Public Health Reviews
Questionnaires for rapid screening of schistosomiasis in sub-Saharan Africa
Christian Lengeler,1 Jürg Utzinger,2 & Marcel Tanner3
Abstract New initiatives are aiming to reduce the global burden of schistosomiasis, mainly through the large-scale application of chemotherapy. To target chemotherapy effectively, rapid assessment procedures are needed for identifying high-risk communities that are foci for the disease. In this review, we examine the development and validation of simple school questionnaires for screening communities for Schistosoma haematobium and S. mansoni rapidly and inexpensively. The focus is on sub-Saharan Africa, where 85% of the current schistosomiasis burden is concentrated.
For more than a decade, the questionnaire approach has been validated in 10 countries, with 133 880 children interviewed in 1282 schools, and with 54 996 children examined for S. haematobium. The questionnaires were well accepted, highly reliable, and of low cost. The success of the questionnaires is explained by the fact that S. haematobium infections were easily perceived through the presence of blood in urine.
Evidence from 48 258 children interviewed in 545 schools indicated that reported blood in stools and bloody diarrhoea are valuable indicators for community diagnosis of S. mansoni. However, the diagnostic performance of the questionnaires for S. mansoni was weaker than for S. haematobium, and although these results are encouraging, the questionnaires need additional validation. Recently, questionnaires were extended from community to individual diagnosis and showed considerable promise. Questionnaires are now available for promptly defining the magnitude of schistosomiasis in a large area, which will allow limited resources for morbidity control to be allocated optimally.
Keywords Schistosomiasis haematobia/diagnosis; Schistosomiasis mansoni/diagnosis; Risk assessment; Questionnaires; Africa South of the Sahara (source: MeSH, NLM).
Mots clés Schistosomiase urinaire/diagnostic; Schistosomiase intestinale/diagnostic; Evaluation risque; Questionnaires; Afrique subsaharienne (source: MeSH, INSERM).
Palabras clave Esquistosomiasis haematobia/diagnóstico; Esquistosomiasis mansoni/diagnóstico; Medición de riesgo; Cuestionarios, Africa del Sur del Sahara (fuente: DeCS, BIREME).
Introduction
Schistosomiasis is a widespread parasitic disease of the tropics that places an enormous toll on the public health of affected regions. Of the 200 million people infected worldwide, 85% of the burden is concentrated in Africa south of the Sahara (1, 2). In most epidemiological settings, the intermediate host snails cannot be controlled by cost-effective interventions, and in the absence of a vaccine, schistosomiasis control largely relies on chemotherapy, with praziquantel as the drug of choice (1). An important feature of the disease is its focal distribution (3). This results in a patchy distribution of risk, and communities across a region or country do not attach the same importance to schistosomiasis. Praziquantel is therefore not required everywhere and proper targeting is crucial, given the limited resources and the many other problems facing primary health care systems in sub-Saharan Africa.
The first step in targeting health interventions is to map the disease geographically and rank it according to the risk of infection and morbidity. In 1987, the first attempt to systematically map schistosomiasis on a global scale resulted in the Atlas of the global distribution of schistosomiasis (4). A more recent effort using geographical information systems highlighted the scarcity of data for Africa (5), and underscored the need for a rapid and inexpensive epidemiological assessment tool that can be fully integrated within existing administrative systems. Such a tool, relying on simple school questionnaires, was developed more than a decade ago for Schistosoma haematobium and has since been validated in a variety of ecological, epidemiological, and sociocultural settings across sub-Saharan Africa. More recently, the approach was extended to S. mansoni and its validity assessed in several large-scale studies.
This article is a comprehensive review of the experiences and evidence from sub-Saharan Africa with questionnaires for rapidly screening for schistosomiasis. The questionnaires can be used at both community and individual levels, and this approach allows communities with a high risk of schistosomiasis to be identified. Resources for controlling the parasite can thus be allocated in a more cost-effective way (6). We also discuss how this tool will contribute to a more sustainable and integrated system of control of schistosomiasis.
Questionnaires for diagnosing Schistosoma haematobium infection at a community level
The presence of blood in urine (haematuria) has been associated with S. haematobium infection since ancient times, but its use as an indirect indicator for this parasite was first investigated only two decades ago, in a study that simply asked community members living in Ghana and Zambia about their history of haematuria. These studies showed that haematuria was promising as an indirect indicator, but there was considerable variation in its diagnostic performance between the two settings (7).
Urinary schistosomiasis as illness was well perceived and correlated with infection in a rural community of the Kilombero District in the United Republic of Tanzania in the mid-1980s (8, 9). As a result, a district-wide study that emphasized rapid and inexpensive community diagnosis was initiated in 1986. The study aimed to identify high-risk communities, rather than infected individuals, because the highest priority for control was to target praziquantel chemotherapy in areas at greatest risk. A simple questionnaire that asked respondents whether they had experienced any of eight symptoms and eight diseases common in the area was developed and administered to all primary schools through the existing education system (10). The key features of this questionnaire are described in Box 1 (11, 12). Within six weeks, 75 of 77 schools returned completed questionnaires with a total of 6772 children interviewed. A mobile laboratory team then visited 56 schools for parasitological validation.
A comparison between the questionnaires and the parasitological data revealed a striking correlation. The percentage of positive answers to the two key questions "Did you have blood in urine during the last month?" and "Did you suffer from schistosomiasis during the last month?" showed significant positive associations with the prevalence of S. haematobium (for both questions: r = 0.90, P S. haematobium was of high importance and correctly excluded those schools where the parasite was less of a problem (Table 1). The questionnaire approach was also rapid and cost 20-fold less than standard parasitological examinations.
In 1988, the questionnaire approach was successfully replicated in the neighbouring district of Kilosa. In this study, biomedical validation of the questionnaires was carried out by teachers who were trained in reagent-stick testing during a one-day workshop. The questionnaire showed an excellent diagnostic performance with high predictive values (Table 1). The study confirmed that the questionnaire approach was rapid and low-cost (14).
Between 1990 and 1992, a multicountry initiative was carried out to validate the questionnaire approach more extensively. The initiative was supported financially by the United Nations Development Programme/World Bank/WHO Special Programme for Research and Training in Tropical Diseases (TDR), and it used a standardized questionnaire in areas that were endemic for S. haematobium and that had many different ecological and sociocultural features. The participating countries were Cameroon, Congo, Democratic Republic of the Congo, Ethiopia, Malawi, Zambia, and Zimbabwe (13, 16, 17, 20, 21). More recently, similar questionnaires were validated in Côte d'Ivoire (19), Nigeria (18), and in the Magu and Muheza districts of the United Republic of Tanzania (15, 22, 23).
In summary, a total of 133 880 children were interviewed in 1282 schools, and 54 996 children were screened using urine filtration and/or reagent-stick testing. In all countries except one, questionnaires proved to be accurate, well accepted, operationally feasible (school return rates: 75100%), and of low-cost (Table 1). Positive predictive values ranged from 31% to 92% (median: 71%) and negative predictive values from 75% to 100% (median: 89%). The school system proved to be outstanding for this task, despite sociopolitical crises and conflicts in some of the countries. Ethiopia was the only country where the diagnostic performance of the questionnaire was deemed insufficient for large-scale application (although the results for the question "Did you have pain while urinating?" were moderately good). This was explained by the low awareness of schistosomiasis (the study population had recently immigrated from non-endemic highlands) (13, 21).
At country level, there was also a strong relationship between the overall prevalence of S. haematobium and the percentage of positive answers to "Did you have blood in urine?" and "Did you have schistosomiasis?". Regression analysis of 12 studies carried out in Africa revealed a highly significant correlation between the overall prevalence of S. haematobium and the prevalence of reported blood in urine (r = 0.90, P Fig. 1a), as well as reported schistosomiasis (r = 0.88, P Fig. 1b).
In most settings, a second questionnaire aimed at teachers was distributed with the questionnaire addressed to children. In the United Republic of Tanzania, a third questionnaire was addressed to community leaders (10). The questionnaires for teachers and community leaders inquired about priorities among health problems, as well as the priority of health among other issues in the community. This simple approach clearly demonstrated the proposed link between schistosomiasis endemicity and its priority for control (13, 24). Interestingly, the threshold at which schistosomiasis became a top health priority (rank: 13) was around an infection prevalence of 50%, which is also the high-endemicity threshold suggested by WHO (25).
Questionnaires for diagnosing Schistosoma haematobium infection in individuals
Recent studies investigated whether the questionnaire approach could be adapted for diagnosing S. haematobium in individuals, to see if chemotherapy could be targeted more selectively. Recent evidence from Egypt, Ghana, Nigeria, and the United Republic of Tanzania suggested that reported blood in urine and reported schistosomiasis were also useful indicators for individual infection status (10, 15, 22, 23, 2629). Although questionnaires alone missed a significant proportion of infected children, most of those missed had light infections, so this might not be a problem for a morbidity control programme.
Two studies carried out in the United Republic of Tanzania observed that girls were more likely to be missed than boys (15, 23). This confirmed previous reports of underreporting of blood in urine and schistosomiasis by girls at school level from Cameroon, the Democratic Republic of the Congo, and Malawi (13), and from the island of Pemba, United Republic of Tanzania (30). As a result, the sensitivity and specificity of questionnaires may differ by sex (15, 23), just as it may differ by age and overall endemicity. These factors need to be taken into account when planning large-scale screening, and appropriate questionnaire cut-offs should be selected.
Finally, it is unclear how the questionnaire approach would work over time. For example, once the children become aware that receiving treatment depends on the answer to a single question, the potential for response bias is obviously high.
Schistosoma mansoni illness
For intestinal schistosomiasis due to S. mansoni there are no simple, sensitive, and specific signs or symptoms. Several epidemiological and hospital-based studies have been carried out in sub-Saharan Africa to relate clinical symptoms and perceived morbidity indicators to S. mansoni infection. Study participants were usually interviewed with a standardized clinical questionnaire, followed by the examination of one or more stool specimens to assess infection intensity. These studies found that S. mansoni infections (especially those which were moderate and heavy) were frequently associated with abdominal pain, blood in stool, (bloody) diarrhoea, colicky cramps, hepatomegaly, and splenomegaly (31, 32). The most consistent finding was the association between a recent history of blood in stools and an S. mansoni infection, especially in individuals with more than 100 eggs/g stool (3344).
We reanalysed the data of these previous studies and found the diagnostic performance of reported and/or observed blood in stool had a low-to-moderate sensitivity (766%, median: 16%) and usually a high specificity (5496%, median: 94%). These factors resulted in a moderate-to- high positive predictive value for blood in stool (2088%, median: 64%) and in general a moderate negative predictive value (3295%, median: 59%) (Table 2). There was considerable variation in the results, which may have stemmed from factors such as the overall prevalence and intensity of infection, individual disease perception and the reference diagnostic techniques used for validation. In two studies, a significant association was also found between reported bloody diarrhoea and S. mansoni (45, 46). For practical applications, the low sensitivity of this approach is a concern, although it remains to be seen what percentage of heavy infections can be detected.
Questionnaires for diagnosing Schistosoma mansoni in a community
Given the findings on S. mansoni above, and in view of the wide distribution and public health significance of S. mansoni, it was essential to develop and validate questionnaires for rapidly screening for this species. In the first study, in an area of the Democratic Republic of the Congo with mixed S. haematobium and S. mansoni infections, the correlation between the prevalence of reported blood in stools and S. mansoni was moderate, with an adjusted correlation coefficient of 0.33 (P13, 20). Interestingly, the adjusted correlation coefficient was much better for reported schistosomiasis (r = 0.61, PTable 3).
Following a promising pilot study carried out in 10 schools in Ethiopia (49), a large-scale study was initiated in the Gondar region, which found an excellent diagnostic performance for both reported blood in stools and schistosomiasis (44) (Table 3). Another study was carried out in 30 schools of the Morogoro rural district of the United Republic of Tanzania (26), but since only two schools had an S. mansoni prevalence above 10%, the results are not reported here.
A series of studies were carried out in western Côte d'Ivoire, in an area known to be endemic for S. mansoni. A pilot study in three villages investigated common signs and symptoms by conducting focus group discussions with the most heavily infected children. Blood in stool and bloody diarrhoea were perceived as common symptoms, with three specific terms for these two symptoms known in the vernacular language. Comparisons between children's responses and their S. mansoni infection levels revealed that reported blood in stools showed the best diagnostic performance, especially for those children with more than 100 eggs/g stool (38). These findings were subsequently integrated into a large-scale screening. The percentage of positive answers to "Did you have blood in stool during the last month?" and "Did you have bloody diarrhoea during the last month?" were significantly associated with the prevalence of S. mansoni infection, but the diagnostic performance of these symptoms was only moderate (47).
Finally, a recent study in Kenya collected pairwise questionnaire and parasitological data from 46 schools. The results confirmed that reported blood in stools was significantly correlated with the prevalence of S. mansoni infection (48), but the diagnostic performance was only moderate (Table 3), in accordance with previous findings from Côte d'Ivoire (47).
In summary, 48 258 children were interviewed for the presence of S. mansoni in 545 schools, using simple questionnaires. The diagnostic performance of the questionnaires was weaker for S. mansoni than for S. haematobium, and although the results are encouraging, additional validation is needed before this approach can be used in a given setting.
Extensions of the questionnaire approach
The results described inspired more work in sub-Saharan Africa, South America, and Asia that focused on detecting high-risk individuals. It was suggested that questionnaires for S. mansoni screening might be improved by adding a wider range of risk factors for infection, such as migratory status, frequency and nature of water-contact patterns, and history of previous schistosomiasis treatment. This approach was undertaken in Brazil (5053) and has recently been extended to Egypt (29), Côte d'Ivoire (54), and Kenya (48). The studies showed that the questionnaire approach had good potential for identifying infected individuals, but the questions were often very specific for a particular setting and their generalization remains questionable. Potentially useful, however, are recent findings from Kenya that schools located less than 5 km from the shore of Lake Victoria were at high risk for S. mansoni infection (prevalence >50%), whereas schools further away normally had lower infection prevalences (48). In China, a similar approach to screening for S. japonicum in schoolchildren showed a high sensitivity (86%) and specificity (98%), and the high-risk schoolchildren were identified by only three simple yes/no questions (concerning frequent water contact, frequent weakness, and frequent diarrhoea). If successfully validated in other endemic areas, this approach might be more widely applied in Chinese schistosomiasis control programmes (55).
Implications for schistosomiasis control
Questionnaires to screen for communities at highest risk of S. haematobium and/or S. mansoni infection in sub-Saharan Africa are well accepted and operationally feasible, and are faster and less expensive than standard parasitological diagnoses. They build directly on a community's perception of disease, involve the active participation of teachers and schoolchildren, and represent a first step towards involving the community in control activities. A ranked list of schools allows the schistosomiasis risk to be mapped and communities prioritized for control activities. From there, one approach is to decide on the number of schools or communities that will benefit from treatment, taking into account overall available resources. Another possibility is to define an intervention threshold, such as the prevalence of reported blood in urine of >30% (which often corresponds to an S. haematobium infection prevalence of >50%). When prevalence exceeds 50%, all schools or communities would benefit from specific control measures, for example, universal treatment with praziquantel (25).
The evidence for using questionnaires to screen for S. haematobium is now compelling and guidelines have been developed for district health managers (12). Despite the extensive validation, it is still recommended that the diagnostic performance of questionnaires be assessed on a limited scale, either when the questionnaire has been significantly altered or when health authorities need to be convinced about the usefulness of this method (12).
The use of large-scale screening with questionnaires to diagnose S. mansoni infections in a community could now be considered, but should always be undertaken after a validation step in the selected setting. Blood in stools, bloody diarrhoea, and suffering from schistosomiasis are valuable markers and can be recommended for screening. Other questions that are relevant to the setting, such as the distance from the lakeshore in the Kenyan study (48), should always be considered.
A largely unexplored issue is the performance of the questionnaires in areas with mixed S. haematobium/S. mansoni infections since the answers to the question "Did you have schistosomiasis during the last month?" will be influenced by both infections. These areas represent a significant part of the African continent (4). This issue should always be explored first using available information, either from previous studies or from available health statistics. A simple way to investigate for mixed infections with questionnaires is to plot the answers to "Did you have schistosomiasis during the last month?" against those for "Did you have blood in urine during the last month?". In the presence of S. mansoni infections, the usual tight linear relationship will be altered by schools with a much higher percentage of reported "schistosomiasis" than would be expected, as has been demonstrated in the Democratic Republic of the Congo (20).
Using questionnaires for programme monitoring is another application that has yet to be explored. It is difficult to predict how well questionnaires can work for this purpose, since effective control through chemotherapy will affect the prevalence and morbidity patterns. On Pemba Island, for example, repeated treatment substantially reduced the level of measured and perceived haematuria over two years, and this followed a similar decline in infection rates (56).
Conclusions
We have presented the successful development of a rapid assessment procedure that has public health significance. It is important to highlight the long time required for thorough validation. Development and validation of questionnaires has taught us much about how schistosomiasis is perceived by affected individuals and communities, and confirmed that the priority given to the disease is highly dependent on endemicity and morbidity. Questionnaires are now readily available for rapidly screening for schistosomiasis. We believe that novel large-scale control initiatives will find this tool useful as a first step towards defining the distribution and magnitude of the problem, and improving the implementation of control measures by an evidence-based process of resource optimization. 
Acknowledgements
Most studies reviewed here received financial support from the United Nations Development Fund/World Bank/WHO Special Programme for Research and Training in Tropical Diseases (TDR). CL acknowledges support by the Swiss National Science Foundation (PROSPER grant 32-41632.94). JU is grateful to the Swiss National Science Foundation and the Centre for Health and Wellbeing at Princeton University.
Conflicts of interest: none declared.
Résumé
Questionnaires pour le dépistage rapide de la schistosomiase en Afrique subsaharienne
De nouvelles initiatives visent à réduire la charge mondiale de la schistosomiase, essentiellement par l'application de la chimiothérapie à grande échelle. En vue d'un ciblage efficace de la chimiothérapie, il est nécessaire de disposer d'une méthode d'évaluation rapide pour identifier les communautés à haut risque qui constituent des foyers de la maladie. Dans le présent article, nous examinons l'établissement et la validation de questionnaires scolaires simples destinés à dépister de façon rapide et peu coûteuse les infections à Schistosoma haematobium et à S. mansoni dans la communauté. Ces questionnaires s'adressent surtout à l'Afrique subsaharienne, qui regroupe actuellement 85 % de l'ensemble des cas de schistosomiase.
Depuis plus de dix ans, l'approche par questionnaire a été validée dans dix pays, avec 133 880 enfants interrogés dans 1282 écoles et 54 996 examinés à la recherche de S. haematobium. Les questionnaires étaient bien acceptés, fiables et de faible coût. Le succès de l'utilisation des questionnaires s'explique par le fait que les infections à S. haematobium sont facilement perçues par la présence de sang dans les urines.
D'après les données recueillies auprès de 48 258 enfants interrogés dans 545 écoles, la mention de la présence de sang dans les selles et celle de diarrhées sanglantes sont des indicateurs valables en ce qui concerne le diagnostic des infections à S. mansoni dans la communauté. En revanche, la valeur diagnostique des questionnaires était moins bonne pour S. mansoni que pour S. haematobium, et malgré des résultats encourageants, les questionnaires auraient besoin d'un complément de validation. Récemment, des questionnaires ont été étendus au diagnostic individuel et semblent très prometteurs à cet égard. Il existe maintenant des questionnaires pour déterminer rapidement l'importance de la schistosomiase dans une région de grande étendue, ce qui permettra de répartir de façon optimale les resources limitées attribuées à la lutte contre la morbidité.
Resumen
Cuestionarios para el cribado rápido de la esquistosomiasis en el África subsahariana
Una serie de nuevas iniciativas tienen por objeto reducir la carga mundial de esquistosomiasis, principalmente mediante la aplicación de antibioticoterapia en gran escala. A fin de enderezar con precisión los esfuerzos de tratamiento antibiótico, se necesitan procedimientos de evaluación rápida para identificar las comunidades de alto riesgo que actúen como focos de la enfermedad. En el presente análisis examinamos el desarrollo y validación de cuestionarios escolares sencillos concebidos para el cribado rápido y económico de las comunidades en lo que respecta a la presencia de Schistosoma haematobium y S. mansoni. El centro de interés es el África subsahariana, donde se concentra el 85% de la actual carga de esquistosomiasis.
Durante más de una década, el método de los cuestionarios se ha validado en 10 países, habiéndose alcanzado la cifra de 133 880 niños entrevistados en 1282 escuelas, y de 54 996 niños examinados para detectar S. haematobium. Los cuestionarios tuvieron buena aceptación y fueron una herramienta altamente fiable y de bajo costo. Su éxito se explica por el hecho de que las infecciones por S. haematobium se detectaban fácilmente mediante la presencia de sangre en la orina.
Los datos aportados por 48 258 niños entrevistados en 545 escuelas muestran que las referencias a la presencia de sangre en las heces y de diarrea sanguinolenta son indicadores valiosos para el diagnóstico comunitario de S. mansoni. Sin embargo, la eficacia diagnóstica de los cuestionarios para S. mansoni fue menor que para S. haematobium. Aunque estos resultados son alentadores, es necesario validar mejor los cuestionarios. Recientemente se ha ampliado el uso diagnóstico de los cuestionarios del nivel comunitario al nivel individual, con resultados bastante prometedores. Disponemos ahora de cuestionarios que nos permiten determinar rápidamente la magnitud del problema de la esquistosomiasis en un área extensa, lo que permitirá asignar de forma óptima los limitados recursos disponibles para combatir la morbilidad.
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1 Project Leader, Swiss Tropical Institute, Department of Epidemiology and Public Health, PO Box, CH-4002 Basel, Switzerland (email: christian.lengeler@unibas.ch). Correspondence should be addressed to this author.
2 Visiting Research Fellow, Princeton University, Office of Population Research, Princeton, NJ 08544, USA.
3 Professor and Director of the Swiss Tropical Institute, Basel, Switzerland.
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