Prevalence and risk factors of helicobacter pylori in Turkey: a nationally-representative, cross-sectional, screening with the 13C-Urea breath test

  • Nilufer Ozaydin1Email author,

    Affiliated with

    • Sinan A Turkyilmaz2 and

      Affiliated with

      • Sanda Cali1

        Affiliated with

        BMC Public Health201313:1215

        DOI: 10.1186/1471-2458-13-1215

        Received: 31 July 2013

        Accepted: 13 December 2013

        Published: 21 December 2013

        Abstract

        Background

        Helicobacter pylori is an important global pathogen infecting approximately 50% of the world’s population. This study was undertaken in order to estimate the prevalence rate of Helicobacter pylori infections among adults living in Turkey and to investigate the associated risk factors.

        Method

        This study was a nationally representative cross sectional survey, using weighted multistage stratified cluster sampling. All individuals aged ≥18 years in the selected households were invited to participate in the survey. Ninety two percent (n = 2382) of the households in 55 cities participated; 4622 individuals from these households were tested with the 13C-Urea breath test. Helicobacter pylori prevalence and associated factors were analysed by the t test, chi square and multiple logistic regression with SPSS11.0.

        Results

        The weighted overall prevalence was 82.5% (95% CI: 81.0-84.2) and was higher in men. It was lowest in the South which has the major fruit growing areas of the country. The factors included in the final model were sex, age, education, marital status, type of insurance (social security), residential region, alcohol use, smoking, drinking water source. While education was the only significant factor for women, residential region, housing tenure, smoking and alcohol use were significant for men in models by sex.

        Conclusion

        In Turkey, Helicobacter pylori prevalence was found to be very high. Individuals who were women, elderly adults, single, had a high educational level, were living in the fruit growing region, had social security from Emekli Sandigi, were drinking bottled water, non smokers and regular alcohol consumers, were under less risk of Helicobacter pylori infection than others.

        Keywords

        Helicobacter pylori prevalence Risk factors of helicobacter pylori infection Smoking Alcohol use

        Background

        Helicobacter pylori was first discovered in 1983, and eleven years later in 1994 the International Agency for Research on Cancers (IARC) classified H.pylori as a definite class 1 carcinogen [1, 2]. It is a small, spiral, gram-negative bacillus which inhabits the mucus layer overlying the gastric epithelial cells in humans. It produces a potent urease. The isolation of H.pylori from the human gastric mucosa and the demonstration of its involvement in gastritis, peptic ulcer disease and gastric cancers have radically changed our perception of these diseases. Development of atrophy and metaplasia of the gastric mucosa are strongly associated with H.pylori infection [25].

        The greatest risk for infection appears to be during childhood and early adult years [6]. Although infected individuals often have histological evidence of gastritis, the vast majority of infections are asymptomatic [2]. Current evidence indicates that disparate disease outcomes are not related solely to the genetic diversity of H.pylori, but also to host factors and environmental agents [7]. Further delineation of the host response to infection, to specific environmental exposures or to bacterial virulence factors is required to identify which patients infected with H.pylori are at greatest risk of developing disease. Identifying and understanding such interactions should promote the development of optimal outcomes.

        H.pylori is a public health problem in both developed and developing countries [8]. The IARC has stressed that the need for effective, population based screening programs is essential for tackling cancer [9].

        Most previous studies have been carried out in clinical settings on small samples. There is limited evidence concerning the prevalence, determinants and mode of infection in representative population samples. This is the first population based study of a country-wide representative sample with a high response rate using the most sensitive and specific test the 13Carbon Urea Breath Test (13C-UBT) to have been carried out in Turkey. The aim of this survey was to estimate the prevalence rate of H.pylori infection among adults aged ≥18 years and to investigate the factors associated with an H.pylori infection in Turkey.

        Methods

        Study population

        A study of the prevalence and risk factors of H.pylori infection in Turkey (TURHEP) was a nationally representative, population based cross-sectional screening with the 13C-Urea Breath Test. A weighted, multistage, stratified cluster sampling approach was used in the selection of the sample. For this study, 100 different residential areas were selected as clusters for an optimal distribution with a target sample size of 2500 selected households based on the results of the General Population Count of Turkey held in 2000 (Additional file 1: Figure S1). Households which were to be visited in each cluster were selected randomly by the Turkish Statistical Institute.

        The eligible individuals were all those aged ≥ 18 who had been present in the selected household on the night before the day of the visit. Among the individuals interviewed those who had undergone a gastrectomy, who had used antibiotics during the preceding 30 days or who had used any proton pump inhibitors during the preceding 14 days were excluded from the survey. The next step was the performance of the 13C-UBT on those who accepted this test [10, 11] (Figure 1).
        http://static-content.springer.com/image/art%3A10.1186%2F1471-2458-13-1215/MediaObjects/12889_2013_6113_Fig1_HTML.jpg
        Figure 1

        Flowchart of TURHEP study in Turkey.

        Breath sample collection

        At the first visit, eligible and willing people were informed about a required minimal six-hour period of fasting. At the second visit, after ensuring that they had fasted, two breath samples were collected as first samples. The test solution, 75 mg 13C-urea in 30 ml drinkable water (Helicobacter Test INFAI, Germany), was given after 200 ml of standard orange juice had been drunk. Thirty minutes later two breath samples were taken. Samples were measured by isotope ratio mass spectrometry (IRMS) in Istanbul between August 2003 and February 2004.

        The test results were evaluated as H.pylori-negative when the 13C difference between 0th minute sample and 30th minute sample was lower than 4.00 and as H.pylori-positive when it was equal to or higher than 4.00.

        Ethical issues

        The study protocol was reviewed and approved by the Research Ethics Committee of the School of Medicine of Marmara University. All participants signed a written informed consent.

        IRMS measurements were performed in the University and a trained technician employed by Marmara Health Education and Research Foundation measured the samples during the period of the study.

        Variable definitions

        The primary outcome variable, the results of the H.Pylori UBT were categorized as positive or negative. Demographic variables (age, sex, residential region, geographic region, marital status, education), economic status (occupation, social security status 1a(Emekli Sandigi, SSK, BAG-KUR, Green Card, private insurance, foreign insurance or none), housing tenure, environmental condition (number in household, bedrooms, source of drinking water, type of toilet system, source of heating) in or out of the home as well as cigarette and alcohol consumption were considered in the analysis.

        The geographic regions defined five major regions of the country (West, South, Central, North and East) (Additional file 1: Figure S1).

        Statistical methods

        All analyses incorporated sampling weights that were adjusted for the complex study design of TURHEP.

        The characteristics of H.pylori-positive and H.pylori-negative participants were compared using the chi-square test for categorical variables and the two sample t-test for continuous variables.

        Odds ratios (OR) and 95% confidence intervals (CI) for the association between H.Pylori infection and each potential risk factor were estimated using multivariable logistic regression models. The covariates included in the models were those significantly associated with H.Pylori in the univariate analyses (p < 0.05). The group presenting the lowest infection risk was chosen as the indicator. The final model was developed using a stepwise procedure with backward elimination, with inclusion and exclusion criteria set at the significance level of 0.05 and 0.10 respectively. The multiple logistic regression model fit was determined by the Hosmer-Lemeshow test statistic. A model fits the data if the Hosmer-Lemeshow statistic has a p > 0.05. Significant predictors were identified and ORs calculated with 95% CIs. The following variables were considered in the model: sex, age, region (West, South, Central, North, East), residence (urban, rural), marital status (never married, currently married, widowed/divorced), education level (no education, primary complete, secondary complete, high school +), type of insurance (Emekli Sandigi, private/foreign, BAG KUR, SSK, none, green-card), occupation (employed/unemployed) housing-tenure (owned by a household-member, lodging/no-rent paid), household population per bedroom, source of drinking-water (bottled-water, piped-water, public-fountain, others:‘river/rain-water/etc.’, smoking (never, current-nonsmoker, current-occasional-smoker, regular-smoker) and alcohol consumption (regular drinker, current occasional-drinker, current non-drinker, never).

        Results

        In TURHEP, 2382 households in 100 clusters from 55 cities (Among 81 cities) were available for interview (Additional file 1: Figure S1) and 91.8% were successfully interviewed. The household response rate for urban areas were 89.9% and for rural areas 96.0% (Table 1, Figure 1). The main reasons that the field teams were unable to interview was that some of the houses were vacant at the time of the interview or household members were away for an extended period.
        Tables 1

        Results of the household, individual interviews and breathe samples

         

        Residence

         

        Results

        Urban

        Rural

        Total

        Household Interviews

           

        Dwellings sampled

        1753

        751

        2504

        Households found

        1652

        730

        2382

        Households interviewed

        1485

        701

        2186

        Household Response Rate (%)

        89.9

        96.0

        91.8

        Individual Interviews

           

        Eligible individual

        3616

        1939

        5555

        Eligible individual interviewed

        3611

        1938

        5549

        Eligible Individual Response Rate (%)

        99.9

        99.9

        99.9

        13 C-UBT’s

           

        Number of people who had gastrectomy

        0

        1

        1

        Number of the people who had antibiotic treatment during the last 30 days

        294

        78

        372

        Number of people who used PPI during the last 14 days

        174

        68

        242

        Eligible people for test

        3174

        1799

        4973

        Eligible people tested

        2941

        1722

        4663

        Eligible people tested rate (%)

        92.6

        95.7

        93.7

        Among 5555 eligible individuals in households, 5549 were successfully interviewed (99.9%). The total number of eligible people for breath test was 4973 and of these 4663 breath samples were collected (93.7%). Three hundred and seventy two individuals who had used antibiotic therapy for any reason during the last 30 days, 242 individuals who had used proton- pump inhibitors during the last 14 days and 1 person who had had a gastrectomy were excluded. The main reason for failure to collect breath samples from the eligible people was that they could not stand the 6-hour fast or were unwilling to undertake the 6-hour fast. Also, a number of eligible individuals were obliged to be outside or working after 6 hrs and a few people did not agree to give breath samples although they gave no reason.

        Of the 4663 breath samples, 4622 were measured (99.1%). Forty one breath-samples could not be measured for technical reasons (Table 1).

        The basic socio-demographic characteristics and H. pylori infection

        The H.pylori infection prevalence was 82.5% in the population aged ≥18. It was more prevalent in men than women after controlling for confounding factors (Tables 2 and 3, Additional file 2: Figure S2). There was an inverse association between age and H.pylori infection (OR:0.98, 95%CI 0.97-0.99) (Tables 2 and 3). Those living in Central or Eastern Turkey were more at risk than those living in Southern Turkey (Tables 2 and 3, Additional file 2: Figure S2).
        Table 2

        Socio-demographic factors associated with Helicobacter pylori infection

        Socio-demographic factors

        Hp positive

        Hp negative

         
         

        n

        (%)*

        n

        (%)*

        Total

        P**

        Sex

              

        Female

        2075

        (81.4)

        457

        (18.6)

        2532

        0.014

        Male

        1777

        (83.9)

        313

        (16.1)

        2090

         

        Age groups

              

        18–24

        736

        (79.6)

        170

        (20.4)

        906

        0.000

        25–34

        957

        (86.3)

        145

        (13.7)

        1102

         

        35–44

        746

        (84.2)

        123

        (15.8)

        869

         

        45–54

        599

        (83.7)

        108

        (16.3)

        707

         

        55–64

        372

        (78.9)

        99

        (21.1)

        471

         

        65 +

        442

        (78.6)

        125

        (21.4)

        567

         

        Region

              

        West

        1027

        (80.3)

        247

        (19.7)

        1274

        0.000

        South

        444

        (78.7)

        118

        (21.3)

        562

         

        Central

        1089

        (85.0)

        192

        (15.0)

        1281

         

        North

        369

        (82.3)

        83

        (17.8)

        452

         

        East

        923

        (88.1)

        130

        (11.9)

        1053

         

        Residence

              

        Urban

        2411

        (81.7)

        509

        (18.3)

        2920

        0.020

        Rural

        1441

        (84.0)

        261

        (16.0)

        1702

         

        Total

        3852

        (82.5)

        770

        (17.5)

        4622

         

        *weighted , **p based on X2 test.

        Table 3

        Adjusted odds ratios for Helicobacter pylori positivity for various risk factors in final model

        Variable and categories

        B

        P

        OR

        95% CI

        Sex

             

          Female

          

        1.0

          

          Male

        0.217

        0.035

        1.242

        1.015,

        1.519

        Age

        -0.015

        0.000

        0.986

        0.979,

        0.992

        Education

             

          High school +

          

        1.0

          

          No education

        0.484

        0.003

        1.623

        1.176,

        2.239

          Primary complete

        0.511

        0.000

        1.666

        1.333,

        2.083

          Secondary complete

        0.405

        0.013

        1.499

        1.091,

        2.059

        Marital status

             

          Never married

          

        1.0

          

          Widowed/Divorced

        0.425

        0.030

        1.530

        1.042,

        2.246

          Currently married

        0.554

        0.000

        1.739

        1.378,

        2.197

        Social security

             

          Emekli sandigi

          

        1.0

          

          Private/foreign

        -0.532

        0.187

        0.587

        0.266,

        1.295

          BAG-KUR

        0.009

        0.952

        1.009

        0.757,

        1.345

          SSK

        0.450

        0.001

        1.568

        1.213,

        2.026

          None

        0.439

        0.002

        1.550

        1.174,

        2.048

          Green Card

        0.383

        0.077

        1.467

        0.960,

        2.241

        Source of drinking water

             

          Bottled water/demijohn/pet water

          

        1.0

          

          Piped water (in house/garden/outside)

        0.572

        0.000

        1.772

        1.404,

        2.236

          Spring/public fountain

        0.517

        0.002

        1.677

        1.218,

        2.308

          Other (river. rain water etc.)

        0.495

        0.008

        1.640

        1.135,

        2.371

        Smoking

             

          Never

          

        1.0

          

          Tried at past. currently non-smoker

        0.038

        0.750

        1.039

        0.821,

        1.316

          Tried at past. currently occasional smoker

        -0.003

        0.985

        0.997

        0.703,

        1.413

          Regular smoker

        0.350

        0.005

        1.419

        1.113,

        1.808

        Alcohol

             

          Regular consumer

          

        1.0

          

          Tried at past. currently drinking occasionally

        0.586

        0.028

        1.798

        1.066,

        3.032

          Tried at past. currently non-drinker

        0.687

        0.012

        1.988

        1.161,

        3.403

          Never

        0.692

        0.010

        1.997

        1.182,

        3.374

        Region

             

          South

          

        1.0

          

          West

        0.186

        0.147

        1.204

        0.937,

        1.549

          North

        0.172

        0.343

        1.188

        0.832,

        1.696

          Central

        0.382

        0.007

        1.466

        1.111,

        1.934

          East

        0.563

        0.001

        1.756

        1.264,

        2.439

        Constant

        -0.473

        0.173

        0,623

          

        Variables entered in the model: sex, age, residence, region, marital status, education, social security, occupation, housing tenure, source of drinking water, the number of the household per sleeping room, smoking, and alcohol consumption.

        Socio-economic status and H.pylori infection

        A current H.pylori infection was associated with education, social-security status and water supply (Tables 4 and 3). Occupation, the number in the household, the source of heating and the total monthly family income were not in the final logistic regression models. Housing tenure was the only significant factor in the men’s model (Table 5). There was an inverse association of educational level and H.pylori infection; individuals with lower educational levels had a higher risk than high school graduates and those with a higher education.
        Table 4

        Socio-economic factors associated with Helicobacter pylori infection

        Socio-economic Factors

        Hp positive

        Hp negative

          
         

        n

        (%)*

        n

        (%)*

        Total

        p

        Education (n = 4577)

              

          No education

        747

        (82.6)

        163

        (17.4)

        910

        0.000

          Primary complete

        1801

        (86.0)

        276

        (14.0)

        2077

         

          Secondary complete

        355

        (85.2)

        59

        (14.8)

        414

         

          High school +

        913

        (75.4)

        263

        (24.6)

        1176

         

        Social security** (n = 4573)

              

          SSK

        1266

        (83.9)

        228

        (16.1)

        1494

        0.000

          Emekli sandigi

        431

        (74.5)

        139

        (25.5)

        570

         

          BAG-KUR

        546

        (78.5)

        148

        (21.5)

        694

         

          Green Card

        324

        (87.2)

        42

        (12.8)

        366

         

          Private/foreign

        21

        (63.9)

        10

        (36.1)

        31

         

          None

        1223

        (85.4)

        195

        (14.6)

        1418

         

        Housing tenure (n = 4597)

              

          Owned by a household member

        2761

        (81.6)

        583

        (18.4)

        3344

        0.05

          Rented

        762

        (84.5)

        134

        (15.5)

        896

         

          Lodging/no money paid

        306

        (85.3)

        51

        (14.7)

        357

         

        Occupation (n = 4503)

              

          Agriculture & animal husbandry

        516

        (86.0)

        83

        (14.0)

        599

        0.000

          Industry

        228

        (86.0)

        35

        (14.0)

        263

         

          Construction

        111

        (92.7)

        9

        (7.3)

        120

         

          Service

        360

        (78.7)

        87

        (21.3)

        447

         

          Housewife/retired/unemployed

        522

        (78.7)

        120

        (21.3)

        642

         

          Other

        2021

        (82.9)

        411

        (17.1)

        2432

         

        Household population

              

          1–3 person/home

        1000

        (79.3)

        250

        (20.7)

        1250

        0.000

          4–5 person/home

        1592

        (81.4)

        334

        (18.6)

        1926

         

          6 + person/home

        1260

        (87.3)

        186

        (12.7)

        1446

         

        Rooms for sleeping (n = 4575)

              

          1–2

        2354

        (82.2)

        482

        (17.8)

        2836

        0.06

          3–4

        1382

        (82.5)

        277

        (17.5)

        1659

         

          5 +

        73

        (93.0)

        7

        (7.0)

        80

         

        Source of the drinking water (n = 4594)

              

          Piped water (in house/garden/outside)

        2342

        (83.6)

        445

        (16.4)

        2787

        0.00

          Spring/public fountain

        726

        (83.8)

        141

        (16.2)

        867

         

          Bottled water/demijohn/pet water

        327

        (72.9)

        109

        (27.1)

        436

         

          Other ((river, rain water etc.))

        430

        (85.4)

        74

        (14.6)

        504

         

        Type of toilet system (n = 4598)

              

          Connected to drainage system

        2778

        (82.6)

        551

        (17.4)

        3329

        0.76

          Closed pit

        1033

        (81.9)

        215

        (18.1)

        1248

         

          Other (No facility)

        18

        (86.7)

        3

        (13.3)

        21

         

        Source of heating (n = 4553)

              

          Radiator (Central heating)

        366

        (75.0)

        102

        (25.0)

        468

        0.00

          Radiator (Private)

        147

        (71.0)

        62

        (29.0)

        209

         

          Natural gas stove

        83

        (84.8)

        14

        (15.2)

        97

         

          Stove (Cool/wood)

        2985

        (84.4)

        536

        (15.6)

        3521

         

          Animal excrement

        103

        (86.4)

        17

        (13.6)

        120

         

          Electricity

        85

        (83.7)

        18

        (16.3)

        103

         

          Gas stove

        28

        (78.0)

        7

        (22.0)

        35

         

        Family income (USD/month)*** (n = 4194)

              

          14–179

        874

        (84.6)

        147

        (15.4)

        1021

        0.00

          183–394

        1472

        (83.7)

        272

        (16.3)

        1744

         

          398–538

        503

        (83.8)

        103

        (16.2)

        606

         

          541 +

        632

        (75.1)

        191

        (24.9)

        823

         

          Total

        3852

        (82.5)

        770

        (17.5)

        4622

         

        *Weighted, **The group (disabled / orphan hood payment by government, n = 29) is excluded. ***1 USD = 1 395 000 TL.

        Table 5

        Adjusted odds ratios for Helicobacter pylori positivity for various risk factors by sex

         

        Sex

         

        Men

        Women

        Variables

        B

        P

        OR

        CI 95%

        B

        P

        OR

        CI 95%

        Age

        -0.013

        0.009

        0.987

        0.977,

        0.997

        -0.013

        0.005

        0.987

        0.978,

        0.996

        Education

                  

          High school +

               

        1.0

          

          No education

             

        0.813

        0.000

        2.254

        1.517,

        3.350

          Primary complete

             

        0.762

        0.000

        2.142

        1.593,

        2.880

          Secondary complete

             

        0.679

        0.006

        1.971

        1.213,

        3.203

        Marital Status

                  

          Never married

          

        1.0

            

        1.0

          

          Widowed/Divorced

        0.450

        0.242

        1.568

        0.738,

        3.335

        0.294

        0.209

        1.342

        0.848,

        2.122

          Currently married

        0.551

        0.005

        1.735

        1.182,

        2.547

        0.537

        0.000

        1.712

        1.272,

        2.304

        Social Security

                  

          Emekli sandigi

          

        1.0

            

        1.0

          

          Private/foreign

        0.541

        0.428

        1.718

        0.451,

        6.546

        -1.216

        0.023

        0.296

        0.104,

        0.848

          BAG-KUR

        0.385

        0.083

        1.469

        0.951,

        2.269

        -0.186

        0.339

        0.831

        0.568,

        1.215

          SSK

        0.768

        0.000

        2.155

        1.478,

        3.140

        0.276

        0.110

        1.317

        0.940,

        1.847

          None

        0.894

        0.000

        2.444

        1.632,

        3.661

        0.178

        0.340

        1.194

        0.829,

        1.720

          Green Card

        0.593

        0.068

        1.809

        0.956,

        3.422

        0.302

        0.290

        1.353

        0.773,

        2.369

        Housing Tenure

                  

          Owned by household members

          

        1.0

               

          Rented

        0.276

        0.109

        1.317

        0.940,

        1.845

             

          Lodging/no money paid

        0.692

        0.034

        1.997

        1.055,

        3.779

             

        Source of Drinking Water

                  

          Bottled water/demijohn/pet

          

        1.0

            

        1.0

          

          Piped water

        0.418

        0.023

        1.518

        1.060,

        2.174

        0.684

        0.000

        1.981

        1.477,

        2.657

          Spring/public fountain

        0.073

        0.763

        1.076

        0.669,

        1.728

        0.901

        0.000

        2.461

        1.644,

        3.684

          Other (river. rain water etc.)

        0.808

        0.012

        2.244

        1.198,

        4.204

        0.438

        0.050

        1.550

        1.001,

        2.402

        Smoking

                  

          Never

          

        1.0

               

          Tried at past. currently non-smoker

        0.167

        0.381

        1.182

        0.813,

        1.719

             

          Tried at past. currently occasional smoker

        -0.073

        0.792

        0.929

        0.539,

        1.602

             

          Regular smoker

        0.449

        0.017

        1.566

        1.083,

        2.264

             

        Alcohol

                  

          Regular consumer

          

        1.0

               

          Tried at past. currently drinking occasionally

        0.731

        0.009

        2.078

        1.202,

        3.590

             

          Tried at past. currently non-drinker

        0.764

        0.009

        2.148

        1.214,

        3.799

             

          Never

        0.779

        0.007

        2.180

        1.243,

        3.822

             

        Region

                  

          South

          

        1.0

               

          West

        0.423

        0.032

        1.526

        1.037,

        2.246

             

          North

        0.451

        0.118

        1.570

        0.891,

        2.764

             

          Central

        0.653

        0.002

        1.922

        1.258,

        2.936

             

          East

        0.816

        0.002

        2.262

        1.353,

        3.782

             

        Constant

        -0.404

        0.388

        0.668

          

        0.335

        0.172

        1.398

          

        Variables entered in the model: age, residence, region, marital status, education, social security, occupation, housing tenure, source of drinking water, the number of the household per sleeping room, smoking, alcohol consumption.

        Social security status was the only socio-economic status indicator in the final models. Those who had SSK and no social security were at greater risk than those who had insurance of Emekli Sandigi (Table 3).

        The source of drinking water was a significant factor in the final models. The people who used piped water, spring/public fountain and other (river, rain water etc.) were at greater risk than those who used bottled water/demijohn/PET bottled water as drinking water (Table 3).

        Housing was a significant factor only in the men’s model. Men lodging/or paying no money for their housing were at more risk than those who lived in a house owned by a household member (Table 5).

        Lifestyle factors and prevalence of H.pylori infection

        Smoking and alcohol consumption were associated with H.pylori infection. Regular smokers were at higher risk than non smokers. But this association did not hold for females (Tables 6 and 5). In contrast, regular alcohol consumption was a protective factor for H.pylori infection. All of those who never drink alcohol, those who had only tried in the past and the occasional drinkers had a higher risk than regular alcohol consumers (Tables 6 and 5).
        Table 6

        Lifestyle factors associated with Helicobacter pylori infection

        Lifestyle factors

        Hp positive

        Hp negative

          
         

        n

        (%)*

        n

        (%)*

        Total

        P

        Smoking cigarettes (n = 4605)

              

          Never

        1662

        (80.8)

        370

        (19.2)

        2032

        0.00

          Tried at past, currently non-smoker

        745

        (81.6)

        159

        (18.4)

        904

         

          Tried at past, currently occasional smoker

        245

        (82.4)

        47

        (17.6)

        292

         

          Regular smoker

        1190

        (85.9)

        187

        (14.1)

        1377

         

        Drinking alcohol (n = 4593)

              

          Regular consumer

        69

        (74.7)

        18

        (25.3)

        87

        0.03

          Others

        3762

        (82.8)

        744

        (17.2)

        4506

         

        Total

        3852

        (82.5)

        770

        (17.5)

        4622

         

        * Weighted.

        Analysis of factors and H.pylori infection by sex

        Since sex was a significant factor for H.pylori infection it was necessary to analyze factors separately for each sex. In men, age, marital status, social security status, housing tenure, type of drinking water, smoking, alcohol use and geographic region were factors. However, for women, age, marital status, social security status, type of drinking water and education were factors (Table 5).

        Discussion

        So far as we know this study is the most representative one that is based on a sample derived from the population of one country, estimating the factors associated with the prevalence of Helicobacter pylori infection and using the 13C-UBT. Furthermore, the response rates were very high. In this study, it was produced highly significant estimates [Design effect (DEFT) = 2.01 and standard error = 0.008].

        Awareness of Helicobacter pylori is little more than a decade old. Yet there have been many studies all over the world about its epidemiology. Most prevalence data have used random sampling of blood donors, clinic attendees or industrial employees; none of these groups provides a truly normal population as emphasised by Pounder [12].

        Studies that have used labelled breath tests in a normal population to detect Helicobacter pylori infection are very rare. However, they are highly sensitive, specific and are also recommended by the Maastricht 2–2000 Consensus Report and by the Canadian Helicobacter Study Group Consensus conference, 2004 [7, 13, 14].

        When comparing the rates from previous studies directly with our study, it should be kept in mind that other studies also differ from ours in terms of variation by age, type of population, type of diagnostic test and study time at which the study was done.

        In TURHEP, the weighted overall prevalence of Helicobacter pylori infection was 82.5% (95% CI 81.0-84.2) with 13C-UBT. Helicobacter pylori prevalence has been reported to reach 70% or more in developing countries and to be less than 40% in developed countries [1537].

        There was an inverse association between age and infection in our study. Earlier studies have shown differing trends regarding age and Helicobacter pylori prevalence. Whereas Helicobacter pylori prevalence increased with age at earlier ages, there was a slight decrease in populations over 60 years of age in France and over 50 years in the other countries (Vietnam, Algeria and Ivory Coast) [15]. Infection increased up to the 40–49 age group, then decreased in analyses for Southern Brazil and Northern India [17, 30]. Also, the prevalence peaked at ages 45 to 64 and dropped after the age 65 in Chile and the Czech Republic [31, 37]. In Ankara (Turkey), seroprevalence was 58.4% for ages 15–19, 62.6% for ages 20–29, 67.6% for ages 30–39, 81.3% for ages 40–49 and 66.3% for over 50 years [38]. In India also the prevalence was increasing to 100% by 60 then decreasing to 80% by 70 years (n = 238, ages 3–70) and in Athens, whereas the seroprevalence was increasing from 14.2% for ages 15–24 to 67.4% for ages 55–64, it decreased to 57.9% for ages >65 [18, 32]. Only in Beninese populations, in 2005 (n = 446, over 2 years old) no association was found between seroprevalence and age [28]. In contrast, some studies claimed that Helicobacter pylori prevalence increased with age [15, 16, 19, 21, 2426, 29, 3335, 3943].

        We found that men in Turkey were at greater risk than women for Helicobacter pylori infection. Likewise, in Northern California, men had a higher prevalence of antibodies across all strata of race/ethnicity, age, education and income (OR = 2.0, 95% CI 1.2-3.1) [42]. Also, in Northern Ireland, infection was more common in males (60.9%) than females (55.2%, p < 0.01, Or for males versus females was 1.19 (95% CI 1.02-1.40) [35]. In Leeds (UK), Spain and Chile, it was higher in men [31, 36, 44]. Conversely, in some studies, which mostly had small samples, there was no difference found in Helicobacter pylori prevalence between the sexes [1518, 21, 22, 2426, 28, 29, 34, 3739],[43]. To our knowledge, only one study from Israel found that the relative risk of Helicobacter pylori infection was increased in women smokers [19]. We agree with Moayyedi-et-al. that the positive association of Helicobacter pylori with the male sex should probably not be interpreted as a direct causal relationship [36]. The reason for the possible gender difference is unclear but may relate to young boys having poorer hygiene than young girls. Because of social gender roles in Turkey, men seek less healthy facilities for toilet needs than women, and men are outdoors more than women, which brings more risks of infection. Further, men tend to participate in more of the risky behaviours such as smoking, alcohol drinking than women.

        The current residential region was found to be a risk factor for H.pylori infection. In Turkey, the western areas are more developed, more crowded, better educated, and have better housing conditions; families are smaller than in the East. The reason why H.pylori infections are lowest in individuals living in the South must be related to this being a major area for growing citrus fruits. These contain high levels of Vitamin C. People in the South can eat oranges, lemons, tangerines or bitter oranges frequently and continuously or drink the juices because citrus fruits are cheap and plentiful all the year round. It is known that Vitamin C is effective in the prevention of most infections. Also H.pylori can be expected not to survive in acidic gastric conditions produced by the acidic citrus fruits. Moreover, for regular smokers the highest H.pylori prevalence may result from an interaction between tobacco and Vitamin C. In contrast, the highest H.pylori infections were found in subjects living in eastern Turkey, which has the least available citrus fruits; they cannot be grown, and snow prevents their transport for several months each year; Besides, this region is the least developed. Although in TURHEP, dietary habits and daily consumptions were not included, supportive studies are available [4548]. Additionally, garlic is frequently used in southern Turkey. One study presented garlic as a possible protective factor for gastric lesions with H.pylori infection [46].

        Some studies with small sample sizes comparing the regions are available from Turkey. H.pylori infection was found to be 73.8% in the West, 48%-81% in the Central, 60%-85.4% in the Eastern parts of the country [38, 39, 4951].

        In most of studies it was found that H.pylori infections were inversely related to level of education [16, 22, 24, 34, 37, 42, 43]. Likewise in TURHEP, the lower the education of the subjects, especially for females, the higher the risk for H.pylori infection. However, two other studies found no association [19, 28].

        The status of social security was a significant factor in the TURHEP study’s final model and in the models by sex. To our knowledge, this variable has not previously been used as a socio-economic status indicator in any study related with H.pylori infection. Some previous studies have presented an inverse association between H.pylori infection and family income as a socio-economic status indicator [29, 38, 42, 43, 5254]. In TURHEP, the lower the income of the subjects, the higher the infection, but only in a univariate analysis. Some researchers have also studied the association between infection and social class/socio-economical class. In Korea in adults, the rate of infection was high and independent of socio-economic class. However, in children, it was inversely related to the socio-economic class of the child’s family [21]. In Northern Ireland, the adjusted OR of infection in subjects from manual workers relative to those from non-manual occupations was 1.7 (95% CI: 1.47-1.98) [35]. In Northern England, infection was more common in the lower social class groups [36]. In Libya, 91% of a low socio-economic class was H.pylori-positive, while those of middle and high socio-economic classes showed 53% and 57% positivity respectively [24]. In Northern India infection was not associated with socio-economic status [17].

        Housing tenure, as another socio-economic indicator was found significant only in a model for males in TURHEP. In contrast, another study, showed no association between prevalence of H.pylori and type of housing (owned/rented)[21].

        In TURHEP, a water- H.pylori infection association was found in the final models. This association is a question about H.pylori infection being one of the water-borne contagious diseases. This association was mentioned in many studies from different parts of the world and it has been found that there is mostly a positive significant relation [1, 21, 25, 52]. On the other hand, no association was found in studies from Benin and Turkey [28, 39].

        Smoking was a significant factor for H.pylori infection in TURHEP except for the female model. Similar results have been presented in some studies [19, 3537]. However smoking was not associated with H.pylori infection in some other studies [15, 16, 21, 23, 30, 34, 43].

        In TURHEP, regular alcohol consumption was found to be a protective factor except for the females model. Similar results have also been presented in some earlier studies [5356]. In a EUROGAST Study, a univariate analysis showed that alcohol consumption was associated with a reduced prevalence of H.pylori, but this effect disappeared completely after adjustment in the multivariate analysis [34]. No association was found between H.pylori and alcohol use in other studies [15, 21, 30, 35, 36].

        Conclusions

        In Turkey, H.pylori prevalence was found to be very high. Individuals, who were women, elderly adults, single, at high educational levels, living in southern Turkey, having social security of Emekli Sandigi, drinking bottled water, non-smokers and regular alcohol consumers, were under less risk of H.pylori infection than others.

        In the TURHEP study, whereas prevalence was estimated as 82.5% (95%CI 81.0-84.2) in the adult population, age, sex, education and marital status were suggested as playing critical roles as co-factors for H.pylori infection. Social security, housing tenure and also water have dependant role. Whereas smoking, a common habit especially in men was positively associated, alcohol use, not as common as smoking, was a protective factor for H.pylori. Living in the southern region of Turkey, a citrus fruit growing area, is seen as a protective factor for H.pylori infection and was the most interesting result in TURHEP.

        We have presented high quality data from normal, healthy individuals, representative of the whole country, from Turkey. The results of the TURHEP study, offer important public health implications for the prevention of H.pylori. In the future, cohort studies should be implemented to help define more significant risk factors.

        Endnotes

        aEmekli Sandigi: The pension fund for civil servants, SSK ‘Social Security Institution’ the insurance of employee, BAG-KUR: the insurance of tradesman, artists and other freelance workers, Green-Card: limited insurance of people do not have any other insurance.

        Declarations

        Acknowledgements and funding

        The research leading to these results has received funding from SANDOZ Pharmaceutical Company and Marmara Health Education and Research Foundation.

        The authors thank the members of Public Health Department of the School of Medicine of Marmara University, data collectors, all participants, Prof. Dr. Sibel Kalaca for her critical review of the analysis and Prof. Ray W. Guillery for his editing of the manuscript.

        Authors’ Affiliations

        (1)
        Department of Public Health, School of Medicine, Marmara University
        (2)
        Institution of Population Studies, Hacettepe University

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        57. Pre-publication history

          1. The pre-publication history for this paper can be accessed here:http://​www.​biomedcentral.​com/​1471-2458/​13/​1215/​prepub

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