Introduction

The parasite Toxoplasma gondii (T. gondii) is a zoonotic pathogen belonging to apicomplexan parasites [1]. Infections of this parasite occur widely around the world [2]. It is estimated that about 30% of people are seropositive to T. gondii worldwide [3]. Cats and other Felidae are the definitive hosts of T. gondii, whereas a wide variety of warm-blooded animals, including humans, are intermediate hosts [4]. Humans can become infected with T. gondii through ingestion of oocyst-contaminated soil and water, tissue cysts in undercooked meat, or congenitally [5]. Infections with T. gondii are usually asymptomatic, but the parasite may induce severe disease in fetuses and immunocompromised patients [6]. Furthermore, T. gondii can cause posterior uveitis with vision loss [7]. Infection with T. gondii has also been linked to an increased incidence of several psychiatric diseases [8]. Chronic infections with T. gondii have been more recently linked to behavioral changes [9]. Suicide attempters have shown a higher seroprevalence of T. gondii infection than healthy controls [10]. In addition, infections with T. gondii have been linked to traffic [11, 12] and work accidents [13].

To the best of our knowledge, there have not been any studies done on the seroepidemiology of T. gondii infection in people with alcohol consumption. We believe it is important to study the seroepidemiology of T. gondii infection in this population group because alcohol consumption has been linked to infection with T. gondii in several studies. Seropositivity to T. gondii was associated with alcohol consumption in patients with heart disease [14]. In two studies of decedents in Poland, researchers found a positive association between T. gondii seropositivity and the presence of alcohol in the blood [15, 16]. In addition, alcohol consumption leads to an impaired immune response and dysregulated inflammatory state that contributes to an increased risk for infection [17]. On the other hand, infection with T. gondii has been associated with depression [18, 19], an illness that may lead to alcohol consumption. Therefore, we see a need to study the magnitude of infection with T. gondii and the factors associated with this infection in people with alcohol consumption. In this study, we sought to determine the seroprevalence of T. gondii infection in alcohol consumers in the northern Mexican city of Durango, and the T. gondii seroprevalence association with sociodemographic, clinical, and behavioral characteristics of the population studied.

Materials and methods

Results

Most participants were female (65.7%) and were born in the state of Durango (89.8%). Mean age of participants was 39.4±14.0 years (range: 15–93 years). Of the 1544 people surveyed, 173 (11.2%) were positive for anti-T. gondii IgG antibodies. Of these 173 seropositive individuals, 82 (47.4%) had anti-T. gondii IgG levels between 8 to 99 IU/ml, 15 (8.7%) between 100 to 150 IU/ml, and 76 (43.9%) higher than 150 IU/ml. We were able to test 167 of the 173 anti-T. gondii IgG positive sera for anti-T. gondii IgM antibodies. Fifty-five (32.9%) of these 167 serum samples were positive for anti-T. gondii IgM antibodies. Table 1 shows the sociodemographic and housing data of participants and the seroprevalence of T. gondii infection. Bivariate analysis showed that the sociodemographic characteristics gender, residence area, educational level, occupation, and socioeconomic status were significantly (P<0.05) associated with T. gondii IgG seropositivity, whereas the variables age group, birthplace, and place of residence showed P values higher than 0.05 in the bivariate analysis. Concerning housing characteristics, bivariate analysis showed that availability of potable water, type of flooring, form of elimination of excretes, and education of the head of the family were significantly (P<0.05) associated with T. gondii IgG seropositivity. Overcrowding was not associated with T. gondii seropositivity. Bivariate analysis showed that the clinical conditions visual impairment, history of surgery, and hepatitis were negatively associated (P<0.05) with T. gondii infection. Whereas other clinical variables as presence of any disease, dizziness, frequent abdominal pain or headache, impairments in memory, reflexes, and hearing, and history of blood transfusion, organ transplantation, and lymphadenopathy, showed P values higher than 0.05 in the bivariate analysis. Of the obstetric characteristics of women, only the variable of pregnancy history was significantly (P<0.05) associated with T. gondii IgG seropositivity. Table 2 shows the clinical data of participants and the seroprevalence of T. gondii infection.

Table 1

Socio-demographic and housing characteristics of participants and seroprevalence of T. gondii infection.

Characteristic	Participants tested No.	Prevalence of T. gondii infection		P value
		No.	%
Age groups (years)
30 or less	460	39	8.5	0.07
31–50	746	90	12.1
>50	338	44	13.0
Gender
Male	530	90	17.0	0.00
Female	1014	83	8.2
Birthplace
Durango State	1387	148	10.7	0.06
Other Mexican State	151	25	16.6
Abroad	6	0	0.0
Residence place
Durango State	1532	171	11.2	0.71
Other Mexican State	11	2	18.2
Abroad	1	0	0.0
Residence area
Urban	1200	86	7.2	0.00
Suburban	190	29	15.3
Rural	154	58	37.7
Educational level
No education	22	8	36.4	0.00
1 to 6 years	248	65	26.2
7–12 years	773	71	9.2
>12 years	501	29	5.8
Occupation
Agriculture	36	6	16.7	0.00
Housewife	401	53	13.2
Business	94	7	7.4
Construction	11	1	9.1
Employee	386	30	7.8
Student	97	4	4.1
Cattle raising	4	0	0.0
Day laborer	7	1	14.3
Factory worker	27	3	11.1
Professional	238	10	4.2
Miner	67	42	62.7
Sex worker	27	3	11.1
None	43	1	2.3
Other	106	12	11.3
Socio-economic level
Low	353	62	17.6	0.00
Medium	1184	109	9.2
High	7	2	28.6
Floor at home
Ceramic or wood	932	75	8.0	0.00
Concrete	578	86	14.9
Soil	32	12	37.5
Availability of potable water
In the home	1195	86	7.2	0.00
In the land	24	4	16.7
In the street	194	60	30.9
Toilet facilities
Sewage pipes	1304	92	7.1	0.00
Latrine or another	122	58	47.5
Crowding at home
No	579	52	9.0	0.05
Semi-crowded	538	57	10.6
Overcrowded	277	40	14.4
Education of the head of family
Seven years or more	920	60	6.5	0.00
Four to six years	360	57	15.8
Up to 3 years	140	35	25.0

Table 2

Bivariate analysis of clinical data and infection with T. gondii in people with alcohol consumption.

Characteristic	Subjects tested No.	Prevalence of T. gondii infection		P value
		No.	%
Clinical status
Healthy	1093	127	11.6	0.46
Ill	446	46	10.3
Lymphadenopathy ever
Yes	412	40	9.7	0.24
No	1126	133	11.8
Abdominal pain
Yes	503	49	9.7	0.20
No	1039	124	11.9
Headache frequently
Yes	768	89	11.6	0.64
No	774	84	10.9
Memory impairment
Yes	597	60	10.1	0.29
No	942	111	11.8
Dizziness
Yes	448	55	11.3	0.97
No	1053	118	11.2
Reflexes impairment
Yes	257	29	11.3	0.97
No	1285	144	11.2
Hearing impairment
Yes	233	27	11.6	0.84
No	1310	146	11.1
Visual impairment
Yes	577	51	8.8	0.02
No	965	122	12.6
Surgery ever
Yes	892	87	9.8	0.03
No	650	86	13.2
Transplantation
Yes	3	0	0	1.00
No	1538	173	11.2
Blood transfusion
Yes	206	25	12.1	0.65
No	1335	148	11.1
Hepatitis
Yes	88	4	4.5	0.04
No	1454	169	11.6
Pregnancies
Yes	850	77	9.1	0.03
No	150	6	4.0
Deliveries
Yes	609	61	10.0	0.13
No	239	16	6.7
Cesarean sections
Yes	382	37	9.7	0.57
No	466	40	8.6
Miscarriages
Yes	284	28	9.9	0.58
No	562	49	8.7
Stillbirths
Yes	49	6	12.2	0.43
No	789	70	8.9

With respect to behavioral characteristics, bivariate analysis showed many variables associated with T. gondii seropositivity. Table 3 shows all behavioral characteristics significantly associated with T. gondii seropositivity in the bivariate analysis. The variables domestic travel, consumption of beef, mutton, chicken, turkey or horsemeat, frequency of meat consumption, degree of meat cooking, consumption of dried meat, sausages, and frequency of eating away from home were not associated with T. gondii seropositivity. Logistic regression analysis showed that T. gondii seropositivity was associated with the following variables: consumption of armadillo meat (OR = 2.33; 95% CI: 1.04–5.22; P = 0.03), and the use of latrines for elimination of excretes (OR = 2.27; 95% CI: 1.07–4.80; P = 0.03) (Table 4). Other sociodemographic, housing, or behavioral variables included in our study were not associated with T. gondii seropositivity by logistic regression analysis.

Table 3

Bivariate analysis of selected behavioral factors and infection with T. gondii in the population studied.

Characteristic	Subjects tested No.	Prevalence of T. gondii infection		P value
		No.	%
Cats at home
Yes	543	89	16.4	0.00
No	999	84	8.4
Cats in the neighborhood
Yes	1011	127	12.6	0.02
No	531	46	8.7
Cleaning cat excrement
Yes	400	57	14.3	0.02
No	1134	115	10.1
Birds at home
Yes	480	70	14.6	0.005
No	1061	103	9.7
Raising farm animals
Yes	423	87	20.6	0.00
No	1119	86	7.7
Traveled abroad
Yes	430	31	7.2	0.002
No	1112	142	12.8
Goat meat consumption
Yes	312	71	22.8	0.00
No	1227	102	8.3
Boar meat consumption
Yes	167	59	35.3	0.00
No	1372	114	8.3
Pigeon meat consumption
Yes	129	47	36.4	0.00
No	1411	126	8.9
Duck meat consumption
Yes	104	23	22.1	0.00
No	1435	150	10.5
Quail meat consumption
Yes	117	36	30.8	0.00
No	1423	137	9.6
Rabbit meat consumption
Yes	346	62	17.9	0.00
No	1194	111	9.3
Venison consumption
Yes	405	89	22.0	0.00
No	1134	83	7.3
Squirrel meat consumption
Yes	155	48	31.0	0.00
No	1384	125	9.0
Opossum meat consumption
Yes	60	30	50.0	0.00
No	1478	142	9.6
Armadillo meat consumption
Yes	72	40	55.6	0.00
No	1467	133	9.1
Iguana meat consumption
Yes	49	17	34.7	0.00
No	1492	156	10.5
Snake meat consumption
Yes	200	36	18.0	0.001
No	1341	137	10.2
Fish consumption
Yes	1380	163	11.8	0.03
No	161	10	6.2
Skunk meat consumption
Yes	22	11	50.0	0.00
No	1522	162	10.6
Chorizo consumption
Yes	1395	164	11.8	0.04
No	147	9	6.1
Consumption of cow brain
Yes	287	45	15.7	0.008
No	1257	128	10.2
Liver consumption
Yes	883	118	13.4	0.00
No	546	34	6.2
Cow raw milk consumption
Yes	468	76	16.2	0.00
No	1076	97	9.0
Goat raw milk consumption
Yes	37	12	32.4	0.00
No	1507	161	10.7
Unwashed raw vegetables
Yes	325	69	21.2	0.00
No	1219	104	8.5
Unwashed raw fruits
Yes	414	81	19.6	0.00
No	1128	92	8.2
Untreated water
Yes	564	99	17.6	0.00
No	976	74	7.6
Tobacco consumption
Yes	727	97	13.3	0.01
No	817	76	9.3
Drug use
Yes	159	27	17.0	0.01
No	1383	146	10.6
Sexual promiscuity
Yes	193	39	20.2	0.00
No	1346	133	9.9
Soil contact
Yes	899	124	13.8	0.00
No	642	49	7.6
Washing hands before eating
Yes	1448	153	10.6	0.001
No	91	20	22.0

Table 4

Multivariate analysis of selected characteristics of people with alcohol consumption and their association with T. gondii infection.

Characteristic	Odds ratio	95% confidence interval	P value
Gender (male)	1.10	0.74–1.92	0.45
Residence area (area)	1.70	0.37–7.98	0.48
Educational level (no education)	1.00	0.24–4.21	0.97
Occupation (none)	0.25	0.03–1.98	0.19
Socioeconomic level (low)	1.44	0.91–2.26	0.11
Cats at home (yes)	1.48	0.92–2.36	0.09
Cats in the neighborhood (yes)	0.83	0.52–1.34	0.45
Cleaning cat excrement (yes)	0.90	0.55–1.47	0.69
Birds at home (yes)	1.11	0.71–1.75	0.63
Raising farm animals (yes)	1.51	0.94–2.43	0.08
Traveled abroad (yes)	0.68	0.4–1.16	0.16
Goat meat consumption (yes)	0.95	0.55–1.66	0.87
Boar meat consumption (yes)	1.44	0.73–2.84	0.28
Pigeon meat consumption (yes)	1.08	0.52.31	0.84
Duck meat consumption (yes)	1.24	0.56–2.74	0.59
Quail meat consumption (yes)	1.31	0.622.74	0.47
Rabbit meat consumption (yes)	0.92	0.52–1.62	0.77
Venison consumption (yes)	1.41	0.82–2.43	0.21
Squirrel meat consumption (yes)	1.28	0.65–2.49	0.46
Opossum meat consumption (yes)	0.95	0.37–2.45	0.93
Armadillo meat consumption (yes)	2.33	1.04–5.22	0.03
Iguana meat consumption (yes)	1.56	0.63–3.87	0.33
Snake meat consumption (yes)	0.64	0.34–1.22	0.18
Fish consumption (yes)	1.21	0.56–2.60	0.62
Skunk meat consumption (yes)	1.09	0.27–4.42	0.89
Chorizo consumption (yes)	1.42	0.58–3.48	0.43
Consumption of cow brain (yes)	0.95	0.55–1.64	0.86
Liver consumption (yes)	1.37	0.84–2.25	0.20
Cow raw milk consumption (yes)	0.89	0.56–143	0.65
Goat raw milk consumption (yes)	0.47	0.14–1.54	0.21
Unwashed raw vegetables (yes)	1.46	0.76–2.79	0.24
Unwashed raw fruits (yes)	0.69	0.35–1.35	0.28
Untreated water (yes)	1.40	0.87–2.23	0.15
Tobacco consumption (yes)	1.21	0.79–1.85	0.35
Drug use (yes)	0.82	0.43–1.57	0.55
Sexual promiscuity (yes)	1.07	0.6–1.89	0.80
Soil contact (yes)	0.99	0.62–1.56	0.96
Washing hands before eating (yes)	1.02	0.46–2.23	0.95
Floor at home (soil)	0.78	0.25–2.42	0.66
Availability of potable water (in the street)	1.69	0.92–3.10	0.08
Toilet facilities (latrine)	2.27	1.07–4.80	0.03
Education of the head of family (up to 3 years)	1.26	0.68–2.33	0.44

Our final task was to determine the association between high (>150 IU/ml) anti-T. gondii IgG antibody levels and the sociodemographic, housing, and behavioral characteristics of participants. Bivariate analysis showed that several variables are associated (P<0.05) with high (>150 IU/ml) anti-T. gondii IgG antibody levels. The variables associated with high anti-T. gondii IgG antibody levels by bivariate analysis were selected for further analysis by logistic regression analysis (Table 5). This additional analysis showed that high anti-T. gondii IgG antibodies were associated only with consumption of armadillo meat (OR = 2.25; 95% CI: 1.01–5.02; P = 0.04) and crowding at home (OR = 1.63; 95% CI: 1.02–2.61; P = 0.03).

Table 5

Multivariate analysis of selected characteristics of people with alcohol consumption and their association with high (>150 IU/ml) anti-T. gondii IgG antibodies.

Characteristic	Odds ratio	95% confidence interval	P value
Age (more than 50 years)	1.07	0.63–1.84	0.78
Gender (male)	1.2	0.75–1.90	0.43
Residence area (rural)	1.25	0.59–2.67	0.55
Educational level (no education)	0.99	0.22–4.31	0.99
Occupation (none)	0.24	0.03–1.86	0.17
Socioeconomic level (low)	1.31	0.84–2.06	0.22
Cats at home (yes)	1.49	0.98–2.25	0.05
Raising farm animals (yes)	1.48	0.94–2.33	0.08
Traveled abroad (yes)	0.69	0.41–1.18	0.18
Goat meat consumption (yes)	0.9	0.52–1.57	0.73
Boar meat consumption (yes)	1.34	0.68–2.64	0.38
Pigeon meat consumption (yes)	1.04	0.49–2.20	0.91
Duck meat consumption (yes)	1.16	0.52–2.58	0.7
Quail meat consumption (yes)	1.32	0.63–2.75	0.44
Rabbit meat consumption (yes)	0.92	0.52–1.61	0.78
Venison consumption (yes)	1.48	0.86–2.54	0.14
Squirrel meat consumption (yes)	1.32	0.68–2.55	0.4
Opossum meat consumption (yes)	0.83	0.33–2.07	0.7
Armadillo meat consumption (yes)	2.25	1.01–5.02	0.04
Iguana meat consumption (yes)	1.48	0.60–3.64	0.39
Snake meat consumption (yes)	0.64	0.34–1.20	0.16
Skunk meat consumption (yes)	1.12	0.29–4.36	0.86
Chorizo consumption (yes)	1.45	0.59–3.58	0.4
Liver consumption (yes)	1.39	0.86–2.25	0.17
Cow raw milk consumption (yes)	0.74	0.46–1.18	0.21
Unwashed raw vegetables (yes)	1.44	0.76–2.74	0.25
Unwashed raw fruits (yes)	0.75	0.39–1.46	0.4
Untreated water (yes)	1.39	0.87–2.21	0.15
Washing hands before eating (yes)	1.06	0.49–2.30	0.86
Floor at home (soil)	0.64	0.21–1.97	0.44
Availability of potable water (in the street)	1.72	0.93–3.19	0.08
Toilet facilities (latrine)	1.94	0.82–4.59	0.12
Crowding (yes)	1.63	1.02–2.61	0.03
Education of the head of the family (up to 3 years)	1.23	0.67–2.24	0.5

Discussion

The seroprevalence and risk factors associated with T. gondii infection in people with alcohol consumption are largely unknown. Consequently, we attempted to determine the rate of T. gondii seropositivity and the seroprevalence association with the sociodemographic, clinical, behavioral, and housing characteristics in people with alcohol consumption in Durango, Mexico. The 11.2% seroprevalence of T. gondii infection found in this study is higher than the 6.1% seroprevalence of this infection reported in the general population of Durango City, Mexico [20], but is lower than the 23.8% T. gondii seroprevalence reported in the general population in rural communities in Durango State, Mexico [22]. It is unclear why alcohol consumers had a different seroprevalence of T. gondii infection from those in the general population in urban and rural Durango. In these surveys the same enzyme immunoassay was used. However, differences in the risk factors between the population groups might exist. Seroprevalence of T. gondii infection increases with age [21] and is high in rural areas [22]. The mean age of people in the present study (39.4±14.0 years) was comparable to the mean age (37.04±16.1 years) found in the survey in Durango City [21], but lower than that (42.5 ± 17.6 years) found in people in rural Durango [22]. The high seroprevalence of T. gondii infection in the subset of people from rural areas observed in our present study might have contributed to an increase in the general seroprevalence. However, the seroprevalence found in people with alcohol consumption is lower than those found in other population groups in our region, including waste pickers (21.1%) [23], schizophrenic patients (20%) [24], inmates (21.1%) [25], or miners (60%) [26]. This relatively low seroprevalence found in our study coincides with the finding of a study of the Finnish general population, where researchers found that T. gondii seroprevalence was not associated with alcohol use disorders [28]. It is unknown whether T. gondii-induced behavioral changes might lead to alcohol consumption or whether alcohol consumption may lead to risky behavior for T. gondii infection. This study was performed over a 4-year period; however, this fact does not affect the interpretation of the results as the immunoassays were the same and no change in the seroprevalence of T. gondii infection in Durango during the last 10 years has been reported.

We sought to determine the risk factors associated with T. gondii seropositivity and serointensity. Logistic regression analysis of sociodemographic, housing, and behavioral characteristics of people with alcohol consumption showed that T. gondii seropositivity was associated with consumption of armadillo meat, and the use of latrines for elimination of excretes. In an epidemiological study in elderly people in Durango, Mexico, we found that T. gondii seropositivity was associated with consumption of armadillo meat [29]. Thus, we demonstrate this association for the second time in Mexico. Serological evidence of T. gondii infection in armadillos has been established in Brazil [30, 31]. However, to the best of our knowledge, no study about T. gondii infection in armadillos in Mexico has been reported. Our conclusions coincide with a previous report in Mexico examining the association between T. gondii seropositivity and the use of latrines. This association was noted in an epidemiological study of pregnant women in the central Mexican city of Aguascalientes [32]. Additionally, high anti-T. gondii IgG antibodies were associated with consumption of armadillo meat and crowding at home. Incidence of toxoplasmosis increases with crowding and poor sanitary habits [33]. The association between high antibody levels and crowding found in the present study is in line with a previous report of an association between seroreactivity (IgG and IgM) to T. gondii and crowding in the US [34].

As to clinical characteristics, the negative association between T. gondii seropositivity and visual impairment, history of surgery, and hepatitis suggests that T. gondii infection did not play an important role in these clinical factors in the study population. In the women studied, the higher frequency of T. gondii seropositivity in women with pregnancies than in women without pregnancies may be due to a higher age in women with pregnancies than in those without pregnancies.

The current study has the following limitations: 1) Although the sample size was large, we studied subjects in only one Mexican state, and the results of this study cannot be extrapolated to other Mexican states; and 2) the quantity and frequency of alcohol intake was not correlated with T. gondii exposure. Epidemiological studies to evaluate the link between seropositivity and serointensity of T. gondii infection and alcohol consumption including several Mexican states and quantification of alcohol intake are needed.

Conclusions

This is the first study about the epidemiology of T. gondii exposure in alcohol consumers. We found a different T. gondii seroprevalence in alcohol consumers from those previously found in population groups in the region. This is the first study to show the association between high anti-T. gondii antibodies and overcrowding in Mexico, and the second study on the association between T. gondii infection and consumption of armadillo meat and the use of latrines in this country. We believe the epidemiology of T. gondii infection in people with alcohol consumption merits further investigation. We further believe identification of factors associated with T. gondii seropositivity in this study may help inform and contribute to the effective planning of prevention and control measures against infection with T. gondii and its sequelae.