726 Advances in Environmental Biology, 6(2): 726-732, 2012 ISSN 1995-0756

This is a refereed journal and all articles are professionally screened and reviewed ORIGINAL ARTICLE

Pathological Study on Parasitism in Racing Pigeons; An Indication of Its Effects on Community Health

1Ali Mohammad Bahrami, 2Alizaman Doosti, 3Hossein Nahrevanian, 4Morteza shamsi

1School of Veterinary Sciences, Ilam University, Ilam, Iran 2Department of biology, Payam-e Noor University of Ilam, Iran 3Associate Professor & Chief of Parasitological Laboratory, Pasteur Institute of Iran,Tehran Iran 4School of Veterinary Sciences, Ilam University, Ilam, Iran

Ali Mohammad Bahrami, Alizaman Doosti, Hossein Nahrevanian, Morteza shamsi: Pathological Study on Parasitism in Racing Pigeons; An Indication of Its Effects on Community Health

ABSTRACT

Objective: Several non-official reports from different clinics, governmental veterinary head-quarters and bird keeper indicated that most of the young pigeon die with suspicious of infection to parasites. In addition, the pigeon owners were complaining of skin itching on there head. Therefore, this study was conducted to determine pathological study on parasitism in racing pigeons with an indication of its effects on community health. Materials & Methods: This research was carried out from May to September 2011, by experimental study on 250 (168 adults and 82 nestlings) blood and faecal samples (Soulsby, 1982) randomly collected from suspected pigeons, mostly young and 25 specific free pathogen birds as control. Tissue samples of both infected and control birds for were removed to compare for histological study. Moreover, 12 hair samples from candidates of pigeon owner were checked for external parasites. Results: The data indicated prevalence rate of various helminthes including Raillietina achinobothridia (10.4%), Syngamus trachea (8.4%), Capillaria colombae (6%) and Ascaridia colombae (8.4%). The results revealed some porotozan infections including colombae (20.8%), Trichomonas gallinae (26.8%) spp (1.2%) and spp (21.6%) and also ectoparasites including Lipeurus spp (3.2%), Menopen gallinae (15.2%), Ceratophyllus colombae (10.4%) and Louse fly (12%). Multiple infections were observed with internal parasites was 19/4%. However, co-infection of internal and external parasites was 24.4%. Meanwhile, 5 out of 12 of the hair samples from pigeon owners have been infected with the fleas (Ceratophyllus colombae) and lice (Menopen gallinae) with clinical manifestation of allergic urticarial reaction and itching. Histological studis showed a visible vascular congestion and a massive lymphoplasmacytic infiltration inside the smooth muscular layer of the small intestine of infected pigeons. This result indicates that racing pigeons and their owners may be at high risk of single or multiple parasitic infections.

Key words: Endoparasite, Ectoparasites, Ovum, Birds, Epidemiology.

Introduction are swimming with filth and disease, as everyone knows [3,15]. Those who watch these birds can Pigeon are seen in more region of the world barely imagine how detrimental their disorderly except the poles. Pigeon live side by side with human reproduction may be and how many risk them post to and other animal species in the nature and they are human health [20]. bred as a source of food as a hobby, symbol and for Pigeons can carry or transmit pigeon experimental aims [5,9]. Encephalitis, Histoplasmosis, Newcastle disease, Pigeon are probably the most common nuisance Ornithosis, Cryptococcosis, Coccidiosis, bird. Everyone knows that pigeons have adapted to Toxoplasmosis, Pseudo-tuberculosis, and life in the city, and they seem to be everywhere in Salmonellosis. Pigeons can carry fleas, ticks, mites, urban environments. Unfortunately, the bird lovers of and other parasites [3,15]. It is interaction with man the world feed them, and they have developed a and other domestic and wild birds portends it as a dependence upon people, thus reinforcing their potential carrier of zoonotic parasites [1]. Several dependency upon urban areas. They roost on signs, health problems can affect pigeon, but parasite ledges, almost anywhere, and they bring nesting infections play a major role. Information on the material and leave droppings everywhere. Pigeons parasitic infection of domesticated pigeon in

Corresponding Author Dr. Ali Mohammad Bahrami PhD, Animal Pathology -Post-Doc, Microbiology: Fax: 00988412224308 E-mail1: [email protected] 727 Adv. Environ. Biol., 6(2): 726-732, 2012 different region of Iran appears to be poorly Sampling from pigeons: documented [16]. The prevalence of pigeon parasites was studied on south Khorasan, Iran, were Ascaridia The tray at the bottom of cages of the control colombae (16.66%), Cotugnia digonopora (13.79%), and experimental pigeon were completely washed Raillietina achinobothridia (32.35%), Menopon and disinfected. Then lay in cages again, we had galline (44.11%), Pseudolynchia canariensis collected fresh faeces (at least 3 grams) from each (63.72%), Columbicola colombae (79.41%), bird. Data were collected according questionnaire Cryptosporidium oocyst (2.94%), Eimeria spp form prepared before including information (40.19%) and Haemoproteus colombae (47.05%). In regarding, No of the birds, No of the death, No of the Costa Rica, Haemoproteus spp was detected in 4.8% sick birds, weight of the birds, environmental of birds; in Queensland, Australia, a total of 3, 059 temperature, information regarding medicine used birds were examined and Haemoproteus spp was for the bide from 30 days before, No of the feed per a found in 31.4% of them [21,2]. In the state of Minas day, feed ingredient, It will be necessary to mention Gerais, in southeastern Brazil, a research study with the owner name, date of sampling and characteristic free living pigeons showed that all pigeons were of bird, and the samples were tested in laboratory infested with Pseudolynchia canariensis a blood quickly. feeding louse fly and with Haemoproteus colombae and Eimeria spp. oocysts. Ascaridia colombae was Sampling from bird keepers detected in 4.91% of pigeons and 3.27% presented with mixed infections caused by A. colombae and Twelve person of pigeon owner how were Raillietina spp [20]. engaged more than 2 hours per a day with the birds The aim of current study was to determine the and had history of etching their head, candidate for presence of ectoparasites and endoparasites in pigeon checking their hair of their head for ectoparasites to that congregate around the public squares of lages check them for their complain about etching may be and to check the pigeon owner to see is there any its due to ectoparasites , For this propose we had relationship of common ectoparasites between the close around the neck of the person with the white man and birds. cloth and then the hire of the head had been combed with cotton mixed with Ether, try had been make to Materials and Methods combed all the head from each direction, and than the cloth were shacked in the jar and then sample of Study area: the jar were proceed for identification under the microscope. Several non-official reports from different clinics, governmental veterinary headquarters and Diagnostic methods: bird keeper indicated that most of the young pigeon die with suspicious of infection to parasites. In faecal samples of control and experimental birds addition, the pigeon owners were complaining of were examined by direct smear method whereas egg skin itching on there head. Therefore, this study was per gram (EPG) was counted by modified McMaster conducted to determine pathological study on technique and centrifugal flotation method using parasitism in racing pigeons with an indication of its Sheather’s saturated sugar solution [19]. The effects on community health of the Ilam city, located ectoparasites were collected as described by Soulsby in western part of Iran sharing 465 km common [19], briefly after killing the pigeons by anaesthesia, border line with Iraq country, with the sub they were immediately placed in a polythene bag and climatically environment condition. the parasites collected after leaving the pigeons, 90% of the samples collected were dead pigeon. The nest Birds: material for ectoparasites was preserved for identification purposes in 70% alcohol. This research was carried out from May to Subcutaneous nodules of each bird were fixed in September 2011, by experimental study on 250 (168 10% potassium, heated for 20 min in a jar containing adults and 82 nestlings) blood and faecal samples water and their sediments were searched for parasite. [19] randomly collected from suspected pigeons, The blood samples were collected from control mostly young and 25 specific free pathogen birds as and other experimental groups of the birds using an control. Tissue samples of both infected and control insulin syringe inserted through a brachial vein birds for were removed to compare for histological catheter. Each sample proceeded, fixed and stained study. Moreover, 12 hair samples from candidates of with Giemsa dyes. For diagnosis of trichomonans pigeon owner were checked for external parasites. gallinae, wet and sterile swab were taken from The care was taken to avoid any contamination from surface of mouth, throat and larynx of birds and after outside to animal house, located at School of preparation slide smears, the samples were studied Veterinary Sciences, Ilam University. under the light microscope. All parasites were identified using the parasitological keys [19].

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For internal parasites entire alimentary tract, gallinae (26.8%) Cryptosporidium spp (1.2%) and respiratory system, liver, heart, kidney and Eimeria spp (21.6%) and also ectoparasites including reproductive tract were searched and examine. The Lipeurus spp (3.2%), Menopen gallinae (15.2%), parasites removed and washed by water and a Ceratophyllus colombae (10.4%) and Louse fly number of nematodes were cleared in lacto phenol (12%). Multiple infections were observed with for identification and cestodes were fixed in 10% internal parasites was 19/4%. However, co-infection formalin and stained with carmine acid for further of internal and external parasites was 24.4%. studies. SPSS version 9.0 for Windows was used for Meanwhile, 5 out of 12 of the hair samples from statistical analysis of the experimental data. pigeon owners have been infected with the fleas (Ceratophyllus colombae) and lice (Menopen Histological study: gallinae) with clinical manifestation of allergic urticarial reaction and itching (Table 2). The nest of Tissues of different organ including, thymus, the pigeon has been checked for external parasites intestine (jejunum, ceaca) liver of the infected and and we found Ceratophyllus colombae and Menopen control birds separated and preserved in 5% gallinae. The maximum and minimum formalin. Tissues were prepared for microtome, cut environmental temperature of area measured and in in 8 μM and stained in haematoxylin and eosin. order was 32 and 43 ̊с and the maximum humidity of Slides were studied on Olympus camera attached area was 6%. microscope. Observation was recorded and microphotography was done for projection slides and Histological founding: photographs. A comparison of control and infected tissues Statistical analysis: shows that, the thymus and intestinal tissue sample of infected young and adult birds due to infection The computer software, SPSS Version 9.0 for they became very small, oedematous or with windows (SPSS Inc., Chicago, LL, USA) and Chi- petechial haemorrhages. Histological studis showed a Square tests were used for statistical analysis. visible vascular congestion and a massive lymphoplasmacytic infiltration inside the smooth Results: muscular layer of the small intestine of infected pigeons. Out of 250 pigeon sample 224 (89.6%) were Multiple haemorrhages were seen in the mucosa positive with at least one of parasitic infections. of the intestine and ceaca. Patches of necrotic Among them, 16.62% had multiple infections with epithelial cells and multifocal areas of lymphocytic internal parasites, 20.08% were infected with infiltrates in mucosa of jejunum of infected pigeon ectoparasites and 27.23% presented infections with were observed Extensive zone of necrosis were seen both internal and external parasites. The entire in infected young pigeon. The intestinal villous experimental birds as control were free of any atrophy and shortening of microvilli were observed internal and external parasites (Table 1). in infected birds. A cross-section of liver from Symptoms of worms consist of weight loss and pigeons infected by internal parasites shows, massive in case of sever multiple worm infestation diarrheal congestion of central vein and also dilation of hepatic were seen in the pigeons. Infected young birds grow sinusoids. (Figs 1-4). slower and were even losing much body weight Out of 12 pigeons owner check for external resulting high rate of mortality. parasites 5 of them they were carry lice (Menopen The data indicated prevalence rate of various gallinae) and one person with fleas (Ceratophyllus helminthes including Raillietina achinobothridia columbae), all of 5 infected pigeon owner were had (10.4%), Syngamus trachea (8.4%), Capillaria filling of itching their head with allergic urticarial colombae (6%) and Ascaridia colombae (8.4%). The reaction. results revealed some porotozan infections including Haemoproteus colombae (20.8%), Trichomonas

Table 1: Percentage of internal and external parasites and multiple infections in pigeons Parasite No. infection Overall Percentage* Adults Nestling n % n % Multiple infection with internal parasites 23 13.69 12 14.63 16.625 Multiple infection with external parasites 27 16.07 18 21.95 20.08

Multiple infection with internal and external 37 22.02 24 29.26 27.23 parasites Total pigeon 168 82 * Out of 224 infected pigeon

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Table 2: Prevalence of endoparasites and ectoparasites in pigeons Parasite No. infection Overall Percentage Adults Nestling n % n % Helminths Raillietina spp 21 12.5 5 6.09 10.4 Syngamus trachea 19 11.3 2 2.43 8.4 Capllaria spp 15 8.92 0 0 6 Ascaridia colombae 18 10.71 3 3.65 8.4 Ectoparasites Lipeurus spp 6 3.57 2 2.43 3.2 Louse fly 19 11.3 11 13.41 12 Ceratophylus columbae 18 10.71 8 9.75 10.4 Menopen gallinae 21 12.5 17 20.73 15.2 protozoan Haemoproteus columbae 42 25 10 12.19 20.8 Trichomonas gallinae 38 22.6 29 35.36 26.8 Cryptosporidium spp 3 1.78 0 0 1.2 Eimeria spp 23 13.96 31 37.8 21.6 Total parasites 243 118

Fig. 1: Photomicrograph showing a cross-section of a small vein of intestine from a pigeon infected by internal parasites. It shows a visible vascular congestion inside the smooth muscular layer of small intestine. (H&E 400×).

Fig. 2: Photomicrograph showing a cross-section of muscular layer of intestine from a pigeon infected by internal parasites. It shows a massive congested vessel inside the smooth small intestine. (H&E 400×).

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Fig. 3: Photomicrograph showing a cross-section of mucosal layer of intestine from a pigeon infected by internal parasites. It shows villous atrophy and shortening of microvilli. (H&E 400×).

Fig. 4: Photomicrograph showing a cross-section of liver from a pigeon infected by internal parasites. It shows massive congestion of central vein and also dilation of hepatic sinusoids is obvious. (H&E 400×).

Discussion: than nestling pigeon (p<0.05). Louse fly, Ceratophylus columbae and Haemoproteus Parasites are emerging as a significant avian columbae were significantly also higher in adults pathogen on a global scale, both ecologically and pigeon than in nestling (p<0.05). The present study is economically. However, important gaps remain in more or less resembling the result has been reported our understanding of its epidemiology and previously by and Msoffe et al. [12]. pathogenicity in wild populations, particularly in The helmenthes have been identified in this non-native hosts. study including Raillietina achinobothridia, In Iran, only few studies have been carried out in Syngamus trachea, Capillaria colombae and relation to parasite infections in pigeons. This is the Ascaridia colombae. Present results are similar to the first study to compare, the prevalence and intensity previous reports that R. achinobothridia, S. trachea, rates of parasites among pigeon species in the Ilam C. colombae and A. colombae were more pronounce province, western part of Iran. Categorization of than the other helmenths parasites in the pigeon birds into adult pigeon and nestling enable to show [7,14,17]. R. achinobothridia and A. colombae were that Eimeria spp were significantly more prevalent in shown to be important helminthes of pigeons. nestling than in adults, while helminthiasis due to T. Although, this is generally considered to be relatively gallinae, H. colombae and Ceratophylus columbae. harmless parasites, it will be interesting to study the Eimeria spp were significantly higher in in adults

731 Adv. Environ. Biol., 6(2): 726-732, 2012 reason of pigeons to be more susceptible or urticarial reaction. The most traumatic experience for helminthes a compared to other birds. the couple, however, was to learn that they were Protozoa parasites were identified in these invaded by fleas (initially, they had presumed they research study were consist of Haemoproteus were bothered by mosquitoes). This information colombae, Ttichomonas gallinae, Cryposporidium resulted in severe psychological distress with phobic and Eimeria that resembling reported by they work reactions and insomnia. Despite the successful on external and internal parasites of the pigeon from removal of the fleas and the pigeons that were source east of Iran. In comparison the results of this research of the pest, parasitophobia of the man persisted over with previous study shows that the percentage the following 4 months. This case is discussed from prevalence of parasites are more less than reported the broader aspect of health risks related to pigeons by [20]. All the samples collected from Eimeria and animal fleas. infected pigeons were infected by multiple parasites, showing associations between Eimeria sp and other Conclusion: parasites, that is in agreement with Tietz-Marques et al., [20]. In 13.96% of the adult’s pigeon and in Clean, sanitary lofts are most beneficial to 37.8% of the nestling pigeon Eimeria oocysts were keeping worms in check, but since pigeons often detected. Coccidiosis is one of the important mingle with many hundreds of other birds, a bird can protozoan diseases of birds. The diseases has a become infested through ingestion of worm eggs subclinical course in adults but young pigeons from the basket or through contact with stray exhibit such symptoms of clinical coccsidiosis as pigeons. Therefore, it is advisable to develop a fluffy feathers, anorexia and watery diarrhoea with preventative worming program in which all birds are mucus and [11]. The highest overall percentage rate wormed at least twice a year. Use of mask and cap of parasitic infection was T. gallinae (26.8%) that is for pigeon owner could protect them from allergic in agreement with reported by Bunbury et al., [4]. reaction. The reason for high prevalence may be due to the fact that the transmission of the parasites occurs Acknowledgments generally when the adults feed their young but can occur through food in feeders and water [10]. Adult This work was supported, in part, with grants birds may remain infected for a year or more and are from the Research Administrative Committee of Ilam a constants source of infection for their young [19]. University. 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