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. 2011 Jun 17;4:112. doi: 10.1186/1756-3305-4-112

Toxoplasma gondii infection and abdominal hernia: evidence of a new association

Cosme Alvarado-Esquivel 1,✉, Sergio Estrada-Martínez 2
PMCID: PMC3130683  PMID: 21682896

Abstract

Background

We performed a retrospective, observational study in 1156 adult subjects from the general population of Durango City, Mexico, Fifty five subjects with a history of abdominal hernia repair and 1101 subjects without hernia were examined with enzyme-linked immunoassays for the presence of anti-Toxoplasma IgG and IgM antibodies.

Results

The seroprevalence of anti-Toxoplasma IgG antibodies and IgG titers was significantly higher in subjects with abdominal hernia repair than those without hernia. There was a tendency for subjects with hernia repair to have a higher seroprevalence of anti-Toxoplasma IgM antibodies than subjects without hernia. The seroprevalence of anti-Toxoplasma IgG antibodies in subjects with hernia repair was significantly higher in subjects ≥ 50 years old than those < 50 years old. Further analysis in subjects aged ≥ 50 years showed that the seroprevalence of anti-Toxoplasma IgG antibodies was also significantly higher in individuals with hernia repair than those without hernia (OR = 2.72; 95% CI: 1.10-6.57). Matching by age and sex further showed that the seroprevalence of Toxoplasma infection was significantly higher in patients with hernia repair than those without hernia (OR: 4.50; 95% CI: 1.22-17.33).

Conclusions

Results indicate that infection with Toxoplasma is associated with abdominal hernia. The contributing role of infection with Toxoplasma in abdominal hernia was observed mainly in subjects aged ≥ 50 years old. Our results might have clinical, prevention and treatment implications and warrant for further investigation.

Findings

The protozoan parasite Toxoplasma gondii (T. gondii) is widely distributed around the world [1,2]. Human infections with T. gondii occur by ingesting food or water that is contaminated with oocysts shed by cats or by eating undercooked or raw meat containing tissue cysts [2-4]. Infections with T. gondii may result in an asymptomatic state or lead to disease. The parasite disseminates within the host's body and may affect lymph nodes, eyes, central nervous system, and other tissues [3,5-9]. In addition, primary infection during pregnancy may lead to severe damage to the fetus [2,3]. We have explored the seroprevalence of and risk factors for T. gondii infection in some healthy [10-12] and ill [13-16] populations in Durango, Mexico. In a recent study in liver disease patients, we reported that subjects with abdominal hernia repair showed a significantly higher seroprevalence of T. gondii infection than individuals without hernia [16]. Therefore, we sought to determine whether the seroprevalence of T. gondii infection and anti-T. gondii IgG levels are associated with a history of abdominal hernia repair in subjects of the general population in Durango, Mexico. Furthermore, we investigated socio-demographic, clinical, and behavioral characteristics associated with T. gondii seropositivity in subjects with abdominal hernia repair.

Through a retrospective, observational study design, we studied 1156 subjects of the general population of Durango City, Mexico that were examined for T. gondii antibodies in our Faculty of Medicine from January 2009 to December 2010. Of the 1156 subjects, 55 had a history of abdominal hernia repair while 1101 subjects did not report any suffering from abdominal hernia or having had any abdominal hernia repair.

Socio-demographic, clinical and behavioral characteristics of the participants were obtained with the aid of a standardized questionnaire and kept in records. Socio-demographic data included age, gender, place of birth, place of residence, residence area (urban, suburban, rural), educational level, socioeconomic status, and occupation. Clinical data included the presence of diseases, presence or history of lymphadenopathy, frequent presence of headache; history of blood transfusion, transplant, or surgery; and memory, reflex, hearing, and visual impairments. Behavioral data included animal contacts, contact with cat feces, traveling 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, frequency of eating out of home (at restaurants or fast food outlets), contact with soil (gardening or agriculture), and type of floors at home.

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.

This study was approved by the Institutional Ethical Committee of the Institute of Security and Social Services of the State Workers in Durango City.

Results were analyzed with the aid of the software Epi Info version 3.5.1 and SPSS 15.0 (SPSS Inc. Chicago, Illinois). For comparison of the frequencies among groups, the Fisher exact test was used. A bivariate analysis was used to assess the association between subject's characteristics and T. gondii infection. Odds ratio (OR) and 95% confidence interval (CI) were calculated to assess associations. A P value less than 0.05 was considered statistically significant.

Anti-T. gondii IgG antibodies were found in 9 (16.4%) of 55 subjects with hernia repair and in 76 (6.9%) of 1101 subjects without hernia (OR = 2.64; 95% CI: 1.16-5.85; P = 0.01). The seroprevalence of T. gondii infection and the socio-demographic characteristics of the subjects with hernia repair are shown in Table 1. Seroprevalence of T. gondii infection in subjects with hernia repair was significantly higher in individuals who were not born in Durango State than those born in Durango State (P = 0.03), and in individuals of medium socioeconomic level than those of low socioeconomic level (P = 0.04). Anti-T. gondii IgG levels were significantly higher in subjects with hernia repair than those without hernia (P = 0.03) (Table 2). Anti-T. gondii IgM antibodies were found in 4 (7.3%) subjects with hernia repair and in 27 (2.5%) subjects without hernia (P = 0.05). An age-stratified seroprevalence of T. gondii infection is shown in Table 3. Seroprevalence of anti-T. gondii IgG antibodies in hernia subjects was significantly higher in subjects ≥ 50 years old (9/36: 26.7%) than those < 50 years old (0/18: 0%) (P = 0.02). Since T. gondii infection in subjects with hernia repair was found only in individuals aged ≥ 50 years old, we used this age group for further comparison. Seroprevalence of anti-T. gondii IgG antibodies in subjects aged ≥ 50 years old was significantly higher in individuals with hernia repair (9/36: 25%) than those without hernia (42/385: 10.9%) (OR = 2.72; 95% CI: 1.10-6.57; P = 0.02). We further matched these subjects (≥ 50 years old) with a history of hernia with those without any history of hernia by age and sex. We analyzed two controls for each case, and the seroprevalence of T. gondii infection was significantly higher in patients with a history of hernia (9/35: 25.7%) than those without any history of hernia (5/70: 7.1%) (OR: 4.50; 95% CI: 1.22-17.33).

Table 1.

Socio-demographic characteristics of subjects with abdominal hernia repair and seroprevalence of T. gondii infection.

Prevalence of T. gondii infection P value
Characteristic No.a % No. %
Age groups (years)
 30 or less 7 13 0 0 0.06
 31-50 11 20.4 0 0
 > 50 36 66.7 9 100
Sex
 Male 32 58.2 3 9.4 0.14
 Female 23 41.8 6 26.1
Birth place
 Durango State 45 83.3 5 11.1 0.03
 Other Mexican State 9 16.7 4 44.4
Residence place
 Durango State 55 100 9 16.4 -
Residence area
 Urban 48 88.9 9 18.8 0.50
 Suburban 2 3.7 0 0.0
 Rural 4 7.4 0 0.0
Educational level
 No education 1 1.9 0 0.0 0.67
 1-6 years 19 35.2 4 21.1
 7-12 years 14 25.9 1 7.1
 > 12 years 20 37.0 4 20.0
Socio-economic level
 Low 15 28.3 0 0.0 0.04
 Medium 38 71.7 9 23.7
Occupation
 Non-laborerb 15 27.3 2 13.3 1.00
 Laborerc 40 72.7 7 17.5
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aIn some strata the sum does not add up to the total because of a few missing values.

bNon laborer = none occupation, student or housewife.

cLaborer = Employee, professional, business, agriculture, cattle rising, factory worker, construction worker or other.

Table 2.

Comparison of anti-Toxoplasma IgG levels in subjects with hernia repair and subjects without hernia.

Anti-Toxoplasma IgG levels Subjects with hernia repair (n = 55) Subjects without hernia (n = 1101) P value
No. % No. %
< 90 IU/ml 2 3.6 18 1.6 0.25
≥ 90 IU/ml 7 12.7 58 5.3 0.03
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Table 3.

Seroprevalence of anti-T. gondii IgG antibodies in subjects with hernia repair and subjects without hernia according to age groups.

Age groups
(years)		 Subjects with hernia repair Subjects without hernia
No. T. gondii infection No. T. gondii infection Odds ratio P value
tested No. % tested No. % (95% Confidence interval)
≤ 29 7 0 0.0 403 15 3.7 0.00 (0.00-19.66) 1.00
30-39 7 0 0.0 184 15 8.2 0.00 (0.00-8.62) 1.00
40-49 4 0 0.0 122 4 3.3 0.00 (0.00-59.51) 1.00
50-59 6 1 16.7 153 14 9.2 1.99 (0.04-19.58) 0.45
60-69 15 4 26.7 115 13 11.3 2.85 (0.57-11.50) 0.11
≥ 70 15 4 26.7 117 15 12.8 2.47 (0.50-9.76) 0.23
≥ 50 36 9 25.0 385 42 10.9 2.72 (1.10-6.57) 0.02
All 54a 9 16.7 1094a 76 6.9 2.68 (1.17-5.95) 0.01
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aSubjects with available age.

None of the clinical characteristics including the presence of underlying diseases, presence or history of lymphadenopathy, frequent presence of headache; history of blood transfusion, transplant, or other surgeries; and memory, reflex, hearing, and visual impairments in subjects with hernia repair were associated with T. gondii seropositivity. Concerning behavioral characteristics, the bivariate analysis showed that T. gondii infection was negatively associated with the variable untreated water consumption (P = 0.02). Other behavioral characteristics in the subjects with hernia repair did not show any association with T. gondii infection.

In this study, we found a significantly higher seroprevalence of anti-T. gondii IgG antibodies in subjects with a history of abdominal hernia than subjects without history of hernia. Anti-T. gondii IgG antibody levels were also significantly higher in subjects with a history of hernia than subjects without this history. Prevalence of anti-T. gondii IgM antibodies was higher in subjects with hernia repair than those without hernia, and this difference in seroprevalences among the groups showed a borderline statistical significance. Results indicate a stronger seropositivity to T. gondii in subjects with a history of abdominal hernia than subjects without hernia. The association of T. gondii infection and abdominal hernia was found in the whole population studied and especially in subjects aged ≥ 50 years old. Overall, the prevalence of hernia among the general population studied was low (4.8%). Therefore, the hernia group was small compared with the much larger control group. However, a reduction of the control group size by age and sex matching (two controls for every case) confirmed our results and even increased the odd ratio. It is not clear why the seroprevalence of T. gondii infection was higher in abdominal hernia patients than in subjects without hernia. Transmission of T. gondii infection by surgical procedures other than transplantation is not currently acknowledged. In a previous study in psychiatric patients, we found that patients with a history of surgery had a significantly higher seroprevalence of T. gondii infection than patients without this history [13]. In the present study, transmission of infection by the surgical procedure during hernia repair cannot be ruled out. However, this route of infection seems unlikely since some subjects without hernia repair has had other surgical procedures too and their seroprevalence was lower than those with hernia repair. On the other hand, there is not any published data concerning a role of T. gondii infection in the pathogenesis of abdominal hernia. Alterations in skeletal muscles of the abdominal wall have been involved in the pathogenesis of abdominal hernia; these alterations include disruption of muscles [17], and degenerative changes in muscle fibers [18]. The parasite T. gondii exists in skeletal muscles of infected humans and animals [2,19,20], and viable T. gondii can be isolated from animal muscular tissues [21]. In humans, infections with T. gondii may cause muscle disease (myositis or polymyositis) that may lead to myalgias and muscular weakness [22-26]. In mice experimentally infected with T. gondii, severity of muscle alterations depended upon concentration of parasites [20]. Therefore, T. gondii might contribute in the pathogenesis of abdominal hernia in some individuals by affecting their abdominal muscles.

Why high anti-T. gondii IgG levels were more frequency observed in subjects with hernia repair than in subjects without hernia is not clear. It is likely that a continuous parasite antigenic stimulation may induce a high antibody production in the hosts. On the other hand, the stress of the surgical procedure might have reactivated latent T. gondi infections leading to an increase of anti-T. gondii IgG antibodies. Surgical procedures may cause immunodepression [27-29], and reactivations of viral and parasitic infections after surgery have been reported in humans and animals [30-33].

In the present study with an independent population, we confirmed our previous report of an association of T. gondii infection with abdominal hernia [16]. Our results might have clinical, prevention and treatment implications. The results warrant for further investigation.

Competing interests

The authors declare that they have no competing interests.

Authors' contributions

CAE conceived and designed the study protocol, participated in the coordination and management of the study, applied the questionnaires, performed the laboratory tests, the data analysis and statistical analysis, and wrote the manuscript. SEM performed the statistical analysis. Both authors approved the final version of the manuscript.

Funding

This study was supported by The Faculty of Medicine and Nutrition. Universidad Juárez del Estado de Durango. Durango City, Mexico.

Contributor Information

Cosme Alvarado-Esquivel, Email: alvaradocosme@yahoo.com.

Sergio Estrada-Martínez, Email: semdurango@hotmail.com.

References

  1. Hill DE, Chirukandoth S, Dubey JP. Biology and epidemiology of Toxoplasma gondii in man and animals. Anim Health Res Rev. 2005;6:41–61. doi: 10.1079/AHR2005100. [DOI] [PubMed] [Google Scholar]
  2. Dubey JP. Toxoplasmosis of animals and humans. 2. Boca Raton, Florida: CRC Press; 2009. [Google Scholar]
  3. Montoya JG, Liesenfeld O. Toxoplasmosis. Lancet. 2004;363:1965–1976. doi: 10.1016/S0140-6736(04)16412-X. [DOI] [PubMed] [Google Scholar]
  4. Dawson D. Foodborne protozoan parasites. Int J Food Microbiol. 2005;103:207–227. doi: 10.1016/j.ijfoodmicro.2004.12.032. [DOI] [PubMed] [Google Scholar]
  5. Walker M, Zunt JR. Parasitic central nervous system infections in immunocompromised hosts. Clin Infect Dis. 2005;40:1005–1015. doi: 10.1086/428621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Balasundaram MB, Andavar R, Palaniswamy M, Venkatapathy N. Outbreak of acquired ocular toxoplasmosis involving 248 patients. Arch of Ophthal. 2010;128:28–32. doi: 10.1001/archophthalmol.2009.354. [DOI] [PubMed] [Google Scholar]
  7. Ortego TJ, Robey B, Morrison D, Chan C. Toxoplasmic chorioretinitis and hepatic granulomas. Am J Gastroenterol. 1990;85:1418–1420. [PubMed] [Google Scholar]
  8. Bonacini M, Kanel G, Alamy M. Duodenal and hepatic toxoplasmosis in a patient with HIV infection: review of the literature. Am J Gastroenterol. 1996;91:1838–1840. [PubMed] [Google Scholar]
  9. Nunura J, Vásquez T, Endo S, Salazar D, Rodriguez A, Pereyra S, Solis H. Disseminated toxoplasmosis in an immunocompetent patient from Peruvian Amazon. Rev Inst Med Trop Sao Paulo. 2010;52:107–110. doi: 10.1590/s0036-46652010000200008. [DOI] [PubMed] [Google Scholar]
  10. Alvarado-Esquivel C, Sifuentes-Alvarez A, Narro-Duarte SG, Estrada-Martinez S, Diaz-Garcia JH, Liesenfeld O, Martinez-Garcia SA, Canales-Molina A. Seroepidemiology of Toxoplasma gondii infection in pregnant women in a public hospital in northern Mexico. BMC Infect Dis. 2006;13:6–113. doi: 10.1186/1471-2334-6-113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Alvarado-Esquivel C, Mercado-Suárez MF, Rodríguez-Briones A, Fallad-Torres L, Ayala-Ayala JO, Nevarez-Piedra LJ, Duran-Morales E, Estrada-Martínez S, Liesenfeld O, Márquez-Conde JA, Martínez-García SA. Seroepidemiology of infection with Toxoplasma gondii in healthy blood donors of Durango, Mexico. BMC Infect Dis. 2007;13:7–75. doi: 10.1186/1471-2334-7-75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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;97:40–43. doi: 10.1645/GE-2612.1. [DOI] [PubMed] [Google Scholar]
  13. Alvarado-Esquivel C, Alanis-Quiñones OP, Arreola-Valenzuela MA, Rodríguez-Briones A, Piedra-Nevarez LJ, Duran-Morales E, Estrada-Martínez S, Martínez-García SA, Liesenfeld O. Seroepidemiology of Toxoplasma gondii infection in psychiatric inpatients in a northern Mexican city. BMC Infect Dis. 2006;6:178. doi: 10.1186/1471-2334-6-178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Alvarado-Esquivel C, Liesenfeld O, Torres-Castorena A, Estrada-Martínez S, Urbina-Alvarez JD, Ramos-de la Rocha M, Márquez-Conde JA, Dubey JP. Seroepidemiology of Toxoplasma gondii infection in patients with vision and hearing impairments, cancer, HIV, or undergoing hemodialysis in Durango, Mexico. J Parasitol. 2010;96:505–508. doi: 10.1645/GE-2378.1. [DOI] [PubMed] [Google Scholar]
  15. Alvarado-Esquivel C, Urbina-Álvarez JD, Estrada-Martínez S, Torres-Castorena A, Molotla-de-León G, Liesenfeld O, Dubey JP. Toxoplasma gondii infection and schizophrenia: A case control study in a low Toxoplasma seroprevalence Mexican population. Parasitol Int. 2011;60:151–155. doi: 10.1016/j.parint.2010.12.003. [DOI] [PubMed] [Google Scholar]
  16. Alvarado-Esquivel C, Torres-Berumen JL, Estrada-Martínez S, Liesenfeld O, Mercado-Suarez MF. Toxoplasma gondii infection and liver disease: a case-control study in a Northern Mexican population. Parasit Vectors. 2011. in press . [DOI] [PMC free article] [PubMed]
  17. Morales-Conde S, Socas M, Barranco A. Sportsmen hernia: what do we know? Hernia. 2010;14:5–15. doi: 10.1007/s10029-009-0613-z. [DOI] [PubMed] [Google Scholar]
  18. Amato G, Marasa L, Sciacchitano T, Bell SG, Romano G, Gioviale MC, Lo Monte AI, Romano M. Histological findings of the internal inguinal ring in patients having indirect inguinal hernia. Hernia. 2009;13:259–262. doi: 10.1007/s10029-009-0483-4. [DOI] [PubMed] [Google Scholar]
  19. Dubey JP. Distribution of tissue cysts in organs of rats fed Toxoplasma gondii oocysts. J Parasitol. 1997;83:755–757. [PubMed] [Google Scholar]
  20. Tonino P, Finol HJ, Marquez A. Skeletal muscle pathology in mice experimentally infected with Toxoplasma gondii. J Submicrosc Cytol Pathol. 1996;28:521–526. [PubMed] [Google Scholar]
  21. Dubey JP. Refinement of pepsin digestion method for isolation of Toxoplasma gondii from infected tissues. Vet Parasitol. 1998;74:75–77. doi: 10.1016/S0304-4017(97)00135-0. [DOI] [PubMed] [Google Scholar]
  22. Plonquet A, Bassez G, Authier FJ, Dray JM, Farcet JP, Gherardi RK. Toxoplasmic myositis as a presenting manifestation of idiopathic CD4 lymphocytopenia. Muscle Nerve. 2003;27:761–765. doi: 10.1002/mus.10376. [DOI] [PubMed] [Google Scholar]
  23. Calore EE, Minkovski R, Khoury Z, Seguro AC, Perez Calore NM, Cavaliere MJ. Skeletal muscle pathology in 2 siblings infected with Toxoplasma gondii. J Rheumatol. 2000;27:1556–1559. [PubMed] [Google Scholar]
  24. Cuturic M, Hayat GR, Vogler CA, Velasques A. Toxoplasmic polymyositis revisited: case report and review of literature. Neuromuscul Disord. 1997;7:390–396. doi: 10.1016/S0960-8966(97)00098-9. [DOI] [PubMed] [Google Scholar]
  25. Adams EM, Hafez GR, Carnes M, Wiesner JK, Graziano FM. The development of polymyositis in a patient with toxoplasmosis: clinical and pathologic findings and review of literature. Clin Exp Rheumatol. 1984;2:205–208. [PubMed] [Google Scholar]
  26. Montoya JG, Jordan R, Lingamneni S, Berry GJ, Remington JS. Toxoplasmic myocarditis and polymyositis in patients with acute acquired toxoplasmosis diagnosed during life. Clin Infect Dis. 1997;24:676–683. doi: 10.1093/clind/24.4.676. [DOI] [PubMed] [Google Scholar]
  27. Verhoef J. Transient immunodepression. J Antimicrob Chemother. 1990;26(Suppl):C:23–29. doi: 10.1093/jac/26.suppl_c.23. [DOI] [PubMed] [Google Scholar]
  28. Iagmurov OD. Morphofunctional characteristics of human immune system in surgical stress. Arkh Patol. 1999;61:10–16. [PubMed] [Google Scholar]
  29. Wu HY, Li F, Tang QF. Immunological effects of laparoscopic and open cholecystectomy. J Int Med Res. 2010;38:2077–2083. doi: 10.1177/147323001003800623. [DOI] [PubMed] [Google Scholar]
  30. Shimomura Y. Herpes simplex virus latency, reactivation, and a new antiviral therapy for herpetic keratitis. Nippon Ganka Gakkai Zasshi. 2008;112:247–264. [PubMed] [Google Scholar]
  31. Dubey JP, Benson J, Larson MA. Clinical Sarcocystis neurona encephalomyelitis in a domestic cat following routine surgery. Vet Parasitol. 2003;112:261–267. doi: 10.1016/S0304-4017(03)00019-0. [DOI] [PubMed] [Google Scholar]
  32. Salomon A, Delanghe F, Jeanjean P. Postoperative herpetic meningoencephalitis after lumbar surgery: a case report. Ann Fr Anesth Reanim. 2010;29:732–735. doi: 10.1016/j.annfar.2010.07.007. [DOI] [PubMed] [Google Scholar]
  33. Fontaine F, Fourmaux E, Colin J. Reactivation of ocular toxoplasmosis after laser in situ keratomileusis. J Fr Ophtalmol. 2006;29:e11. doi: 10.1016/S0181-5512(06)73741-X. [DOI] [PubMed] [Google Scholar]

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