Prevalence and new histopathological aspects of Haemoproteus spp. in pigeons from Iran


Keywords:
Haemoproteus spp Pigeon Semi- nested PCR Histopathology Iran
S. BAHRAMI
S. ESMAEILZADEH
A. R. ALBORZI
S. NIKNEJAD
Abstract

Haemoproteus spp. is pathogenic protozoan that effecting blood circulatory system of birds. The present study was undertaken to evaluate the presence of Haemoproteus spp. in pigeons from Iran and associatedhistopathological changes. A total of 108 blood samples were taken from pigeons to investigate Haemoproteus spp. presence by blood smear and semi-nested PCR targeting the cytochrome b gene methods. Also, to evaluate histopathological changes 12 infected pigeons to Haemoproteus were sacrificed and studied. 34.2% of pigeons infected with Haemoproteus showed macro and microgametocytes in their erythrocytes while based on the molecular method 63.8% were infected. Focal lymphocytic aggregates, pigmentation and cell swelling were the main histopathological lesions in infected livers. Multifocal non- suppurative interstitial nephritis, pigmentation and splenic lymphoid hyperplasia were also seen in the infected pigeons. Mild lymphocytic myocarditis in the heart of one pigeon was the other finding. No histopathological changes were seen in brain, intestine, and pancreas. Schizonts with variable shapes and sizes were detected in infected livers, lungs, kidneys, and spleens but megaloschizonts were not found. This study also reports the molecular prevalence of Haemoproteus spp. in Iran

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Atkinson CT, Woods KL, Dusek RJ, Sileo LS & Iko WM (1995) Wildlifedisease and conservation in Hawaii: pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected Iiwi (Vestiaria coccinea). Parasitol 111(S1): 59-69.
Atkinson CT, Greiner EC & Forrester DJ (1986) Pre-erythrocytic development and associated host responses to Haemoproteus meleagridis (Haemosporina: Haemoproteidae) in experimentally infected domestic turkeys. J Protozool 33: 375-381.
Atkinson CT, Forrester DJ & Greiner EC (1988) Pathogenicity of Haemoproteus meleagridis (Haemosporina: Haemoproteidae) in experimentally infected domestic turkeys. J Protozool 74: 228-239.
Atkinson CT & Van Riper IIIC (1991) Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. Vol 1, 1th ed, Oxford University Press, London, PP: 30-38.
Atkinson CT, Dusek RJ, Woods KL & Iko WM (2000) Pathogenicity of avian malaria in experimentally-infected Hawaii Amakihi. J Wildl Dis 36(2): 197-201.
Baker JR (1966) The host-restriction of Haemoproteus sp. indet. of the wood pigeon Columba p. palumbus. J Protozool 13: 406-418.
Bennett GF, Peirce MA & Ashford RW (1993) Avian haematozoa: mortality and pathogenicity. J Nat Hist 27: 993-1001.
Bensch S, Stjernman M, Hasselquist D, Örjan Ö, Hannson B, Westerdahl H & Pinheiro RT (2000) Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc R Soc Lond B Biol Sci 267(1452): 1583-1589.
Bermudez AJ (2003) Miscellaneous and sporadic protozoal infections. In: Diseases of poultry, ed. Saif YM, Barnes HJ, Glisson JR, et al., 11th ed., pp. 1014-1015. Iowa State University Press, Ames, IA.
Bierer BW, Vickers CL and Thomas JB (1959) A parasitism in turkeys due to a Hemoproteus-like blood parasite. J Am Vet Med Assoc 135(3):181-182.
Campbell TW (1995) Common avian blood parasites. In: Avian hematology and cytology, Iowa State Press, Ames, IA, 2nd ed., pp: 30-31.
Cannell BL, Krasnec KV, Campbell K, Jones HI, Miller RD & Stephens N (2013) The pathology and pathogenicity of a novel Haemoproteus spp. infection in wild Little Penguins (Eudyptula minor). Vet Parasitol 197(1): 74-84.
Cardona CJ, Ihejirika A & McClellan L (2002) Haemoproteus lophortyx infection in bobwhite quail. Avian Dis 46: 249-255.
Clark P, Boardman WSJ & Raidal SR (2009) Atlas of Clinical Avian Hematology. Wiley-Blackwell, Oxford. PP: 198.
Dey ARN, Begum SC, Paul M, Noor KM & Islam KM (2010) Prevalence and pathology of blood protozoa in pigeons reared at mymensingh district, Bangladesh. Int J Biol Res 2: 25-29.
Donovan TA, Schrenzel M, Tucker TA, Pessier AP & Stalis IH (2008) Hepatic hemorrhage, hemocoelom, and sudden death due to Haemoproteus infection in passerine birds: eleven cases. J Vet Diagn Invest 20: 304-313.
Dranzoa C, Ocaido M & Katete P (1999) The ecto, gastro-intestinal and haemo-parasites of live pigeons (Columba livia) in Kampala, Uganda. Avian Pathol 28(2): 119-124.
Durrant L, Beadell JS, Ishtiaq F, Graves GR, Olson SL, Gering E, Peirce MA, Milensky CM, Schmidt BK, Gebhard C & Fleischer RC (2006) Avian hematozoa in South America: a comparison of temperate and tropical zones. Ornithol Monographs 60: 98-111.
Earle RA, Bastianello SS, Bennett GF & Krecek RC (1993) Histopathology and physiology of the tissue stages of Haemoproteus columbae causing mortality in Columbiformes. Avian Pathol 22: 67-80.
Garamszegi LZ (2010) The sensitivity of microscopy and PCR-based detection methods affecting estimates of prevalence of blood parasites in birds. J Parasitol 96(6): 1197-1203.
Garnham PCC (1966) Malaria parasites and other Haemosporidia. 1th ed. Vol 1, Oxford, Blackwell, London, PP: 48-92.
Gicik Y & Arslan MÖ (2001) Blood parasites of wild pigeons in Ankara District. Turk J Vet Anim Sci 25(2): 169-172.
Hamilton WD & Zuk M (1982) Heritable true fitness and bright birds: a role for parasites?. Science 218: 384-387.
Jarvi SI, Schultz JJ & Atkinson CT (2002) PCR diagnostics underestimate the prevalence of avian malaria (Plasmodium relictum) in experimentally-infected passerines. J Parasitol 88(1): 153-158.
Kruse W (1890) Ueber Blutparasiten. Archive of Pathology Anatomy and Physiology, 121: 359-72. Quoted by: Valkiūnas G 2005. Avian malaria parasites and other haemosporidia. Vol 1, 2nd ed, CRC Press, Boca Raton, FL, PP: 294, 564.
Lederer R, Adlard RD & O’Donoghue PJ (2002) Severe pathology associated with protozoal schizonts in two Pied Currawongs (Strepera graculina) from Queensland. Vet Rec 150: 520-522.
Lefèvre T, Roche B, Poulin R, Hurd H, Renaud F. & Thomas F (2008) Exploiting host compensatory responses: the ‘must’of manipulation?. Trends Parasitol 24(10): 435-439.
Macchi BM, Miranda FJB, de Souza FS, de Carvalho ECQ, Albernaz AP, do Nascimento JLM & DaMatta RA (2013) Chickens treated with a nitric oxide inhibitor became more resistant to Plasmodium gallinaceum infection due to reduced anemia, thrombocytopenia and inflammation. Vet Res 44(1): p.8.
Macwhirter P (1994) Section 7, comparative medicine and management, chapter 43, passeriformes. In: Avian medicine: principles and application, ed. Ritchie BW, Harrison GJ, Harrison LR, Wingers Publishing, Lake Worth, FL. pp. 1192-1193.
Marchiafava E & Celli A (1885) Weitere untersuchungen uber die malariainfektion. Fortschritte der Medizin, Berlin, 3: 787-792. Quoted by: Valkiūnas, G. (2005). Avian malaria parasites and other haemosporidia. Vol 1, 2nd ed, CRC Press, Boca Raton, FL, PP: 10.
Martinsen ES, Paperna I & Schall JJ (2006) Morphological versus molecular identification of avian Haemosporidia: an exploration of three species concepts. Parasitol 133(3), 279-288.
Martínez J, La Puente JM, Herrero J, Del Cerro S, Lobato E, Aguilar JR, Vásquez RA & Merino S (2009) A restriction site to differentiate Plasmodium and Haemoproteus infections in birds: on the inefficiency of general primers for detection of mixed infections. Parasitol 136:713-722.
Massey JG, Graczyk TK & Cranfield MR (1996) Characteristics of naturally acquired Plasmodium relictum capistranoae infections in naive Hawaiian crows (Corvus hawaiiensis) in Hawaii. J Parasitol 82(1):182-185.
McLaughlin ET (1968) Blood parasites of the cowbird, grackle, redwing and starling in New Jersey. Bird-Band 39(3):193-199.
Merino S, Moreno J, Sanz JJ & Arriero E (2000) Are avian blood parasites pathogenic in the wild? A medication experiment in blue tits (Parus caeruleus). Proc R Soc Lond B Biol Sci 267: 2507-2510.
Msoffe PLM, Muhairwa AP, Chiwanga GH & Kassuku AA (2010) A study of ecto-and endo-parasites of domestic pigeons in Morogoro Municipality, Tanzania. Afr J Agric Res 5(3): 264-267.
Mushi EZ, Binta MG, Chaba Ndebele RG & Panzirah RR (2000) Parasites of domestic pigeon (Columbia livia domestica) in Sebele, Gaborone. J S Afr Vet Assoc 7: 249-250.
Nermean MH & Abdelrahim EA (2016) Haemoproteus columbae infection and its histopathological effects on pigeons in Qena Governorate, Egypt. IOSR J Pharm Biol Sci 11(1): 79-90.
Nourani L, Aliabadian M, Mirshamsi O, Dinparast Djadid N (2018) Molecular detection and genetic diversity of avian haemosporidian parasites in Iran. PLoS ONE 13(11): e0206638.
Orjih AU (2001) On the mechanism of hemozoin production in malaria parasites: activated erythrocyte membranes promote beta-hematin synthesis. Exp Biol Med 226: 746-752.
Pagola S, Stephens PW, Bohle DS, Kosar AD & Madsen SK (2000) The structure of malaria pigment β-haematin. Nature 404(6775): 307-310.
Peirce MA & Bevan BJ (1977) Blood parasites of imported psittacine birds. The Vet Rec 100(14): 282-283.
Peirce MA & Bennett GF (1993) Validation and synonymy of some haemoproteids of the avian family Muscicapidae. J Nat His 27(2): 505-506.
Peirce MA, Lederer R, Adlard RD & O’Donoghue PJ (2004) Pathology associated with endogenous development of haematozoa in birds from southeast Queensland. Avian Pathol 33(4): 445-450.
Perkins SL & Schall J (2002) A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J Parasitol 88(5): 972-978.
Richner H, Christe P & Oppliger A (1995) Paternal investment affects prevalence of malaria. Proc Natl Acad Sci USA 92: 1192-1194.
Ricklefs RE & Fallon SM (2002) Diversification and host switching in avian malaria parasites. Proc R Soc Lond B Biol Sci 269(1494): 885-892.
Tavassoli M, Esmaeilnejad B, Malekifard F, Mardani K (2017) PCRRFLP detection of Haemoproteus spp. (Haemosporida: Haemoproteidae) in pigeon blood samples from Iran. Bulg J Vet Med. (Online first).
Tolgay N (1972) Cesitli kanatlilarin Plasmodium, Haemoproteus ve Leucocytozoon enfeksiyonlari uzerinde arastirmalar. Ankara Üniv Vet Fak Derg 19: 271-286.
Tostes R, Martinele I, Vashist U, Castanon MCMN, de Faria Pinto P, Daemon E, D’Agosto M (2015) Molecular characterization and biochemical and histopathological aspects of the parasitism of Haemoproteuss spp. In Southern Caracaras (Caracara plancus). Pesqui Vet Bras 35(1): 67-74.
Valkiūnas G (2005) Avian malaria parasites and other haemosporidia. Vol 1, 2nd ed, CRC Press, Boca Raton, FL, PP: 113-114, 191-192.
Valkiūnas G (1993) Pathogenic influence of haemosporidians and trypanosomes on wild birds in the field conditions: facts and hypotheses. Ekologija 1: 47-60.
Valkiūnas G, Iezhova TA, Križanauskienė A, Palinauskas V, Sehgal RN & Bensch S (2008) A comparative analysis of microscopy and PCRbased detection methods for blood parasites. J Parasitol 94(6): 1395-1401.
Valkiūnas G, Iezhova TA, Palinauskas V, Ilgūnas M & Bernotienė R (2015) The evidence for rapid gametocyte viability changes in the course of parasitemia in Haemoproteus parasites. Parasitol Res 114(8): 2903-2909.
Valkiūnas G, Žiegytė R, Palinauskas V, Bernotienė R, Bukauskaitė D, Ilgūnas M, Dimitrov D and Iezhova TA (2015) Complete sporogony of Plasmodium relictum (lineage pGRW4) in mosquitoes Culex pipiens pipiens, with implications on avian malaria epidemiology. Parasitol Res 114(8): 3075-3085.
van Riper C, van Riper SG, Goff ML & Laird M (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr 56(4): 327-344.
Waldenström J, Bensch S, Hasselquist D & Östman Ö (2004) A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. J Parasitol 90(1): 191-194.
Walker D & Garnham PCC (1972) Aberrant Leucocytozoon infection in parakeets. Vet Rec 91: 70-72.
Youssefi MR, Sadeghian AG & Esfandiari B (2010) Prevalence of Haemoproteus columbae infection in Columba livia in North of Iran. WJZ 5(4): 275-277.
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