IJCRR - 14(1), January, 2022
Pages: 09-15
Date of Publication: 03-Jan-2022
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Spatial Patterns and Temporal Trends of Human Leishmaniasis Incidence in Khemisset Province, Morocco
Author: Hanna M, Boussaa S, Raghay K, Mabchour I, Fadli M
Category: Healthcare
Abstract:Leishmaniases are parasitic diseases caused by Leishmania species and transmitted by the phlebotomine sandflies. In Morocco, Leishmaniases are a major public health problem with two clinical forms: cutaneous and visceral Leishmaniasis. Khemisset Province is one of the Moroccan regions where cases of both cutaneous and visceral Leishmaniasis were reported without official data about epidemiological status. Epidemiological and entomological investigations were conducted in Khemisset Province based on 20-year epidemiological data (1997-2016). The results showed the presence of both clinical forms of Leishmaniasis in the study area. All ages and both genders were affected by these different forms of the disease. Five sandfly species were identified morphologically in the study area with the dominance of Phlebotomus sergenti (61.11%). The Province of Khemisset should be regarded as a potential focus for Leishmaniasis in the region because of the presence of all the components of the disease transmission cycles. It is suggested that the competent authorities monitor the Khemisset area constantly to prevent the danger and spread of this epidemic.
Keywords: Leishmaniasis, Phlebotomy, Sandfly, Epidemiology, Morocco, Epidemic
Full Text:
Leishmaniasis is a complex of diseases caused by Leishmania species and transmitted by a Phlebotomine sandfly (Diptera:Psychodidae). These parasitic diseases present a wide range of clinical symptoms and epidemiological entities. It is among the second most apparent resurging vector-borne disease, after Malaria; that currently threaten 350 million people in 88 countries.1 In Morocco, Leishmaniasis outbreaks are endemic and constitute a major public health threat.2 The cutaneous (CL) and visceral (VL) forms coexist with three species of parasites (Leishmania major, L. tropica and L. infantum) which share responsibility for cases of cutaneous leishmaniasis, while only L. infantum is responsible for the visceral.3
Three major sandfly vectors were found associated with dynamics of VL across Morocco; Phlebotomus ariasi, P. perniciosus and P. longicuspis, .P. papatasi and P. sergenti are the proven vectors of L. major and L. tropica, respectively.4,5 Several mammals’ reservoirs were associated with the disease transmission across the country; dogs for zoonotic VL, rodents for zoonotic CL and human for anthroponotic CL.6
The problem of Leishmaniasis has been identified as a priority for the national Ministry of Health. Since 1995. Leishmaniasis has become a notifiable disease and in 1997 our country invested in the fight against these diseases by implementing an action plan with general objectives as early management of cases of VL and disease control in outbreaks of cutaneous leishmaniasis.2
Khemisset is one of the Moroccan regions where epidemiological status of human Leishmaniasis is unknown. In spite of the presence of canine Leishmaniasis, and its position beside the active Leishmaniasis outbreaks in central Morocco: in the Fez-Meknes region, and in the Benimellal-Khenifra region, no data about entomological or epidemiological investigations, in Khemisset region, were recorded.7, 8
The objective of our investigation is to study, for the first time, the epidemiological status of leishmaniasis in Khemisset province where cases of both forms of human leishmaniasis have been recorded.
Materials and Methods
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Study area:
Administratively, Khemisset Province is part of Rabat - Salé - Kenitra region (Figure 1), the total area of the province is 781,000 hectares, of which 47.7% is agricultural land, 40.6% forest and 11.7% rangeland and wasteland.9 The province is made up of 4 Circles, 32 rural municipalities and three urban municipalities. In 2014, the total population was 542025 inhabitants with the majority in rural municipalities.10
The dominant climate type in the region is semi-arid to arid with some years characterized by a sub-humid climate when annual rainfall exceeds 600mm/year.11 geographically; Khemisset province is composed of two entities: plateaus and depressions.12
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Epidemiological data:
The present study is a retrospective analysis of the leishmaniosis status at Khemisset province. Epidemiological data were obtained from the register of the Laboratory of Epidemiology and Environmental Health, in the local Delegation of Ministry of Health. The authorization has been obtained from the Regional and local Health Department to examine these registers.
All microscopic preparations concerning leishmaniasis cases, carried out in the different health districts of KhemissetProvince, are sent and archived in this laboratory. Thereby, we collected 20-year epidemiological data (1997-2016) for analysis.
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Entomological data:
Specimens were collected from ten stations in the study area using 30sticky traps by the station during the entomological season (May-July 2018). Thus, traps were placed in the evening, in different biotopes, and recovered the next morning. Traps were prepared with A4 sheets coated with castor oil. The collected specimens were stored in 70° alcohol for lightening and rapid assembly in the chloral balm for species identification.13
The identification was made morphologically by examining the male genitalia, female spermathecae and pharynges based on the key for the determination of Moroccan sandflyMahjour et al. (1997), and referring to Boussaa Samia, (2008), for the identification of species of the subgenus Larroussius.3,14
Results
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Epidemiological status of leishmaniasis in Khemisset:
According to epidemiological data, both forms of leishmaniasis (CL and VL) were recorded in Khemisset Province (Table 1). According to epidemiological data (Table 1), both forms of leishmaniasis (CL and VL) were recorded in Khemisset Province. The rural area is more affected by leishmaniasis cases (76%) compared to (15%) in urban areas. The epidemiological profile of leishmaniasis in our study area assumes that the disease affects both sexes and different age groups (Figure 2). The epidemiological profile of leishmaniasis in our study area assumes that the disease affects both sexes and different age groups (Figure 2). Figure 3 shows the distribution of leishmaniasis forms according to age.
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Spatiotemporal trends of leishmaniasis in Khemisset:
Figure 4 presents maps illustrating the spatial evolution of visceral leishmaniasis (a) and cutaneous leishmaniasis (b) in Khemisset Province based on epidemiological data. Analysis of secular trend of leishmaniasis (both VL and CL) cases (Figure 5) shows that the highest number of 6 cases was noted in 2010. The seasonal fluctuation of leishmaniasis cases recorded in the study area (Figure 6) shows the difference in the number of visceral leishmaniasis cases recorded by season.
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Sandfly species composition in Khemisset:
Thus, our entomological investigations were conducted in urban and rural municipalities of Khemisset Province where leishmaniasis cases were detected in the study area as shown in Table 2. The study area covered an altitude range of 225-1221m.
Table 3 shows the percentages of different species collected in our study area where five species were morphologically identified. Five species were identified morphologically. Phlebotomussergenti was the most dominant species (61.11%), followed by P. longicuspis (20.37%), Sergentomiyaminuta (11.11%), P. ariasi (5.56%) and P. perniciosus (1.85%).
Discussion
As noted recently in Morocco, both forms of leishmaniasis coexist in several northern and central regions, such as Taza, Moulay yaacoub, SidiKacem, Chefchaoune, El Haouz and Lhoceima.2 In the study area, the recorded VL cases are due to Leishmania infantum while L. tropical and L. major are responsible for the cases of CL. The visceral leishmaniasis by L. infantum is the dominant form (52%) of leishmaniasis in the province. Results suggesting the local L. infimum transmission cycle since Natami et al. (2000), reported canine leishmaniasis by L. infantumin this area with a serape valence of 16.71%.15. Concerning the rural area is more infected with leishmaniasis than the urban area, this results is in line with the WHO reports confirming the rural nature of this disease.16 Thus far, leishmaniasis affects the rural sector more than the urban sector in Morocco, as confirmed by different investigations in leishmaniasis foci in northern and central Morocco.17
The results show that there is no relationship between sex and leishmaniasis. It is statistically confirmed, whether visceral (P=0.19) or cutaneous (P=0.23) form. But results confirmed a relationship between leishmaniasis and patient age. Our result is in agreement with those of other works. In Morocco as 81% of VL cases are less than 9 years old (Mahjour et al. 1997).3 In Tunisia, Aounet al.(2009), concluded that children under five years old are the most affected group by VL. Globally, VL is known as infantile disease but it can affect adults, particularly in HIV-L. infantum co-infection condition. 3, 18, 19 On the other hand, the age-specific risk depends on the parasitic species and the population's exposure history. Thus, in endemic area of L. infantum, the median age of clinical cases of VL tends to be lower (generally < 5 years), while it occurs in adults mainly in cases of severe immune deficiency.20, 21
Concerning CL distribution according to age groups (Figure 3), 52% of cases range between 15 and 49. These results are consistent with the results found in other regions in Morocco by Arroub et al. (2012) , in Tunisia by Abda et al. (2010 ) and in Iran by Fazaeli et al. (2009) showing that the young population is the most affected by CL.22-24
For the visceral form we can see that in 1997, five municipalities were affected by the disease while between 1998 and 2016, the number of affected municipalities increased from 5to 14 (Figure 4-a) For cutaneous form we can see that in 1997, one municipality was affected by the disease while between 1998 and 2016, the number of affected municipalities increased from 1 to 10 (Figure 4-a). As a secular trend of leishmaniasis cases (both LV and CL) the highest number of 6 cases was noted in 2010 as well. According to the same distribution (Figure 5), only VL was recorded between 1997 and 1999, while CL was introduced since 2000. In 1997-2016 period, VL cases peaked in 2003 whereas CL cases peaked ten years later in 2013 (Figure 5). We noted also the dominance of the visceral form until 2010, then, CL cases became more frequent.
Most cases of visceral leishmaniasis were detected in December and July. This seasonality could be related to the seasonal dynamics of vector species and the incubation period of the disease. For cutaneous leishmaniasis, the recording of cases is spread over a precise period, with an absence of cases in April, August and September. Studying the sandfly species composition and its bionomics is an interesting tool for a better understanding of the disease transmission dynamic and it contributes to the planning for the prevention and control against leishmaniasis particularly in the areas where the risk of leishmaniasis extension is thought to be significant.
The vector species for two clinical forms of leishmaniasis in Morocco coexist in our study area; namely Phlebotomus sergenti, the proven vector of CL caused by L. tropica and the three species (P. longicuspis, P. ariasi and P. perniciosus) of VL caused by L. infantum.4 Results explain the presence of cases of both clinical forms of leishmaniasis in the Khemisset Province and confirm the hypothesis of local transmission cycles. The Zonerisk of leishmaniasis can be characterized by vector abundance (The abundance of vector species is an important risk factor for characterization of a leishmaniasis endemic area). According to biotopes, entomological data (Table 1) shows the presence of sandfly in both urban and rural areas, with altitudes between 225 and 1221m. The five species were collected in rural area; while only P. sergenti collected in urban area. The sandfly species diversity in rural areas is favored by the presence of reservoir animals coupled with poor hygiene and sanitation facilities, and the abundance of organic matter.2
In Morocco, sandfly seasonality is widely studied. In semi-arid area of Marrakech (at 466m), P. sergenti was active especially during the period of April–May–June and absent in the rest of the year.13 In semi-arid area of Chichaoua Province (at 1148 m), P. sergenti population reached peak density during July and August and was lowest from September through November.25
For Larroussius species activity, in semi-arid area of Ourika (at 850 m), P. perniciosus, P. longicuspis and P. ariasi activities show a bimodal seasonal trend with two abundance peaks, in summer (May–June–July) and in autumn (September–October), while in Yabora (at 1155 m), their activities show a mono-modal annual pattern with a long activity period extending from March to November with the highest density recorded in June.25 P. sergenti and Larroussius species activities determine necessarily the seasonal fluctuation of leishmaniasis cases recorded in the study area (Figure 6).
Conclusion:
The number of cases recorded in our study area is not alarming but obviously informative on the local presence of all the components of the disease transmission cycle. Consequently, the Province of Khemisset should be regarded as a potential focus for leishmaniasis because of the following tangible reasons:
- Leishmania species, confirmed by recorded human cases;
- Animal reservoir, confirmed by canine leishmaniasis cases;
- Proven vectors of CL and VL in Morocco
- Active human leishmaniasis foci in the region with human population movements;
Taking into consideration the under-reporting of human cases, particularly in rural areas, the results of the present study are enough for continuous epidemiological surveillance to prevent the risk.
Acknowledgement:
We are very grateful to all medical staff in the Health Delegation of the Moroccan Ministry of Health in Khemisset province. Also, the authors acknowledge the immense help received from the scholars whose articles are cited and included in references of this manuscript. The authors are also grateful to authors/editors/publishers of all those articles, journals and books from where the literature for this article has been reviewed and discussed.
Source of funding:Nil
Conflict of Interest:Nil
Authors’ Contribution:
Author's name
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Contribution
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Hanna Marwa
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Writing the article
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BoussaaSamia
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Critical revision of the article
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Raghay Kawtar
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Data analysis and interpretation
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Mabchour Insaf
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Interpretation of data
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Mohamed Fadli
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Final approval of the article
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References:
-
Alvar J., Vélez I.D., Bern C., Herrero M., Desjeux P., Cano, J. et al. 2012. Leishmaniasis Control Team. Leishmaniasis worldwide and global estimates of its incidence. PloS one,7(5).
-
Laamrani IA., Lakranbimbs. Elabandouni M., Nhammi H., Ameur B. 2010. Guide des activités de lutte contre les Leishmaniose. Ministère de la Santé. Direction d’épidémiologie,(143 p)
-
Mahjour J., Laamrani EL Idrissi A., Lyacoubi M., Mouki B., Barkia A., Lhayati M. 1997. Guide des activités lutte contre les Leishmaniose. Ministère de la Santé. Direction d’épidémiologie éditeur,(107 p).
-
Mhaidi I., El Kacem S., Kbaich MA., El Hamouchi A., Sarih M. H., Akarid K., et al. 2018. Molecular identification of Leishmania infection in the most relevant sandfly species and in patient skin samples from a cutaneous leishmaniasis focus, in Morocco. PLo. Negl.Tro. Dis,12(3), e0006315.
-
Ajaoud M., Es-sette N., Hamdi S., El-Idrissi A. L., Riyad M, Lemrani, M. 2013. Detection and molecular typing of Leishmania tropica from Phlebotomus sergenti and lesions of cutaneous leishmaniasis in an emerging focus of Morocco. Parasites & vectors, 6(1), 217.
-
Echchakery M., Nieto J., Boussaa S., El Fajali N., Ortega S., Souhail K et al.(2018). Asymptomatic carriers of Leishmania infantum in patients infected with human immunodeficiency virus (HIV) in Morocco. Par. Res., 117(4), 1237-1244.
-
Natami A., Sahibi H., Lasri S., Boudouma M., Guessouss-Idrrissi N., Rhalem A. 2000. Serological, clinical and histopathological changes in naturally infected dogs with Leishmaniainfantum in the Khemisset province, Morocco. Veter. Resh, 31(3), 355-363.
-
Talbi F. Z., El OualiLalami A., JanatiIdrissi A., Sebti F., Faraj C. 2015. Leishmaniasis in central Morocco: seasonal fluctuations of phlebotomine sandfly in Aichoun locality, from Sefrou province. Path. Res. Inter, p 25.
-
EL Fihrim. L. C. 1991. Pancréatite aiguë et grossesse: expérience du CHU Mohamed VI de Marrakech.
-
Moroccanministry of Heath. 2008.Bilan des activités des programmes de lutte contre les maladies parasitaires Ministère de la Santé. Direction d’épidémiologie, p230.
-
Hanna M., Boussaa S, and Fadli M. 2018. Contribution à l’étude de l’effet des changements climatiques sur la biodiversité des phlébotomes dans la région de zemmour, Maroc, Proceedings of the First National Colloquium :"Biotechnology of Natural Substances and the Environment" Khenifra April 19th,p 118-121
-
MICHARD. 1976. André. Eléments de géologie marocaine. Notes et memoires du Services geologique (Maroc).
-
Boussaa S., Guernaoui S., Pesson B, Boumezzough A. 2005. Seasonal fluctuations of phlebotomine sandfly populations (Diptera: Psychodidae) in the urban area of Marrakech, Morocco. Acta tropica, 95(2), 86-91.
-
Boussaa S. 2008. Epidémiologie des leishmanioses dans la région de Marrakech, Maroc: effet de l’urbanisation sur la répartition spatio-temporelle des Phlébotomes et caractérisation moléculaire de leurs populations. 2008. Thèse de Ph.D. Strasbourg 1.
-
El Aasri A., El Madhi Y., Najy M., El Rhaouat O, Belghyti D. 2016. Epidemiology of cutaneous leishmaniasis in SidiKacem province, northwestern Morocco (2006–2014). As. Pac. J. Tro. Dis,6(10), 783-786.
-
WHO.2014. Activité de l’OMS dans la Région de la Méditerranée orientale: rapport annuel du Directeur régional 2014. World Health Organization. Regional Office for the Eastern Mediterranean, p 235.
-
Aoun K., Jeddi F., AmriF., Ghrab J.,Bouratbine, A. 2009. Actualités épidémiologiques de la leishmaniose viscérale en Tunisie. Méd. Mal.Infe, 39(10), 775-779.
-
Elkohli M., Laqraa E., Adlaoui E., Faraj C.2015. Abondance et distribution spatiotemporelle de Phlebotomus sergenti, vecteur de la leishmaniose cutanée à Leishmania tropica, au Maroc, Bulletin de l’institut national d’hygiéneedition semestrielle janvier-juinN°3 ministére de la santé royaume du Maroc, pages 2-3
-
ELKOHLI M., LAQRAA E., ADLAOUI E., FARAJ C. 2015. Abondance et distribution spatiotemporelle de Phlebotomus sergenti, vecteur de la leishmaniose cutanée à Leishmania tropica, au Maroc, Bulletin de l’institut national d’hygiéneedition semestrielle janvier-juin2015 N°3 ministére de la santé royaume du Maroc, pages 2-3
-
Arroub H., Alaoui A., Lemrani M.,Habbari, K. 2012. Cutaneous leishmaniasis in foumjamâa (Azilal, Morocco): micro-environmental and socio-economical risk factors. J. Agric Soc Sci, 8, 10-6.
-
Abda A. B., Hassine M., Jaoua M., Masmoudi M. 2010. Topological sensitivity analysis for the location of small cavities in Stokes flow. SI.J. Cont.Opt, 48(5), 2871-2900.
-
Fazaeli A., Fouladi B, Sharifi I. 2009. Emergence of cutaneous leishmaniasis in a border area at south-east of Iran: an epidemiological survey. J.Vec.Bor.Dis, 46(1), 36.
-
Guernaoui S., Boumezzough A., Pesson B, Pichon, G. 2005. Entomological investigations in Chichaoua: an emerging epidemic focus of cutaneous leishmaniasis in Morocco. J. Med. Entom., 42(4), 697-701.
-
Kholoud K., Samia B., Fouad O., Ali B.2015 Species composition of phlebotomine sandfly fauna in an area with sporadic cases of Leishmaniain fantum human visceral leishmaniasis, Morocco. Acta tropica, 148, 58-65.