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ABSTRACT |
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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3); age (OR = 0.96 per year, 95% CI = 0.94–0.99); study site (OR = 1.45, 95% CI = 1.34–1.56 to 5.32, 95% CI = 4.92–5.75) for comparison with the reference site; and no maternal education (OR = 1.38, 95% CI = 1.15–1.66) compared with any education. Other predictors (in subgroups) were bed net use (OR = 0.49, 95% CI = 0.48–0.50); preventive sulfadoxine-pyrimethamine doses (OR = 0.25, 95% CI = 0.24–0.25); and infection with human immunodeficiency virus (HIV) (OR = 1.49, 95% CI = 1.11–2.00). Programmatic priorities should respond to heterogeneous distribution of multiple risk factors, including prevalance of malaria and infection with HIV, and maternal socioeconomic status. |
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). Identification of highest-risk populations would facilitate definition of highest-priority target groups for introduction of new interventions, so that the most vulnerable might be reached first.10
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Only two studies had formally measured the prevalence of maternal peripheral malaria parasitemia in Sofala and Manica Provinces. With the aim of providing data to inform the provincial policy-making process, we analyzed predictors of maternal malaria infection in the combined data sets from the two investigations.
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METHODS |
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Syphilis study. Between August 2003 and January 2004 (low-transmission season for malaria), a cross-sectional study was conducted in six urban and peri-urban antenatal clinics operated by the MOH in the city of Beira and the adjacent district of Dondo, both in Sofala Province. The primary aim of the study was to evaluate the diagnostic accuracy of a new rapid test for maternal syphilis. Because malaria infection had been reported to affect the diagnostic accuracy of some syphilis tests, maternal peripheral blood smears were evaluated by microscopy for the presence of malaria parasitemia in all study subjects.15,16 IPTp was not yet available for this population.
IPTp study. Between April and June 2004 (peak transmission season), a cross-sectional study of maternal peripheral malaria parasitemia prevalence (again using microscopy) was conducted in two MOH IPTp pilot sites: Gondola district (Manica Province) and Nhamatanda district (Sofala Province). The primary aim of this study was to compare malaria and anemia prevalence in women who had used ITNs and/or had received IPTp with sulfadoxine-pyrimethamine (SP) to that in women who had not used either intervention.
Study settings. The city of Beira (four syphilis study clinics) is the second largest city in Mozambique. Its antenatal HIV prevalence (29.1–34.4% in sentinel surveillance) is thought to be the highest in the country.17 Malaria transmission occurs year round with seasonal peaks, but has been somewhat attenuated by spraying campaigns and widespread commercial access to ITNs. The adjacent district of Dondo (two syphilis study sites) is part of the Beira peri-urban area; only part of it is routinely sprayed.
Nhamatanda (one IPTp study site) is approximately 100 km west of Beira in a rural agricultural region that undergoes frequent seasonal flooding. Gondola (one IPTp study site) is approximately 80 km west of Nhamatanda. It is also rural and agricultural, but less subject to flooding because of its higher elevation. Malaria transmission occurs year round with seasonal peaks in both towns, but no spraying campaigns are conducted, and access to ITNs was still very limited at the time of the study.18 In all four districts, more than half the population were thought to live in poverty.19 Figure 1 describes the study locations.
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Laboratory evaluation. In both studies, capillary blood was taken by finger prick; blood smears were stained with Giemsa and read independently by two microscopists who counted asexual P. falciparum parasites against 500 leukocytes. The parasite count was normalized to a presumed leukocyte count of 8,000/µL. If the two readings differed, a third microscopist examined the slide. The same microscopists were responsible for quality control of malaria smears from both studies. In the IPTp study only, HemoCue (HemoCue Ltd., Ängelholm, Sweden) devices were used to measure maternal hemoglobin levels, again using capillary blood obtained by finger-prick.
Syphilis status of participating women was ascertained by rapid plasma reagin (RPR) and Treponema pallidum hemagglutination (performed by clinic staff and in a reference laboratory) in the syphilis study, and by on-site RPR or rapid testing (performed by clinic staff) in the IPTp study.
In both studies, women who elected to undergo voluntary counseling and testing for HIV-1 as a routine option in antenatal care were asked to share their test results with the investigators, but HIV testing was not a study procedure, and the study team did not confirm the results obtained by local MOH staff. At the time of the study, HIV testing had been available in some sites for nearly two years, was in the process of becoming available in other sites, and still had not been introduced in two sites. Antiretroviral therapy was available in two regional sites.
Data analysis. Means and proportions were calculated to describe the characteristics of the two patient populations. Differences between the two populations were described using t-tests and chi-square tests of significance, using P = 0.05 as the upper boundary of statistical significance. Bivariate and multivariate logistic regression, using robust confidence limits to reflect possible correlation of responses within health units, were then used to estimate associations between the primary outcome measure (presence of any asexual P. falciparum parasites on at least two readings of a peripheral blood smear) and patient factors. The initial models included factors previously known to be associated with malaria infection (e.g., gravidity), as well as factors of intrinsic interest to the investigators (e.g., study site); non-significant covariates (as determined by the Wald test) were then eliminated serially. We conducted separate multivariate analyses for subjects of known HIV status and all subjects because women with known HIV serostatus comprised less than half of the study subjects and could not be assumed to be a representative sample of the overall study population.
We did not adjust for gestational age because its assessment is highly imprecise in this setting, and because it is based almost entirely on fundal height, which could in turn be affected by malaria-related or HIV-related intrauterine growth retardation.14
Ethical considerations. Informed consent was obtained from all participants in Portuguese or local languages. Both studies were reviewed and approved by the pertinent committees at the Mozambican National Institutes of Health and at the University of Washington, and by the Provincial Health Directorates of Sofala and/or Manica Provinces.
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RESULTS |
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. The study populations were dissimilar in several respects. The syphilis study subjects were younger and of lower gravidity, their educational levels were higher, and they were predominantly urban. They were also more likely to be infected with HIV and/or syphilis.
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The association of site with malaria prevalence was similar to the association between season of data collection and malaria prevalence. The unadjusted odds ratio (OR) for comparison of malaria prevalence between the highest-prevalence syphilis site and the lowest-prevalence syphilis site (both evaluated during the low-transmission season) was 2.18 (95% confidence interval [CI] = 1.64–2.90), which was similar to the unadjusted OR for comparison of IPTp sites (studied during the wet-season transmission peak) to syphilis sites, which was 2.31 (95% CI = 1.97–2.72).
Results of HIV serologic analysis were available for 1,884 women (1,563 from the syphilis study and 321 from the IPTp study). The HIV prevalence varied significantly by site, from 9.1% in 1 IPTp site to 27.1% in 1 syphilis site. This prevalence was significantly increased in women 20–29 years of age (OR = 1.73, 95% CI = 1.39–2.15 for comparison with both younger and older women) and was negatively associated with gravidity (OR = 0.92, 95% CI = 0.87–0.97 per pregnancy).
In bivariate analyses (Table 3), younger age, lower gravidity, lower socioeconomic status, non-use of bed nets, lower maternal hemoglobin levels, and more frequent or more recent IPTp administration were all significantly associated with maternal peripheral malaria parasitemia, as expected. Malaria prevalence in bed net users was 14.2% versus 27.6% in non-users; malaria prevalence in women who had had any preventive SP was 5.1% versus 39.3% in women who had not yet had their first dose. There was also significant heterogeneity among study sites, as described above. Of note, there was no significant association between false-positive RPR test results and malaria parasitemia (OR = 1.41, 95% CI = 0.78–2.54) in the syphilis study group.
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), HIV infection was associated with higher prevalence of malaria parasitemia regardless of gravidity, and the IPTp study subjects had higher prevalences of parasitemia than the syphilis study subjects regardless of HIV serostatus or level of gravidity. HIV infection was significantly associated with malaria parasitemia in syphilis study subjects (OR = 1.43, 95% CI = 1.02–2.00), but not in the IPTp subjects (OR = 1.22, 95% CI = 0.67–2.21). However, few women in the IPTp study had been tested for HIV.
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), age, gravidity, educational level, and study site retained their significance for both groups. In the syphilis study group, HIV infection and absence of electricity were also significantly associated with malaria parasitemia. In the IPTp study group, use of ITNs and SP both retained their significance without substantial changes in ORs, which suggested that ITNs and SP contribute independently to reduction of malaria risk in pregnancy. An alternative analysis of the IPTp data showed that elapsed time since the last dose of preventive SP also retained its significance in multivariate analysis (OR = 9.01, 95% CI = 3.19–25.38 for association of malaria parasitemia and last SP dose 57 days prior to study, and OR = 22.05, 95% CI = 1.44–336.96 for no SP compared with the reference category of SP administration 
56 days previously). However, collinearity prevented concurrent insertion of the two measures (number of IPTp doses, elapsed time since last IPTp dose) into the same model.
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). However, subjects with known HIV status comprised a small subgroup of the study population as a whole, and HIV testing was unavailable in two sites. Evaluation for interaction between HIV status and other covariates failed to yield important interaction terms; the observed change in ORs appeared to be caused primarily by the exclusion of two entire study sites and 65% of the study subjects from the analyses that included HIV status. |
DISCUSSION |
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The site with the lowest observed prevalence (8.8%) was an urban clinic characterized by high HIV seroprevalence (27.1% in those tested), higher proportion of women tested for HIV (50.7%), higher socioeconomic status, regular coverage by an indoor residual spraying campaign, and data collection during the dry (low-transmission) season. The highest observed level was 48.1% (31.0% if women who had previously received preventive SP were included) in a rural site with lower socioeconomic status, lower HIV seroprevalence (18.4%), a similar proportion of women tested for HIV (52.1%), no coverage by spraying, and data collection during the rainy season. Overall, only 35.1% of the parasitemic women were of known HIV status, and only 9.1% of the parasitemic women had documented HIV infection.
Our findings suggest that differences in socioeconomic status, HIV prevalence, access to malaria-prevention interventions (especially bed nets and spraying), and geographic location are as important as seasonal effects in this setting. Previous studies conducted in Mozambique support this contention. For example, a study conducted in Beira and Dondo in 2002 found a malaria parasitemia prevalence of 30.3% in 413 individuals from the unsprayed sectors of Dondo, and 6.7% in a contemporary sample of 705 individuals from the sprayed sectors of Beira, with parallel differences in the observed density of anopheline vectors (João FI and others, unpublished data). The demographic and health survey in 2003 found that only 4.1% of young children in Sofala Province and 6.6% in Manica Province slept under ITNs, and that ITN use was 2.2 times more likely in urban children compared with rural children nationwide.20 Our own program-evaluation data in 2004 indicated that household-level ITN coverage ranged from under 15% in rural subsistence-farming communities to more than 50% in urban settings.18
Because HIV prevalence was substantially higher at sites with higher socioeconomic status, better access to bed nets and spraying, and lower levels of maternal peripheral malaria parasitemia, and because IPTp and ITN use had substantially reduced the prevalence of malaria parasitemia in IPTp program participants, our data may actually underestimate the association between socioeconomic status, geographic location, and malaria.
The primary limitation of our analyses is that the methods for the syphilis study and the IPTp study were not identical. In addition to the above-noted difference in season of data collection, socioeconomic data were not collected for the IPTp study participants (with the exception of educational level), and data on bed net use and antimalarial treatment were not collected for the syphilis study participants.
Another important limitation is that HIV serostatus was unknown for most participants, particularly in the rural areas and in the IPTp study participants. This is consistent with national-level patterns of HIV testing in Mozambique. In 2003, only 5.4% of urban women and 0.6% of rural women were believed to know their HIV status.20 Also, HIV disease stage was unknown in seropositive subjects, and women who elected both to be tested for HIV and to share their results with us may not have been representative of the study population as a whole. However, we believe that these weaknesses are offset by benefits of the large sample size, the consistency of methods used to determine maternal malaria status, and the heterogeneity of the eight study sites.
Our study findings have multiple implications for priority setting in MiP program implementation. Based on the observed heterogeneity of HIV and malaria parasitemia prevalence in the study subjects, and on observed patterns of participation in HIV testing, we believe that preferential implementation of MiP interventions for communities with larger populations and higher burdens of HIV, as had been proposed by some funders and advocacy groups, would not serve to correct inequities in the observed burden of malaria in the sites we evaluated because resources would be directed to regions of lower, rather than higher, malaria prevalence. Similarly, restriction of MiP interventions to individuals with documented HIV infection would have missed more than 90% of the parasitemic women we studied.
A better strategy for identifying high priority populations would be based on consideration of malaria transmission intensity and socioeconomic status, in addition to HIV prevalence, population size, and availability of preventive interventions, with universal provision of MiP interventions where vulnerability is great. This was the method adopted by the Sofala and Manica provincial health authorities in the aftermath of our study. Both the poorest and most malaria-endemic districts and the sites with highest estimated HIV seroprevalence were targeted for early expansion of IPTp programs. Later, new funding from bilateral donors permitted one-time targeted free bed net distribution for rural and peri-urban sites without access to spraying campaigns; future campaigns are now in the planning stages. Teams responsible for implementation and supervision of IPTp and antenatal HIV services were merged; the resulting increase in efficiency supported IPTp implemention in every single district in both provinces. As of this writing, the combination of political will, data-driven strategic analysis, and increased funding has begun to reduce the onerous burden of deciding which of many vulnerable women and infants should or should not be protected from malaria and its sometimes fatal consequences.
Received September 25, 2006. Accepted for publication April 12, 2007.
Acknowledgments: We are grateful to the following entities and individuals for technical support and/or assistance with study implementation: Direcção Provincial de Saúde, Província de Sofala; Direcção Provincial de Saúde, Província de Manica; Direcção Distrital de Saúde, Distrito de Gondola; Direcção Distrital de Saúde, Distrito de Nhamatanda; the National Malaria Control Program of Mozambique, the Malaria Branch of the Centers for Disease Control and Prevention (Atlanta, GA), Pedro João Corda, David Ehlert, Maria Felicidade Faria, Florência Floriano, Sheila Lukehart, Marquês Machaieie, Tom Martin, Josefa Sairosse, Benjamin Stubbs, and Fernanda Toalha.
Financial support: This study was supported by a cooperative agreement from the Centers for Disease Control and Prevention through the Association of Schools of Public Health (grant U36/CCU300430-20), and by the Bill and Melinda Gates Foundation.
* Address correspondence to Paula E. Brentlinger, Department of Health Services, School of Public Health and Community Medicine, University of Washington, Seattle, WA 98195. E-mail: brentp2{at}u.washington.edu 
Authors’ addresses: Paula E. Brentlinger, Kenneth Gimbel-Sherr, Mary Anne Mercer, and Stephen Gloyd, Department of Health Services, School of Public Health and Community Medicine, University of Washington, Seattle, WA 98195, Telephone: 206-543-8382, Fax: 206-543-3964, E-mails: brentp2{at}u.washington.edu, ksherr{at}u.washington.edu, mamercer{at}u.washington.edu, and gloyd{at}u.washington.edu. Pablo Montoya and Ana Judith Blanco Rojas, Health Alliance International, Rua Mayor Serpa Pinto 294, 4° Andar, Sector da Repartição de Saúde da Comunidade, Beira, Mozambique, Telephone: 258-3-324-271, Fax: 258-3-325-882, E-mails: pablom{at}teledata.mz and anajublan{at}hotmail.com. Maria Ana Chadreque Correia, Health Alliance International, Rua Dr. Araújo de Lacerda 147 CP 266 Chimoio, Mozambique, Telephone: 258-51-23251, E-mail: ma.correia{at}teledata.mz. Martinho Dgedge, Training Department, Department of Human Resources, Ministry of Health, Av Eduardo Mondlane c/Salvador Allende, C.P. 264 Maputo, Mozambique, E-mail: mdgedge{at}dnsdee.misau.gov.mz. Francisco Saúte, National Malaria Control Program of Mozambique, Communicable Disease Division, Ministry of Health, Av Eduardo Mondlane c/Salvador Allende, C.P. 264 Maputo, Mozambique, Telephone: 258-82-326-527, Fax: 258-1-311-621, E-mail: fsaute{at}dnsdee.misau.gov.mz.
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| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
