Clinical Science: Concise Communication
Nelfinavir and nevirapine side effects during pregnancy
Timmermans, Saraha; Tempelman, Clairea; Godfried, Mieke Hc; Nellen, Jeaninec; Dieleman, Jeanneb; Sprenger, Hermane; Schneider, Margriet EEf; de Wolf, Frankg; Boer, Keesd; van der Ende, Marchina Ea; for the Dutch HMF Study Group
From the aDepartment of Internal Medicine
bDepartment of Medical Informatics, Erasmus Medical Centre Rotterdam
cDepartment of Internal Medicine
dDepartment of Gynaecology, Academic Medical Centre University of Amsterdam, Amsterdam
eDepartment of Internal Medicine, Academical Hospital Groningen
fDepartment of Internal Medicine, Utrecht Medical Centre
gDutch HIV monitoring foundation.
Received 15 September, 2004
Revised 20 December, 2004
Accepted 5 January, 2005
Correspondence to M.E. van der Ende, Department of Internal Medicine, Erasmus MC, Dr Molewaterplein 40, 3015GD Rotterdam. E-mail: firstname.lastname@example.org
Background: The risk of vertical transmission of HIV has been substantially reduced since the introduction of highly active antiretroviral therapy (HAART); however, the impact of taking HAART during pregnancy on the woman, the fetus and the infant is not yet understood.
Objective: To assess and compare tolerability, safety and efficacy of nelfinavir- or nevirapine-containing HAART in a cohort of pregnant and non-pregnant HIV-infected women in the Netherlands.
Design: Retrospective comparative study.
Methods: In 15 centres specializing in HIV in the Netherlands, data on patient characteristics, HAART, adverse events, viral load response, mode of delivery and HIV status of the neonate were obtained from medical records of HIV-infected pregnant women who received HAART during pregnancy between January 1997 and June 2003. These data were compared with a control group of HIV-infected non-pregnant women that was obtained from the Dutch HIV-monitoring foundation database.
Results: Data from 186 pregnant and 186 non-pregnant HIV-infected women using a nelfinavir- or nevirapine-containing regimen were analysed. The pregnant women were younger, used a nelfinavir containing regimen more often, had higher CD4 cell counts and lower HIV RNA levels. Nelfinavir-related gastrointestinal symptoms (P < 0.001), hyperglycaemia (P < 0.001) and nevirapine-related hepatotoxicity (P = 0.003) occurred more often during pregnancy. The risk of nevirapine-induced rash was not increased. No major adverse events occurred.
Conclusion: Nelfinavir- or nevirapine-containing HAART regimens during pregnancy are well tolerated. Side effects of antiretroviral therapy are more frequent in pregnant than in non-pregnant women.
Vertical transmission accounts for the vast majority of paediatric HIV infections worldwide . The risk of mother-to-child transmission, without interventions, is 15–40% and is associated with high plasma HIV RNA levels in the mother [2,3]. This risk of vertical transmission is markedly reduced by administering antiretroviral therapy to reduce maternal HIV RNA levels.
During pregnancy, physiological changes may affect the pharmacokinetics of antiretroviral treatment. A recent report showed decreased nelfinavir (NFV) plasma levels in pregnant women compared with non-pregnant women . As a consequence, pregnant women may be more susceptible to viral failure. Furthermore, pregnancy may increase the risk of side effects of antiretroviral therapy, such as vomiting, hepatitis or hyperglycaemia, resulting in increased toxicity or decreased adherence. To investigate this, efficacy, tolerability and safety of antiretroviral regimens were compared in pregnant and non-pregnant women.
This was a retrospective cohort study at Dutch reference centres for HIV/AIDS between 1996 and 2003.
The study group consisted of all treatment-naive HIV-1-infected pregnant women who were treated predominantly with regimens containing nevirapine (NVP) or NFV during pregnancy and delivered at > 20 weeks of gestation. If a woman had multiple pregnancies while using highly active antiretroviral therapy (HAART), only data from her first pregnancy while on therapy were used. Patients were followed from the start of HAART until delivery. Pregnant women were identified from hospital listings in 15 Dutch reference centres for HIV/AIDS.
The comparison group consisted of treatment-naive HIV-1-infected non-pregnant women < 45 years of age, who first received HAART containing NVP or NFV during the same period of time (1997–2003). This group was followed for a period of 6 months from the start of first HAART, which was the average follow-up time in pregnant women. Non-pregnant women were identified from the database of the Dutch HIV-monitoring Foundation (HMF). The HMF is recognized by the Ministry of Health as the executive organization for the monitoring of HIV in the Netherlands. All Dutch HIV-treatment centres are obliged to collect data on HIV-infected patients and to submit these data to the HMF . The HMF Advisory Board approved the study.
For both groups, information was collected on patient characteristics (age, transmission risk group, country of birth and ethnicity). Furthermore, data were collected on antiretroviral treatment history, duration and composition of the regimen and the occurrence of adverse clinical events leading to a treatment switch or biochemical events during HAART. CD4 cell counts and plasma HIV-1 RNA levels were collected according to standard hospital protocols, which is at intervals of 3 to 6 months. Baseline values were obtained from a period of 0–6 months prior to initiation of HAART. Finally, data were collected on the duration of pregnancy, mode of delivery, complications during delivery and the HIV status of the newborn in the pregnant women group. Prematurity was defined as the birth of an infant before 37.0 weeks of gestation and low birth weight was defined as < 2500 g.
The treatment outcomes were defined as tolerability, indicated by clinical events leading to a treatment switch; safety, indicated by liver toxicity and glucose intolerance; and efficacy, indicated by virological response (HIV RNA < 500 copies/ml). Hepatotoxicity was defined aspartate aminotransferase or alanine aminotransferase ≥ 3× upper limit of normal. Glucose intolerance was defined as a random blood glucose ≥ 7.8 mmol/l . Paediatric HIV infection was diagnosed if HIV RNA values were positive at a minimal age of 6 months.
Pearson chi-square for categorical variables tested the differences in characteristics between pregnant and non-pregnant HIV-1-infected women. Differences in risk of treatment intolerance, liver toxicity or glucose intolerance, and in treatment efficacy, were analysed by means of univariate and multivariate logistic regression analysis. All factors associated with the outcomes at a P value of 0.1 were included in the multivariate analysis. Analyses were carried out with SPSS version 10.1 (Systat, Chicago, Illinois, USA).
From January 1997 to June 2003, 267 HIV-positive pregnant women from 15 reference centres for HIV and AIDS had been identified, of whom 186 were eligible for the study. The remaining 81 women did not meet the inclusion criteria because they were already on therapy while becoming pregnant (n = 66), the moment of start of HAART was unknown (n = 2) or because they used antiretroviral regimens not containing NVP or NFV (n = 13). From the HMF database, 186 non-pregnant women were identified, of whom 95 started a regimen containing NVP and 91 one containing NFV.
Baseline characteristics of both groups of women are shown in Table 1. Pregnant women were younger, used a NFV-containing regimen more often and had higher CD4 cell counts and lower HIV RNA levels before the start of HAART. There were no statistically significant differences in baseline characteristics between NVP-treated and NFV-treated women in both the pregnant and non-pregnant group.
In general, pregnancy was associated with more side effects of HAART (Table 2). In pregnant women, NVP use was associated with significant more hepatotoxicity (P = 0.003); 11% of the pregnant women were positive for hepatitis C and/or hepatitis B surface antigen; there were equal rates in both treatment groups. NFV use was associated with more gastrointestinal complaints (P < 0.001). Hyperglycaemia occurred more often in pregnant than in non-pregnant women of the same treatment group: 15.6% and 8.6% of the pregnant women using NFV and NVP, respectively, had glucose levels > 7.8 mmol/l. (P = 0.019 and 0.001). Rash occurred equally in pregnant and non-pregnant women. Seven of the eleven pregnant women taking NVP with hepatotoxicity had to discontinue NVP, one of them was positive for the hepatitis B surface antigen. In the other four women, the liver enzyme elevations resolved spontaneously and they could continue NVP. In the NFV group, six pregnant women switched from NFV because of gastrointestinal side effects, compared with one in the non-pregnant group.
There was a difference in treatment response. Before delivery, or after an average follow-up of 6 months in the control group, HIV RNA viral load was undetectable in 153 pregnant women (82.3%) and 130 non-pregnant women (69.9%) (P = 0.0095). There were 23 premature deliveries (12.8%), which were equally distributed across the NVP and NFV groups (13.8% and 11.7%, respectively; P = 0.652). There was also no difference in the average birth weight (3063 and 3094 g, respectively) or in the rate of low birth weight (8.6% and 13.3%, respectively; P = 0.412) between these two groups.
Two infants became HIV-infected. The first HIV-seropositive male infant was born at 39 weeks of gestation and had a birth weight of 3750 g. The mother had been taking a regimen of lamivudine 150 mg/zidovudine 300 mg (Combivir) with NFV for 4 weeks from 35 weeks of gestation. She did not experience any side effects nor did she switch regimen. At the time of delivery, her viral load was 29 400 copies/ml and her CD4 cell count was 297 × 106 cells/l. The infant was delivered through an elective caesarean section. The second HIV-infected infant was a boy born at 37 weeks of gestation with a birth weight of 1940 g. The mother took the same regimen (lamivudine/zidovudine/NFV) from 24 weeks of gestation. She did not experience any side effects nor did she switch the regimen. Her viral load during delivery was < 50 copies/ml. The infant was delivered through secondary caesarean section because of prolonged rupture of membranes (9 h).
In both infants zidovudine and lamivudine were administrated according to the Dutch guidelines as postexposure prophylaxis after birth .
In this study safety, tolerability and efficacy of HAART was compared in 327 HIV-1-infected pregnant and non-pregnant women. In general, HAART was well tolerated in the pregnant women, although the rate of manageable side effects was higher than in the non-pregnant women.
Use of an NFV-containing regimen resulted more frequently in gastrointestinal disturbances, such as nausea and usually mild diarrhoea, among the pregnant women. The high rate of gastrointestinal symptoms was reflected in a higher rate of therapy switches in the pregnant women because of gastrointestinal side effects. These were probably not a consequence of high NFV plasma levels, as plasma levels have been shown to be lower in pregnant than in non-pregnant women .
NVP-associated rash is frequently reported, with an overall occurrence of 14–22% [8–10]. Several risk factors for NVP rash have been suggested in previous studies, such as age < 35 years, CD4 cell count > 200 × 106 cells/l, higher baseline HIV-1 RNA level, female sex and higher NVP plasma concentration [11–13]. In our study, we found no difference in the occurrence of rash between the pregnant and non-pregnant women taking NVP (10.5% versus 8.6%). Because the pregnant women in our study were, on average, younger (27 years) and had higher CD4 cell counts, we would have expected a higher incidence of rash. Pharmacokinetic changes or possibly lower baseline HIV RNA levels may have made the pregnant women less susceptible to the development of rash.
Another matter of concern in NVP users is hepatotoxicity. In other reported cohort studies, percentages varied between 8% and 10% after an average follow-up time of 8 months and even increased to 37% in patients coinfected with hepatitis C [14–16]. In our study, 19% (n = 11) of the 58 NVP-using pregnant women developed hepatitis, compared with 4.2% of the non-pregnant women using NVP. The more frequent occurrence of hepatotoxicity in the pregnant women is in agreement with previously published studies and is possibly associated with a higher CD4 cell count at entry . The mean baseline CD4 cell count in pregnant and non-pregnant women with hepatotoxicity was 307 × 106 cells/l (range, 90–710) and 130 × 106 cells/l (range, 10–370), respectively.
Gestational diabetes complicates 2–3% of pregnancies . Hyperglycaemia may also occur as a consequence of treatment with HIV protease inhibitors through decreased insulin sensitivity, which develops within 8 weeks after starting the drug [18–20]. A recent study showed an increased risk of diabetes or glucose intolerance among pregnant women taking protease inhibitor drugs . In our study, hyperglycaemia occurred more often in pregnant women: 8.6% in the NVP and 15.6% in the NFV group. The risk of hyperglycaemia in the NFV group was twice the risk in the NVP group (odds ratio, 1.96; 95% confidence interval, 0.70–5.52); however, the numbers were too small to demonstrate an attributive effect of NFV on hyperglycaemia.
The response rate to HAART in the pregnant women was comparable to the results in non-pregnant women (82% versus 70%). There is some debate about the increased risk of premature delivery associated with protease inhibitor use [22,23]. We found prematurity rates of 13.8% in the NVP group and 11.7% in the NFV group. The number of children born with low birth weight did not differ between the two groups.
HAART is well tolerated in pregnancy. The risk of NFV-induced diarrhoea and NVP-induced hepatotoxicity seems to be increased, but not the risk of NVP-induced rash. The rate of development of hyperglycaemia during pregnancy was high but did not differ between the NVP and the NFV groups. In the Netherlands, NVF-containing regimens during pregnancy are recommended (as in most industrialized countries). NVP-containing HAART during pregnancy is an alternative but can only be recommended in countries where careful monitoring of hepatotoxicity is possible. Prolonged treatment during pregnancy with NVP in resource-poor settings with less-intense monitoring must be discouraged. The risk of vertical transmission is reduced to < 1% and the regimens did not increase the risk of preterm birth.
Sponsorship: This study was supported by the National Health Insurance Council (97–46486) Amstelveen, The Netherlands.
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Members of the the Dutch HMF Project participating in the mother-to-child transmission study: A. J. Schneider (Erasmus MC Rotterdam), R. H. Kauffmann (ZH Leyenburg Den Haag), R. Vriesenkoop (Medisch Centrum Haaglanden Den Haag), J. R. Juttmann (St Elizabeth Ziekenhuis Tilburg), F. P. Kroon (Leiden Universitair Medisch Centrum), G. Schreij (Academisch Ziekenhuis Maastricht), P. P. Koopmans (UMC St Radboud Nijmegen), C. Richter (ZH Rijnstate Arnhem), C. H. H. Ten Napel (Medisch Spectrum Twente Enschede), K. Brinkman (Onze Lieve Vrouwe Gasthuis Amsterdam), W. L. Blok (ZH Walcheren Vlissingen).
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