Abstract
Cryptosporidium is one of the most important parasitic protozoa that can be transmitted through food and water contamination. With the increasing report of Cryptosporidium infections in wild birds, especially in herbivorous waterfowl, concerns have been raised for oocyst contamination of water and food supplies, which in turn can cause human and domestic animal infections in areas neighboring wild birds’ habitats. This review discusses the epidemiology, species, and genotypes distribution of Cryptosporidium in wild birds around the world. The overall prevalence of Cryptosporidium in wild birds was calculated as 3.96% (1945/49129), with 6 Cryptosporidium species (C. andersoni, C. parvum, C. meleagridis, C. avium, C. baileyi, and C. galli) and 5 genotypes (Goose genotype I, Goose genotype II, Avian genotype I, Avian genotype III, and Avian genotype VI) reported. As wild birds mainly live in the wild, control method for the Cryptosporidium infection in wild birds is still lacking, which increases the probability of disease transmission from wild birds to humans. The main purpose of this review is to highlight the Cryptosporidium infection in wild birds and its transmission, associated risk factors, and their prevention, illustrating the necessity of multidisciplinary approaches toward screening and control of Cryptosporidium infections.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ajjampur SS, Sankaran P, Kang G (2008) Cryptosporidium species in HIV-infected individuals in India: an overview. Natl Med J India 21(4):178–184
Amer S, Wang C, He H (2010) First detection of Cryptosporidium baileyi in Ruddy Shelduck (Tadorna ferruginea) in China. J Vet Med Sci 72(7):935–938. https://doi.org/10.1292/jvms.09-0515
Areeshi MY, Beeching NJ, Hart CA (2007) Cryptosporidiosis in Saudi Arabia and neighboring countries. Ann Saudi Med 27(5):325–332. https://doi.org/10.5144/0256-4947.2007.325
Azmanis P, di Somma A, Pappalardo L, Silvanose CD, Bangoura B (2018) First detection of Cryptosporidium parvum in falcons (Falconiformes): diagnosis, molecular sequencing, therapeutic trial and epidemiological assessment of a possible emerging disease in captive falcons. Vet Parasitol 252:167–172. https://doi.org/10.1016/j.vetpar.2018.02.012
Baines D, Newborn D, Richardson M (2020) Correlates of pathological lesions associated with respiratory cryptosporidiosis prevalence in shot red grouse Lagopus lagopus scotica from moors in northern England. Avian Pathol 49(1):74–79. https://doi.org/10.1080/03079457.2019.1667478
Benskin CM, Wilson K, Jones K, Hartley IR (2009) Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biol Rev Camb Philos Soc 84(3):349–373. https://doi.org/10.1111/j.1469-185X.2008.00076.x
Blagburn BL, Lindsay DS, Giambrone JJ, Sundermann CA, Hoerr FJ (1987) Experimental cryptosporidiosis in broiler chickens. Poult Sci 66(3):442–449. https://doi.org/10.3382/ps.0660442
Bouzid M, Hunter PR, Chalmers RM, Tyler KM (2013) Cryptosporidium pathogenicity and virulence. Clin Microbiol Rev 26(1):115–134. https://doi.org/10.1128/cmr.00076-12
Camargo VDS, Santana BN, Ferrari E, Nakamura AA, Nagata WB, Nardi ARM, Meireles MV (2018) Detection and molecular characterization of Cryptosporidium spp. in captive canaries Serinus canaria using different diagnostic methods. Rev Bras Parasitol Vet 27(1):61–66. https://doi.org/10.1590/s1984-296120180010
Chelladurai JJ, Clark ME, Kváč M, Holubová N, Khan E, Stenger BL, Giddings CW, McEvoy J (2016) Cryptosporidium galli and novel Cryptosporidium avian genotype VI in North American red-winged blackbirds (Agelaius phoeniceus). Parasitol Res 115(5):1901–1906. https://doi.org/10.1007/s00436-016-4930-8
Coldwell L, Caldow G, Holliman A, Mearns R, Errington H, Giles M, Willoughby K, Wood A (2012) Cryptosporidium baileyi in wild red grouse with ‘bulgy eye.’ Vet Rec 170(23):603–604. https://doi.org/10.1136/vr.e3940
Čondlová Š, Horčičková M, Sak B, Květoňová D, Hlásková L, Konečný R, Stanko M, McEvoy J, Kváč M (2018) Cryptosporidium apodemi sp. n. and Cryptosporidium ditrichi sp. n. (Apicomplexa: Cryptosporidiidae) in Apodemus spp. Eur J Protistol 63:1–12. https://doi.org/10.1016/j.ejop.2017.12.006
Current WL, Upton SJ, Haynes TB (1986) The life cycle of Cryptosporidium baileyi n. sp. (Apicomplexa, Cryptosporidiidae) infecting chickens. J Protozool 33(2):289–296. https://doi.org/10.1111/j.1550-7408.1986.tb05608.x
Curtiss JB, Leone AM, Wellehan JF Jr, Emerson JA, Howerth EW, Farina LL (2015) Rental and cloacal cryptosporidiosis (Cryptosporidium avian genotype V) in a major Mitchell’s cockatoo (Lophochroa leadbeateri). J Zoo Wildl Med 46(4):934–937. https://doi.org/10.1638/2015-0025.1
Elkarim Laatamna, A., Holubova, N., Sak, B. and Kvac, M. (2017). Cryptosporidium meleagridis and C. baileyi (Apicomplexa) in domestic and wild birds in Algeria. Folia Parasitol (Praha) 64. https://doi.org/10.14411/fp.2017.018
Elmberg J, Berg C, Lerner H, Waldenström J, Hessel R (2017) Potential disease transmission from wild geese and swans to livestock, poultry and humans: a review of the scientific literature from a One Health perspective. Infect Ecol Epidemiol 7(1):1300450. https://doi.org/10.1080/20008686.2017.1300450
Fayer R (2010) Taxonomy and species delimitation in Cryptosporidium. Exp Parasitol 124(1):90–97. https://doi.org/10.1016/j.exppara.2009.03.005
Feng SY, Chang H, Luo J, Huang JJ, He HX (2019) First report of Enterocytozoon bieneusi and Cryptosporidium spp. in peafowl (Pavo cristatus) in China. Int J Parasitol Parasites Wildl 9:1–6. https://doi.org/10.1016/j.ijppaw.2019.03.014
Gardiner CH, Imes GD Jr (1984) Cryptosporidium sp in the kidneys of a black-throated finch. J Am Vet Med Assoc 185(11):1401–1402
Gharagozlou MJ, Dezfoulian O, Rahbari S, Bokaie S, Jahanzad I, Razavi AN (2006) Intestinal cryptosporidiosis in turkeys in Iran. J Vet Med A Physiol Pathol Clin Med 53(6):282–285. https://doi.org/10.1111/j.1439-0442.2006.00843.x
Glisson JR, Brown TP, Brugh M, Page RK, Kleven SH, Davis RB (1984) Sinusitis in turkeys associated with respiratory cryptosporidiosis. Avian Dis 28(3):783–790
Gomes RS, Huber F, da Silva S, do Bomfim TC (2012) Cryptosporidium spp. parasitize exotic birds that are commercialized in markets, commercial aviaries, and pet shops. Parasitol Res 110(4):1363–1370. https://doi.org/10.1007/s00436-011-2636-5
Goodwin MA (1988) Small-intestinal cryptosporidiosis in a chicken. Avian Dis 32(4):844–848
Goodwin MA, Krabill VA (1989) Diarrhea associated with small-intestinal cryptosporidiosis in a budgerigar and in a cockatiel. Avian Dis 33(4):829–833
Graczyk TK, Fayer R, Trout JM, Lewis EJ, Farley CA, Sulaiman I, Lal AA (1998) Giardia sp. cysts and infectious Cryptosporidium parvum oocysts in the feces of migratory Canada geese Branta canadensis. Appl Environ Microbiol 64(7):2736–2738
Holsback L, Cardoso MJ, Fagnani R, Patelli TH (2013) Natural infection by endoparasites among free-living wild animals. Rev Bras Parasitol Vet 22(2):302–306. https://doi.org/10.1590/s1984-29612013005000018
Holubová N, Tůmová L, Sak B, Hejzlarová A, Konečný R, McEvoy J, Kváč M (2020) Description of Cryptosporidium ornithophilus n. sp. (Apicomplexa: Cryptosporidiidae) in farmed ostriches. Parasit Vectors 13(1):340. https://doi.org/10.1186/s13071-020-04191-2
Holubová N, Zikmundová V, Limpouchová Z, Sak B, Konečný R, Hlásková L, Rajský D, Kopacz Z, McEvoy J, Kváč M (2019) Cryptosporidium proventriculi sp. n. (Apicomplexa: Cryptosporidiidae) in Psittaciformes birds. Eur J Protistol 69:70–87. https://doi.org/10.1016/j.ejop.2019.03.001
Hurtado R, Parsons NJ, Gous TA, der Spuy SV, Klusener R, Stander N, van Wilpe E, Vanstreels RET. Outbreak of cryptosporidiosis in African penguins Spheniscus demersus. Dis Aquat Organ. 140:143-149. https://doi.org/10.3354/dao03504
Jian Y, Jian Y, Zhang X, Li X, Schou C, Charalambidou I, Ma L, Karanis P (2021) Occurrence of Cryptosporidium and Giardia in wild birds from Qinghai Lake on the Qinghai-Tibetan Plateau. China Parasitol Res 120(2):615–628. https://doi.org/10.1007/s00436-020-06993-w
Jokipii L, Jokipii AM (1986) Timing of symptoms and oocyst excretion in human cryptosporidiosis. N Engl J Med 315(26):1643–1647. https://doi.org/10.1056/nejm198612253152604
Karanis P, Kourenti C, Smith H (2007) Waterborne transmission of protozoan parasites: a worldwide review of outbreaks and lessons learnt. J Water Health 5(1):1–38. https://doi.org/10.2166/wh.2006.002
Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque AS, Zaidi AK, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acácio S, Biswas K, O’Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM (2013) Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382(9888):209–222. https://doi.org/10.1016/s0140-6736(13)60844-2
Kuhn RC, Rock CM, Oshima KH (2002) Occurrence of Cryptosporidium and Giardia in wild ducks along the Rio Grande River valley in southern New Mexico. Appl Environ Microbiol 68(1):161–165. https://doi.org/10.1128/aem.68.1.161-165.2002
Ley DH, Moresco A, Frasca S Jr (2012) Conjunctivitis, rhinitis, and sinusitis in cliff swallows (Petrochelidon pyrrhonota) found in association with Mycoplasma sturni infection and cryptosporidiosis. Avian Pathol 41(4):395–401. https://doi.org/10.1080/03079457.2012.697624
Lendner M, Daugschies A (2014) Cryptosporidium infections: molecular advances. Parasitology 141(11):1511–1532. https://doi.org/10.1017/s0031182014000237
Li J, Qi M, Chang Y, Wang R, Li T, Dong H, Zhang L (2015) Molecular characterization of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi in captive wildlife at Zhengzhou Zoo, China. J Eukaryot Microbiol 62(6):833–839. https://doi.org/10.1111/jeu.12269
Meisel JL, Perera DR, Meligro C, Rubin CE (1976) Overwhelming watery diarrhea associated with a Cryptosporidium in an immunosuppressed patient. Gastroenterology 70(6):1156–1160
Molina-Lopez RA, Ramis A, Martin-Vazquez S, Gomez-Couso H, Ares-Mazas E, Caccio SM, Leiva M, Darwich L (2010) Cryptosporidium baileyi infection associated with an outbreak of ocular and respiratory disease in Otus owls (Otus scops) in a rehabilitation centre. Avian Pathol 39(3):171–176. https://doi.org/10.1080/03079451003717589
Nime FA, Burek JD, Page DL, Holscher MA, Yardley JH (1976) Acute enterocolitis in a human being infected with the protozoan Cryptosporidium. Gastroenterology 70(4):592–598
O’Donoghue PJ (1995) Cryptosporidium and cryptosporidiosis in man and animals. Int J Parasitol 25(2):139–195. https://doi.org/10.1016/0020-7519(94)e0059-v
Oliveira BCM, Nagata WB, Arana DG, Ferreira GC, Sitton HA, de Oliveira MRF, Meireles MV (2017) Cryptosporidium baileyi in wild captive psittacines in Brazil. Vet Parasitol Reg Stud Reports 10:154–156. https://doi.org/10.1016/j.vprsr.2017.10.007
Osman M, El Safadi D, Benamrouz-Vanneste S, Cian A, Moriniere R, Gantois N, Delgado-Viscogliosi P, Guyot K, Bosc S, Chabé M, Petit T, Viscogliosi E, Certad G (2017) Prevalence, transmission, and host specificity of Cryptosporidium spp. in various animal groups from two French zoos. Parasitol Res 116(12):3419–3422. https://doi.org/10.1007/s00436-017-5645-1
Pagès-Manté A, Pagès-Bosch M, Majó-Masferrer N, Gómez-Couso H, Ares-Mazás E (2007) An outbreak of disease associated with cryptosporidia on a red-legged partridge (Alectoris rufa) game farm. Avian Pathol 36(4):275–278. https://doi.org/10.1080/03079450701439389
Pavlasek, I. (2001). Findings of cryptosporidia in the stomach of hens and of exotic and wild birds. Veterinarstvi.
Petersen HH, Dalsgaard A, Vinneras B, Jensen LS (2020) Inactivation of Cryptosporidium parvum oocysts and faecal indicator bacteria in cattle slurry by addition of ammonia. J Appl Microbiol 130(5):1745–1757. https://doi.org/10.1111/jam.14881
Randall CJ (1986) Renal and nasal cryptosporidiosis in a junglefowl (Gallus sonneratii). Vet Rec 119(6):130–131. https://doi.org/10.1136/vr.119.6.130
Reboredo-Fernández A, Ares-Mazás E, Cacciò SM, Gómez-Couso H (2015) Occurrence of Giardia and Cryptosporidium in wild birds in Galicia (Northwest Spain). Parasitology 142(7):917–925. https://doi.org/10.1017/s0031182015000049
Ryan U (2010) Cryptosporidium in birds, fish and amphibians. Exp Parasitol 124(1):113–120. https://doi.org/10.1016/j.exppara.2009.02.002
Ryan U, Hijjawi N (2015) New developments in Cryptosporidium research. Int J Parasitol 45(6):367–373. https://doi.org/10.1016/j.ijpara.2015.01.009
Ryan UM, Xiao L, Read C, Sulaiman IM, Monis P, Lal AA, Fayer R, Pavlasek I (2003) A redescription of Cryptosporidium galli Pavlasek, 1999 (Apicomplexa: Cryptosporidiidae) from birds. J Parasitol 89(4):809–813. https://doi.org/10.1645/ge-74ri
Salama RY, Abdelbaset AE, Takeda Y, Imai K, Ogawa H, Igarashi M (2020) Molecular characterization of Cryptosporidium spp. from migratory ducks around Tokachi subprefecture, Hokkaido, Japan. J Vet Med Sci 82(5):571–575. https://doi.org/10.1292/jvms.19-0586
Sandoval-Rodríguez A, Marcone D, Alegría-Morán R (2021) Cryptosporidium spp. and Giardia spp. in free-ranging introduced Monk Parakeets from Santiago, Chile. Animals (Basel) 11(3). https://doi.org/10.3390/ani11030801
Seixas M, Taroda A, Cardim ST, Sasse JP, Martins TA, Martins FDC, Minutti AF, Vidotto O, Barros LD, Garcia JL (2019) First study of Cryptosporidium spp. occurrence in eared doves (Zenaida auriculata). Rev Bras Parasitol Vet 28(3):489–492. https://doi.org/10.1590/s1984-29612019016
Sevá Ada P, Funada MR, Richtzenhain L, Guimarães MB, Souza Sde O, Allegretti L, Sinhorini JA, Duarte VV, Soares RM (2011) Genotyping of Cryptosporidium spp. from free-living wild birds from Brazil. Vet Parasitol 175(1–2):27–32. https://doi.org/10.1016/j.vetpar.2010.09.031
Silva Novaes R, Pires MS, Sudré AP, Bergamo do Bomfim TC (2018) Captive-bred neotropical birds diagnosed with Cryptosporidium Avian genotype III. Acta Trop 178:297–302. https://doi.org/10.1016/j.actatropica.2017.12.013
Slavin D (1955) Cryptosporidium meleagridis (sp. nov.). J Comp Pathol 65(3):262–266. https://doi.org/10.1016/s0368-1742(55)80025-2
Smith HV, Rose JB (1998) Waterborne cryptosporidiosis: current status. Parasitol Today 14(1):14–22. https://doi.org/10.1016/s0169-4758(97)01150-2
Sponseller JK, Griffiths JK, Tzipori S (2014) The evolution of respiratory cryptosporidiosis: evidence for transmission by inhalation. Clin Microbiol Rev 27(3):575–586. https://doi.org/10.1128/cmr.00115-13
Sréter T, Varga I (2000) Cryptosporidiosis in birds–a review. Vet Parasitol 87(4):261–279. https://doi.org/10.1016/s0304-4017(99)00178-8
Tarwid JN, Cawthorn RJ, Riddell C (1985) Cryptosporidiosis in the respiratory tract of turkeys in Saskatchewan. Avian Dis 29(2):528–532
Thompson RC, Lymbery AJ, Smith A (2010) Parasites, emerging disease and wildlife conservation. Int J Parasitol 40(10):1163–1170. https://doi.org/10.1016/j.ijpara.2010.04.009
Trampel DW, Pepper TM, Blagburn BL (2000) Urinary tract cryptosporidiosis in commercial laying hens. Avian Dis 44(2):479–484
Tyzzer EE (1910) An extracellular Coccidium, Cryptosporidium Muris (Gen. Et Sp. Nov.), of the gastric Glands of the Common Mouse. J Med Res 23(3):487-510.3
van Zeeland YR, Schoemaker NJ, Kik MJ, van der Giessend JW (2008) Upper respiratory tract infection caused by Cryptosporidium baileyi in three mixed-bred falcons (Falco rusticolus x Falco cherrug). Avian Dis 52(2):357–363. https://doi.org/10.1637/8121-100207-Case.1
Vanathy K, Parija SC, Mandal J, Hamide A, Krishnamurthy S (2017) Cryptosporidiosis: a mini review. Trop Parasitol 7(2):72–80. https://doi.org/10.4103/tp.TP_25_17
Wang, K., Gazizova, A., Wang, Y., Zhang, K., Zhang, Y., Chang, Y., Cui, Y., Zhang, Y., Zhang, S. and Zhang, L. (2019). First detection of Cryptosporidium spp. in migratory Whooper Swans (Cygnus cygnus) in China. Microorganisms 8(1). https://doi.org/10.3390/microorganisms8010006.
Wang R, Zhao G, Gong Y, Zhang L (2017) Advances and perspectives on the epidemiology of bovine Cryptosporidium in China in the past 30 years. Front Microbiol 8:1823. https://doi.org/10.3389/fmicb.2017.01823
Xiang L, Guo F, Yu Y, Parson LS, LaCoste L, Gibson A, Presley SM, Peterson M, Craig TM, Rollins D, Fedynich AM, Zhu G (2017) Multiyear survey of coccidia, cryptosporidia, microsporidia, histomona, and hematozoa in wild quail in the rolling plains ecoregion of Texas and Oklahoma, USA. J Eukaryot Microbiol 64(1):4–17. https://doi.org/10.1111/jeu.12330
Xiao L, Fayer R (2008) Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. Int J Parasitol 38(11):1239–1255. https://doi.org/10.1016/j.ijpara.2008.03.006
Xiao L, Fayer R, Ryan U, Upton SJ (2004) Cryptosporidium taxonomy: recent advances and implications for public health. Clin Microbiol Rev 17(1):72–97. https://doi.org/10.1128/cmr.17.1.72-97.2004
Xiao L, Feng Y (2017) Molecular epidemiologic tools for waterborne pathogens Cryptosporidium spp. and Giardia duodenalis. Food Waterborne Parasitol 8–9:14–32. https://doi.org/10.1016/j.fawpar.2017.09.002
Ziegler PE, Wade SE, Schaaf SL, Stern DA, Nadareski CA, Mohammed HO (2007) Prevalence of Cryptosporidium species in wildlife populations within a watershed landscape in southeastern New York State. Vet Parasitol 147(1–2):176–184. https://doi.org/10.1016/j.vetpar.2007.03.024
Funding
This study was supported in part by the National Natural Science Foundation of China (U1904203), Higher Education Teaching Reform Research and Practice Project of Henan Province in 2019 (2019SJGLX006Y), National Key Research and Development Program of China (2017YFD0501305, 2019YFC1605700), and the Leading Talents of the Thousand Talents Program of Central China (19CZ0122). The sponsors played no role in the study design, in the collection, analysis, or interpretation of the data, in writing the report, or in the decision to submit the article for publication. We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.
Author information
Authors and Affiliations
Contributions
LZ conceived and designed the review. YW developed the draft manuscript and analyzed the data. KZ and YC analyzed the data. XL revised the draft manuscript.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Section Editor: Lihua Xiao
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Wang, Y., Zhang, K., Chen, Y. et al. Cryptosporidium and cryptosporidiosis in wild birds: A One Health perspective. Parasitol Res 120, 3035–3044 (2021). https://doi.org/10.1007/s00436-021-07289-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-021-07289-3