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A Case Control Study of Association

A Case Control Study of Association

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Published by: GUIMEDIC ASOCIACIÓN MÉDICA on Sep 25, 2011
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ORIGINAL INVESTIGATION
d
A Case-Control Study of Associationof 
Helicobacter pylori
Infection With MorbidObesity in Taiwan
Ming-Shiang Wu, MD; Wei-Jei Lee, MD; Hsih-Hsi Wang, MD; Shi-Pei Huang, MD; Jaw-Town Lin, MD
Background
:
Obesityisanincreasinghealthproblemindevelopedcountries,wheretheprevalenceof 
Helicobacter  pylori
infectionisdecreasing.Recentstudiessuggestedcolo-nizationofthestomachby
Hpylori
mightaffectgastricex-pression of appetite- and satiety-related hormone and pa-tients cured of 
H pylori
infection gained weight. It washypothesizedthat
H pylori
couldbeacontributingpatho-genic factor in childhood and adult obesity.
Methods
:
To determine whether
H pylori
infection islinked to obesity, a case-control study composed of 414patients with morbid obesity (a body mass index [cal-culated as weight in kilograms divided by the square of height in meters] of 
35 with serious comorbidity or abodymassindexof 
40)and683controlsubjects(abodymass index of 
25) with a comparable socioeconomicstatus was conducted. Immunoglobulin G antibodiesagainst
Hpylori
weremeasuredfromfrozenserumsamplesbyanenzyme-linkedimmunosorbentassay.Logisticre-gression was used to calculate the odds ratio (OR) and95% confidence interval (CI).
Results
:
Theoverallseropositivitywassignificantlylowerinobesepatients(181[43.7%]of414)thancontrols(410[60.0%]of683)(OR,0.50;95%CI,0.39-0.65;
P
.001).Differencesintheestimatedriskofthepresenceof 
Hpy-lori
weremorepronouncedinyoungeragegroups,withORs of 0.32 (95% CI, 0.10-1.00;
P
=.05) in those aged10to19years,0.55(95%CI,0.34-0.89;
P
=.01)inthoseaged 20 to 29 years, 0.49 (95% CI, 0.30-0.80;
P
=.007)in those aged 30 to 39 years, and 0.58 (95% CI, 0.33-1.00;
P
=.05) in those aged 40 years or older.
Conclusions
:
Our data indicated an inverse relation-ship between morbid obesity and
H pylori
seropositiv-ity. These findings raise the hypothesis that a lack of 
H pylori
infection, especially during childhood, mightenhance the risk of the development of morbidobesity.
 Arch Intern Med. 2005;165:1552-1555
O
BESITY HAS BECOME A MA
- jor public health prob-lem of global signifi-cance.Healthconditionscausedorexacerbatedbyobesity include hypertension, diabetesmellitus, sleep apnea, obesity-related hy-poventilation, back and joint problems,cardiovascular disease, and gastroesopha-geal reflux disease. The body mass index(BMI)(calculatedasweightinkilogramsdi-vided by the square of height in meters) isthe most commonly accepted measure-mentforobesity.ABMIexceeding25iscon-sidered overweight, while obesity is de-fined as a BMI of 30 or more. A BMI of 35ormorewithseriouscomorbidityoraBMIof 40 or more is considered morbid obe-sity.
1
The incidence of obesity has in-creased rapidly during the past 2 decades.Thisincreasehadbeenmostdramaticinaf-fluentcountries.Thefactorsunderlyingthisincrease are largely unknown. Althoughmultiplestudiesshowthatthegeneticcon-tribution is significant,ourgenes havenotchangedappreciablyduringthisperiod.Anincreasing obesigenic lifestyle of excessivecaloricintakeanddecreasedphysicalactiv-ityareassumedtoplayacentralroleinthisepidemiologic trend.
2
 Whether there areother environmental factors likely to ex-plaintheepidemicofobesityremainstobeelucidated.
Helicobacterpylori
isagram-negativeba-cillus. It was estimated that half of theworld’s adult population harbors
H pylori
in their stomach. In developing countries,the infectious process occurs early andreaches60%to80%inadulthood.Thean-nual incidence of 
H pylori
acquisition byadults is much lower in developed coun-tries. The increase by age largely reflects abirthcohortphenomenon.
3
Helicobacterpy-lori
is the main causative factor of chronicgastritis. Epidemiologic studies have con-sistentlylinked
Hpylori
infectiontopeptic
Author Affiliations:
Department of Primary CareMedicine, College of Medicine,National Taiwan University, andDepartment of InternalMedicine, National TaiwanUniversity Hospital, Taipei(Drs Wu, Huang, and Lin); andDepartments of Surgery(Dr Lee) and Internal Medicine(Dr Wang), En-Chu KongHospital, Taipei Hsien, Taiwan.
Financial Disclosure:
None.
(REPRINTED) ARCH INTERN MED/VOL 165, JULY 11, 2005 WWW.ARCHINTERNMED.COM
©2005 American Medical Association. All rights reserved.
 on August 22, 2011www.archinternmed.comDownloaded from 
 
ulcer and gastric malignancies.
4
The diverse outcomes of 
H pylori
infection are ascribed to the difference in extentand severity of gastritis, which leads to variation in theamountofgastricsecretionandcreatesapermissivelumi-nal milieu for disease to develop.
5
Recently, the spectrumof 
H pylori
–related diseases has expanded to include gas-troesophagealrefluxdiseaseandobesity.Theparallelepi-demicofgastroesophagealrefluxdiseaseandobesitycom-binedwithdecreasing
Hpylori
infectioninwesterncountriessuggests
Hpylori
mightplayaprotectiveroleinthedevel-opment of obesity and gastroesophageal reflux disease.
6,7
Basedonthefindingsthateradicationof 
Hpylori
couldin-fluencethedynamicofghrelinandincreasebodyweight,
8-11
BlaserandAtherton
12
proposedthat
Hpylori
infectionmightinfluencefoodintakeandcaloriehomeostasisthroughde-fectivesignalingofappetite-relatedhormoneinthestom-ach. A possible inverse relationship between exposure to
Hpylori
andtheoccurrenceofobesityhasbeenfurtherad-dressed in studies of morbid obesity.
13-15
Preliminary databy histological examinations have shown that the infec-tion rate of 
H pylori
in these patients ranged from 24% to38%.
13-15
However,controversialresultsexisted,andwhether
H pylori
infection plays a role in childhood and adult adi-posity remains to be determined.
12-18
Taiwan is a newly industrialized country where theincidence of obesity is accelerating and
H pylori
infec-tion is prevalent.
19,20
A recent mass screening programeven showed the increase of childhood diabetes melli-tus on this island is due to obesity.
21
To clarify the rela-tionship between obesity and
H pylori
infection, we in-vestigated, in a case-control study, the seroprevalencesof 
Hpylori
amongpatientswithmorbidobesityandcon-trol subjects with a normal weight.
METHODS
STUDY SUBJECTS
Studied concomitantly in a random order,
22
we selected con-secutive patients affected by morbid obesity between January1, 2001, and December 31, 2003. A case was defined as a pa-tient with a BMI of 35 or more with a serious comorbidity orwith a BMI of 40 or more who was admitted to En-Chu KongHospital for evaluation of the possibility of weight reductionsurgery. Blood samples for a prospective investigation of theeffect of surgery on these patients were collected. Finally, 414eligible patients (115 men and 299 women; mean±SD age,31.9.2years)wereenrolled.Inthesameperiod,wealsoen-rolled controls from healthy subjects with a BMI of less than25whounderwentahealthcheckupatthesamecenter.Atotalof 683 controls (337 men and 346 women; mean±SD age,32.3±9.5 years) fulfilling the criteria were selected. Cases andcontrols were from the geographical area of northern Taiwanand had a similar socioeconomic status, judged by work typeand level of instruction. Written informed consent was ob-tained from each participant, and the ethical committee of thehospital approved the study.
LABORATORY ASSESSMENT
Venousbloodsampleswereobtainedfromthepatientsandcon-trolsafteranovernightfast.Serumwasseparatedinacoldcen-trifuge at 2000 rpm for 10 minutes and was stored in a deepfreezer at −20°C until studied concomitantly in a random or-der. The fasting glucose concentration was determined usinganenzymaticcolorimetricmethod(SigmaChemical,StLouis,Mo). Serum insulin levels were measured by an immune lu-minescence assay (Access; Beckman Coulter, Brea, Calif). In-sulinresistancewasestimatedbythehomeostasismodelofas-sessmentbasedonthefollowingformula:[fastinginsulinlevel(measured in micro–international units per milliliter)
fastingglucoselevel(measuredinmilligramspermilliliter)]22.5. High-sensitivity C-reactive protein was measured usingimmunonephelometry (Nephelometer Analyzer II; Dade Beh-ring, Deerfield, Ill). A commercially available enzyme-linkedimmunosorbent assay kit (IBL, Hamburg, Germany) with re-ported sensitivity and specificity of more than 95% was usedto investigate the prevalence of 
H pylori
infection. All assayswere performed in duplicate and interpreted by a single labo-ratoryinvestigator(M.-S.W.)unawareofsamplestatustoavoidthe possibility of interobserver variability.
STATISTICAL ANALYSIS
All data for cases and controls were computerized, and statis-ticalanalysiswasperformedusingacommerciallyavailablesoft-ware program (SPSS, version 11.0; SPSS Inc, Chicago, Ill).
2
And
t
tests were used for categorical and continuous data, re-spectively.Nonparametrictests(Kruskal-Wallis)havebeenusedfor cases of nonnormality. The strength of association be-tween
H pylori
and sex or age was measured by binary logisticregression to estimate the odds ratio and 95% confidence in-terval (CI).
RESULTS
The seroprevalence of 
H pylori
was 43.7% (181/414) forcases of morbid obesity and 60.0% (410/683) for con-trols(oddsratio,0.50;95%CI,0.39-0.65;
P
.001).Thedistributionsofseropositivityof 
H pylori
withrespecttoage and sex in cases and controls are summarized in
Table 1
. Differences in the estimated risk of the pres-ence of 
H pylori
were more pronounced in younger agegroups, with odds ratios of 0.32 (95% CI, 0.10-1.00;
P
=.05)inthoseaged10to19years,0.55(95%CI,0.34-0.89;
P
=.01)inthoseaged20to29years,0.49(95%CI,0.30-0.80;
P
=.007)inthoseaged30to39years,and0.58(95%CI,0.33-1.00;
P
=.05)inthoseaged40yearsorolder.On the other hand, sex has no effect on the distributionof 
Hpylori
seropositivity.Theclinical,demographic,andmetabolicvariableswerefurthercomparedbetween
Hpy-lori
–positive and
H pylori
–negative patients with mor-bid obesity. No difference in BMI, age, sex, white bloodcellcount,hemoglobinconcentration,high-sensitivityC-reactiveproteinlevel,glycosylatedhemoglobinlevel,andhomeostasismodelofassessmentvaluewasobservedbe-tween these 2 groups (
Table 2
).
COMMENT
Increasing attention has recently been paid to the roleof 
H pylori
in the pathogenesis of nutritional problemsandobesity.
8-18
Theresultsofthiscase-controlstudyshowastatisticallysignificantinverserelationshipbetweenmor-bid obesity and
H pylori
seropositivity. Of special inter-est is that the younger the age, the greater the influence
(REPRINTED) ARCH INTERN MED/VOL 165, JULY 11, 2005 WWW.ARCHINTERNMED.COM
©2005 American Medical Association. All rights reserved.
 on August 22, 2011www.archinternmed.comDownloaded from 
 
of 
Hpylori
.Thesefindingsraisethehypothesisthatalackof 
Hpylori
infection,particularlyduringchildhood,mightfavor the development of obesity.The prevalence of 
H pylori
infection is related to sev-eral confounding factors, such as age and socioeco-nomic status.
20
There is evidence of a decreased sero-prevalence of 
H pylori
in developed countries duringrecent decades.
3,4
The decrease in
H pylori
seropreva-lence seems to coincide with the increase in the inci-dence of obesity. Previous studies
19,20
in Taiwan indi-cated that the seropositivity of 
H pylori
in the generalpopulation varied from 54% to 63% and the incidenceof obesity has increased to the level of developed coun-tries. In the present study, the seroprevalence of 
H py-lori
inthecontrolgroupwaswithinthereportedrange.
20
Furthermore, the marked decrease in seroprevalence of 
H pylori
with decreasing age in morbidly obese patientssupports the notion that populations with a low preva-lence of 
H pylori
have more obese individuals.
12
How-ever, certain limitations were noted in interpreting ourobservations. Although both groups were said to be of the same socioeconomic status, it is likely that a moresensitive assessment would have found among the con-trols more individuals from larger sibships, who hadgrownupinmorecrowdedhomes.Effectively,thinpeoplearemorelikelytobeoflowersocioeconomicstatusthanage-matchedobesepeople.
23
Inaddition,wehadnodataregarding exposure to antibiotics between the 2 groups.Prior studies
13-18
have not uniformly demonstrated aclear association of 
H pylori
with obesity. Scapa et al
13
first recognized that the incidence of 
H pylori
in stom-achs of morbidly obese patients was low: 26.7% in 15obese patients by culture and biopsy urease test results.Renshaw et al
14
and Ramaswamy et al
15
have docu-mented that 38% and 24% of patients undergoing sur-geryformorbidobesityhaveevidenceof 
Hpylori
byhis-tologicalexaminationresult,respectively.Consistentwiththeseearlierstudies,theseroprevalenceof 
Hpylori
inourlarge cohort of morbidly obese patients was relativelylower(43.7%)comparedwithourcontrols.Ontheotherhand, several studies
16-18
with a non–case-control de-sign have described the lack of any difference in preva-lence of 
H pylori
with respect to body weight. Kawanoet al
16
reported that
H pylori
infection was not related toBMI in asymptomatic subjects. Kyriazanos et al
17
foundthat the incidence of 
H pylori
is not increased in obesepeople. Perdichizzi et al
18
even showed
H pylori
infec-tion tended to increase in hyperglycemic obese sub- jects. Collectively, the major controversy from differentstudiesseemedtoarisefrommethod.Smallsamplesizes,different definition of obesity and selection of patients,variousdetectingmethodsof 
H pylori
infection,nocon-trolgroup,andlackofconsiderationofconfoundingfac-tors are among the reasons to explain the discrepant re-sults.Furtherlarge-scaleprospectivestudiesofcomparablesubjects with full consideration of the confounding fac-tors are warranted to definitely establish the protectiverole of 
H pylori
in morbidly obese patients.It is not possible to deduce from our study the causalrelationship between
H pylori
infection and obesity. Themechanisms underlying the inverse association have re-mainedobscure,butseveralpotentialinteractionsareop-
Table 1. Seroprevalences of
Helicobacter pylori 
in Patients With Morbid Obesity and Control Subjects With Respect to Age and Sex
*
Age, yPatients With Morbid Obesity ControlsMale Female All Male Female All
10-19 0/6 4/16 (25.0)
4/22
(18.2) 33/77 (42.9) 30/77 (39.0)
63/154
(40.9)20-29 21/63 (33.3) 50/130 (38.5)
71/193
(36.8) 35/58 (60.3) 22/53 (41.5)
57/111
(51.4)30-39 14/33 (42.4) 42/85 (49.4)
56/118
(47.5) 42/66 (63.6) 47/74 (63.5)
89/140
(63.6)
40 9/13 (69.2) 41/68 (60.3)
50/81
(61.7) 94/136 (69.1) 107/142 (75.4)
201/278
(72.3)All 44/115 (38.3) 137/299 (45.8)
181/414
(43.7) 204/337 (60.5) 206/346 (59.5)
410/683
(60.0)
*
Data are given as number/total (percentage) of each group.
Table 2. Demographic and Clinical Data Between
Helicobacter pylori 
–Positive and
H pylori 
–Negative Patients With Morbid Obesity
*
Variable
H pylori 
–Positive Patients(n = 181)
H pylori 
–Negative Patients(n = 233)All Patients(N = 414)
Value†
Male-female ratio 44:137 71:162 115:299 .18Age, y 34.3 ± 9.3 30.0 ± 8.6 31.9 ± 9.2 .13BMI 40.1 ± 7.8 40.5 ± 7.7 40.3 ± 7.7 .69WBC count,
10
3
 /µL 8.5 ± 2.3 8.6 ± 2.4 8.5 ± 2.4 .74Hb level, g/dL 13.6 ± 1.6 13.7 ± 1.4 13.6 ± 1.5 .63hsCRP level, mg/L 0.8 ± 1.5 0.8 ± 1.2 0.8 ± 1.3
.99Glycosylated hemoglobin level, % 5.8 ± 1.0 5.9 ± 1.1 5.8 ± 1.1 .51HOMA value95.5 ± 279.8 79.5 ± 212.9 86.5 ± 244.2 .64Abbreviations: BMI, body mass index (calculated as weight in kilograms divided by the square of height in meters); Hb, hemoglobin; HOMA, homeostasis modelof assessment; hsCRP, high-sensitivity C-reactive protein; WBC, white blood cell.
*
Data are given as mean ± SD unless otherwise indicated.†Data given for the comparison between
H pylori 
–positive and
H pylori 
–negative groups.‡The formula for this value is given in the “Laboratory Assessment” subsection of the “Methods” section.
(REPRINTED) ARCH INTERN MED/VOL 165, JULY 11, 2005 WWW.ARCHINTERNMED.COM
©2005 American Medical Association. All rights reserved.
 on August 22, 2011www.archinternmed.comDownloaded from 

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