Genetic variation of Plasmodium and Haemoproteus parasites in birds of Iran




Malaria, PCR, blood parasites, Haemosporidian, Veterinary, Iran


Background: Plasmodium and Haemoproteus are common parasites transferred to birds by Culicidae, Ceratopogonidae, and Hippoboscidae vectors. These parasites are of particular concern to healthcare researchers and veterinarians due to their impact on avian malaria, association with other animals and humans, and phylogenetic link with human Plasmodium species.

Methods: This bibliographic review article was designed to deliver a report on the avian malaria infections of Plasmodium spp. and Haemoproteus spp. in birds in Iran. Published reports in Google Scholar, PubMed, and Science Direct were used for this revision until April 2023.

Results: The highest number of recorded infections with Haemoproteus spp. and Plasmodium spp. was found in Passeridae, as revealed by genetic analysis of Cytb DNA sequences. In this revision, following preceding investigations, the overall prevalence of Haemoproteus spp. was greater than that of Plasmodium spp. discovered by molecular techniques in Iran. Besides, the frequency of published genetic variants (lineages) of Haemoproteus is higher than that of Plasmodium. Our result indicated that the frequency of novel genetic variants Haemoproteus and Plasmodium in published reports was 38% and 12.5% of diagnosed lineages, respectively.

Conclusion: The region needs more studies to detect parasites in unexplored hosts and vectors, as there is a lack of research. Understanding the prevalence, epidemiology, transmission approach, and vectors of avian blood parasites is crucial for pet health care, zoos, parks, aviaries, and rehabilitation facilities.

Author Biography

Leila Nourani, Pasteur Institute of Iran

Malaria and Vector Research Group (MVRG), Biotechnology Research Center (BRC), Pasteur Institute of Iran, Tehran, Iran


Atkinson CT, Thomas NJ, Hunter DB. Parasitic diseases of wild birds: John Wiley & Sons; 2009.

Atkinson CT, van Riper III C. Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. Bird–parasite interactions. 1991:19-48.

Ferraguti M, Martínez-de la Puente J, Muñoz J, Roiz D, Ruiz S, Soriguer R, et al. Avian Plasmodium in Culex and Ochlerotatus mosquitoes from southern Spain: effects of season and host-feeding source on parasite dynamics. PloS One. 2013;8(6):e66237.

Bensch S, Stjernman M, Hasselquist D, Örjan Ö, Hannson B, Westerdahl H, et al. Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc Royal Soc B. 2000;267(1452):1583-9.

Palinauskas V, Iezhova TA, Križanauskienė A, Markovets MY, Bensch S, Valkiūnas G. Molecular characterization and distribution of Haemoproteus minutus (Haemosporida, Haemoproteidae): a pathogenic avian parasite. Parasitol Int. 2013;62(4):358-63.

Valkiūnas G, Iezhova TA, Brooks DR, Hanelt B, Brant SV, Sutherlin ME, et al. Additional observations on blood parasites of birds in Costa Rica. J Wildl Dis. 2004;40(3):555-61.

Nourani L, Zakeri S, Dinparast Djadid N. Dynamics of prevalence and distribution pattern of avian Plasmodium species and its vectors in diverse zoogeographical areas-A review. Infect Genet Evol. 2020;81:104244.

Oakgrove KS, Harrigan RJ, Loiseau C, Guers S, Seppi B, Sehgal RN. Distribution, diversity and drivers of blood-borne parasite co-infections in Alaskan bird populations. Int J Parasitol. 2014;44(10):717-27.

Synek P, Albrecht T, Vinkler M, Schnitzer J, Votýpka J, Munclinger P. Haemosporidian parasites of a European passerine wintering in South Asia: diversity, mixed infections and effect on host condition. Parasitol Res. 2013;112(4):1667-77.

Bensch S, Waldenström J, Jonzén N, Westerdahl H, Hansson B, Sejberg D, et al. Temporal dynamics and diversity of avian malaria parasites in a single host species. J Anim Ecol. 2007;76(1):112-22.

Zehtindjiev P, Ilieva M, Westerdahl H, Hansson B, Valkiūnas G, Bensch S. Dynamics of parasitemia of malaria parasites in a naturally and experimentally infected migratory songbird, the great reed warbler Acrocephalus arundinaceus. Exp Parasitol. 2008;119(1):99-110.

Zélé F, Vézilier J, L’Ambert G, Nicot A, Gandon S, Rivero A, et al. Dynamics of prevalence and diversity of avian malaria infections in wild Culex pipiens mosquitoes: the effects of Wolbachia, filarial nematodes and insecticide resistance. Parasit Vector. 2014;7(1):437.

Belo N, Passos L, Júnior L, Goulart C, Sherlock T, Braga E. Avian malaria in captive psittacine birds: Detection by microscopy and 18S rRNA gene amplification. Prevent Vet Med. 2009;88(3):220-4.

Ciloglu A, Yildirim A, Duzlu O, Onder Z, Dogan Z, Inci A. Investigation of avian haemosporidian parasites from raptor birds in Turkey, with molecular characterisation and microscopic confirmation. Folia Parasitol. 2016;63.

Tostes R, Vashist U, Scopel KK, Massard CL, Daemon E, D'Agosto M. Plasmodium spp. and Haemoproteus spp. infection in birds of the Brazilian Atlantic Forest detected by microscopy and polymerase chain reaction. Pesq Vet Bras. 2015;35(1):67-74.

Valkiunas G, Iezhova TA, Krizanauskiene A, Palinauskas V, Sehgal RN, Bensch S. A comparative analysis of microscopy and PCR-based detection methods for blood parasites. J Parasitol. 2008;94(6):1395-401.

Zehtindjiev P, Krizanauskiene A, Bensch S, Palinauskas V, Asghar M, Dimitrov D, et al. A new morphologically distinct avian malaria parasite that fails detection by established polymerase chain reaction-based protocols for amplification of the cytochrome B gene. J Parasitol. 2012;98(3):657-65.

Nourani L, Aliabadian M, Mirshamsi O, Dinparast Djadid N. Molecular detection and genetic diversity of avian haemosporidian parasites in Iran. PloS One. 2018;13(11):e0206638.

Nourani L, Aliabadian M, Mirshamsi O, Dinparast Djadid N. Prevalence of co-infection and genetic diversity of avian haemosporidian parasites in two rehabilitation facilities in Iran: implications for the conservation of captive raptors. BMC Ecol Evol. 2022;22(1):114.

Nourani L, Baghkheirati AA, Zargar M, Karimi V, Djadid ND. Haemoproteosis and avian malaria in Columbidae and Corvidae from Iran. Vet Med Sci. 2021;7(5):2043-50.

Nourani L, Dinparast Djadid N, editors. Molecular identification of avian malaria in wild birds from Iran. 2nd International Congress of Climate Change & vector borne Diseases and 4th National Congress of Medical; 2019.

Nourani L, Djadid ND, Rabiee K, Mezerji MS, Shakiba M, Bakhshi H, et al. Detection of haemosporidian parasites in wild and domestic birds in northern and central provinces of Iran: Introduction of new lineages and hosts. Int J Parasitol: Parasit and Wildl. 2020;13:203-12.

Bobeva A, Ilieva M, Dimitrov D, Zehtindjiev P. Degree of associations among vectors of the genus Culicoides (Diptera: Ceratopogonidae) and host bird species with respect to haemosporidian parasites in NE Bulgaria. Parasitol Res. 2014;113(12):4505-11.

Dinhopl N, Mostegl MM, Richter B, Nedorost N, Maderner A, Fragner K, et al. Application of in-situ hybridization for the detection and identification of avian malaria parasites in paraffin wax-embedded tissues from captive penguins. Avian Pathol. 2011;40(3):315-20.

Scaglione FE, Cannizzo FT, Pregel P, Perez Rodriguez AD, Bollo E. Blood parasites in hooded crows (Corvus corone cornix) in Northwest Italy. Vet Itali. 2016;52(2):111-6.

Shurulinkov P, Chakarov N, Daskalova G. Blood parasites, body condition, and wing length in two subspecies of yellow wagtail (Motacilla flava) during migration. Parasitol Res. 2012;110(5):2043-51.

Bensch S, Hellgren O, Pérez‐Tris J. MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol Ecol Res. 2009;9(5):1353-8.

Krone O, Priemer J, Streich J, Sommer P, Langgemach T, Lessow O. Haemosporida of birds of prey and owls from Germany. Acta Protozool. 2001;40(4):281-90.

Krone O, Waldenström J, Valkiūnas G, Lessow O, Müller K, Iezhova T, et al. Haemosporidian blood parasites in European birds of prey and owls. J Parasitol. 2008;94(3):709-15.

Chasar A, Loiseau C, Valkiūnas G, Iezhova T, Smith TB, Sehgal RN. Prevalence and diversity patterns of avian blood parasites in degraded African rainforest habitats. Mol Ecol. 2009;18(19):4121-33.

Drovetski SV, Aghayan SA, Mata VA, Lopes RJ, Mode NA, Harvey JA, et al. Does the niche breadth or trade‐off hypothesis explain the abundance–occupancy relationship in avian Haemosporidia? Mol Ecol. 2014;23(13):3322-9.

Hellgren O, Waldenström J, Peréz‐Tris J, Szöll E, Si Ö, Hasselquist D, et al. Detecting shifts of transmission areas in avian blood parasites-a phylogenetic approach. Mol Ecol. 2007;16(6):1281-90.

Kim K, Tsuda Y. Seasonal changes in the feeding pattern of Culex pipiens pallens govern the transmission dynamics of multiple lineages of avian malaria parasites in Japanese wild bird community. Mol Ecol. 2010;19(24):5545-54.

Kim K, Tsuda Y. Avian Plasmodium lineages found in spot surveys of mosquitoes from 2007 to 2010 at Sakata wetland, Japan: do dominant lineages persist for multiple years? Mol Ecol. 2012;21(21):5374-85.

Scordato ES, Kardish MR. Prevalence and beta diversity in avian malaria communities: host species is a better predictor than geography. J Anim Ecol. 2014;83(6):1387-97.

Dickinson E, Remsen Jr J. The Howard and Moore Complete Checklist of the Birds of the World. 1 Non-passerines. Aves Press, Eastbourne, UK l; 2013.

Scott DA, Adhami A. An updated checklist of the birds of Iran. Podoces. 2006;1(1/2):1-16.

Nourani L, Aliabadian M, Dinparast-Djadid N, Mirshamsi O. New Host Records for Haemoproteus spp. (Apicomplexa: Haemosporidiasina) in Passeriformes from North-West of Iran. J arthropod-born Dis. 2017;11(2):236.

Nourani L, Aliabadian M, Djadid Nd, Mirshamsi O. Occurrence of Haemoproteus spp. (Haemosporida: Haemoproteidae) in New Host Records of Passerine Birds from the East of Iran. Iran J Parasitol. 2018;13(2):267-74.

Nourani L, Aliabadian M, Mirshamsi O, Djadid ND, editors. Detection of the avian blood parasites from northeast of Iran. 1st International Congress on Vector-Borne Diseases and Climate Change; 2017.

Nourani L, Aliabadian M, Amini H, Mirshamsi O. Prevalence of haemosporidian parasite infections in raptors of Iran. J Rapt Res. 2020;54(4):455-62.

Rahmati M, Norouzian H, Nayebzadeh H, Shokrani H. Molecular Detection and Phylogenetic Analysis of Avian Haemosporidian Parasites in House Sparrows (Passer domesticus) of Western Iran. J Wildl Dis. 2023.

Shokrani H, Norouzian H, Dezfoulian O. Exo-erythrocytic stages of Haemoproteus sp. in common buzzard (Buteo buteo): A histopathological and molecular study. Int J Parasitol: Parasit and Wildl. 2021;16:64-9.

Amrei SFE, Haghi AM, Nateghpour M, Mohebali M, Youssefi MR, Raiesi O, et al. Detection of Malaria Parasites and Other Haemosporidia in Migratory and Native Birds in Mazandaran and Golestan Provinces, Iran. J Arthorpod-Born Dis. 2022;16(1):26–33-26–33.

Fakhar M, Kalani H, Rahimi-Esboei B, Armat S. Hemoprotozoa in free-ranging birds from rural areas of Mazandaran Province, northern Iran. Comp Clin Path. 2013;22(3):509-12.

Ghaemitalab V, Mirshamsi O, Valkiūnas G, Aliabadian M. Prevalence and Genetic Diversity of Avian Haemosporidian Parasites in Southern Iran. Pathogens. 2021;10(6):645.

Gorji SF, Shemshadi B, Habibi H, Jalali S, Davary M, Sepehri M. Survey on parasites in sparrows of Amol (Mazandaran Province, Iran). J Life Sci. 2012;6(7):783.

Mirzaei F, Siyadatpanah A, Norouzi R, Pournasir S, Nissapatorn V, Pereira MdL. Blood parasites in domestic birds in Central Iran. Vet Sci. 2020;7(3):126.

Mohaghegh MA, Namdar F, Azami M, Ghomashlooyan M, Kalani H, Hejazi SH. The first report of blood parasites in the birds in Fasa district, Southern Iran. Comp Clin Path. 2018;27(2):289-93.

Shemshadi B, Ranjbar-Bahadori S, Faghihzadeh-Gorgi S. Occurrence of parasitic protozoa in wild waterfowl in southern coastal Caspian sea lagoons. Iran J Vet Med. 2015;8(4):261-7.

Valkiūnas G. Avian malaria parasites and other haemosporidia: CRC press; 2005.

Waldenström J, Bensch S, Kiboi S, Hasselquist D, Ottosson U. Cross‐species infection of blood parasites between resident and migratory songbirds in Africa. Mol Ecol. 2002;11(8):1545-54.

Nazifi S, Razavi S, Yavari F, Rajaifar M, Bazyar E, Esmailnejad Z. Evaluation of hematological values in indigenous chickens infected with Plasmodium gallinaceum and Aegyptianella pullorum. Comp Clin Path. 2008;17(3):145.

Kalani H, Faridnia R, Pestechian N, Cheraghipor K. The first report of hematozoa in migratory and native birds in Isfahan Province, Iran. Comp Clin Path. 2015;24(1):65-8.

Motta ROC, Marques MVR, Junior FCF, de Assis Andery D, Horta RS, Peixoto RB, et al. Does haemosporidian infection affect hematological and biochemical profiles of the endangered Black-fronted piping-guan (Aburria jacutinga)? PeerJ. 2013;1:e45.

Deem SL. The role of veterinarians in the conservation of avian species. J Avian Med Surg. 2011;25(3):225-30.

Deem SL, Karesh WB, Weisman W. Putting theory into practice: wildlife health in conservation. Conserv Biol. 2001;15(5):1224-33.

Aghayan S. Migratory birds as a tool to colonize new territories for avian haemosporidians. ЕСТЕСТВЕННЫЕ НАУКИ. 2012;1:18.

Fallon SM, Fleischer RC, Graves GR. Malarial parasites as geographical markers in migratory birds? Biol Let. 2006;2(2):213-6.

Gutierrez-Lopez R, Gangoso L, Martinez-de la Puente J, Fric J, Lopez-Lopez P, Mailleux M, et al. Low prevalence of blood parasites in a long-distance migratory raptor: the importance of host habitat. Parasit Vector. 2015;8:189.

Hubálek Z. An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildl Dis. 2004;40(4):639-59.

Dezfoulian O, Zibaei M, Nayebzadeh H, Haghgoo M, Emami-Razavi A, Kiani K. Leucocytozoonosis in domestic birds in southwestern iran: an ultrastructural study. Iran J Parasitol. 2013;8(1):171.

Laird M. Plasmodium durae Herman from the introduced common peafowl in northern Nigeria. J Protozool. 1978;25(1):21-4.




How to Cite

Nourani, L. (2024). Genetic variation of Plasmodium and Haemoproteus parasites in birds of Iran . Afghanistan Journal of Infectious Diseases, 2(1), 51–62.