Pregnancy in HIV-infected teenagers in London

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1 DOI: /j x HIV Medicine (2011), 12, ORIGINAL RESEARCH r 2010 British HIV Association Pregnancy in HIV-infected teenagers in London A Elgalib, 1 A Hegazi, 2 A Samarawickrama, 3 S Roedling, 4 S Tariq, 5 E Draeger, 6 J Hemelaar, 7 T Rathnayaka, 8 A Azwa, 9 D Hawkins, 10 S Edwards, 4 K Perez, 11 J Russell, 11 C Wood, 12 M Poulton, 3 R Shah, 13 H Noble, 6 M Rodgers, 2 GP Taylor, 8 J Anderson 14 and A de Ruiter 1 1 Guy s and St Thomas NHS Foundation Trust, London, UK, 2 Mayday University Hospital, London, UK, 3 Caldecot Centre, King s College Hospital, London, UK, 4 Genitourinary Medicine, Mortimer Market Centre (MMC), Camden PCT, London, UK, 5 City University London, London, UK, 6 Greenway Centre, Newham University Hospital NHS Trust, London, UK, 7 Nuffield Department of Obstetrics and Gynaecology, Oxford University, The Women s Centre, John Radcliffe Hospital, Oxford, UK, 8 Imperial College London, London, UK, 9 Chelsea and Westminster Hospital NHS Foundation Trust, London, UK, 10 HIV/GUM Directorate, Chelsea and Westminster Hospital, London, UK, 11 Trafalgar Clinic, Queen Elizabeth Hospital, Woolwich, London, UK, 12 North Middlesex University Hospital, London, UK, 13 Barnet and Chase Farm Hospitals NHS Trust, London, UK and 14 Homerton University Hospital NHS Foundation Trust, London, UK Objective The aim of the study was to describe pregnancies in HIV-infected teenagers. Methods A review of the case notes of HIV-infected pregnant teenagers aged years from 12 London hospitals was carried out for the period Results There were 67 pregnancies in 58 young women, of whom one was known to have acquired HIV vertically. The overall mother-to-child transmission (MTCT) rate of HIV was 1.5% (one of 66). There were 66 live births. Median ages at HIV diagnosis and conception were 17 and 18 years, respectively. Sixty-three per cent of women were diagnosed with HIV infection through routine antenatal screening. Eighty-two per cent of pregnancies (41 of 50) were unplanned, with 65% of women (26 of 40) using no contraception. Forty-three per cent of the women (20 of 46) had a past history of a sexually transmitted infection (STI). In 63 pregnancies, antiretroviral therapy was started postconception, with prevention of HIV MTCT the only indication in 81% of cases. Fifty-eight per cent of those on highly active antiretroviral therapy (HAART) had an undetectable HIV viral load by delivery. Eighty-seven per cent were uncomplicated pregnancies. Seventy-one per cent delivered by Caesarean section and 21% (14 of 64) had a preterm delivery (o37 weeks). In the 12 months after delivery, 45% of women received contraceptive advice and 25% of women became pregnant again. Conclusion Obstetric and virological outcomes were favourable in this group of HIV-infected young women. However, the majority of pregnancies were unplanned with poor documentation of contraception use and advice and low rates of STI screening. A quarter of women conceived again within 12 months of delivery. Effective measures to reduce STIs, unplanned pregnancies and onward HIV transmission in HIV-infected teenagers are needed. Keywords: HIV infection, pregnancy, teenagers Accepted 25 June 2010 Introduction The success of highly active antiretroviral therapy (HAART) has meant that more children with vertically acquired HIV Correspondence: Dr A. Elgalib, The Heath Clinic, Mayday University Hospital, 530 London Road, Croydon CR7 7YE, UK. Tel: ; fax: ; alielgalib@yahoo.co.uk infection are surviving into adolescence and young adulthood; the size of this cohort in the UK is expected to continue to increase [1]. In addition, young people aged 16 to 24 years account for around 11% of new HIV diagnoses in the United Kingdom each year [2]. Studies of HIV-infected adolescents have noted a high prevalence of psychosocial problems, recreational drug use 118

2 Pregnancy in HIV-infected teenagers 119 and sexual risk-taking behaviour as well as poor uptake of nonbarrier contraception and high rates of sexually transmitted infections (STIs) [3 9]. There is significant overlap between the social, demographic and behavioural determinants of teenage pregnancy and the characteristics of adolescents living with HIV [10]. Studies exploring pregnancy in HIV-infected adolescents are limited. The largest described 1183 live births in 1090 pregnant adolescents in the United States, the majority of whom had acquired HIV infection sexually [11]. Most pregnancies were unplanned (83%) and occurred in teenagers who had previously been pregnant (67%). A prospective cohort study of 638 vertically infected girls, again in the USA, reported 45 pregnancies, with 17% of girls experiencing a first pregnancy by their 19th birthday [8]. Of the 32 pregnancies resulting in live births, one infant was HIV-infected, 29 were uninfected and two had unknown infection status. Chibber and Khurranna also reported favourable obstetric outcomes and no cases of vertical transmission in a study of 30 pregnant vertically infected adolescents in India [12]. Other case series have described similar findings [13 15]. In a small European study, there were nine live births with no mother-to-child transmissions [16]. To date there have been no studies in the UK looking at pregnancy in teenagers living with HIV. In this study we reviewed the pregnancies of 58 HIVinfected teenagers attending for care at 12 London hospitals. We explore the medical and social features of this group and describe their sexual and reproductive health issues, their response to antiretroviral therapy (ART) and pregnancy outcome. Methods We conducted a retrospective case note review of HIVinfected pregnant female patients aged between 13 and 19 years who conceived and delivered between 1 May 2000 and 1 May 2007 at 12 London hospitals. Patients were identified from clinic databases. Terminations of pregnancy and miscarriages were excluded because of incomplete data. Data were collected retrospectively from the medical records using a standardized pro forma across all 12 centres. Maternal demographic, clinical, immunological, virological and socioeconomic data were obtained, including Centers for Disease Control and Prevention disease classification, HIV acquisition risk factors, CD4-positive T lymphocyte count (CD4 cell count) and plasma HIV viral load (VL) copy number at booking, ART use and pregnancy outcome. Social data included smoking, alcohol and recreational drug use during pregnancy, occupation, housing and financial issues, history of domestic violence or sexual abuse and living circumstances. Sexual and reproductive health data such as previous pregnancies, contraception use prior to index pregnancy, contraception advice in the 12 months preceding pregnancy and post delivery, conception within 12 months after delivery, sexual health screens and past history of STIs were also collected. Maternal ART in pregnancy was classified as zidovudine (ZDV) monotherapy, protease inhibitor (PI)-based HAART and nonnucleoside reverse transcriptase inhibitors (NNRTI)- based HAART. Data were obtained on reported side effects, self-reported adherence (with 100% adherence defined as patients stating that they did not miss a single dose of ART), HIV VL log 10 drop at 4 weeks from ART initiation and HIV VL at or closest to delivery (pre-delivery only). Mode of delivery was categorized as normal vaginal delivery, elective Caesarean section and emergency Caesarean section. Planned and actual modes of deliveries were recorded. Gestational age in completed weeks at delivery was grouped as 37, 35 36, and o32 weeks. Infants were considered uninfected if the HIV DNA polymerase chain reaction (PCR) was negative after 3 months of age or if the HIV antibody test was negative after 18 months of age. All analyses were conducted in Microsoft Office Excel The study protocol was submitted to Guy s and St Thomas NHS Foundation Trust Ethics Committee who advised that informed consent from patients whose notes were reviewed was not required. Results Maternal characteristics (Table 1) There were 67 pregnancies in 58 women, of whom 34 (59%) were of Black African origin and 10 (17%) were of Black Caribbean origin. One patient was diagnosed at 6 years of age and vertical transmission could not be excluded in 25 (43%) who were already sexually active when diagnosed with HIV infection in their early teens. Median CD4 count at booking was 379 cells/ml [interquartile range (IQR) cells/ml] and six patients (9%) had had an AIDS-defining illness. The majority of women (63%) were diagnosed with HIV infection through routine antenatal screening. A history of sexual abuse was reported by 45% of patients (18 of 40). Housing and financial problems were reported by over half of the group [58% (36 of 62) and 62% (34 of 55), respectively]. Over half of the patients were unemployed. Of 23 students, six were of compulsory schooling age at conception.

3 120 A Elgalib et al. Table 1 Maternal characteristics (n 5 67*) Characteristic Number (%)* Ethnicity (n 5 58) Black African 34 (59) Black Caribbean 10 (17) Caucasian 8 (14) Other 6 (10) Born in the UK (n 5 58) 16 (28) Age at conception (years) [median (IQR)] 18 (17 19) Age at HIV diagnosis (years) [median (IQR)] 17 (16 18) Known HIV-infected pre-conception 25 (37) Gestation age at HIV diagnosis when not 18 (15 30) previously known (weeks) [median (IQR)] HIV risk Vertical transmission 1 (1) From endemic country 42 (63) HIV-infected/high-risk partner 24 (36) Injecting drug user 0 (0) CD4 count (cells/ml) [median (IQR)] 379 ( ) HIV VL (copies/ml) [median (IQR)] 6510 ( ) HIV disease stage Asymptomatic HIV 58 (87) Symptomatic HIV 3 (5) AIDS 6 (9) Living circumstances (n 5 50) Living with parents 11 (22) Living with partner 17 (34) Living alone 22 (44) Housing problems (n 5 62) Yes 36 (58) No 26 (42) Financial problems (n 5 55) Yes 34 (62) No 21 (38) History of domestic violence (n 5 49) Yes 5 (10) No 44 (90) History of sexual abuse (n 5 40) Yes 18 (45) No 22 (55) Smoking during pregnancy (n 5 64) Yes 23 (36) No 41 (64) Recreational drug use during pregnancy (n 5 52) Yes 8 (15) No 44 (85) Alcohol drinking during pregnancy (n 5 53) Yes 23 (43) No 30 (57) Occupation (n 5 61) Unemployed 33 (54) Employed 5 (8) Student 23 (38) IQR, interquartile range; VL, viral load. Sexual health and contraception (Table 2) An STI screen in the 12-month period pre-conception was documented in 92% of women (33 of 36) and there were no data for 46% (31 of 67). A history of STIs was reported by 43% of women (20 of 46), with no documentation in 31% (21 of 67). Table 2 Sexual health and contraception (n 5 67*) Characteristic Number (%) Number of male partners in preceding 12 months (n 5 48) 1 43 (90) 41 (range 2 10) 5 (10) STI screen (n 5 36) 6 months pre-conception 20 (56) 12 months pre-conception 13 (36) Never tested 3 (8) Past history of STIs (n 5 46) Yes 20 (43) No 26 (53) Contraception use (n 5 40) Condoms 14 (35) Nonbarrier method 0 (0) None 26 (65) Contraception discussion in 12 months preceding 15 (60) conception in known HIV cases (n 5 25) Contraception discussion in 12 months post delivery 30 (45) Conceived within 6 months after previous delivery 7 (10) Conceived within 12 months after previous delivery 10 (15) STI, sexually transmitted infection. Condoms were used by 35% of women (14 of 40) and 65% (26 of 40) reported no contraception use, while contraception use was not documented in 40% (27 of 67). Contraception advice in the 12 months preceding pregnancy was documented in 60% of women (15 of 25) diagnosed with HIV infection before pregnancy. Discussion of contraception post-delivery was only documented in less than half (45%) of the notes reviewed. Conception within 6 months after delivery occurred in 10% (seven of 67) and a further 15% (10 of 67) conceived within 12 months; 47% (eight of 17) of these pregnancies occurred despite documented contraception advice, 88% (15 of 17) were unplanned and 12% (two of 17) were terminated (data not shown). Obstetric history and ART during pregnancy (Table 3) The majority of pregnancies (82%; 41 of 50) were unplanned. Only four patients were taking HAART at conception. Of the 94% (63 of 67) who started ART during pregnancy, prevention of vertical transmission was the sole indication in 81% (51 of 63). ZDV monotherapy was prescribed in 22% of patients. Forty-eight per cent were on a PI-based regimen and 30% on an NNRTI-based combination. ART-associated side effects were reported by 31% of women (20 of 63), the most frequent being nausea and vomiting (14 of 20). Two patients developed a rash. Treatment was interrupted in 15% of women (three of 20) who reported side effects (data not shown). One hundred

4 Pregnancy in HIV-infected teenagers 121 Table 3 Obstetric history and antiretroviral therapy (ART) during pregnancy (n 5 67*) Characteristic per cent adherence was self-reported by 59% of women (34 of 58). An HIV VL o50 copies/ml at or closest to delivery was documented in 62% of women (39 of 63). Pregnancy outcome (Table 4) Number (%)* Parity Primigravida 38 (57) Gravida 2 23 (34) Gravida 3 6 (9) Planned pregnancy (n 5 50) Yes 9 (18) No 41 (82) Gestational age at booking (weeks) [median (IQR)] 17 (4 34) Gestational age at 1st HIV appointment in new cases (weeks) 20 (9 37) [median (IQR)] On HAART at conception 4 (6) Reason for starting ART during pregnancy (n 5 63) For prevention of MTCT only 51 (81) For prevention of MTCT and maternal health (low CD4 cell count) 12 (19) Type of ART started during pregnancy (n 5 63) ZDV monotherapy 14 (22) PI-based HAART 30 (48) NNRTI-based HAART 19 (30) Gestational age at initiation of ART (weeks) [median (IQR)] 28 (12 37) Developed ART-associated side effects 20 (31) Adherence to ART (n 5 58) 100% 34 (59) o100% 24 (41) 1 log 10 drop in HIV VL 4 weeks after starting ART (n 5 63) 43 (68) Undetectable HIV VL at or closest to delivery 39 (62) HAART, highly active antiretroviral therapy; IQR, interquartile range; MTCT, mother-to-child transmission; PI, protease inhibitor; NNRTI, nonnucleoside reverse transcriptase inhibitors; VL, viral load; ZDV, zidovudine. Pregnancy-related complications such as gestational diabetes (n 5 1), pre-eclamptic toxaemia (n 5 2) and antepartum haemorrhage (n 5 1) were seen in 13% of patients (individual data not shown). Mode of delivery was normal vaginal delivery in 29%, elective Caesarean section in 56% and emergency Caesarean section in 15%. Of the 67 deliveries, 14 (21%) were preterm (o37 weeks) with more than half (eight of 14) occurring at 34 weeks. More than half of patients (64%; 36 of 56) received intrapartum intravenous ZDV. There were 66 (99%) live births, of which 82% (50 of 61) received ZDV monotherapy as prophylaxis. The one HIV-infected infant had a positive HIV DNA PCR test within 48 h of delivery, indicating in utero transmission. All 66 uninfected infants had either a negative HIV DNA PCR at 3 months of age or a negative HIV antibody test at age 18 months. The HIV-infected infant s mother had an HIV VL of copies/ml at booking at 29 weeks, Table 4 Pregnancy outcome (n 5 67*) Characteristic Number (%) Pregnancy complications 9 (13) Planned mode of delivery (n 5 63) Normal vaginal delivery 21 (33) Elective Caesarean section 42 (67) Actual mode of delivery (n 5 65) Normal vaginal delivery 19 (29) Elective Caesarean section 36 (56) Emergency Caesarean section 10 (15) Gestational age at delivery (n 5 64) 37 weeks 50 (78) weeks 6 (9) weeks 7 (11) o32 weeks 1 (1) Live birth 66 (99) Intrapartum treatment (n 5 56) Intravenous ZDV 36 (64) None 20 (36) Sex of infants (n 5 66) Female 33 (50) Male 33 (50) Birth weight (n 5 57) 43kg 22 (39) kg 16 (28) o2.5 kg 19 (33) ART received by infants (n 5 61) ZDV monotherapy 50 (82) HAART 11 (18) Neonatal complications 6 (9) HIV-infected infants 1 (1.5) ART, antiretroviral therapy; HAART, highly active antiretroviral therapy; ZDV, zidovudine. and she started a PI-based HAART regimen at 29 weeks. Her HIV VL at 36 weeks was 180 copies/ml and she delivered by elective Caesarean section at 38 weeks. The HIV-infected infant was asymptomatic and was started on HAART within a month of delivery. She was well when last seen in clinic. Discussion Reassuringly, despite the difficult medical and social circumstances of this vulnerable group of young women with HIV infection and high rates of unplanned pregnancy, the obstetric and virological outcomes were favourable. This is consistent with previous studies [9,11,12,16] and with pregnancies in HIV-infected adults from the UK and Ireland [17]. The overall HIV mother-to-child transmission rate was 1.5%. The percentage of women with an undetectable HIV VL at or closest to delivery was 58%, and 21% had preterm delivery (o37 weeks). The favourable outcome in this study may in part be explained by the multidisciplinary care the patients received. In all 12 centres, HIV-infected pregnant women were cared for by a team comprised of, at least, an HIV specialist, obstetrician,

5 122 A Elgalib et al. paediatrician and specialist midwife, as per the British HIV Association pregnancy guidelines [18]. Out of 67 pregnancies, 18 occurred in centres (three of 12) with dedicated adolescent HIV services; however, most of these pregnancies preceded the development of such specialist services. As other studies have reported [6,11], there were significant and complex psychosocial problems among this group. About half (44%; 22 of 50) lived alone, 58% (36 of 62) had housing problems, 10% (five of 49) had a history of domestic violence, 45% (18 of 40) reported a history of sexual abuse and over half of the women (62%; 34 of 55) encountered financial difficulties. As seen in American teenagers with HIV infection [9], the majority of pregnancies in this group were unplanned. Previous studies showed that the rates of high-risk sexual behaviour among HIV-infected adolescents and young adults were substantial [4 10,19]. In this study we found a striking lack of documentation of contraception use (40%; 27 of 67), past history of STIs (31%; 21 of 67) and date of the latest STI screen (46%; 31 of 67) in a significant proportion of patients. It is of particular concern that only 35% of the women (14 of 40) used condoms and 65% (26 of 40) used no contraception at all, with implications for onward HIV transmission and further unplanned pregnancy. Furthermore, although approximately half the patients were documented as having received advice regarding contraception post delivery, a quarter conceived within 12 months after delivery, of whom 53% (nine of 17) had not received contraception advice. The vast majority (88%) of pregnancies after delivery were unplanned. A limitation of this study is inherent to retrospective medical case note review. Documentation bias and the considerable amount of missing data mean that point estimates may be an underestimate of the true proportions, especially when relating to socioeconomic characteristics and condom use. It is possible that some pregnancies in eligible patients were not recorded in the computerized hospital databases which might have resulted in underestimating the number of pregnancies included in the study period. In addition, the small number of pregnancies reported makes our findings entirely descriptive. However, this study identifies a need for more effective strategies in the management of HIV-infected teenagers with particular emphasis on sexual and reproductive health. This may be achieved by establishing specialist HIV services for adolescents and teenagers within HIV networks. A multidisciplinary team facilitates the provision of comprehensive, seamless and integrated services with appropriately tailored reproductive health services. Within specialized services, teenagers would receive a one-stop shop service including HIV care, sexual and reproductive health input and psychosocial support in an appropriate environment provided by skilled staff in a sensitive and nonjudgmental manner. To conclude, this study is the largest in Europe looking specifically at pregnant HIV-infected teenagers. Although pregnancy and virological outcomes are favourable in this group, there is a strikingly high level of social vulnerability and poor sexual and reproductive health resulting in a high rate of further unplanned pregnancy. This is of considerable concern especially as this may be an underestimate because of the amount of missing data. Prospective analytical multicentre studies to identify HIV-infected teenagers medical and social needs and barriers to contraception and adherence in the United Kingdom are clearly warranted. These should be complemented by qualitative research that explores the complex socioeconomic factors that drive risk taking and sequential pregnancy in this vulnerable group. Acknowledgements We acknowledge Rozanna Issa, Specialist Midwife-Sexual Health, Robyn Cross, Paediatrics Clinical Nurse Specialist and Veronica Magaya, Clinical Nurse Specialist at Guy s and St Thomas NHS Foundation Trust. References 1 Foster C, Judd A, Tookey P et al. Young people in the United Kingdom and Ireland with perinatally acquired HIV: the pediatric legacy for adult services. AIDS Patient Care STDs 2009; 23: Sexually transmitted infections and young people in the United Kingdom: 2008 Report. In: Health Protection Agency Centre for Infections. July Moscicki AB, Ma Y, Holland C, Vermund SH. Cervical ectopy in adolescent girls with and without human immunodeficiency virus infection. J Infect Dis 2001; 183: Ferrand RA, Miller RF, Jungmann EA. 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