بررسی سرولوژیک آلودگی به توکسوپلاسما گوندی انسانی در مناطق شمالی و مرکزی ایران

نویسندگان

1 دانشیار انگل شناسی، دانشگاه شهرکرد، ایران

2 دکتری دامپزشکی، دانشگاه شهرکرد، ایران،

3 دانشیار انگل شناسی، دانشگاه علوم پزشکی شهرکرد، ایران

چکیده

  مقدمه: توکسوپلاسما گوندی یک انگل تک یاخته ای مهم مشترک انسان و حیوانات است که می‏تواند انسان و حیوانات را آلوده کند. این عامل بیماری زا در دوران بارداری می‏تواند جنین را از طریق انتقال مادرزادی آلوده کند. هدف از این مطالعه، بررسی آلودگی به توکسوپلاسما در افراد مراجعه کننده به مراکز بهداشتی درمانی در مناطق شمالی و مرکزی ایران است .   مواد و روش ‏‏ ها: نمونه های سرمی از 712 نفر از استان های مازندران، اصفهان و استان چهارمحال و بختیاری برای سنجش IgG ضد توکسوپلاسما گوندی به روش الایزا بررسی شد. شیوع آلودگی به توکسوپلاسما گوندی بر حسب سن و جنس بررسی شد .   نتایج: شیوع IgG ضد توکسوپلاسما گوندی در افراد مورد مطالعه در کل 05/72 درصد بود. در استان های مازندران، اصفهان و چهارمحال و بختیاری، در جمعیت مردان به ترتیب 6/87، 46/41 و 81/61 درصد و در جمعیت زنان به ترتیب 31/89، 61/47 و 44/64 درصد از نظر IgG ضد توکسوپلاسما گوندی سرم مثبت بودند. شیوع سرمی IgG ضد‏توکسوپلاسما گوندی در مناطق شمالی و مرکزی ایران، در زنان بالاتر از مردان بود .   بحث و نتیجه ‏ گیری: مطالعه حاضر شیوع بالای آلودگی به توکسوپلاسما در مناطق شمالی و مرکزی ایران را نشان می‏دهد و شیوع بیشتر آلودگی به توکسوپلاسما در زنان مشاهده شد. تفاوت معنی داری که در میزان آلودگی بین افراد ساکن در مناطق شمالی و مرکزی در ایران یافت شد ( p value < 0.05 ) ، نشان داد که آلودگی به توکسوپلاسما به مکان زندگی وابسته است. تحقیقات عمیق تر در مورد عوامل خطر بالقوه که جمعیت ایرانیان به ویژه زنان را تهدید می کنند، توصیه می شود .  

کلیدواژه‌ها

موضوعات


عنوان مقاله [English]

Serological survey of human Toxoplasma gondii infection in northern and central regions of Iran

نویسندگان [English]

  • Khodadad Pirali-Kheirabadi 1
  • Hossein Tahmasby 2
  • Kurosh Manouchehri-Naeini 3
  • Saeid Masoumi-Ghajari
1 Associate Professor of Parasitology, Shahrekord University, Iran
2 DVM, University of Shahrekord, Iran
3 Associate Professor of Medical Parasitology, Shahrekord University of Medical Sciences, Iran
چکیده [English]

Introduction: Toxoplasma gondii is an important zoonotic protozoan parasite that can infect man and animals. The pathogen can infect the fetus by congenital transmission during pregnancy. The aim of this study was to investigate T. gondii infection in people referred to health care centers in northern and central regions of Iran.
Materials and methods: Serum samples from 712 individuals in Mazandaran, Isfahan and ChaharmahalvaBakhtiari provinces, Iran, were examined for the levels of anti-T. Gondii IgG by ELISA. Prevalence of T. gondii infection in respect of gender and age was analyzed.
Results: The overall anti-T. gondii IgG prevalence in the study population was 72.05%. In Mazandaran, Isfahan and ChaharmahalvaBakhtiari provinces,in male population respectively 87.6, 41.46 and 61.81% and in female population respectively 89.31, 47.61 and 64.44% were sero-positive with anti-T. gondii IgG. Sero-prevalance of anti-T.gondii IgG in the females was higher than in the males in the northern and central regions of Iran.
Discussion and conclusion:The present study demonstrates high prevalence of Toxoplasma infection in northern and central regions of Iran and a higher prevalence of T. gondii infection was observed in females. Significant difference in infection rate between individuals living in northern and central areas in Iran was found (p <0.05), which indicated that T. gondii infection is dependent on living places. Deeper investigations for the potential risk factors that threat the Iranian populations, especially female are recommended.

کلیدواژه‌ها [English]

  • Toxoplasma
  • prevalence
  • risk factor
  • infection

Introduction

Toxoplasma gondii is a protozoan parasite that is considered as the most prevalent parasitic zoonotic disease worldwide (1). The Pathogen can infect virtually all warm-blooded animals and humans. In healthy people, the parasite remains in their body in an inactive state, because their immune system usually keeps the parasite from causing illness. It can become reactivated if the person becomes immunosuppressed, such as patients with AIDS or organ transplantation (1- 3). Up to a third of the world's human population is approximated to carry a T. gondii infection (2- 5). Additionally, up to 14.8% of patients with Acquired Immunodeficiency Syndrome (AIDS) in Southeast Asia were infected with toxoplasmosis of central nervous system (6). Toxoplasmosis during pregnancy may result in congenital infection and manifest as mental illness and blindness in the infant (7, 8). Therefore investigation of Toxoplasma infection and the distribution of the oocysts in the human living environments are considered important about prevention of toxoplasmosis (9).

Sporulated oocysts remain viable and infectious in a warm, humid environment for a number of years, because they can largely resist threats such as heat and cold. In laboratory conditions, sporulated oocysts remained alive up to 54 months at 4°C and for 106 days of freezing at −10°C. It has been also demonstrated that sporulated oocysts survived at least 32 days at 35°C and 9 days at 40°C, while exposure at a temperature of 37°C during a period of 24 h had destructive effects for non-sporulated oocysts (10- 12).

Climatic conditions directly influence the risk of infection in cats. It is demonstrated that prevalence of antibodies against T. gondii is related to the interaction between temperature and rain (13). The infection risk increases when the weather is both warm and humid, or moderated and less humid. Humid conditions can increase oocyst survival during longer periods of heat (13; 14). In the USA, the lowest seroprevalence of T. gondii infection in cats were encountered in the most arid regions (15).

Origins of human T. gondii infection are cats which have intestinal infection and will be shedding oocysts in feces that may be ingested by humans by consumption of uncooked fruit, berries, or vegetables (16) or tissue cysts from infected meat animals (17- 19).

Although experimental results of many studies have indicated a positive correlation between Enzyme-Linked Immunosorbent Assay (ELISA) and Immuno-Fluorescent Antibody (IFA) test for detection of IgG antibodies to T. gondii, ELISA can be used as a qualitative test to screen more samples in a given time (20, 21).

The epidemiological studies in Iran like other countries have been done, but the prevalence of T. gondii in Mazandaran and ChaharmahalvaBakhtiari in recent years is not clear. Hence, in this study, we investigated the prevalence of anti-T. gondii IgG in the sera of more than 700 Iranian individuals referred to health care centers in the northern and central regions of Iran by ELISA method.

 

Materials and Methods

Study populations and Serum samples

 

712 serum samples were collected from health care centers in Mazandaran (north), Isfahan and ChaharmahalvaBakhtiari provinces (center) from May 2009 to October 2010 (Table 1). The age of the studied population spanned from 8 to 84 years of age. The study was carried out with permission from the Research Institute of Zoonotic Diseases of Shahrekord, Shahrekord University, Iran.

 

 

 

Serological assay

 

Sera were kept frozen at -20°C and sent to the Research Institute of Zoonotic Diseases (university of Shahrekord, Iran) to be tested for Toxoplasma-specific IgG using ELISA (Dia.pro; Milano, Italy). The procedure was performed according to the manufacturer’s instructions.

 

Statistical Analysis

 

SPSS 16.0 software package was used to analyze the anti-T. gondii Ig Gseroprevalence in respect of gender, age and residence of the populations. Logistic regression analysis was used to assess the association with gender, age and residence of the subjects and T. gondii infection in populations. Adjusted odds ratio (OR) and 95% confidence interval (CI) were calculated by multivariate analysis using logistic regression.

 

Results

 

The overall prevalence of anti-T.gondii IgG in the studied population was 72.05% (Table 1). The general seroprevalence of individuals living in Mazandaran, Isfahan and ChaharmahalvaBakhtiari provinces were 88.73, 46.1, and 63.68% respectively.

 

 

Table 1- Number of serum samples from study regions, gender distribution and seroprevalence

Total

ChaharmahalvaBakhtiari

Isfahan

Mazandaran

Gender

71.91 (356/495)

64.44 (87/135)

47.61 (60/126)

89.31 (209/234)

Female

72.35 (157/217)

61.81 (34/55)

41.46 (17/41)

87.6 (106/121)

Male

72.05 (513/712)

63.68 (121/190)

46.1 (77/167)

88.73 (315/355)

Total

 

 

Sera which had anti-T.gondii antibodies were divided into 5 groups based on the age (<20, 20-29, 30-39, 40-49 and >50 years) of the individuals. The seroprevalence of the five age groups were 55, 66.17, 84.7, 79.62 and 70.76% respectively in the clinically healthy population (Fig. 1). Furthermore, the difference of T. gondii infection rate between male and female in less than 20 years old was more obvious, with 46.42% in male population and 58.33% in female population.

Discussion and Conclusion

 

During a national-wide survey carried out in previous years (22), the prevalence of T. gondii infection in general population of Iran was reported to be around 51.8%. In the current study, we investigated more than 700 individuals living in northern and central regions of Iran. The overall infection rate of T. gondii in the studied population was 72.05%, which was more than previous studies (22).

 

 

 

Fig1-Seroprevalence of T. gondii antibody in different age groups in Mazandaran, Isfahan and ChaharmahalvaBakhtiari provinces

 

Like findings in previous studies in Mazandaran province (north), 72.5% prevalence in schizophrenia patients referred to Psychiatric Hospital (23), 63.9% prevalence in matrimonial women (24), 77.4% prevalence in rehabilation centers )25) and 78.7% prevalence in butchers (26), our study proved high frequency of T. gondii infection in Mazandaran. But the results of the present study showed a higher prevalence of Toxoplasma infection (88.73%) in Mazandaran province.

The results which we obtained in our investigation showed that Isfahan province had a lower prevalence (46.1%) than both Mazandaran (88.73%) and ChaharmahalvaBakhtiari (63.68%) provinces. Mostafavi et al study result (2012) was somewhat similar to our study. Although they reported a 47.5% positive rate in women of childbearing age from Isfahan (27), Mahmodi et al., reported 18.4% among high-school girls in Isfahan (28).

In comparison with previous studies, our study showed an increase in infection rate in the people of ChaharmahalvaBakhtiari province (63.68%). Manouchehri-Naeini et al reported 27.4% prevalence in rural pregnant woman from ChaharmahalvaBakhtiari (29) and 27.6% prevalence in pregnant woman from ChaharmahalvaBakhtiari (30).

Some studies indicated high prevalence of infection among intermediate and definitive hosts as potential sources of Toxoplasma infection in different parts of Iran (31, 32).

Our research suggests increasing prevalence of T. gondii infection rate in northern and central regions of Iran. The high prevalence in humans found here could be due to having pet animals and changes in consumption habits, consuming raw or undercooked meat in northern and central regions of Iran. So consumption of perfectly cooked meat, safe handling, and appropriate disposal of faecal material from pet cats are important to avoid Toxoplasma infection.

Environmental conditions are important for survival of the resistant stage of the parasite (oocysts). T. gondii is more prevalent in humid tropical areas and less prevalent in hot and dry areas. Additionally, prevalence of the T. gondii in arctic areas is low (1). Change of climate causes increasing temperatures, drier summers, and more humidity during the winter. Because mean winter temperature is rising, the parasite survival is likely to increase. This can have consequences for prevalence of T. gondii in intermediate and final hosts. The infection risk increases when the weather is both warm and humid, or moderated and less humid (33).

Significant difference (p<0.05) in infection rate between individuals living in northern and central areas in Iran was found (fig. 1), which indicated that T. gondii infection is dependent on living places. In Mazandaran province (north) environmental conditions are more humid than Isfahan and ChahamahalvaBakhtiari (center) provinces (34) and prevalence of Toxoplasma was higher in Mazandaran.

The finding that seroprevalance of anti-T.gondii IgG in the females is higher than in the males in the northern and central regions of Iranian population, indicates that females are at higher risk of contracting T. gondii infection. This may be due to many factors, such as spending more time to their pets including cats, having contact with raw or undercooked meat more often than men.

This study showed that infection rate of T. gondii in the studied population was higher than what was recorded by previous studies, and importantly, results suggest that women have a higher risk of being infected by T. gondii than men in northern and central regions of Iran. Since T. gondii reactivation may occur during gestation, it poses threat to the life of fetuses and newborns. Thus knowledge of disease prevention is more important to females. These results emphasize for more attention in prevention of T. gondii infection in the female population and in particular pregnant women. Significant difference (p<0.05) in infection rate between individuals living in northern and central areas in Iran was found, which indicated that T. gondii infection is dependent on living places.

 

Acknowledgement

This study was carried out with research institute of zoonotic diseases supports, Shahrekord University, Iran.

 

Reference

(1)  TenterAM, Heckeroth AR, Weiss LM. Toxoplasmagondii: from animals to humans. Int J Parasitol 2000; 30: 1217- 58.

(2)  Montoya JG, Liesenfeld O. Toxoplasmosis. Lancet 2004; 363(9425):1965- 76.

(3)  Dubey JP, Jones JL. Toxoplasmagondii infection in humans and animals in the United States. Int J Parasitol 2008; 38(11): 1257–78

(4)  Alvarado-Esquivel C, Torres-Castorena A, Liesenfeld O, García-López C, Estrada-Martínez S, Sifuentes-Álvarez A, et al. Seroepidemiology of Toxoplasma gondii infection in pregnant women in rural Durango, Mexico. J Parasitol 2009; 95(2): 271- 74.

(5)  Liu Q, Wei F, Gao S, Jiang L, Lian H, Yuan B, et al. Toxoplasma gondii infection in pregnant women in China. Trans R Soc Trop Med Hyg 2009; 103(2): 162- 66.

(6)  Nissapatorn V. Lessons learned about opportunistic infections in Southeast Asia. Southeast Asian J Trop Med Publ Health 2008; 39(4)625- 41.

(7)  Elsheikha EM. Congenital toxoplasmosis: Priorities for further health promotion action. PublHealth 2008; 122(4): 335- 53.

(8)  Kravetz JD, Federman DG. Toxoplasmosis in pregnancy. Am J Med 2005; 118(3): 212- 16.

(9)  Xiao Y, Yin J, Jiang N, Xiang M, Hao L, Lu H, et al. Seroepidemiology of human Toxoplasma gondii infection in China. BMC Infect Dis 2010; 7(10): 4.

(10) Dubey JP, Beattie CP. Toxoplasmosis of Animals and Man. USA: CRC Press; 1988; 40.

(11)   Dubey JP. Toxoplasma gondii oocyst survival under defined temperatures. J Parasitol 1988; 84(4): 862- 65

(12)    Dubey JP, Miller NL, Frenkel JK. The Toxoplasma gondii oocyst from cat feces. J Exp Med 1970; 132(4): 636- 62

(13)   Afonso E, Thulliez P, Gilot-Fromont E. Transmission of Toxoplasma gondii in an urban population of domestic cats (Feliscatus). Int J Parasitol 2006; 36(13): 1373- 82

(14)  Frenkel JK, Ruiz A, Chinchilla M. Soil survival of Toxoplasma oocysts in Kansas and Costa Rica. Am J Trop Med Hyg 1975; 24 (3): 439- 43

(15)  Vollaire MR, Radecki SV, Lappin MR. Seroprevalence of Toxoplasma gondii antibodies in clinically ill cats in the United States. Am J Vet Res 2005; 66(5): 874- 77

(16)  Kapperud G, Jenum PA, Stray-Pedersen B, Melby KK, Eskild A, Eng J. Risk factors for Toxoplasma gondii infection in pregnancy: results of a prospective case–control study in Norway. ObstetGynecolSurv 1997; 52(3): 158-59

(17)  Meerburg BG, Riel JWV, Cornelissen JB, Kijlstra A, Mul MF. Cats and goat whey associated with Toxoplasma gondii infection in pigs. Vector Borne Zoonotic Dis 2006; 6(3): 266- 74

(18) Kijlstra A, Jongert E. Control of the risk of human toxoplasmosis transmitted by meat. Int JParasitol 2008; 38(12): 1359- 70

(19)  Kijlstra A, Jongert E. Toxoplasma-safe meat: close to reality? Trends Parasitol. 2009; 25(1): 18- 22

(20)Mehrabani D, Malekpour A, Zahedi S, Dehghani S, Tondro G. Comparison of Dot-ELISA with IFA test for diagnosis of human toxoplasmosis and Seroepidemiological evaluation of the disease. Middle-East J Sci Res 2012; 11 (11): 1530- 35.

(21) NourollahiFard SR, Shad-Del F, Hosseini SMH, RazaviDinani SM. Standardization and comparison of Dot-ELISA with IFA test for diagnosis of human toxoplasmosis. Iran J Vet Res 2004; 5(2 (10)): 91- 96.

(22) Assmar M, Amirkhani A, Piazak N, Hovanesian A, Kooloobandi A, Etessami R. Toxoplasmosis in Iran, results of a seroepidemiological study. Bull SocPatholExot 1997; 90(1): 19- 21.

(23)  Daryani A, Sharif M, Hosseini SH, Karimi SA, Gholami S. Serological survey of Toxoplasma gondii in schizophrenia patients referred to Psychiatric Hospital, Sari City, Iran. Trop Biomed 2010; 27(3): 476- 82

(24) Youssefi MR, Sefidgar AA, Mostafazadeh A, MahdaviOmran S. Serologic Evaluation of toxoplasmosis in matrimonial women in Babol by Elisa, first semester 2004. Pakistan J BiolSci‎ 2007; 10(9): 1550- 52

(25) Ajami A, Sharifi M, Ziaee H. Serological study of toxoplasmosis in Mazandaran rehabilation centers. J MazandaranUniv Med Sci 2005; 15(46): 64- 9.

(26) Sharifi M, Ajami A, Haghpanah B. Seroprevalence of Toxoplasma gondii and effective agents of its in butchers in Sari. J GilanUniv Med Sci 1999; 8(31): 42-6.

(27)Mostafavi N, Ataei B, Nokhodian Z, Monfared LJ, Yaran M, Ataie M, et al. Toxoplasma gondii infection in women of childbearing age of Isfahan, Iran: A population-based study. Adv Biomed Res 2012;1:60. doi: 10.4103/2277-9175.100181.

(28) Mahmodi M, Mohebali M, Hejazi H, Keshavarz H, AlaviNaeini AM, Izadi S. Seroepidemiological study on toxoplasmic infection among high-school girls by IFA test in Isfahan City Iran. J SchPubl Health InstPubl Health Res 2004; 3(1):29-42.

(29) Manouchehri-Naeini K, Deris F, Zebardast N. The immunity status of the rural pregnant women in Chaharmahal and Bakhtyari province against Toxoplasma infection 2001–2002. J Shahrekord Med Sci 2004; 6(3):63–72.

(30)  Manouchehri-Naeini K, Keshavarz H, Abdizadeh-Dehkordi R, Zebardast N, Kheiri S, Khalafian P, et al. Seroprevalence of anti-Toxoplasma antibodies among pregnant women from Chaharmahal and Bakhtyari province using indirect immunoflurescent in 2006-2007. J Shahrekord Med Sci 2007; 8(4):74- 80.

(31) Ghorbani M, Gharavi MJ, Kahnamoui A. Serological and parasitological investigations on Toxoplasma infection in domestic fowls in Iran. Iranian J Publ Health 1990; 19(1–4):9- 17.

(32)Hoghooghi-Rad N, Afraa M. Prevalence of toxoplasmosis in humans and domestic animals in Ahwaz, capital of Khoozestan province, south-west Iran. J Trop Med Hyg 1993; 96(3):163- 68.

(33) Meerburg BG, Kijlstra A. Changing climate-changing pathogens: Toxoplasma gondii in North-Western Europe. Parasitol Res 2009;105(1):17- 24.

(34) Statistical Center of Iran. Available at: http://salnameh.sci.org.ir/.