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HEALTH POLICY AND PLANNING; 16(1): 29–34 © Oxford University Press 2001 Antenatal syphilis in sub-Saharan Africa: missed opportunities for mortality reduction STEPHEN GLOYD,1 SANDERS CHAI2 AND MARY ANNE MERCER1 1Department of Health Services and 2Department of Environmental Health, University of Washington School of Public Health and Community Medicine, Seattle, Washington, USA Purpose: Between 4–15% of pregnant women are believed to be infected with syphilis in sub-Saharan Africa. Active infection with syphilis in pregnant women results in foetal or infant death or disability for 50–80% of affected pregnancies, and is a major cause of adult morbidity as well. Antenatal syphilis screening is cheap and effective; however, it is often poorly implemented in countries with high syphilis risk. This study sought to estimate the missed opportunities for antenatal syphilis screening in sub-Saharan Africa. Methods: Survey data were collected from 22 ministries of health in sub-Saharan Africa, complemented by data from published sources and key informants. Informants described their country’s policies and experience with antenatal syphilis screening and estimated their national syphilis screening rates. Findings: Seventy-three percent of women are reported by WHO to receive antenatal care in the study countries. Of women in antenatal care, 38% were estimated by survey respondents to be screened for syphilis. Costs and the organization of services were the principal reported obstacles to screening. With syphilis seroprevalence estimated at 8.3%, approximately 1 640 000 pregnant women with syphilis are undetected annually, including 1 030 000 women who attend antenatal care. Discussion: Syphilis testing and treatment is a cost-effective intervention that deserves much greater attention, particularly in sub-Saharan Africa and other countries where syphilis infection is high. Introduction Active infection with syphilis in pregnant women has long been recognized as a major cause of death or disability in the infants born to infected women. It is estimated that active syphilis infection in pregnancy causes adverse outcomes in 50–80% of pregnancies surviving past 12 weeks gestation, primarily as spontaneous abortions in the second and early third trimester, stillbirths, and congenital syphilis.1 Syphilis infection in pregnancy is highly prevalent in many areas of the world. Among women attending antenatal clinics in Africa, estimates of syphilis sero-reactivity range from 4–15%.1 Data from Zambia and Malawi suggest that between 26–42% of stillbirths and 8% of infant deaths in those countries may be attributable to syphilis alone.1,2 Syphilis is also a significant cause of morbidity in adults, and has been identified as a principal cofactor facilitating the transmission of HIV.3,4 The technology to address maternal syphilis has been widely available for decades. Syphilis screening and treatment in antenatal care has been cited as one of the most cost-effective ways to reduce foetal and infant mortality and morbidity in the developing world, comparing very favourably with immunizations against childhood infectious diseases.5 The treatment of syphilis-infected mothers represents an opportunity to also treat their partners, and thus interrupt further transmission of syphilis as well as HIV infection. In Tanzania, a reduction in rates of sexually transmitted infections (STIs) in a community was associated with a reduction in the risk of transmitting HIV by 40%.6 Although syphilis is an important cause of morbidity and mortality, and antenatal screening is relatively feasible and effective, this intervention has not been promoted to the extent of other, less efficacious interventions. Even where antenatal syphilis screening is a national policy and where antenatal care is widely utilized, syphilis screening appears to be sporadically implemented at best. Few estimates exist as to how well this problem is being addressed in areas of the world where screening and treatment could have an enormous impact. This study was designed to determine the extent to which health systems in sub-Saharan Africa have addressed the issue of antenatal syphilis screening. The research objectives were to (1) identify the national policies in sub-Saharan Africa regarding antenatal syphilis screening, and (2) estimate the proportion of pregnant women already attending antenatal care who are not being screened for syphilis. Recognizing the paucity of precise data regarding both infection levels and programme efforts, the emphasis of the study was to provide orders of magnitude estimates of the current 30 Stephen Gloyd et al. state of antenatal syphilis screening for policy-makers, providing guidance for allocation of scarce health sector resources. Researchers thus sought to estimate the magnitude of the missed opportunities to reduce maternal, foetal and infant mortality and morbidity due to syphilis among women already receiving antenatal care. The study focused on the countries of sub-Saharan Africa where syphilis prevalence is known to be high and where the potential for reducing mortality and morbidity due to maternal syphilis infection is correspondingly great. Methods The data for this study were collected from a survey of national ministries of health conducted by the authors, complemented by data from published sources and key informants of participating countries. Published sources include The state of the world’s children,7 the Demographic and Health Survey series,8 World Health Organization (WHO) publications9,10 and epidemiological studies of maternal syphilis infection rates.11–13 Whenever possible, the authors corroborated information from more than one source. Estimates of the effectiveness of syphilis screening on neonatal outcomes were derived from Schulz et al.5 The survey instrument consisted of a one-page, 14-item questionnaire. Questions covered national syphilis screening policy and targets, prenatal care rates, rates of antenatal syphilis screening and reported results of that screening, location of screening, source of information for the survey, including whether they had methods of routinely assessing syphilis screening, and reported obstacles to screening. The survey was directed at the 110 countries in the world with populations over 1 million and with the highest reported under-5 mortality rates. This analysis focuses on a sub-sample of 38 countries in mainland sub-Saharan Africa and Madagascar. Surveys were sent between January and July of 1996 to the 33 countries from this group for which a fax number or postal address was available to the authors; follow-up continued through July of 1997. In five countries, personal visits were made with Ministry of Health officials responsible for maternal health services to obtain questionnaire information. All responses were confidential. Antenatal care coverage figures for each country were based on DHS surveys and/or WHO estimates,10 using the most recent national figure when two or more differing estimates were available. The proportion of women screened for syphilis was based on rates provided by the respondents from each country. Syphilis seroprevalence was calculated based on published literature and the survey estimates. Pregnancies per year were calculated by multiplying the crude birth rate times the country population by 1.15 in order to adjust for pregnancy losses.10 ‘Missed opportunities’ were estimated as the number of pregnant women with active syphilis already attending antenatal care but who were not screened, and thus, whose infections were not detected. These estimates were based on several assumptions discussed below. The literature used in estimating syphilis infection rates among antenatal care attendees sometimes failed to specify whether screening (RPR or VDRL) or confirmatory treponemal (FTA or TPHA) tests were used in the studies described.i In such cases, we cross-referenced the cited figures with other comparable studies in the country. If other study data could not be located, we assumed that ‘screening’ meant unconfirmed (RPR or VDRL only) seropositive rates and projected that 80% of those screened positive by nontreponemal tests would have been confirmed cases of syphilis by treponemal tests.14 In countries where multiple values for antenatal syphilis seroprevalence were substantially different, data from the most recent and most representative sample were used. Aggregate means of antenatal care attendance, syphilis screening, and syphilis prevalence levels were weighted by country population for the calculations. ‘Nonrespondent countries’ were defined as sample countries not responding to mailed or faxed questionnaires and countries to which questionnaires were not sent. Results Of the 33 target countries in sub-Saharan Africa to which the survey was sent, respondents from 17 countries returned the questionnaire. We added questionnaires filled out during the personal visits to five countries which had not returned questionnaires; thus, the total sample was 22 countries. Although the questionnaire was directed to the maternal–child health (MCH) division of each ministry of health, only three of the 17 returned questionnaires were signed by MCH division staff, nine were signed by STD/AIDS programme staff, four were signed by statistics or epidemiology staff, and one was signed by someone whose division was unknown to the authors. Seventeen (77%) of the 22 respondents reported universal syphilis screening to be a national norm of pregnancy care in their country. VDRL was reported to be used as the principal treponemal screening test by 10 (45%) of the responding countries, RPR by seven (32%), and both VDRL and RPR by five (23%) countries. Verification of positive screening tests by TPHA or FTA was reported to be the norm in six (27%) of the responding countries. No country reported national targets or indicators for monitoring progress of antenatal syphilis screening. Routine contact tracing was reported to be an integral part of antenatal syphilis follow-up in eight (36%) of the respondent countries. No country reported routine repeat screening for women near the end of pregnancy. Nineteen respondents provided estimates of syphilis screening rates among women in antenatal care. The data were estimated by seven respondents, six used specific investigations from sample populations (not necessarily representative), and nine reported data from STI registries or routine statistics (some indicated more than one source). Eight of the above respondents were able to estimate screening levels by capital city, other urban, or rural areas. Table 1 provides overall summary data on population size, pregnancies, antenatal care and syphilis screening among the 22 respondent countries. The population of those 22 countries Antenatal syphilis screening in Africa Table 1. 31 Estimated antenatal syphilis screening in 22 reporting countries of sub-Saharan Africa (in millions) Characteristic n (millions) (%) Total population represented by sample (% of total population of sub-Saharan Africa) Estimated pregnancies/year in reporting countries (% of total population in reporting countries) Estimated pregnant women who received antenatal care (% of pregnancies/year) Estimated pregnant women screened for syphilis (% of those receiving antenatal care) 397.5 19.9 14.5 5.5 (73) (5) (73) (38) Obstacle reported to be important Number reporting each obstacle antenatal syphilis prevalence from 14 countries of subSaharan Africa, 11 of which were from the 22 sample countries.11–13 The weighted mean for syphilis seroprevalence from these studies was 8.3%, the median was 8.75% and the range was 0.9–20.8%. Cost (to patient) of testing Organization of services Cost (to patient) of treatment Transport costs to testing facility Inadequate priority of MOH Social/cultural resistance Vacations, absence of health workers Provider compliance/awareness 10 7 6 4 3 3 2 2 Table 3 provides estimates of syphilis screening and missed opportunities for all of sub-Saharan Africa, based on the data from the study sample and using the weighted syphilis prevalence estimate of 8.3%. Over 2 million pregnant women in sub-Saharan Africa would be actively infected with syphilis each year if it were possible to generalize this prevalence through the region. Table 2. Reported obstacles to universal antenatal syphilis screening in sub-Saharan Africa (n = 21) represents approximately 73% of the total population of subSaharan Africa. The weighted mean of antenatal care coverage reported by WHO for respondent countries was 73% compared to 50% for the non-respondent countries. The weighted mean of the estimated proportions of antenatal patients screened for syphilis in the 19 countries that provided that information was 38%, with a range of 1–92%. Table 2 summarizes survey data on reported obstacles to screening for the 21 countries that responded to this question. Cost of testing or treatment and the organization of services were reported to be the principal obstacles. The weighted mean reported syphilis screening positivity rate among pregnant women in antenatal care estimated by the 14 countries responding to this question was 10.9%. Assuming that 80% of those screened as positive would be women with active syphilis infection, the weighted mean proportion of antenatal active syphilis in responding countries was estimated to be 8.7%. The authors’ reviewed 23 recent studies on We estimated the antenatal syphilis screening rate for all of sub-Saharan Africa by applying the 38% reported screening rate of responding countries to all countries times their antenatal care attendance rates. If survey data on antenatal screening are representative of the rest of sub-Saharan Africa, approximately 630 000 pregnant women with syphilis are currently detected and treated (assuming 100% accurate detection and timely treatment). Another 1 640 000 pregnant women with syphilis are undetected, including about 1 030 000 women who attend antenatal care. Discussion The survey data demonstrate that although antenatal syphilis screening is a national policy in over three-quarters of respondent countries, most pregnant women who attend antenatal care are not screened. These findings suggest that inadequate syphilis screening and treatment in pregnancy represents an enormous missed opportunity to reduce maternal, perinatal and infant mortality and morbidity in sub-Saharan Africa. In addition, inadequate syphilis screening probably represents Table 3. Estimated annual missed opportunities for prevention of stillbirths, late abortion, and congenital syphilis for sub-Saharan Africa (in millions) Characteristic Number (millions) Method Total pregnant woman per year Pregnant women with active syphilis infection Pregnant women with active syphilis infection – detected 27.4 2.3 0.63 @5% of total population @8.3% infection rate @73% ANC coverage @38% screening Total women with syphilis minus those detected @73% ANC coverage @62% not screened Pregnant women with active syphilis – undetected Missed opportunities: pregnant women with active syphilis who are already in antenatal care – undetected 1.64 1.03 32 Stephen Gloyd et al. an important missed opportunity for reduction of HIV infection among adults. The study data are imprecise and subject to error. The authors believe that the antenatal syphilis screening rate from our survey of 38% may be an overestimate of the real syphilis screening rate in all of sub-Saharan Africa for the following reasons. • The screening rates for respondents to the survey are likely to be higher than non-respondents because of response bias. Respondent countries had much higher levels of antenatal care utilization (using WHO figures) than nonrespondent countries. Among respondents, countries with higher antenatal care coverage had significantly higher antenatal syphilis screening than those with lower antenatal coverage, suggesting that non-respondent countries may also have lower antenatal syphilis screening rates. • The rates of antenatal syphilis screening within responding countries may be overestimated. Three respondents appeared to have overestimated their syphilis screening rates according to key informants, possibly because they might have wanted to put a favourable face on their antenatal syphilis activities. • Where screening is done, treatment may be given too late in gestation to effectively prevent adverse perinatal outcomes. Studies in Mozambique suggest that even when screening is operational, only 20% of those receiving prenatal care received treatment prior to 28 weeks of gestation due to late first antenatal visits and delayed (or no) treatment.15 Although validation of the accuracy of the data reported in the survey is difficult, it appeared that nearly all respondents filled out the questionnaires with considerable care, and most indicated where data were not available. All of the officials from the five countries for whom personal visits were made said that no routine data were kept in their countries regarding syphilis screening rates; thus, their estimates were guesses based on their experience. The fact that most of the respondents were from epidemiology or STD sectors of their Ministries of Health casts some doubt on the accuracy of the antenatal care data. However, it would have been difficult for these officials to obtain information on antenatal syphilis screening policy and prenatal care attendance without consulting the MCH officials in the ministries. Moreover, the unweighted mean antenatal screening rate reported by study respondents (79.5%) was nearly identical to that available from WHO reports (78.5%).12 In addition, the weighted mean reported syphilis seroprevalence from the sample countries (8.7%) was very similar to the weighted mean from the literature (8.3%). These findings support the likelihood that information gained from the survey is a reasonably accurate picture of syphilis screening practices in Africa. A series of assumptions were needed to generate estimates of the missed opportunities, any of which could lead to errors. We assume that having active syphilis in pregnancy is pathogenic, although only observational data have been presented for this assumption.2 The precise level of risk to infants of active syphilis infection is difficult to measure, since the risk depends on the length of time that the mother has been infected as well as the stage of infection and the gestation of the pregnancy when treatment is provided. We base our assumptions on 100% effectiveness of testing; however, false negatives do occur, especially among early infections. A high proportion of false negatives would reduce the number of women among those screened who are detected. We did not take into account false negative laboratory results caused by early syphilis infection or poor quality testing; a high proportion of false negative results could reduce the potential to prevent adverse outcomes. Nevertheless, our estimates are consistent with what is currently known about gestational syphilis, its risks, its diagnosis in common practice, and efficacy of treatment. Despite some uncertainties, it is clear that a substantial unmet need for syphilis screening and treatment exists. According to WHO/CDC estimates, 58% of pregnancies with active gestational syphilis will suffer adverse foetal outcomes (stillbirth, third trimester abortion and congenital syphilis). By our rough calculations, every year approximately 600 000 opportunities are missed to reduce adverse foetal and infant outcomes due to maternal syphilis infection in sub-Saharan Africa. These estimates, however imprecise, suggest perinatal wastage on a substantial scale. Although the benefits are substantial, the cost of antenatal syphilis screening is low. The cost of the screening tests (RPR) for each woman is approximately US$0.20.5 Treatment of RPR-positive women (and their partners) with benzathine penicillin is very effective and costs about US$1.00 per dose. The cost per death or adverse event prevented with antenatal syphilis screening is comparable to the highest predicted mortality reduction from other interventions, including immunization programmes. A study in The Gambia estimated the cost of immunization per childhood death prevented to be approximately US$41, US$100 and US$153 for measles, pertussis and neonatal tetanus, respectively. By comparison, in most of sub-Saharan Africa, US$12 would avert an adverse outcome associated with syphilis during pregnancy, taking into account the costs of screening and the drug treatment.5 At a national level, the fact that most respondents were from STD, statistics or epidemiogy units of the MOH rather than maternal health units suggests that antenatal syphilis screening may be less a priority of the MCH section than of the STD sector. Most antenatal care norms include a long list of interventions and risk assessment with little prioritization of these activities. Few countries have clear strategies of how these many interventions are to be carried out in low resource settings. Syphilis screening is usually not a high priority and, like many other antenatal norms, is carried out sporadically. In areas with limited resources, programmes which are not viewed as important or which do not have explicit targets tend to be placed at a low priority by peripheral health workers who have many other competing demands. In light of the potential importance of antenatal syphilis screening, this intervention is clearly accorded inadequate priority. International donor agencies infrequently make Antenatal syphilis screening in Africa explicit reference to syphilis screening in their lists of priority interventions in antenatal care. Donor funding for antenatal syphilis screening is minimal. The recent trend promoting screening of STIs during pregnancy may refocus efforts on syphilis screening. However, syphilis screening per se should be emphasized in countries with high prevalence, since the other common STIs usually represent less serious problems and are much more difficult to screen and treat. The authors suggest the following to re-prioritize antenatal syphilis screening and treatment within current health programmes. The following measures need to be applied in any country where syphilis prevalence is high. • Establish antenatal syphilis screening as a clearly identified priority. Syphilis screening should be identified as one of the three or four principal interventions of antenatal care with strategies developed to carry it out. • Develop systems to assure that adequate stocks of syphilis screening tests and treatment are available and distributed to appropriate health facilities. This implies allocation of adequate resources for supplies, logistics and training. If syphilis screening were carried out in all pregnant women, current stocks of VDRL/RPR tests and penicillin would be inadequate in most countries. • Promote early attendance at antenatal care and publicize the existence of syphilis screening and treatment as an incentive to come early. • Reduce costs of testing and treatment for pregnant women. • Strengthen methods to improve contact tracing and treatment for partners. • Establish clear indicators and targets for adequacy of screening and mechanisms for monitoring the achievement of these indicators at the health facility level, using methods proven successful in immunization programmes. Antenatal syphilis is not just a problem of sub-Saharan Africa. Recent reports suggest that syphilis prevalence may be of a similar order of magnitude in some countries in Asia, Latin America and the Caribbean.16 In our survey, respondents from outside of sub-Saharan Africa estimated syphilis prevalence ranging from 0.16–14.5%. The highest figures emanated from Asia and Eastern Europe, where country estimates were as high as 8 and 14.5%, respectively. The cost of antenatal syphilis screening and treatment is well within the means of most, if not all, developing countries. Donor agencies can provide direction and start-up funds to initiate activities, with ministries of health mustering the political will to maintain them as priorities. This study suggests that the impact on the health of infants and their mothers will be enormous. 33 Non-treponemal tests are widely available and relatively inexpensive; however, their effectiveness is limited by lack of sensitivity in early and late syphilis and by false-positive reactions. Treponemal tests are more expensive, but have higher sensitivity and specificity than non-treponemal tests. References 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 Schulz KF, Cates W Jr, O’Mara PR. Pregnancy loss, infant death, and suffering: legacy of syphilis and gonorrhea in Africa. Genitourinary Medicine 1987; 63: 320–5. McDermott J, Steketee R, Larsen S, Wirima J. Syphilis-associated perinatal and infant mortality in rural Malawi. Bulletin of the World Health Organization 1993; 71: 773–80. Gelmon LJ, Piot P. The interactions between HIV and other sexually transmitted infections. In: Mann J, Tarantola D (eds). AIDS in the world II. New York: Oxford University Press, 1996: 99. Hutchinson CM, Rompalo AM, Reichart CA, Hook EW. Characteristics of patients with syphilis attending Baltimore STD clinics. Archives of Internal Medicine 1991; 151: 511–6. Schulz KF, Schulte JM, Berman SM. Maternal health and child survival: opportunities to protect both women and children from the adverse consequences of reproductive tract infections. In: Germain A et al. (eds). Reproductive tract infections. New York: Plenum Press, 1992. Grosskurth H, Mosha F, Todd J et al. Impact of improved treatment of sexually transmitted diseases on HIV infection in rural Tanzania: randomised controlled trial. Lancet 1995; 346: 530–6. UNICEF. The state of the world’s children, 1995. Oxford: Oxford University Press, 1995. Macro International, Demographic and Health Services Internet Web Site, 1998: http://www.macroint.com/dhs/ WHO. Report of WHO consultation on maternal and perinatal infections, 28 November–2 December 1988. WHO/MCH/91.10. Geneva: World Health Organization, 1991. WHO. Coverage of maternity care: A listing of available information. WHO/RHT/MSM/96.28. Geneva: World Health Organization, 1997. De Schryver A, Meheus A. Epidemiology of sexually transmitted diseases: the global picture. Bulletin of the World Health Organization 1990; 68: 639–54. Over M, Piot P. HIV Infection and Sexually Transmitted Diseases. In: Jamison DT, Mosley WH, Measham AR, Bobadilla JL (eds). Disease control priorities in developing countries. Washington DC: Oxford University Press for IBRD/WB, 1993: 458. Tsui AO, Wasserheit JN, Haaga JG. Reproductive health in developing countries: expanding dimensions, building solutions. Washington DC: National Academy Press, 1997: 46. Tramont EC. Treponema Pallidum. In: Mandell G, Bennett J, Dolin R (eds). Mandell, Douglas and Bennett’s principles and practices of infectious disease. New York: Church, Livingstone Inc., 1995. Lafort Y, Seunda M, Floriano F, Gloyd S. Evaluation of screening for syphilis and high risk pregnancy in prenatal clinics of Mozambique. Presentation at IX Jornadas de Saude, Maputo, Mozambique, December 13–16, 1994. UNAIDS. Global prevalence and incidence of selected curable sexually transmitted diseases: overview and estimates. WHO/ GPA/STD/95.1. Geneva: UNAIDS, 1995. Biographies Endnotes i VDRL = Veneral Disease Research Laboratory test; RPR = Rapid Plasma Reagin test; FTA = Fluorescent Treponemal Antibody test; TPHA = Treponema Pallidum Hemaglutination test. These tests are all serological, either treponemal (FTA, TPHA), which test for presence of antibody to the syphillis organism, or nontreponemal (VDRL, RPR), which test for presence of antibodies to other substances present in the sera of patients infected with syphilis. Stephen Gloyd, MD, MPH, is an Associate Professor in the Department of Health Services at the School of Public Health and Community Medicine at the University of Washington (UW), as well as the Director of the UW International Health Program. He is also Project Director of Health Alliance International (HAI), a Seattlebased non-governmental organization with health-related projects in Africa and Asia. His research interests are in primary health care systems; programme evaluation; rapid assessment methods; and the 34 Stephen Gloyd et al. epidemiology and control of measles, tuberculosis, diarrhoea and HIV. Steve has experience in Mozambique, Somalia, Honduras, Mexico, Zimbabwe, Côte d’Ivoire and Swaziland. Sanders Chai, MD, is an Acting Instructor in the Department of Pediatrics at the University of Washington School of Medicine and a Senior Fellow in the Department of Environmental Health in the School of Public Health and Community Medicine. He is currently conducting research in Vietnam and Nicaragua on environmental risk factors for children’s respiratory health. He also sits on several local and national committees on children’s environmental health and childcare health. A board certified pediatrician and board eligible occupational and environmental medicine physician, Dr Chai has had experience in India implementing a TB control programme and in Vietnam conducting course work for the Ministry of Health. Mary Anne Mercer, DrPH, MPH, is a Lecturer with the Department of Health Services at the School of Public Health and Community Medicine at the University of Washington. She is also Deputy Director of Health Alliance International (HAI), a Seattle-based nongovernmental organization with health-related projects in Africa and Asia. Her research interests are in the design, management, training and evaluation for community-based maternal–child health programmes, including primary health care and programmes responding to HIV/AIDS. Mary Anne has an additional focus on the social and economic determinants of health status, and has experience in Nepal, Thailand and East and Southern Africa. Correspondence: Stephen Gloyd, Department of Health Services, Box 357660, University of Washington School of Public Health and Community Medicine, Seattle, WA 98195, USA.