Research Article | Open Access
Cosme Alvarado-Esquivel, Jesús Hernández-Tinoco, Luis Francisco Sánchez-Anguiano, "Lack of Association between Toxocara Exposure and Suicide Attempts in Psychiatric Patients", Journal of Parasitology Research, vol. 2015, Article ID 608604, 5 pages, 2015. https://doi.org/10.1155/2015/608604
Lack of Association between Toxocara Exposure and Suicide Attempts in Psychiatric Patients
Infection with Toxocara may affect the central nervous system. A high seroprevalence of Toxocara infection has been reported in psychiatric patients. To the best of our knowledge, there is no previous report about an association of Toxocara infection with suicide attempts. Therefore, we sought to determine whether Toxocara exposure is associated with suicide attempts in psychiatric patients. We studied 282 psychiatric outpatients (156 with suicide attempts and 126 without suicide attempts). Sera of patients were analyzed for the presence of anti-Toxocara IgG antibodies by using a commercially available enzyme immunoassay. One of the 156 (0.6%) suicide attempters and 1 (0.8%) of the 126 controls were positive for anti-Toxocara IgG antibodies (OR = 0.80; 95% CI: 0.04–13.02; ). Toxocara seropositivity was significantly higher () in male patients with consumption of raw dried goat meat than male patients without this consumption. Results suggest that Toxocara exposure is not associated with suicide attempts in psychiatric outpatients in Durango City, Mexico. However, further studies with larger samples sizes to confirm our results should be conducted. Too few patients were seropositive to assess further associations of Toxocara exposure with sociodemographic, clinical, and behavioral characteristics of the psychiatric patients.
The nematode parasite Toxocara causes infections in intestines of dogs and cats . Local environment is contaminated with parasite eggs shed by infected cats and dogs [2, 3]. Humans acquire an infection with Toxocara by accidental consumption of infecting parasite eggs or larvae [4, 5]. Infection with Toxocara is one of the most widespread zoonotic parasitic infections  and causes a disease known as toxocariasis . The burden of toxocariasis in North America is significant ; however, toxocariasis is recognized as a neglected zoonotic disease [6, 7]. The seroprevalence of Toxocara infection varies substantially among population groups, that is, 2%–5% in adults in urban areas, 14.2%–37% in rural areas, and 63.2%–92.8% in some tropical countries . Toxocara does not mature in the human intestines but instead migrates through tissues and organs of the body . Dissemination of Toxocara may occur to muscles, eyes, liver, lungs, and central nervous system . Infections with Toxocara are usually asymptomatic [4, 7]. However, some infections may lead to severe toxocariasis and death . Toxocara infection of the eye is a major cause of blindness . Visceral toxocariasis is commonly associated with liver and pulmonary damage . Less commonly, toxocariasis may manifest with pericardial effusion or myocarditis . Toxocara may invade the brains of humans ; however, neurotoxocariasis or cerebral toxocariasis remains a poorly understood phenomenon . Toxocara infection may lead to eosinophilic meningitis , meningoencephalitis, myelitis, cerebral vasculitis, optic neuritis , epilepsy , and multiple cerebral infarction . In addition, toxocariasis has been associated with dementia [11, 15, 16] and mental confusion . A high seroprevalence of Toxocara infection has been found in psychiatric patients [18–20]. In a study in Italy, researchers found a 13% seroprevalence of Toxocara infection in psychiatric patients . In a recent study in Mexico, 4.7% of 128 psychiatric inpatients were seropositive for Toxocara infection , whereas, in a study in China, a 16.4% seroprevalence of Toxocara infection in psychiatric patients was found .
Very little is known about the association of infections with suicide attempts. Only few infectious agents have been studied in relation with suicide attempts including influenza B  and Toxoplasma gondii infections [22, 23]. Several studies have shown that Toxocara affects the brain of humans  and rodents [24–26]. However, it is unknown whether Toxocara infection is associated with suicide attempts. Therefore, we performed a case-control seroprevalence study to determine whether Toxocara infection is associated with suicide attempts in psychiatric outpatients in Durango City, Mexico.
2. Materials and Methods
2.1. Study Population
This case-control study was performed using stored serum samples from a recent Toxoplasma gondii study in psychiatric patients in Durango City, Mexico . Subjects () enrolled in the study were psychiatric outpatients who attended two public hospitals in Durango City: the Hospital of Mental Health “Miguel Vallebueno” and the General Hospital of the Secretary of Health. Inclusion criteria for suicide attempters were the following: (1) psychiatric outpatients with history of one or more suicide attempts; (2) those aged 18 years and older; and (3) those who accepted to participate in the study. In total, 156 suicide attempters were enrolled in the study. They were 18–61 years old (mean 34.01 ± 10.25 years) and included 119 females and 37 males. Inclusion criteria for psychiatric controls were the following: (1) psychiatric outpatients without history of suicide attempts; (2) those aged 18 years and older; and (3) those who accepted to participate in the study. Gender was not a restrictive criterion for enrollment of cases and controls. The control group included 126 (75 females, 51 males) patients aged 18–69 years (mean 38.00 ± 11.59 years).
2.2. General Sociodemographic, Clinical, and Behavioral Characteristics of Patients
Sociodemographic, clinical, and behavioral characteristics of the psychiatric patients were obtained with a questionnaire through a face-to-face interview. Sociodemographic items were age, gender, birthplace, educational level, occupation, and socioeconomic status. Clinical items included diagnosis of current psychiatric disease and concomitant diseases, suicidal ideation, history and number of suicide attempts, time from last suicide attempt, and method of suicide attempts. This study relied on the information about suicide attempts provided by the patients. It is unclear how sensitive the face-to-face interview to detect suicide attempts used is. In addition, other clinical data including lymphadenopathy, frequent headache, impairments in memory, reflexes, hearing, and vision, and history of blood transfusion, transplant, surgery, alcohol consumption, drug abuse, or sexual history from all participants were obtained. Behavioral items were the following: contact with animals and cat excrement, traveling, type of meat consumed, consumption of raw or undercooked meat, unpasteurized milk, dried or cured meat, unwashed raw vegetables and fruits or untreated water, frequency of eating in restaurants or fast food outlets, contact with soil, and type of flooring at home.
2.3. Detection of Anti-Toxocara Antibody
Sera of patients were kept frozen at −20°C until analyzed. All serum samples were analyzed for anti-Toxocara IgG antibodies with a commercially available enzyme immunoassay (EIA) “Toxocara” kit (Diagnostic Automation, Inc., Calabasas, CA, USA). All EIA were performed according to instructions of the manufacturer. An absorbance reading ≥ 0.3 optical density units was used as a cut-off for seropositivity. Positive and negative controls were included in each EIA. Serum samples of cases and controls were analyzed in the same run. Laboratory personnel were not blinded to study samples.
2.4. Statistical Analysis
We performed the statistical analysis with the software Epi Info version 7 and SPSS 15.0 (SPSS Inc., Chicago, Illinois, USA). For calculation of the sample size, we used a 95% confidence level, a power of 80%, a reference seroprevalence of 4.7%  as the expected frequency of exposure in controls, and an odds ratio of 3.5. The result of the sample size calculation was 106 cases and 106 controls. These values were taken as the minimum number of participants for each group. To assess the association between Toxocara infection and suicide attempts and other characteristics of the patients a bivariate analysis was used. The two-tailed Fisher exact test was used to compare the frequencies among the groups. Variables with values obtained in the bivariate analysis were further analyzed with stratification by gender. Statistical significance was set at value .
2.5. Ethical Aspects
The study was performed using only residual serum samples and questionnaires from a previous survey in psychiatric outpatients . The Ethical Committees of the General Hospital and the Hospital of Mental Health in Durango City approved the previous study. The purpose and procedures of the survey were explained to all participants, and a written informed consent was obtained from all of them. The additional analysis of serum samples and questionnaires was approved by the Ethical Committee of the Instituto de Seguridad y Servicios Sociales de los Trabajadores del Estado in Durango City, Mexico.
One of the 156 (0.6%) suicide attempters and 1 (0.8%) of the 126 controls were positive for anti-Toxocara IgG antibodies (OR = 0.80; 95% CI: 0.04–13.02; ). The suicide attempter seropositive for Toxocara had a low anti-Toxocara IgG antibody level (optical density units = 0.608). Similarly, the seropositive control has a low anti-Toxocara IgG antibody level (optical density units = 0.839).
None of the sociodemographic characteristics including age, gender, birthplace, educational level, occupation, and socioeconomic status showed an association with Toxocara seropositivity (Table 1). Likewise, none of the clinical characteristics studied including psychiatric disease and concomitant diseases, number of suicide attempts, time from last suicide attempt, method of suicide attempts, lymphadenopathy, frequent headache, impairments in memory, reflexes, hearing, and vision, and history of blood transfusion, transplant, surgery, alcohol consumption, drug abuse, or sexual history showed an association with Toxocara seropositivity. In contrast, bivariate analysis of the behavioral characteristics of the psychiatric patients (cases and controls together) showed four variables with value : consumption of meat from boar (), pigeon (), and squirrel () and consumption of raw dried goat meat (). Other behavioral characteristics of patients including contact with animals and cat excrement, traveling, consumption of unwashed raw vegetables and fruits, unpasteurized milk or untreated water, frequency of eating in restaurants or fast food outlets, and contact with soil showed values in the bivariate analysis. Stratification by gender showed that Toxocara seroprevalence was significantly higher in male patients with consumption of raw dried meat (1/1: 100%) than male patients without this consumption (0/88: 0%) (). Toxocara seroprevalence was comparable in male patients with consumption of meat from boar, pigeon, and squirrel than male patients without these consumption acts (). Toxocara seroprevalence was similar in female patients with consumption of meat from boar, pigeon, and squirrel and raw dried goat meat than female patients without these consumption acts.
Toxocara infection is one of the five more common nematodal infections of the nervous system . Migration of Toxocara to brain does not frequently induce a recognizable neurological syndrome . Toxocara infection was associated with depression in a 65-year-old woman confirmed with psychometric tests . Brain involvement during Toxocara infection may lead to disease and possibly to changes in behavior. Therefore, the present study aimed to determine whether Toxocara exposure was associated with suicide attempts in psychiatric patients. We found a low prevalence of Toxocara exposure among psychiatric outpatients, and Toxocara seropositivity was not associated with suicide attempts. In a previous study in psychiatric patients, a 4.7% seroprevalence of Toxocara exposure was found . The lower prevalence found in the present study than that previously reported in psychiatric patients can be explained by differences in the characteristics of the patients; that is, we studied outpatients, whereas in the previous study only inpatients were examined . Results of the present study suggest that Toxocara exposure did not represent a risk for suicide attempts in the psychiatric patients studied. However, this is the first study of its kind and results should be confirmed. Other population groups including inpatients and people living in high seroprevalence places (rural areas, tropical countries) with larger sample sizes should be studied.
We searched for contributing factors of Toxocara exposure in the psychiatric patients studied. We found that consumption of raw dried goat meat was associated with Toxocara exposure. This behavioral characteristic was the only variable associated with Toxocara exposure. However, the very low seroprevalence of Toxocara infection found among psychiatric patients did not allow us to obtain further statistically significant associations. Remarkably, consumption of goat meat was previously associated with Toxocara exposure in psychiatric inpatients in Durango City . The fact that consumption of goat meat was associated with Toxocara exposure in two independent studies points towards the importance of this factor for the transmission of Toxocara infection to humans. In the present study, we examined new cases and a larger sample size () of psychiatric patients than those () included in the previous study . In the present study, an association of Toxocara exposure with the consumption of raw dried meat from goat was found. To the best of our knowledge, this is the first report of an association of consumption of raw “dried” goat meat with Toxocara exposure. In a recent study, a clinical case of a 51-year-old man with lower motor neuron disease was linked to consumption of raw goat meat . Toxocara infections in goats have been poorly studied. We found only one seroprevalence report in goats. A 10.1% seroprevalence of anti-Toxocara antibodies was found in goats in Thessaly, Greece . Further studies about Toxocara infection in goats are needed.
Results suggest that Toxocara exposure is not associated with suicide attempts in psychiatric outpatients in Durango City, Mexico. However, further studies with larger samples sizes to confirm our results should be conducted. The association between Toxocara seropositivity and consumption of raw dried goat meat deserves further investigation. Too few patients were seropositive to assess further associations between Toxocara exposure and sociodemographic, clinical, and behavioral characteristics of patients.
Conflict of Interests
The authors declare that there is no conflict of interests regarding the publication of this paper.
This study was supported by Juárez University of Durango State, Durango, Mexico.
The questionnaire used in this study is included as supplementary material.
- C. Fan, C. V. Holland, K. Loxton, and U. Barghouth, “Cerebral toxocariasis: silent progression to neurodegenerative disorders?” Clinical Microbiology Reviews, vol. 28, no. 3, pp. 663–686, 2015.
- P. A. M. Overgaauw and F. van Knapen, “Veterinary and public health aspects of Toxocara spp,” Veterinary Parasitology, vol. 193, no. 4, pp. 398–403, 2013.
- P. Deplazes, F. van Knapen, A. Schweiger, and P. A. M. Overgaauw, “Role of pet dogs and cats in the transmission of helminthic zoonoses in Europe, with a focus on echinococcosis and toxocarosis,” Veterinary Parasitology, vol. 182, no. 1, pp. 41–53, 2011.
- C. N. L. Macpherson, “The epidemiology and public health importance of toxocariasis: a zoonosis of global importance,” International Journal for Parasitology, vol. 43, no. 12-13, pp. 999–1008, 2013.
- A. Borecka and T. Kłapeć, “Epidemiology of human toxocariasis in Poland—a review of cases 1978–2009,” Annals of Agricultural and Environmental Medicine, vol. 22, no. 1, pp. 28–31, 2015.
- R. M. Lee, L. B. Moore, M. E. Bottazzi, and P. J. Hotez, “Toxocariasis in North America: a systematic review,” PLoS Neglected Tropical Diseases, vol. 8, no. 8, Article ID e3116, 2014.
- G. Rubinsky-Elefant, C. E. Hirata, J. H. Yamamoto, and M. U. Ferreira, “Human toxocariasis: diagnosis, worldwide seroprevalences and clinical expression of the systemic and ocular forms,” Annals of Tropical Medicine and Parasitology, vol. 104, no. 1, pp. 3–23, 2010.
- J. F. Magnaval, L. T. Glickman, P. Dorchies, and B. Morassin, “Highlights of human toxocariasis,” Korean Journal of Parasitology, vol. 39, no. 1, pp. 1–11, 2001.
- H. Pelloux and O. Faure, “Toxocariasis in adults,” Revue de Medecine Interne, vol. 25, no. 3, pp. 201–206, 2004.
- J. F. Arevalo, J. V. Espinoza, and F. A. Arevalo, “Ocular toxocariasis,” Journal of Pediatric Ophthalmology and Strabismus, vol. 50, no. 2, pp. 76–86, 2013.
- J. Finsterer and H. Auer, “Parasitoses of the human central nervous system,” Journal of Helminthology, vol. 87, no. 03, pp. 257–270, 2013.
- J. Finsterer and H. Auer, “Neurotoxocarosis,” Revista do Instituto de Medicina Tropical de Sao Paulo, vol. 49, no. 5, pp. 279–287, 2007.
- G. Quattrocchi, A. Nicoletti, B. Marin, E. Bruno, M. Druet-Cabanac, and P.-M. Preux, “Toxocariasis and epilepsy: systematic review and meta-analysis,” PLoS Neglected Tropical Diseases, vol. 6, no. 8, Article ID e1775, 2012.
- H. H. Kwon, “Toxocariasis: a rare cause of multiple cerebral infarction,” Infection & Chemotherapy, vol. 47, no. 2, pp. 137–141, 2015.
- E. Richartz and G. Buchkremer, “Cerebral toxocariasis: a rare cause of cognitive disorders. A contribution to differential dementia diagnosis,” Nervenarzt, vol. 73, no. 5, pp. 458–462, 2002.
- J.-F. Magnaval, V. Galindo, L. T. Glickman, and M. Clanet, “Human Toxocara infection of the central nervous system and neurological disorders: a case-control study,” Parasitology, vol. 115, no. 5, pp. 537–543, 1997.
- Y. Maiga, S. Wiertlewski, H. Desai, M. Marjolet, and P. Damier, “Presentation of cerebral toxocariasis with mental confusion in an adult: case report and review of the literature,” Bulletin de la Societe de Pathologie Exotique, vol. 100, no. 2, pp. 101–104, 2007.
- M. Di Fiore, A. Virga, V. Usticano, S. Di Rosa, and G. B. Rini, “Antibodies against Toxocara canis in human serum from western Sicily,” Bollettino dell'Istituto Sieroterapico Milanese, vol. 68, no. 1, pp. 93–96, 1989.
- C. Alvarado-Esquivel, “Toxocara infection in psychiatric inpatients: a case control seroprevalence study,” PLoS ONE, vol. 8, no. 4, Article ID e62606, 2013.
- W. Cong, X. X. Zhang, N. Zhou et al., “Toxocara seroprevalence among clinically healthy individuals, pregnant women and psychiatric patients and associated risk factors in Shandong Province, Eastern China,” PLoS Neglected Tropical Diseases, vol. 8, no. 8, Article ID e3082, 2014.
- O. Okusaga, R. H. Yolken, P. Langenberg et al., “Association of seropositivity for influenza and coronaviruses with history of mood disorders and suicide attempts,” Journal of Affective Disorders, vol. 130, no. 1-2, pp. 220–225, 2011.
- T. A. Arling, R. H. Yolken, M. Lapidus et al., “Toxoplasma gondii antibody titers and history of suicide attempts in patients with recurrent mood disorders,” Journal of Nervous and Mental Disease, vol. 197, no. 12, pp. 905–908, 2009.
- C. Alvarado-Esquivel, L. F. Sánchez-Anguiano, C. A. Arnaud-Gil et al., “Toxoplasma gondii infection and suicide attempts: a case-control study in psychiatric outpatients,” Journal of Nervous and Mental Disease, vol. 201, no. 11, pp. 948–952, 2013.
- I. Capo and N. Rokvić, “Neuropathology of experimental toxocariasis in Syrian golden hamsters,” Medicinski Pregled, vol. 62, no. 11-12, pp. 603–607, 2009.
- C. V. Holland and C. M. Hamilton, “The significance of cerebral toxocariasis: a model system for exploring the link between brain involvement, behaviour and the immune response,” The Journal of Experimental Biology, vol. 216, no. 1, pp. 78–83, 2013.
- L. Heuer, M. Beyerbach, F. Lühder, A. Beineke, and C. Strube, “Neurotoxocarosis alters myelin protein gene transcription and expression,” Parasitology Research, vol. 114, no. 6, pp. 2175–2186, 2015.
- M. D. Walker and J. R. Zunt, “Neuroparasitic infections: nematodes,” Seminars in Neurology, vol. 25, no. 3, pp. 252–261, 2005.
- J. Finsterer, V. Kallab, and H. Auer, “Neurotoxocariasis associated with lower motor neuron disease: report of one case,” Revista Médica de Chile, vol. 138, no. 4, pp. 483–486, 2010.
- V. Kantzoura, A. Diakou, M. K. Kouam, H. Feidas, H. Theodoropoulou, and G. Theodoropoulos, “Seroprevalence and risk factors associated with zoonotic parasitic infections in small ruminants in the Greek temperate environment,” Parasitology International, vol. 62, no. 6, pp. 554–560, 2013.
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