Seasonal Distribution of Phlebotomus papatasi, Vector of Zoonotic Cutaneous Leishmaniasis

Abstract

Purpose

The activity of Phlebotomus papatasi Scopoli, a vector of cutaneous leishmaniasis, is known to be seasonal, but the information describing these patterns is sparse in time and space. The purpose of his paper is to conduct a meta-analysis to depict the seasonality of P. papatasi at the global scale.

Methods

The current paper uses data from a collection of 1200 scientific papers, where 300 are about the vector and 36 include monthly data (of 61 sites) of the P. papatasi from 15 countries published from 1994 to 2017.

Results

The activity peaked mainly in dry periods in all explored sites. A map of seasonal distribution depicted a peak activity in August, followed by September. Geographically (geographic preference), August and September at the latitude 33° showed the highest abundance at a global scale. Concerning the latitude P. papatasi distribution, the high number is localized between 27° and 35°. However, the high number of this species according to the longitude is localized between − 4° and 58°, which shows a high interval of activity. Locally, for the habitat preference, the findings show a preference of this vector to indoor than to outdoor.

Conclusions

All these results can be helpful in identifying the period and sites of a future potential risk of leishmaniasis. This is the first attempt at the update of the vector activity both at global and local scale.

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Fig. 1

source: this meta-analysis Climatic data source: ESRI grids, resolution 10 min after WorldClim 1.4 (current conditions) by www.worldclim.org; [25])

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References

  1. 1.

    Adegboye OA, Adegboye M (2017) Spatially correlated time series and ecological niche analysis of cutaneous leishmaniasis in Afghanistan. Int J Environ Res Public Health 14(3):309. https://doi.org/10.3390/ijerph14030309

    PubMed Central  Article  Google Scholar 

  2. 2.

    Abedi-Astaneh F, Akhavan AA, Shirzadi MR, Rassi Y, Yaghoobi-Ershadi MR, Hanafi-Bojd AA, Raufi H (2015) Species diversity of sand flies and ecological niche model of Phlebotomus papatasi in central Iran. Acta Trop 149:246–253. https://doi.org/10.1016/j.actatropica.2015.05.030

    PubMed  Article  Google Scholar 

  3. 3.

    Akhavan AA, Yaghoobi-Ershadi MR, Mehdipour D, Abdoli H, Farzinnia B, Mohebali M, Hajjaran H (2003) Epidemic outbreak of cutaneous leishmaniasis due to Leishmania major in Ghanavat rural district, Qom Province, Central Iran. Iran J Public Health 32(4):35–41. https://ijph.tums.ac.ir/index.php/ijph/article/view/1938

  4. 4.

    Alten B, Maia C, Afonso MO, Campino L, Jiménez M, González E, Toty C (2016) Seasonal dynamics of phlebotomine sand fly species proven vectors of Mediterranean leishmaniasis caused by Leishmania infantum. PLoS Negl Trop Dis 10(2):e0004458. https://doi.org/10.1371/journal.pntd.0004458

    PubMed  PubMed Central  Article  Google Scholar 

  5. 5.

    Alipour H, Darabi H, Dabbaghmanesh T, Bonyani M (2014) Entomological study of sand flies (Diptera: Psychodidae: Phlebotominae) in Asalouyeh, the heartland of an Iranian petrochemical industry. Asian Pac J Trop Biomed 4:S242–S245. https://doi.org/10.12980/APJTB.4.2014C678

    PubMed  PubMed Central  Article  Google Scholar 

  6. 6.

    Ali RM, Loutfy NF, Awad OM, Suliman NK (2016) Bionomics of phlebotomine sandfly species in west Alexandria, Egypt. J Entomol Zool Stud 4:349–353

    Google Scholar 

  7. 7.

    Aoun K, Bouratbine A (2014) Cutaneous leishmaniasis in North Africa: a review. Parasite 21:14. https://doi.org/10.1051/parasite/2014014

    PubMed  PubMed Central  Article  Google Scholar 

  8. 8.

    Arif M (1994) Systematics and biology of Phlebotomine sandflies of the visceral Leishmaniasis foci of Northern Pakistan. Doctoral Dissertation, London School of Hygiene and Tropical Medicine

  9. 9.

    Atakan E, Akbaba M, Sütoluk Z, Alptekin D, Demirhindi H, Uludağ SK (2010) Hocallıve Turunçlu (Adana) köylerindephlebotomus (Diptera; Psychodidae; Phlebotomine) türlerinin populasyonyoğunluğuvekutanöz leishmaniasis ileilişkisi. Türk Parazitol Derg 34:106–111

    Google Scholar 

  10. 10.

    Barhoumi W, Fares W, Cherni S, Derbali M, Dachraoui K, Chelbi I, Zhioua E (2016) Changes of sand fly populations and Leishmania infantum infection rates in an irrigated village located in arid central Tunisia. Int J Environ Res Public Health 13(3):329. https://doi.org/10.3390/ijerph13030329

    CAS  PubMed Central  Article  Google Scholar 

  11. 11.

    Belen A, Alten B (2011) Seasonal dynamics and altitudinal distributions of sand fly (Diptera: Psychodidae) populations in a cutaneous leishmaniasis endemic area of the Cukurova region of Turkey. J Vector Ecol 36:s1. https://doi.org/10.1111/j.1948-7134.2011.00116.x

    Article  Google Scholar 

  12. 12.

    Berger R, Wasserberg G, Warburg A, Orshan L, Kotler BP (2014) Zoonotic disease in a peripheral population: persistence and transmission of Leishmania major in a putative sink-source system in the Negev Highlands, Israel. Vector Borne Zoonotic Dis 14(8):592–600. https://doi.org/10.1089/vbz.2013.1535

    PubMed  PubMed Central  Article  Google Scholar 

  13. 13.

    Boudrissa A (2005) Étude éco-épidémiologique de la leishmaniose cutanée dans la wilaya de M’Sila, thèse de Magister, Algérie

  14. 14.

    Bounoua L, Kahime K, Houti L, Blakey T, Ebi K, Zhang P, Imhoff M 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(8):3172–3191. https://doi.org/10.3390/ijerph10083172

    PubMed  PubMed Central  Article  Google Scholar 

  15. 15.

    Boussaa S, Guernaoui S, Pesson B, Boumezzough A (2005) Seasonal fluctuations of phlebotomine sand fly populations (Diptera: Psychodidae) in the urban area of Marrakech, Morocco. Acta Trop 95(2):86–91. https://doi.org/10.1016/j.actatropica.2005.05.002

    CAS  PubMed  Article  Google Scholar 

  16. 16.

    Cross ER, Newcomb WW, Tucker CJ (1996) Use of weather data and remote sensing to predict the geographic and seasonal distribution of Phlebotomus papatasi in southwest Asia. Am J Trop Med Hyg 1996(54):530–536. https://doi.org/10.4269/ajtmh.1996.54.530

    Article  Google Scholar 

  17. 17.

    Chelbi I, Derbali M, Al-Ahmadi Z, Zaafouri B, El Fahem A, Zhioua E (2007) Phenology of Phlebotomus papatasi (Diptera: Psychodidae) relative to the seasonal prevalence of zoonotic cutaneous leishmaniasis in central Tunisia. J Med Entomol 44(2):385–388. https://doi.org/10.1093/jmedent/44.2.385

    CAS  PubMed  Article  Google Scholar 

  18. 18.

    Doha SA, Samy AM (2010) Bionomics of phlebotomine sand flies (Diptera: Psychodidae) in the province of Al-Baha, Saudi Arabia. Mem Inst Oswaldo Cruz 105(7):850–856. https://doi.org/10.1590/S0074-02762010000700002

    PubMed  Article  Google Scholar 

  19. 19.

    Dokhan MR, Kenawy MA, Doha SA, El-Hosary SS, Shaibi T, Annajar BB (2016) Entomological studies of phlebotomine sand flies (Diptera: Psychodidae) in relation to cutaneous leishmaniasis transmission in Al Rabta, North West of Libya. Acta Trop 154:95–101. https://doi.org/10.1016/j.actatropica.2015.11.004

    PubMed  Article  Google Scholar 

  20. 20.

    Durrani AZ, Durrani HZ, Kamal N (2012) Prevalence of Leishmania in sand fly in Pakistan. Pak J Zool 44(1):61–65

    Google Scholar 

  21. 21.

    Elnaiem DA, Hassan HK, Ward RD (1997) Phlebotomine sandflies in a focus of visceral leishmaniasis in a border area of eastern Sudan. Ann Trop Med Parasitol 91(3):307–318. https://doi.org/10.1080/00034983.1997.11813143

    CAS  PubMed  Article  Google Scholar 

  22. 22.

    Emami MM, Yazdi M (2008) Entomological survey of phlebotomine sand flies (Diptera: Psychodidae) in a focus of visceral leishmaniasis in central Iran. J Vector Borne Dis 45(1):38 (PMID:18399315)

    PubMed  Google Scholar 

  23. 23.

    Halimi M, Cheghabaleki ZZ, Modrek MJ, Delavari M (2016) Temporal dynamics of phlebotomine sand flies population in response to ambient TEMPERATURE variation, Bam, Kerman Province of Iran. Ann Glob Health 82(5):824–831. https://doi.org/10.1016/j.aogh.2016.07.009

    PubMed  Article  Google Scholar 

  24. 24.

    Hanafi HA, Fryauff DJ, Modi GB, Ibrahim MO, Main AM (2007) Bionomics of phlebotomine sandflies at a peacekeeping duty site in the north of Sinai, Egypt. Acta Trop 101:106–114. https://doi.org/10.1016/j.actatropica.2006.12.005

    PubMed  Article  Google Scholar 

  25. 25.

    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 

  26. 26.

    Hunter PR (2003) Climate change and waterborne and vector-borne disease. J Appl Microbiol Symp Suppl 94:37S–46S. https://doi.org/10.1046/j.1365-2672.94.s1.5.x

    Article  Google Scholar 

  27. 27.

    Karmaoui A (2018) The cutaneous leishmaniasis vulnerability index (CLVI). Acta Ecol Sin. https://doi.org/10.1016/j.chnaes.2018.01.001

    Article  Google Scholar 

  28. 28.

    Karmaoui A, Zerouali S (2018) Modeling the vulnerability to zoonotic cutaneous leishmaniasis at the local scale. Sciences 11(4):172–182. https://doi.org/10.3923/ajaps.2018.172.182

    Article  Google Scholar 

  29. 29.

    Kasap ÖE, Belen A, Kaynas S, Simsek FM, Biler L, Ata N, Alten B (2009) Activity patterns of sand fly (Diptera: Psychodidae) species and comparative performance of different traps in an endemic cutaneous leishmaniasis focus in Cukurova Plain, Southern Anatolia, Turkey. Acta Vet Brno 78(2):327–335. https://doi.org/10.2754/avb200978020327

    Article  Google Scholar 

  30. 30.

    Kassahun A, Sadlova J, Benda P, Kostalova T, Warburg A, Hailu A, Votypka J (2015) Natural infection of bats with Leishmania in Ethiopia. Acta Trop 150:166–170. https://www.nal.usda.gov/

  31. 31.

    Kassem HA, Siri J, Kamal HA, Wilson ML (2012) Environmental factors underlying spatial patterns of sand flies (Diptera: Psychodidae) associated with leishmaniasis in southern Sinai, Egypt. Acta Trop 123(1):8–15. https://doi.org/10.1016/j.actatropica.2012.02.067

    PubMed  Article  Google Scholar 

  32. 32.

    Kassiri H, Javadian E, Sharififard M (2013) Monthly activity of Phlebotominae sand flies in Sistan-Baluchistan Province, Southeast Iran. J Insect Sci 13(1):153. https://doi.org/10.1673/031.013.15301

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  33. 33.

    Kayedi MH, Abdali N, Rostami R (2016) Seasonal activity of sand flies (Diptera Psychodidae) in Khorramabad County, Lorestan Province, Iran. Nat Sci 14(1):89

    Google Scholar 

  34. 34.

    Lahouiti K, Maniar S, Bekhti K (2013) Seasonal fluctuations of phlebotomines sand fly populations (Diptera: Psychodidae) in the Moulay Yacoub province, centre Morocco: effect of ecological factors. Afr J Environ Sci Technol 7(11):1028–1031

    Google Scholar 

  35. 35.

    MohammedAl–Obaidi JL, Ibrahim K, Adnan T, Al Hadi E, Akram E, Qazi Z, Talal L (2013) Epidemiological study to investigate a possible vector of visceral leishmaniasis in the Central Region of Iraq. Al-Mustansiriyah J Sci 24(6):2013

    Google Scholar 

  36. 36.

    Morsy TA, Abou EER, Rifaat MM, Al Dakhil MA (1995) The seasonal and daily activities of Phlebotomus papatasi in Riyadh, Saudi Arabia. J Egypt Soc Parasitol 25(3):699–711 (PMID: 8586865)

    CAS  PubMed  Google Scholar 

  37. 37.

    Müller GC, Kravchenko VD, Schlein Y (2011) Seasonal and spatial changes of sand fly species in a canyon in the Carmel Mountains. J Vector Ecol 36:s1

    Article  Google Scholar 

  38. 38.

    Orshan L, Szekely D, Khalfa Z, Bitton S (2010) Distribution and seasonality of Phlebotomus sand flies in cutaneous leishmaniasis foci, Judean Desert, Israel. J Med Entomol 47(3):319–328. https://doi.org/10.1093/jmedent/47.3.319

    CAS  PubMed  Article  Google Scholar 

  39. 39.

    Orshan L, Elbaz S, Ben-Ari Y, Akad F, Afik O, Ben-Avi I, Zonstein I (2016) Distribution and dispersal of Phlebotomus papatasi (Diptera: Psychodidae) in a zoonotic cutaneous leishmaniasis focus, the Northern Negev, Israel. PLoS Negl Trop Dis 10(7):e0004819. https://doi.org/10.1371/journal.pntd.0004819

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  40. 40.

    Özbel Y, Karakuş M, Arserim SK, Kalkan ŞO, Töz S (2016) Molecular detection and identification of Leishmania spp. in naturally infected Phlebotomus tobbi and Sergentomyia dentata in a focus of human and canine leishmaniasis in western Turkey. Acta Trop 155:89–94. https://doi.org/10.1016/j.actatropica.2015.12.018

    CAS  PubMed  Article  Google Scholar 

  41. 41.

    Papadopoulos B, Tselentis Y (1994) Sandflies in the greater Athens region. Greece Parasite 1(2):131–140. https://doi.org/10.1051/parasite/1994012131

    CAS  PubMed  Article  Google Scholar 

  42. 42.

    Parvizi P, Akhoundi M, Mirzaei H (2012) Distribution, fauna and seasonal variation of sandflies, simultaneous detection of nuclear Internal transcribed spacer ribosomal DNA gene of leishmania major in Rhombomysopimus and Phlebotomus papatasi, in Natanz District in Central Part of Iran. Iran Biomed J 16(2):113. https://doi.org/10.6091/ibj.1038.2012

    PubMed  PubMed Central  Article  Google Scholar 

  43. 43.

    Pratlong F, Lami P, Ravel C, Balard Y, Dereure J, Serres G et al (2013) Geographical distribution and epidemiological features of Old World Leishmania infantum and Leishmania donovani foci, based on the isoenzyme analysis of 2277 strains. Parasitology 140:423–434. https://doi.org/10.1017/S0031182012001825(PMID: 23146283)

    CAS  PubMed  Article  Google Scholar 

  44. 44.

    Ready PD (2010) Leishmaniasis emergence in Europe. EuroSurveillance 15(10):1–11. https://doi.org/10.2807/ese.15.10.19505-en

    Article  Google Scholar 

  45. 45.

    Reza FM, Mansour N (2006) Entomological studies of Phlebotomus papatasi and P. sergenti (Diptera: Psychodidae) as vectors of cutaneous leishmaniasis in Shiraz, Iran. Southeast Asian J Trop Med Public Health 37:115–117 (PMID:17547064)

    PubMed  Google Scholar 

  46. 46.

    Sari B, Limoncu ME, Balcioglu IC, Aldemir A, Tasci GT, Kiliç Y, Olgen MK (2015) Seroepidemiological and entomological survey in a new focus of zoonotic visceral leishmaniasis in Kars province. Northeast Turk Vet Parasitol 209(3):179–187. https://doi.org/10.1016/j.vetpar.2015.02.021

    Article  Google Scholar 

  47. 47.

    Sawalha SS, Ramlawi A, Sansur RM, Salem IM, Amr ZS (2017) Diversity, ecology, and seasonality of sand flies (Diptera: Psychodidae) of the Jenin District (Palestinian Territories). J Vector Ecol 42(1):120–129. https://doi.org/10.1111/jvec.12246

    PubMed  Article  Google Scholar 

  48. 48.

    Soltani Z, Fakoorziba MR, Moemenbellah-Fard MD, Kalantari M, Akbarpour M, Faramarzi H, Azizi K (2015) Phlebotomus papatasi (Diptera: Psychodidae) as the vector of leishmania major in Kharameh District, Southern Iran. J Health Sci Surveill Syst 3(4):160–164

    Google Scholar 

  49. 49.

    Srinivasan R, Jambulingam P, Kumar NP, Selvakumar M, Edwin B, Kumar TD (2015) Temporal distribution and behaviour of sand flies (Diptera: Psychodidae) in a cutaneous leishmaniasis focus of the Kani Tribe settlements in the Western Ghats, India. Acta Trop 148:147–155. https://doi.org/10.1016/j.actatropica.2015.04.015

    CAS  PubMed  Article  Google Scholar 

  50. 50.

    Talbi FZ, El OualiLalami A, Janati Idrissi A, Sebti F, Faraj C (2015) Leishmaniasis in central Morocco: seasonal fluctuations of phlebotomine sand fly in Aichoun locality, from Sefrou province. Pathol Res Int 2015:438749. https://doi.org/10.1155/2015/438749

    Article  Google Scholar 

  51. 51.

    Wasserberg G, Yarom I, Warburg A (2003) Seasonal abundance patterns of the sandfly Phlebotomus papatasi in climatically distinct foci of cutaneous leishmaniasis in Israeli deserts. Med Vet Entomol 17(4):452–456. https://doi.org/10.1111/j.1365-2915.2003.00461.x

    CAS  PubMed  Article  Google Scholar 

  52. 52.

    WHO (2008) A human rights-based approach to neglected tropical diseases. World Health Organization, Geneva

    Google Scholar 

  53. 53.

    Yaghoobi-Ershadi MR, Marvi-Moghadam N, Jafari R, Akhavan AA, Solimani H, Zahrai-Ramazani AR, Dehghan-Dehnavi AR (2015) Some epidemiological aspects of cutaneous leishmaniasis in a new focus, central Iran. Dermatol Res Pract. https://doi.org/10.1155/2015/286408

    PubMed  PubMed Central  Article  Google Scholar 

  54. 54.

    Yaghoobi-Ershadi MR, Hakimiparizi M, Zahraei-Ramazani AR, Abdoli H, Akhavan AA, Aghasi M, Ranjbar AA (2010) Sand fly surveillance within an emerging epidemic focus of cutaneous leishmaniasis in southeastern Iran. J Arthropod Borne Dis 4(1):17 (PMCID: PMC3385542. PMID: 22808384)

    Google Scholar 

  55. 55.

    Yaghoobi-Ershadi MR, Akhavan AA, Abai MR, Ebrahimi B, Zahraei-Ramazani AR, Vafaei-Nezhad R, Jafari R (2004) Epidemiological study in a new focus of cutaneous leishmaniasis in the Islamic Republic of Iran. East Mediterr Health J 10(4–5):688. https://www.who.int/iris/handle/10665/119335

  56. 56.

    Yaghoobi-Ershadi MR, Akhavan AA, Zahraei-Ramazani AR, Jalali-Zand AR, Piazak N (2005) Bionomics of Phlebotomus papatasi (Diptera: Psychodidae) in an endemic focus of zoonotic cutaneous leishmaniasis in central Iran. J Vector Ecol 30(1):115 (PMID:16007964)

    PubMed  Google Scholar 

  57. 57.

    Yaman MEHMET, Özbel Y (2004) The sandflies (Diptera: Psychodidae) in the Turkish province of Hatay: some possible vectors of the parasites causing human cutaneous leishmaniasis. Ann Trop Med Parasitol 98(7):741–750. https://doi.org/10.1179/000349804225021415

    CAS  PubMed  Article  Google Scholar 

  58. 58.

    Yuval B, Warburg A, Schlein Y (1988) Leishmaniasis in the Jordan Valley. V. Dispersal characteristics of the sandfly Phlebotomus papatasi. Med Vet Entomol 2(4):391–395. https://doi.org/10.1111/j.1365-2915.1988.tb00213.x

    CAS  PubMed  Article  Google Scholar 

  59. 59.

    Zouirech M, Belghyti D, El Kohli M, Faraj C (2013) Entomological investigation of an emerging leishmaniasis focus in Azilal province, Morocco. Pak Entomol 35:11–15

    Google Scholar 

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Karmaoui, A. Seasonal Distribution of Phlebotomus papatasi, Vector of Zoonotic Cutaneous Leishmaniasis. Acta Parasit. 65, 585–598 (2020). https://doi.org/10.2478/s11686-020-00201-6

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Keywords

  • Sand fly
  • Phlebotomus papatasi
  • Seasonal transmission
  • Habitat preference
  • Potential risk