Diagnosed HIV-positive women accessing HIV clinical care in the UK include women of different ethnicities, ages and levels of morbidity. The characteristics of this diverse group continue to change with an increasing proportion of older women and women on antiretroviral therapy (ART) [1,2]. With advances in ART and prescribing practice [3–5] leading to improved wellbeing and longevity [6,7], coupled with effective prevention of mother-to-child-transmission (PMTCT) , many HIV-positive women choose to have children [9,10] and an increasing number have repeat pregnancies [11,12].
Changes in the characteristics and clinical features of pregnant HIV-positive women are likely to reflect changes among women accessing HIV clinical care, as well as changes in the pregnancy rate among specific groups. An increase or decrease in pregnancy incidence among subgroups could have implications for the planning of antenatal and HIV services. Pregnancy status is not currently reported as part of national surveillance of adults attending HIV clinical care  and, although antenatal studies of HIV-positive women can inform us about the characteristics of HIV-positive pregnant women, neither can be used to assess changes in pregnancy incidence.
Using data from two studies linked at the person level, a cohort study of adults accessing HIV care and a national surveillance study of HIV-positive pregnant women, our aim was to identify factors predictive of having a pregnancy among women accessing HIV care at 13 large UK clinics and to describe trends in the pregnancy rate in 2000–2009.
Creating a combined dataset
Data were obtained from two studies, the UK Collaborative HIV Cohort (UK CHIC) study and the National Study of HIV in Pregnancy and Childhood (NSHPC). The UK CHIC study annually collates data on HIV-related clinical care from (currently) 13 large HIV clinics, but does not record pregnancy-related data . It represents approximately 30% of women aged 16–49 years who accessed HIV care in the UK in 2000–2009. The NSHPC collates pregnancy data on HIV-positive women accessing antenatal care from all maternity units in the UK and Ireland using active surveillance. The records of women found in both these pseudonymized datasets were merged to create a dataset containing routine clinical and antenatal data for women with a pregnancy in 1996–2009 who were HIV-diagnosed before or during pregnancy (n = 2054). The methods used to link datasets has been described elsewhere [13–15] and further information on each study is available from http://www.nshpc.ucl.ac.uk and http://www.ukchic.org.uk. In brief, as neither study collects unique patient identifiers, UK CHIC records were first linked to NSHPC records using date of birth (DOB) to create a temporary dataset containing all pairs of records with identical DOB. These pairs were then assessed using fields, including CD4 cell count, HIV diagnosis date and clinic, to identify which pairs were likely to be genuine matches, that is relating to the same woman. A dataset was then created containing records for all women who accessed HIV care at a UK CHIC site in 2000–2009, incorporating antenatal data (from NSHPC) for those with a pregnancy. The dataset contained one row per woman per year and only included data for years when women accessed care at a UK CHIC site and were of childbearing age (16–49 years).
Variables and definitions
Index pregnancy refers to the first pregnancy after HIV diagnosis in the UK or the pregnancy during which HIV diagnosis occurred. Repeat pregnancy refers to any subsequent pregnancy (even if it was their first in 2000–2009). As pregnancies could overlap two calendar years, year of pregnancy refers throughout to the year of conception. Estimated date of conception was calculated as 266 days before expected date-of-delivery.
Variables in the dataset included ethnicity, exposure group, age and ART status at start of year, earliest CD4 cell count in the year (determined using UK CHIC data) and whether they became pregnant. For women with a pregnancy, data were also included on the estimated date of conception, pregnancy outcome and whether the pregnancy was an index or repeat pregnancy.
Pregnancies resulting in a live or stillbirth were categorized as ending at delivery and pregnancies resulting in miscarriage or termination, and ectopic pregnancies were categorized as ending early. Wherein pregnancy outcome was not known (n = 23), the pregnancy was excluded from the analysis of factors predictive of pregnancy outcome.
Analyses were carried out using SAS version 9.1 (SAS Institute Inc., Cary, North Carolina, USA). The characteristics of women under follow-up and with a pregnancy in each year were first described. Trends seen in the characteristics of pregnant women are likely to reflect changes in the characteristics of women accessing HIV care, and do not necessarily reflect the impact of any particular characteristic on the rate of pregnancy itself. Thus, the pregnancy rate was described for each calendar year using women (aged 16–49 years) with clinical data in UK CHIC as the denominator and women conceiving (all pregnancy outcomes) as the numerator. If a woman was HIV diagnosed during her index pregnancy and attended HIV care for the first time during that calendar year (463 pregnancies), the attendance and pregnancy for that year were excluded (i.e. removed from the numerator and denominator for that year). However, all future years during which the woman attended care (and any subsequent pregnancies) were included. If a woman had multiple pregnancies starting in the same calendar year, only the first was considered. Trends in index pregnancies were assessed by excluding data for all years following the year of index pregnancy.
Predictors of pregnancy were identified using generalized estimating equations (Poisson regression), unadjusted and adjusted for year, age, CD4 cell count, ethnicity and ART use, accounting for repeat measures. The addition of interaction terms between calendar year and each covariate in the model were also considered in order to investigate whether calendar year trends varied in some subgroups.
Factors associated with pregnancy ending in delivery versus ending early were also assessed using generalized estimating equations. Factors considered were age, HIV exposure group, ethnicity, calendar year, ART use and CD4 cell count.
Characterizing women accessing HIV care
In total, 7853 women aged 16–49 years accessed HIV care at UK CHIC sites in 2000–2009, the number doubling from 4555 in 2000/2001 to 9942 in 2008/2009. The majority were of black African ethnicity and most were infected via heterosexual sex (Table 1). During 2000–2009, the characteristics of women accessing care changed somewhat; the proportion of women of black African, black Caribbean or black other ethnicity increased, whereas the proportion of white women decreased. The proportion that had been infected via heterosexual sex or via MTCT increased and the proportion infected via IDU or contaminated blood/blood products decreased. The average age of women increased with the number aged 36–49 years almost quadrupling (Table 1).
Age varied by ethnicity; compared with black African women, women of black Caribbean, black other or ‘other’ ethnicities were more likely to be aged 16–25 years, whereas white women were less likely to be in this age group (P < 0.001) (data not shown). The proportion of women born in the UK varied by ethnicity (white, 64.3%, 594 of 924; black African, 7.3%, 231 of 2284; black Caribbean, 38.3%, 88 of 230, wherein country-of-birth was reported).
Pregnancies among women accessing HIV care
There were 1637 pregnancies among 1291 women who accessed HIV care during the period 2000–2009: 1000 (77.5%) women had a single pregnancy, 245 (19.0%) had two and 46 (3.6%) had three or more. The number of pregnancies rose, from 156 in 2000/2001 to 450 in 2008/2009. The characteristics of pregnant women under follow-up are presented in Table 2.
Over time there was an increase in the age of pregnant women, with a rise in the proportion over 35 years and a decrease in the proportion aged 26–35 years. The proportion of pregnancies which were repeat pregnancies increased from 30.1% (47 of 156) in 2000/2001 to 52.2% (235 of 450) in 2008/2009 (P < 0.001), with 735 (44.9%) overall. This rise in the proportion of repeat pregnancies was seen in all age groups [16–25 years, 25.0% (four of 16) in 2000/2001 to 46.4% (32 of 69) in 2008/2009, P < 0.001; 26–35 years, 33.0% (37 of 112) to 51.3% (139 of 271), P < 0.001; and 36–49 years, 21.4% (six of 28) to 58.2% (64 of 110), P < 0.001].
There was an increase in the proportion of pregnant women on ART (at the start of the year they conceived) (P < 0.001). In line with this, among pregnant women, the median CD4 cell count (at start of year) gradually increased over time and the proportion with CD4 cell count less than 350 cells/μl decreased (P < 0.001). The proportion of pregnancies among women of black African or black Caribbean ethnicity increased (P < 0.001) and that among white women decreased (P < 0.001) (Table 2). Most pregnancies were among women infected via heterosexual sex (97.0%, 1432 of 1477, in which exposure group was reported), with 1.9% (n = 28) among women infected via IDU, 0.7% (n = 11) among women infected via MTCT and 0.4% (n = 6) among women infected via other routes.
Pregnancy incidence and predictors of pregnancy
Pregnancy incidence was 3.4% [156 of 4555, 95% confidence interval (CI) 2.9–4.0] in 2000/2001 and 4.5% (450 of 9942, 95% CI 4.1–4.9) in 2008/2009 (Table 2). The highest incidence was in 2006 (4.8%, 216 of 4528, 95% CI 4.1–5.4). The likelihood that women had a pregnancy increased over the study period [relative rate per later year 1.03 (95% CI 1.01–1.05), P < 0.001], this was also the case after controlling for other factors [adjusted relative rate (aRR) 1.05 (95% CI 1.03–1.07), P < 0.001) (Table 3).
There were a number of independent predictors of pregnancy; older women were less likely to have a pregnancy than younger women [aRR 0.44 per 10 year increment in age (95% CI 0.41–0.46), P < 0.001) as were women with CD4 cell count less than 200 cells/μl compared with women with CD4 cell count 200–350 cells/μl [aRR 0.65 (95% CI 0.55–0.77), P < 0.001]. Women of white ethnicity were less likely to have a pregnancy than women of black African ethnicity [aRR 0.67 (95% CI 0.57–0.80), P < 0.001] as were women of black Caribbean ethnicity after controlling for age, ART use and CD4 cell count [aRR 0.75 (95% CI 0.58–0.97), P = 0.03]. Women infected via IDU were less likely to have a pregnancy than women infected via heterosexual sex [aRR 0.58 (95% CI 0.35–0.97), P = 0.04]. In unadjusted analyses, women on ART were less likely to have a pregnancy than women not on ART [relative rate 0.82 (95% CI 0.74–0.91), P < 0.001], but this was not the case after adjustment for other factors (Table 3).
The pregnancy rate increased for women in all age groups [16–25 years, aRR 1.07 per later calendar year (95% CI 1.02–1.12), P = 0.004; 26–35 years, aRR 1.06 (95% CI 1.04–1.09), P < 0.001; 36–49 years, aRR 1.05 (95% CI 1.00–1.09), P = 0.03] (Fig. 1). The rate of increase in pregnancy incidence was not significantly different for the three age groups (P-value for interaction = 0.15). Similarly, there was an increase in pregnancy rate for all CD4 groups with no evidence that the rate of increase was significantly different for any of these groups (P-value for interaction = 0.07). Pregnancy incidence increased among women of black African ethnicity [aRR 1.06 (95% CI 1.03–1.08), P < 0.001]. There was no evidence that the rate of change of pregnancy incidence differed for any ethnic group from that of women of black African ethnicity, apart from women categorized as ‘black other’, who experienced a somewhat slower increase in pregnancy rate (P = 0.02). As only a small proportion of women with a pregnancy were infected via routes other than heterosexual sex, it was not possible to assess trends in pregnancy rate for different exposure groups. The rate of increase in pregnancy incidence over this period did not significantly differ between women on ART and women not on ART (P-value for interaction = 0.14), with predictors of pregnancy being the same regardless of treatment.
The number of index pregnancies doubled from 109 in 2000/2001 to 215 in 2008/2009. The index pregnancy rate increased over the period 2000–2009 [aRR per later year 1.04 (95% CI 1.02–1.07), P = 0.001]. This increase was among women aged 26–35 years [aRR 1.06 (95% CI 1.03–2.00), P < 0.001], rather than among older women [aRR 1.02 (95% CI 0.96–1.18), P = 0.60] (P-value for interaction = 0.004), but the rate of increase did not significantly differ by ART group (P-value for interaction = 0.26), CD4 category (P-value for interaction = 0.15) or ethnicity (P-value for interaction = 0.31 for black Caribbean compared with black African women and P-value for interaction = 0.08 for white compared with black African women).
The majority of pregnancies resulted in a delivery (86.8%, 1421 of 1637; 1401 live births and 20 stillbirths) and 193 (11.8%) pregnancies ended early (126 miscarriages, 63 terminations and four ectopic pregnancies). Information on pregnancy outcome was unavailable for eight (0.5%) pregnancies, with a further 15 (0.9%) still ongoing at data submission. Among pregnant women, older women were less likely to have a pregnancy resulting in delivery [aRR 0.95 (95% CI 0.92–0.99), P = 0.02] and women infected via contaminated blood/blood products were more likely to have a pregnancy resulting in delivery than women infected via heterosexual sex [aRR 1.22 (95% CI 1.10–1.34), P = 0.001]. Neither ethnicity, ART use or CD4 cell count were predictive of pregnancy outcome. The proportion of pregnancies resulting in delivery increased over time [aRR 1.01 (95% CI 1.00–1.02), P = 0.05] and the proportion resulting in a termination decreased [from 12.8% (20 of 156) in 2000/2001 to 2.9% (13 of 450) in 2008/2009, P < 0.001].
We report an increase in pregnancy rate among HIV-positive women accessing HIV clinical care at 13 large clinics in the UK over the period 2000–2009. Although the characteristics of these women changed over this period, in line with elsewhere in Europe , the increased pregnancy rate remained after adjusting for these changes. There was no evidence that the overall pregnancy rate increased more among women on ART or among women of a particular age, ethnicity or CD4 category.
The increase in pregnancy rate was due to a rise in both repeat pregnancies, as has previously been reported from the UK and elsewhere [11,12], and index pregnancies. These changes are likely to reflect improvements in HIV treatment and management which have led to reduced morbidity [6,7] and MTCT rates [8,14]. Changes in pregnancy rates and attitudes toward childbearing following these improvements have previously been reported [10,17,18] and may also explain the reduction in terminations, also reported elsewhere . Although this could also be due to less unplanned pregnancies, thought to be high among this population , no data were available on pregnancy intention or use of contraception. It should be noted that the number of terminations in our study is likely to be an underestimation due to underreporting.
There were a number of characteristics predictive of having a pregnancy. Younger women were more likely to become pregnant than older women, as has been reported from HIV studies of pregnancy rate [17,20] and pregnancy intention [21,22]. Women infected via IDU were less likely to have a pregnancy than women infected via heterosexual sex. This is likely to reflect differences in health, lifestyle, desire for children  or menstrual changes associated with drug use , and has been reported elsewhere [22,24]. Women of black African ethnicity were more likely to have a pregnancy than women of white or black Caribbean ethnicity, as seen elsewhere [20,22], probably due to differences in attitudes to childbearing and family size. Differences in pregnancy rate between women of black African and black Caribbean ethnicity may reflect cultural differences or differences in the proportion that were UK-born.
Women with CD4 cell count less than 200 cells/μl were less likely to have a pregnancy than women with CD4 cell count 200–350 cells/μl, presumably because they had poorer health and were less likely to desire a pregnancy or conceive . As is the case elsewhere, an increasing proportion of women conceived while using ART [16,25]. ART use was not an independent predictor of pregnancy, although it has been found to be in some studies [17,26]. However, analyses that consider the impact of ART on pregnancy rate may suffer from the problems of time-varying confounding, and can be biased as a result.
In our study, the number of pregnancies increased from 156 in 2000/2001 to 450 in 2008/2009, due to an increase in the number of women accessing and remaining in care , and an increase in pregnancy incidence. Among all HIV-positive women in the UK and Ireland, including those diagnosed during pregnancy, the number of pregnancies stabilized in 2006 at around 1500 pregnancies per year , when pregnancy incidence in our study was highest (4.8%). This plateau may be due to the increasing number of older women accessing care, women who, in general, are less likely to become pregnant.
As the number of pregnancies has risen, so has the use of specialist antenatal services. All HIV-positive women who are pregnant or planning a pregnancy require a high level of clinical care. Many also require support relating to ART adherence, HIV disclosure and social/immigration issues . Demand for services is likely to increase further, particularly as an increasing number of older women have pregnancies (as is the case in the UK population ). Older women, particularly those over 40 years, are at increased risk of experiencing fertility problems  and pregnancy complications [30,31], some of which are also associated with antenatal ART use [16,32–35].
As well as implications for clinical services, the increase in pregnancy rate has implications for women and their children. Although MTCT in the UK is now rare among diagnosed women, with a transmission rate of 1.2% in 2000–2006 , an increasing number of infants are at risk of transmission and are exposed to ART drugs in utero, increasingly for the full duration of pregnancy. The long-term implications, particularly of exposure to newer ART drugs, are not fully understood and are difficult to monitor . For HIV-positive women, pregnancy has become increasing normal. However, questions remain regarding the direct and indirect effects of pregnancy and antenatal ART use on HIV progression and future treatment responses [37,38].
There were a number of limitations to the study. Some possible predictors of pregnancy, such as parity, were not available in UK CHIC, and as such were not assessed. Pregnancies during which HIV was diagnosed were not included in the analysis and factors predictive of pregnancy among women not aware of their HIV status may differ from those of diagnosed women. Also, the first CD4 cell count in the year and ART use at start of the year were used and these may have changed by the time the woman conceived. ART status did not take into account whether the woman was on ART for her own health or for PMTCT during an earlier pregnancy. Women whose pregnancies ended in termination or first trimester miscarriage may not have accessed antenatal care. As such, the proportion of pregnancies ending early is a minimum estimate and changes in the rate of miscarriages may have been undetectable due to small numbers.
As both datasets are pseudonymized, identifying women reported to UK CHIC and NSHPC relied on the use of demographic and clinical variables available from both studies. As a result, there is likely to be incomplete linkage between datasets and an underestimation of pregnancy incidence. However, this is unlikely to affect the predictors of pregnancy or trends over time. A higher proportion of women in the UK CHIC dataset accessed care in London than is the case nationally, although a direct comparison was not possible. Pregnant women accessing care in London may differ from those accessing care elsewhere, but pregnancy trends are likely to be similar.
An increase in pregnancies among women accessing HIV clinical care reflects increases in the pregnancy rate as well as increases in the number of women accessing care. HIV-positive women with or planning a pregnancy require a high level of clinical care and this is likely to continue, particularly as more older women have pregnancies.
S.E.H. undertook the statistical analysis with guidance from C.A.S. S.E.H. drafted the article with C.T., C.A.S. and P.A.T. All other authors contributed to the interpretation of results. All authors have read and approved the final manuscript.
The views expressed in this manuscript are those of the researchers and not necessarily those of the funders.
The UK Collaborative HIV Cohort (UK CHIC):
Steering Committee: Jonathan Ainsworth, J.A., Abdel Babiker, David Chadwick, Valerie Delpech, David Dunn, Martin Fisher, Brian Gazzard, Richard Gilson, Mark Gompels, Phillip Hay, T.H., Margaret Johnson, Stephen Kegg, Clifford Leen, Mark Nelson, Chloe Orkin, Adrian Palfreeman, Andrew Phillips, D.P., Frank Post, C.A.S. (Principal Investigator), Memory Sachikonye, Achim Schwenk and John Walsh.
Central Coordination: UCL Research Department of Infection and Population Health, London (T.H., S.E.H., Sophie Josie, Andrew Phillips, C.A.S., Alicia Thornton); Medical Research Council Clinical Trials Unit (MRC CTU), London (David Dunn, Adam Glabay).
Participating Centres: Barts and The London NHS Trust, London (C. Orkin, N. Garrett, J. Lynch, J. Hand, C. de Souza); Brighton and Sussex University Hospitals NHS Trust, London (M. Fisher, N. Perry, S. Tilbury, D. Churchill); Chelsea and Westminster Hospital NHS Trust, London (B. Gazzard, M. Nelson, M. Waxman, D. Asboe, S. Mandalia); Health Protection Agency – Centre for Infections, London (HPA) (V. Delpech); Homerton University Hospital NHS Trust, London (J.A., S. Munshi); King's College Hospital NHS Foundation Trust, London (H. Korat, J. Welch, M. Poulton, C. MacDonald, Z. Gleisner, L. Campbell); Mortimer Market Centre, London (R. Gilson, N. Brima, I. Williams); North Middlesex University Hospital NHS Trust, London (A. Schwenk, J. Ainsworth, C. Wood, S. Miller); Royal Free NHS Trust and UCL Medical School, London (M. Johnson, M. Youle, F. Lampe, C. Smith, H. Grabowska, C. Chaloner, D. Puradiredja); St Mary's Hospital, London (J. Walsh, J. Weber, F. Ramzan, N. Mackie, A. Winston); The Lothian University Hospitals NHS Trust, Edinburgh (C. Leen, A. Wilson); North Bristol NHS Trust (M. Gompels, S. Allan); University of Leicester NHS Trust (A. Palfreeman, A. Moore); South Tees Hospitals NHS Foundation Trust (D. Chadwick, K. Wakeman).
National Study of HIV in Pregnancy and Childhood (NSHPC): The authors gratefully acknowledge the contribution of the midwives, obstetricians, genitourinary physicians, paediatricians, clinical nurse specialists and all other colleagues who report to the NSHPC through the British Paediatric Surveillance Unit of the Royal College of Paediatrics and Child Health, and the obstetric reporting scheme run under the auspices of the Royal College of Obstetricians and Gynaecologists. The authors thank Janet Masters who coordinates the study and manages the data and Icina Shakes for administrative support.
Ethics approval for NSHPC was renewed following review by the London Multi-Centre Research Ethics Committee in 2004 (MREC/04/2/009).
UK CHIC is funded by the Medical Research Council (MRC), UK (grants G00001999 and G0600337). NSHPC receives core funding from the Health Protection Agency (grant number GHP/003/013/003). Data is collated at the UCL Institute of Child Health which receives a proportion of funding from the Department of Health's National Institute for Health Research Biomedical Research Centres funding scheme. S.E.H. has a UCL Studentship, funded by the MRC, for postgraduate work. C.T. holds a Wellcome Trust Research Career Development Fellowship.
Conflicts of interest
There are no conflicts of interest.
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