Open Access

Toxoplasma gondii infection in workers occupationally exposed to unwashed raw fruits and vegetables: a case control seroprevalence study

  • Cosme Alvarado-Esquivel1Email author,
  • Sergio Estrada-Martínez2 and
  • Oliver Liesenfeld3, 4
Parasites & Vectors20114:235

DOI: 10.1186/1756-3305-4-235

Received: 23 September 2011

Accepted: 16 December 2011

Published: 16 December 2011

Abstract

Background

Through a case control seroprevalence study, we sought to determine the association of Toxoplasma gondii infection with occupational exposure to unwashed raw fruits and vegetables.

Methods

Subjects, numbering 200, who worked growing or selling fruits and vegetables, and 400 control subjects matched by age, gender, and residence were examined by enzyme immunoassays for the presence of anti-Toxoplasma IgG and IgM antibodies. Socio-demographic, clinical, and behavioral characteristics from the study subjects were obtained.

Results

Of the 200 fruit and vegetable workers, 15 (7.5%) of whom, and 31 (7.8%) of the 400 controls were positive for anti-Toxoplasma IgG antibodies (P = 0.96). Anti-Toxoplasma IgM antibodies were found in 2 (1%) of the fruit workers and in 11 (2.8%) of the control subjects (P = 0.23). Seroprevalence of Toxoplasma antibodies increased with age (P = 0.0004). In addition, seropositivity to Toxoplasma was associated with ill status (P = 0.04), chronic tonsillitis (P = 0.03), and reflex impairment (P = 0.03). Multivariate analysis showed that Toxoplasma infection was associated with consumption of raw meat (OR = 5.77; 95% CI: 1.15-28.79; P = 0.03), unwashed raw fruits (OR = 2.50; 95% CI: 1.11-5.63; P = 0.02), and living in a house with soil floors (OR = 3.10; 95% CI: 1.22-7.88; P = 0.01), whereas Toxoplasma infection was negatively associated with traveling abroad (OR = 0.28; 95% CI: 0.12-0.67; P = 0.005).

Conclusions

This is the first report of seroprevalence and contributing factors for Toxoplasma infection in workers occupationally exposed to unwashed raw fruits and vegetables, and the results may help in the design of optimal preventive measures against Toxoplasma infection especially in female workers at reproductive age.

Keywords

Case-control study fruits workers occupational exposure seroprevalence epidemiology

Background

Toxoplasma gondii (T. gondii) infects humans worldwide [13]. Infections with T. gondii may result in asymptomatic latent infections or lymph node, ocular, or central nervous system disease [13]. We have been studying the epidemiology of T. gondii infection in humans [49] and other animals [10, 11] in Durango, Mexico. Occupational exposure to parasite tissue cysts [12, 13] and oocysts [13, 14] in some population groups has been evaluated. Infections with T. gondii have been associated with the consumption of unwashed raw fruits and vegetables contaminated with oocysts in several countries [1520]. Therefore, occupational exposure to unwashed raw fruits and vegetables could represent a hazard for T. gondii infection. To our knowledge, an association between occupational exposure to unwashed raw fruits and vegetables and T. gondii infection has not been evaluated. Therefore, through a case control exploratory study we sought to determine (1) the seroprevalence and levels of anti-T. gondii IgG antibodies in workers occupationally exposed to unwashed raw fruits and vegetables in Durango, Mexico, (2) the association of seropositivity to T. gondii with occupational exposure to unwashed raw fruits and vegetables, and (3) socio-demographic, clinical, and behavioral characteristics associated with T. gondii seropositivity in workers occupationally exposed to unwashed raw fruits and vegetables.

Methods

Study design and study populations

Through a case-controlled seroprevalence study design, we assessed the association of T. gondii infection with occupational exposure to unwashed raw fruits and vegetables in workers occupationally exposed to unwashed raw fruits and vegetables and control subjects in Durango, Mexico from December 2009 to November 2011.

Workers occupationally exposed to unwashed raw fruits and vegetables

The subjects, 200 in number, who worked growing (n = 100) or selling (n = 100) fruits or vegetables were included in the study. Workers selling fruits and vegetables worked in 40 fruit and vegetable shops in the 3 largest fruit markets in Durango City. These 3 markets sell fruits and vegetables to wholesalers and retailers and are the main distributors of fruits and vegetables in Durango State. Inclusion criteria for workers occupationally exposed to fruits and vegetables were: 1) to have been currently working in fruit shops or growing fruits and vegetables for at least 6 months, 2) aged 15 years and older, 3) any gender; 4) any socioeconomic level, and 5) who accepted to participate in the study. Of the 200 workers occupationally exposed to unwashed raw fruits and vegetables, 155 (77.5%) were male and 45 (22.5%) were female. The mean age of the workers was 42.13 ± 18.84 years old (range, 15-86 years).

Control subjects

Control subjects, who numbered 400, matched with workers by age, gender, and residence were included in the study. The mean age in controls was 42.13 ± 18.83 (range: 15-88) and comparable with that in workers (P = 1.00). Control subjects were obtained from the general population of Durango, Mexico.

Ethical aspects

The study was approved by the Ethical Committee of the Faculty of Medicine in Durango City. 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 the characteristics of the participants with the aid of a standardized questionnaire. Socio-demographic data included age, gender, place of birth, place of residence, residence area (urban, suburban, rural), educational level, and socioeconomic status. Contributing and confounding risk factors of behavioral data from all participants were also obtained. These factors included animal contacts, contact with cat feces, travellling in Mexico and abroad, meat consumption (pork, beef, goat, sheep, boar, chicken, turkey, pigeon, rabbit, venison, squirrel, horse, opossum, or other), degree of meat cooking, consumption of unpasteurized milk, dried or cured meat (ham, sausages, salami, or chorizo), unwashed raw vegetables, fruits, or untreated water, contact with soil (gardening or agriculture), and type of floors at home. Questions regarding contributing and confounding risk factors of behavioral data from all participants refer to "in their entire life". Clinical data included current suffering from any disease, presence or history of lymphadenopathy, frequent presence of headaches; history of blood transfusion, transplantation or surgery; and memory, reflex, hearing, and visual impairments.

Laboratory tests

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

Statistical analysis

Results were analyzed with the aid of the software 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 the groups, the Yates Corrected Test and when indicated the Fisher Exact Test, were used. Bivariate and multivariate analyses were used to evaluate the association between the characteristics of the subjects and T. gondii infection. Variables were included in the multivariate analysis if they had a P value equal to or less than 0.20 in the bivariate analysis. Odd ratio (OR) and 95% confidence interval (CI) were calculated by multivariate analysis using multiple, unconditional, logistic regression. A P value less than 0.05 was considered statistically significant.

Results

Of the 200 fruit and vegetable workers, 15 (7.5%) of whom and 31 (7.8%) of the 400 controls were positive for anti-T. gondii IgG antibodies. No statistically significant difference (P = 0.96) in seroprevalence of anti-T. gondii IgG antibodies between the groups was found. Anti-T. gondii IgG antibody levels were obtained from 12 of 15 seropositive fruit workers and from 26 of 31 seropositive control subjects. Of the 12 seropositive fruit workers, 8 (66.7%) of whom and 18 (69.2%) of the 26 seropositive controls had high levels (> 150 IU/ml) of anti-T. gondii IgG antibodies with no statistically significant difference among the groups (P = 0.84). Anti-T. gondii IgM antibodies were found in 2 (1%) of the fruit workers and in 11 (2.8%) of the control subjects. No statistically significant difference (P = 0.23) in seroprevalence of anti-T. gondii IgM antibodies between the groups was found. Seroprevalence of T. gondii infection in workers growing fruits and vegetables was comparable (P = 0.59) with that found in workers of fruit shops (9% vs 6%, respectively). Seroprevalence of T. gondii infection was comparable among workers of the 3 fruit markets: 3 of 34 (8.8%), 5 of 60 (8.3%), and 1 of 6 (16.7%) (P = 0.79). Seropositive workers were found in 7 (17.5%) of the 40 fruit shops studied.

General socio-demographic characteristics of the workers occupationally exposed to unwashed raw fruits and vegetables and control subjects are shown in Table 1. Seroprevalence of T. gondii antibodies increased with age in all groups. Other socio-demographic characteristics including gender, birth place, residence, educational level, and socioeconomic status did not show an association with T. gondii seropositivity.
Table 1

Socio-demographic characteristics of the study populations and seroprevalence of T. gondii infection.

 

Fruit and vegetable workers (n = 200)

Controls (n = 400)

All (n = 600)

   

Prevalence of

   

Prevalence of

   

Prevalence of

 
   

T. gondii infection

P

  

T. gondii infection

P

  

T. gondii infection

P

Characteristic

No.

%

No.

%

value

No.

%

No.

%

value

No.

%

No.

%

value

Age groups (years)

               

   30 or less

74

37.0

4

5.4

0.06

148

37

10

6.8

0.001

222

37.0

14

6.3

0.0004

   31-50

60

30.0

2

3.3

 

120

30

3

2.5

 

180

30.0

5

2.8

 

   51-70

41

20.5

7

17.1

 

84

21

8

9.5

 

125

20.8

15

12

 

   > 70

25

12.5

2

8.0

 

48

12

10

20.8

 

73

12.2

12

16.4

 

Gender

               

   Male

155

77.5

12

7.7

1.00

310

77.5

27

8.7

0.26

465

77.5

39

8.4

0.29

   Female

45

22.5

3

6.7

 

90

22.5

4

4.4

 

135

22.5

7

5.2

 

Birth place

               

   Durango State

165

90.2

10

6.1

0.33

351

88.4

25

7.1

0.32

516

89.0

35

6.8

0.22

   Other Mexican states

18

9.8

2

11.1

 

45

11.3

6

13.3

 

63

10.9

8

12.7

 

   Abroad

-

    

1

0.3

0

0.0

 

1

0.2

0

0

 

Residence place

               

   Durango State

198

99.0

15

7.6

1.00

391

98.5

30

7.7

0.56

589

98.7

45

7.6

0.77

   Other Mexican states

2

1.0

0

0.0

 

5

1.3

1

20.0

 

7

1.2

1

14.3

 

   Abroad

-

    

1

0.3

0

  

1

0.2

0

0

 

Residence area

               

   Urban

132

67.3

9

6.8

0.42

300

77.5

23

7.7

0.88

432

74.1

32

7.4

0.56

   Suburban

9

4.6

0

0.0

 

24

6.2

2

8.3

 

33

5.7

2

6.1

 

   Rural

55

28.1

6

10.9

 

63

16.3

6

9.5

 

118

20.2

12

10.2

 

Educational level

               

   No education

15

7.5

2

13.3

0.56

16

4

3

18.8

0.22

31

5.2

5

16.1

0.20

   1-6 years

100

50.0

9

9.0

 

104

26.2

8

7.7

 

204

34.2

17

8.3

 

   7-12 years

66

33.0

3

4.5

 

141

35.5

13

9.2

 

207

34.7

16

7.7

 

   > 12 years

19

9.5

1

5.3

 

136

34.3

7

5.1

 

155

26.0

8

5.2

 

Socio-economic level

               

   Low

83

44.1

6

7.2

1.00

124

31.7

10

8.1

1.00

207

35.8

16

7.7

0.89

   Medium

105

55.9

8

7.6

 

267

68.3

21

7.9

 

372

64.2

29

7.8

 
With respect to clinical characteristics (Table 2), the seroprevalence of T. gondii infection was significantly (P = 0.04) higher in ill (11.8%) than in healthy (5.3%) control subjects. Seropositive subjects suffered from various underlying diseases including diabetes, arterial hypertension, spinal disease, chronic tonsillitis, and other diseases. However, chronic tonsillitis was the only disease associated with T. gondii seropositivity. The seroprevalence of T. gondii infection was significantly (P = 0.03) higher in patients with chronic tonsillitis (2/3; 66.7%) than that (15/154; 9.7%) in patients with other diseases. In control subjects, the seroprevalence of T. gondii infection was significantly (P = 0.03) higher in those suffering from reflex impairment (15.9%) than those without this clinical characteristic (6.2%). In the entire population (cases and controls), the seroprevalence of T. gondii infection was also significantly (P = 0.03) higher in subjects suffering from reflex impairment (14.9%) than those without this clinical feature (6.8%). Other clinical characteristics including presence or history of lymphadenopathy, frequent presence of headaches; history of blood transfusion, transplantation or surgery; and memory, hearing, and visual impairments did not show an association with T. gondii seropositivity.
Table 2

Bivariate analysis of clinical data and infection with T. gondii in fruit and vegetable workers and controls.

 

Workers (n = 200)

Controls (n = 400)

All (n = 600)

 

No. of

Prevalence of

 

No. of

Prevalence of

 

No. of

Prevalence of

 
 

subjects

T. gondii infection

P

subjects

T. gondii infection

P

subjects

T. gondii infection

P

Characteristic

tested

No.

%

value

tested

No.

%

value

tested

No.

%

value

Health status

            

   Healthy

113

11

9.7

0.53

266

14

5.3

0.04

379

25

6.6

0.13

   Ill

47

4

8.5

 

110

13

11.8

 

157

17

10.8

 

Lymphadenopathy ever

            

   Yes

30

3

10.0

0.46

68

4

5.9

0.44

98

7

7.1

0.93

   No

115

9

7.8

 

296

22

7.4

 

411

31

7.5

 

Headaches frequently

            

   Yes

37

5

13.5

0.15

104

7

6.7

0.93

141

12

8.5

0.77

   No

109

7

6.4

 

262

20

7.6

 

371

27

7.3

 

Blood transfusion

            

   Yes

23

3

13.0

0.24

33

1

3.0

0.49

56

4

7.1

1.00

   No

176

12

6.8

 

365

30

8.2

 

541

42

7.8

 

Transplantation

            

   Yes

0

0

0.0

-

1

0

0.0

1.00

1

0

0

1.00

   No

194

15

7.7

 

397

31

7.8

 

591

46

7.8

 

Surgery ever

            

   Yes

60

7

11.7

0.63

165

15

9.1

0.35

225

22

9.8

0.25

   No

99

8

8.1

 

200

12

6.0

 

299

20

6.7

 

Memory impairment

            

   Yes

49

7

14.3

0.11

75

6

8.0

0.99

124

13

10.5

0.30

   No

115

8

7.0

 

306

22

7.2

 

421

30

7.1

 

Reflex impairment

            

   Yes

30

4

13.3

0.28

44

7

15.9

0.03

74

11

14.9

0.03

   No

134

11

8.2

 

337

21

6.2

 

471

32

6.8

 

Hearing impairment

            

   Yes

31

3

9.7

0.54

63

6

9.5

0.43

94

9

9.6

0.61

   No

127

11

8.7

 

320

22

6.9

 

447

33

7.4

 

Visual impairment

            

   Yes

66

5

7.6

0.98

164

17

10.4

0.07

230

22

9.6

0.18

   No

91

8

8.8

 

219

11

5.0

 

310

19

6.1

 
Bivariate analysis showed a number of behavioral characteristics with a P value equal to or less than 0.20 including cats at home, soil floors at home, traveling abroad, consumption of boar, pigeon, deer, and squirrel meats, consumption of raw meat and unwashed raw fruits, and consumption of ham and salami. Results of multivariate analysis of selected behavioral characteristics are shown in Table 3. Seropositivity to T. gondii was associated with consumption of raw meat (OR = 5.77; 95% CI: 1.15-28.79; P = 0.03) and unwashed raw fruits (OR = 2.50; 95% CI: 1.11-5.63; P = 0.02), and living in a house with soil floors (OR = 3.10; 95% CI: 1.22-7.88; P = 0.01), whereas traveling abroad was negatively associated with T. gondii seropositivity (OR = 0.28; 95% CI: 0.12-0.67; P = 0.005). Other behavioral characteristics including consumption of any type of meat; unpasteurized milk, untreated water, unwashed raw vegetables; or contact with cats or other animals did not show any association with T. gondii seropositivity.
Table 3

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

 

Adjusted

95%

 
 

odds

Confidence

P

Characteristic a

ratio b

interval

value

Cats at home

1.62

0.78-3.39

0.19

Travel abroad

0.28

0.12-0.67

0.005

Boar meat consumption

1.41

0.46-4.26

0.53

Pigeon meat consumption

1.48

0.56-3.91

0.41

Venison consumption

0.86

0.36-2.07

0.75

Squirrel meat consumption

1.27

0.49-3.25

0.61

Raw meat consumption

5.77

1.15-28.79

0.03

Ham consumption

0.60

0.17-2.13

0.43

Salami consumption

0.64

0.29-1.43

0.28

Unwashed raw fruits

2.50

1.11-5.63

0.02

Soil floor at home

3.10

1.22-7.88

0.01

aThe variables included were those with a p < 0.20 obtained in the bivariate analysis.

bAdjusted by age and the rest of characteristics included in this Table.

Discussion

We found comparable seroprevalences and levels of anti-T. gondii IgG antibodies and seroprevalences of anti-T. gondii IgM antibodies among workers occupationally exposed to unwashed raw fruits and vegetables and their controls. Although unwashed raw fruits and vegetables could be contaminated with T. gondii, our results suggest that handling of these products seems not to be a major occupational risk for T. gondii infection. The lack of association of T. gondii seropositivity with exposure to fruits and vegetables could probably be explained by both a low frequency and a low concentration of oocysts in the fruits and vegetables handled. In addition, there is no direct entry of T. gondii into the body by handling fruits or vegetables as occurs by eating these products. Presence of oocysts in fruits may depend on contact of fruits with contaminated soil. Therefore, the low frequency of T. gondii seropositivity in our fruit workers might also be explained by the fact that workers collect fruits more frequently from trees than from the soil. Other factors might be involved in T. gondii transmission in fruit workers including frequency of eating fruits and vegetables, washing hands before eating, or other unknown factors. Further research to evaluate the association of T. gondii infection with occupational exposure to unwashed raw fruits and vegetables is needed.

Results of the present study indicate that some factors including consumption of raw meat and unwashed raw fruits, and living in a house with soil floors play a more important contributing role in T. gondii infection than handling unwashed raw fruits and vegetables. Multivariate analysis showed that seropositivity to T. gondii was associated with consumption of raw meat. Eating raw meat is a major cause of T. gondii infection [1, 3]. Moreover, multivariate analysis showed that consumption of unwashed raw fruits was associated with T. gondii infection. Remarkably, we have repeatedly found an association of T. gondii infection with consumption of unwashed raw fruits in Durango, Mexico. In a previous study of psychiatric patients, we found a positive association of T. gondii infection with unwashed raw fruit consumption [4]. Similarly, in a recent study, an association between T. gondii infection and consumption of unwashed fruits was found in workers occupationally exposed to water, sewage, and soil [13]. Our results suggest that occupational exposure to raw fruits and vegetables per se does not seem to contribute substantially in increasing the seroprevalence of T. gondii infection, but seroprevalence increases substantially when eating unwashed raw fruits. It is known that T. gondii infection can be prevented in large part by peeling or thoroughly washing fruits and vegetables before eating [21]. Consumption of unwashed raw fruit has epidemiological concern in fruit workers especially in female fruit workers during the reproductive age.

Contaminated fruits and vegetables may represent a risk of infection in animals consumed by humans. Unwashed raw fruits and vegetables are frequently used to feed pigs in backyards in Durango. In fact, in a recent study, serological evidence of T. gondii infection in pigs in Durango was reported [11]. Furthermore, in the present work, an association between T. gondii infection and soil floors at home was found. In a previous study of pregnant women attending a public hospital in Durango City, we found that T. gondii infection was associated with living in a house with soil floors [5]. In a further study of pregnant women of 9 communities in rural Durango State, a similar association was found [7]. Therefore, our results confirm that living in a house with soil floors contributes to the increase in seroprevalence of T. gondii infection in Durango State. In contrast, our study showed that T. gondii infection was negatively associated with travelling abroad. This finding suggests that most T. gondii infections may have been acquired in Mexico.

The seroprevalence of T. gondii infection increased significantly with age in the subjects studied. This finding follows a typical tendency of infection in humans as reported elsewhere [3, 9]. In general, the seroprevalence of T. gondii infection was higher in ill than in healthy subjects. In particular, the seroprevalence of T. gondii infection was higher in patients with chronic tonsillitis than in patients with other diseases. There is scarce and conflicting information in the role of T. gondii in the etiology of tonsillitis [22, 23]. In the present study, there were few cases of chronic tonsillitis; hence, further research with a larger sample size should be conducted to determine the association of T. gondii with chronic tonsillitis.

Remarkably, the seroprevalence of T. gondii infection was higher in subjects with reflex impairment than in those without this clinical feature. This finding agrees with those reported in 2 previous studies in Durango, Mexico. In a first study of patients with vision impairment, those with reflex impairment had a significantly higher frequency of T. gondii infection than those with normal reflexes [24]. In a second study of patients suffering from liver disease, the seroprevalence of T. gondii infection was higher in those with reflex impairment than in those without this impairment [8]. Several reports indicate that T. gondii infection may affect the reaction time in infected individuals. In a double blind study, Havlícek et al [25] reported significantly longer reaction times of subjects with latent toxoplasmosis in comparison with those of controls. Novotná et al [26] reported that heterozygous men with both the RhD plus and the RhD minus alleles were protected against prolongation of reaction times caused by infection with T. gondii. In a further study of men and women, Flegr et al [27] confirmed that RhD-positive subjects were less sensitive to the influence of latent toxoplasmosis on reaction times than RhD-negative subjects. In the present study, the associations of T. gondii seropositivity with several clinical characteristics including ill status, chronic tonsillitis, and reflex impairment suggest that T. gondii infection is impacting the health of our population.

Conclusions

This is the first report of contributing factors for T. gondii infection in workers occupationally exposed to unwashed raw fruits and vegetables. The results may help in the design of optimal preventive measures.

Declarations

Acknowledgements

This study was supported by The Faculty of Medicine and Nutrition, Universidad Juárez del Estado de Durango, Durango City, Mexico. Authors thank Dr. J. P. Dubey for his valuable suggestions for editing the manuscript.

Authors’ Affiliations

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

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