Predictors of <i>H. pylori</i> infection in a safety-net hospital in Arizona

doi:10.4236/ojgas.2013.34039

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Open Journal of Gastroenterology, 2013, 3, 231-236 OJGas

doi:10.4236/ojgas.2013.34039 Published Online August 2013 (http://www.scirp.org/journal/ojgas/)

Predictors of H. pylori infection in a safety-net hospital in

Arizona*

Sailaja Boddu, David Drachman, Jyotsna Ravi, Abdul Nadir

Maricopa Medical Center, Phoenix, USA

Email: [email protected]

Received 22 June 2013; revised 25 July 2013; accepted 4 August 2013

which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

ABSTRACT

Objective: The purpose of this study was to deter-

mine the risk factors associated with having H. pylori

infection as proven by endoscopic biopsy at Maricopa

Medical Center (MMC), a safety-net hospital in phoe-

nix, Arizona which serves primarily patients with

limited financial and insurance resources. Methods:

A total of 1116 biopsies were identified in a Depart-

ment of Pathology database searched from Novem-

ber 2004 to March 2013. To be included, the subjects

had to have an endoscopy with gastric biopsy. After

the inclusion criteria were applied, 282 control sub-

jects without histological evidence of H. pylori infec-

tion and 256 cases with histological evidence of H.

pylori infection were identified. Patient charts were

reviewed to extract information on variables collected

for this study. Results: The mean age of cases and

controls was 50.5 and 52.3 years respectively. The

BMI of the cases and controls was 28.1 and 28.0 res-

pectively. The mean number of upper endoscopic

exams performed was 1.3 in cases and 1.4 in controls

respectively. Potential predictors examined were gen-

der, history of drug abuse, history of alcohol abuse,

chronic pain medication use, smoking, employment

status, outpatient vs. inpatient upper endoscopy exam,

language spoken (English, Spanish, or bilingual), race/

ethnicity, type of insurance, heart burn, dysphagia,

abdominal pain, gastroduodenal ulcers, intestinal me-

taplasia, and having vs. not having a primary care

physician. Based on univariate analyses, having a

gastroduodenal ulcer, having a history of abdominal

pain, Hispanic race, government insurance status,

self-pay insurance status, and speaking Spanish only

were found to be significantly related to having H.

pylori infection. These variables were next entered

into a multivariate analysis. The multivariate analysis

revealed that gastroduodenal ulcer, abdominal pain,

Hispanic race and self-pay insurance status remained

significant predictors of H. pylori infection. For the

last 119 subjects, information regarding the country

of their birth was available. These 119 subjects were

separately analyzed. Country of birth, age, sex, His-

panic race, self-pay insurance status, Spanish speaker,

and having government insurance were included in a

multivariate analysis. Twenty seven percent of pa-

tients without H. pylori were born in the US, com-

pared to fifty eight percent H. pylori positive patients

who were born outside of the US. Conclusion: His-

panics are at high risk for H. pylori infection. In a

multivariate model, pa tients with H. pylori were found

to have a higher risk of ulcers, Hispanic race, abdo-

minal pain and self-insurance status. When self-insur-

ance and Hispanic race were included in another ana-

lysis with place of birth, only birth outside US re-

mained significant.

Keywords: H. pylori; Insurance; Foreign Born

1. INTRODUCTION

Despite the decreasing prevalence of H. pylori within the

indigenous United States population [1], migration from

Mexico, particularly in Texas and California [2], has re-

sulted in a higher burden of H. pylori infection. Data

from El Paso, Texas, and Ciudad Juarez, Mexico utiliz-

ing stool antigen test for H. pylori among asymptomatic

patients revealed a prevalence 38.2% of H. pylori [3]. In

the San Francisco Bay area, the prevalence of H. pylori

in immigrants, first degree and second generation US-

born Hispanics were reported at 31.4%, 9.1% and 3.1%

respectively [4]. Recently, 37.9% prevalence of H. pylori

infection based on gastric biopsies was reported from

northwestern Ontario [5]. The Canadian Helicobacter Study

group has recommended focusing on treating Canadians

*This research was presented as a poster at Digestive Disease Week

(DDW) 2013 in Orland o, Florida.

Published Online August 2013 in SciRes. http://www.scirp.org/journal/ojgas

S. Boddu et al. / Open Journal of Gastroenterology 3 (2013) 231-236

232

with the highest prevalence of H. pylori infection [6].

Based on 2010 US census data, 26.9% of the popula-

tion in Maricopa County Arizona comprised individuals

of Hispanic or Latino origin, third after Texas and Cali-

fornia, where 37.6% of the population is Hispanic [2].

We did not find any data on the characteristics of pa-

tients with H. pylori infection in Arizona which shares

approximately 370 miles of porous border with Mexico.

The purpose of this study was to de termine the predicto rs

of H. pylori infection in patients seen at a safety-net hos-

pital located in Maricopa County, Pho enix, Arizona.

2. MATERIALS AND METHODS

Maricopa Medical Center (MMC) is located in Phoenix.

The hospital is supported by the government to provide

care to individuals who are either on Medicaid (gover-

nment support) or are uninsured. Less than 5% of pa-

tients with commercial insurance are also seen in this

hospital. The hospital is staffed by full-time employed

gastroenterologists who see patients in the clinics as well

as when they are admitted to the hospital. Typically pa-

tients admitted to the hospital undergo upper endoscopy

examinations (EGD) for GI bleeding or unexplained up-

per abdominal pain, while outpatients undergo EGDs for

dyspepsia, abdominal pain, occult GI bleeding or screen-

ing for varices.

We identified 1116 biopsies obtained during EGD in

the department of pathology database from November

2004 to March 2013. Patients having only esophageal

or/and duodenal biopsies were excluded, and only pa-

tients with EGD and gastric biopsies with or without any

other biopsies were included. A total of 256 patient s were

identified to have histological evidence of H. pylori in-

fection. Another 282 patients without histological evi-

dence of H. pylori were selected as controls. Gastric bi-

opsies were read by four pathologists at MMC. Modi-

fied Giemsa stain was used for confirmation of H. pylori

infection. All endoscopists obtained at least two biop-

sies from the gastric antrum.

Data were retrospectively collected on age, gender, sex,

ethnicity, BMI, history of alcohol or drug abuse, narcotic

prescription for chronic pain, dysphagia, heart burn, ab-

dominal pain, gastroduodenal ulcer on EGD, patients

having a follow up with a physician, EGD performed on

in patients or out patients, presence or absence of intes-

tinal metaplasia on gastric biopsies, having government

insurance, self-pay status, language spoken (Spanish,

English, or bilingual) retired status, employed, and num-

ber of EGDs performed. The data were obtained from a

computerized database. Self-reported information was col-

lected on drug or alcohol abuse, ethnicity, languages

spoken, and employment status. A research assistant

went through each electronic medical chart to obtain

relevant data. For the last 119 patients seen from Sep-

tember 2012 to March 201 3, infor mation r egarding coun -

try of birth was prospectively identified besides other

information collected on all patients. The information

available was analyzed for all subjects and separately

analyzed also for subjects with information available on

the country of birth (Tables 1-5).

The data were analyzed using SPSS version 20. Uni-

variate as well as multivariate analyses were conducted

to identify significant predictors of positive H. pylori

infection. For insurance status, language status, and em-

ployment status, dummy variables were created with

commercial insurance, English only, and employed used

as the reference variables, respectively.

Table 1. Univariate analyses—dichotomous variables (general characteristics).

Percentage with this characteristic

Characteristic Controls Cases

p value*

Male 48% (135/282) 49% (125/256) 0.821

African-America n 13% (33/257) 10% (22/228) 0.336

Hispanic 48% (123/257) 72% (164/228) <0.0005

Spanish-Speaking 15% (41/279) 31% (75/245) <0.0005

Bilingual 7% (19/279) 7% (17/245) 1.000

Unemployed 68% (191/282) 70% (179/256) 0.714

Retired 19% (53/282) 16% (40/256) 0.336

Government Insurance 86% (234/273) 72% (164/228) <0.0005

Self-Pay 5% (13/273) 23% (54/236) <0.0005

*Continuity-correcte d chi-square test with 1 degree of freedom.

S. Boddu et al. / Open Journal of Gastroenterology 3 (2013) 231-236 233

Table 2. (a) Univariate analyses—dichotomous variables (clinical characteristics); (b) Univariate analyses—continuous variables.

(a)

Percentage with this characteristic

Characteristic

Controls Cases p value*

Has Primary Care Provider 78% (159/204) 74% (150/204) 0.352

Inpatient 31% (64/205) 25% (52/210) 0.143

Hx of Alcohol Abuse 37% (37/273) 38% (93/245) 0.900

Smoker 48% (131/273) 40% (98/245) 0.098

Chronic Pain Meds 34% (93/276) 28% (69/247) 0.157

Dysphagia 13% (36/279) 11% (27 /25 3) 0.619

Abdominal Pain 46% (128/279) 72% (181/252) <0.0 005

Heart Burn 37% (102/278) 45% (113/253) 0.060

Intestinal Metaplasia 11% (30/278) 9% (22/249) 0.562

Gastric Duodenal Ulcer 2% (5/252) 14% (34/249) <0.0005

(b)

Means

Characteristic Controls (N) Cases (N) p value**

Age 52.3 (282) 50. 5 (256) 0.516

Number of Endoscop ies 1.4 (282) 1.3 (255) 0.207

BMI 28.0 (258) 28.1 (239) 0.959

*Continuity-correcte d chi-square test with 1 degree of freedom; **Independent groups t-test.

Table 3. Multivariate logistic regression analysis.

95% CI for odds ratio

p value Odds ratio Lower Upper

Gastric Duodenal Ulcer <0.0005 8.140 3.100 21.372

Abdominal Pain <0.0005 3.377 2.143 5.322

Hispanic 0.001 2.343 1.399 3.925

Government Insurance 0.384 1.479 0.613 3.565

Self-Pay 0.002 6.236 2.001 19.433

Spanish-Speaker 0.709 0.888 0.475 1.660

All predictors with a p value of 0.05 or less wer e entered into a logistic regression model. A total of 409 cases were analyzed. Hosmer-Lemeshow test: p = 0.911;

Nagelkerke R-squar ed = 0.292.

3. RESULTS

The univariate analyses revealed that Hispanic race,

speaking Spanish only, reporting abdominal pain, having

either a duodenal or gastric ulcer, having government

insurance, and self-pay status were significantly related

to a positive finding for H. pylori. The multivariate ana-

lysis revealed that abdominal pain, presence if gastro-

duodenal ulcer, self-pay status and Hispanic race re-

mained significant when the impact of all of the predic-

tors together was assessed. For the last 119 subjects,

complete data on age, gender, Hispanic race, self-pay

status, having government insurance, speaking Spanish

only and foreign born status were available on 103 sub-

jects. Sub-analysis on this data in a multivariate regres-

sion model showed that foreign born status remained

significant Table 5.

4. DISCUSSION

The prevalence of H. pylori has been reported to be de-

creasing in industrialized nations such as the US be-

S. Boddu et al. / Open Journal of Gastroenterology 3 (2013) 231-236

234

Table 4. Analysis of US born vs. foreign born variable (N = 118).

Group

Control Case

Percentage foreign born Percentage foreign born

27% (20/75) 58% (24/43)

Table 5. Gender, age, hispanicity, self-pay, government insurance, Spanish speaker, and foreign born vs. US born were entered into a

logistic regression model. A total of 103 cases were available for this analysis.

95% CI. for EXP ( B)

Sig. Exp (B)

Lower Upper

Age 0.374 0.985 0.952 1.019

Male_Gender 0.300 0.610 0.240 1.554

Hisp 0.365 1.686 0.544 5.225

Selfpay 0.304 4.255 0.269 67.289

Govt 0.819 1.147 0.356 3.690

Spa 0.904 1.085 0.290 4.056

Foreign Born 0.008 4.513 1.481 13.757

Foreign Born vs. US Born remained significant, even after adjustment for the other variables. Hosmer-Lemeshow test: p = 0.585. Nagelkerke R-squared =

0.253.

cause of better hygiene, a higher standard of living, and

use of antibiotics [7]. The Data reported in this study

show that patients undergoing endoscopy at a safety net

hospital who have a gastric duodenal ulcer are more than

eight times more likely to be H. pylori positive than

those who do not have an ulcer; and patients undergoing

endoscopy who report abdominal pain are more than

three times more likely to be H. pylori positive compared

to those who do not report abdominal pain.

Results of this data also showed significantly higher

odds of H. pylori positivity among patients who spoke

Spanish, were Hispanic in origin and had no insurance

(Table 3). On a separate analysis where place of birth

(foreign born versus US born) was included in addition

to race, language spoken and uninsured status, only place

of birth remained significant (Table 5 ). Taken together,

these data reveal H. pylori is more common in our hos-

pital among those Hispanics who are born in Mexico.

Nonetheless, many patients are infected with H. pylori

who are not migrants from a foreign country and the

source of H. pylori within that sub-set is not clear. It is

possible that within the family members of H. pylori

infected individuals, there is clustering of H. pylori in-

fection [4].

Lower socioeconomic status has been consistently

shown to be associated with H. pylori infection [8]. Ex-

posure to vomitus or feces or residence in an over-

crowded household is likely the cause of spread of H.

pylori infection [9]. Approximately 2 million people of

Hispanic or Latino originally live in Arizona; of them

524,480 people were born in Latina America [10,11].

The percentage of Hispanics without health coverage has

been reported to be 30.1%; higher than the overall rate

reported as 15.7%. The rates of non-insurance for White

non-Hispanics, Blacks and Asians have been reported to

be 11.1%, 19.5% and 16.8% respectively [12]. Lack of

insurance is also a surrogate marker of poverty and the

non-coverage rates range from 25.4% in households with

income less than $25,000 to 7.8% when household in-

come was $75,000 or more [13]. This information sug-

gests that not having insurance and Hispanicity are both

associated with poverty and might be related to factors

that predispose such individuals to H. pylori infection.

Since data were collected from a safety net hospital,

many undocumented subjects were included in our ana-

lyses although exact information on illegal individuals

was not available. Nonetheless, non-citizens (legal and

undocumented) are about three times more likely to be

uninsured than citizens [14].

Intestinal metaplasia, alcohol/drug abuse and use of

narcotics did not have any predictive value for H. pylori

infection in our database. Intestinal metaplasia, atrophic

gastritis and gastric cancer have been widely reported to

be associated with H. pylori infection. 2.9% percent of

patients with H. pylori infection can develop gastric

cancer [15]. Intestinal metaplasia associated with H. py-

lori can be seen in gastric body as well as antrum. In our

study, two biopsies were obtained on each patient; how-

S. Boddu et al. / Open Journal of Gastroenterology 3 (2013) 231-236 235

ever, they were uniformly obtained from antrum and

gastric body. Because of the retrospective nature of our

study and lack of follow up endoscopic biopsies, we did

not see any difference in prevalence of H. pylori in cases

and controls in reported subjects of this study [16].

Conflicting data have been reported regarding asso-

ciation of H. pylori and alcohol consumption. Negative

effect on H. pylori has been reported with moderate al-

cohol consumption [17]. However, among patients with

functional dyspepsia, H. pylori has been shown to be

associated with alcohol consumption [18]. Data reported

in this database did not show any difference in alcohol

use between patients with and without H. pylori, al-

though specific amount of alcohol consumption is not

available. Similarly, data regarding H. pylori and smok-

ing are mixed. One study shows no significant relation-

ship between H. pylori serology and smoking [19], while

the other one reports a higher prevalence of H. pylori in

smokers compared to non-smoker [20]. Our data did not

show any relationship between smoking and H. pylori

(Table 2(a)).

Findings reported in this study are important. First,

data reported about predictors of H. pylori have never

been reported from Arizona which is bordering Mexico

and has one of the highest numbers of Hispanic

population who have either emigrated from Mexico or

born in US; several Hispanics live undocumented in

Arizona and seek medical care at our safety net hospital.

Second, this study shows that H. pylori remains a signi-

ficant cause of peptic ulcer disease that requires hospita-

lization straining an already over stretched health care

system. Finally and most importantly, the data reported

herein identify a sub-group of patients including those

who are uninsured or born outside US, who should be

properly screened with either H. pylori stool antigen test

or endoscopy, depending on an individual’s circums-

tances and treating them accordingly with appropriate

medications, particularly because H. pylori besides being

a significant cause of peptic ulcer disease has also been

classified as a class 1 carcinogen by WHO [6].

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