Journal of Parasite Research
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Research Article | Open Access
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    Domestic Pigeons As A Potential Hazzard For Transmission Of Some Human Protozoan Parasites

    Refaat M.A. Khalifa 1       Abdallah A.E. Hassan 1     Mohsen I. Arafa 2     Hanan E. M. Eldeek 1     Wafaa G. Mahmoud 3    

    1Parasitology Departement, Faculty of Medicine, Assiut University, Egypt

    2Animal Health Institute-Assiut Branch, Assiut, Egypt,

    3Faculty of Veterinary Medicine, New Valley University

    Abstract

    Domestic pigeons (Columba liviadomestica) of the order Columbiformes are ubiquitous birds and can be found in virtually every town and city around the globe. Their interaction with humans and domestic animals and wild birds makes them a potential carrier of zoonotic parasites. The present study aimed to detect the prevalence of different zoonotic protozoans that affect different-aged domestic pigeons in different localities in Assiut Governorate, Egypt. A total of 50 fecal samples from 20 young and 30 adult pigeons were collected and examined for identification and estimation of prevalence of Cryptosporidium sp. and Microsporidium sp. using modified Kinyoun acid-fast stain. For detection of the prevalence of Toxoplasma gondii, serum samples from 50 pigeons were examined serologically for the presence of Toxoplasma antibodies by using Latex Agglutination test. The prevalence of Cryptosporidium sp. infection was 20%; 6.7% in adult pigeons and 40 % in young pigeons while that of Microsporidium sp. was 40% both in adult and young pigeons. Mixed infection was detected in only two young pigeons (10%). Regarding Toxoplasma gondii detection, the number of seropositive cases detected by LAT was 29 out of 50 (58%). The positive agglutination titers, among 14 (48.27%) seropositive pigeons ranged between 1:2 -1:128. It was concluded that domestic pigeons may be considered as a reservoir host for Cryptosporidium, Microsporidium, and Toxoplasmagondii human infection which represents a serious human public health problem especially for high risk groups of population living in the same dwellings with pigeons. Moreover, the present pilot results provide a baseline data for planning future researches and control strategies against domestic pigeon's parasites.

    Received 20 Jan 2020; Accepted 14 Feb 2020; Published 14 Feb 2020;

    Copyright©  2020 Refaat M.A. Khalifa, et al.

    License
    Creative Commons License    This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

    Competing interests

    The authors have declared that no competing interests exist.

    Citation:

    Refaat M.A. Khalifa, Abdallah A.E. Hassan, Mohsen I. Arafa, Hanan E. M. Eldeek, Wafaa G. Mahmoud (2020) Domestic Pigeons As A Potential Hazzard For Transmission Of Some Human Protozoan Parasites. Journal of parasite research - 1(2):1-7.
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    DOI10.14302/issn.2690-6759.jpar-20-3184

    Introduction

    Pigeons occur worldwide and are reared as a symbol of peace, love, gentleness and spirit messengers and nowadays also for meat, ornamental pet bird. Unfortunately, they may suffer from many zoonotic protozoan infections10.

    Domestic pigeons (Columba liviadomestica) of the order columbiformes are ubiquitous birds and can be found in virtually every town and city around the globe. Columba livia is a species that descended from wild rock pigeon25.

    Poultry industry is the most effective and economical source of animal protein in shortest possible time. Poultry producers are looking for some substitute of chicken meat, which in the future will come in the form of pigeon meat to contribute towards its increase in gross domestic production through livestock sector4.

    Among the birds, importance of domestic pigeons cannot be ignored, as they act as reservoir hosts or carriers and important source of parasitic infections for other avian hosts which share the common parasitic fauna and sometimes harbor zoonotic parasites26. Moreover domestic pigeons are part of subsistence farming done by most poor families 9.

    Aim of the Present Study

    The aim of the present work is to do a pilot study of the prevalence of different zoonotic protozoans affecting different-aged domestic pigeons in different localities in Assiut Governorate, Egypt including Cryptosporidium sp. and Microsporidium sp. through examination of fecal samples by modified kenyoun acid fast stain and Toxoplasma gondii through serological estimation of Toxoplasma gondii antibodies by Latex Agglutination test.

    Material and Methods

    The present study was conducted from October through December 2018 in the Department of Medical Parasitology, Faculty of Medicine, Assiut University and Animal Health Research Institute (Assiut branch), Assiut, Egypt.

    In this study, a total of 50 fecal samples, were collected from domestic pigeons (Columba liviadomestica) of different ages (20 young and 30 adult) from different localities of Assiut Governorate and examined for identification and estimation of prevalence of Cryptosporidium sp. and Microsporidium sp. The specimens, consisted of concentrated sediment of fresh stool, prepared and stained using Modified Kinyoun acid-fast stain according to 16.

    For serological examination, a total of 50 serum samples were examined for the presence of Toxoplasma antibodies by Latex Agglutination test according to41. All samples were examined qualitatively, 14 of the positive samples were examined quantitatively. The presence of agglutination indicated an antibody concentration equal or more than 4 IU/ml and the titer, in the quantitative method were defined as the highest dilution showing a positive result.

    Statistical analysis was carried out using35 program, version 8.2 for differences between young and adult domestic pigeons in numbers of infected samples. The significance differences between young and adult pigeon means were tested by Duncan Multiple Range Test37. The data was presented in mean ± Standard error of means (S.E.M). Level of significance was set at P<0.05.

    Results

    The examination of 50 (20 young and 30 adult) pigeon's fecal samples by Kinyoun's acid fast stain showed that the total prevalence of Cryptosporidium sp. infection was 20 %. It was found in 6.7% in adult pigeons and 40 % in young pigeons (Table 1). On the other hand the total prevalence of Microsporidium sp. infection was 40 % in both adult and young pigeons (Table 1). Mixed infection of Microsporidium sp. with Cryptosporidium sp. was detected in only two young pigeons (10%). The difference was not statistically significant; p value =0.347.

    Table 1. Examination of fecal samples of pigeons by modified Kinyoun acid-fast stain.
    Parasites Samples
    Fecal N=50
    young n=20 adult n=30 total
    Inf. % Inf. % Inf.  
    C,Wtosporidium sp. 8 40 2 6.7 10 20
    Microsporidium sp. 8 40 12 40 20 40
    Mixed infection 2 10 0 0 2 4

    Using Latex Agglutination serological test for toxoplasmosis, the number of seropositive cases in domestic pigeons was 29 out of 50 (58%). Quantitatively, among seropositive pigeons; 14 (48.27%) were positive at titers ranging from 1/2 to1/128. Four samples (28.57%) were detected positive at a titer of 1/16 as well as at a titer of 1/32. Three samples (21.42%) were detected positive at a titer of 1/64.One sample (7.14%) was detected positive at a titer of 1/2, 1/4, and 1/128. On the other hand, no samples were detected positive at a titer of 1/8 (Table 2)

    Table 2. Distribution of Latix titers for 14 positive serum samples of pigeons.
     Titer 1/2 1/4 1/8 1/16 1/32 1/64 1/128
    Positive samples   1 1 0 4 4 3 1
      7.14 7.14 0 28.57 28.57 21.42 7.14

    Discussion

    Endoparasitic infections are of great importance in poultry industry especially in backyard pigeon worldwide8.

    In the present study the prevalence of Cryptosporidium sp. in young domestic pigeons was 40%, which was higher than adult pigeons (6.7%); this agreed with 12 who stated that the development of the disease in young pigeons might indicate that the immunologic status could have played an important role in the spread of the infection. The parasite was reported from pigeons in Turkey, Spain, Iran, Thailand, Malaysia and Brazil 5, 21, 22, 28, 29, 32, 33, 34.

    From Egypt, 2 recorded for the first time the occurrence of Cryptosporidium sp. in 46.2% out of 322 examined domestic pigeons from Gharbia Governorate.

    In all previously mentioned works, Cryptosporidium oocysts were identified only to the generic level. For the first time, 1 reported the occurrence of the human species C. hominis in 5.9% of 34 domestic pigeons from Canary Islands based on DNA findings. Later on, zoonotic crypto-sporidiosis; particularly C. meleagridiswas detected in pigeons in Thailand through molecular identification21. Moreover, 15 detected cryptosporidial oocysts in droppings in 40% out of 120 pigeons collected from house roofs in Baghdad, Iraq and identified them according to their size to be small-sized (4x5.2µ) C. meleagridis, medium-sized (6.2x4.5µ) C. baileyiand large-sized (8x6.5µ) C. galli. Recently, 23 characterized pigeon's cryptosporidia in Southern China by DNA sequencing of small subunit ribosomal RNA (SSU rRNA) gene, and detected them in 0.82% out of 244 domestic pigeons. They added that they were morphologically and genetically belonging to C. meleagridis(5.15x4.6µ) and C. baileyi(6.11x5.16µ).As the present cryptospodial oocysts were small-sized (4.5-5µ), they belong to the zoonotic C. meleagridis.

    It is worth mentioning that during the present study, cryptosporidian oocysts were reported from pigeons in Assiut for the first time. As this parasite is one of the most serious human protozoan parasites, it is recommended that domestic pigeons in all Egyptian Governorates should be examined genetically to find out if the cryptosporidian oocysts found in their droppings are actually of human origin as this will indicate that these pigeons act as reservoir hosts to human beings in the surrounding dwellings.

    In the present study, the total prevalence of Microsporidium sp. in fecal samples of fifty examined droppings of domestic birds was 40 % and this disagreed with36 who showed that there was 8.6% microsporidial spores found in droppings from urban feral pigeons in Poland. This may be attributed to environmental pollution with microsporidial spores in Assiut and may be potentially infectious to domestic animals and birds by direct contact with them.

    Although these spores were reported frequently from fecal droppings of pigeons 18, 19 from Spain, 6 from the Netherlands, 12 from Brazil, 36 from Poland, 3 from Iraq, 31 from Iran) it had been not reported from Egyptian pigeons before; denoting that our record is for the first time from Egypt.

    The discovery of zoonotic strains of microsporidiosis that can infect man even by inhalation of pigoen's droppings 6, 17, 36 highlights the extreme risk of human infection particularly pigeon fanciers living in association with domestic pigeons.

    Hence, future studies are recommended to examine domestic pigeons, droppings not only by acid fast stain but also by genotyping techniques in order to explore their exact role as reservoir hosts for human microsporidiosis.

    Regarding Toxoplasma gondii, detection of the parasite in tissue lesions was very difficult because the disease is usually manifested by mild clinical symptoms and developed as an unapparent infection, accompanied by low parasitaemia27. Therefore; the detection of anti-Toxoplasma antibody response appeared to be the suitable tool for early and accurate diagnosis 24.

    In the present study, the prevalence of toxoplasmosis in fifty domestic pigeon's sera was estimated by latex agglutination test which showed that the seroprevalence of infection was 58%. The advantages of using Latex Agglutination test agreed with30 in that it detects total antibody level. Moreover, it is simple to perform, and required no expensive capital equipment. Toxoplasmosis seroprevalence studies conducted with pigeons from different continents exhibited different prevalence rates. In Portugal; rates ranging from 4.0% to 5.9% 38, in Colorado in United States was 6–10% of domestic pigeons tested by the Sabin–Feldman dye test 13.

    The levels of pigeon's antibodies to T. gondii in southern China was evaluated by Modified Agglutination Test (MAT) mainly because of its high specificity, sensitivity and cost-effectiveness; the cut-off titer of MAT for positive infection in pigeon was 1:5 which was considered indicative of T.gondii exposure 39.

    Seven (58.3%) out of 12 inoculated pigeons in southeastern Brazil were tested positive for anti-T. gondii antibodies by MAT (modified agglutination test) and IFAT(Indirect Fluorescent Antibody Test), Titers ranged from 1:40 to 1:5120 by MAT and 1:512 to 1:4096 by IFAT14.

    40found that the seropositivity of 275 domestic pigeon serum samples was 8.7% in southern China using Modified Agglutination Test (MAT), the difference in seropositvity of T. gondii in pigeons may be attributed to differences between feral and domestic pigeons, under different geographical conditions, serologic tests used, as well as bird husbandry practices and bird welfares. The high prevalence of T. gondii in the examined domestic pigeons is probably due to technical deficiencies in the management of pigeon breeding where the circulation of cats may be permitted. Sero-prevalence of Toxoplasma antibodies in northwest China was detected in 11.86% of examined domestic pigeons with titer 1:5-1:100 11. Moreover, T. gondii antibodies were with overall percentage of 62.5% was detected in sera of doimestic pigeons in Nigeria 7.

    From Egypt, 20 using serological, histopathological and immunohistochemical diagnostic methods, Toxoplasma gondii was detected in domestic pigeons from Giza, Fayoom, Beni-Suef and Minya Governorates (Egypt). Their study indicated soil contamination and observable infection in pigeons which could be considered a major danger of human infection.

    The present study is the first study of toxoplasmosis detection in domestic pigeons in Assiut, Egypt. As domestic pigeons live in intimate association with human beings in their dwellings, they could be a very dangerous reservoir host in transmitting the disease to man. However, future studies are recommended to find out if pigeon's Toxoplasma strain is of the pathogenic human strain.

    Conclusion

    Microsporidium sp. was recorded from domestic pigeons in Egypt for the first time and the present study indicated that domestic pigeons may be considered as a reservoir host for Toxoplasma,Cryptosporidium and Micro-sporidiumhuman infection which represents a serious human public health problem especially for high risk group of population living in the same dwellings with pigeons. Moreover our results provide a base line data for planning future researches and control strategies against possible zoonotic domestic pigeons, parasites.

    Ethical Considerations

    All applicable international, national and institutional guidelines for the care and use of animals were followed and the study and steps of practical experiments were approve by the Research Ethical Committee of the Faculty of Medicine, Assiut University, Egypt.

    Acknowledgments

    We confirm that this research was not funded by any organization.

    Author's Contribution

    Refaat M.A. Khalifa; Planning the study design , supervising and revising the manuscript

    Abdallah A.E. Hassan: Follow up of parasitological studies

    Mohsen I. Arafa: Revising and writing the results

    Hanan E. M. Eldeek: Follow up of serological studies

    Wafaa G. Mahmoud: Undergoing the practical tests and writing the mauscript

    References

    1.Abreu-Acosta N, Forondo-Rodiguiz P, López M, Valladare B. (2009) . Occurrence ofCryptosporidium hominisin pigeons (Columbalivia). ActaParasitologica,54 1, 1-5.
    2.N E Ahmed, L M El-Akabawy, R S El-Madawy, E I Toulan. (2013) Studies on intestinal protozoa of poultry in. , Gharbia Governorate,Benha.Veterinary Medical Journal 25(2), 78-81.
    3.Al-Sadi H I, Al-Mahmood S S. (2013) Microsporidial infection in some domestic and laboratory animals in. , Iraq.International Journal of Basic and Applied Medical Science 3(3), 78-91.
    4.A M Bahrami, Hosseini E, Razmjo M. (2013) Important parasite in pigeon, its hematological parameter and pathology of intestine.World. , Apply Science Journal 21(9), 1361-1365.
    5.Bamaiyi P H, Redhuan N E. (2016) Prevalence and risk factors for cryptosporidiosis: a global emerging neglected zoonosis. , Asian Biomedicine 10(4), 309-325.
    6.Bart A, E M Wentink-Bonnema, E R Hendrema, Buija J, T van Gool. (2008) Frequent occurrence of human-associated microsporidia in fecal droppings of urban pigeons in Amesterdam, The Netherlands.Applied andEvironmentalMicrobiology. 74(22), 7056-7058.
    7.Bata S, Karshima N S.Oshada AHet al.,(2020): Detection ofToxoplasmagondiiantibodies in domestic pigeons (Columbaliviadomestica) in Jos, north cebtral Nigeria. Parasitol Vector Biol., Open Access, Article. in press
    8.S A Bhat, J K Khajuria, Katoch R, M Y Wani, Dhama K. (2014) Prevalence of endoparasites in backyard poultry in North Indian Region: A performance based assessment study.Asian. , Journal animal veterinary Advances 9(8), 479-488.
    9.Borji H, Meghaddas E, G R Razmi, Azad M. (2012) A survey of ecto- and endo-parasites of domestic pigeons (Columbalivia). in Mashhad, Iran. Iranian Journal of Veterinary Science and Technology 4(2), 37-42.
    10.Borkatiki B, Katoch P, Goswami P, Godara R, J K Khajura et al. (2013) Incidence ofHaemoproteuscolumbaein pigeons of Jammu district.Journal of Parasitic Diseases.
    11.Cong W, Huang S, Zhou D, Xu M, Wu S et al. (2012) First report ofToxoplasma gondiiinfection in market-sold adult chickens, ducks and pigeons in North West China. Parasites and Vectors. 5, 110.
    12.W L Current, B L. (1990) Infections in man and domestic animals. In: Coccidiosis of man and domestic animals. P. L. Long, ed , Boca Raton, FL 155-185.
    13.J P Dubey, T A Felix, O C Kwok. (2010) Serological and parasitological prevalence ofToxoplasma Gondiiin wild bird from Colorido.Journal of Parasitology. 96(5), 937-939.
    14.Godoi F S L, S M Nishi, H F Pena, S M Gennari.2010.Toxoplasmagondii:diagnosis of experimental and natural infection in pigeons (Columbalivia)by serological, biological and molecular techniques.RevistaBrasileiradeParasitologiaVeterinaria,19. 4, 238-243.
    15.Faraj A A. (2014) Distribution ofCryptosporidiumspp infection in wild pigeons. in Baghda city,Iraq.BasrahJournal of Veterinary Research 1(2), 48-53.
    16.Gracia L S.. (2001).DiagnosticMedical Parasitology.ASM Press,Washington,DC
    17.T K Graczyk, Sunderland D, A M Rule, J Da Silva A, I N Moura et al. (2007) Urban feral pigeons (Columbialivia) as a source for air and water borne contamination withEnterocytozoonbieneusispores.Applied and Environmental. , Microbiology; 73, 4357-4358.
    18.Haro M, Izquirdo F, Henrique-Gil N, Andres I, Alonso F et al. (2005) First detection and genotyping of human-associated microsporidia in pigeons from urban Parks.Applied and Environmental. , Microbiology 71(6), 3153-3157.
    19.Haro M, Henriques-Gil N, Fenoy S, Izquierdo F, Alonso F et al. (2006) . Detection and genotyping ofEnterocytozoonbieneusiin pigeons.Journal of Eukaryotic Microbiology, 53 Suppl s1: 58-60.
    20.Ibrahim H M, Osman G Y.Mohamed AHet al.,(2018):Toxoplasmgondii:Prevalence of natural infection in pigeons and ducks from middle and upper Egypt using serological, histopathological and immunohistochemical diagnostic methods. , Vet. Parasitol. Reg. Stud. Reports 13, 45-49.
    21.Koompapong K, Mori H, Thammasonthijaren N, Prasertbun R, A R Pintong et al. (2014) Molecular identification ofCryptosporidiumspp. in seagulls, pigeons, dogs and cats in Thailand.Parasite. 21(52), 1-7.
    22.M A Lallo, Calabria P, Milanelo L. (2012) spores in stool from pigeons and exotic birds: Microsporidia spores in birds.Veterinary Parasitology-journal,190(3-4):. 418-422.
    23.Li J, Lin X, Zhang L, Qi N, Liao S et al. (2015) Molecular characterization ofCryptosporidiumspp. in domestic pigeons (Columbaliviadomestica). in Guangdong Province, Southern China.The journal Parasitology Research 114(6), 2237-2241.
    24.Marghany M E. Faculty of Medicine, Assiut University(2004).Some studies on toxoplasmosis in poultry transmissible toman M.D. Thesis , Egypt
    25.S M Marques, R M Quadros, C J Silva, Baldo M. (2007) Parasites of pigeons (Columbalivia) in urban areas of Lages. , Southern Brazil.ParasitoogiaLatinoamericana, Chile 62, 183-187.
    26.W R Maslin, K S Latimer. (2009) Atoxoplasmosis in canary fledglings: Severe lymphocytic enteritis with preferential parasitism. , of B lymphocytes.Avian Diseases 53(3), 473-476.
    27.A M Masoud, W D David, D C Armah. (1990) Toxoplasmosis in sheep in. , North Eastern United States.Journal of the American Veterinary Medical Association 196, 263-265.
    28.BCM Oliveira, Ferran E D.da Cruz MEet al.(2017): First description ofCryptosporidium parvumin carrier pigeons (Columbalivia).Vet. Parasitol.,30 !$#): 148-150.
    29.I A Özkul, Aydin Y. (1994) Small-intestinal cryptosporidiosis in a young pigeon.Asian. , Pathology 23, 369-372.
    30.S P Parker.Cubitt W.D. 1992.Modified latex agglutination test for antibodies toToxoplasma gondiiin eluates from Guthrie cards.Clinical. , Pathology 45, 907-909.
    31.Pirestani M, Sadraei J, Forouzandeh M. (2013) Molecular characterization and genotyping of human related microsporidia in free-ranging and captive pigeons of Tahran, Iran.Infection. , Genetics and Evolution 20, 495-9.
    32.M H Radfar, Fathi S, E N Asl, M, H R Seghinsara. (2011) A survey of parasites of domestic pigeons (Columbaliviadomestica). in South Khorasan,Iranian Veterinary Research 4(1), 18-23.
    33.Rodríguez F, Orós J, Rodríguez L, González J, Castro P et al. (1997) Intestinal cryptosporidiosis in pigeons. , Avian Diseases 41, 748-750.
    34.Sari B, Karatepe B, Karatepe M, Kara M. (2008) Parasites of domestic (Columbaliviadomestica) and wild (Columbalivialivia) pigeons in Nigde. , Turkey.Bulletin of the Veterinary Institute inPulawy 52, 551-554.
    35.SAS. (2001) SAS/ STAT Guide for personal computer (version 8.2. , End). SAS. INST., Cary, N.C.Co., New York
    36.Slodkowiicz-Kowalska A, T K Graczyke, Nowosad A, Majewska A. (2013) First detection of microsporidia in raised pigeons. in Poland.Annals of Agricultural and Environmental Medicine 20(1), 13-15.
    37.R G Steel, J H Torrie. (1982) . Principles and Procedures of Statistics”. A Biometrical Approach (2 nd Ed) Mc Grow- .
    38.Waap H, Vilares A, Rebelo E, Gomes S, Angelo H. (2008) Epidemiological and genetic characterization ofToxoplasma gondiiin urban pigeons from the area of Lisbon (Portugal).Veterinary Parasitology. 157, 306-309.
    39.Yan C, Yue C L, Z G Yuan, He Y, C et al. (2009) gondiiinfection in domestic ducks, free-range and cadult chickens in southern China.Veterinary Parasitology. 165, 337-340.
    40.Yan C, C L Yue, S B Qiu, H L Li, Zhang H et al. (2011) Sero-prevalence ofToxoplasma gondiiinfection in domestic pigeon (Columbalivia) in Guangdong Province of southern China.Veterinary Parasitology. 177, 371-373.
    41.D S Young. (1995) . Effects of drugs on clinical laboratory tests,5thed.AACCPress .