Abstract
Through a cross-sectional study design, 326 women with a history of miscarriage were examined for anti-Toxoplasma gondii IgG and IgM antibodies in Durango City, Mexico. Prevalence association with sociodemographic, clinical, and behavioral characteristics in women with miscarriage was also investigated.
Twenty-two (6.7%) of the 326 women studied had anti-T. gondii IgG antibodies and two (0.6%) were also positive for anti-T. gondii IgM antibodies. Seroprevalence of T. gondii infection was not influenced by age, birth place, occupation, educational level, or socioeconomic status. In contrast, logistic regression showed that T. gondii exposure was associated with consumption of raw or undercooked meat (OR = 6.84; 95% CI: 1.04–44.95; P = 0.04) and consumption of chicken brains (OR = 18.48; 95% CI: 1.26–269.43; P = 0.03).
This is the first study on the seroepidemiology of T. gondii infection in women with a history of miscarriage in Northern Mexico. Of interest, we also observed an association of T. gondii exposure with consumption of chicken brains. Contributing factors for T. gondii exposure found in the present study should be taken into consideration for public health measures to avoid infection with T. gondii and its sequelae.
Keywords: cross-sectional study, epidemiology, Mexico, miscarriage, risk factors, seroprevalence, Toxoplasma
Introduction
The parasite Toxoplasma gondii (T. gondii) causes infections in humans worldwide [1, 2]. Infections with T. gondii are commonly asymptomatic. However, some infections with T. gondii may lead to disease including cervical lymphadenopathy or chorioretinitis [1]. In addition, primary infections with T. gondii in pregnant women may lead to congenital disease [1, 3]. Damage to the fetus is characterized by severe necrotic changes to the central nervous system, i.e., the brain and eyes [4, 5]. These commonly occur when infection with T. gondii is acquired during the first trimester of pregnancy [1, 3].
Very little is known about the epidemiology of T. gondii infection in women with abortions. Seroprevalences of infection with T. gondii varying from 17% to 43.8% in women with abortions have been reported in Pakistan [6], Egypt [7], and India [8]. However, very poor knowledge exists about the characteristics of the women with miscarriages and T. gondii infection. In a previous survey, we found an association of T. gondii seropositivity with abortion in rural pregnant women in Durango State, Mexico, especially in communities with high seroprevalence of T. gondii infection [9]. However, there is no information about the seroprevalence and risks associated with of T. gondii infection in urban women with a history of miscarriage in Northern Mexico. Therefore, we performed a survey to determine the prevalence of T. gondii, the concentrations of anti-T. gondii IgG, and the sociodemographic, clinical, and behavioral characteristics associated to T. gondii seropositivity in women with a history of miscarriage.
Materials and methods
Study populations and study design
Through a cross-sectional study design, we studied 326 women with a history of miscarriage in a public primary health care center (Centro de Salud con Servicios Ampliados 450) and the General Hospital of the Secretary of Health from August to December 2013 in Durango City, Mexico. Inclusion criteria for enrollment in the study were: 1) women with a history of miscarriage (spontaneous fetal loss during the first 20 weeks of pregnancy); 2) residing in Durango City; 3) aged 16 years and older; and 4) who accepted to participate in the study.
Sociodemographic, clinical, and behavioral data
We used a standardized questionnaire to obtain sociodemographic, clinical, and behavioral characteristics from the women studied. Sociodemographic items included age, birth place, residence, occupation, educational, and socioeconomic status. Clinical data included obstetric history (number of pregnancies, deliveries, cesarean section, and miscarriages); presence of any underlying disease, frequent headaches, and impairments of memory, reflexes, vision, and hearing; and history of blood transfusions or transplants. Behavioral items obtained were animal contacts; foreign travel; consumption of raw or undercooked meat (pork, lamb, beef, goat, boar, chicken, turkey, rabbit, deer, squirrel, horse, or other); eating away of home (in restaurants and fast food outlets); consumption of dried or cured meat (chorizo, ham, sausages, or salami), unpasteurized milk, untreated water, and unwashed raw vegetables or fruits; and contact with soil (gardening or agriculture).
Laboratory tests
Sera of the women studied were examined for anti-T. gondii IgG antibodies by a commercially available enzyme immunoassay “Toxoplasma IgG” kit (Diagnostic Automation Inc., Calabasas, CA, USA). Sera positive for anti-T. gondii IgG antibodies were further analyzed for anti-T. gondii IgM antibodies by a commercially available enzyme immunoassay “Toxoplasma IgM” kit (Diagnostic Automation Inc., Calabasas, CA, USA). Both tests were performed following the instructions of the manufacturers.
Statistical analysis
The statistical analysis was performed with the aid of the software: Epi Info version 3.5.4 and SPSS version 15.0. We used the Pearson’s c2 and the Fisher exact test (when values were less than 5) for comparison of frequencies among groups. Bivariate and multivariate analyses were used to evaluate the association between the characteristics of the women and T. gondii seropositivity. Variables with a P value equal to or less than 0.10 obtained in the bivariate analysis were included in the multivariate analysis. Odd ratios (ORs) and 95% confidence intervals (CIs) were calculated by multivariate analysis using backward stepwise logistic regression analysis. Statistical significance was set at a P value less than 0.05.
Ethics statement
This study was approved by the ethical committees of the Centro de Salud de Servicios Ampliados 450 and the General Hospital of the Secretary of Health in Durango City. The purpose and procedures of the study were explained to all women, and a written informed consent was obtained from all participants.
Results
Of 326 women with miscarriage history, 22 (6.7%) had anti-T. gondii IgG antibodies and two (0.6%) were also positive for anti-T. gondii IgM antibodies. Of 22 anti-T. gondii IgG positive participants, 12 (54.5%) had IgG levels higher than 150 IU/ml, one (4.5%) between 100 to 150 IU/ml, and nine (41%) between 9 to 99 IU/ml. General sociodemographic characteristics of the 326 women and their relation with T. gondii seropositivity are shown in Table 1. Most women were born in Durango State, Mexico, unemployed (housewives, students, or no occupation), and of medium socioeconomic status. The mean age of the women was 35.57 ± 12.43 years (range 15–71 years). Seroprevalence of T. gondii infection was not significantly influenced by age, birth place, occupation, educational level, or socioeconomic status of women.
Table 1.
Sociodemographic characteristics of women with miscarriage history and seroprevalence of Toxoplasma gondii infection
| Characteristic | No. of women tested | Prevalence of T.
gondii infection |
Odds ratio | 95% Confidence interval |
P value | |
|---|---|---|---|---|---|---|
| No. | % | |||||
| Age groups (years) | ||||||
| 30 or less | 124 | 6 | 4.8 | 1.0 | ||
| 31–50 | 160 | 11 | 6.9 | 1.5 | 0.48–4.56 | 0.47 |
| >50 | 42 | 5 | 11.9 | 2.7 | 0.66–10.61 | 0.14 |
| Birth place | ||||||
| Durango State | 300 | 21 | 7.0 | 1.9 | 0.25–39.08 | 1 |
| Other Mexican State | 26 | 1 | 3.8 | 1.0 | ||
| Educational level | ||||||
| No education | 8 | 1 | 12.5 | 4.6 | 0.00–196.79 | 0.35 |
| 1–6 years | 79 | 9 | 11.4 | 4.1 | 0.49–91.34 | 0.27 |
| 7–12 years | 206 | 11 | 5.3 | 1.8 | 0.23–38.65 | 1 |
| 13 or more years | 33 | 1 | 3.0 | 1.0 | ||
| Occupation | ||||||
| Unemployed | 249 | 17 | 6.8 | 1.1 | 0.35–3.40 | 0.91 |
| Employed | 77 | 5 | 6.5 | 1.0 | ||
| Socioeconomic status | ||||||
| Low | 105 | 7 | 6.7 | 1.0 | ||
| Medium | 221 | 15 | 6.8 | 1.0 | 0.37–2.86 | 0.96 |
Concerning clinical data, seroprevalence of T. gondii infection was not associated with characteristics including obstetric history (number of pregnancies, deliveries, cesarean section, and miscarriages); presence of underlying diseases, frequent headaches, and impairments of memory, reflexes, vision, and hearing; and history of blood transfusions or transplants.
With respect to behavioral characteristics (Table 2), the bivariate analysis showed a number of variables with a P value equal to or less than 0.10 including cleaning cat excrement (P = 0.06); raising farm animals (P = 0.01); having traveled abroad (P = 0.03); and consumption of horse meat (P = 0.05), raw or undercooked meat (P = 0.03), chicken brains (P = 0.01), and unwashed raw fruit (P = 0.05). Other behavioral variables including presence of cats at home; consumption of untreated water, unwashed raw vegetables, unpasteurized milk, dried or cure meat; eating away of home; or soil contact showed P values higher than 0.10 in the bivariate analysis. Further analysis by using logistic regression (Table 3) showed that T. gondii exposure was positively associated with consumption of raw or undercooked meat (OR = 6.84; 95% CI: 1.04–44.95; P = 0.04) and consumption of chicken brains (OR = 18.48; 95% CI: 1.26–269.43; P = 0.03).
Table 2.
Bivariate analysis of selected putative risk factors for infection with Toxoplasma gondii in women with miscarriage history in Durango, Mexico
| Characteristic | Women tested* |
Prevalence of T.
gondii infection |
P value | |
|---|---|---|---|---|
| No. | No. | % | ||
| Cleaning cat excrement | ||||
| Yes | 92 | 10 | 10.9 | 0.06 |
| No | 233 | 12 | 5.2 | |
| Birds at home | ||||
| Yes | 122 | 11 | 9 | 0.2 |
| No | 204 | 11 | 5.4 | |
| Raising farm animals | ||||
| Yes | 125 | 14 | 11.2 | 0.01 |
| No | 200 | 8 | 4 | |
| Traveled abroad | ||||
| Yes | 69 | 9 | 13 | 0.03 |
| No | 254 | 13 | 5.1 | |
| Chicken meat consumption | ||||
| Yes | 324 | 21 | 6.5 | 0.13 |
| No | 2 | 1 | 50 | |
| Pigeon meat consumption | ||||
| Yes | 31 | 4 | 12.9 | 0.14 |
| No | 294 | 18 | 6.1 | |
| Duck meat consumption | ||||
| Yes | 41 | 5 | 12.2 | 0.17 |
| No | 285 | 17 | 6 | |
| Horse meat consumption | ||||
| Yes | 22 | 4 | 18.2 | 0.05 |
| No | 304 | 18 | 5.9 | |
| Degree of meat cooking | ||||
| Raw | 1 | 0 | 0 | 0.03 |
| Undercooked | 6 | 2 | 33.3 | |
| Well done | 319 | 20 | 6.3 | |
| Consumption of chicken’s brain | ||||
| Yes | 3 | 2 | 66.7 | 0.01 |
| No | 323 | 20 | 6.2 | |
| Unwashed raw vegetables | ||||
| Yes | 84 | 8 | 9.5 | 0.23 |
| No | 242 | 14 | 5.8 | |
| Unwashed raw fruits | ||||
| Yes | 116 | 12 | 10.3 | 0.05 |
| No | 210 | 10 | 4.8 | |
| Untreated water | ||||
| Yes | 207 | 16 | 7.7 | 0.35 |
| No | 119 | 6 | 5 | |
| Soil contact | ||||
| Yes | 214 | 16 | 7.5 | 0.46 |
| No | 112 | 6 | 5.4 | |
| Floor at home | ||||
| Ceramic or wood | 121 | 5 | 4.1 | 0.34 |
| Concrete | 167 | 14 | 8.4 | |
| Soil | 38 | 3 | 7.9 | |
Table 3.
Results of the multivariate analysis
| Characteristic | P value | Odds ratio | 95% Confidence interval |
|---|---|---|---|
| Raising farm animals | 0.075 | 2.36 | 0.91–6.10 |
| Traveled abroad | 0.057 | 2.59 | 0.97–6.90 |
| Consumption of: | |||
| Horse meat | 0.057 | 3.65 | 0.96–13.91 |
| Raw or undercooked meat | 0.045 | 6.84 | 1.04–44.95 |
| Chicken brains | 0.033 | 18.48 | 1.26–269.43 |
Discussion
The present study allows us to obtain new epidemiological knowledge of T. gondii infection in women with a history of miscarriage. Studying the epidemiology of infection with T. gondii is important to understand the magnitude of the infection as a public health problem and to find transmission routes of the infection. Such information is useful for planning optimal measures against infection. In the international context, only few epidemiology studies in women with a history of miscarriage exist. The seroprevalence of infection with T. gondii in women with abortion has been reported high (17% to 43.8%) in some African [7] and Asian countries [6, 8]. We found a low (6.7%) seroprevalence of T. gondii infection in women with miscarriage history in Durango City, Mexico. The seroprevalence found is comparable with a 6.1% seroprevalence reported in pregnant women [10] and the general population in Durango City [11]. The fact that women with a history of miscarriage in Durango City have a similar seroprevalence of infection than other populations in the same city might suggest that T. gondii is not associated with miscarriages in urban women. However, this was not the case in rural women in Durango State; a previous study in pregnant women living in rural areas in Durango State showed that T. gondii infection was associated with abortion [9]. In studies of women with spontaneous abortion in the Southern Mexican state of Yucatan, researchers found high (47%–55%) seroprevalences of T. gondii infection [12, 13]. Similarly, in Guadalajara City in central Mexico, researchers found a 44.9% seroprevalence in women with habitual abortions [14]. The seroprevalence found in women in Durango is much lower than those reported in the studies in Guadalajara City and Yucatan State. However, difference of seroprevalences can be explained by a lower seroprevalence in populations in northern than in central and southern Mexican states [15].
Previous studies in Durango State have shown a number of sociodemographic and housing factors associated with T. gondii infection including age [11, 16], low education [16], low socioeconomic conditions [9], and soil flooring at home [10]. However, in the present study, we did not find any sociodemographic or housing characteristic associated with T. gondii infection. Similarly, we did not find an association of T. gondii exposure with clinical characteristics of the women. This lack of association might be due to the presence of mostly chronic T. gondii infections. In fact, only two women had anti-T. gondii IgM antibodies suggesting recent infections.
Of the behavioral characteristics, multivariate analysis showed that T. gondii exposure was associated with consumption of raw or undercooked meat. Consumption of meat from T. gondii-infected animals is a major route for T. gondii infection in humans [1]. The association of T. gondii exposure with consumption of raw or undercooked meat in our study suggests that miscarriage in our setting might be more related with ingestion of meat containing parasite cysts than ingestion of contaminated water or food containing oocysts shed by cats. Multivariate analysis did not allow us to identify any meat from specific animals involved in T. gondii exposure. Therefore, meat from any animal could be involved. In fact, serological evidence of T. gondii infection has been reported in a number of edible animals in our setting including chickens [17], goats [18], sheep [19], and pigs [20]. Remarkably, we found an association of T. gondii seropositivity with consumption of chicken brains. Although chicken brains are usually eaten cooked, it is likely that chicken brains remain undercooked because of thermic protection of the chicken skull. To the best of our knowledge, this is the first report of an association of consumption of chicken brains with T. gondii seropositivity in humans. Interpretation of this finding should be taken with care because a limited number of subjects were studied and a wide 95% confidence interval of the odd ratio was obtained. However, serological and molecular evidence of T. gondii infection has been reported in chickens in Mexico [17, 21]. Chickens studied in Mexico have been found infected with T. gondii of the clonal type III lineage [21]. It is known that T. gondii may infect chicken brains [22], and such tissue is frequently selected to search for T. gondii cysts [23, 24]. Nested polymerase chain reaction (PCR) has demonstrated T. gondii DNA in brains of chickens [25]. Therefore, results of the present study suggest that consumption of chicken brains represents a new risk factor for T. gondii infection, and such risk might be higher than consumption of chicken flesh.
This is the first study on the seroepidemiology of T. gondii infection in women with a history of miscarriage in Northern Mexico and of an association of T. gondii exposure with consumption of chicken brains. Contributing factors for T. gondii exposure found in the present study should be taken into consideration for avoiding T. gondii infection.
Contributor Information
C. Alvarado-Esquivel, 1 Biomedical Research Laboratory, Faculty of Medicine and Nutrition, Juárez University of Durango State, Avenida Universidad S/N, 34000 Durango, Mexico.
S. J. Pacheco-Vega, 1 Biomedical Research Laboratory, Faculty of Medicine and Nutrition, Juárez University of Durango State, Avenida Universidad S/N, 34000 Durango, Mexico.
J. Hernández-Tinoco, 1 Biomedical Research Laboratory, Faculty of Medicine and Nutrition, Juárez University of Durango State, Avenida Universidad S/N, 34000 Durango, Mexico; 2 Institute for Scientific Research “Dr. Roberto Rivera-Damm,” Juárez University of Durango State, Avenida Universidad S/N, 34000 Durango, Mexico.
M. M. Centeno-Tinoco, 3 Health Center 450, Secretary of Health, Toma de Zacateas 129, 34000 Durango, Mexico.
I. Beristain-García, 4 Faculty of Nursing and Obstetrics, Juárez University of Durango State, Avenida Cuauhtémoc 223, 34000 Durango, Mexico.
L. F. Sánchez-Anguiano, 1 Biomedical Research Laboratory, Faculty of Medicine and Nutrition, Juárez University of Durango State, Avenida Universidad S/N, 34000 Durango, Mexico; 2 Institute for Scientific Research “Dr. Roberto Rivera-Damm,” Juárez University of Durango State, Avenida Universidad S/N, 34000 Durango, Mexico.
O. Liesenfeld, 5 Institute for Microbiology and Hygiene, Campus Benjamin Franklin, Charité Medical School, Hindenburgdamm 27, D-12203 Berlin, Germany.
E. Rábago-Sánchez, 1 Biomedical Research Laboratory, Faculty of Medicine and Nutrition, Juárez University of Durango State, Avenida Universidad S/N, 34000 Durango, Mexico.
L. O. Berumen-Segovia, 1 Biomedical Research Laboratory, Faculty of Medicine and Nutrition, Juárez University of Durango State, Avenida Universidad S/N, 34000 Durango, Mexico.
References
- 1.Montoya JG, Liesenfeld O. Toxoplasmosis. Lancet. 2004 Jun 12;363(9425):1965–1976. doi: 10.1016/S0140-6736(04)16412-X. [DOI] [PubMed] [Google Scholar]
- 2.Hill DE, Chirukandoth S, Dubey JP. Biology and epidemiology of Toxoplasma gondii in man and animals. Anim Health Res Rev. 2005 Jun;6(1):41–61. doi: 10.1079/ahr2005100. [DOI] [PubMed] [Google Scholar]
- 3.Rorman E, Zamir CS, Rilkis I, Ben-David H. Congenital toxoplasmosis – prenatal aspects of Toxoplasma gondii infection. Reprod Toxicol. 2006 May;21(4):458–472. doi: 10.1016/j.reprotox.2005.10.006. [DOI] [PubMed] [Google Scholar]
- 4.Roberts F, Mets MB, Ferguson DJ, O'Grady R, O'Grady C, Thulliez P, Brézin AP, McLeod R. Histopathological features of ocular toxoplasmosis in the fetus and infant. Arch Ophthalmol. 2001 Jan;119(1):51–58. [PubMed] [Google Scholar]
- 5.Villena I, Ancelle T, Delmas C, Garcia P, Brezin AP, Thulliez P, Wallon M, King L, Goulet V. Congenital toxoplasmosis in France in 2007: first results from a national surveillance system. Euro Surveill. 2010 Jun 24;15(25):19600. doi: 10.2807/ese.15.25.19600-en. [DOI] [PubMed] [Google Scholar]
- 6.Pal RA, Qayyum M, Yaseen M. Seroprevalence of antibodies to Toxoplasma gondii, with particular reference to obstetric history of patients in Rawalpindi-Islamabad, Pakistan. J Pak Med Assoc. 1996 Mar;46(3):56–58. [PubMed] [Google Scholar]
- 7.Attia RA, el-Zayat MM, Rizk H, Motawea S. Toxoplasma IgG. & IgM. antibodies. A case control study. J Egypt Soc Parasitol. 1995 Dec;25(3):877–882. [PubMed] [Google Scholar]
- 8.Gogate A, Deodhar LP, Shah PK, Vaidya P. Detection of Chlamydia trachomatis antigen & Toxoplasma gondii (IgM) & Mycoplasma hominis (IgG) antibodies by ELISA in women with bad obstetric history. Indian J Med Res. 1994 Jul;100:19–22. [PubMed] [Google Scholar]
- 9.Alvarado-Esquivel C, Torres-Castorena A, Liesenfeld O, García-López CR, Estrada-Martínez S, Sifuentes-Alvarez A, Marsal-Hernández JF, Esquivel-Cruz R, Sandoval-Herrera F, Castañeda JA, Dubey JP. Seroepidemiology of Toxoplasma gondii infection in pregnant women in rural Durango, Mexico. J Parasitol. 2009 Apr;95(2):271–274. doi: 10.1645/GE-1829.1. [DOI] [PubMed] [Google Scholar]
- 10.Alvarado-Esquivel C, Sifuentes-Alvarez A, Narro-Duarte SG, Estrada-Martínez S, Díaz-García JH, Liesenfeld O, Martínez-García SA, Canales-Molina A. Seroepidemiology of Toxoplasma gondii infection in pregnant women in a public hospital in northern Mexico. BMC Infect Dis. 2006 Jul 13;6:113. doi: 10.1186/1471-2334-6-113. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Alvarado-Esquivel C, Estrada-Martínez S, Pizarro-Villalobos H, Arce-Quiñones M, Liesenfeld O, Dubey JP. Seroepidemiology of Toxoplasma gondii infection in general population in a northern Mexican city. J Parasitol. 2011 Feb;97(1):40–43. doi: 10.1645/GE-2612.1. [DOI] [PubMed] [Google Scholar]
- 12.Zavala-Velázquez J, Guzmán-Marín E, Barrera-Pérez M, Rodríguez-Félix ME. [Toxoplasmosis and abortion in patients at the O'Horan Hospital of Merida, Yucatan] Salud Publica Mex. 1989 Sep-Oct;31(5):664–668. [PubMed] [Google Scholar]
- 13.Vado-Solís IA, Suárez-Solís V, Jiménez-Delgadillo B, Zavala-Velázquez JE, Segura-Correa JC. Toxoplasma gondii presence in women with spontaneous abortion in Yucatan, Mexico. J Parasitol. 2013 Apr;99(2):383–385. doi: 10.1645/GE-3189.1. [DOI] [PubMed] [Google Scholar]
- 14.Galván Ramírez ML, Soto Mancilla JL, Velasco Castrejón O, Pérez Medina R. Incidence of anti-Toxoplasma antibodies in women with high-risk pregnancy and habitual abortions. Rev Soc Bras Med Trop. 1995 Oct-Dec;28(4):333–337. doi: 10.1590/s0037-86821995000400005. [DOI] [PubMed] [Google Scholar]
- 15.Velasco-Castrejón O, Salvatierra-Izaba B, Valdespino JL, Sedano-Lara AM, Galindo-Virgen S, Magos C, Llausás A, Tapia-Conyer R, Gutiérrez G, Sepúlveda J. [Seroepidemiology of toxoplasmosis in Mexico] Salud Publica Mex. 1992 Mar-Apr;34(2):222–229. [PubMed] [Google Scholar]
- 16.Alvarado-Esquivel C, Liesenfeld O, Burciaga-López BD, Ramos-Nevárez A, Estrada-Martínez S, Cerrillo-Soto SM, Carrete-Ramírez FA, López-Centeno Mde L, Ruiz-Martínez MM. Seroepidemiology of Toxoplasma gondii infection in elderly people in a northern Mexican city. Vector Borne Zoonotic Dis. 2012 Jul;12(7):568–574. doi: 10.1089/vbz.2011.0875. [DOI] [PubMed] [Google Scholar]
- 17.Alvarado-Esquivel C, González-Salazar AM, Alvarado-Esquivel D, Ontiveros-Vázquez F, Vitela-Corrales J, Villena I, Dubey JP. Seroprevalence of Toxoplasma gondii infection in chickens in Durango State, Mexico. J Parasitol. 2012 Apr;98(2):431–432. doi: 10.1645/GE-2979.1. [DOI] [PubMed] [Google Scholar]
- 18.Alvarado-Esquivel C, García-Machado C, Vitela-Corrales J, Villena I, Dubey JP. Seroprevalence of Toxoplasma gondii infection in domestic goats in Durango State, Mexico. Vet Parasitol. 2011 Dec 29;183(1-2):43–46. doi: 10.1016/j.vetpar.2011.06.021. [DOI] [PubMed] [Google Scholar]
- 19.Alvarado-Esquivel C, García-Machado C, Alvarado-Esquivel D, Vitela-Corrales J, Villena I, Dubey JP. Seroprevalence of Toxoplasma gondii infection in domestic sheep in Durango State, Mexico. J Parasitol. 2012 Apr;98(2):271–273. doi: 10.1645/GE-2958.1. [DOI] [PubMed] [Google Scholar]
- 20.Alvarado-Esquivel C, García-Machado C, Alvarado-Esquivel D, González-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 Aug;97(4):616–619. doi: 10.1645/GE-2755.1. [DOI] [PubMed] [Google Scholar]
- 21.Dubey JP, Velmurugan GV, Alvarado-Esquivel C, Alvarado-Esquivel D, Rodríguez-Peña S, Martínez-García S, González-Herrera A, Ferreira LR, Kwok OC, Su C. Isolation of Toxoplasma gondii from animals in Durango, Mexico. J Parasitol. 2009 Apr;95(2):319–322. doi: 10.1645/GE-1874.1. [DOI] [PubMed] [Google Scholar]
- 22.Dubey JP, Salant H, Sreekumar C, Dahl E, Vianna MC, Shen SK, Kwok OC, Spira D, Hamburger J, Lehmann TV. High prevalence of Toxoplasma gondii in a commercial flock of chickens in Israel, and public health implications of free-range farming. Vet Parasitol. 2004 May 26;121(3-4):317–322. doi: 10.1016/j.vetpar.2004.03.004. [DOI] [PubMed] [Google Scholar]
- 23.Dubey JP, Ruff MD, Camargo ME, Shen SK, Wilkins GL, Kwok OC, Thulliez P. Serologic and parasitologic responses of domestic chickens after oral inoculation with Toxoplasma gondii oocysts. Am J Vet Res. 1993 Oct;54(10):1668–1672. [PubMed] [Google Scholar]
- 24.Dubey JP, Webb DM, Sundar N, Velmurugan GV, Bandini LA, Kwok OC, Su C. Endemic avian toxoplasmosis on a farm in Illinois: clinical disease, diagnosis, biologic and genetic characteristics of Toxoplasma gondii isolates from chickens (Gallus domesticus), and a goose (Anser anser) Vet Parasitol. 2007 Sep 30;148(3-4):207–212. doi: 10.1016/j.vetpar.2007.06.033. [DOI] [PubMed] [Google Scholar]
- 25.Chumpolbanchorn K, Lymbery AJ, Pallant LJ, Pan S, Sukthana Y, Thompson RC. A high prevalence of Toxoplasma in Australian chickens. Vet Parasitol. 2013 Sep 1;196(1-2):209–211. doi: 10.1016/j.vetpar.2013.01.009. [DOI] [PubMed] [Google Scholar]