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HIV TESTING, KNOWLEDGE, ATTITUDES,
     BELIEFS, AND PRACTICES AMONG
MINORrTIES: PREGNANT WOMEN OF NORTH-
AFRICAN ORIGIN IN SOUTHEASTERN FRANCE
            Antoine Messiah, MD, PhD, Dominique Rey, MD, Yolande Obadia, MD, Michel Rotily, MD,
                                         and Jean-Paul Moatfi, PhD
                                              Marseille, France


                       Since 1991, the French public health ministry has recommended that human immunod-
                  eficiency virus (HIV) testing be offered to all pregnant women. This study was undertaken to
                  determine whether this recommendation is followed independently of a woman's ethnicity. It
                  is based on a 1992 survey regarding knowledge, attitudes, beliefs, and practices on HIV
                  infection and testing among pregnant women in southeastern France.
                       Survey results revealed that North-African women (n=207) were more likely to have a
                  low socioeconomic and educational level, receive their health care at public health institu-
                  tions, and be less knowledgeable about HIV transmission than French women (n=2234).
                  They were also more likely to have been tested for HIV without their knowing it and less like-
                  ly to perceive themselves as being at risk. Consent to undergo HIV testing during pregnancy
                  was dependent on their North-African origin after controlling for significant covariates.
                       These results indicate that routine prenatal screening appears insufficient to ensure ade-
                  quate HIV testing and counseling of women of ethnic minorities. The development of HIV pre-
                  vention programs that are cultural-specific and that aim at increasing physicians' compliance
                  with the official recommendation is needed. (J Nati Med Assoc. 1 998;90:87-92.)


   Key words: * human immunodeficiency virus                            ate for general policies of human immunodeficiency
      (HIV) * HIV transmission * minorities                             virus (HIV) screening and counseling to reach all
                                                                        women.2 This is especially true in France, where the
   In France, as in most other industrialized countries,                public social insurance system guarantees universal
the proportion of women among the total number of                       health coverage for all pregnant women living in the
registered acquired immunodeficiency syndrome                           country. Since the early 1970s, a minimum of four
(AIDS) cases has increased steadily since the begin-                    free-of-charge prenatal care medical consultations
ning of the epidemic (from 13.9% in 1987 to 20.4% in                    (including testing for syphilis, rubella, and toxoplas-
1995.1 Prenatal care is viewed as especially appropri-                  mosis at the first visit) have been mandatory. It is wide-
                                                                        ly accepted that this legislation greatly contributed to
From the South-Eastern French Center for Disease Control and the        recent progress in prenatal care and prevention of pre-
Institut Paoli-Calmettes, Marseille, France. This study was supported   term births and children's handicaps.3
by the French Agency for Aids Research. Requests for reprints              In December 1991, the French Ministry of Health
should be addressed to Dr Antoine Messiah, INSERM U-379, Institut       issued an official recommendation that general practi-
Paoli Calmettes, 232 bd Sainte Marguerite, BP 156, 13273                tioners, gynecologists, and obstetricians systematically
Marseille Cedex 09, France.                                             offer, an HIV test to all pregnant women consulting

JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 90, NO. 2                                                                    87
HIV TESTING AMONG MINORITIES




                                                           foreigners; among them, 35% come from North
       Table 1. Sociodemographic Data and Conditions       Africa.6 Evidence from other countries strongly sug-
                of Pregnancy, by Ethnic Group              gests that HIV prevention programs have specific dif-
                          % North-                         ficulties in reaching women from ethnic minorities
                           African % French                and emphasizes the need for culturally adapted mes-
                          Women      Women                 sages and interventions.79 It is therefore important to
                           (n=207) (n=2234) P Value        know, if despite the official recommendation, there
     Age (years)                                           are differences in access to HIV testing and counsel-
       <25                    26          21               ing between members and nonmembers of these
       25 to 34               60          67    NS         minorities and to determine to which factors these dif-
        ,35                   14          12               ferences are related.
     Matrimonial status                                       A survey on HIV screening among pregnant
       Married                71          64               women conducted in southeastern France in 1992,
       Unmarried but living
         with a partner       13          28   <.001       the Prevagest survey,'0'11 included North-African and
       Living alone           16           7               French women. The survey examined sociodemo-
     Level of education                                    graphic characteristics, pregnancy conditions, HIV
       University graduate    15          52               testing experience, risk situation and risk perception,
       Secondcary school                                   and knowledge and beliefs about HIV transmission.
          graduate            44          37   <.001
       Lower level of                                      METHODS
          education           41          11               Population
     Occupational status                                      The Prevagest survey is described elsewhere.'0"'1 It
       Employed               27          70   <.00 1      consists of three subsurveys directed at pregnant
       Unemployed             73          30               women and the health-care institutions caring for
     Level of income
        ,6000 francs          58          14   <.001       them. The first subsurvey is an unlinked anonymous
       >6000 francs           42          86               HIV seroprevalence survey. The second subsurvey,
     Religion                                              which is analyzed in this article, is a survey on the
       None or not                                         knowledge, beliefs, attitudes, and practices of the
          practicing          30          64   <.001       women. Through the data collected by the third sub-
       Practicing             70          36               survey, directed at the institution, we could determine
     Prenatal care                                         whether the women were in a ward conducting sys-
      delivered by                                         tematic testing; the accuracy of this information was
       Private ambulatory                                  checked by direct observation at each site. In south-
         physicians           44          76   <.001       eastern France, 77 wards attend pregnant women for
       Public prenatal                                     delivery. Seventy-one wards agreed to participate in
          institutions        56          24
     No. of prenatal                                       the study during April 1992. A total of 3148 women
      consultations                                        were cared for during the study period; of these, 114
      <4                       2           1               (4%) neither spoke nor read French and 209 (7%)
      4                        6           1   <.001       refused to participate. The remaining 2825 women
      I,< 4                   92          98               included North Africans (n=207), French metropoli-
     Abbreviations: NS=not significant.                    tans (born in continental France) (n=2234), French
                                                           Caribbeans (n=37), Europeans (n=207), sub-Saharan
                                                           Africans (n=35), other (n=63), and unknown (n=42).
                                                           For the purpose of this article, the first two groups
for prenatal care, provided the women gave informed        were compared.
consent and could decline the offer. In this context,
screening appears as a universal policy, expected to be    Data Collection and Analysis
equal for everyone, but it assumes that preventive            A self-administered anonymous questionnaire was
counseling targeted at the general population is able to   proposed by a nurse to all the hospitalized women
reach all subgroups, including cultural minorities.4'5     within 3 days after childbirth. Topics included
   Of the entire population living in France, 6.3% are     detailed sociodemographic information, the woman's

88                                                         JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 90, NO. 2
HIV TESTING AMONG MINORITIES




experience with prenatal care and HIV testing during
her pregnancy, HIV-related individual risk behaviors                    Table 2. Risk Behavior and Individual Risk
and perception, and knowledge concerning horizon-                              Perception, by Ethnic Group
tal and vertical HIV transmission. For the institutions                          % North-
whose policy was systematic testing, a woman's                                    African     % French
answers to the question, "Were you offered an HIV               Risk           Women          Women
test here?" allowed us to determine whether she had             Behavior       (n=207)       (n=2234)        P Value
been tested with or without her knowledge.                      Multiple sexual partners in the past 2 years
    Univariate comparisons between ethnic groups                  Yes             5              7            NS
were performed with the chi-squared test (qualitative             No            95             93
data) and Student's t-test (quantitative data).'2 All sig-      Intravenous drug use (at least once)
nificant variables (P<.05) were introduced into a                Yes              1              1            NS
logistic regression model,'3 with a woman's declara-              No            99             99
                                                                HIV-positive sexual partner (at least once)
tion of having been tested (versus not) during her               Yes             0               0            NS
pregnancy as the dependent variable. The final                    No           100            100
model consisted of variables with P<.10. Calculations           Intravenous drug user sexual partner (at least once)
were done using SPSS software.                                   Yes             0               2            NS
                                                                  No           100             98
RESULTS                                                         Declared
Sociodemographic Data and Conditions of                          At least one of
Pregnancy                                                          the above 6                 8             NS
   Regarding age, North-African women were similar               None of
to French metropolitan women (Table 1). North-                     the above 94              92
African women were more likely to live alone, to be             Declared higher or average risk of being infected,
                                                                 in comparison with overall women's population
unemployed and less educated, to have a low                       Yes            7            20            <.001
income, to practice a religion, and to have their pre-            No           93            80
natal care delivered by public institutions. French
metropolitan women were more likely to have more                Abbreviations: NS=not significant and HIV=human
than four prenatal consultations.
                                                                immunodeficiency virus.

HIV Testing Experience, Risk Situation and Risk
Perception, Knowledge, and Beliefs About HIV                  tan women (P<.001) had had a routine HIV test with-
Transmission                                                  out their being aware of it because of a lack or inade-
   Declaration of prenatal HIV testing was signifi-           quacy of informed consent procedures. Thus, the
cantly lower among North-African women (42%)                  actual frequency of prenatal HIV testing was similar
than among French metropolitan women (65%;                    between North-African women (75%) and French
P<.001). Eighty-three percent of French metropolitan          metropolitan women (73%).
women declared that they had been tested at least                North-African women declared HIV-related risk
once for HIV, including the ones who had a test               behaviors as frequently as French metropolitan
before the pregnancy, versus 49% among North-                 women did (Table 2). However, they were less likely
African women (P<.001). Among the 907 women                   to perceive themselves at higher or average risk.
who said they had not been tested for HIV during                 Knowledge about the main routes of HIV trans-
pregnancy, only a few (3.3% of North-African women            mission was less accurate among North-African
and 1.3% of French metropolitan women) had                    women; the difference was larger for horizontal than
refused the test offered to them; this contrasts with         for vertical transmission (Table 3). North-African
68% of North-African women and 56% of French                  women more frequently believed in HIV transmis-
metropolitan women to whom the test had not been              sion through casual contact and mosquito bite.
proposed (P<.001). When the women's statements
and those of the medical ward attending them were             Multivariate Analysis
pooled, it appeared that an additional 33% of North-             To determine how differences in HIV testing dur-
African women versus only 8% of French metropoli-             ing pregnancy were correlated with the variables dif-

JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 90, NO. 2                                                            89
HIV TESTING AMONG MINORITIES




              Table 3. Knowledge and Beliefs About HIV Horizontal and Vertical Transmissions, by Ethnic Group

     Knowledge                                          % North-African               % French
     & Beliefs                                          Women (n=207)              Women (n=2234)               P Value
     Horizontal Transmission
     Correct answers to 'People can get AIDS from'*
       Sexual intercourse (yes)                                73                          95                   <.001
       Intravenous drug use (yes)                              73                          91                   <.001
       Receiving blood (yes)                                   68                          88                   <.001
       Donating blood (no)                                     31                          55                   <.001
       Being admitted in the same hospital ward as
         a person with AIDS (no)                               44                         72                    <.001
       Using public lavatories (no)                            32                         60                    <.001
       Drinking in a glass used by a person with AIDS (no)     41                         65                    <.001
      A mosquito bite (no)                                     33                         57                    <.001
       Knowledge scoret                                       m=4.3                      m=5.9                  <.001
                                                             SD=2.2                     SD=1.7
     Vertical Transmission
     Correct answers to "HIV can be transmitted
        from an infected mother to her baby"*
       During pregnancy (yes)                               69                      90                  <.001
       During delivery (yes)                                19                      37                  <.001
       Through breast-feeding (yes)                         32                      39                   NS
       By taking care of the child after birth (no)         37                      68                  <.001
       Knowledge scoret                                   m=1.7                   m=2.4                 <.001
                                                         SD=1.1                  SD=1.0
     Abbreviations: HIV=human immunodeficiency virus, AIDS=acquired immunodeficiency virus, SD=standard deviation,
     and NS=not significant.
     *The correct answer is given in parentheses.
     tThe score (minimum=0, maximum=8) was built by counting each correct answer as 1 and summing them.
     $The score (minimum=0, maximum=4) was built by counting each correct answer as 1 and summing them.

ferentiating North-African women from French met-                   nant women delivering in southeastern France were
ropolitan women, logistic regression was performed                  surveyed during the study period, but not all could be
(Table 4). It showed a positive correlation between                 reached because the study protocol was restricted to
knowledge scores, risk perception, and the likeli-                  French-speaking women for practical reasons. It is
hood of being tested (with the woman's knowledge).                  likely, however, that if non-French speaking women
It also showed that those women who were married,                   had been included, differences between migrants and
had a low educational level, and low income level                   nonmigrants would have been even larger. Southern
were significantly less likely to be tested. Finally, it            France has historical links with North Africa and is
showed that even when these covariates were con-                    the focus for migration and travel to Europe; effec-
trolled for, being a North-African women was still                  tively, non-French women in our sample were pri-
significantly associated with a lower likelihood of                 marily from North Africa. Only small populations
being tested with informed consent.                                 come from other non-European countries, which pre-
                                                                    vented their inclusion in this analysis. The situation of
DISCUSSION                                                          these other minorities may be quite different, but in-
   This survey was the first in France to compare                   depth analysis would require surveys in French
access to HIV screening and counseling between                      regions where they are better represented.
migrant and metropolitan women. Most of the preg-                      The French public social insurance system guaran-

90                                                                  JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 90, NO. 2
HIV TESTING AMONG MINORITIES




   Table 4. Logistic Regression Analysis of Women's Declaration of Having Had an HIV Prenatal Test (Yes Versus No)*
                                                        OR                   95% Cl                    P Value
  Matrimonial status
    Married                                           0.59                  0.39-0.88                  .010
    Unmarried but living with a partner               0.83                  0.55-1.27                  .398
    Living alone*                                      1 .00
  Level of education
    University graduate*                               1.00
    Secondary school graduate                         0.59                  0.49-0.73                <.001
    Lower level of education                          0.53                  0.39-0.71                <.001
  Level of income
    <6000 francs                                      0.75                  0.57-1.00                  .050
    >6000 francs*                                     1.00
  Individual risk perception of being HIV infected
     when compared with average risk among women
    Higher or average risk                            1.25                 0.99-1.58                   .066
    Lower or no risk, or no evaluation*               1.00
  Knowledge scores (numeric variables)
    Of horizontal HIV transmissiont                                                                    .027
    Of vertical HIV transmissiont                                                                      .019
  Ethnic group
    North-African women                               0.61                 0.44-0.90                   .007
    French women*                                     1.00
  Abbreviations: OR=adjusted odds ratio and CI=95% confidence interval.
  *Category of reference.
  tOR=1.06 per point of score.
  tOR=1 .12 per point of score.


tees universal coverage for all pregnant women living         HIV transmission through casual contact and mos-
in the country, and the legislation recommends that           quito bite, as found in other ethnic minorities.8'9 Such
all pregnant women be offered HIV screening, pro-             cultural beliefs create specific challenges for HIV pre-
vided they give informed consent. Screening policy            vention.'4"5 In addition, married women were less
therefore is expected to be equal for everyone. Our           likely to have been tested for HIV, contrasting with
survey shows that if all HIV tests taken with or with-        unmarried women living with their partner. This sug-
out the woman's knowledge are considered, the fre-            gests that marriage restrains women of ethnic minori-
quency of prenatal HIV testing is similar between             ties from being tested. Until now, North Africa was
groups independently of ethnic origin. However, the           relatively unaffected by the epidemic; most HIV-
survey also shows that equality is not achieved in            positive women were infected by their husbands.'6
practice. It reveals a dramatic difference in applica-        In France, only 3% of cumulated AIDS patients in
tion of the testing policy: North-African women were          1993 were born in North Africa." It often is argued
more frequently tested without their knowledge and            that the traditional cultural norms of North-African
less likely to have been proposed a test by the physi-        women have a protective effect against HIV infec-
cian, suggesting a lack of adequate preventive coun-          tion.18 Some of the HIV-related beliefs of these
seling associated with testing for these women. This is       women are closely linked to the Islamic religion, eg,
especially unfortunate because, as the survey shows,          risk of vertical contamination through breast-feed-
North-African women lack knowledge about AIDS                 ing and, more generally, risk of transmission
transmission and are less likely to feel at risk although     through contact with body fluids.
they declared at risk behaviors as frequently as                 Numerous aspects differentiating North-African
French women did.                                             women from French women, including lower
    North-African women more frequently believed in           socioeconomic and educational levels, could

JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 90, NO. 2                                                           91
HIV TESTING AMONG MINORITIES




explain the lesser tendency of North-African women                    Naitre en France, dix ans d'ivolution. Paris, France: Doin-INSERM;
                                                                       1984.
of knowing that they had a test. Even when these                             4. Steffen M. France: social solidarity and scientific exper-
parameters were controlled for, being of North-                       tise. In: Kirp DL, Bayer R eds. AIDS in the Industrialized
African origin was still correlated with this tendency.               Democracies. Passions, Politics and Policies. New Brunswick, NJ:
This suggests that institutional factors might be at                  Rutgers University Press; 1992:221-251.
play with these women. Such factors include the                              5. MoattiJ, Dab W, Loundou A, Quenel P, Beltzer N, Ames
                                                                      A, et al. Impact on the general public of media campaigns against
wards' screening policy toward these women and                        AIDS: a French evaluation. Health Policy. 1992;21:233-247.
the physicians' perceptions of women's risk and                              6. Labat J. La Population Etrangere. Recensement de la
their ability to deal with HIV prevention. They can-                  Population de 1990. Paris, France: INSEE Premiere; 1991.
not be attributed to language barriers since women                            7. O'Leary A. Women at Risk: Issues in the Primary Prevention
who neither spoke nor understood French did not                       ofAIDS New York, NY: Plenum Press; 1995
                                                                             8. Peruga A, Rivo M. Racial differences in AIDS knowledge
participate in the study.                                             among adults. AIDS Educ Prev. 1992;4:52-60.
   Our survey strongly suggests that universal routine                       9. Nyamathi A, Bennett C, Leake B, Lewis C, FlaskerudJ.
prenatal HIV screening does not guarantee adequate                    AIDS-related knowledge, perceptions and behaviors among
counseling, especially for women of ethnic minorities.                impoverished minority women. AmJPublic Health. 1993;83:65-71.
Additional studies on ethnic minorities other than                         10. Obadia Y, Rey D, Moatti JP, Pradier C, Couturier E,
                                                                      Brossard Y, et al. HIV prenatal screening in South-Eastern
North-African women are necessary to confirm this                     France: differences in seroprevalences and screening policies by
in the French context.                                                pregnancy outcomes. AIDS Care. 1994;1:29-38.
   Zidovudine treatment of HIV-infected mothers,                           11. Rey D, Moatti J, Obadia Y, Rotily M, Dellamonica P,
which significantly reduces the risk of vertical trans-               GilletJ, et al. Differences in HIV testing, knowledge and attitudes
mission,19'20 creates more incentives for the develop-                in pregnant women who deliver and those who terminate:
                                                                      Prevagest 1992-France. AIDS Care. 1995;7:S39-S46.
ment of systematic HIV prenatal screening. It                              12. Armitage P, Berry G. Statistical Methods in Medical
underscores the need for culturally sensitive pro-                    Research. 2nd ed. Oxford, England: Blackwell Scientific
grams for the medical community for these women                       Publications; 1987.
to benefit from the recent therapeutic advances in                         13. Kleinbaum D, Kupper L, Morgenstern H. Epidemiologic
prevention of vertical transmission, without contra-                  research principles and quantitative methods. New York, NY:
                                                                      Van Nostrand Reinhold; 1982.
vening the ethical principle of patients' individual                       14. Ulin P. African women and AIDS: negotiating behavioral
freedom of choice. Additional prevention programs                     change. Soc Sci Med. 1992;34:63-73.
therefore are needed, with some targeted at ethnic                         15. Guerin A. Le modele culturel de la femme Africaine. Un
minorities and others targeted at physicians and                      entretien avec Francoise Heritier-Auge. Le Journal du Sida.
their institutions.                                                   1994;64-65:33-34.
                                                                           16. Maaroufi A, Chakib A, El Aouad R, Squalli M, Zahraoui
                                                                      M, Himmich H. Aspects Cliniques et Therapeutiques de l'infection 2
Acknowledgments                                                       VIH au Maroc. In: The Proceeding of the VIII International
   The authors thank Claire Julian-Reynier and Michel Morin           Conference on AIDS in Africa, Marrakech 1993. Abstract.
for help and advice during manuscript preparation, Colette                  17. Lariven S, Bouvet E, Verdon R, Casalino E, Laporte A,
Boirot and Fabienne Micollier for documentation, Anderson             Vachon F. HIVInfection in Maghrebin Population in France. In: The
Loundou for computations, Carole Giovannini for typing the            Proceeding of the VIII International Conference on AIDS in
manuscript, and Gary Burkhart for editing the text. Antoine           Africa, Marrakech 1993. Abstract.
Messiah is supported by a fellowship from the Fondation pour la           18. Moumen-Marcoux R. Migrants et Perception du Sida: Le
Recherche Medicale.                                                   Maitre des Infideles. Paris, France: L'harmattan; 1993
                                                                          19. Boyer P, Dillon M, Navaie M, Deveikis A, Keller M,
Literature Cite                                                       O'Rourke S, et al. Factors predictive of maternal-fetal transmis-
     1. Reseau National de Sante Publique. Surveillance du Sida       sion of HIV-1: preliminary analysis of zidovudine given during
en France (situation au 31 Decembre 1995). Bulletin Epidemiologique   pregnancy and/or delivery.JAAL4. 1994;271:1925-1930.
Hebdomadaire. 1996;10:45-51.                                              20. Connor E, Sperling R, Gelber R, Kiselev P, Scott G,
    2. Minkoff H, Holman S, Beller E, Delke I, Fishbone A,            O'Sullivan M, et al. Reduction of maternal infant transmission of
Landesman SH. Routinely offered prenatal HIV testing. NEngIJ          human immunodeficiency virus type 1 with zidovuline treatment.
Med. 1988;319:1018. Letter.                                           Pediatric AIDS Clinical Trial Group Protocol 076 Study Group.
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92                                                                    JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 90, NO. 2

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Hiv testing in minorities and women 1999

  • 1. HIV TESTING, KNOWLEDGE, ATTITUDES, BELIEFS, AND PRACTICES AMONG MINORrTIES: PREGNANT WOMEN OF NORTH- AFRICAN ORIGIN IN SOUTHEASTERN FRANCE Antoine Messiah, MD, PhD, Dominique Rey, MD, Yolande Obadia, MD, Michel Rotily, MD, and Jean-Paul Moatfi, PhD Marseille, France Since 1991, the French public health ministry has recommended that human immunod- eficiency virus (HIV) testing be offered to all pregnant women. This study was undertaken to determine whether this recommendation is followed independently of a woman's ethnicity. It is based on a 1992 survey regarding knowledge, attitudes, beliefs, and practices on HIV infection and testing among pregnant women in southeastern France. Survey results revealed that North-African women (n=207) were more likely to have a low socioeconomic and educational level, receive their health care at public health institu- tions, and be less knowledgeable about HIV transmission than French women (n=2234). They were also more likely to have been tested for HIV without their knowing it and less like- ly to perceive themselves as being at risk. Consent to undergo HIV testing during pregnancy was dependent on their North-African origin after controlling for significant covariates. These results indicate that routine prenatal screening appears insufficient to ensure ade- quate HIV testing and counseling of women of ethnic minorities. The development of HIV pre- vention programs that are cultural-specific and that aim at increasing physicians' compliance with the official recommendation is needed. (J Nati Med Assoc. 1 998;90:87-92.) Key words: * human immunodeficiency virus ate for general policies of human immunodeficiency (HIV) * HIV transmission * minorities virus (HIV) screening and counseling to reach all women.2 This is especially true in France, where the In France, as in most other industrialized countries, public social insurance system guarantees universal the proportion of women among the total number of health coverage for all pregnant women living in the registered acquired immunodeficiency syndrome country. Since the early 1970s, a minimum of four (AIDS) cases has increased steadily since the begin- free-of-charge prenatal care medical consultations ning of the epidemic (from 13.9% in 1987 to 20.4% in (including testing for syphilis, rubella, and toxoplas- 1995.1 Prenatal care is viewed as especially appropri- mosis at the first visit) have been mandatory. It is wide- ly accepted that this legislation greatly contributed to From the South-Eastern French Center for Disease Control and the recent progress in prenatal care and prevention of pre- Institut Paoli-Calmettes, Marseille, France. This study was supported term births and children's handicaps.3 by the French Agency for Aids Research. Requests for reprints In December 1991, the French Ministry of Health should be addressed to Dr Antoine Messiah, INSERM U-379, Institut issued an official recommendation that general practi- Paoli Calmettes, 232 bd Sainte Marguerite, BP 156, 13273 tioners, gynecologists, and obstetricians systematically Marseille Cedex 09, France. offer, an HIV test to all pregnant women consulting JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 90, NO. 2 87
  • 2. HIV TESTING AMONG MINORITIES foreigners; among them, 35% come from North Table 1. Sociodemographic Data and Conditions Africa.6 Evidence from other countries strongly sug- of Pregnancy, by Ethnic Group gests that HIV prevention programs have specific dif- % North- ficulties in reaching women from ethnic minorities African % French and emphasizes the need for culturally adapted mes- Women Women sages and interventions.79 It is therefore important to (n=207) (n=2234) P Value know, if despite the official recommendation, there Age (years) are differences in access to HIV testing and counsel- <25 26 21 ing between members and nonmembers of these 25 to 34 60 67 NS minorities and to determine to which factors these dif- ,35 14 12 ferences are related. Matrimonial status A survey on HIV screening among pregnant Married 71 64 women conducted in southeastern France in 1992, Unmarried but living with a partner 13 28 <.001 the Prevagest survey,'0'11 included North-African and Living alone 16 7 French women. The survey examined sociodemo- Level of education graphic characteristics, pregnancy conditions, HIV University graduate 15 52 testing experience, risk situation and risk perception, Secondcary school and knowledge and beliefs about HIV transmission. graduate 44 37 <.001 Lower level of METHODS education 41 11 Population Occupational status The Prevagest survey is described elsewhere.'0"'1 It Employed 27 70 <.00 1 consists of three subsurveys directed at pregnant Unemployed 73 30 women and the health-care institutions caring for Level of income ,6000 francs 58 14 <.001 them. The first subsurvey is an unlinked anonymous >6000 francs 42 86 HIV seroprevalence survey. The second subsurvey, Religion which is analyzed in this article, is a survey on the None or not knowledge, beliefs, attitudes, and practices of the practicing 30 64 <.001 women. Through the data collected by the third sub- Practicing 70 36 survey, directed at the institution, we could determine Prenatal care whether the women were in a ward conducting sys- delivered by tematic testing; the accuracy of this information was Private ambulatory checked by direct observation at each site. In south- physicians 44 76 <.001 eastern France, 77 wards attend pregnant women for Public prenatal delivery. Seventy-one wards agreed to participate in institutions 56 24 No. of prenatal the study during April 1992. A total of 3148 women consultations were cared for during the study period; of these, 114 <4 2 1 (4%) neither spoke nor read French and 209 (7%) 4 6 1 <.001 refused to participate. The remaining 2825 women I,< 4 92 98 included North Africans (n=207), French metropoli- Abbreviations: NS=not significant. tans (born in continental France) (n=2234), French Caribbeans (n=37), Europeans (n=207), sub-Saharan Africans (n=35), other (n=63), and unknown (n=42). For the purpose of this article, the first two groups for prenatal care, provided the women gave informed were compared. consent and could decline the offer. In this context, screening appears as a universal policy, expected to be Data Collection and Analysis equal for everyone, but it assumes that preventive A self-administered anonymous questionnaire was counseling targeted at the general population is able to proposed by a nurse to all the hospitalized women reach all subgroups, including cultural minorities.4'5 within 3 days after childbirth. Topics included Of the entire population living in France, 6.3% are detailed sociodemographic information, the woman's 88 JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 90, NO. 2
  • 3. HIV TESTING AMONG MINORITIES experience with prenatal care and HIV testing during her pregnancy, HIV-related individual risk behaviors Table 2. Risk Behavior and Individual Risk and perception, and knowledge concerning horizon- Perception, by Ethnic Group tal and vertical HIV transmission. For the institutions % North- whose policy was systematic testing, a woman's African % French answers to the question, "Were you offered an HIV Risk Women Women test here?" allowed us to determine whether she had Behavior (n=207) (n=2234) P Value been tested with or without her knowledge. Multiple sexual partners in the past 2 years Univariate comparisons between ethnic groups Yes 5 7 NS were performed with the chi-squared test (qualitative No 95 93 data) and Student's t-test (quantitative data).'2 All sig- Intravenous drug use (at least once) nificant variables (P<.05) were introduced into a Yes 1 1 NS logistic regression model,'3 with a woman's declara- No 99 99 HIV-positive sexual partner (at least once) tion of having been tested (versus not) during her Yes 0 0 NS pregnancy as the dependent variable. The final No 100 100 model consisted of variables with P<.10. Calculations Intravenous drug user sexual partner (at least once) were done using SPSS software. Yes 0 2 NS No 100 98 RESULTS Declared Sociodemographic Data and Conditions of At least one of Pregnancy the above 6 8 NS Regarding age, North-African women were similar None of to French metropolitan women (Table 1). North- the above 94 92 African women were more likely to live alone, to be Declared higher or average risk of being infected, in comparison with overall women's population unemployed and less educated, to have a low Yes 7 20 <.001 income, to practice a religion, and to have their pre- No 93 80 natal care delivered by public institutions. French metropolitan women were more likely to have more Abbreviations: NS=not significant and HIV=human than four prenatal consultations. immunodeficiency virus. HIV Testing Experience, Risk Situation and Risk Perception, Knowledge, and Beliefs About HIV tan women (P<.001) had had a routine HIV test with- Transmission out their being aware of it because of a lack or inade- Declaration of prenatal HIV testing was signifi- quacy of informed consent procedures. Thus, the cantly lower among North-African women (42%) actual frequency of prenatal HIV testing was similar than among French metropolitan women (65%; between North-African women (75%) and French P<.001). Eighty-three percent of French metropolitan metropolitan women (73%). women declared that they had been tested at least North-African women declared HIV-related risk once for HIV, including the ones who had a test behaviors as frequently as French metropolitan before the pregnancy, versus 49% among North- women did (Table 2). However, they were less likely African women (P<.001). Among the 907 women to perceive themselves at higher or average risk. who said they had not been tested for HIV during Knowledge about the main routes of HIV trans- pregnancy, only a few (3.3% of North-African women mission was less accurate among North-African and 1.3% of French metropolitan women) had women; the difference was larger for horizontal than refused the test offered to them; this contrasts with for vertical transmission (Table 3). North-African 68% of North-African women and 56% of French women more frequently believed in HIV transmis- metropolitan women to whom the test had not been sion through casual contact and mosquito bite. proposed (P<.001). When the women's statements and those of the medical ward attending them were Multivariate Analysis pooled, it appeared that an additional 33% of North- To determine how differences in HIV testing dur- African women versus only 8% of French metropoli- ing pregnancy were correlated with the variables dif- JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 90, NO. 2 89
  • 4. HIV TESTING AMONG MINORITIES Table 3. Knowledge and Beliefs About HIV Horizontal and Vertical Transmissions, by Ethnic Group Knowledge % North-African % French & Beliefs Women (n=207) Women (n=2234) P Value Horizontal Transmission Correct answers to 'People can get AIDS from'* Sexual intercourse (yes) 73 95 <.001 Intravenous drug use (yes) 73 91 <.001 Receiving blood (yes) 68 88 <.001 Donating blood (no) 31 55 <.001 Being admitted in the same hospital ward as a person with AIDS (no) 44 72 <.001 Using public lavatories (no) 32 60 <.001 Drinking in a glass used by a person with AIDS (no) 41 65 <.001 A mosquito bite (no) 33 57 <.001 Knowledge scoret m=4.3 m=5.9 <.001 SD=2.2 SD=1.7 Vertical Transmission Correct answers to "HIV can be transmitted from an infected mother to her baby"* During pregnancy (yes) 69 90 <.001 During delivery (yes) 19 37 <.001 Through breast-feeding (yes) 32 39 NS By taking care of the child after birth (no) 37 68 <.001 Knowledge scoret m=1.7 m=2.4 <.001 SD=1.1 SD=1.0 Abbreviations: HIV=human immunodeficiency virus, AIDS=acquired immunodeficiency virus, SD=standard deviation, and NS=not significant. *The correct answer is given in parentheses. tThe score (minimum=0, maximum=8) was built by counting each correct answer as 1 and summing them. $The score (minimum=0, maximum=4) was built by counting each correct answer as 1 and summing them. ferentiating North-African women from French met- nant women delivering in southeastern France were ropolitan women, logistic regression was performed surveyed during the study period, but not all could be (Table 4). It showed a positive correlation between reached because the study protocol was restricted to knowledge scores, risk perception, and the likeli- French-speaking women for practical reasons. It is hood of being tested (with the woman's knowledge). likely, however, that if non-French speaking women It also showed that those women who were married, had been included, differences between migrants and had a low educational level, and low income level nonmigrants would have been even larger. Southern were significantly less likely to be tested. Finally, it France has historical links with North Africa and is showed that even when these covariates were con- the focus for migration and travel to Europe; effec- trolled for, being a North-African women was still tively, non-French women in our sample were pri- significantly associated with a lower likelihood of marily from North Africa. Only small populations being tested with informed consent. come from other non-European countries, which pre- vented their inclusion in this analysis. The situation of DISCUSSION these other minorities may be quite different, but in- This survey was the first in France to compare depth analysis would require surveys in French access to HIV screening and counseling between regions where they are better represented. migrant and metropolitan women. Most of the preg- The French public social insurance system guaran- 90 JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 90, NO. 2
  • 5. HIV TESTING AMONG MINORITIES Table 4. Logistic Regression Analysis of Women's Declaration of Having Had an HIV Prenatal Test (Yes Versus No)* OR 95% Cl P Value Matrimonial status Married 0.59 0.39-0.88 .010 Unmarried but living with a partner 0.83 0.55-1.27 .398 Living alone* 1 .00 Level of education University graduate* 1.00 Secondary school graduate 0.59 0.49-0.73 <.001 Lower level of education 0.53 0.39-0.71 <.001 Level of income <6000 francs 0.75 0.57-1.00 .050 >6000 francs* 1.00 Individual risk perception of being HIV infected when compared with average risk among women Higher or average risk 1.25 0.99-1.58 .066 Lower or no risk, or no evaluation* 1.00 Knowledge scores (numeric variables) Of horizontal HIV transmissiont .027 Of vertical HIV transmissiont .019 Ethnic group North-African women 0.61 0.44-0.90 .007 French women* 1.00 Abbreviations: OR=adjusted odds ratio and CI=95% confidence interval. *Category of reference. tOR=1.06 per point of score. tOR=1 .12 per point of score. tees universal coverage for all pregnant women living HIV transmission through casual contact and mos- in the country, and the legislation recommends that quito bite, as found in other ethnic minorities.8'9 Such all pregnant women be offered HIV screening, pro- cultural beliefs create specific challenges for HIV pre- vided they give informed consent. Screening policy vention.'4"5 In addition, married women were less therefore is expected to be equal for everyone. Our likely to have been tested for HIV, contrasting with survey shows that if all HIV tests taken with or with- unmarried women living with their partner. This sug- out the woman's knowledge are considered, the fre- gests that marriage restrains women of ethnic minori- quency of prenatal HIV testing is similar between ties from being tested. Until now, North Africa was groups independently of ethnic origin. However, the relatively unaffected by the epidemic; most HIV- survey also shows that equality is not achieved in positive women were infected by their husbands.'6 practice. It reveals a dramatic difference in applica- In France, only 3% of cumulated AIDS patients in tion of the testing policy: North-African women were 1993 were born in North Africa." It often is argued more frequently tested without their knowledge and that the traditional cultural norms of North-African less likely to have been proposed a test by the physi- women have a protective effect against HIV infec- cian, suggesting a lack of adequate preventive coun- tion.18 Some of the HIV-related beliefs of these seling associated with testing for these women. This is women are closely linked to the Islamic religion, eg, especially unfortunate because, as the survey shows, risk of vertical contamination through breast-feed- North-African women lack knowledge about AIDS ing and, more generally, risk of transmission transmission and are less likely to feel at risk although through contact with body fluids. they declared at risk behaviors as frequently as Numerous aspects differentiating North-African French women did. women from French women, including lower North-African women more frequently believed in socioeconomic and educational levels, could JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 90, NO. 2 91
  • 6. HIV TESTING AMONG MINORITIES explain the lesser tendency of North-African women Naitre en France, dix ans d'ivolution. Paris, France: Doin-INSERM; 1984. of knowing that they had a test. Even when these 4. Steffen M. France: social solidarity and scientific exper- parameters were controlled for, being of North- tise. In: Kirp DL, Bayer R eds. AIDS in the Industrialized African origin was still correlated with this tendency. Democracies. Passions, Politics and Policies. New Brunswick, NJ: This suggests that institutional factors might be at Rutgers University Press; 1992:221-251. play with these women. Such factors include the 5. MoattiJ, Dab W, Loundou A, Quenel P, Beltzer N, Ames A, et al. Impact on the general public of media campaigns against wards' screening policy toward these women and AIDS: a French evaluation. Health Policy. 1992;21:233-247. the physicians' perceptions of women's risk and 6. Labat J. La Population Etrangere. Recensement de la their ability to deal with HIV prevention. They can- Population de 1990. Paris, France: INSEE Premiere; 1991. not be attributed to language barriers since women 7. O'Leary A. Women at Risk: Issues in the Primary Prevention who neither spoke nor understood French did not ofAIDS New York, NY: Plenum Press; 1995 8. Peruga A, Rivo M. Racial differences in AIDS knowledge participate in the study. among adults. AIDS Educ Prev. 1992;4:52-60. Our survey strongly suggests that universal routine 9. Nyamathi A, Bennett C, Leake B, Lewis C, FlaskerudJ. prenatal HIV screening does not guarantee adequate AIDS-related knowledge, perceptions and behaviors among counseling, especially for women of ethnic minorities. impoverished minority women. AmJPublic Health. 1993;83:65-71. Additional studies on ethnic minorities other than 10. Obadia Y, Rey D, Moatti JP, Pradier C, Couturier E, Brossard Y, et al. HIV prenatal screening in South-Eastern North-African women are necessary to confirm this France: differences in seroprevalences and screening policies by in the French context. pregnancy outcomes. AIDS Care. 1994;1:29-38. Zidovudine treatment of HIV-infected mothers, 11. Rey D, Moatti J, Obadia Y, Rotily M, Dellamonica P, which significantly reduces the risk of vertical trans- GilletJ, et al. Differences in HIV testing, knowledge and attitudes mission,19'20 creates more incentives for the develop- in pregnant women who deliver and those who terminate: Prevagest 1992-France. AIDS Care. 1995;7:S39-S46. ment of systematic HIV prenatal screening. It 12. Armitage P, Berry G. Statistical Methods in Medical underscores the need for culturally sensitive pro- Research. 2nd ed. Oxford, England: Blackwell Scientific grams for the medical community for these women Publications; 1987. to benefit from the recent therapeutic advances in 13. Kleinbaum D, Kupper L, Morgenstern H. Epidemiologic prevention of vertical transmission, without contra- research principles and quantitative methods. New York, NY: Van Nostrand Reinhold; 1982. vening the ethical principle of patients' individual 14. Ulin P. African women and AIDS: negotiating behavioral freedom of choice. Additional prevention programs change. Soc Sci Med. 1992;34:63-73. therefore are needed, with some targeted at ethnic 15. Guerin A. Le modele culturel de la femme Africaine. Un minorities and others targeted at physicians and entretien avec Francoise Heritier-Auge. Le Journal du Sida. their institutions. 1994;64-65:33-34. 16. Maaroufi A, Chakib A, El Aouad R, Squalli M, Zahraoui M, Himmich H. Aspects Cliniques et Therapeutiques de l'infection 2 Acknowledgments VIH au Maroc. In: The Proceeding of the VIII International The authors thank Claire Julian-Reynier and Michel Morin Conference on AIDS in Africa, Marrakech 1993. Abstract. for help and advice during manuscript preparation, Colette 17. Lariven S, Bouvet E, Verdon R, Casalino E, Laporte A, Boirot and Fabienne Micollier for documentation, Anderson Vachon F. HIVInfection in Maghrebin Population in France. In: The Loundou for computations, Carole Giovannini for typing the Proceeding of the VIII International Conference on AIDS in manuscript, and Gary Burkhart for editing the text. Antoine Africa, Marrakech 1993. Abstract. Messiah is supported by a fellowship from the Fondation pour la 18. Moumen-Marcoux R. Migrants et Perception du Sida: Le Recherche Medicale. Maitre des Infideles. Paris, France: L'harmattan; 1993 19. Boyer P, Dillon M, Navaie M, Deveikis A, Keller M, Literature Cite O'Rourke S, et al. Factors predictive of maternal-fetal transmis- 1. Reseau National de Sante Publique. Surveillance du Sida sion of HIV-1: preliminary analysis of zidovudine given during en France (situation au 31 Decembre 1995). Bulletin Epidemiologique pregnancy and/or delivery.JAAL4. 1994;271:1925-1930. Hebdomadaire. 1996;10:45-51. 20. Connor E, Sperling R, Gelber R, Kiselev P, Scott G, 2. Minkoff H, Holman S, Beller E, Delke I, Fishbone A, O'Sullivan M, et al. Reduction of maternal infant transmission of Landesman SH. Routinely offered prenatal HIV testing. NEngIJ human immunodeficiency virus type 1 with zidovuline treatment. Med. 1988;319:1018. Letter. Pediatric AIDS Clinical Trial Group Protocol 076 Study Group. 3. Rumeau-Rouquette C, Du Mazaubrun C, Rabarison Y. NEnglJMed. 1994;331:1173-1180. 92 JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION, VOL. 90, NO. 2