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Socio-Economic and Environmental Factors Associated with Montenegro Skin Test Positivity in an Endemic Area of Visceral Leishmaniasis in Northern Morocco

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Socio-Economic and Environmental Factors Associated with Montenegro Skin Test Positivity in an Endemic Area of Visceral Leishmaniasis in Northern Morocco Microbiology Research 2012; volume 3:e7 Socio-economic and with fatal spontaneous evolution.1 The domes- tic dog constitutes the principal reservoir of Correspondence: Meryem Lemrani, Institut environmental factors infection and is important in zoonotic trans- Pasteur du Maroc, 1 Place Louis Pasteur, associated with Montenegro mission.2 The worldwide incidence of VL is Casablanca, Morocco. skin test positivity in an approximately 0.5 million cases per year.3 Tel. +212.661.46.48.18 - Fax: +212.522.26.09.57. E-mail: [email protected] endemic area of visceral Visceral leishmaniasis is widespread in northern Morocco (Chefchaoun, Taounate, leishmaniasis in northern Key words: asymptomatic visceral leishmaniasis, Taza, Fes, Moulay Yacoub, Meknes, Sefrou, AL socio-economic factors, environmental factors, Morocco houceima and Sidi Kacem) (Figure 1). Few Montenegro skin test. epidemiological data are, however, available Salsabil Hamdi,1 Abdellah Faouzi,1 concerning its epidemiology and clinical fea- Contributions: SH carried out the project, con- Rajaa Ejghal,1 Abderahmane Laamrani,2 tures. However, a new type of cutaneous leish- ducted the field work, collected and analyzed Hamid Amarouch,3 Mohammed Hassar,1 maniasis due to Leishmania infantum was data, and prepared the final draft of the manu- 4 script; AF, RE, helped in the statistical analysis; Meryem Lemrani1 recently described. Before 1995, human vis- ceral leishmaniasis was not an obligatory noti- AL, HA, helped in the study design; MH, revised 1Laboratoire des Recherches et d’Étude fiable disease. The incidence of VL is about the manuscript; ML overviewed the study for sur les Leishmanioses, Institut Pasteur du intellectual content. 152 cases per year5 predominantly affecting Maroc, Casablanca; 2Service de children under the age of 5 years. Extension of Acknowledgments: we would like to thank the Parasitologie, DELM, Ministère de la arid zones and an increase in temperatures 3 Ministry of Health, Department of Parasitology, Santé, Rabat; Faculté des Sciences have a synergic role on the risks of an increase Direction d’Epidémiologie et de Lutte Contre les Hassan II, Ain Chock, Casablanca, in the number of cases of leishmaniasis in Maladies, the Health Delegation of the Province Morocco these regions.5 The sand fly vectors of L. infan- of Zouagha My Yacoub (Dr. Boubker Mouniem, tum in these regions are: Phlebotomus perni- Mr Dehmani), the Health Delegation of the ciosus,6 Phlebotomus longicuspis7 and P. ari- Province of Taounate (Dr Ouddiche, Mr Boumadiane) and the local authorities of the two asi.8 Dog is the main reservoir of L. infantum provinces.only Abstract in Morocco.8-10 Zymodeme MON-1 is predomi- nant in Morocco; however, zymodeme MON-24 Received for publication: 28 September 2011. In Marocco, many aspects of human asymp- has been occasionally isolated from a dog.11 Revision received: 18 January 2012. tomatic visceral leishmaniasis (VL) still have This zymodeme was considered a sporadicuseAccepted for publication: 8 February 2012. to be clarified and little information is avail- form of CL. This work is licensed under a Creative Commons Epidemiological patterns are changing in able about the factors that predispose individ- Attribution NonCommercial 3.0 License (CC BY- uals to asymptomatic infection. A prospective the Mediterranean area due to several factors, NC 3.0). study was carried out in 889 healthy children such as the widespread migration from rural to under the age of 15 years living in two urban and peri-urban areas, climatic changes ©Copyright S. Hamdi et al., 2012 provinces in the endemic area in northern increasing exposure to the sand fly and also, in Licensee PAGEPress, Italy Morocco (the provinces of Taounate and My urban areas, an increase in HIV infection. Microbiology Research 2012; 3:e7 doi:10.4081/mr.2012.e7 Yacoub) from April to May 2010. The aim of the Human activity is the leading factor in the sig- study was to evaluate the prevalence and the nificant changes recently observed in the ecol- socio-economic and environmental character- ogy and behavior of many vector-borne dis- 12 istics associated with infection by Leishmania eases. Most parasite-driven processes are or have an oligosymptomatic form of the dis- asymptomatic or subclinical; however, some infantum. The Montenegro skin test (MST) ease.21 Although the extent of this phenome- result in severe visceral diseases that are was used to detect asymptomatic infection. non has not been fully evaluated, people with- 13 The prevalence of transmission of infection lethal if not treated. It is not well understood out a definite history of disease may have evi- was 11.4% and approximately 2 times higher in why the parasite-driven processes remain dence of infection as demonstrated by a posi- Taounate than in My Yacoub, as measured by asymptomatic in certain subjects and cause a tive Delayed-Type Hypersensitivity (DTH) MST. Asymptomatic infection was associatedNon-commerciallethal disease in others. It has been suggested reaction assessed by the Leishmanin skin test, with gender, age, presence of familial links, that environmental factors that affect sand fly also called the Montenegro skin test (MST). 14 proximity to chickens, and the number of peo- ecology, human activities that increase expo- This test is currently used to assess the preva- ple in the house and locality, but it was not sure to sand flies,15 and the presence of other lence of Leishmania infection in the human associated to education status, presence of animals permissive to the Leishmania life population.22 The MST is considered the most dogs, livestock waste, sewage disposal, water cycle all play critical roles in the development complementary test in diagnosis, and is also supply system or use of insecticides. of the human disease.1 Poor economic condi- used in epidemiological studies and as an indi- tions,16,17 malnutrition18 and impaired reactiv- cator of unapparent infection with ity of the immune system19 have also been Leishmania.23 shown to increase the risk of VL. Furthermore, There are no statistical data in Morocco con- Introduction certain age groups are at a greater risk of VL cerning the force of transmission of visceral than others.20 Field studies showed that leishmaniasis in endemic areas. Studies of a Leishmaniasis constitute a group of dis- asymptomatic infection may occur in endemic marker of cellular immune response, such as eases caused by an obligatory, intracellular, areas. In these areas of VL, only about 20% of the Montenegro skin test, might be useful protozoan parasite of the Leishmania genus the subjects infected by Leishmania chagasi since the response rarely disappears with that causes a spectrum of diseases, ranging will develop classical VL, the majority of the time. Therefore, the objective of this study was from self-limiting, self-curing cutaneous leish- infected individuals have a subclinical infec- to identify socio-economic and environmental maniasis (CL) to visceral leishmaniasis (VL) tion that may remain completely asymptomatic factors associated with Montenegro skin test [page 28] [Microbiology Research 2012; 3:e7] Article positivity in an endemic area in northern where appropriate) and multivariate analysis 95% confidence intervals for the association Morocco, and estimate the force of transmis- (logistic regression). Statistical analysis was with outcome. Most variables studied (Tables 2 sion and the frequency of healthy carriers. performed using STATA 11.0 software (Stata and 3) were associated with a significant Corporation, College Station, TX, USA). prevalence of MST positivity. There was a sig- nificant difference in exposure to infection with L. infantum between males and females. Material and Methods Risk factor of infection was approximately two Results times greater for males than for females. On Study area the other hand, this risk increases with age (PR=1 for children under the age of eight This study was undertaken from April to Force of transmission of visceral May 2010 in two rural endemic areas in north- years and PR=1.85 for children over the age of ern Morocco, Zouagha Moulay Yacoub and leishmaniasis in northern Morocco ten years), presence or absence of familial Taounate provinces (Figure 1 and Table 1). A total of 889 healthy children were included links (PR=2.87 for children tested with a famil- This is a mountainous region with variable in the study. All were from the northern region ial link), and according to province and locali- relief and it is, therefore, common to find a where visceral leishmaniasis is endemic. The ty. Exposure to risk infection is more prevalent wide range of vegetation and bioclimatic vari- mean age of the population studied was in Taounate (PR=1.72) than in My Yacoub. ation. We studied 8 localities at altitudes of 8.5±2.23 years; the median age was eight Bouadel, a site in Taounate, has the highest 300-600 m with a semi-arid climate, a mild years (81% under the age of ten years); 417 prevalence of infection (PR=2.34) in this winter and yearly precipitation of 400-800 mm females (47%) and 472 males (53%). The study, even though the difference was not sig- in Zouagha Moulay Yacoub and 900-1000 mm prevalence of MST positivity was 11.4% and nificant. in Taounate. Rural populations under the age approximately two times greater in Taounate Table 3 shows the association between nod- of 15 years number 20,600 and 51,000 in than in My Yacoub. The number of asympto- ule size and gender, age, familial links and matic cases was 66 males (66.34%) and 34 provinces. There was a significant difference Taounate and My Yacoub, respectively.5 females (33.66%). between nodule size and familial link and Table 2 shows the prevalence of MST posi- province. Nodule size increased with familial Study population tivity according to the variables investigated linksonly (PR=3.20) and this difference was more A questionnaire that included socio-eco- and the crude prevalence ratios and respective common in Taounate (PR=3.95).
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