High Seroprevalence of Helicobacter Pylori Infection in Inmates: A Case Control Study in a Northern Mexican City

Background The epidemiology of Helicobacter pylori infection in inmates has not been previously studied. Therefore, we determine the seroepidemiology of H. pylori infection in inmates. Methods Through a case-control study, inmates from a state correctional facility in Durango, Mexico and subjects without incarceration of the same city were examined for the presence of anti-H. pylori IgG antibodies using enzyme-linked immunoassays. Seroprevalence association with socio-demographic, incarceration, clinical and behavioral characteristics of the inmates was also investigated. Results Antibodies to H. pylori were found in 140 (83.3%) of 168 inmates and in 101 (60.1%) of 168 controls. Seroprevalence of anti-H. pylori IgG antibodies was significantly higher in inmates than in controls (OR = 3.32; 95% CI: 1.93 - 5.71; P = 0.000002). The seroprevalence of H. pylori infection was not influenced by gender, age, or socioeconomic status of inmates. Seropositivity to H. pylori was found in 3 of 3 inmates with peptic ulcer and in 1 of 2 inmates with gastritis. The seroprevalence of H. pylori exposure was high regardless the jail section, duration (years) in incarceration and number of incarcerations. Multivariate analysis revealed that H. pylori exposure was positively associated with having tattoos (OR = 3.34; 95% CI: 1.14 - 9.70; P = 0.02), and negatively associated with drug abuse (OR = 0.28; 95% CI: 0.11 - 0.70; P = 0.007). Conclusions Seroprevalence of H. pylori exposure in inmates is higher than those found in non-incarcerated people and other populations in the region. Results indicate that inmates may represent a new risk group for H. pylori exposure. Results warrant for further research on the potential role of incarceration and behavioral features of inmates for H. pylori infection.


Introduction
Infections with the bacterium Helicobacter pylori are common among the world's population [1]. The clinical spectrum of infections with H. pylori varies from asymptomatic state to severe gastric disease. Infections with H. pylori cause chronic gastritis, peptic ulcer, gastric mucosa-associated lymphoid tissue lymphoma and gastric cancer [1][2][3][4]. In addition, H. pylori infections have been linked with extra-gastric diseases including sideropenic anemia, idiopathic thrombocytopenic purpura and other conditions [4][5][6]. A number of transmission routes for H. pylori have been reported including oral-oral or fecal-oral [7], person-to-person [8] and consumption of contaminated water [7,9].
The epidemiology of H. pylori infection in inmates has not been studied. Inmates should be considered a group of population with epidemiologic importance for H. pylori infection since they have a number of relevant characteristics for acquiring such infection. In Mexico and probably in other countries, inmates live mostly in overcrowding conditions. Overcrowding may facilitate the oral-oral and fecaloral routes of H. pylori infection. In addition, overcrowding and confinement may facilitate the person to person route of infection with H. pylori too. Therefore, this study was aimed to determine the seroprevalence of anti-H. pylori antibodies in inmates in Durango City, Mexico. In addition, seroprevalence association with socio-demographic, clinical, incarceration and behavioral characteristics in inmates was examined.

Study design and study populations
Through a case-control study using serum samples from previous Toxoplasma gondii and viral hepatitis serosurveys [10,11], 168 inmates (cases) and 168 controls were examined for the presence of anti-H. pylori IgG antibodies. Inclusion criteria for the inmates were: 1) current incarceration in the state correctional in Durango City, Mexico; 2) aged 18 years and older; 3) any gender; 4) incarceration for at least 6 months; and 5) who accepted to participate in the study. Inmates included in the study were 18 -73 (mean = 33.2 ± 10.79) years old: 129 were males and 39 were females. Controls were subjects without incarceration from the same Durango, City. Controls were matched with cases by age and gender. They were 18 -73 (mean = 33.7 ± 11.60) years old: 129 were males and 39 were females. Age was comparable between cases and controls (P = 0.73).

Socio-demographic, clinical, incarceration and behavioral data
A questionnaire was administered to collect socio-demographic, clinical, incarceration and behavioral characteristics of the participants. Socio-demographic items included age, gender, birthplace, residence, marital status, occupation and socioeconomic level. Clinical items included the presence of underlying diseases in general and gastric disease in particular. In women, obstetric history was obtained. Incarceration characteristics assessed included number of incarcerations, jail section and duration of current incarceration. Behavioral items included foreign travel, alcoholism, drug abuse, piercing and tattoos.

Serologic detection of H. pylori antibodies
A commercially available enzyme-linked immunosorbent assay (ELISA) kit, Anti-H. pylori IgG AccuBind ELISA (Monobind Inc, Lake Forest, California) was used to detect IgG antibodies against H. pylori in the serum of the participants. The ELISA used allows qualitative and quantitative analyses of anti-H. pylori IgG antibodies. Anti-H. pylori IgG antibody levels were expressed as Units (U)/mL, and a value higher than 20 U/mL was considered a positive result. All tests were performed following the manufacturer's instructions.

Statistical analysis
Analyses In addition, inmates characteristics with a P value ≤ 0.25 obtained in the bivariate analysis were entered into a multivariate analysis using a conditional backward stepwise logistic regression analysis. Odds ratios (OR) and 95% confidence intervals (CI) were calculated, and a P value < 0.05 was considered statistically significant.

Ethics statement
Only archival serum samples and data from previous surveys were examined in the present study. However, in the previous surveys, the purpose and procedures of the studies were explained to all participants, and a written informed consent was obtained from each participant. This study was approved by the Ethical Committee of the Instituto de Seguridad y Servicios Sociales de los Trabajadores del Estado in Durango City. Of the socio-demographic and incarceration characteristics (Table 1), only two characteristics had P values ≤ 0.25: marital status (P = 0.01) and duration of current incarceration (P = 0.12). Other socio-demographic and incarceration characteristics in inmates including age, gander, birth place, residence, occupation, socioeconomic status, jail section and number of incarcerations had P values > 0.25.

Anti
The seroprevalence of H. pylori infection in healthy inmates (82.0%) was comparable with that (85.5%) found in ill inmates (P = 0.57). There were 3 inmates suffering from peptic ulcer and all 3 were positive for anti-H. pylori antibodies. In addition, there were 2 inmates suffering from gastritis and one of them was positive for anti-H. pylori antibodies. None of the obstetric characteristics in women including pregnancies, deliveries, cesarean sections and abortions was associated with H. pylori seropositivity.
Of the behavioral characteristics of inmates examined (Table 2), the following variables had P values ≤ 0.25 in the bivariate analysis: national trips (P = 0.24), traveled abroad (P = 0.22), drug abuse (P = 0.04) and having tattoos (P = 0.20). Multivariate analysis of socio-demographic, incarceration and behavioral characteristics of inmates that had P values ≤ 0.25 in the bivariate analysis revealed that only 2 characteristics were associated with H. pylori seropositivity: having tattoos had a positive association (OR = 3.34; 95% CI: 1.14 -9.70; P = 0.02), and drug abuse had a negative association (OR = 0.28; 95% CI: 0.11 -0.70; P = 0.007).

Discussion
In the present study, a statistically significant difference in H. pylori seropositivity between inmates and controls was found. Remarkably, inmates had a higher seroprevalence of H. pylori exposure than controls. In addition, the seroprevalence found in inmates (83.3%) represents the highest seroprevalence reported in people in the region so far. In recent studies in ethnic groups in Durango, Mexico, the seroprevalences of H. pylori exposure in Mennonites [12] and Tepehuanos [13] were 50.7% and 66.0%, respectively. The seroprevalence found in inmates is also higher than a 66.7% seroprevalence found in waste pickers in Durango City [14]. Furthermore, the seroprevalence found in inmates is higher than the mean national seroprevalence (66%) reported in Mexico [15]. It is not clear why inmates had a higher serop-revalence of H. pylori exposure than controls. However, all known routes for H. pylori infection including oral-oral or fecal-oral [7], person-to-person [8] and consumption of contaminated water [7,9] might be present in inmates. In contrast, such routes of transmission in non-incarcerated people might be less frequent. Inmates live mostly in overcrowding conditions in Mexico and such factor might account for transmission of H. pylori infection by the oral-oral and fecal-oral routes. Crowding has been found associated with H. pylori infection [15][16][17] and is clearly an important factor that could contribute for explaining the high seroprevalence of H. pylori in inmates. Of the socio-demographic, incarceration and behavioral characteristics of inmates, multivariate analysis revealed that H. pylori seropositivity was positively associated with having tattoos and negatively associated with drug abuse (OR = 0.28; 95% CI: 0.11 -0.70; P = 0.007). Such associations were unexpected. To the best of our knowledge H. pylori seropositivity has not been associated with having tattoos and drug abuse. It is not clear why inmates with tattoos had a higher seroprevalence of H. pylori exposure than those without tattoos. It is uncertain whether H. pylori can be transmitted by tattooing. It is possible that inmates with tattoos have had an unknown behavioral risk for H. pylori infection. Further studies to confirm or challenge the association of H. pylori infection with having tattoos are needed. On the other hand, the negative association of drug abuse with H. pylori is intriguing too. We are not aware of previous reports of such association. It is not clear why inmates with drug abuse had a lower seroprevalence of H. pylori exposure than inmates without drug abuse. This finding might just indicate that drug abuse did not have any role in H. pylori infection. Nevertheless, it raises the question whether any drug used by inmates might have an adverse effect against H. pylori. It is also possible that inmates without drug abuse have had an unknown behavioral risk factor for H. pylori. Further studies to confirm or challenge the negative association of H. pylori infection with drug abuse are needed.
The seroprevalence of H. pylori exposure in inmates is higher than those found in non-incarcerated people and other reported seroprevalences in the region. Results indicate that inmates represent a new risk group for H. pylori exposure. Results warrant for further research on the potential role of incarceration and behavioral features of inmates for H. pylori infection.