Author: Asgari, Qasem; Sarkari, Bahador; Amerinia, Maryam; Panahi, Saed; Mohammad-pour, Iraj; Sarvestani, Afrooz Sadeghi
Date published: May 1, 2013
Journal code: JJMB
Toxoplasma gondii is a worldwide parasite which infects any nucleated cells of birds and mammals including human. In human, it may cause severe medical complications in immunocompromised individuals or in congenitally acquired cases. The parasite can cause congenital abnormalities such as abortion, chorioretinitis, hydrocephaly and jaundice (1). The disease is severe in HIV positive individuals where HIV positive cases develop toxoplasmic encephalitis (2, 3).
G. gondii infection in livestock such as sheep and goats is responsible for considerable economic losses due to abortion of fetus. Infections with this zoonotic parasite are acquired mostly by consumption of undercooked or raw meat, which contains tissue cysts, or water contaminated with oocysts of G. gondii. T. gondii oocysts are shed by domestic cats and other felines resulting in widespread contamination of the environment. Domestic cats are most likely the main source of contamination as they are common and produce large numbers of oocysts (4).
Rate of Toxoplasma infection in farm animals is considered as the indicator of contaminated soil to oocyst of parasite. Moreover, consumption of meat and milk of farm animals has been considered as main sources of human infection. The current study was conducted to determine the seroprevalence of Toxoplasma infection in farm animals in southern Iran.
3. Materials and Methods
3.1. Study Area
The study was conducted in Fars province, south of Iran. The main city and capital of Fars province is Shiraz which is the sixth most populous city in Iran (the 2009 estimated population for the city was 1,455,073 people). Fars province has a moderate climate with relatively rainy mild winters and hot dry summers. Shiraz is located in the mountainous region of the province with an average altitude of 5,200 ft. The rainfall in recent years, during which an atmospheric condition has changed perceptibly, has been comparatively sufficient and has reached 23 inches in a year, but the average rainfall is between 14 and 18 inches. Figure 1 shows the location of this province in the country.
3.2. Animal Samples
A total of 346 serum samples from animals including 33 dogs, 35 horses, 80 cows, 95 sheep, 90 goats, 9 turkeys and 4 geese were collected from sub-urban farms and Shiraz slaughterhouse in 2010 and 2011. All serum samples were stored at -20° C until use.
3.3. Detection of Anti-Toxoplasma Antibodies in Sera Samples
Modified Agglutination Test (MAT) was used to detect specific antibodies to T. gondii in collected sera as originally described by Desmonts and Remington (5). The formaldehyde-killed whole tachyzoites of RH strain of I. gondii were used as antigens. Sera were diluted two-fold (1:20 to 1:160) and evaluated for anti-Toxop/asma antibodies while positive and negative controls were included in each plate. Antibody titers of > 1:20 were considered as positive.
Anti-Toxop/asma antibodies were detected in sera of 121 out of 346 (34.9%) animals. Most of animals (86%) had antibody titer of 1:20 while higher antibody titers, up to 1:640, were detected in sera of the rest of animals. The highest rate of Toxoplasma infection (55%) was found in cattle followed by dogs (51.5%), horses (40%), sheep (29.5%), goats (18.8%) and turkey (11.1%) No antibody was detected in any sera of the four geese.
Considering the sex of animals, 34.3 % of male and 40% of female animals were seropositive for Toxoplasma but the differences was not statistically significant (P > 0.05). Moreover, no significant correlation was found between the age of animals and seropositivity to toxoplasmosis.
Toxoplasmosis is a worldwide zoonotic disease which is caused by the protozoon T. gondii. The disease has got its public health as well as economic importance. It has been estimated that around 30% of the world population have serological evidence of Toxoplasma infection (6).
Human can be infected with T. gondii by ingestion of undercooked or raw meat containing tissue cysts (6). The relative roles of various potential sources of Toxoplasma infection for human are not well described. Knowledge of sources of infection within an area can provide valuable information for designing cost-effective food safety and preventive interventions. Evaluating the scale of infection in farm animals, especially those with edible meat, may help to estimate the scale of problem in any given region. Seroprevalence of toxoplasmosis is relatively high among human population in Iran (7-9). In a comprehensive study, 13,018 sera samples collected by stratified cluster random sampling method from 12 provinces in Iran were evaluated for toxoplasmosis and anti-Toxoplasma antibodies were detected in 51.8% of the samples (10).
Moreover, seroprevalence of Toxoplasma among animals is relatively high in Iran. In a study conducted by Hashemi-Fesharaki et al. in Iran, serum samples from 3311 sheep and 638 goats were examined for antibodies to G. gondii and antibodies were found in 24.50% of sheep and 19.25% of goats (11). In the current study seropositive rate of toxoplasmosis in sheep and goats were 29.5% and 18.8% respectively. This is consistent with currently available data on seroprevalence of toxoplasmosis in animals in other parts of the country (11-13).
Several studies stated a connection between age and sex of animals with the rate of Toxoplasma infection (11, 14), however such connection was not observed in the current study. Consumption of meat of infected lambs and goats is considered as one of the main sources of human infection, although consumption of milk might also be considered as another source of infection (15). In the authors " previous study in Fars province samples of brain, tongue, liver, and muscles of neck, intercostals, and femoral of sheep and goats were tested by PCR forloxopJ asm a infection. Infection was confirmed in tissues of 22.7% of goats and 37.5% of sheep (16).
The rate of toxoplasmosis in cattle in the current study was 55%, which is relatively higher than those reported from south-west (15.77%), north (21.6%) and south-west (37.5%) parts of the country (17-19). In th current study the seroprevalence rate of the infection in dogs was 51.5%. The dogs were referred to clinics for check up and clinically were found healthy. The seroprevalence of T.gondii antibodies in dogs in west and central parts of Iranusing an optimized indirect ELISA was 8.94% (20). Rate of toxoplasmosis in horses was 40% in the current study. The prevalence of toxoplasmosis in sport horses from Qazvin, in north-west of Iran, reported to be 71.2% (14).
The differences of prevalence rates of Toxoplasma in farm animals in Iran and also in other areas of the world might be due to variability of the susceptibility of hosts and also the serological methods which have been used to evaluate the seroprevalence. Furthermore, other factors such as management and hygienic standards in breeding, density of cats and environmental conditions are effective on the acquisition of!, gondii oocysts by animals (21). MAT has been the method of choice in most of the studies which evaluated the seroprevalence of toxoplasmosis in animals (22-24). However different studies have been using molecular methods to assess the rate of Toxoplasma infection in animals (16, 25). Whether the rate of molecular infection is well correlated to the seroprevalence rate, is still unclear.
The overall rate oiToxoplasma infection in farm animals in the current study was relatively high. It is noteworthy that the majority of these animals are raised by nomadic tribes. In Fars province, nomads and their animals move from one place to another place within Fars or neighboring provinces during summer and winter in search of food for their animals. This may increase the chance of acquiring the infection while their animals are grazing in different regions with relatively different climates.
In conclusion, high seroprevalence of toxoplasmosis observed in this region indicates that farm animals may play a major role in transmitting the infection to human through consumption of undercooked meats. Moreover, economic losses duo to Toxoplasma infection in these animal would be considerable. Further studies are required to explore the other epidemiological factors related to animal infection and to find out the strains of the parasite in different animals in the region.
The study has been the subject of a medical student thesis (Afrooz Sadeghi Sarvestani).
This study was financially supported by the office of Vice-Chancellor for research of Shiraz University of Medical Sciences (Grant No. 91-01-43-4257).
1. Montoya JG, Remington JS. Management of Toxoplasma gondii infection during pregnancy. Clin Infect Dis. 2008;47(4):554-66
2. Davarpanah MA, Mehrabani D, Neirami R, Ghahremanpoori M, Darvishi M. Toxoplasmosis in HIV/AIDS patients in Shiraz, southern Iran .1 RCMJ. 2007;9(l):22-27
3. Nissapatorn V. Toxoplasmosis in HIV/AIDS: a living legacy. Southeast Asian J Trop Med Public Health. 2009;40(6):115 8-78
4. Dubey JP. Toxoplasmosis - a waterborne zoonosis. Vet Parasitol. 2004?26(1-2):57-72
5. Desmonts G, Remington JS. Direct agglutination test for diagnosis oiToxoplasma infection: method for increasing sensitivity and specificity.; Clin Microbiol. 198u;ll(6)562-8
6. Elmore SA [ones JL, Conrad PA Patton S, Lindsay DS, Dubey JP. Toxoplasma gondii: epidemiology, feline clinical aspects, and prevention. Trends Parasitol. 2010;26(4):l90-6
7. Hatam G, Shamseddin A, Nikouee F. Seroprevalence of toxoplasmosis in high school girls in Fasa district, Iran. ///.2005;2(3):177
8. Mostafavi SN, Ataei B, Nokhodian Z, Yaran M, Babak A. Seroepidemiology of Toxoplasma gondii infection in Isfahan province, central Iran: A population based study. ./Res Med Sci. 201l;l6(4):496501
9. Sharif M, Daryani A Barzegar G, Nasrolahei M. A seroepidemiological survey for toxoplasmosis among schoolchildren of Sari, Northern Iran. Trop Biomed. 2010;27(2):220-5
10. Assmar M, Amirkhani A Piazak N, Hovanesian A, Kooloobandi A, Etessami R. [Toxoplasmosis in Iran. Results of a seroepidemiological study]. Bull Soc Pathol Exot. 1997;90(1):19-21
11. Hashemi-Fesharki R. Seroprevalence of Toxoplasma gondii in cattle, sheep and goats in Iran. Vet Parasitol. 1996;61(l-2):l-3
12. Bonyadian M, Hematzade F, Manuchehri K. Seroprevalence of antibodies to Toxoplasma gondii in sheep in center of Iran. Pak] Biol Sci. 2007;lO(18):3228-30
13. Sharif M, Gholami Sh, Ziaei H, Daryani A Laktarashi B, Ziapour SP, et al. Seroprevalence of Toxoplasma gondii in cattle, sheep and goats slaughtered for food in Mazandaran province, Iran, during 2005. Vet]. 2007;l74(2):422-4
14. Hajialilo E, Ziaali N, Harandi MF, Saraei M, Hajialilo M. Prevalence of anti-Toxop/asma gondii antibodies in sport horses from Qazvin, Iran. TropAnim Health Prod. 2010;42(7):l321-2
15. Asgari Q.Mehrabani D.Motazedian MH, Kalantari M, Nouroozi J, Adnani Sadati SJ. The viability and infectivity of Toxoplasma gondii tachyzoites in dairy products undergoing food processing. Asian] Animal Sci. 2011;5:202-207
16. Asgari Q, Sarnevesht J, Kalantari M, Sadat SJ, Motazedian MH, Sarkari B. Molecular survey of Toxoplasma infection in sheep and goat from Fars province, Southern Iran. Trop Anim Health Prod. 201l;43(2):389-92
17. Ghorbani M, Hafizi A, Shegerfcar MT, Rezaian M, Nadim A Anwar M, et al. Animal toxoplasmosis in Iran. J Trop Med Hyg. 1983;86(2):73-6
18. Hamidinejat H, Ghorbanpour M, Nabavi L, Haji Hajikolaie MR, Razi Jalali MH. Occurrence of anti-Toxop/asma gondii antibodies in female cattle in south-west of Iran. Trop Anim Health Prod. 2010;42(5):899-903
19. Hoghooghi-Rad N, Afraa M. Prevalence of toxoplasmosis in humans and domestic animals in Ahwaz, capital of Khoozestan Province, south-west IranJTrop Med Hyg. 1993;96(3):l63-8
20. Hosseininejad M, Malmasi A, Hosseini F, Selk-Ghaffari M, Khorrami N, Mohebali M, et al. Seroprevalence of Toxoplasma gondii Infection in Dogs in Tehran, Iran. Iran J Parasitol. 20ll;6(l):8l-5
21. Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Jnt;Parasito/.200030(12-13):l217-58
22. Alvarado-Esquivel C, Estrada-Malacon M, Reyes-Hernandez S, Perez-Ramirez J, Trujillo-Lopez J, Villena I, et al. High Prevalence of Toxoplasma gondii Antibodies in Domestic Pigs in Oaxaca State, MexicoJ Parasitol. 2012
23. Alvarado-Esquivel C, Estrada-Malacon MA Reyes-Hernandez SO, Perez-Ramirez JA Trujillo-Lopez JI, Villena I, et al. Seroprevalence of Toxoplasma Gondii in Domestic Sheep in Oaxaca State, Mexico. 7 Parasi toi. 2012
24. Garcia-Bocanegra I, Cabezon O, Arenas-Montes A Carbonero A Dubey JP, Perea A et al. Seroprevalence of Toxoplasma gondii in equids from Southern Spain. Parasitol M.2012;61(3):421-4
25. Asgari Q, Motazedian MH, Esmaeelzadeh B, Kalantari M, Hatam GR. The Prevalence of Toxoplasma Infection among Free-Ranging Chickens in Southern Iran Using IFAand Nested-PCR. Iranian ] Parasitol. 2009;4(4):29-36
Qasem Asgari 1, Bahador Sarkari 2,* , Maryam Amerinia 3, Saed Panahi 3, Iraj Mohammadpour 1, Afrooz Sadeghi Sarvestani 1
1 Department of Parasitology and Mycology, Shiraz University of Medical Sciences, Shiraz, IR Iran
2 Center for Basic Researches in Infectious Diseases,, Shiraz University of Medical Sciences, Shiraz, IR Iran
3 Department of Parasitology, School of Veterinary Medicine, Shiraz University, Shiraz, IR Iran
* Conesponding author Bahador Sarkari, Center for Basic Researches in Infectious Diseases, Shiraz University of Medical Sciences, Shiraz, IR Iran.Tel/Fax: +98-7112305291, E-mail: firstname.lastname@example.org.