Open Access

Toxoplasma gondii infection and liver disease: a case-control study in a Northern Mexican population

  • Cosme Alvarado-Esquivel1Email author,
  • José Luis Torres-Berumen2,
  • Sergio Estrada-Martínez3,
  • Oliver Liesenfeld4, 5 and
  • Miguel Francisco Mercado-Suarez2
Parasites & Vectors20114:75

https://doi.org/10.1186/1756-3305-4-75

Received: 14 April 2011

Accepted: 13 May 2011

Published: 13 May 2011

Abstract

Background

Infection with the protozoan parasite Toxoplasma gondii may cause liver disease. However, the impact of the infection in patients suffering from liver disease is unknown. Therefore, through a case-control study design, 75 adult liver disease patients attending a public hospital in Durango City, Mexico, and 150 controls from the general population of the same region matched by gender, age, and residence were examined with enzyme-linked immunoassays for the presence of anti-Toxoplasma IgG and anti-Toxoplasma IgM antibodies. Socio-demographic, clinical and behavioral characteristics from the study subjects were obtained.

Results

Seroprevalence of anti-Toxoplasma IgG antibodies and IgG titers did not differ significantly in patients (10/75; 13.3%) and controls (16/150; 10.7%). Two (2.7%) patients and 5 (3.3%) controls had anti-Toxoplasma IgM antibodies (P = 0.57). Seropositivity to Toxoplasma did not show any association with the diagnosis of liver disease. In contrast, seropositivity to Toxoplasma in patients was associated with consumption of venison and quail meat. Toxoplasma seropositivity was more frequent in patients with reflex impairment (27.8%) than in patients without this impairment (8.8%) (P = 0.05). Multivariate analysis showed that Toxoplasma seropositivity in patients was associated with consumption of sheep meat (OR = 8.69; 95% CI: 1.02-73.71; P = 0.04) and rabbit meat (OR = 4.61; 95% CI: 1.06-19.98; P = 0.04).

Conclusions

Seropositivity to Toxoplasma was comparable among liver disease patients and controls. Further studies with larger sample sizes are needed to elucidate the association of Toxoplasma with liver disease. Consumption of venison, and rabbit, sheep, and quail meats may warrant further investigation.

Background

Human infection with the protozoan parasite Toxoplasma gondii occurs worldwide [1, 2]. Major routes of T. gondii infections include ingesting food or water that is contaminated with oocysts shed by cats or by eating undercooked or raw meat containing tissue cysts [24]. The clinical spectrum of T. gondii infection varies from an asymptomatic state to severe illness. The parasite can affect the host's lymph nodes, eyes, central nervous system, liver, and heart [3, 5, 6]. In liver, the parasite has been associated with a number of pathological changes including hepatomegaly, granuloma, hepatitis, and necrosis [714]. In addition, an epidemiological study has reported an association of T. gondii infection with liver cirrhosis [15]. However, epidemiological studies on the association of infection with T. gondii and liver disease are scarce, and have not been performed in Mexico. Therefore, we performed a case-control study in Northern Mexico to determine the seroprevalence of T. gondii infection and anti-T. gondii IgG levels in adult patients with liver disease attending the Department of Gastroenterology in a secondary-care public hospital in Durango City. Furthermore, we investigated socio-demographic, clinical, and behavioral characteristics associated with T. gondii seropositivity in these patients.

Methods

Study design and study populations

Through a case-control study design, we studied the association of liver disease with infection with T. gondii in adult patients and control subjects in Durango City, Mexico from January 2009 to December 2010.

Liver disease patients

Seventy five outpatients attended in the Gastroenterology Department of a public secondary-care hospital (Mexican Social Security Institute) in Durango City, Mexico were enrolled in the study. Forty seven patients were male and twenty eight were female. The mean age of the patients was 58.65 ± 14.41 years (range: 22-85 years). All patients resided in Durango State. Patients suffered from liver cirrhosis (n = 67), steatosis (n = 4), chronic hepatitis (n = 2), acute hepatitis (n = 1), and amoebic liver abscess (n = 1). The etiology of liver cirrhosis was alcohol consumption in 35 patients, hepatitis C virus in 4 patients, and unknown in 28 patients.

Control subjects

One hundred and fifty control subjects matched with patients by age, gender, and residence were included in the study. The mean age in controls was 58.68 ± 14.35 (range: 22-86) and comparable with that in patients (P = 0.99). Control subjects were obtained from the general population of Durango City, Mexico.

Ethical aspects

This study was approved by the Institutional Ethical Committee of the Mexican Social Security Institute. The purpose and procedures of the study were explained to all participants, and a written informed consent was obtained from all of them.

Socio-demographic, clinical and behavioral data

We explored socio-demographic, clinical and behavioral characteristics of the participants with the aid of a standardized questionnaire. Socio-demographic data including age, gender, birthplace, residence area, educational level, occupation, and socio-economic level were obtained from all participants. Clinical data explored in patients included type and duration of liver disease, clinical response to treatment, presence of concomitant diseases, presence or history of lymphadenopathy, frequent headache, impairments in memory, reflexes, hearing and vision, blood transfusion, transplant or surgery history. Behavioral data included animal contacts, contact with cat feces, foreign travel, kind of meat consumption (pork, beef, goat, sheep, boar, chicken, turkey, pigeon, rabbit, deer, squirrel, horse, opossum, or other), consumption of raw or undercooked meat, unpasteurized milk, dried or cured meat (chorizo, ham, sausages or salami), consumption of unwashed raw vegetables, fruits, or untreated water, frequency of eating away from home (in restaurants or fast food outlets), contact with soil (gardening or agriculture), and types of floors at home.

Laboratory tests

Serum samples of participants were obtained and kept frozen at -20°C until analyzed. Sera were analyzed by qualitative and quantitative methods for anti-T. gondii IgG antibodies with the commercially available enzyme immunoassay kit "Toxoplasma IgG" (International Immuno-Diagnostics, Foster City, California). Anti-T. gondii IgG antibody levels were expressed as International Units (IU)/ml, and a result equal or greater than 8 IU/ml was considered positive. In addition, sera positive for anti-T. gondii IgG antibodies were further analyzed for anti-T. gondii IgM antibodies by the commercially available enzyme immunoassay "Toxoplasma IgM" kit (International Immuno-Diagnostics). All tests were performed following the instructions of the manufacturer.

Statistical Analysis

Results were analyzed with the aid of Epi Info version 3.5.1 and SPSS 15.0 (SPSS Inc. Chicago, Illinois). Age among the groups was compared by the student's t test. For comparison of the frequencies among groups, the Yates corrected or, when indicated, the Fisher exact test, were used. Bivariate and multivariate analyses were used to assess the association between subject's characteristics and T. gondii infection. Variables were included in the multivariate analysis if they had a P value equal or less than 0.25 in the bivariate analysis. Odd ratio (OR) and 95% confidence interval (CI) were calculated by multivariate analysis using multiple, unconditional, logistic regression. When a cell in the 2 × 2 contingency table had a value of zero, the odds ratio was calculated by adding 0.5 to all table cells [16]. A P value less than 0.05 was considered statistically significant.

Results

Anti-T. gondii IgG antibodies were found in 10 (13.3%) of 75 patients and in 16 (10.7%) of 150 controls (P = 0.71). Of the 10 anti-T. gondii IgG positive patients, 6 (8.0%) had IgG levels higher than 150 IU/ml, and 4 (5.3%) between 8 to 99 IU/ml. In comparison, of the 16 anti-T. gondii IgG positive controls, 9 (6.0%) had IgG levels higher than 150 IU/ml, 2 (1.3%) between 100 to 150 IU/ml, and 5 (3.3%) between 8 to 99 IU/ml. Anti-T. gondii IgG levels were comparable among patients and controls (P = 0.60). Anti-T. gondii IgM antibodies were found in 2 patients and in 5 controls (2.7% vs 3.3%, respectively; P = 0.57). The socio-demographic characteristics among seropositive and seronegative patients were not significantly different (Table 1). Seropositivity to T. gondii was significantly higher in patients with an occupation of truck driver than those with other occupations (3/3: 100% vs 8/65: 12.3%; P = 0.003). The type, duration and clinical response to treatment of liver disease did not show any association with the seroprevalence and levels of anti-T. gondii IgG (Table 2). The frequency of T. gondii seropositivity was higher in patients with reflex impairment (27.8%) than patients without this impairment (8.8%) (P = 0.05). Patients with a history of abdominal hernia repair had a significantly higher seroprevalence of T. gondii infection than those without this history (3/5: 60% vs 7/70: 10%, respectively; P = 0.01). In contrast, no statistically significant differences were observed among T. gondii positive and T. gondii negative patients in the frequencies of other clinical characteristics including concomitant diseases, frequent headaches, presence or history of lymphadenopathy, blood transfusion, or transplant, and impairments in memory, hearing or vision (Table 3).
Table 1

Socio-demographic characteristics of the patients and seropositivity to T. gondii.

   

Prevalence of T. gondii infection

 

Characteristic

No.

%

No.

%

P value

Gender

     

   Male

47

62.7

8

17.0

0.19

   Female

28

37.3

2

7.1

 

Age groups (years)

     

   30 or less

3

4.0

0

0.0

 

   31-50

17

22.7

2

11.8

0.56

   51-70

41

54.7

6

14.6

 

   >70

14

18.7

2

14.3

 

Residence place

     

   Durango City

75

100.0

10

13.3

 

Birth place

     

   Durango State

67

89.3

9

13.4

0.71

   Other Mexican State

8

10.7

1

12.5

 

Residence area

     

   Urban

49

65.3

5

10.2

0.2

   Suburban

1

1.3

0

0.0

 

   Rural

25

33.3

5

20.0

 

Socio-economic level

     

   Low

50

72.5

8

16.0

0.44

   Medium

19

27.5

2

10.5

 

Educational level

     

   No education

6

8.0

1

16.7

0.58

   Up to 6 years

63

84.0

8

12.7

 

   7-12 years

6

8.0

1

16.7

 

Occupation

     

   No laborerb

26

34.7

1

3.8

0.07

   Laborerc

49

65.3

9

18.4

 

bNon laborer = none occupation, student or housewife.

cLaborer = Employee, business, agriculture, construction worker, driver or other.

Table 2

Bivariate analysis of liver disease characteristics in patients and seropositivity to T. gondii infection.

 

No. of subjects tested

Prevalence of T. gondii infection

P value

Anti-T. gondii IgG levels >150 IU/ml

Characteristic

 

No.

%

 

No.

%

Diagnosis

      

   Acute hepatitis

1

0

0.0

 

-

 

   Chronic hepatitis

2

0

0.0

 

-

 

   Cirrhosis

67

9

13.4

0.89

5

55.6

   Steatosis

4

1

25.0

 

1

100

   Amoebic abscess

1

0

0.0

 

-

 

Alcohol related disease

      

   Yes

35

6

17.1

0.28

3

50

   No

40

4

10.0

 

3

75

Duration of disease

      

   Less than 1 year

30

5

16.7

0.35

3

60

   1 to 5 years

34

4

11.8

 

3

75

   More than 5 years

11

1

9.1

 

1

100

Treatment response

      

   Good

50

8

16.0

 

4

50

   Regular

4

1

25.0

 

1

100

   Bad

3

1

33.3

0.44

1

100

Table 3

Bivariate analysis of clinical data and infection with T. gondii in patients.

 

No. of subjects tested

Prevalence of T. gondii infection

P value

Characteristic

 

No.

%

 

Concomitant disease

    

   Yes

49

5

10.2

0.22

   No

26

5

19.2

 

Lymphadenopathy ever

    

   Yes

11

1

9.1

0.54

   No

64

9

14.1

 

Headache frequently

    

   Yes

25

3

12

0.55

   No

50

7

14

 

Blood transfusión

    

   Yes

50

6

12

0.44

   No

25

4

16

 

Transplantation

    

   Yes

4

0

0

0.55

   No

71

10

14.1

 

Surgery ever

    

   Yes

42

7

16.7

0.27

   No

33

3

9.1

 

Memory impairment

    

   Yes

32

4

12.5

0.56

   No

43

6

14

 

Reflex impairment

    

   Yes

18

5

27.8

0.05

   No

57

5

8.8

 

Hearing impairment

    

   Yes

48

6

12.5

0.51

   No

27

4

14.8

 

Visual impairment

    

   Yes

27

3

11.1

0.48

   No

48

7

14.6

 
Bivariate analysis showed a number of behavioral characteristics with a P value equal or less than 0.25 including cats at home, raising animals, traveling abroad, consumption of sheep, chicken, turkey, pigeon, rabbit, deer, squirrel, quail, skunk and armadillo meats, consumption of raw milk, ham, unwashed raw fruits, and untreated water, soil contact and soil floors at home. Multivariate analysis of these behavioral characteristics showed that consumption of sheep meat (OR = 8.69; 95% CI: 1.02-73.71; P = 0.04), rabbit meat (OR = 4.61; 95% CI: 1.06-19.98; P = 0.04), venison (OR = 40.46; 95% CI: 2.25-725.75; P < 0.01), and quail meat (OR = 38.50; 95% CI: 1.70-871.99; P < 0.01) were significantly associated with T. gondii infection in patients (Table 4). Other behavioral characteristics did not show an association with T. gondii infection. Raw data of patients and controls are included in additional files [additional file 1-cases and additional file 2-controls, respectively].
Table 4

Multivariate analysis of selected characteristics of patients and their association with T. gondii infection.

 

Raw numbers

   

Characteristic

Yes

No

Odds ratio

95% Confidence interval

P value

Cats at home

7/41

3/34

1.99

0.45 - 8.81

0.36

Raising animals

8/48

2/27

2.53

0.48 - 13.37

0.27

Traveling abroad

6/34

4/41

2.24

0.54 - 9.23

0.26

Sheep meat consumption

9/43

1/32

8.69

1.02 - 73.71

0.04

Chicken meat consumptiona

9/74

1/1

0.04

0.001-1.27

0.01

Turkey meat consumption

9/51

1/24

5.97

0.68 - 51.93

0.10

Pigeon meat consumption

3/12

7/63

2.42

0.46 - 12.69

0.29

Rabbit meat consumption

7/31

3/44

4.61

1.06 - 19.98

0.04

Venison consumptiona

10/36

0/39

40.46

2.25-725.75

<0.01

Squirrel meat consumption

5/24

5/51

2.46

0.59 - 10.29

0.21

Quail meat consumptiona

2/2

8/73

38.50

1.70-871.99

<0.01

Skunk meat consumption

2/5

8/70

3.11

0.43 - 22.39

0.25

Armadillo meat consumption

1/2

9/73

7.11

0.08-566.52

0.05

Raw milk consumption

6/31

4/44

2.26

0.56 - 8.99

0.24

Ham consumption

7/63

3/12

0.46

0.09 - 2.21

0.33

Unwashed raw fruits

5/24

5/51

2.4

0.60 - 9.58

0.21

Untreated water

9/47

1/28

6.73

0.75 - 60.49

0.08

Soil contact

9/53

1/22

3.86

0.45 - 33.17

0.21

Soil floor at home

4/16

6/59

2.35

0.51 - 10.72

0.26

aOdd ratios for these characteristics were calculated by adding 0.5 to each cell of the 2 × 2 table.

Discussion

In this seroprevalence case-control study, we found a comparable frequency of anti-T. gondii IgG and IgM antibodies in liver disease patients and controls. Similarly, levels of anti-T. gondii IgG antibodies were comparable among these groups indicating that T. gondii infection is not likely to substantially contribute to the etiology of liver disease in our patient population. We are not aware of previous reports about the association of T. gondii infection in liver disease patients in Mexico, and reports in other countries are scarce. Our results conflict with those reported in a Turkish study where researchers found an association of T. gondii infection with liver cirrhosis [15]. Most of our patients suffered from liver cirrhosis but we did not find any association between seropositivity to T. gondii and cirrhosis. Similarly, the comparable seroprevalence of T. gondii infection in patients and controls differs from those reported in an Egyptian study where researchers found a 65.5% seroprevalence of T. gondii antibodies in patients with acute and chronic hepatic diseases against a 27% seroprevalence found in controls [17]. Certainly, differences in the characteristics of the studies might explain the differences in the seroprevalences including the use of different laboratory methods and matching procedures, difference in ages of participants and proportions of controls and patients.

None of the socio-demographic characteristics and diagnosis of liver disease associated with T. gondii seropositivity in our patients. Concerning behavioral characteristics, it was noteworthy that there was an association between T. gondii seropositivity and sheep meat consumption (OR = 8.69; 95% CI: 1.02-73.71; P = 0.04). Infections with T. gondii have been reported in sheep [18]. In addition, viable T. gondii has been found in lambs destined for meat consumption in the USA [19], and ovine meat consumed in France [20]. It will therefore be of interest to examine the seroprevalence of T. gondii infection in sheep in Durango. In a recent study in the USA, elevated risk of recent T. gondii infection was associated with eating rare lamb [21]. Even frozen lamb meat has been associated with acute T. gondii infection in Brazil [22]. The association of T. gondii infection and consumption of sheep meat in our patients was unexpected since lamb meat consumption was negatively associated with T. gondii infection in a previous study in psychiatric patients in Durango [23]. We are not aware of any previous report about a positive association of T. gondii infection and consumption of sheep meat in Mexico. Remarkably, consumption of rabbit meat was also associated with T. gondii infection in patients (OR = 4.61; 95% CI: 1.06-19.98; P = 0.04). Infections with T. gondii in rabbits have been reported in several countries [2426]. Antibodies against T. gondii were found in 77 (26.9%) of 286 domestic rabbits from three rabbit farms in Mexico [25]. However, the seroprevalence of T. gondii infection in rabbits in Durango is unknown. To the best of our knowledge there is not any previous report about the association of T. gondii infection and consumption of rabbit meat. In the present study, we also found an association between T. gondii seropositivity and consumption of quail meat (P < 0.01). Experimental infections with T. gondii in bobwhite [27] and Japanese quail [28] have been reported. We are not aware of any previous epidemiological report about the association of T. gondii infection and consumption of quail meat. More expectedly, we observed an association between T. gondii seropositivity and consumption of venison (P = < 0.01). Infections with T. gondii have been reported in deer [29, 30]. Consumption of undercooked or uncooked venison has been linked to ocular toxoplasmosis in deer hunters [31]. Interestingly, toxoplasmosis with liver involvement has been reported in deer hunters who had eaten undercooked venison [32].

The frequency of T. gondii seropositivity was higher in patients with reflex impairment (27.8%) than patients without this impairment (8.8%), and this difference showed a borderline significance (P = 0.05). In a previous study in patients with visual impairment in Durango, we found that patients with reflex impairment had a significantly higher frequency of T. gondii infection than those with normal reflexes [33]. Reflex impairment might contribute to reducing the quality of life in T. gondii infected patients.

Conclusions

Seropositivity to T. gondii was comparable among liver disease patients and controls. Further studies with larger sample sizes are needed to elucidate the association of T. gondii with liver disease. Consumption of venison, and rabbit, sheep, and quail meats may warrant further investigation.

Funding

This study was supported by Fondos Mixtos Durango-Consejo Nacional de Ciencia y Tecnología, Mexico. Grant No. 66718.

Declarations

Authors’ Affiliations

(1)
Faculty of Medicine, Juárez University of Durango State
(2)
Mexican Social Security Institute
(3)
Institute for Scientific Research, Juárez University of Durango State
(4)
Institute for Microbiology and Hygiene, Campus Benjamin Franklin, Charité Medical School
(5)
Roche Molecular Diagnostics

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© Alvarado-Esquivel et al; licensee BioMed Central Ltd. 2011

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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