RESEARCH
Preventing trachoma through environmental sanitation: a review of the evidence base
Prévention du trachome par lassainissement de lenvironnement : analyse des faits
Prevención del tracoma mediante el saneamiento ambiental: examen de la base científica
A. PrüssI; S.P. MariottiII
ITechnical Officer, Water, Sanitation and Health, Protection of the Human Environment, World Health Organization, 1211 Geneva 27, Switzerland
IIMedical Officer, Prevention of Blindness and Deafness, Injury Prevention and Rehabilitation, World Health Organization, Geneva, Switzerland
ABSTRACT
A review of the available evidence for the associations between environmental sanitation and transmission of trachoma was undertaken with a view to identifying preventive interventions. The WHO Global Alliance for the Elimination of Trachoma by the Year 2020 (GET2020) has adopted the SAFE strategy, consisting of four components: Surgery, Antibiotic treatment, promotion of Facial cleanliness and initiation of Environmental changes.
This review of 19 studies selected from the 39 conducted in different parts of the world shows that there is clear evidence to support the recommendation of facial cleanliness and environmental improvements (i.e. the F and E components of the SAFE strategy) to prevent trachoma. Person-to-person contact and flies appear to constitute the major transmission pathways. Improvement of personal and community hygiene has great potential for a sustainable reduction in trachoma transmission. Controlled clinical trials are needed to estimate the relative contribution of various elements to the risk of transmission of trachoma and the effectiveness of different interventions. These could show the relative attributable risks and effectiveness of interventions to achieve improvement of personal hygiene and fly control by environmental improvements, alone or in combination, and with or without antibiotic treatment.
Keywords: clinical trials; cross-sectional studies; evidence-based medicine; sanitation; trachoma, prevention and control, and transmission
RÉSUMÉ
Cet article passe en revue les éléments qui plaident en faveur dune association entre lassainissement de lenvironnement, lhygiène, et la transmission du trachome, dans lintention didentifier des interventions à but préventif. LAlliance OMS pour lElimination mondiale du Trachome dici 2020 a adopte la stratégie « CHANCE », qui comporte quatre éléments : CHirurgie du trichiasis, traitement Antibiotique des cas de trachome évolutif, Nettoyer le visage pour prévenir la transmission de la maladie et Changer lEnvironnement.
On a examiné 19 études spécialement choisies parmi les 39 effectuées entre 1958 et 1998 dans différentes parties du monde. Ces études ont été répertoriées dans MEDLINE EXPRESS (1966-1999) et HEALTHSTAR (1988-1999). Les références citées dans ces articles ont également été étudiées. La recherche na pas été limitée aux articles rédigés en anglais.
On trouvera également dans le présent article un cadre servant a` lévaluation de limpact de lassainissement de lenvironnement sur une maladie précise prise comme « cas décole ».
On a mis en évidence un effet protecteur médian contre la transmission du trachome pour les paramètres environnementaux suivants : proximité dune source deau, 27%; quantité deau disponible, 21%; présence de latrines, 24%; collecte des ordures ménagères, 69%; faible densité des mouches ou nombre réduit de mouches sur le visage des enfants, 39%; propreté du visage, 41 %. On a estimé que la densité des mouches et la propreté du visage associées au trachome devaient être moins sujettes à erreur, puisquelles sont plus étroitement impliquées dans les mécanismes de transmission. Des paramètres plus « distants », tels que la disponibilité en eau, la présence de latrines et la collecte des ordures ménagères, ninfluent probablement sur la transmission que de façon indirecte. Par exemple, ils peuvent favoriser une toilette plus fréquente du visage ou réduire les gîtes larvaires et lattraction exercée sur les mouches.
Les études ont été analysées en fonction de leur qualité méthodologique ; celles qui ont été considérées comme «plus précises» ont davantage pesé dans linterprétation des résultats. Le lien de causalité entre le trachome et les « environnements sales » favorisant la prolifération des mouches ou lattraction exercée sur elles est linterprétation la plus vraisemblable que lon puisse faire des résultats, selon les critères de Bradford Hill sur les relation de cause à effet rencontrées pour le trachome dans les études environnementales. Lorsque le visage nest pas propre, ces critères sont remplis, même si les résultats sont moins uniformes. Les résultats expérimentaux nont pas montré un effet constant lorsquon associe lenseignement de lhygiène à une campagne de traitement de masse.
Ces résultats montrent que lon dispose de suffisamment déléments pour recommander la propreté du visage et des interventions sur lenvironnement (à savoir, les éléments N et CE de la stratégie CHANCE) pour prévenir le trachome. Plusieurs études laissent à penser quune diminution de la densité des mouches associée à un enseignement de lhygiène permettent de diminuer la transmission du trachome. Les contacts interpersonnels et les mouches semblent bien constituer les principaux modes de transmission. Lamélioration de lhygiène individuelle et communautaire offre une possibilité importante de réduire durablement la transmission. Le traitement des cas dendémie serait une aide, car il permettrait de réduire le réservoir de germes pathogènes. Il serait utile de mieux connaître la contribution respective des divers éléments qui entrent en jeu dans le risque de transmission du trachome et lefficacité des différentes interventions. Il faudrait procéder à des essais cliniques contrôlés pour déterminer les risques attribuables relatifs et lefficacité des interventions pour ce qui est de parvenir à améliorer lhygiène individuelle et la lutte contre les mouches, quelles soient associées ou appliquées isolément.
On a montré que, outre le fait quelles transmettent le trachome, les mouches étaient porteuses de toutes sortes de germes pathogènes et le fait de diminuer leur population en assainissant lenvironnement pourrait donc permettre dabaisser le nombre de cas dautres maladies dendémie dans la communauté. Lassainissement de lenvironnement dont on sait quil pourrait ainsi contribuer grandement à la prévention du trachome (par exemple en facilitant laccès à leau) est également associé à un large éventail deffets positifs, tant sur le plan sanitaire que social et économique.
RESUMEN
En el presente artículo se analiza la base científica disponible para relacionar el saneamiento ambiental, en particular la higiene, y la transmisión del tracoma; dicho estudio se realizó para identificar medidas preventivas. La Alianza Mundial OMS para la Eliminación del Tracoma para el Año 2020 ha adoptado la estrategia «SAFE», compuesta de cuatro elementos: corrección quirúrgica de la triquiasis tracomática, tratamiento antibiótico de los casos activos, fomento de la higiene facial e introducción de cambios ambientales.
El análisis abarcó 19 estudios específicamente seleccionados de los 39 realizados entre 1958 y 1998 en diferentes partes del mundo. Los estudios se identificaron mediante MEDLINE EXPRESS (1966-1999) y HEALTHSTAR (1988-1999). También se buscaron las referencias citadas en los artículos identificados y la búsqueda no se limitó a los artículos redactados en inglés.
Este artículo facilita asimismo un marco para evaluar los efectos del saneamiento ambiental en una enfermedad concreta tomada como «ejemplo».
Se determinó la mediana del efecto protector en la reducción de la transmisión del tracoma para las siguientes variables ambientales: proximidad del agua, 27%; cantidad de agua disponible, 21%; existencia de letrinas, 24%; recogida de basuras, 69%; baja densidad o bajo número de moscas en la cara de los niños, 39%; e higiene facial, 41%. Se consideró que el número de moscas y la higiene facial eran las variables que menos se prestaban a confusión, dada su mayor implicación en los mecanismos de transmisión. Otras variables «distantes», como la disponibilidad de agua, la existencia de letrinas y la recogida de basuras posiblemente sólo influyen en la transmisión de un modo indirecto. Por ejemplo, pueden fomentar una higiene facial más frecuente o reducir los criaderos y el potencial de atracción de moscas.
Se analizó la calidad metodológica de los estudios, y al interpretar los resultados se dio más importancia a los estudios considerados «más exactos». Conforme a los criterios de Bradford Hill relativos a la causalidad en estudios ambientales, la interpretación más probable de los resultados es que existe una relación causa-efecto entre los «ambientes sucios» que fomentan la proliferación de moscas o atraen a estos insectos y el desarrollo de tracoma. Estos criterios de causalidad se cumplen igualmente en el caso de la falta de higiene facial, aunque los resultados son menos coherentes. Diversos resultados experimentales no han mostrado un efecto coherente en respuesta a la inclusión de medidas de educación sobre higiene en una campaña de tratamiento masivo.
Estos resultados revelaron que existen pruebas suficientes para apoyar la recomendación de fomentar la higiene facial y los cambios ambientales (los dos últimos componentes de la estrategia SAFE) a fin de prevenir el tracoma. Algunos estudios llevan a pensar que la reducción de la densidad de moscas y la educación sobre higiene conducen a la disminución de la transmisión del tracoma. El contacto personal y las moscas parecen ser las principales vías de transmisión. La mejora de la higiene personal y comunitaria posiblemente contribuye a la reducción sostenible de la transmisión. El tratamiento de los casos endémicos ayudaría a reducir el reservorio de patógenos. Convendría conocer más a fondo las contribuciones relativas de los diversos factores al riesgo de transmisión del tracoma, así como la eficacia de las diferentes intervenciones. Es preciso realizar ensayos clínicos controlados para determinar los riesgos relativos imputables y la eficacia de las intervenciones orientadas a mejorar la higiene personal y la lucha contra las moscas, ya se emprendan por separado o en conjunción.
Además de transmitir el tracoma, las moscas han demostrado ser portadoras de una gran diversidad de patógenos, por lo que la reducción de su densidad, mediante mejoras ambientales, puede ayudar a reducir otras enfermedades endémicas en la comunidad. Las mejoras ambientales que han demostrado contribuir considerablemente a la prevención del tracoma (como el acceso al agua) también se asocian con una gran variedad de beneficios sanitarios, sociales y económicos.
Introduction
This review of the available evidence for the associations between environmental sanitation and hygiene and transmission of trachoma was undertaken with a view to identifying preventive interventions. Trachoma is an infection of the eye caused by Chlamydia trachomatis, which may result in blindness after repeated reinfections. The disease remains the main cause of preventable blindness globally (1). WHO has therefore initiated a Global Alliance for the Elimination of Trachoma by the Year 2020 (GET2020). The alliance has adopted the SAFE strategy, consisting of four components to give a combined medical, behavioural and environmental approach: Surgery of trachomatous trichiasis; Antibiotic treatment of active cases; promotion of Facial cleanliness; and initiation of Environmental changes to reduce the transmission of trachoma.
The association between personal and environmental sanitation and hygiene and trachoma transmission has been noted previously (24). There is, however, still the need to investigate the role played by poor personal and environmental hygiene in the light of recent studies, and to guide the F and E components of the SAFE strategy.
This article also establishes a framework for assessing the impact of environmental sanitation on a specific disease, providing a case example of how environmental factors may influence disease transmission and control.
Literature search
Studies were identified through MEDLINE EXPRESS (196699) and HEALTHSTAR (199099). The keywords used for the searches included trachoma, hygiene, education, sanitation, face-washing, water, latrine, toilet, environment, flies and Musca. The searches were not restricted to English language articles. References cited in identified studies were checked for additional articles. Literature mentioned at the Third Meeting of the WHO Global Alliance for the Elimination of Trachoma (1920 October 1998) was also included. Finally, three reviews undertaken about 10 years ago were checked for further studies.
Mechanisms of trachoma transmission
The literature was searched as described above for information on all transmission mechanisms for trachoma and the relative importance of transmission pathways. Relatively few publications were found on the role of flies (58). One study investigated the effect on trachoma transmission of reducing the fly population (9). The main findings were as described below.
The secretions of the eyes of infected persons contain the infective agent, C. trachomatis (7).
The transmission of C. trachomatis by the housefly, Musca domestica, and by M. sorbens is possible under laboratory conditions (5, 8).
Chlamydiae can be isolated from flies feeding at the eyes of children; although one reference did not specify the type of fly (5), another specified that the most likely insect vector was M. sorbens (9).
These findings indicate that flies are probably involved in trachoma transmission. Several types of flies may be implicated; the relative importance of each may vary according to region (6).
Several results reported by epidemiological studies also support the involvement in transmission of direct contact and personal hygiene, measured through factors such as crowding (10, 11) and the number of siblings with trachoma (1214).
Evidence of environmental causation
Studies addressing the associations of interest for environmental causes of trachoma transmission were searched as described above. Studies were excluded if they did not satisfy the following criteria: use random selection for inclusion of study participants; use multivariate analysis with analysis of major confounders; describe exposure to risk factors quantitatively; provide information on the significance of the results; use an adequate sample size at least 130 study participants are required to permit detection of a significant relative risk (RR) or odds ratio (OR) of 3 with a power of 80% and a confidence interval of 95%1.
Of the 39 studies identified (947), 19 were selected (Table 1) (927). Of these, four were clinical trials (of which three are listed in the Cochrane Library (48)), and 15 were observational surveys. Parameters of interest analysed in these studies include water availability, garbage collection, absence of latrine/toilet, frequency of face-washing, facial cleanliness, personal hygiene, fly density, presence of animals inside the house and indoor air quality.
Study results
The results are summarized in Table 2.
Water availability was analysed by measuring access to a water source, in terms of walking time or distance, availability of water inside the house or daily water quantity in the house. The median protective effect on trachoma prevalence for improved access to water was 27% (range, 1183%) when considering distance to the water source. Six studies had positive results (10, 12, 17, 19, 24), one study had non-significant results (13) and one had negative results (27). The influence of the quantity of available water was positive in two studies, with a median protective effect of 21% and 76%, respectively (17, 18), and non-significant in one study (24). The availability of piped water inside the house also had a significant protective effect in one study (18).
The presence of a latrine was reported to be significant by all four studies that investigated this parameter, with a median reduction of trachoma prevalence of 28% (12, 16, 18, 22, 27).
Garbage collection showed a median protective effect of 69% in two studies (11, 18).
The presence of animals inside the house was assessed by one study as being non-significant (11).
While sleeping next to a cooking fire exhibited a negative effect in two studies (22, 24), cooking in a central room had a protective effect in another (11). Traditional cooking usually creates smoke in the room, which tends to decrease fly density. On the other hand, the use of one central room for cooking and sleeping (i.e. crowding, which also plays a role in trachoma transmission) may have influenced the results.
Four of the studies that investigated the impact of flies on the faces of children or fly density on trachoma showed a protective effect for fewer flies (14, 15, 22, 23), and one reported a non-significant result (25), with a 39% median reduction in prevalence of trachoma.
Facial cleanliness was reported by four studies to be inversely associated with the prevalence of trachoma in children (13, 22, 24, 25) and as non-significant by one study (14). The median protective effect was 41%. Frequency of face-washing was non-significant in the three studies that investigated the impact of this parameter (12, 18, 26).
Satisfactory personal hygiene was reported by one study to have a positive impact by reducing trachoma prevalence by 48% (19).
A clinical trial of the effects of introducing a community-based care group into a selected community reduced the prevalence of trachoma by 62% over a study period of 3 years, while the reduction in the control community was negligible (21). A clinical trial providing mass treatment with topical tetracycline, accompanied or not by a face-washing intervention programme, showed that a sustainable clean face had a significantly protective effect against constant severe trachoma (13). Another clinical trial found that a health education programme did not improve the effectiveness of mass treatment campaigns; there was even a negative interaction between the two interventions (20).
A clinical trial investigating the effect of reducing the fly population (9) reported a decrease of 75% in new trachoma cases compared with the control group.
Discussion
The validity of the studies covered here can be affected by several factors. The main bias may arise because environmental risk factors, such as water availability, presence of latrine and garbage collection, tend to occur together in the same families and confound each other, unless sufficient control for this effect is introduced. This would lead to an overestimation of the studied association. By considering less distant risk factors, which are more directly related to the transmission mechanisms, such as fly density or facial cleanliness (9, 1315, 22, 23, 25), confounding would be reduced. In addition, the relation of trachoma to environmental risk factors affecting more than one particular household (e.g. the effects of absence of latrine or garbage collection, or fly density) could lead to a non-differential misclassification bias when assessing outcomes and risk factors on an individual rather than a community basis. This would result in an underestimation of effect. Therefore, studies that assess these risk factors and the outcome on a community basis (9, 21, 22) would be expected to be more accurate. In studies that include children and adults, the effects of risk factors will be lower than in those investigating children only. Since prevalence in children is usually higher, the inclusion of adults leads to a diluting effect unless transmission mechanisms are different. In summary, studies that define the study unit precisely and assess less distant risk factors are expected to be the most accurate. In this review they are, therefore, given more weight in the evaluation of evidence.
Causation of trachoma by unclean environments fostering the proliferation or attraction of flies (i.e. uncollected excreta or garbage) can be considered as the most likely interpretation of the results, according to Bradford Hills considerations for causation in environmental studies (49).
The strength of association was verified by relative risks ranging between 1 and 4.
The association of interest was consistent in studies carried out in several countries.
The association was specific, since the exposures to flies were related to a specific pathogen.
The associations were temporally consistent, since exposures were usually continuously present.
The biological gradient was verified in most of the few studies in which it was investigated.
The relationship is plausible, since laboratory trials have shown the ability of flies to carry the pathogens, and breeding and attraction places are known for these flies.
The results are coherent, since the cause-and-effect interpretation of the data does not conflict with previous knowledge of the disease.
Preventive action has been shown in two experiments (9, 21).
There is analogy to the transmission of a number of other diseases by flies, although not with this specific pathogen.
For unclean faces, the criteria for causation are similarly fulfilled, although the results are less consistent. Experimental results did not show a systematic effect when hygiene education was associated with a mass treatment campaign (13, 20). Although only two clinical trials investigated this association, this may indicate that other important transmission factors were not considered.
Causation by more distant risk factors is less evident. For example, the direct relationship with distance to water source and water quantity used in the house (24), or with frequency of face-washing was not always verified. Nevertheless, the review results strongly suggest that water availability has a positive effect, decreasing trachoma prevalence.
Overall, the results indicate that trachoma transmission is a function of fly density, its endemicity and personal hygiene, including facial cleanliness and person-to-person contact. However, direct quantitative conclusions on the relative attributable risks of transmission cannot be drawn. The three factors are related to each other; for example, an increase in unclean infected eyes will lead to an increase in pathogen-carrying flies; and an increase in pathogen-carrying flies will in turn tend to infect more eyes. Person-to-person contact and flies seem to play a significant role and constitute the major transmission pathways for trachoma. On the basis of the best available data for the environments studied, the role of flies seems to be of greater importance, which suggests that an attributable risk for trachoma transmission by flies of 50% should be considered to be conservative. This is supported by the studies in this review, which were selected for their methodological quality and were conducted in a wide variety of countries. However, the attributable fractions may vary according to local levels of hygiene, trachoma prevalence, and fly density in the community. These findings do not suggest that flies are the single most important mode but that they carry a major weight in trachoma transmission. For example, qualitative observations on hyperendemic trachoma reported it to occur even with low fly densities (46).
Only two studies assessed hygiene practices and flies in the same communities (14, 22). One showed that an increased number of flies around the house was a predictor of presence of infection, while the association of facial cleanliness with infection was not significant (14). The other showed similar relative risks for poor facial cleanliness (1.72; 95% confidence interval (CI) = 1.172.50) and household fly density (for high fly counts: 1.63; 95% CI = 1.172.29) (22).
In addition to transmitting trachoma, flies have been shown to carry a wide variety of pathogens, and the reduction of their population by environmental improvements may thus contribute to a decline in other endemic diseases in the community. Environmental improvements that have been demonstrated to contribute significantly to the prevention of trachoma (such as access to water) are also associated with a wide range of health, social and economic benefits.
In terms of preventive action, it is likely that both hygiene education and fly control by environmental improvements have a significant impact. The specific effectiveness of these two interventions is, however, likely to depend on the existing levels of hygiene and fly density in the community. In a population where trachoma is endemic, an initial antibiotic treatment to reduce the reservoir of C. trachomatis will have an immediate impact, reducing trachoma prevalence in the short term, while hygiene and environmental improvements are likely to lead to a sustainable reduction. The effectiveness of interventions may also be affected by the dominant eye-seeking fly species in the local setting, and targeted actions to destroy breeding sites and attraction may be beneficial.
Recommendations
There is sufficient evidence to support the recommendation of facial cleanliness and environmental interventions (i.e. the F and E components of the SAFE strategy) to prevent trachoma. Several studies have suggested that reducing fly densities and hygiene education decrease transmission of trachoma. Personal and domestic hygiene appear to have great potential for a sustainable reduction in transmission. Effective antibiotic treatment of active cases would also assist in reducing the pathogen reservoir.
In order to improve the targeting of interventions, a better understanding of the relative contributions of the various elements to the risk of trachoma transmission and the effectiveness of different interventions is required. Controlled clinical trials are needed to determine the relative attributable risks and effectiveness of interventions to improve personal hygiene and fly control, alone and in combination. Baseline levels of hygiene, fly density and prevalence of trachoma should be assessed, since the relative importance of transmission mechanisms may vary according to the specific local circumstances. 
Acknowledgements
The authors acknowledge the valuable comments of Dr J. Bartram, Acting Coordinator, Water, Sanitation and Health and Dr S. Resnikoff, Acting Coordinator, Prevention of Blindness and Deafness, WHO, Geneva, Switzerland.
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Correspondence
A. Prüss
Sanitation and Health, Protection of the Human Environment, World Health Organization
1211 Geneva 27, Switzerland
1 Using Epi Info 6, version 6.04, 1997 Centers for Disease Control and Prevention and World Health Organization.