Seroprevalence of Toxoplasma Gondii Infection in Chickens and Humans in Beni Suef, Egypt

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1 Global Veterinaria 11 (2): , 2013 ISSN IDOSI Publications, 2013 DOI: /idosi.gv Seroprevalence of Toxoplasma Gondii Infection in Chickens and Humans in Beni Suef, Egypt S.M. Aboelhadid, A.E. Abdel-Ghany, M.A. Ibrahim and H.A. Mahran 1 Departmant of Parasitology Fac. Vet. Med. Beni-Suef University, Egypt 2 Hygiene, Management and Zoonoses Departmant Fac. Vet. Med. Beni-Suef University, Egypt Abstract: This study was performed to determine the seroprevalence of T. gondii infection in both domestic chickens and humans in Beni-Suef area, Egypt. The sera of 215 (90 free-range and 125 farmed) chickens were examined using the modified agglutination test kits (MAT). Besides, 250 human sera samples were also examined for IgG by ELISA kit. The obtained results revealed that antibodies against T. gondii were detected at a rate of 20% and 9.6% in free-range and farmed chickens respectively. Statistically, the difference between the two groups was significant (P<0.05). Regarding humans, the seroprevalence of T. gondii infection was 35.2%. Although statistically non significant (P>0.05), a higher seroprevalence of T. gondii antibodies in poultry contacts (37.5%) than non-poultry contacts (30.5%) was recorded. No significant difference between males (34.7%) and females (35.8%) was found (P>0.05). Regarding the age, the highest seropositivity of 45.0% and 41.66% was observed among individuals of years and >50 years respectively. From this study, preventive measures to avoid transmission of infection to humans and animals must be done. Key words: Toxoplasma Gondii Chickens Humans Seroprevalence INTRODUCTION in the environment and are used as sentinel animals in areas where t he prevalence of human infection is high Toxoplasma gondii (T. gondii) is an important [5-7]. The role of farmed chickens in Toxoplasma intracellular protozoan parasite widely prevalent in transmission to humans is of low importance, since their humans and animals, including poultry, throughout the breeding is fast and contact with felines is not allowed, in world [1, 2]. The infection caused by T. gondii is generally contrast to domestic breeding in low scale, where the transmitted to humans either congenitally, or via ingestion birds live for years in the same ecosystem as felines [8, 9]. of undercooked or raw meat from infected animals, or It has been estimated that one third of the world ingestion of food or water contaminated with oocysts population has been infected with T. gondii [10]. excreted by infected felids [3]. Most infections in immunocompetent humans are In Egypt, the role of domestic chickens asymptomatic (latent) and in up to 10% of infected (Gallus domesticus) in the transmission of T. gondii was individuals, cervical lymphadenopathy or ocular disease investigated only in a few studies. Poultry meat is an occur (3). On the contrary, toxoplasmosis is most important part of cuisine, consumed widely allover the dangerous to two populations: immunocompromised world; therefore, consumption of uncooked or not persons and fetuses whose mothers acquire acute properly cooked poultry meat may pose a risk factor for infection during pregnancy [11]. In immunocompromised T. gondii infection in humans or animals [4]. individuals, it can cause life-threatening infections such Free-range (FR) chickens are considered important as encephalitis, pneumonia and chorioretinitis [12]. intermediate hosts of T. gondii, as cats preying on these Acute maternal infection during pregnancy can lead to infected animals can shed millions of environmentally transplacental transmission and subsequent infection in resistant oocysts on the ground surrounding human the fetus causing abortion or severe damage to the fetus households. Chickens feeding from the ground are, at birth or later in life (11). The rising prevalence of therefore, a good indicator of the prevalence of T. gondii toxoplasmosis and the increasing clinical cases in Corresponding Author: Shawky M. Aboelhadid, Departmant of Parasitology Fac. Vet. Med., Beni-Suef University, Mob: , Fax:

2 immunocompromised patients and patients with collected. The blood samples were transferred in ice tank congenital toxoplasmosis should draw attention to to the laboratory where serum samples were obtained and address toxoplasmosis as a serious public health problem. stored in - 20 C until further analyzed. The occurrence of T. gondii in poultry and their role in spread of infection to humans is still a disputable Serological Examination of Serum Samples: matter. In addition, little information is available on Chicken Sera: Sera from chickens were diluted two-fold infection rates in domestic birds in Egypt. Therefore, this starting at 1:40 to 1: 2560 and assayed for T. gondii study was performed to throw lights on the epidemiologic antibodies with the modified agglutination test (MAT) aspects of T. gondii infection in chickens and humans in conducted as previously described by Dubey and Beni-Suef Governorate, Egypt. Desmonts [13] using TOXO-HAI FUMOUZE kit. MAT titers of 1:80 or higher were considered positive for MATERIALS AND METHODS T. gondii antibodies. Sample Collection: The samples were obtained Human Sera: Serum samples were examined by ELISA to from different localities in Beni-Suef Governorate identify the presence of IgG, using Toxoplasma IgG (30 13' N, 31 40' E), situated 120 kilometers south to Cairo, enzyme immunoassay test kit, catalog number: IGGT-96. Egypt with an average altitude of 46 meters. A total of Kit. Antibody levels were evaluated by following the 465 samples including chickens (215) and humans (250) instructions of the set manufacturers and the results were were collected during the period from July 2011 to March expressed in titers [14] The samples were investigated serologically in the department of Parasitology, Faculty of Veterinary Statistical Analyses: Differences in the seroprevalence of Medicine, Beni Suef University for detection of T. gondii T. gondii-infected FR chickens and farmed chickens and antibodies. between the different groups of the examined humans were analyzed using a Chi square test in SPSS for Chicken Samples Windows (Release 18.0 standard version, SPSS Inc. Free-Range Chickens: A total of 90 free-range chickens Chicago, Illinois). The differences were considered were purchased from rural households. They were statistically significant when P<0.05. approximately 1 year old, kept free ranging on ground and had free access to feed and water. Chickens were RESULTS AND DISCUSSION transported to the laboratory where about 5 ml blood was taken from each after slaughtering and serum was In this study, investigation of the prevalence of T. obtained by centrifugation of coagulated blood. gondii infection in chickens (both free-range and farmed) and humans in Beni-Suef Governorate was determined Farmed Chickens: Blood samples were collected from serologically. 125 broiler chickens which were slaughtered at poultry The results obtained in Table (1) indicated that, by shops. The broilers were about 45 days old and came from using MAT, the overall T. gondii seroprevalence in different farms. Samples were transferred in ice tank to the chickens was 13.95%. The seroprevalence in FR chickens laboratory where serum samples were obtained. The sera and farmed chickens was 20% and 9.6% respectively. were stored in - 20 C until further analyzed. Statistically, the difference between the two groups was significant (P<0.05). MAT was chosen because it is Human Samples: A total of 250 blood samples were taken sensitive and specific for detecting T. gondii antibodies from apparently healthy individuals consisted of 144 men in bird species compared to other serologic methods (92 poultry contacts and 52 non-poultry contacts) and [4, 15]. Several studies indicated serologic prevalence of 106 women (76 poultry contacts and 30 non-poultry T. gondii MAT antibodies in chickens at a rate of 47% contacts) of different age groups. Most of the sampled from Egypt [16], 36.5% from Brazil [5], 39.5% from India subjects were found in the age range years old. [17] and 7.26% from China [18]. However, these studies The blood samples were collected from farmers' houses are not strictly comparable because little was known and inhabitants related to poultry rearing. All poultry about the husbandry methods used to raise the chickens. contact individuals were residents in rural areas from The seroprevalence of T. gondii infection in FR chickens which poultry (free-range chickens) samples were in this study was corroborated with that reported in many 140

3 Table 1: Seroprevalence of T. gondii infection in chickens by modified agglutination test (MAT) Positive No. (%) of each positive titer Chickens No. examined Total (%) 1:80 1:160 1:320 Free-range (20.0) 3 (16.66) 7 (38.88) 8 (44.44) Farmed (9.6) 9 (75.0) 2 (16.66) 1 (8.33) Total (13.95) 12 (40) 9 (30.0) 9 (30.0) Table 2: Seroprevalence of T. gondii antibodies among humans in each category investigated during the study (n = 250) Variable Category No.examined No. Positive % of positive individuals Contact with poultry Poultry contacts Non-poultry contacts Sex Male Female Age group (years) > Total countries allover the world [4]. The lower seroprevalence In many instances, especially in developing of T. gondii antibodies observed in farmed chickens was countries, FR chickens are slaughtered at home or in expected, since the confinement, management and certain unsupervised slaughter facilities and their viscera are left hygiene measures reduce or even extinguish the contact for scavengers or improperly disposed off. T. gondii with sources for T. gondii infection. The same was not infection can be transmitted if care is not taken to wash true for FR chickens, since they spend some time inside hands thoroughly after cutting and during cooking of the sheds, have free access to grazing areas and therefore meat; however, risk assessment studies have not been were more susceptible to the contact with different undertaken [4]. infection sources of the parasite. Moreover, the FR The overall seroprevalence of T. gondii antibodies in chickens were slaughtered later, aged about one year old, the study population was 35.2 % as shown in Table (2), a which increased the chance of getting into contact with result which is similar to that reported by Yaneza. and possible sources of infection. Although lower than that of Kumari and Ibrahim et al. [21, 22]. On the other hand, this FR chickens, the seroprevalence of T. gondii antibodies result was lower than that found by [23-26] who could in farmed chickens should be taken into account. It can be detect T. gondii infection in humans at a rate of 54%, explained by the improper hygiene demonstrated in these 56.7%, 51.8% and 59% respectively. The result of this farms which might have allowed contamination of the study demonstrated a wide evidence of human exposure environment, including feed and water by oocysts. to T. gondii in Egypt as previously reported byelsheikha The role of broilers raised on an industrial scale was et al. and Ibrahim et al.and. Ghoneim et al. [26-28]. discussed by Garcia et al. [19], considering them of minor Globally, there is a wide geographic variation in the importance in T. gondii transmission to humans, not only prevalence of latent T. gondii infection. Studies from because of the fast raising system, but also because it did different continents such as Latin America, Europe, Asia not allow contact with cats. However, the results and Africa have reported a range of prevalence estimates presented in this paper show that the broilers can and of 30%-75%, whereas prevalence estimates from USA should be considered as a source of infection. studies have had a range of 3%-42% [29]. The prevalence FR chickens exhibited higher levels of antibody titers of T. gondii infection changes according to social and than farmed ones (Table 1) which may be related to the cultural habits, geographic factors, climate and age of birds (about 1 year in FR chickens and about transmission route [30]. 45 days in those farmed). This can be better explained in Table (2) also indicated that poultry contacts show a light of the report of Dubey [20] who indicated that higher seroprevalence of T. gondii antibodies (37.5%) Toxoplasma antibodies were detected within 3 weeks of than non-poultry contacts (30.49%), although the infection and persisted in high titers for 5 years even in difference was not statistically significant (P>0.05). the absence of re-infection. The high seroprevalence of T. gondii infection in poultry 141

4 contacts might be related to the fact that most of the Toxoplasma infection may have been higher in the past examined individuals were peasants that having the because the use of frozen meat was less common and chances of contact with animals including poultry and animal rearing practices have subsequently improved [41]. cats, beside their living style such as poor sanitary habits and probably low level of hygiene during food CONCLUSION preparation [10]. It is worth mentioning that the high seroprevalence of T. gondii in poultry contacts does not The present work revealed the seroprevalence of necessarily indicate that the occupational exposure to T. gondii in chickens (both free-ranged and farmed) chickens has a correlation with seropositivity of T. gondii beside human population resident in Beni-Suef infection in humans, as there are other important risk Governorate, Egypt, which indicated that the distribution factors may contribute to the prevalence of T. gondii of T. gondii in the living environment of local people is infection including food handling and preparation quite high and, moreover, suggested that the potential hygiene, eating habits (establishment of restaurants risk of domestic birds as a source of T. gondii infection in serving a quick meat meals which may be insufficiently humans and animals in this region, so preventive cooked or eating raw vegetables without washing), level measures might be very necessary to avoid transmission of natural immunity, level of environment contamination of infection to humans and animals. with oocysts and the degree of contact with cats [31, 32]. ÇThis might be the explanation of the seropositivity of ACKNOWLEDGMENT T. gondii in non-poultry contacts. In this investigation, no significant difference in the The authors are greatly thanks for Dr. Mahdy, EA for seroprevalence of T. gondii infection between males support. They appreciated greatful thanks for Dr. Safaa (34.72%) and females (35.85%) was found (P>0.05), AM. for helping. suggesting that sex does not influence exposure to and or/ immune response to T. gondii [33, 34]. This finding REFERENCES correlates with that of Carmen et al. [35] who found that there is no difference in the seropositivity of 1. Dubey, J.P., 2010a. Toxoplasmosis of Animals and toxoplasmosis between males and females. In contrast, Humans. Secondth edition. Boca Raton, New York: [36] found higher percentage of seropositivity to CRC Press Inc., pp: toxoplasmosis in males (66%) than females (58%) and 2. Zhou, P., Z.Chen, H.L. Li, H. Zheng, S. He, R.Q. Lin Coelho et al. [37] reported a seroprevalence of 79.9% in and X.Q. Zhu, Toxoplasma gondii infection in men and of 63.4% in women. Also Uneke et al. [34] humans in China. Parasites & Vectors, 4: 165. indicated that men are more prone to T. gondii infection 3. Montoya, J.G. and O. Liesenfeld, than women. However, Hamadato et al. [38] found that Toxoplasmosis. Lancet, 363: Toxoplasma antibodies were more in females than males 4. Dubey, J.P., 2010b. Toxoplasma gondii infections in especially above 40 years old. chickens (Gallus domesticus): prevalence, clinical Regarding the age of the examined population, the disease, diagnosis and public health significance. highest seropositivity of 45.0% and 41.66% was observed Zoonoses Public Health, 57: among individuals of years and >50 years 5. Dubey, J.P., D.H Graham, C.R.T. Blackston, respectively, while the lowest (11.1%) was amongst the S.M. Lehmann, A.M. Gennari, S.M. Ragozo, 20 year's age group (Table2). Similar age-related S.K. Nishi, O.C. Shen, D.E. Kwok, P. Hill and increases in Toxoplasma seroprevalence have been P. Thulliez, Biological and genetic reported in numerous studies of various populations characterization of Toxoplasma gondii isolates from worldwide [39]. On the contrary, Swai and Schoonman chickens (Gallus domesticus) from São Paulo, Brazil: [32] reported that the higher seroprevalence rates of Unexpected findings. International Journal for toxoplasmosis were found in age group ( 20 years) as Parasitology, 32: compared to age group (51-60 years). The increased 6. Dubey, J.P., S.M. Gennari, M.B. Labruna, seropositivity of toxoplasmosis with age might be due to L.M. Camargo, M.C. Vianna, P.L. Marcet and probability of contact with oocysts of Toxoplasma during T. Lehmann, Characterization of Toxoplasma professional activity, gardening, etc. The age trends could gondii isolates in free-range chickens from Amazon, also be explained by a cohort effect [40] as the risk of Brazil. Journal of Parasitology, 92:

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