In Europe, many HIV infections have been diagnosed in immigrants from countries with generalized HIV epidemics [1,2]. Approximately 7000 new cases are diagnosed annually in France, of which 40% in women [1,3,4]. Half of these women emigrated from a sub-Saharan African country. Pregnancy is the most common reason for HIV diagnosis in sub-Saharan African women, whereas it is second, after clinical symptoms, among French-born women [3,5,6].
Strategies for prevention of mother-to-child transmission (MTCT) of HIV have resulted in a sharp decrease in the rate of MTCT, from 20% before 1994  to less than 2% in the highly active antiretroviral therapy (HAART) era in industrialized countries [8–13].
Optimal prevention of MTCT requires timely access to prenatal care and HIV management, as well as adherence to preventive measures. Universal voluntary HIV testing in the first trimester has been recommended in France since 1993 and national guidelines for HIV care and prevention of MTCT have been issued and regularly updated since 1997 . The migratory and socioeconomic context of many sub-Saharan Africans may be an obstacle to care and lead to delays in performing HIV screening and starting antiretroviral therapy (ART) . Among HIV-infected persons, as well as in the general population, immigrants have been shown to live in much more precarious conditions [3,5,16–18], which may limit access to adequate healthcare structures. In addition, some African women may find it difficult to accept measures such as elective caesarean section or breastfeeding for financial reasons, cultural barriers or risk of stigmatization in the family and social network. Moreover, clinicians may anticipate such difficulties by offering simplified, but less optimal, prevention strategies.
Our objective was to compare indicators of access to prevention of MTCT as well as the rate of transmission between sub-Saharan African and French mothers enrolled in the French Perinatal Cohort (EPF) since 1984.
Materials and methods
All human immunodeficiency virus type 1 (HIV-1)-infected women enrolled in the French Perinatal HIV cohort (EPF – ANRS CO1-CO11) were included in this study if they delivered in mainland France between 1984 and 2004.
EPF has prospectively collected data on HIV-infected pregnant women and their children in 96 centers throughout France since 1984. Informed consent was obtained from all mothers. Semestrial clinical and biologic examinations were collected since birth to 18 years for infected children and to 24 months for the others. No specific recommendations for obstetrical and HIV care was made, but investigators were encouraged to follow current French guidelines for prevention of MTCT . The cohort study was approved, according to French laws, by the Cochin Hospital Institutional Review Board and the French database watchdog commission (Commission Nationale de l'Informatique et des Libertés).
Geographical origin was categorized as French for mothers from mainland France, and African for women born in sub-Saharan Africa. We recorded age, intravenous drug use, date of HIV diagnosis, obstetrical characteristics, strategies used for prevention of MTCT (date of initiation, duration and type of prepartum, perpartum and neonatal ART, mode of delivery, breastfeeding), and maternal plasma HIV-1 RNA and CD4 cell counts closest to the delivery. An infant was considered as infected if HIV-1 was detected by virological tests done on sites on two separate samples as previously reported  or if anti-HIV-1 antibodies detected by enzyme-linked immunosorbent assay (ELISA) and western blot persisted after 18 months. An infant was considered as uninfected when tested negative on two separate samples, or, if serology was negative after 18 months.
Late access to MTCT prevention was defined as HIV diagnosis or booking at the maternity in the last gestational trimester (after 28 weeks). We defined five situations as substandard care which were clearly contrary to guidelines as early as 1994: no ART during pregnancy, starting ART after 32 weeks gestational age, no intrapartum prophylaxis (intravenous zidovudine or nevirapine), no neonatal prophylaxis and breastfeeding. Elective cesarean section was not recommended until 1997, recommended systematically from 1998 to 2002, and then recommended for women with detectable (>400 copies/ml) plasma viral load since 2002. Use of HAART was restricted to women requiring therapy for their own health from 1997 to 2000, was recommended as MTCT prevention for women whose viral load was over 10 000 copies/ml from 2000 to 2004, and for all women since mid-2004. Two attitudes remained contrary to the guidelines throughout all periods since 1997: zidovudine monotherapy when the viral load was higher than 10 000 copies/ml and vaginal delivery when the viral load was above 400 copies/ml or in case of zidovudine monotherapy. We also studied neonatal outcomes such as stillbirths, neonatal deaths, lack of HIV diagnosis and length of follow-up.
Changes in the proportion of women from sub-Saharan Africa among those enrolled in EPF over the 1984–2004 study period were estimated using the chi-squared test for trends. We then compared African and French mothers concerning demographic, medical and obstetrical characteristics, and substandard care. We excluded, from comparisons, the 1032 mothers from other countries, including French Caribbean or other Caribbean nations, Guyana, North Africa, Europe, or Asia. Comparisons were conducted overall and in each of four different periods, according to major changes in standards of ART: before 1994, between 1994 and 1996, 1997–2000, and from 2001 to 2004. As a quarter of mothers were enrolled in the cohort at least twice for successive pregnancies (mean number of 2.1 births per woman), we considered only the last pregnancy globally, and for each period.
Percentages were estimated with 95% confidence intervals (CI), and medians with interquartile range. We used the chi-squared test or two-sided Fisher exact test to compare percentages, and Student t test or Wilcoxon test to compare means of continuous variables.
A multivariate analysis was conducted for the HAART era, 1997–2004. Logistic regressions were performed for various dependent variables: late HIV diagnosis, late booking, substandard care as defined above, HAART use (vs. no HAART), and maternal viral load near delivery (less than 400 copies/ml vs. equal or higher), low CD4 cell count (less than 200 cells/μl). Adjusted odds ratios (aORs) associated with geographical origin (African vs. French) were then compared with crude ORs. Bivariate models were first performed to study specifically: the role of late access to diagnosis for the relation between geographical origin and late initiation of ART, the confounding role of year of delivery for the relation between geographical origin and HAART use, the role of late initiation of ART for the relation between geographical origin and virological success near delivery. The final models for each dependent variable were adjusted for parity, year of delivery and all potential confounding variables indicated in tables.
For the analysis concerning mother-to-child HIV transmission, we restricted the population to women receiving ART during pregnancy, who delivered between 1997 and 2004 and whose infant's HIV infection status was determined.
Statistical analyses were performed using SAS (version 9.1; SAS Institute Inc., Cary, North Carolina, USA) .
Overall, 7090 HIV-1-infected mothers, representing 9245 pregnancies delivering in mainland France were included: 3292 mothers came from sub-Saharan Africa, 2766 from mainland France, and 1032 mothers from other geographical areas. Between 1984 and 2004, the proportion of African pregnancies was 48.8% (4507/9245). It increased from 11.8% in 1984–1986 to 45.4% in 1996–1998 and 64.0% in 2002–2004, with a parallel trend in primiparas (Fig. 1). The main countries of origin were Cote d'Ivoire (30.9%), the Congos (28.5%), Cameroon (9.3%), Mali (7.2%), Senegal (3.3%), Central African Republic (2.5%), Angola (2.3%), Guinea (2.0%), Togo (2.0%) and Ghana (1.9%).
Compared with French mothers, Africans tended to be younger, more often multiparous (19.5 vs. 5.6%, respectively; P < 0.0001) and rarely were injecting drug users (0.1 vs. 5.1%, respectively; P < 0.0001). Gestational age at delivery was similar in both groups (median 38 weeks). Trends for maternal characteristics in both groups are presented in Table 1. Median follow-up and neonatal mortality were similar in African and French mothers.
Access to HIV screening and booking at obstetrical care center
There was a significant decrease over time in the proportion of women who started their pregnancy without knowing their HIV status, received HIV screening or booked at the maternity center in the third trimester, in African as well as French mothers (Table 1). However, these situations all remained more frequent in African than in French women. In the period 1997–2004, HIV infection was diagnosed in the third trimester in 6.8% of African women, vs. 1.2% of French women (P < 0.001) (Table 3). Late HIV diagnosis remained significantly associated with geographical origin after adjustment for period, maternal age, drug use and parity (OR = 7.1, 95% CI 4.2–12.0). Late booking occurred in 14.1% of Africans vs. 9.8% of the French (P < 0.001), but was 8.9% in both African and French mothers diagnosed with HIV before 28 gestational weeks. The association between late booking and geographical origin disappeared when adjusting for late HIV diagnosis.
Lack of antiretroviral therapy or late initiation during pregnancy
The proportion of women without ART during the pregnancy rapidly decreased from 15.6% in 1994–1996 to around 3.0% in the period 1997–2004 (Table 2). Between 1997 and 2004, the proportion was higher in African than in French women, especially in primiparas: 4.2 vs. 1.2%, P < 0.05. Among mothers who received ART, it was started after 32 gestational weeks in 7.6% of Africans vs. 4.1% of French women, P < 0.001 (Table 3).
Lack of ART was strongly associated with gestational age at HIV diagnosis and booking at the obstetrical center. During the period 1997–2004, the proportion of mothers who did not receive ART was 29.1% when HIV was diagnosed in the third trimester, 7.9% when it was diagnosed earlier but booking occurred in the third trimester, and 1% among women whose HIV diagnosis and booking took place in the first or second trimester. After adjustment in bivariate models (Table 3), African and French women did not differ for lack of ART (aOR 0.8, 95% CI 0.5–1.3) and for late initiation of ART (aOR 1.0, 95% CI 0.8–1.5). Adjustment for additional variables did not change the odds ratios.
Zidovudine monotherapy and vaginal delivery despite poor viral control
Among women whose last viral load before delivery was at least 10 000 copies/ml, the proportion receiving zidovudine monotherapy decreased from 20.6% in 1997 to 10% in 2004 (P < 0.001), with no difference between African and French women. This situation involved fewer than 2% of the study population. The proportion of mothers who delivered vaginally despite a viral load equal to or above 400 copies/ml was also similar in both groups (7.5%) (Table 3).
ORs adjusted for birth period, maternal age, parity, time at booking, time at ART initiation, and CD4 cell counts were similar to crude ORs, not significantly different from one.
Highly active antiretroviral therapy use and virologic success at delivery
The proportion of mothers who received HAART during pregnancy increased from 1.6% in 1997 to 74.1% in 2004 (P < 0.001). During this period, it was higher in African than in French women (52.8 vs. 43.9%, OR 1.4, 95% CI 1.3–1.6). This association was explained by the increase in enrollment of African mothers over time. Stratifying by each period of delivery, the proportion receiving HAART was similar in African and French women. The aOR declined to 1.0 (0.8–1.1), after adjustment for year of delivery. The proportion with an undetectable viral load (<400 copies/ml) was the same in African and French women (65.0 vs. 66.6%; aOR 0.9, 95% CI 0.7–1.0, P = 0.5). However, the CD4 cell counts at delivery were lower in African compared with French women, even after adjusting for gestational age at ART initiation and viral load at delivery (aOR 2.5, 95% CI 1.9–3.3, P < 0.001) (Table 3).
Perpartum and neonatal prophylaxis, breastfeeding and infant follow-up
African and French mothers did not differ according to lack of intrapartum zidovudine (5.8%), lack of neonatal prophylaxis (1.5%), nor for the proportion of breastfeeding (0.4%), both in univariate and multivariate analyses (Table 3).
Among mothers who received ART during pregnancy, the overall MTCT rate was 1.5% in the period 1997–2004. It was higher in African women 1.8% (43/2348) than in French women 0.8% (10/1232) (P = 0.016), with a crude OR of 2.3 (95% CI 1.1–4.6). The overall difference remained for mothers with CD4 cell counts above 350 cells/μl: 1.5 vs. 0.7%, crude OR 2.4 (95% CI 1.0–5.8); P = 0.06. The difference was no longer significant after adjusting for parity, maternal age, CD4 cell count, viral load, gestational age at delivery, antepartum, intrapartum and neonatal prophylaxis (OR 1.7; 95% CI 0.8–3.7, P = 0.17). There was no difference between African and French women among the 2110 mothers who had full-term deliveries (≥37 weeks) with a viral load less than 400 copies/ml (0.8 vs. 0.6%, respectively; P = 0.5).
The proportion of pregnancies in mothers from sub-Saharan Africa increased from 12% in 1984–1986 to 64% in 2003–2004 in the EPF cohort. We found that, in comparison with French-born mothers, immigrants from sub-Saharan African countries had more delayed access to HIV testing and care, whatever period was considered. The proportion of women who were unaware of their HIV status before becoming pregnant was higher in African than in French women. Moreover, among women who discovered their HIV status during the pregnancy, screening was done later in African mothers. Furthermore, after HIV diagnosis, the booking visit in the maternity occurred later in African than in French women. Late access to diagnosis or to care accounted for the higher rate of late initiation of ART during pregnancy in African than in French women. The relation between delays in screening and treatment initiation has also been reported in an American survey . A higher rate of late diagnosis has been observed in contexts other than pregnancy among immigrants in several European countries [2,3,5,21]. We could not study whether this was related to the time since arrival in France, as this date was not recorded.
Precarious housing, poverty and poor literacy are more frequent among HIV-infected immigrants than French natives [17,18,22]. We found that despite these obstacles, once women from sub-Saharan Africa accessed obstetrical care and HIV diagnosis, they benefited from the same prevention strategies as French women and were no more likely to be undertreated. Follow-up and care for children were similar in both groups. Contrary to widespread beliefs, and in contrast with practices in Africa, African women delivering in France did not have a lower rate of elective cesarean section than French women, and cases of breastfeeding were exceptional. We previously showed that geographic origin was not associated with lack of antiretroviral prophylaxis in the period 1996–1999 . Only one other report investigated the relationship between geographical origin and MTCT and found no association between race/ethnicity and use of antiretroviral prophylaxis or elective cesarean section when indicated . In nonpregnant patients, some European studies reported that access to ART following HIV diagnosis was equivalent in immigrant and natives [21,24].
Uncontrolled viral load is the major risk factor for MTCT [8,9,25–33]. In our study, African origin was not associated with a higher viral load at delivery during the period 1997–2004. This contrasts with findings from the United States where black or Hispanic mothers had higher viral loads at delivery than white mothers . The CD4 cell count at delivery was lower in African compared with French mothers in EPF, and the difference remained significant after adjustment for delay in starting ART and for viral load at delivery. Lower CD4 counts at diagnosis or treatment initiation in HIV-infected patients originating from Africa was found in several European cohorts [22,24,34–38]. The reason for the difference of CD4 level according to the geographical origin and its impact on virological response to treatment is unclear [22,34,38–40]. Although the overall MTCT rate was higher in African than French women enrolled in EPF, lower CD4 cell counts did not account for this difference, the transmission rate remained higher in African than in French mothers who delivered with more than 350 cells/μl. The association was no longer statistically significant, however, when adjusting for delay at starting ART, gestational age, plasma viral load and CD4 cell count at delivery. Moreover, the MTCT rate was under 2% in both treated populations in the 1997–2004 period, and did not differ between French and African women who term delivered with a viral load less than 400 copies/ml, as we reported previously . Thus, our findings do not support the hypothesis that genetic susceptibility or HIV subtypes, associated with geographical origin may play a major role in MTCT when the viral load at delivery is controlled. However, we cannot exclude that, among mothers with uncontrolled viral load, differences in viral resistances or subtypes, not collected routinely in the EPF cohort, may partly explain the higher transmission rate in mothers originating from sub-Saharan Africa.
Our results are encouraging as, once HIV diagnosis is made, MTCT prevention is similar in French and sub-Saharan Africa women delivering in France. Such results are likely owing to our universal free access to care for HIV infection and antenatal care, also offered to immigrants with nonregular status until recently. It thus appears important to maintain such access in a context of illegal immigration. Further efforts should be made to extend timely access to HIV screening and obstetrical care for all women, including recent immigrants.
C.J. realized the statistical analysis and contributed to conception, interpretation of data and drafting the article. L.M. and R.T. contributed to conception, design and drafting the paper. J.L.C. and J.-P.T. contributed to acquisition of data, analysis and interpretation. A.F., C.D., C.R. and S.B. contributed to conception, design and interpretation. J.W. is the principal investigator of the EPF and was responsible for the whole scientific process of this study. All authors revised the paper and approved the final version.
This study was supported by the French National Agency for AIDS Research (ANRS), Paris, France. We thank Valerie Benhammou, Karima Hamrene, Yassine Benmebarek, Aziz Diop, Nancy Zeller, Corinne Laurent, Elisa Ramos, Marlène Peres, Thierry Wack, Leila Boufassa, Paulette Huynh and Robert Murphy.
The following persons and institutions participated in the ANRS French Perinatal Cohort:
Hôpital d'Aix en Provence* (Tadrist B.); Hôpital Nord, Amiens (Schmit J.L., Horlé B.); Hôpital d'Angers (Fournié A.); Hôpital Victor Dupouy, Argenteuil (Brault D.); Hôpital Paris La Roseraie*, Aubervilliers (Rozan M.A.); Hôpital Robert Ballanger, Aulnay (Zakaria A.); Hôpital Saint Claude, Basse-Terre* (Sibille G.); Hôpital de Bastia (Pincemaille O.); Hôpital de la Côte Basque, Bayonne (Cayla C.); Clinique du Blanc Mesnil* (Balde P.); Hôpital Saint Jacques, Besançon (Estavoyer J.M.); Hôpital Avicenne, Bobigny (Bentata M.); Hôpital Jean Verdier, Bondy (Lachassine E., Rodrigues A.); Hôpital Pellegrin, Bordeaux (Roux D., Douard D.); Hôpital Ambroise Paré*, Boulogne Billancourt (Zenaty D.); Hôpital Clémenceau, Caen (Brouard J.); Hôpital André Rosemon, Cayenne (Elenga N.); Hôpital Beaujon*, Clichy (De Curtis A.); Hôpital de Creil (Kingue-Ekollo C.); Hôpital Intercommunal, Créteil (Garrait V., Lemerle S., Pichon C.); Hôpital Béclère, Clamart (Chambrin V., Labrune P., Clech L.); Hôpital Louis Mourier, Colombes (Crenn-Hebert C., Floch-Tudal C.); Hôpital de Compiègne* (Lagrue A.); Hôpital d'enfants, Dijon (Reynaud I.; Martha S.); Hôpital de Dourdan* (Ercoli V.); Hôpital de Dreux* (Denavit M.F.); Hôpital des Feugrais*, Elbeuf (Lahsinat K.); Hôpital Intercommunal, Evreux (Touré K.); Hôpital Francilien Sud, Evry-Corbeil (Devidas A., May A., Granier M.); Hôpital de Fontainebleau (Routier C.); Hôpital Victor Fouche, Fort de France (Hatchuel Y.); Hôpital de Gonesse* (Balde P.); Hôpital Jean Rostand, Ivry (Jault T.); Hôpital de Lagny (Chalvon Demersay A.); Hôpital du Lamentin* (Monlouis M.); Hôpital Les Oudairies, La Roche sur Yon (Perré P); Hôpital de La Seyne sur Mer (Chamouilli J.M.); Hôpital Louis Domergue, La Trinité* (Hugon N.); Hôpital André Mignot, Le Chesnay (Hentgen V., Messaoudi F.); Hôpital de Bicêtre, Le Kremlin-Bicêtre (Peretti D., Fridman S); Hôpital Jeanne de Flandres, Lille (Mazingue F., Hammou Y.); Hôpital Dupuytren*, Limoges (De Lumley L.); Hôpital de Longjumeau (Seaume H.); Hôpital Hôtel Dieu-Hôpital Debrousse, Lyon (Cotte L., Kebaïli K.); Hôpital François Quesnay, Mantes La Jolie (Doumet A.); Hôpital la Conception, Marseille (Cravello L., Thuret I.); Hôpital de Meaux (Karaoui L.); Hôpital de Meulan* (Seguy D.); Hôpital Marc Jacquet, Melun (Le Lorier B.); Hôpital Intercommunal, Montfermeil (Talon P.); Hôpital Arnaud de Villeneuve, Montpellier (Benos P., Lalande M.); Hôpital Intercommunal, Montreuil (Heller-Roussin B.); Maternité Régionale A. Pinard, Nancy (Hubert C.); Hôpital de Nanterre* (Karoubi P.); Hôpital de Nantes (Reliquet, V., Brunet-François C.); Hôpital de Neuilly sur Seine* (Berterottiere D.); Hôpital l'Archet-Fondation Lenval, Nice (Monpoux F., Bongain A., Deville A.); Hôpital Caremeau, Nîmes (Dendale J.); Hôpital Orléans (Arsac P.); Hôpital d'Orsay (De Gennes C.); Hôpital Bichat, Paris (Matheron S., Batallan A.); Hôpital Boucicaut*, Paris (Lafay Pillet M.C.); Hôpital Cochin-Port Royal, Paris (Firtion G., Pannier A); Hôpital Lariboisière, Paris (Ciraru-Vigneron N.); Hôpital des Métallurgistes*, Paris (Rami M.); Institut Mutualiste Montsouris*, Paris (Carlus Moncomble C.); Hôpital Necker, Paris (Parat S., Blanche S., Rouzioux C.); Hôpital Notre Dame du Bon Secours, Paris (Ayral D.); Hôpital Pitié Salpêtrière, Paris (Tubiana R.); Hôpital Robert Debré, Paris (Levine M., Faye A., Ottenwalter A.); Hôpital Rothschild, Paris (Wallet A.); Hôpital Saint-Antoine, Paris (Carbonne B.); Hôpital Hôpital Saint Michel, Paris (Aufrant C.); Hôpital Tenon, Paris (Lebrette M.G.); Hôpital Trousseau, Paris (Dollfus C.); Hôpital Marechal Joffre, Perpignan (Medus M.); Hôpital Les Abymes, Pointe-à-Pitre (Bataille H.); Hôpital de Poissy-Saint-Germain en Laye* (Rousset M.C.); Hôpital René Dubos, Pontoise (Mouchnino G.); Hôpital Américain, Reims (Munzer M.); Hôpital Charles Nicolle, Rouen (Brossard V.); Hôpital de Saint-Denis (Allemon M.C., Ekoukou D., Khuong M.A.); Hôpital Nord, Saint Etienne (Billiemaz K.); Hôpital de Saint Martin (Bissuel F.); Hôpital Esquirol*, Saint-Maurice (Robin M.); Hôpital de Sèvres* (Segard L.); Hôpital de Haute Pierre-Hôpital Civil, Strasbourg (Partisani M., Favreau, J. J, Entz-Werle N.); C.M.C. Foch, Suresnes* (Botto C.); Hôpital Chalucet,Toulon (Hittinger G.); Hôpital La Grave, Toulouse (Berrebi A., Tricoire J.); Hôpital Bretonneau, Tours (Besnier J.M.); Hôpital Brabois, Vandoeuvre les Nancy (Neimann L.); Hôpital Paul Brousse*,Villejuif (Dussaix E.); Hôpital de Villeneuve Saint Georges (Guillot F., Chacé A.).
* sites not active currently
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