Skip to main content

Advertisement

SpringerLink
Log in

Climate Change Influences on the Potential Distribution of the Sand Fly Phlebotomus sergenti, Vector of Leishmania tropica in Morocco

  • Original Paper
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

Background

Leishmaniases are a vector-borne disease, re-emerging in several regions of the world posing a burden on public health. As other vector-borne diseases, climate change is a crucial factor affecting the evolution of leishmaniasis. In Morocco, anthroponotic cutaneous leishmaniasis (ACL) is widespread geographically as many foci across the country, mainly in central Morocco. The objective of this study is to evaluate the potential impacts of climate change on the distribution of ACL due to Leishmania tropica, and its corresponding vector Phlebotomus sergenti in Morocco.

Methods

Using Ecological Niche Modeling (ENM) tool, the estimated geographical range shift of L. tropica and P. sergenti by 2050 was projected under two Representative’s Concentration’s Pathways (RCPs) to be 2.6 and RCP 8.5 respectively. P. sergenti records were obtained from field collections of the laboratory team and previously published entomological observations, while, epidemiological data for L. tropica were obtained from Moroccan Ministry of Health reports.

Results

Our models under present-day conditions indicated a probable expansion for L. tropica as well as for its vector in Morocco, P. sergenti. It showed a concentrated distribution in the west-central and northern area of Morocco. Future predictions anticipate expansion into areas not identified as suitable for P. sergenti under present conditions, particularly in northern and southeastern areas of Morocco. L. tropica is also expected to have high expansion in southern areas for the next 30 years in Morocco.

Conclusion

This indicates that L. tropica and P. sergenti will continue to find suitable climate conditions in the future. A higher abundance of P. sergenti may indeed result in a higher transmission risk of ACL. This information is essential in developing a control plan for ACL in Morocco. However, future investigations on L. tropica reservoirs are needed to confirm our predictions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The data used to support the findings of this study are available as Supplementary files.

References

  1. WHO (2010) Control of the leishmaniases. World Health Organ Tech Rep Ser (949): xii–xiii, 1–186. https://pubmed.ncbi.nlm.nih.gov/21485694/. Accessed 11 June 2021

  2. Alvar J, Yactayo S, Bern C (2006) Leishmaniasis and poverty. Trends Parasitol 22(12):552–557. https://doi.org/10.1016/j.pt.2006.09.004

    Article  PubMed  Google Scholar 

  3. WHO (2014) Manual for case management of cutaneous leishmaniasis in the WHO Eastern Mediterranean region. WHO Regional Publications, Eastern Mediterranean Series; 35. https://apps.who.int/iris/handle/10665/120002

  4. Alvar J, Vélez ID, Bern C et al (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS ONE 7(5):e35671. https://doi.org/10.1371/journal.pone.0035671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Rhajaoui M (2011) Les leishmanioses humaines au Maroc: une diversité nosogéographique [Human leishmaniases in Morocco: a nosogeographical diversity]. Pathol Biol (Paris) 59(4):226–229. https://doi.org/10.1016/j.patbio.2009.09.003

    Article  CAS  Google Scholar 

  6. Boussaa S, Kahime K, Samy AM, Salem AB, Boumezzough A (2016) Species composition of sand flies and bionomics of Phlebotomus papatasi and P. sergenti (Diptera: Psychodidae) in cutaneous leishmaniasis endemic foci Morocco. Parasit Vectors 9:60. https://doi.org/10.1186/s13071-016-1343-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Mhaidi I, El Kacem S, Ait Kbaich M, El Hamouchi A, Sarih M, Akarid K, Lemrani M (2018) Molecular identification of Leishmania infection in the most relevant sand fly species and in patient skin samples from a cutaneous leishmaniasis focus. Morocco PLoS Negl Trop Dis 12(3):e0006315. https://doi.org/10.1371/journal.pntd.0006315

    Article  PubMed  Google Scholar 

  8. Caminade C, McIntyre KM, Jones AE (2019) Impact of recent and future climate change on vector-borne diseases. Ann N Y Acad Sci 1436(1):157–173. https://doi.org/10.1111/nyas.13950

    Article  PubMed  Google Scholar 

  9. Semenza JC, Menne B (2009) Climate change and infectious diseases in Europe. Lancet Infect Dis 9:365–375. https://doi.org/10.1016/S1473-3099(09)70104-5

    Article  PubMed  Google Scholar 

  10. Kahime K, Boussaa S, Bounoua L, Ouanaimi F, Messouli M, Boumezzough A (2014) Leishmaniasis in Morocco: diseases and vectors. Asian Pac J Trop Dis 4:S530–S534. https://doi.org/10.1016/S2222-1808(14)60671-X

    Article  Google Scholar 

  11. Behnassi M, Kahime K, Boussaa S, Boumezzough A, Messouli M (2016) Infectious diseases and climate vulnerability in Morocco: Governance and adaptation options. Exam Role EnvironChange Emerg Infect Dis Pandemics 2016:138–62. https://doi.org/10.4018/978-1-5225-0553-2.ch006

    Article  Google Scholar 

  12. Ready PD (2008) Leishmaniasis emergence and climate change. Rev Sci Tech 27:399–412. https://doi.org/10.20506/rst.27.2.1803 (PMID: 18819668)

    Article  CAS  PubMed  Google Scholar 

  13. Koch LK, Kochmann J, Klimpel S et al (2017) Modeling the climatic suitability of leishmaniasis vector species in Europe. Sci Rep 7:13325. https://doi.org/10.1038/s41598-017-13822-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Naucke TJ, Menn B, Massberg D, Lorentz S (2008) Sandflies and leishmaniasis in Germany. Parasitol Res 103:S65–S68. https://doi.org/10.1007/s00436-008-1052-y

    Article  PubMed  Google Scholar 

  15. Mencke N (2011) The importance of canine leishmaniosis in non-endemic areas, with special emphasis on the situation in Germany. Berl Munch Tierarztl Wochenschr 124:434–42. PMID: 22191164. https://www.vetline.de/system/files/frei/bmtw_2011_11_0434.pdf. Accessed 15 Jan 2022

  16. Kniha E, Dvořák V, Halada P et al (2020) Integrative approach to Phlebotomus mascittii Grassi, 1908: first record in Vienna with new morphological and molecular insights. Pathogens (Basel, Switzerland) 9(12):1032. https://doi.org/10.3390/pathogens9121032

    Article  CAS  Google Scholar 

  17. Dvorak V, Hlavackova K, Kocisova A, Volf P (2016) First record of Phlebotomus (Transphlebotomus) mascittii in Slovakia. Parasite (Paris, France) 23:48. https://doi.org/10.1051/parasite/2016061

    Article  Google Scholar 

  18. Bounoua L, Kahime K, Houti L et al (2013) Linking climate to incidence of Zoonotic Cutaneous Leishmaniasis (L. major) in Pre-Saharan North Africa. Int J Environ Res Public Health 10:3172–3191. https://doi.org/10.3390/ijerph10083172

    Article  PubMed  PubMed Central  Google Scholar 

  19. Jacobson RL (2003) Leishmania tropica (Kinetoplastida: Trypanosomatidae)–a perplexing parasite. Folia Parasitol (Praha) 50(4):241–250. https://doi.org/10.14411/fp.2003.042

    Article  Google Scholar 

  20. Svobodova M, Votypka J, Peckova J et al (2006) Distinct transmission cycles of Leishmania tropica in 2 adjacent foci. Northern Israel Emerg Infect Dis 12(12):1860–1868. https://doi.org/10.3201/eid1212.060497

    Article  CAS  PubMed  Google Scholar 

  21. Ajaoud M, Es-Sette N, Charrel RN, Laamrani-Idrissi A, Nhammi H, Riyad M, Lemrani M (2015) Phlebotomus sergenti in a cutaneous Leishmaniasis focus in Azilal province (High Atlas, Morocco): molecular detection and genotyping of Leishmania tropica, and feeding behavior. Parasit Vectors 9(3):e0003687. https://doi.org/10.1371/journal.pntd.0003687

    Article  CAS  Google Scholar 

  22. Boubidi SC, Benallal K, Boudrissa A et al (2011) Phlebotomus sergenti (Parrot, 1917) identified as Leishmania killicki host in Ghardaïa, south Algeria. Microbes Infect 13(7):691–696. https://doi.org/10.1016/j.micinf.2011.02.008

    Article  CAS  PubMed  Google Scholar 

  23. Ajaoud M, Es-sette N, Hamdi S, El-Idrissi AL, Riyad M et al (2013) Detection and molecular typing of Leishmania tropica from Phlebotomus sergenti and lesions of cutaneous leishmaniasis in an emerging focus of Morocco. Parasit Vectors 6:217. https://doi.org/10.1186/1756-3305-6-217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Chaara D, Bañuls AL, Haouas N et al (2015) Comparison of Leishmania killicki (syn. L. tropica) and Leishmania tropica population structure in Maghreb by microsatellite typing. PLoS Negl Trop Dis 9(12):e0004204. https://doi.org/10.1371/journal.pntd.0004204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Bousslimi N, Ben-Ayed S, Ben-Abda I, Aoun K, Bouratbine A (2012) Natural infection of North African Gundi (Ctenodactylus gundi) by Leishmania tropica in the focus of Cutaneous Leishmaniasis. Southeast Tunisia, Am J Trop Med Hyg 86(6):962–965. https://doi.org/10.4269/ajtmh.2012.11-0572

    Article  Google Scholar 

  26. Ghawar W, Bettaieb J, Salem S et al (2018) Natural infection of Ctenodactylus gundi by Leishmania major in Tunisia. Acta Trop 177:89–93. https://doi.org/10.1016/j.actatropica.2017.09.022

    Article  CAS  PubMed  Google Scholar 

  27. Lemrani M, Nejjar R, Pratlong F (2002) A new Leishmania tropica zymodeme—causative agent of canine visceral leishmaniasis in northern Morocco. Ann Trop Med Parasitol 96:637–638. https://doi.org/10.1179/000349802125001645

    Article  CAS  PubMed  Google Scholar 

  28. Echchakery M, Chicharro C, Boussaa S et al (2017) Molecular detection of Leishmania infantum and Leishmania tropica in rodent species from endemic cutaneous leishmaniasis areas in Morocco. Parasit Vectors 10:454. https://doi.org/10.1186/s13071-017-2398-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Moroccan Ministry of Health (2017). Bulletin of Epidemiology and Public Health. Directorate of Epidemiology and Disease Control, Ministry of Health, Rabat. Available at: https://www.sante.gov.ma/Publications/Etudes_enquete/Documents/2021/sante%20en%20chiffres%202017.pdf. Accessed 15 Jan 2022

  30. Hijmans RJ, Phillips S, Leathwick J, Elith J (2016) dismo: Species distribution modeling. R package version 1.0–15. https://cran.r-project.org/web/packages/dismo/index.html. Accessed 15 May 2020

  31. Daoudi M, Boussaa S, Hafidi M, Boumezzough A (2020) Potential distributions of phlebotomine sand fly vectors of human visceral leishmaniasis caused by Leishmania infantum in Morocco. Med Vet Entomol. https://doi.org/10.1111/mve.12434

    Article  PubMed  Google Scholar 

  32. Daoudi M, Boussaa S, Boumezzough A (2020) Modeling spatial distribution of Sergentomyia minuta (Diptera: Psychodidae) and its potential implication in Leishmaniasis Transmission in Morocco. J Arthropod Borne Dis 14(1):17–28. https://doi.org/10.18502/jad.v14i1.2700

    Article  PubMed  PubMed Central  Google Scholar 

  33. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190(3–4):231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026

    Article  Google Scholar 

  34. Peterson AT, Soberon J, Pearson RG et al (2011) Ecological Niches and Geographic Distributions. Princet Univ Press, Princet. https://doi.org/10.23943/princeton/9780691136868.001.0001

    Article  Google Scholar 

  35. Costa J, Peterson AT, Beard CB (2002) Ecologic niche modeling and differentiation of populations of Triatoma brasiliensis neiva, 1911, the most important Chagas’ disease vector in northeastern Brazil (hemiptera, reduviidae, triatominae). Am J Trop Med Hyg 67(5):516–520. https://doi.org/10.4269/ajtmh.2002.67.516

    Article  PubMed  Google Scholar 

  36. Merow C, Smith MJ, Silander JA (2013) A practical guide to MaxEnt for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography 36:1058–1069. https://doi.org/10.1111/j.1600-0587.2013.07872.x

    Article  Google Scholar 

  37. Moroccan Ministry of Health (2010). Fight against Leishmaniasis. Activity Guide. Directorate of Epidemiology and Disease Control, Parasitic Diseases Service, Ministry of Health, Rabat. http://www.sante.gov.ma/. Accessed 22 Feb 2022

  38. Samy AM, Elaagip AH, Kenawy MA, Ayres CF, Peterson AT, Soliman DE (2016) Climate change influences on the global potential distribution of the mosquito Culex quinquefasciatus, vector of west nile virus and lymphatic filariasis. PLoS ONE 11(10):e0163863. https://doi.org/10.1371/journal.pone.0163863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25(15):1965–1978. https://doi.org/10.1002/joc.1276

    Article  Google Scholar 

  40. Peterson AT, Papeş M, Soberón J (2008) Rethinking receiver operating characteristic analysis applications in ecological niche modeling. Ecol Model 213(1):63–72. https://doi.org/10.1016/j.ecolmodel.2007.11.008

    Article  Google Scholar 

  41. Qiao H, Peterson AT, Campbell LP, Soberón J, Ji L, Escobar LE (2016) NicheA: creating virtual species and ecological niches in multivariate environmental scenarios. Ecography 39(8):805–813. https://doi.org/10.1111/ecog.01961

    Article  Google Scholar 

  42. Omumbo JA, Lyon B, Waweru SM, Connor SJ, Thomson MC (2011) Raised temperatures over the Kericho tea estates: revisiting the climate in the East African highlands malaria debate. Malar J 10:12. https://doi.org/10.1186/1475-2875-10-12

    Article  PubMed  PubMed Central  Google Scholar 

  43. Alonso D, Bouma MJ, Pascual M (2011) Epidemic malaria and warmer temperatures in recent decades in an East African highland. Proc R Soc B 278:1661–1669. https://doi.org/10.1098/rspb.2010.2020

    Article  PubMed  Google Scholar 

  44. Depaquit J, Ferté H, Léger N et al (2002) ITS 2 sequences heterogeneity in Phlebotomus sergenti and Phlebotomus similis (Diptera, Psychodidae): possible consequences in their ability to transmit Leishmania tropica. Int J Parasitol 32(9):1123–1131. https://doi.org/10.1016/S0020-7519(02)00088-7

    Article  CAS  PubMed  Google Scholar 

  45. Pratlong F, Dereure J, Ravel C et al (2009) Geographical distribution and epidemiological features of old world cutaneous leishmaniasis foci, based on the isoenzyme analysis of 1048 strains. Trop Med Int Health 14:1071–1085. https://doi.org/10.1111/j.1365-3156.2009.02336.x

    Article  PubMed  Google Scholar 

  46. Carvalho BM, Rangel EF, Ready PD, Vale MM (2015) Ecological niche modelling predicts Southward expansion of Lutzomyia (Nyssomyia) flaviscutellata (Diptera: Psychodidae: Phlebotominae), vector of Leishmania (Leishmania) amazonensis in South America, under climate change. PLoS ONE 10(11):e0143282. https://doi.org/10.1371/journal.pone.0143282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Cross ER, Hyams KC (1996) The potential effect of global warming on the geographic and seasonal distribution of Phlebotomus papatasi in Southwest Asia. Environ Health Perspect 104(7):724–727. https://doi.org/10.1289/ehp.96104724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Merino-Espinosa G, Corpas-López V, Callejón-Fernández R et al (2016) Differential ecological traits of two Phlebotomus sergenti mitochondrial lineages in southwestern Europe and their epidemiological implications. Trop Med Int Health 21(5):630–641. https://doi.org/10.1111/tmi.12686

    Article  CAS  PubMed  Google Scholar 

  49. Trájer AJ, Sebestyén V. (2019) The changing distribution of Leishmania infantum Nicolle and its Mediterranean sand fly vectors in the last. kys Sci Rep 9(1):11820. https://doi.org/10.1038/s41598-019-48350-7

  50. Chalghaf B, Chemkhi J, Mayala B, Harrabi M, Benie GB, Michael E, Ben Salah A (2018) Ecological niche modeling predicting the potential distribution of Leishmania vectors in the Mediterranean basin: impact of climate change. Parasit Vectors 11(1):461. https://doi.org/10.1186/s13071-018-3019-x

    Article  PubMed  PubMed Central  Google Scholar 

  51. Bogitsh Burton J, Carter Clint E, Oeltmann Thomas N (2013) Blood and Tissue Protozoa I Hemoflagellates. Human Parasitology (Fourth Edition), Academic Press, Elsevier, Amsterdam. https://doi.org/10.1016/B978-0-12-415915-0.00006-6

    Book  Google Scholar 

Download references

Acknowledgements

Authors thank warmly Jenna Lacey for English reviewing.

Author information

Authors and Affiliations

  1. Microbial Biotechnologies, Agrosciences and Environment Laboratory (BioMAgE), Faculty of Sciences Semlalia, Cadi Ayyad University, 40000, Marrakesh, Morocco

    Mohamed Daoudi, Mounia Amane, Mohamed Hafidi, Samia Boussaa & Ali Boumezzough

  2. Laboratory of Microbiology and Virology, Faculty of Medicine and Pharmacy, Cadi Ayyad University, 40000, Marrakesh, Morocco

    Abdelkrim Outammassine

  3. Higher Institute of Nursing and Technical Health Occupations (ISPITS), 10000, Rabat, Morocco

    Samia Boussaa

Authors
  1. Mohamed Daoudi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Abdelkrim Outammassine
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mounia Amane
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mohamed Hafidi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Samia Boussaa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ali Boumezzough
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Samia Boussaa.

Ethics declarations

Conflict of interest

The authors declare that there is no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 17 KB)

Supplementary file2 (DOCX 613 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Daoudi, M., Outammassine, A., Amane, M. et al. Climate Change Influences on the Potential Distribution of the Sand Fly Phlebotomus sergenti, Vector of Leishmania tropica in Morocco. Acta Parasit. 67, 858–866 (2022). https://doi.org/10.1007/s11686-022-00533-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11686-022-00533-5

Keywords

Search

Navigation