Abstract
Toxoplasmosis is a zoonotic infection of humans and animals, caused by the opportunistic protozoan Toxoplasma gondii, a parasite belonging to the phylum Apicomplexa. Infection in pregnant women may lead to abortion, stillbirth or other serious consequences in newborns. Infection in immunocompromised patients can be fatal if not treated. On average, one third of people are chronically infected worldwide. Although very limited information from China has been published in the English journals, T. gondii infection is actually a significant human health problem in China. In the present article, we reviewed the clinical features, transmission, prevalence of T. gondii infection in humans in China, and summarized genetic characterizations of reported T. gondii isolates. Educating the public about the risks associated with unhealthy food and life style habits, tracking serological examinations to special populations, and measures to strengthen food and occupational safety are discussed.
Similar content being viewed by others
Background
Toxoplasmosis, a cosmopolitan disease in humans and most mammals, is caused by the opportunistic protozoan Toxoplasma gondii mainly through peroral infections, bloodstream infections and congenital acquired infections. It has been estimated that one third of the world population has been infected [1, 2]. In most adults it does not cause serious illness, however, blindness and mental retardation can be caused in congenitally infected children and severe diseases in those with compromised immunity. A recent study indicated that infection with T. gondii is associated with abdominal hernia [3].
Toxoplasma gondii needs both definitive hosts and intermediate hosts to complete its sexual and the asexual replication phases in life cycle. The sexual phase only occurs in the intestine of the definitive hosts, felids. All the warm-blooded animals, the intermediate hosts, become infected mainly by consuming food or drink contaminated by oocysts evacuated from felids and tissue cysts from other intermediate hosts [4]. Acute infection happens in the initial few days, with the rapidly growing replication of the tachyzoites. Tachyzoites switch to bradyzoites as time goes by and form tissue cysts parasitizing in host cells. It would be lethal in Toxoplasma infected immune-compromised patients if bradyzoites revert to tachyzoites. In addition to felids, intermediate hosts carried with tachyzoites or tissue cysts are also responsible for the spread of T. gondii. Peroral infection, congenital and blood infection are three major ways for the transmission of this parasite [5].
The first human case of toxoplasmosis in China was report in 1964 in Jiangxi Province [6]. Many human cases were reported in China since the first epidemic survey on toxoplasmosis was carried out in Guangxi Province in 1978 [7]. However, toxoplasmosis cases in China are hardly recognized by western clinicians, for very little information from China was published in English. The rising prevalence of T. gondii infection and the increasing clinical cases [8–10] in immunocompromised patients, and patients with congenital toxoplasmosis and psychosis should draw our attention to address toxoplasmosis as a serious public health problem. It is thus timely and appropriate to review the Chinese literature on Toxoplasma and toxoplasmosis to gain an improved insight into its epidemiology and socioeconomic impact in China. Most of the data quoted in this review were derived from articles published in Chinese on T. gondii infection in humans up to 2011, obtained from The China National Knowledge Infrastructure (CNKI) database via its website http://www.cnki.net, using the keywords "Toxoplasma", "Toxoplasmosis" and "Epidemiology". We intend to provide clinical information, to summarize some key aspects regarding transmission and prevalence of human toxoplasmosis, and genetic characterizations of T. gondii strains in China, and to conclude by making some suggestions for further research and recommendations for the prevention and control of this important human protozoan disease.
Epidemiology
Between 2001 and 2004, the national serological survey of 47,444 people in 15 provinces and autonomous regions estimated a mean prevalence of 7.9% by using enzyme-linked immunosorbent assay (ELISA) [11]. Prevalence in these provinces has increased from 5.2% in the first national survey conducted between 1988 and 1992 [12]. Though a recent serological survey carried out in 3281 individuals from the northeast and the south of China showed a 12.3% anti-T. gondii IgG positive rate, which indicated the increasing growth in prevalence [13], the prevalence of T. gondii in China was still relatively low, comparing with 50-75% seropositive in France, and 20% in UK [14].
Guizhou province and Guangxi province had the highest levels with prevalence of 15.1% and 12.7%, respectively [15]. Prevalence in Miao (25.4%), Buyi (25.3%), Mongol (17.1%) and Zhuang (16.7%) ethnic groups are higher than in other groups of the population [15]. Eating habits play an important role in the parasite infection. People living in southwest of China enjoy eating raw or half-raw meat or animal internal organs in their tradition, such as the 'Sour-meat' (let raw pork or beef ferment and become sour), the 'Shengpi' (is a cooking method which keeps pork and beef half-raw), and even raw pig or cattle liver [16, 17]. The Mongol people like to eat their traditional food 'Mongolian Finger Mutton' by hands after contact with animals or raw meat without appropriate washing procedures, because of the water shortage in their living areas, which could lead to Toxoplasma infection, in addition to other food-borne diseases such as taeniasis, cysticercosis, trichinelliasis and echinococcosis [15].
Human toxoplasmosis in mainland China
Immunocompromised patients with toxoplasmosis
Toxoplasmosis can be life-threatening in immunocompromised patients as a result of reactivation of chronic infection. High seroprevalence of latent T. gondii infection has been found among immunocompromised patients. Prevalence of T. gondii infection in cancer patients ranged from 24% [18] to 79% [19]. Prevalence of T. gondii infection varied with different cancers. Rectal cancer and nasopharyngeal carcinoma sufferers in Changchun city had the highest infection, with prevalence of 63.6% and 46.2%, respectively [18]. However, T. gondii infections in patients with breast cancer, hepatocellular carcinoma and gastric carcinoma in Henan Province were much higher than with other cancers, with a prevalence of 78.9%, 77.8% and 61.1%, respectively [19]. The average prevalence of T. gondii infection was 15.1% in leukemia patients. Moreover, T. gondii prevalence in refractory cases of leukemia patients was up to 35% [20].
Surveys of T. gondii infection in the individuals with tuberculosis and hepatitis B showed that the prevalence were 35.3% [21] and 19.3% [22], respectively. Most of the cases belonged to chronic infections. 70% of individuals infected with T. gondii and tuberculosis had the experience of intimate contact with animals [21]. Similarly, high prevalence of T. gondii infection have been detected among immunocompromised patients especially suffering from malignancy in Egypt and Korea [23, 24]. Although there is no direct association between the susceptibility of toxoplasmosis and the immunocompromised state, the high seroprevalence in immunocompromised patients indicates considerable risks, because toxoplasmosis is a consequence of recrudescence of a previously latent infection in most immunocompromised patients, with the chronic parasite infection activation after the immune system was damaged [25].
The first case of AIDS patient died in China was reported in 1991, and T. gondii was found in the cerebellum of this patient [26]. In a more recent report, 26% of HIV infected patients in Xinjiang were seropositive with T. gondii infection [27].
The CNS is the site most typically affected by T. gondii infection. A series of clinical manifestations including mental status changes, seizures, focal motor deficits, cranial nerve disturbances, sensory abnormalities, cerebellar signs, movement disorders, and neuropsychiatric findings have often been found among toxoplasmic encephalitis (TE) cases. The incidence of TE was from 0.6% [28] to 10.5% [9] among the HIV infected patients in Henan and Yunnan Provinces, with all the CD4+ T-lymphocyte count below 100 cells per microliter. Toxoplasmic lymphadenitis and retinitis were also found in HIV-infected patients, with the incidence of 6% (2/33) [29] and 5.3% (2/38) [9], respectively.
Congenital toxoplasmosis
Congenital infection caused by transplacental transmission can lead to a wide variety of manifestations in the fetus and infant including spontaneous abortion, still-birth, a newborn with classic signs of congenial toxoplasmosis such as hydrocephalus or microcephalus, cerebral calcifications and retinochoroiditis [30, 31]. There were no national reports about congenital toxoplasmosis on newborns in China. Previous studies focused on certain areas with severe cases. The seroprevalence of T. gondii in newborns was between 4.4% to 19.4% in Huizhou city, Shantou city and Dalian city [32–34]. A survey of T. gondii infection in 80 puerperas and their new-born babies showed that the seroprevalence were 8.8% and 6.3%, respectively. The vertical transmission was 70% by using ELISA, which was still serious in Xinxiang city of Henan Province [35].
Most infected newborns have no apparent physical abnormalities at birth, but without treatment, most of them may later develop chorioretinitis, neurologic damage or growth can be delayed later in life. The seroprevalence of T. gondii infection in disabled children with symptoms of hypophrenia, epilepsy, retinochoroiditis, cardiovascular defects and respiratory system defects were 21.7%, 20%, 26.1%, 25% and 14.3%, respectively [36]. A case-control study in Hainan Province, involving 79 cases of infantile cerebral palsy, revealed that the seroprevalence of T. gondii was 41.8%, with significant difference (P < 0.001) from the 256 control cases with seroprevalence of 8.6% [37]. A survey of 592 congenital defect infants in Nanjing city, Jiangsu province revealed a 28.13% seroprevalence of T. gondii infection, which was significantly higher compared with the normal ones (0.6%) [10].
Ocular toxoplasmosis
Ocular toxoplasmosis (OT) may induce more than 30% posterior uveitis cases in western populations [38]. Even though both congenital and acquired infection may develop ocular lesions, it has been suggested that 70% of chorioretinal scar formation is of congenital origin [39]. Congenital ocular toxoplasmosis mainly causes congenital malformation, with anophthalmus, congenital aniridia, chorioretinal, congenital cataract, optic neuritis, strabismus, amblyopia, nystagmus, optic atrophy, visual field defects, etc. Ocular lesions originated from acquired infections occur after birth, which resulted in tissue destruction and inflammatory responses [40]. The first case of OT reported in China also was found in the first human toxoplasmosis case in Jiangxi Province in 1964 [6]. The incidence of OT in China is still unclear. The seroprevalence of OT in ophthalmocace patients was up to 38.8% [41]. Central exudative chorioretinitis and uveitis are the most common symptoms in OT cases reported in China [42, 43].
Toxoplasmosis and schizophrenia
Evidence is mounting to link toxoplasmosis with schizophrenia or similar psychiatric disorders. Recent studies revealed that levels of antibodies to T. gondii have been found to be increased in individuals with schizophrenia compared to controls with an odds ratio for Toxoplasma seropositivity between 2 and 4.4 [44–47]. In prospective studies, an increase in IgG antibodies to T. gondii has been found in mothers of infants who later develop schizophrenia [48].
Many reports revealed that Toxoplasma might represent a major pathogen in some cases of psychosis. It has been proven that the parasite infection could increase the dopamine level in mice brains [49]. Dopamine plays a key role in psychosis cases such as schizophrenia, and bipolar disorder [50–52]. The seroprevalence of T. gondii infection in schizophrenic patients ranged from 1% to 28.7% in China [11, 53]. A report of 67 cases of childhood schizophrenia between 6~17 years old revealed a Toxoplasma-IgG positive rate of 85.7% [54]. Another survey on Toxoplasma infection in 600 cases of the first episode of schizophrenia revealed that the Toxoplasma-IgG positive rate was 13.7% [55]. The prevalence of Toxoplasma IgG in mothers of 252 was 34.8% [55]. The alterations of behavior and psychomotor skills in schizophrenia patients have also been found to be associated with the T. gondii infection [56]. Compared with the seronegative ones, clinical manifestations of excitation, hostility, mannerisms and posturing, disturbance of volition, poor impulse control and anger, difficult to delay fulfilling request and suspiciousness in the seropositive patients were statistically different [56]. The schizophrenic patients living in rural area have a higher infection rate than these lived in cities, with prevalence of 28.6% and 6%, respectively [57].
Poor obstetric outcomes, sterility and toxoplasmosis
There is as yet no direct evidence showing the association between toxoplasmosis and sterility in women. Nevertheless, some studies have demonstrated that T. gondii infection could cause reproductive failure in mice, which was due to an acquired hypogonadotropic hypogonadism secondary to hypothalamic dysfunction, exhibiting histopathological changes with estrus cycling cessation, impaired folliculogenesis and few corpora lutea [58, 59]. It seems that T. gondii infection in pregnant women may cause poor obstetric outcomes such as spontaneous abortion, hydatidiform mole, still-born, teras and sterility. Women who had a poor obstetric outcome history had a seroprevalence of 14.2% [60] to 33.9% [61] which was much higher than that of the normal pregnancy in China. A survey of T. gondii infection in 68 cases of oviducal sterility revealed a prevalence of 44.1%, which was significantly different from that in normal pregnant women (3.3%) [62], indicating that Toxoplasma infection could result in oviducal sterility.
T. gondii infection is also found to be related with the male sterility. Recent zoopery studies revealed that the reproductive parameters including sperm motility and sperm concentration were significantly decreased in T. gondii infected rats, and a marked increase in sperm abnormalities was also found in these infected male rats [63]. Similar results were also observed in male mice experimentally infected with T. gondii [64]. Zhou (2002) [65] found that Toxoplasma infection in infertile human couples was higher than that in fertile couples, possibly related to the antisperm antibodies which were higher in Toxoplasma-infected couples. A recent investigation of T. gondii infection in 100 men with sterility revealed that 16% of them were IgM-positive and 13% were CAg-positive, significantly higher than in healthy men [66]. The seroprevalence of Toxoplasma infection in male sterility cases were 19.8% in Luoyang, Henan province [67], to 22.8% in Yan'an, Shaanxi province [68], significantly higher than in the healthy men. Based on a number of relevant studies and investigations in China, it is concluded that T. gondii infection may result in male sterility [69].
Transmission of toxoplasmosis
Transmission by contact with animals
Some occupations required people to have contact with animals and meats and these frequently possess higher risk of infection with the parasite, such as dairy workers, slaughterhouse workers, veterinarians, meat-processing workers, meat sellers and cooks. Selected serological surveys of T. gondii infection in different occupations in China are summarized in Table 1.
These data suggest that the oral route is the major route of infection. Pork is one of the most popular meats in China. Seroprevalence of T. gondii in pigs is high in some Chinese provinces, for instance 16.9% in Yunan province [76], 27% in Guangdong province [77] and 53.4% in Zhejiang province [78], which are higher than that in USA (2.7%, [79]), Germany (4.1%, [80]) and Mexico (12.7%, [81]). There is still no meat inspection for T. gondii contamination in meat before it is sold for human consumption, nor any strict performance standards for processing meat and animal products, which gives a high risk of infection for these workers. Similar high prevalences of T. gondii infection have also been found in butchers in Finland [82], Egypt [83] and Brazil [84]. A latest Mexican report proposed that occupational exposure to raw meat has no correlationship with seropositivity of T. gondii infection [85]. The reason may be associated with good sanitary conditions in the slaughterhouses and powerful protective facilities to the workers. However, in our investigations of T. gondii infection in slaughter pigs in several provinces in China, we found that butchers do not always wear gloves during work because of the hot and humid environment around the slaughterhouses, which may increase the risk for T. gondii infection when handling raw meat.
Herdsmen possessed a higher T. gondii prevalence in the west China, such as Xinjiang and Inner Mongolia due to inadequate sanitary conditions and the traditional eating habits mentioned above, with seroprevalence ranged from 6.7% [86] to 18.5% [87]. People owning dogs and cats as pets also processed a high risk of infection, with the prevalence ranged from 5.3% [88] to 34.8% [74].
Transmission by blood transfusion
T. gondii can also be transmitted via blood or leucocytes from infected donors [89]. The seroprevalence of T. gondii in blood donors in China varied between 0.4% [90] to 20.2% [91], which were lower than in Egypt (59.6%) [92] and Malaysia (28.1%) [93]. Peasant blood donors had the highest seroprevalence (28.6%), which may be related to the living habits and chances of contacting with animals [91]. Therefore, it is very urgent for a hospital to check all the blood from blood donors. It would be lethal to transmit the parasite from immunocompetent donors to immunocompromised recipients during surgery.
Another pattern of T. gondii transmission by blood is though needles among intravenous drug users (IVDU). The prevalence of T. gondii in IVDU ranged from 17.3% [94] to 21.8% [95], which were significantly higher (P < 0.01) than the prevalence (7.8%) in those who took drugs by the non-intravenous route [95]. Drug addiction history and HIV infection was associated with the susceptibility of Toxoplasma in IVDU. IVDU with 5 years or more addiction history possessed higher seroprevalence compared with those less than 5 years, with seropositivity of 21.8% and 8%, respectively [94]. Toxoplasma prevalence in drug users with HIV was significantly higher than in those with no HIV infection, being 35.8% (29/81) and 5%, respectively [94].
Congenital transmission
When a woman ingests oocysts or cysts of T. gondii for the first time during gestation [2], tachyzoites are disseminated through the body by blood. The fetus becomes infected by the entry of T. gondii to the fetal circulation though the placenta. Maternal acquisition of T. gondii before pregnancy poses a rare risk to the fetus except the infection in immunocompromised women [96]. The risk of congenital infection increases during pregnancy. The acquisition within the first pregnancy trimester has the lowest risk (10-15%) of congenital infection, whereas risks of transmission are much higher during the third trimester [2]. Fortunately, the later in pregnancy that congenital infection occurs, the less severe the consequence is to the fetus.
Since more than 90% of chronic toxoplasmosis infections are asymptomatic, primary prevention is the best way to lower the risk of congenital infection. The detection and treatment of T. gondii in infected pregnant women would be an efficient way of attempting to reduce congenital transmission. In China, surveys of Toxoplasma infection in women were often been carried out before or at the third month of pregnancy. Selected serological surveys in women during pregnancy in different areas in China during 1994 to 2008 are summarized in Table 2. The prevalence of T. gondii infection in pregnant women ranged from 0.5% [106] to 25.5% [104] in China, which were lower than those reported in Austra (35%) [113], France (43.8%) [114] and Brazil (53.0%) [115]. The cultural behaviors and living conditions play an important part for the parasite infection in pregnant women. Those pregnant women who had a history of contact with animals and had habits of consuming undercooked meat or some other raw foods such as un-pasteurized milk or raw eggs, possessed a higher risk for infection.
Genetic characterization of T. gondii strains
The information on genetic characterization of T. gondii strains prevailing in China is limited even though there have been many reports of seroprevalence of T. gondii infection in humans and animals published locally in the Chinese language. But, only a small percentage of exposed humans or animals develop clinical toxoplasmosis, which increases the difficulty for parasite isolation. Based on 10 PCR-RFLP markers, the genetic variability of T. gondii isolates from China has been revealed gradually. A total of 5 genotypes were identified, indicating limited diversity of the parasite in China, which is in sharp contrast to South America where a variety of parasite lineages are transmitted in the environment [116]. Clonal Type I lineages were identified from human patients and pigs in China. The unique genotype in cats in Guangzhou city [117], has also been identified from human patients and pigs [116]. It is the major lineage prevalent in Mainland China, which has also been identified from Colombia, Sri-Lanka, Vietnam, and the USA, indicating that it is widespread in Asia, and South and North America [118].
Conclusion
Suggested control strategies and measures
The control of human toxoplasmosis is dependent on the reduction or elimination of the transmission of the parasite. However, the effective control of toxoplasmosis is still a difficult task in China. As the oral route is the major method of infection, efforts should be undertaken to guarantee the successful implementation of food safety regulations and regulatory control procedures. The Hazard Analysis and Critical Control Points (HACCP) principles [119], recommended by the Food and Agriculture Organization and WHO to be applied to control food-borne parasite infections in humans, should be evaluated by relevant Chinese authorities by relating to the actual conditions in China. Promoting educational programs directed at reducing environmental contamination with T. gondii would eventually reduce the cost of treating humans for clinical toxoplasmosis. There should also be educational programs to guide people to change their habit of consuming uncooked meat and unboiled water, for oocysts can survive for up to 3 years and be transmitted by water through direct drinking [120]. Rules for inspecting meat for T. gondii contamination before being sold should be set up and supported by governments.
Detection of antibodies is very important for pregnant women and women of child-bearing age. This is an effective way to find the infection, and then to provide treatment. It is also an efficient way to stop congenital toxoplasmosis in newborns. Good animal husbandry practice and animal welfare should be set up and popularized for food-producing animals, which may also decrease the risk of human infection. If such strategies and measures can be implemented, it should be possible to effectively control, or at least substantially reduce, the prevalence and intensity of human and animal infections with T. gondii in China.
References
Tenter AM, Heckeroth AR, Weiss LM: Toxoplasma gondii: from animals to humans. Int J Parasitol. 2000, 30: 1217-1258. 10.1016/S0020-7519(00)00124-7.
Dubey JP, Jones JL: Toxoplasma gondii infection in humans and animals in the United States. Int J Parasitol. 2008, 38: 1257-1278. 10.1016/j.ijpara.2008.03.007.
Alvarado-Esquivel C, Estrada-Martínez S: Toxoplasma gondii infection and abdominal hernia: evidence of a new association. Parasit Vectors. 2011, 4: 112-10.1186/1756-3305-4-112.
Montoya JG, Liesenfeld O: Toxoplasmosis. Lancet. 2004, 363: 1965-1976. 10.1016/S0140-6736(04)16412-X.
Dubey JP: Toxoplasmosis of Animals and Humans. 2010, CRC Press, Second
Xie TH: A case report of human toxoplasmosis. Jiangxi Med J. 1964, 4: 121-212. (in Chinese)
Chen XG, Wu K, Lun ZR: Toxoplasmosis researches in China. Chin Med J. 2005, 118: 1015-1521.
Quan HY: Clinical analysis of 38 AIDS cases. Contemporary Med. 2006, 11: 85-86. (in Chinese)
Xia W, Zhang XJ, Chen XW: Investigation of different pregnant results of pregnant women infected with Toxoplasma gondii in Nanjing city. Chin J Schisto Control. 2011, 23: 183-186. (in Chinese)
Li JM, Chang XR, Ge QL: Investigation on infection of Toxoplasma gondii in 604 cases with mental diseases. Chin J Parasit Dis Con. 2002, 15: 150-(in Chinese)
Zhou P, Chen N, Zhang RL, Lin RQ, Zhu XQ: Food-borne parasitic zoonoses in China: perspective for control. Trends Parasitol. 2008, 24: 190-196. 10.1016/j.pt.2008.01.001.
Yu SH, Xu LQ, Jiang ZX, Xu SH, Han JJ, Zhu YG, Chang J, Lin JX, Xu FN: Report on the first national wide survey of the distribution of human parasites in China I: Regional distribution of parasite species. Chin J Parasitol Parasit Dis. 1994, 12: 241-247. (in Chinese)
Xiao Y, Yin JG, Jiang N, Xiang M, Hao LL, Lu HJ, Sang H, Liu XY, Xu HJ, Ankarklev J, Lindh J, Chen QJ: Seroepidemiology of human Toxoplasma gondii infection in China. BMC Infect Dis. 2010, 10: 4-10.1186/1471-2334-10-4.
Darrel OHY: Toxoplasmosis. Medicine. 2009, 37: 665-667. 10.1016/j.mpmed.2009.09.006.
Xu LQ, Chen YD, Sun FH, Cai L, Fang YY, Wang LP, Liu X, Li LS, Feng Y, Li H: A national survey on current status of the important parasitic diseases and control strategies. Chin J Parasitol Parasit Dis. 2005, 23: 332-340. (in Chinese)
Dong Y, Zhang ZX: A review of human parasitic disease prevalence in Yunan Province, China. J Pathogen Biol. 2009, 4: 626-632.
Li XM, Ouyang Y, Yang YC, Lin R, Xu HB, Xie ZY, Li SL, Shang SM: Distribution of food-borne parasitic diseases and dietary habits in human population in Guangxi. Chin J Parasitol Parasit Dis. 2009, 27: 151-152.
Liu Q, Yuan ZG, Gao SY, Liu B, Liu XF: Detection of antibody IgG against Toxoplasma gondii from pregnant/parturient women and cancer patients in Changchun region. J Pathogen Biol. 2008, 3: 122-123. (in Chinese)
Yang ZJ, Wang CB, Hou XF: Analysis of Toxoplasma gondii infection in patients with malignant tumor. J Henan Oncol. 2001, 14: 135-136. (in Chinese)
Cheng YZ, Li ZE, Dong ZX, Li FY: Studies on susceptibility of leukemia patients to infection with Toxoplasma gondii and its clinical value. Chin J Parasit Dis Con. 2001, 14: 188-189. (in Chinese)
Zhang GL, Wang XY, Lai ZH: Serological detection of Toxoplasma gondii infection in patients with lung tuberculosis. Bull Chin Assoc Antituberculosis. 2004, 26: 118-119. (in Chinese)
Yuan WY: Investigation of Toxoplasma gondii infection in patients with hepatitis B. Chin J Parasit Dis Con. 2002, 15: 12-(in Chinese)
Baiomy AM, Mohamed KA, Ghannam MA, Shahat SA, Al-Saadawy AS: Opportunistic parasitic infections among immunocompromised Egyptian patients. J Egypt Soc Parasitol. 2010, 40: 797-808.
Shin DW, Cha DY, Hua QJ, Cha GH, Lee YH: Seroprevalence of Toxoplasma gondii infection and characteristics of seropositive patients in general hospitals in Daejeon, Korea. Korean J Parasitol. 2009, 47: 125-130. 10.3347/kjp.2009.47.2.125.
Araujo FG, Remington JS: Toxoplasmosis in immunocompromised patients. Eur J Clin Microbiol. 1987, 6: 1-2. 10.1007/BF02097180.
Wang NF: The first case of AIDS reported in China mainland. J Chin Med. 1991, 71: 671-(in Chinese)
Zhou M, Huang X, Ku DRT: Infection of toxoplasmosis combining with HIV in the population of Xinjiang province. Chin J Zoon. 2001, 17: 127-(in Chinese)
Su Y, Zhao QX: Clinical analysis of AIDS cases complicated by toxoplasmic encephalitis. Chin J Practical Neruous Dis. 2006, 9: 85-86. (in Chinese)
Cao YH, Zhang XG, Lv Q: Treatment analysis of 33 AIDS cases complicated with lymph node infections. Internal Med Chin. 2007, 2: 942-943. (in Chinese)
Goldenberg RL, Thompson C: The infectious origins of stillbirth. Am J Obstet Gynecol. 2003, 189: 861-873. 10.1067/S0002-9378(03)00470-8.
Gibbs RS: The origins of stillbirth: infectious diseases. Semin Perinatol. 2002, 26: 75-78. 10.1053/sper.2002.29839.
Chen CZ, Pu JZ: Investigation of infection of TORCH in neonate. Maternal Child Health Care China. 2007, 22: 3099-3100. (in Chinese)
Han MJ, Li YJ, Li XH, Zhang D: Study on status of Toxoplasma infection and immunology detection in new-born babies in Dalian region. Chin J Public Health. 2005, 21: 178-179. (in Chinese)
Zhou X, Fu JX, Ye HM: Research and analysis on TORCH infection in neonate in Huizhou. J Practical Med Tech. 2007, 14: 2148-2149. (in Chinese)
Tao GE, Liu SG, Chen JY: Analysis of IgG against Toxoplasma in cord blood serum from puerperals and neonate in Xinxiang city. J Appl Clin Pediatr. 2003, 18: 762-(in Chinese)
Zhou YH, Song LM, Jiang ZQ, Zhao SQ, Wu J, Gao QF, Shen YQ, Huang CY, Wang CG: Serological survey of Toxoplasma gondii infection in invalid children. Chin J Zoon. 2002, 18: 129-130. (in Chinese)
Huang MJ, Fang YH, Rong HQ: Study on the relationship between infantile cerebral palsy and toxoplasmosis. Chin Trop Med. 2001, 1: 33-34. (in Chinese)
Montoya JG, Remington JS: Toxoplasmic chorioretinitis in the setting of acute acquired toxoplasmosis. Clin Infect Dis. 1996, 23: 277-282. 10.1093/clinids/23.2.277.
Mets MB, Holfels E, Boyer KM, Swisher CN, Roizen N, Stein L, Stein M, Hopkins J, Withers S, Mack D, Luciano R, Patel D, Remington JS, Meier P, McLeod R: Eye manifestations of congenital toxoplasmosis. Am J Ophthalmol. 1997, 123: 1-16.
Gaddi PJ, Yap GS: Cytokine regulation of immunopathology in toxoplasmosis. Immunol Cell Biol. 2007, 85: 155-159. 10.1038/sj.icb.7100038.
Chen QJ, Neng HF, Wang JT, Xu XP, Ding ZY: Serology investigation on Toxoplasma infection in 103 ophthalmocace cases. Chin J Zoonoses. 1991, 5: 2-3. (in Chinese)
Liang JH: Report of 15 patients with ocular toxoplasmosis. Chin Trop Med. 2008, 8: 598-599. (in Chinese)
Hu SX, Yan H, Wei ZY, Li M, Xie CF, Lin SC, Zhang Y: Clinical observation of simultaneous FFA and IGGA in ocular toxoplasmosis. Chin Ophthal Res. 2003, 21: 511-514. (in Chinese)
Torrey EF, Yolken RH: Schizophrenia and toxoplasmosis. Schizophr Bull. 2007, 3: 727-728.
Pedersen MG, Stevens H, Pedersen CB, Norgaard-Pedersen B, Mortensen PB: Toxoplasma infection and later development of Schizophrenia in mothers. Am J Psychiatry. 2011, 168: 814-821. 10.1176/appi.ajp.2011.10091351.
Alvarado-Esquivel C, Urbina-Alvarez JD, Estrada-Martinez S, Torres-Castorena A, Molotla-de-Leon G, Liesenfeld Q, Dubey JP: Toxoplasma gondii infection and schizophrenia: a case control study in a low Toxoplasma seroprevalence Mexican population. Parasitol Int. 2011, 60: 151-155. 10.1016/j.parint.2010.12.003.
Hamidinejat H, Ghorbanpoor M, Hosseini H, Alavi SM, Nabavi L, Jalali MH, Borojeni MP, Jafari H, Mohammadaligol S: Toxoplasma gondii infection in first-episode and inpatient individuals with schizophrenia. Int J Infect Dis. 2010, 14: e978-981. 10.1016/j.ijid.2010.05.018.
Brown AS, Schaefer CA, Quesenberry CP, Liu L, Babulas VP, Susser ES: Maternal exposure to toxoplasmosis and risk of schizophrenia in adult offspring. Am J Psychiatry. 2005, 162: 767-773. 10.1176/appi.ajp.162.4.767.
Huber M, Kirchler E, Karner M, Pycha R: Delusional parasitosis and the dopamine transporter. A new insight of etiology?. Med Hypotheses. 2007, 68: 1351-1358. 10.1016/j.mehy.2006.07.061.
Skallova A, Kodym P, Frynta D, Flegr J: The role of dopamine in Toxoplasma induced behavioural alterations in mice: An ethological and ethopharmacological study. Parasitology. 2006, 133: 525-535. 10.1017/S0031182006000886.
Krishnan RR, Keefe R, Kraus M: Schizophrenia is a disorder of higher order hierarchical processing. Med Hypotheses. 2009, 72: 740-744. 10.1016/j.mehy.2008.12.039.
Berdoy M, Webster JP, Macdonld DW: Fatal attraction in rats infected with Toxoplasma gondii. Proc R Soc Lond B Biol Sci. 2000, 267: 1591-1594. 10.1098/rspb.2000.1182.
Sun SX, Li YJ, Fang F: Investigation on Toxoplasma gondii infection in mental disease cases from Dalian city. Chin J Parasit Dis Con. 2005, 18: 157-(in Chinese)
Chen YX, Lin J, Zhang JF, Luo SJ, Yu L, Chen JF: Toxoplasma infection and childhood schizophrenia. Med J Chin Civil Administration. 2001, 13: 199-200. (in Chinese)
Wang HL, Li QY, Wang GH, Shu C, Wang XP, Liu H, Duan JL, Yang XS: Survey on Toxoplasma infection in first-episode schizophrenia and its influence on the clinical manifestation of schizophrenia. Chin J Psychiatry. 2005, 38: 134-137. (in Chinese)
Wang HL, Wang GH, Li QY, Shu C, Wang XP, Wu JH: Clinical features of first-episode schizophrenic patients with and without anti-Toxoplasma IgG. Chin Mental Health J. 2006, 20: 40-42. (in Chinese)
Zhu SY, Lin YQ, Wang SQ, Xu SE: Contrast study on schizophrenia's toxoplasmosis infection rate. Med J Chin People Health. 2003, 15: 405-406. (in Chinese)
Stahl W, Kaneda Y, Noguchi T: Reproductive failure in mice chronically infected with Toxoplasma gondii. Parasitol Res. 1994, 80: 22-27. 10.1007/BF00932619.
Antonios SN, Ismail HI, Essa T: Hypothalamic origin of reproductive failure in chronic experimental toxoplasmosis. J Egypt Soc Parasitol. 2000, 30: 593-599.
Zhang C, Wang XC: Analysis and detection of infection of Toxoplasma gondii in infertile females from 2001 to 2006. J Henan Univ Sci Tech (Med Sci). 2007, 25: 143-144. (in Chinese)
Gong TX, Li H, Lu NN: Analysis of pathogen infections in abnormal pregnancy women of child-bearing age in Xining area. Modern Prev Med. 2006, 33: 1969-(in Chinese)
Wei M, Jing DX, Luo RY, Zhang W, Wu XZ, Yang LD, Chen CY, Lu M: Study on the relationship between toxoplasmosis and oviducal sterility. J Pub Health Prev Med. 2005, 16: 31-(in Chinese)
Terpsidis KI, Papazahariadou MG, Taitzoglou IA, Papaioannou NG, Georgiadis MP, Theodoridis IT: Toxoplasma gondii: reproductive parameters in experimentally infected male rats. Exp Parasitol. 2009, 121: 238-241. 10.1016/j.exppara.2008.11.006.
Yang LD, Chen CY, Lu M, Wu XZ, Gong F: Infertility experiment on male mice infected with Toxoplasma. Chin J Zoonoses. 2005, 21: 592-594. (in Chinese)
Zhou YH, Lu YJ, Wang RB, Song LM, Shi F, Gao QF, Luo YF, Guo XF, Wang P: Survey on infection of Toxoplasma gondii in infertile couples in Suzhou countryside. National J Androl. 2002, 8: 350-352. (in Chinese)
Qi R, Su XP, Gao XL, Liang XL: Study on Toxoplasma infection in males with sterility in Shenyang city. National J Andrology. 2005, 11: 503-504. (in Chinese)
Yue L, Wang LF, Chen SM: Study on the interrelationship between Toxoplasma gondii infection and male sterility. Shaanxi Med J. 2006, 35: 1138-1140. (in Chinese)
Hui QF, Jiang CX, Cui YX, Ai CL, Xu YJ: Detection Ig G and Ig M antibodies against Toxopalsma in sera of males with sterility. J Yanan Univ (Med Sci). 2003, 1: 85-86. (in Chinese)
Lu S: Male infertility caused by Toxoplasma. National J Androl. 1998, 4: 269-270. (in Chinese)
Lin AQ, Zhong WZ, Sun B, Ma ZQ: Serological investigation of CAg, IgM and IgG to T. gondii in workers in slaughter farms from Haerbin. Chin J Zoonoses. 2003, 19: 130-(in Chinese)
Chen ZY, Li AM, Lin GC, Wang XZ: Serological investigation of Toxoplasma infection among different populations of people in Guizhou Province. Acta Academiae Med Zunyi. 2005, 28: 382-383. (in Chinese)
Feng YJ, Liu XN, Ren WF, Pan ZM, Gao YP, Guo RT: Analysis of serological investigation for Toxoplasma in Guangzhou city in 2004. J Trop Med. 2005, 5: 830-832. (in Chinese)
Liang ZB, Feny YJ, Li K, Lu HX, Shen QF: Serological investigation of Toxoplasma gondii in Huadu district in 2004. J Trop Med. 2006, 6: 448-449. (in Chinese)
Zhang Y, Li H: Seroepidemiological investigation of Toxoplasma gondii infection among population in Lanzhou area. Chin J Parasit Dis Con. 2005, 18: 432-433. (in Chinese)
Yang SN, You SF, Xu ZH, Yu CE: Serological investigation on antibody against Toxoplasma gondii for service trade workers in Wuxi city during 1996 to 1999. Practical Prev Med. 2004, 11: 506-507. (in Chinese)
Zou FC, Sun XT, Xie YJ, Li B, Zhao GH, Duan G, Zhu XQ: Seroprevalence of Toxoplasma gondii in pigs in southwestern China. Parasitol Int. 2009, 58: 306-307. 10.1016/j.parint.2009.06.002.
Zhou DH, Liang R, Yin CC, Zhao FR, Yuan ZG, Lin RQ, Song HQ, Zhu XQ: Seroprevalence of Toxoplasma gondii in pigs from southern China. J Parasitol. 2010, 96: 673-674. 10.1645/GE-2416.1.
Yu H, Zhang Z, Liu Z, Qu D, Zhang D, Zhang H, Zhou Q, Du A: Seroprevalence of Toxoplasma gondii infection in pigs, in Zhejiang Province, China. J Parasitol. 2011, 97: 748-749. 10.1645/GE-2713.1.
Hill DE, Haley C, Wagner B, Gamble HR, Dubey JP: Seroprevalence of and risk factors for Toxoplasma gondii in the U.S. swine herd using sera collected during the National Animal Health Monitoring Survey (Swine 2006). Zoonosis Public Health. 2010, 57: 53-59. 10.1111/j.1863-2378.2009.01275.x.
de Buhr K, Ludewig M, Fehlhaber K: Toxoplasma gondii-seroprevalence current results in German swine herds. Arch Lebensmittelhyg. 2008, 59: 5-8.
Alvarado-Esquivel C, Garcia-Machado C, Alvarado-Esquivel D, Gonzalez-Salazar AM, Briones-Fraire C, Vitela-Corrales J, Villena I, Dubey JP: Seroprevalence of Toxoplasma gondii infection in domestic pigs in Durango State, Mexico. J Parasitol. 2011, 97: 616-619. 10.1645/GE-2755.1.
Seuri M, Koskela P: Contact with pigs and cats associated with high prevalence of Toxoplasma antibodies among farmers. Brit J Ind Med. 1992, 49: 845-849.
Ibrahim BB, Salama MM, Gawish NI, Haridy FM: Serological and histopathological studies on Toxoplasma gondii among the workers and the slaughtered animals in Tanta Abattoir, Gharbia Governorate. J Egypt Soc Parasit. 1997, 27: 273-278.
Dias RA, Navarro IT, Ruffolo BB, Bugni FM, Castro MV, Freire RL: Toxoplasma gondii in fresh pork sausage and seroprevalence in butchers from factories in Londrina, Paraná State, Brazil. Rev Inst Med Trop Sao Paulo. 2005, 47: 185-189.
Alvarado-Esquivel C, Liesenfeld O, Estrada-Martinez S, Felix-Huerta J: Toxoplasma gondii infection in workers occupationally exposed to raw meat. Occup Med (Lond). 2011, 61: 265-269. 10.1093/occmed/kqr032.
Huo SL, Song ZZ, Zhang B, Li X, Han S, Bai L, Wu CP: Serological epidemiological survey of Toxoplasma gondii infection in humans in Inner Mongolia Autonomous Region. Med Anim Prev. 2007, 23: 894-896. (in Chinese)
Huang X, Zhang GM, Zhao HZ: Reviews on studies of toxoplasmosis in Xijiang during 1990 to 2000. Endemic Dis Bull. 2001, 16: 98-99. (in Chinese)
Zhao LQ, Liu SQ: Serological surveillance of Toxoplasma infection in Haizhu district in 2004. J Trop Med. 2007, 7: 495-496. (in Chinese)
Castagnini M, Bernazzali S, Ginanneschi C, Marchi B, Maccherini M, Tsioulpas C, Tanganelli P: Fatal disseminated toxoplasmosis in a cardiac transplantation with seropositive match for Toxoplasma: Should prophylaxis be extended?. Transpl Immunol. 2007, 18: 193-197. 10.1016/j.trim.2007.05.016.
Ye DQ, Hao JH, Huan GF, Yu XB: Study on sero-indexes among 2690 qualified blood donors. Chin J Public Health. 2003, 19: 454-455. (in Chinese)
Zhu XM, Yang TH, Yang GQ, Zhao Y, Tu YQ, He Y, Yao FZ: Study on Toxoplasma gondii infection in blood donors of Yunnan Province. J Clin Transfus Lab Med. 2007, 9: 295-298. (in Chinese)
Elsheikha HM, Aboul-Dahab MA, Abdel Maboud AI, El-Sherbini ET: Prevalence and risk factors of Toxoplasma gondii antibodies in asymptomatic Egyptian blood donors. J Egypt Soc Parasitol. 2009, 39: 351-361.
Nissapatorn V, Kamarulzaman A, Init I, Tan LH, Rohela M, Norliza A, Chan LL, Latt HM, Anuar AK, Quek KF: Seroepidemiology of toxoplasmosis among HIV-infected patients and healthy blood donors. Med J Malaysia. 2002, 57: 304-310.
Jin ZS, Feng ZB, Dai HD, Li JR: Study of Toxoplasma infection among intravenous drug users and the affecting factors. Central Chin Med J. 2006, 30: 489-490. (in Chinese)
Chen GX: Investigation of Toxoplasma infection among male intravenous drug users. J Practical Med. 2004, 20: 966-(in Chinese)
Mitchell CD, Erlich SS, Mastrucci MT, Hutto SC, Parks WP, Scott GB: Congenital toxoplasmosis occurring in infants perinatally infected with human immunodeficiency virus 1. J Pediatr Infect Dis. 1990, 9: 512-518. 10.1097/00006454-199007000-00012.
Su CK, Wu ZB: Epidemiological characteristics of Toxoplasma gondii infection in married women of childbearing age in Nanning city. J Guangxi Med Univ. 2002, 19: 88-(in Chinese)
Lu J: Serological survey of Toxoplasma infection among pregnant women in Huainan area. J Trop Dis Parasitol. 2004, 2: 159-160. (in Chinese)
Li SF, Zhao CH, Zhang R, Sun DL: Investigation of antibody IgM against TORCH in pregnant women by MAC-ELISA in Haerbin area. Heilongjiang Med J. 2003, 16: 234-(in Chinese)
Chen HY, Xiao HM, Zeng XJ, Xiong CH, Ge J, Hu GH: Seroepidemiologic investigation of Toxoplasma gondii infection among population in Nanchang area. Chin J Parasit Dis Con. 2005, 18: 436-437. (in Chinese)
Yue XL, Ding XP, Ren YQ, Zhang L: Clinical observation on TORCH infection of pregnant women in Chongqing area. Chin J Birth Health Heredity. 2005, 13: 83-84. (in Chinese)
Jiang SY, Bian HZ, Yang Y, Zhou HJ, Zhou JH, Lu Z: Survey of Toxoplasma gondii infection in pregnant women in Hongkou district, Shanghai city. Shanghai J Prev Med. 2005, 17: 210-212. (in Chinese)
Fan CM, Fan HQ: Survey of TORCH infection in married women of childbearing age in Quanzhou city during April, 2003 to March, 2004. Fujian Med J. 2005, 27: 140-(in Chinese)
Zhong YF, Xue SH: Prevalence of TORCH-IgG antibodies in non-vaccinated married fertile-aged women in Guangzhou. Maternal Child Health Care China. 2006, 21: 3309-3310. (in Chinese)
Liu B, Wu M: Experimental study of Toxoplasma infection among pregnant women in Jilin Area. J Beihua Univ (Nat Sci). 2005, 6: 526-527. (in Chinese)
Cheng ML, Wang J, Wu F: Investigation of infection of TORCH in the pregnancy in Wenlin city. J Clin Exp Med. 2006, 5: 993-(in Chinese)
Li W: Survey of Toxoplasma gondii infection in pregnant women in Baoding. Chin J Birth Health Heredity. 2007, 15: 65-66. (in Chinese)
Tang LN, Xu LN, Lu LD, Li AM, Zhou GR, Lin GC: Serological survey and evaluation of Toxoplasma infection in pregnant women in Guizhou province. Guizhou Med J. 2007, 31: 847-848. (in Chinese)
Suo QL, Yao T: Research on Toxoplasma gondii infection in pregnancy in Wuhan city. Maternal Child Health Care China. 2009, 24: 598-599. (in Chinese)
Ji JF, Luo XM, Lv GM: Serological detection of IgG and IgM against Toxoplamsa gondii in 1491 pregnant women. Contemporary Med. 2009, 15: 157-(in Chinese)
Liu XX: Analysis of Toxoplasma gondii infection in 3559 married women of childbearing age. Shandong Med J. 2009, 49: 107-(in Chinese)
Han M, Huo WX, Zhang DL, Zhang Y, Zhang WQ: Serosurvey of Toxoplasma gondii infection in fertile women in Tongliao city. J Pathogen Biol. 2009, 4: 478-479. (in Chinese)
Edelhofer R, Prossinger H: Infection with Toxoplasma gondii during pregnancy: seroepidemiological studies in Austria. Zoonoses Public Health. 2010, 57: 18-26. 10.1111/j.1863-2378.2009.01279.x.
Berger F, Goulet V, Le Strat Y, Desenclos JC: Toxoplasmosis among pregnant women in France: risk factors and change of prevalence between 1995 and 2003. Rev Epidemiol Sante Publique. 2009, 57: 241-248. 10.1016/j.respe.2009.03.006.
Vaz RS, Thomaz-Soccol V, Sumikawa E, Guimaraes AT: Serological prevalence of Toxoplasma gondii antibodies in pregnant women from Southern Brazil. Parasitol Res. 2010, 106: 661-665. 10.1007/s00436-009-1716-2.
Zhou P, Zhang H, Lin RQ, Zhang DL, Song HQ, Su C, Zhu XQ: Genetic characterization of Toxoplasma gondii isolates from China. Parasitol Int. 2009, 58: 193-195. 10.1016/j.parint.2009.01.006.
Dubey JP, Zhu XQ, Sundar N, Zhang H, Kwok OC, Su C: Genetic and biologic characterization of Toxoplasma gondii isolates of cats from China. Vet Parasitol. 2007, 145: 352-356. 10.1016/j.vetpar.2006.12.016.
Zhou P, Nie H, Zhang LX, Wang HY, Yin CC, Su C, Zhu XQ, Zhao JL: Genetic characterization of Toxoplasma gondii isolates from pigs in China. J Parasitol. 2011, 96: 1027-1029.
Hulebak KL, Schlosser W: Hazard analysis and critical control point (HACCP) history and conceptual overview. Risk Anal. 2002, 22: 547-552. 10.1111/0272-4332.00038.
Dubey JP: Toxoplasmosis - a waterborne zoonosis. Vet Parasitol. 2004, 126: 57-72. 10.1016/j.vetpar.2004.09.005.
Acknowledgements
Project support was provided, in part, by the National Basic Research Program (973 program) of China (Grant No. 2010CB530001), National Natural Science Foundation of China (Grant Nos. 31172316 and 31101812), State Key Laboratory of Veterinary Etiological Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences (Grant Nos. SKLVEB2009KFKT014, SKLVEB2010KFKT010 and SKLVEB2011KFKT004) and the Yunnan Provincial Program for Introducing High-level Scientists (Grant No. 2009CI125). Prof. J. P. Dubey at Animal Parasitic Diseases Laboratory, Animal and Natural Resources Institute, Beltsville Agricultural Research Center, United States Department of Agriculture, USA, and Assoc. Prof. Chunlei Su at Department of Microbiology, the University of Tennessee, Knoxville, USA are gratefully thanked for reading the draft manuscript and for providing constructive comments and suggestions.
Author information
Authors and Affiliations
Corresponding author
Additional information
Competing interests
The authors declare that they have no competing interests.
Authors' contributions
XQZ and PZ conceived and designed the review, and critically revised the manuscript. PZ drafted the manuscript. ZC, HLL, HZ, SH and RQL contributed to drafting the manuscript. All authors read and approved the final manuscript.
Rights and permissions
Open Access This article is published under license to BioMed Central Ltd. This is an Open Access article is distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/2.0 ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
About this article
Cite this article
Zhou, P., Chen, Z., Li, HL. et al. Toxoplasma gondii infection in humans in China. Parasites Vectors 4, 165 (2011). https://doi.org/10.1186/1756-3305-4-165
Received:
Accepted:
Published:
DOI: https://doi.org/10.1186/1756-3305-4-165