol 2009.
      a Percent of visits with documentation of self-reported adherence to antiretroviral regimen.
      Eight patients had a history or a diagnosis of a sexually transmitted infection (STIs) during pregnancy including (in descending order of frequency) Chlamydia, genital herpes simplex virus, Trichomonas, condyloma, or gonorrhea (Table 1). In this group, 7 had an STI diagnosed during the pregnancy. Abnormal cervical cytology was seen in 5 patients in the cohort with cervical intraepithelial neoplasia (CIN) confirmed by biopsy in 4 patients: 2 with CIN 3 and 2 with CIN 1. Two patients underwent cone biopsy prior to pregnancy, and 1 patient underwent loop electrosurgical excision procedure after her second pregnancy.
      Nine patients had previously been exposed to Zidovudine (ZDV) during childhood. Four patients had been treated with 3 or fewer antiretroviral agents prior to the first pregnancy, whereas 1 patient was exposed to 10 antiretroviral (ARV) medications prior to her second pregnancy. Patients were maintained on their previously prescribed treatment regimens unless there was evidence of genotype resistance or inadequate viral suppression on their ARV regimen. Protease inhibitor-based regimens were used in 11 out of the 13 pregnancies; 1 patient received a non–protease inhibitor-based regimen (abacavir/lamivudine/ZDV) in both of her pregnancies with adequate viral suppression (Table 3). ZDV was excluded from the ARV regimen in 3 patients based on evidence of resistance or documentation of previous prolonged monotherapy exposure during childhood. Regimen changes were made in 3 cases because of adverse effects (nausea), evidence of resistance, or inappropriate viral suppression because of the lack of adherence.
      TABLE 3Demographic characteristics and medication regimens
      CaseYear of birthYear of pregnancyAge at deliveryNumber of past ARVsRegimen during pregnancy
      119801997162ZDV, DDI, indinavir
      Regimen changed during pregnancy;
      2a19791999202None
      Patient refused antiretroviral therapy.
      2b197920062710Lamivudine, abacavir, lopinavir/ritonavir
      319832001173ZDV, DDI, indinavir/ritonavir
      4a19852002166Abacavir/lamivudine/ZDV
      4b19852006217Abacavir/lamivudine/ZDV
      519842003195ZDV, DDI, lopinavir/ritonavir
      619862004186ZDV, lamivudine, nelfinavir
      7a19822004213ZDV, lamivudine, nelfinavir
      7b19822007243ZDV, lamivudine, nelfinavir
      819832005216ZDV, DDI, nelfinavir
      Regimen changed during pregnancy;
      919882006184Tenofovir, DDI, lopinavir/ritonavir
      Regimen changed during pregnancy;
      1019872007197Lamivudine, tenofovir, lopinavir/ritonavir
      ARV, antiretroviral medication; DDI, didanosine; ZDV, zidovudine.
      Williams. Pregnancy outcomes in young women with perinatally acquired HIV-1. Am J Obstet Gynecol 2009.
      a Regimen changed during pregnancy;
      b Patient refused antiretroviral therapy.
      Inpatient admissions were required for 2 patients: 1 (case 10) for evaluation of worsening peripheral neuropathy during pregnancy, and the other patient (case 2) was admitted several times throughout her second pregnancy for severe thrombocytopenia, gastrointestinal complaints, pneumonia, and diabetes control (Table 2). Case 2 also developed postpartum endometritis. All other patients had uncomplicated postpartum courses. In addition, there was 1 death in this cohort 3 years after her pregnancy secondary to pulmonary disease.
      There were no neonatal deaths or congenital anomalies in this cohort. Four patients delivered prior to 37 completed weeks. Birthweights ranged from 1200 to 3730 g, 5 (38%) infants were less than 2500 g, of which 2 were term infants and 4 were less than the 10th percentile for gestational age. Care for these HIV-exposed neonates was provided at the FXB clinic. Only 1 child was perinatally infected for a MTCT rate of 7.7%. In this case, the mother refused ARV medications as well as cesarean delivery. There was also 1 infant diagnosed with congenital cytomegalovirus who was HIV negative. The mother of this infant had test results during pregnancy consistent with past exposure (cytomegalovirus immunoglobulin M negative, immunoglobulin G positive), but it is uncertain whether she was reinfected during pregnancy.

      Comment

      This review of our experience over the past 10 years suggests that even with high rates of medical comorbidities and obstetric complications, neonatal outcomes are favorable in most pregnancies (92%) of perinatally infected adolescents. All infants were live born and experienced few neonatal complications. The perinatal HIV transmission rate was higher than the expected national rate, which can be attributed to 1 patient's noncompliance with recommendations to reduce MTCT.
      Adolescent pregnancy has previously been reported to be associated with hypertensive disorders in pregnancy. Satin et al
      • Satin A.J.
      • Leveno K.J.
      • Sherman M.L.
      • Reedy N.J.
      • Lowe T.W.
      • McIntire D.D.
      Maternal youth and pregnancy outcomes: middle school versus high school age groups compared with women beyond the teen years.
      reported a 17% rate of pregnancy-induced hypertension among 16-19 year old females. In our cohort, 4 pregnancies (30.8%) were complicated by gestational hypertension or preeclampsia; of these, 3 were between the ages of 17 and 21 years. Adolescent pregnancies have also been associated with preterm delivery.
      • Jolly M.C.
      • Sebire N.
      • Harris J.
      • Robinson S.
      • Regan L.
      Obstetric risks of pregnancy in women less than 18 years old.
      In our group, premature preterm rupture of membranes and preterm labor complicated 3 pregnancies, 2 of which were of mothers 18 years of age or younger. In this cohort, medical comorbidities were seen in the majority of patients, particularly anemia, but did not lead to adverse maternal or fetal outcomes. Indeed, these observations appear to be consistent with expected complications previously reported by other authors in non–HIV-infected adolescents.
      • Jolly M.C.
      • Sebire N.
      • Harris J.
      • Robinson S.
      • Regan L.
      Obstetric risks of pregnancy in women less than 18 years old.
      • Chen X.K.
      • Wen S.W.
      • Fleming N.
      • Demissie K.
      • Rhoads G.G.
      • Walker M.
      Teenage pregnancy and adverse birth outcomes: a large population based retrospective cohort study.
      There was a high rate of CD (62%) in this group of patients compared with our institutional rate of 32.8%. HIV-indicated cesarean deliveries accounted for 75% of these, highlighting the likelihood of CD secondary to inadequate viral suppression. Inadequate viral suppression frequently seen in HIV-infected adolescent cohorts reinforces the need for close surveillance and counseling on treatment adherence to decrease operative deliveries.
      Perinatal HIV guidelines working group
      Public Health Service Task Force recommendations for use of antiretroviral drugs in pregnant HIV-infected women for maternal health and interventions to reduce perinatal HIV transmission in the United States.
      Complications following CD in our cohort were rare, but prior studies have shown increased morbidity rates in HIV-positive patients after CD.
      • Louis J.
      • Landon M.B.
      • Gersnoviez R.J.
      • et al.
      Perioperative morbidity and mortality among human immunodeficiency virus-infected women undergoing cesarean delivery.
      Prior CD is the most common indication for repeat cesarean section; thus, this group of patients is likely to experience repeat abdominal deliveries in future pregnancies with its associated morbidities.

      Menacker F. Trends in cesarean rates for first births and repeat cesarean rates for low risk women, United States, 1990-2003. National Vital Statistics Report, Center for Disease Control and Prevention. Hyattsville, MD.

      High-risk sexual behavior is also of concern in this group of patients. Abnormal cervical cytology and STIs affected 80% of the patients in our cohort, and 7 patients (70%) were diagnosed with an STI during pregnancy. High rates of STIs, specifically chlamydia and gonorrhea (6-22%), have also been reported in HIV-infected adolescents enrolled in the REACH (Reaching for Excellence in Adolescent Care and Health) and PACTG 219 cohorts.
      • Brogly S.B.
      • Watts D.H.
      • Ylitalo N.
      • et al.
      Reproductive health of adolescent girls perinatally infected with HIV.
      • Vermund S.H.
      • Wilson C.M.
      • Rogers A.S.
      • Partlow C.
      • Moscicki A.B.
      Sexually transmitted infections among HIV infected and HIV uninfected high-risk youth in the REACH Study.
      Abnormal cervical cytology was seen in 50% of our patients, similar to a report from the PACTG 219C cohort.
      • Brogly S.B.
      • Watts D.H.
      • Ylitalo N.
      • et al.
      Reproductive health of adolescent girls perinatally infected with HIV.
      These observations demonstrate the importance of safe-sex practices counseling because this group of adolescents and young adults not only have the potential to transmit HIV to their partners but are at high risk for acquiring new STIs.
      Although our study is limited by the cohort size and retrospective design, it provides information on the issues and concerns of this group of patients who are now reaching child-bearing age. Similar to observations in adult populations, use of highly active antiretroviral therapy has lead to reduced mortality and morbidity of perinatally infected adolescents and young adults. Nonetheless, our current challenges include how and when to address reproductive health issues such as safe-sex practices counseling, contraception, and STI prevention including early access to human papilloma virus immunization to prevent premalignant and malignant genital lesions.
      It is also imperative that we support treatment adherence to achieve and maintain viral suppression to avert operative deliveries for an HIV indication, which can compromise future reproductive health. As we decrease HIV MTCT globally, we must monitor and address the reproductive health issues experienced by this population of perinatally infected adolescents in both high- and low-income countries to improve perinatal outcomes and long-term maternal health.

      Acknowledgments

      We thank Drs James Oleske, Joseph Apuzzio, and Barry Dashefsky, Jocelyn Grandchamp, RN, and Charmaine Calilap-Bernardo, RN, for their care of this population and input in the preparation of this manuscript as well as to the clinic staff at University Obstetric Associates and University Hospital (Newark, NJ) for their excellent support and assistance in the care of these patients.

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