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Re-Emerging foci of visceral leishmaniasis in Armenia – first molecular diagnosis of clinical samples

Published online by Cambridge University Press:  13 February 2019

Anna Sukiasyan ,
Ara Keshishyan ,
Dezdemonia Manukyan ,
Gayane Melik-Andreasyan ,
Liana Atshemyan ,
Hripsime Apresyan ,
Margarita Strelkova ,
Marcus Frohme ,
Sofia Cortes Open the ORCID record for Sofia Cortes [Opens in a new window]  and
Katrin Kuhls Open the ORCID record for Katrin Kuhls [Opens in a new window]
Anna Sukiasyan
Affiliation:
Research Institute of Epidemiology, Virology and Medical Parasitology after A.B. Alexanyan, Ministry of Health, 1 Khudyakov St., 0063, Yerevan, Armenia Division Molecular Biotechnology and Functional Genomics, Technical University of Applied Sciences Wildau, Hochschulring 1, 15745 Wildau, Germany
Ara Keshishyan
Affiliation:
Research Institute of Epidemiology, Virology and Medical Parasitology after A.B. Alexanyan, Ministry of Health, 1 Khudyakov St., 0063, Yerevan, Armenia
Dezdemonia Manukyan
Affiliation:
Research Institute of Epidemiology, Virology and Medical Parasitology after A.B. Alexanyan, Ministry of Health, 1 Khudyakov St., 0063, Yerevan, Armenia
Gayane Melik-Andreasyan
Affiliation:
Research Institute of Epidemiology, Virology and Medical Parasitology after A.B. Alexanyan, Ministry of Health, 1 Khudyakov St., 0063, Yerevan, Armenia
Liana Atshemyan
Affiliation:
Research Institute of Epidemiology, Virology and Medical Parasitology after A.B. Alexanyan, Ministry of Health, 1 Khudyakov St., 0063, Yerevan, Armenia
Hripsime Apresyan
Affiliation:
Yerevan State Medical University after Mkitar Heratsi, 2 Koryun str., 0025, Yerevan, Armenia
Margarita Strelkova
Affiliation:
Martsinovsky Institute of Medical Parasitology, Tropical and Vector-Born Diseases, Sechenov First Moscow State Medical University, Malaya Pirogovskaya 20, 119830 Moscow, Russion Federation
Marcus Frohme
Affiliation:
Division Molecular Biotechnology and Functional Genomics, Technical University of Applied Sciences Wildau, Hochschulring 1, 15745 Wildau, Germany
Sofia Cortes
Affiliation:
Division Molecular Biotechnology and Functional Genomics, Technical University of Applied Sciences Wildau, Hochschulring 1, 15745 Wildau, Germany Global Health and Tropical Medicine, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Rua da Junqueira No 100, 1349-008 Lisboa, Portugal
Katrin Kuhls*
Affiliation:
Division Molecular Biotechnology and Functional Genomics, Technical University of Applied Sciences Wildau, Hochschulring 1, 15745 Wildau, Germany
*
Author for correspondence: Katrin Kuhls, E-mail: Katrin.Kuhls@th-wildau.de
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Abstract

Visceral leishmaniasis (VL) was firstly reported in Armenia in 1913. Following a considerable increase of the number of cases until the mid 1950s, the disease disappeared after 1969 and re-emerged in 1999. Scientific literature about VL in Armenia is available only in Russian or Armenian. This paper presents a historical overview about leishmaniasis in Armenia based on this literature as well as an epidemiological update since the re-emergence of the disease. In 1999–2016, 116 indigenous VL cases were recorded mainly in children in 8 of the 11 districts, however, VL is underreported because of lack of trained medical personal and diagnostic facilities. The aim of this work was to apply for the first time molecular diagnosis of VL in Armenia. Out of 25 VL suspected patients, 22 were positive by microscopy and polymerase chain reaction (PCR). Genotyping using internal transcribed spacer 1-PCR-restriction fragment length polymorphism and sequencing identified the causative agent of VL in Armenia as Leishmania infantum. The present work is an important step towards the inclusion of molecular techniques in the current diagnosis of VL in Armenia and the establishment of local molecular diagnostic facilities.

Keywords

Armeniaemerging infectious diseasesLeishmania infantummolecular diagnosismolecular typingneglected tropical diseasessouthern caucasus regionvisceral leishmaniasis
Type
Research Article
Information
Parasitology , Volume 146 , Issue 7 , June 2019 , pp. 857 - 864
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Copyright
Copyright © Cambridge University Press 2019 

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Footnotes

*

Current affiliation: Department of Biology and Pathology, Medical Faculty of the Yerevan Haybusak University, Yerevan, Armenia

†

Current affiliation: Global Health & Tropical Medicine, Global Health and Tropical Medicine, Instituto de Higiene e Medicina Tropical, UNL, Lisbon, Portugal

References

Abdinia, B, Oliaei-Motlagh, M and Teimouri-Dereshki, A (2016) Pediatric visceral leishmaniasis in northwest of Iran. Medicine (Baltimore) 95, e5261.Google Scholar
Akhoundi, M, Kuhls, K, Cannet, A, Votypka, J, Marty, P, Delaunay, P and Sereno, D (2016) A historical overview of the classification, evolution, and dispersion of Leishmania Parasites and Sandflies. PLoS Neglected Tropical Diseases 10, e0004349.Google Scholar
Akhoundi, M, Downing, T, Votypka, J, Kuhls, K, Lukes, J, Cannet, A, Ravel, C, Marty, P, Delaunay, P, Kasbari, M, Granouillac, B, Gradoni, L and Sereno, D (2017) Leishmania infections: Molecular targets and diagnosis. Molecular Aspects of Medicine 57, 1–29.Google Scholar
Al-Jawabreh, A, Schoenian, G, Hamarsheh, O and Presber, W (2006) Clinical diagnosis of cutaneous leishmaniasis: a comparison study between standardized graded direct microscopy and ITS1-PCR of Giemsa-stained smears. Acta Tropica 99, 55–61.Google Scholar
Alvar, J, Velez, ID, Bern, C, Herrero, M, Desjeux, P, Cano, J, Jannin, J and den Boer, M (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS ONE 7, e35671.Google Scholar
Babuadze, G, Alvar, J, Argaw, D, de Koning, HP, Iosava, M, Kekelidze, M, Tsertsvadze, N, Tsereteli, D, Chakhunashvili, G, Mamatsashvili, T, Beria, N, Kalandadze, I, Ejov, M and Imnadze, P (2014) Epidemiology of visceral leishmaniasis in Georgia. PLoS Neglected Tropical Diseases 8, e2725.Google Scholar
Babuadze, G, Farlow, J, de Koning, HP, Carrillo, E, Chakhunashvili, G, Murskvaladze, M, Kekelidze, M, Karseladze, I, Kokaia, N, Kalandadze, I, Tsereteli, D, Markhvashvili, I, Sidamonidze, K, Chanturia, G, Adeishvili, E and Imnadze, P (2016) Seroepidemiology and molecular diversity of Leishmania donovani complex in Georgia. Parasites & Vectors 9, 279.Google Scholar
Baranets, MS, Darchenkova, NN, Ponirovskii, EN and Zhirenkina, EN (2011) [The spread and epidemiological value of sandflies (Diptera, Psychodidae, Phlebotominae) of the Caucasus]. Meditsinskaia parazitologiia (Mosk) 2, 10–15.Google Scholar
Barati, M, Mohebali, M, Alimohammadian, MH, Khamesipour, A, Akhoundi, B and Zarei, Z (2015) Canine visceral leishmaniasis: seroprevalence survey of asymptomatic dogs in an endemic area of northwestern Iran. The Journal of Parasitic Diseases 39, 221–224.Google Scholar
Croft, SL and Olliaro, P (2011) Leishmaniasis chemotherapy – challenges and opportunities. Clinical Microbiology and Infection 17, 1478–1483.Google Scholar
Darchenkova, NN and Dergacheva, TI (1989) [Patterns in the distribution of visceral leishmaniasis in Transcaucasia]. Meditsinskaia parazitologiia (Mosk) 4, 28–33.Google Scholar
Dergacheva, TI and Oganesian, IA (1987) [Present status of vector populations of the causative agent of leishmaniasis in Armenia]. Meditsinskaia parazitologiia (Mosk) 4, 31–34.Google Scholar
el Tai, NO, Osman, OF, el Fari, M, Presber, W and Schonian, G (2000) Genetic heterogeneity of ribosomal internal transcribed spacer in clinical samples of Leishmania donovani spotted on filter paper as revealed by single-strand conformation polymorphisms and sequencing. Transactions of the Royal Society of Tropical Medicine and Hygiene 94, 575–579.Google Scholar
Giorgobiani, E, Lawyer, PG, Babuadze, G, Dolidze, N, Jochim, RC, Tskhvaradze, L, Kikaleishvili, K and Kamhawi, S (2012) Incrimination of Phlebotomus kandelakii and Phlebotomus balcanicus as vectors of Leishmania infantum in Tbilisi, Georgia. PLoS Neglected Tropical Diseases 6, e1609.Google Scholar
Gishgorn, AJ (1925) [A case of leishmaniasis in a child]. Russian Journal of Tropical Medicine 4, 47.Google Scholar
Gurko, AG (1913) [Four cases of Kala-azar disease]. Medical Review 79, 346–348.Google Scholar
Isaev, LM (1959) [Eradication of leishmaniasis in the USSR during the 7-year-plan]. Meditsinskaia parazitologiia (Mosk) 28, 323–327.Google Scholar
Isaev, LM and Ryabtsev, FI (1958) [Pathogenesis of visceral leishmaniasis in dogs]. Transactions of the Institute of Malaria and Medical Parasitology of Uzbekistan (Samarkand) [Trudy Uzb Inst Malarii i Med Parasitol (Samarkand)] 3, 51.Google Scholar
Isahakyan, AI (1924) [Human and canine leishmaniasis in Armenia and neighboring countries]. Transactions of the Armenian Tropical Institute [Trudy Trop Inst Armenii] 1, 115–138.Google Scholar
Karagezian, LA (1966) [Cutaneous leishmaniasis (Borovskii's disease) in Armenia]. Vestnik Dermatologii i Venerologii 40, 61–64.Google Scholar
Karapetyan, RM (1949) [The case of visceral leishmaniasis in an adult in Yerevan]. Transactions of the Institute of Malaria and Medical Parasitology [Trudy Inst Malarii i Med Parasitol] 4, 152–156.Google Scholar
Karapetyan, RM (1972) [A source of invasion and the natural focality of visceral leishmaniasis in the Armenian SSR]. Meditsinskaia parazitologiia (Mosk) 41, 444–448.Google Scholar
Karapetyan, RM and Baghdasaryan, AB (1970) [Nosogeography of leishmaniasis in the Armenian SSR]. Journal of Experimental and Clinical Medicine 10, 91–95.Google Scholar
Karapetyan, RM and Baghdasaryan, AB (1972) [On the question of distribution of leishmaniasis in Transcaucasia]. Meditsinskaia parazitologiia (Mosk) 3, 291–297.Google Scholar
Karapetyan, RM, Petrosyan, NA, Mnatsakanyan, SS and Avetisyan, AG (1960) [Experiences in the control of visceral leishmaniasis in the city of Yerevan]. Meditsinskaia parazitologiia (Mosk) 6, 665–670.Google Scholar
Karapetyan, RM, Vopyan, DS and Mnatsakanyan, SS (1970) [Leishmaniasis in Armenia] In [Current Problems in Medical Parasitology and Tropical Medicine. Collection of scientific works]. Tbilisi, Georgia: Georgian Scientific Research Institute of Medical Parasitology and Tropical Medicine, pp. 75–79.Google Scholar
Keshishyan, AS and Manukyan, DV (2003) [Improvement of the epidemiological surveillance of leishmaniasis considering the climate changes in Armenia]. In Gabrielyan AH (ed). [Armenia- Challenges of Climate Change] Collected articles, Issue 2. Yerevan, Armenia: Lusabats Publishing House, pp. 237–241.Google Scholar
Keshishyan, A, Grigoryan, OR, Manukyan, DV and Hovsepyan, AA (2013a) [Reported cases of leishmaniasis in Nagorno-Karabach]. In Research Institute of Epidemiology, Virology and Medical Parasitology after A.B. Alexanyan, Ministry of Health, Yerevan, Armenia (eds), Recent Questions in Epidemiology. Yerevan, Armenia: Research Institute of Epidemiology, Virology and Medical Parasitology after A.B. Alexanyan, Ministry of Health, pp. 132–134.Google Scholar
Keshishyan, A, Manukyan, DV and Melik-Andreasyan, G (2013b) Climate change and the problem of Malaria in Armenia. World Academy of Science, Engineering and Technology 75, 522–525.Google Scholar
Kovalenko, DA, Razakov, SA, Ponirovsky, EN, Warburg, A, Nasyrova, RM, Ponomareva, VI, Fatullaeva, AA, Nasereddin, A, Klement, E, Alam, MZ, Schnur, LF, Jaffe, CL, Schonian, G and Baneth, G (2011) Canine leishmaniosis and its relationship to human visceral leishmaniasis in Eastern Uzbekistan. Parasites & Vectors 4, 58.Google Scholar
Kuhls, K, Mauricio, IL, Pratlong, F, Presber, W and Schonian, G (2005) Analysis of ribosomal DNA internal transcribed spacer sequences of the Leishmania donovani complex. Microbes and Infection 7, 1224–1234.Google Scholar
Mamikonyan, MM (1935) [Canine leishmaniasis in Yerevan]. Transactions of the Veterinary Research Institute of Armenia [Trudy Nauch Islied Vet Inst Armenii] 2, 183–185.Google Scholar
Meredith, SE, Zijlstra, EE, Schoone, GJ, Kroon, CC, van Eys, GJ, Schaeffer, KU, el-Hassan, AM and Lawyer, PG (1993) Development and application of the polymerase chain reaction for the detection and identification of Leishmania parasites in clinical material. Archives de l'Institut Pasteur de Tunis 70, 419–431.Google Scholar
Millan, J, Ferroglio, E and Solano-Gallego, L (2014) Role of wildlife in the epidemiology of Leishmania infantum infection in Europe. Parasitology Research 113, 2005–2014.Google Scholar
Mirzoyan, AA (1941) [About the epidemiology of cutaneous leishmaniasis in the Gorish region of the Armenian SSR]. Journal of the Soviet Health Care of Turkmenistan 1–2, 68–80.Google Scholar
Paronyan, L, Apresyan, H, Galstyan, A, Keshishyan, A and Vanyan, A (2015) Trends in visceral leishmaniasis in Armenia 1999–2014. In International Conference on Emerging Infectious Diseases 2015 poster and oral presentation abstacts. Emerg Inf Dis 2015 Sep p. 396. http://www.cdc.gov/EID/pdfs/ICEID2015.pdf.Google Scholar
Paronyan, L, Apresyan, H, Avetisyan, G, Tunyan, A, Gevorgyan, K, Babyan, L and Vanyan, A (2017) Visceral Leishmaniasis as re-emerging problem in Armenia, seroepidemiological study, 2015–2016. In Organizing committee - Instituto Salud Carlos III (ISCIII), Spain; Drugs for Neglected Diseases Initiative (DNDi), Switzerland (J. Alvar, J. Moreno) Abstracts Book – 6th World Congress on Leishmaniasis, 16–20 May, Abstract C2059. Toledo, Spain, p. 1462. www.worldleish2017.org/documents/Abstracts_Book_WL6_2017.pdfGoogle Scholar
Pirumov, KN (1957) [Materials for promoting control of parasitic diseases in Armenian SSR]. Meditsinskaia parazitologiia (Mosk) 5, 578–581.Google Scholar
Rajabi, M, Pilesjo, P, Bazmani, A and Mansourian, A (2017) Identification of Visceral Leishmaniasis-susceptible areas using spatial modelling in Southern Caucasus. Zoonoses and Public Health 64, e5–e22.Google Scholar
Ready, PD (2014) Epidemiology of visceral leishmaniasis. Clinical Epidemiology 6, 147–154.Google Scholar
Saladze, I (1964) [Geographical distribution of sand flies in Georgia]. Transactions of the Virsaladze Institute of Parasitology and Tropical Medicine [Trudy Inst Parazitol i Trop Med im. Virzaladze] 5, 261–265.Google Scholar
Schonian, G, Schweynoch, C, Zlateva, K, Oskam, L, Kroon, N, Graser, Y and Presber, W (1996) Identification and determination of the relationships of species and strains within the genus Leishmania using single primers in the polymerase chain reaction. Molecular and Biochemical Parasitology 77, 19–29.Google Scholar
Schonian, G, Nasereddin, A, Dinse, N, Schweynoch, C, Schallig, HD, Presber, W and Jaffe, CL (2003) PCR diagnosis and characterization of Leishmania in local and imported clinical samples. Diagnostic Microbiology and Infectious Disease 47, 349–358.Google Scholar
Schonian, G, Kuhls, K and Mauricio, IL (2011) Molecular approaches for a better understanding of the epidemiology and population genetics of Leishmania. Parasitology 138, 405–425.Google Scholar
Soleimanzadeh, G, Edrissian, GH, Movahhed-Danesh, AM and Nadim, A (1993) Epidemiological aspects of kala-azar in Meshkin-Shahr, Iran: human infection. Bulletin of the World Health Organization 71, 759–762.Google Scholar
Steverding, D (2017) The history of leishmaniasis. Parasites & Vectors 10, 82.Google Scholar
Strelkova, MV, Ponirovsky, EN, Morozov, EN, Zhirenkina, EN, Razakov, SA, Kovalenko, DA, Schnur, LF and Schonian, G (2015) A narrative review of visceral leishmaniasis in Armenia, Azerbaijan, Georgia, Kazakhstan, Kyrgyzstan, Tajikistan, Turkmenistan, Uzbekistan, the Crimean Peninsula and Southern Russia. Parasites & Vectors 8, 330.Google Scholar
Sukiasyan, A, Keshishyan, A, Manukyan, D, Malik-Andreasyan, G, Atshemyan, L, Frohme, M, Cortes, S and Kuhls, K (2017) Visceral Leishmaniasis in Armenia – first time use of molecular diagnosis. In Organizing committee - Instituto Salud Carlos III (ISCIII), Spain; Drugs for Neglected Diseases Initiative (DNDi), Switzerland (J. Alvar, J. Moreno) Abstracts Book – 6th World Congress on Leishmaniasis, 16–20 May, Abstract C0753, Vol. Abstract C0753. Toledo, Spain, p. 1389. www.worldleish2017.org/documents/Abstracts_Book_WL6_2017.pdfGoogle Scholar
Van der Auwera, G, Bart, A, Chicharro, C, Cortes, S, Davidsson, L, Di Muccio, T, Dujardin, JC, Felger, I, Paglia, MG, Grimm, F, Harms, G, Jaffe, CL, Manser, M, Ravel, C, Robert-Gangneux, F, Roelfsema, J, Toz, S, Verweij, JJ and Chiodini, PL (2016) Comparison of Leishmania typing results obtained from 16 European clinical laboratories in 2014. Euro Surveillance 21, pii=30418.Google Scholar
Vermishev, M (2010) [Pecularities of the economic development in Armenia in the context of climate change] In On the way to Copenhagen. Armenia ahead of the 15th Conference of the Parties on Climate Change, pp. 21–22. Yerevan.Google Scholar
WHO (2010) Control of the leishmaniases. World Health Organ Tech Rep Ser, xii-xiii, 1–186, back cover.Google Scholar
WHO (2015) Investing to Overcome the Global Impact of Neglected Tropical Diseases: Third WHO Report on Neglected Tropical Diseases. Geneva, Switzerland: World Health Organization.Google Scholar
Wright, JH (1903) Protozoa in a case of tropical ulcer (“Delhi Sore”). The Journal of Medical Research 10, 472–482, 477.Google Scholar