Association of Schools of Public Health

Changing Trends in Viral Hepatitis-Associated Hospitalizations in the American Indian/Alaska

Native Population, 1995-2007
Author(s): Kathy K. Byrd, John T. Redd, Robert C. Holman, Dana L. Haberling and James E.
Cheek
Source: Public Health Reports (1974-), Vol. 126, No. 6 (NOVEMBER/DECEMBER 2011), pp. 816-825
Published by: Association of Schools of Public Health
Stable URL: http://www.jstor.org/stable/41639439
Accessed: 25-02-2016 17:08 UTC

REFERENCES
Linked references are available on JSTOR for this article:
http://www.jstor.org/stable/41639439?seq=1&cid=pdf-reference#references_tab_contents

You may need to log in to JSTOR to access the linked references.

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://www.jstor.org/page/
info/about/policies/terms.jsp

JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content
in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship.
For more information about JSTOR, please contact support@jstor.org.

Association of Schools of Public Health is collaborating with JSTOR to digitize, preserve and extend access to Public Health
Reports (1974-).

http://www.jstor.org

This content downloaded from 192.236.36.29 on Thu, 25 Feb 2016 17:08:06 UTC
All use subject to JSTOR Terms and Conditions
Research Articles

Trends in Viral
Changing Hepatitis-

Associated in the
Hospitalizations

American Indian/Alaska Native

Population, 1995-2007

KathyK. Byrd,MD, MPHab ABSTRACT

JohnT. Redd,MD, MPHa,c
RobertC. Holman,MSd
Dana L. Haberling,MSPHd
JamesE. Cheek,MD, MPHa
Objective. We describedthe changingepidemiologyof viralhepatitisamong
the AmericanIndian/AlaskaNative(AI/AN)populationthatuses IndianHealth
Service(IHS) healthcare.
Methods. We used hospitaldischargedata fromthe IHS NationalPatient
InformationReportingSystemto determineratesof hepatitisA-, B-,and
among AI/ANsusingIHS healthcare from1995-
C-associatedhospitalization
2007 and summaryperiods 1995-1997 and 2005-2007.
Results. HepatitisA-associatedhospitalization ratesamong AI/ANpeople
decreased from4.9 per 100,000 populationduring1995-1997 to 0.8 per
100,000 populationduring2005-2007 (riskratio[RR]= 0.2, 95% confidence
change in the overallhepa-
interval[CI] 0.1, 0.2). Whiletherewas no significant
titisB-associatedhospitalization ratebetweentimeperiods,the average annual
ratein people aged 45-64 yearsincreasedby 109% (RR=2.1, 95% CI 1.4, 3.2).
Betweenthe two timeperiods,the hepatitisC-associated hospitalization rate
rose from13.0 to 55.0 per 100,000 population(RR=4.2, 95% CI 3.8, 4.7), an
increaseof 323%. The hepatitisC-associated hospitalization ratewas highest
among people aged 45-64 years,males,and those in the Alaskaregion.
Conclusions. HepatitisA has decreased to near-eradication
levelsamong the
AI/ANpopulationusingIHS healthcare. HepatitisC-associatedhospitalizations
increasedsignificantly;
however,therewas no significantchange in hepatitis
B-associatedhospitalizations.
Emphasis should be placed on continueduniver-
sal childhoodand adolescent hepatitisB vaccinationand improvedvaccination
of high-risk
adults.Prevention and educationeffortsshouldfocuson decreasing
hepatitisC riskbehaviorsand identifying
people with hepatitisC infection
so
theymay be referred
fortreatment.

'IndianHealth Office
Service, ofPublicHealthSupport,
Division
ofEpidemiology
andDiseasePrevention, NM
Albuquerque,
•JohnsHopkins University SchoolofPublicHealth,
Bloomberg GeneralPreventive
MedicineResidency
Program, MD
Baltimore,
cCenters
forDiseaseControl National
andPrevention, CenterforHIV/AIDS, ViralHepatitis,
STD,andTBPrevention,Division
ofViral
GA
Atlanta,
Hepatitis,
dCentersforDiseaseControl
andPrevention, Center
National forEmerging ZoonoticandInfectious Division
Diseases, ofHigh-
Consequence PathogensandPathology,
Adanta,GA
Addresscorrespondenceto:Kathy
K.Byrd,MD,MPH,Centers forDiseaseControlandPrevention,
Division
ofViralHepatitis,
1600CliftonRd.NE,MSG-37, fax404-718-8595;
GA30333;tel.404-718-8541;
Adanta, e-mail
<gdn8@cdc.gov>.

816 O Public Health Reports / November-December2011 / Volume 126

This content downloaded from 192.236.36.29 on Thu, 25 Feb 2016 17:08:06 UTC
All use subject to JSTOR Terms and Conditions

Since 1995, there have been dramatic changes in
the prevalenceand relativefrequenciesof infection
and hospitalizationdue to viralhepatitisin the U.S.,
especiallyamong the AmericanIndian/AlaskaNative
(AI/AN) population.1Historically, hepatitisA was one
of the mostfrequentlyreportednotifiableinfectious
diseases nationally.2The proportionof people ever
infectedwithhepatitisB in the U.S. is estimatedto
be 5%, withapproximately550,000-940,000 people
chronicallyinfected.3HepatitisC is the mostcommon
bloodborne infectionin the U.S., withan estimated
1.6% ofthepopulationeverinfectedand 80% ofthose
individualschronicallyinfected.4
AI/AN people have long sufferedfroma dispro-
portionateburden of infectiousand chronicdiseases,
includingchronic liverdisease and viral hepatitis.5-9
For example,the incidence of hepatitisA among AI/
ANs has historicallybeen 10 times higher than the
nationalaverage.10In 2003, the proportionof deaths
attributableto chronic liver disease among AI/ANs
was approximately fourtimesgreaterthan thatof the
totalU.S. population and was the fifth-leading cause
of death among thisgroup.6,7 HepatitisC is one of the
mostcommon causes of chronicliverdisease among
thispopulation.7
The Indian Health Service (IHS), a Department
of Health and Human Servicesagency,is responsible
for providinghealth care to eligible AI/AN people.
Approximately1.6 million AI/AN people (approxi-
mately60% ofthetotalAI/ANpopulation) are eligible
forIHS-fundedmedical care.11,12 The IHS population
consistsprimarily of AI/ANswho reside in rural,and
oftenremote,areas; much of the remainingAI/AN
populationresidesin urban settingswhereIHS facili-
tiesare oftenunavailable.We describethe changes in
viral hepatitis-associated
hospitalizationssince 1995,
documenting the success of hepatitisA immunization
and theconcomitantrisein hepatitisC. This is thefirst
nationalstudyto describethe changingepidemiology
ofviralhepatitisin the overallAI/AN population that
uses IHS healthcare.
METHODS
We analyzed hospital discharge data from the IHS
National Patient Information Reporting System
(NPIRS) forcalendaryears1995-2007,13withcompari-
son ofthesummaryperiods1995-1997 (period 1) and
2005-2007 (period 2). NPIRS includes all inpatient
discharge records from IHS and triballyoperated
hospitalsand fromhospitalsthathave contractedwith
IHS or withtribesto provide health-careservicesto
patientseligibleforIHS health care.14
Public Health Reports / November-December2011 / Volume 126
This content downloaded from 192.236.36.29 on Thu, 25 Feb 2016 17:08:06 UTC
All use subject to JSTOR Terms and Conditions
IHS Hepatitis Hospitalizations O 817
HepatitisA-, B-, and C-associatedhospitalizations
wereidentifiedusingthefollowingInternationalClas-
sification ofDiseases,NinthRevision,ClinicalModifica-
tion (ICD-9-CM) codes:15070.0 (viralhepatitisA with
coma), 070.1 (viral hepatitisA withoutmention of
coma), 070.2 (viralhepatitisB withcoma), 070.3 (viral
hepatitisB withoutmentionof coma), 070.41 (acute
hepatitisC withcoma) , 070.44 (chronichepatitisC with
coma), 070.51 (acute hepatitisC withoutmentionof
coma) , 070.54 (chronichepatitisC withoutmentionof
coma), 070.70 (unspecifiedhepatitisC withoutmen-
tion of coma), and 070.7 (unspecifiedviralhepatitis
C). Hepatitis C-associatedhospitalizationswere also
dividedinto totalacute (070.41, 070.51) and chronic
(070.44, 070.54) hospitalizations.Those ICD-9-CM
codes listedas one of the top 15 dischargediagnoses
were included in the analysis.The unitof analysisfor
thisstudywas a hospitalization;an individualwho was
hospitalized more than once would thereforehave
each hospitalizationcounted separately.
We expressedannualand averageannualhospitaliza-
tionratesas thenumberofhospitalizations per 100,000
AI/AN people. We estimatedthe annual IHS popula-
tion denominatorsusingthe IHS annual user popula-
tion adjusted by the change in the servicepopulation
fromthefiscalyear2001 userpopulation,excludingthe
IHS Californiaand Portland(i.e.,Washington, Oregon,
and Idaho) areas.8,11,16
We definedtheuserpopulation
as all AI/AN people who receivedIHS-fundedhealth-
care serviceat least once in the previousthreeyears,
whichrepresentsapproximately 81% ofthe 1.6 million
eligible AI/AN people.14
We examinedhospitalizations forhepatitisA, B, and
C by age group (0-4, 5-19, 20-44, 45-64, and >65
years of age), gender,IHS region, and time period.
We definedIHS regionsas follows:East region(Maine,
NewYork,Massachusetts,Connecticut,Rhode Island,
Pennsylvania, NorthCarolina,SouthCarolina,Florida,
Alabama,Mississippi,and Louisiana) ; NorthernPlains
(Montana, Wyoming,North Dakota, South Dakota,
Nebraska,Iowa, Minnesota,Wisconsin,Michigan,and
Indiana); Alaska (Alaska); SouthernPlains (Oklahoma
and Kansas); and Southwest(Arizona, New Mexico,
Colorado, Utah, and Nevada). We excluded the IHS
California (California) and Portland (Washington,
Oregon,and Idaho) regionsfromtheanalysisbecause
neitherregionhad anyIHS- or tribally operatedhospi-
tals.11In addition,the Californiaregiondid not report
contracthealth servicesinpatientdata by diagnosis,
and the Portlandregion had limitedcontracthealth
serviceforinpatientcare.14,16,17
Approximately12% of
all AI/ANpeople receivingcare in IHS facilitiesreceive
care in these two regions.We made comparisonsof
818 O Research Articles
hospitalizationratesbyperiod and characteristicusing
Poisson regressionanalysisto create riskratios (RRs)
with95% confidenceintervals(CIs).18
RESULTS
Fromsummaryperiods1995-1997to 2005-2007,hepa-
titisA-associatedhospitalizationratesdecreased 83%
(RR=0.2, 95% CI 0.1, 0.2). There was no significant
change in hepatitisB-associatedhospitalizationrates.
HepatitisC-associatedhospitalizationrates increased
323% (RR=4.2, 95% CI 3.8, 4.7) (Figure 1).
HepatitisA
From summaryperiods 1995-1997 to 2005-2007, the
average annual hepatitisA-associatedhospitalization
ratedecreasedfrom4.9 to 0.8 per 100,000population.
There were <10 hospitalizationsduring both time
periodsforchildrenaged 0-4 yearsand <10 hospital-
izationsin 2005-2007 forchildrenaged 5-19 years.A
significantrate decrease was seen among those aged
5-19 and 20-44 yearsand in bothgenders.The Alaska
region had <10 hospitalizationsduring both time
periods.In period 2, therewere no reportedhospital-
izationsin the East regionand <10 hospitalizationsin
the Northernand SouthernPlains regions (Table 1).
HepatitisB
There was no significantchange between summary
periodsin theoverallhepatitisB-associatedhospitaliza-
Figure1. Annualhospitalization
rates (per 100,000 population)associated withdiagnoses of
hepatitisA, B, and C amongAI/ANs:IndianHealthService,1995-2007
= American
AI/AN Indian/Alaska
Native
Public Health Reports / November-December2011 / Volume 126
This content downloaded from 192.236.36.29 on Thu, 25 Feb 2016 17:08:06 UTC
All use subject to JSTOR Terms and Conditions
tion rate.However,the averageannual rate increased
by109% among thoseaged 45-64 years(RR=2.1, 95%
CI 1.4, 3.2) (Table 2). There were no hospitalizations
among children0-4 yearsof age and <10 hospitaliza-
tions among children5-19 yearsof age duringboth
time periods. Rates for adults aged 20-44 yearsand
>65 yearsdid not demonstratestatistically significant
changes between time periods. Hospitalizationrates
did not change significantly in eithergender or any
region between time periods.
During 2005-2007, the highest risk of hepatitis
B-associatedhospitalizationwas among people aged
45-64 years (RR=2.6, 95% CI 1.9, 3.6, withpatients
aged 20-44 years as the reference group); males
(RR=1.6, 95% CI 1.9,3.6); and people fromtheAlaska
region (RR=5.6, 95% CI 3.2, 9.6, withthe Northern
Plainsregionas thereferencegroup) (data notshown).
HepatitisC
From summaryperiods 1995-1997 to 2005-2007, the
hepatitisC-associated hospitalizationrate increased
in all age groupswiththe exceptionof childrenaged
0-4 years,for which there were no hospitalizations
during either summaryperiod (Table 3, Figure 2
[Panel A]). There was a 456% (RR=5.6, 95% CI 4.6,
6.6) increase in adults aged 45-64 years.Smallerbut
substantialincreaseswere seen in adults aged 20-44
years(217%, RR=3.0, 95% CI 2.6, 3.4) and >65 years
(298%, RR=4.0, 95% CI 2.5, 6.4).
Both genders and all regions had an increase in
 IHS Hepatitis Hospitalizations O 819

Table 1. HepatitisA-associatedhospitalizations
forAmericanIndians/Alaska
Natives:
IndianHealthService,1995-1997 vs. 2005-2007
1995-1997 2005-2007 1995-1997 vs.2005-2007
Characteristic N Ratea (95%CI) N Ratea (95%CI) Riskratio(95%CI)

Gender
Male 72 4.8 (3.8,6.1) 22 1.2 (0.8,1.9) 0.3 (0.2,0.4)
Female 80 4.9 (3.9,6.2) 9 0.5 (0.2,0.9) 0.1 (0.0,0.2)
Agegroup(inyears)
0-4 2 0.6(0.1,3.0) 2 0.5(0.1,2.2) 0.9(0.1,6.2)
5-19 35 3.5(2.5,4.9) 1 0.1 (0.0,0.6) 0.0(0.0,0.2)
20-44 98 8.6 (7.0,10.5) 13 0.9 (0.5,1.7) 0.1 (0.1,0.2)
45-64 13 2.8 (1.6,4.9) 15 2.3 (1.3,3.9) 0.8 (0.4,1.7)
>65 4 2.2 (0.7,5.9) NA NA NA
Region
East 2 2.0 (0.4,8.4) NA NA NA
NorthernPlains 36 5.2 (3.7,7.3) 7 0.8 (0.4,1.8) 0.2 (0.1,0.4)
SouthernPlains 65 8.4 (6.6,11.0) 5 0.5 (0.2,1.3) 0.1 (0.0,0.2)
Southwest 41 3.3(2.4,4.5) 15 1.0(0.6,1.7) 0.3(0.2,0.6)
Alaska 8 2.6 (1.2,5.3) 4 1.0 (0.3,2.8) 0.4 (0.1,1.3)
Total 152 4.9 (4.2,5.7) 31 0.8 (0.6,1.2) 0.2 (0.1,0.2)
aPer100,000
population
NA= notapplicable

the overallhepatitisC-associatedhospitalizationrate 6.9, 12.2). All other regions experienced significant

betweentime periods. There was a 350% and 295%
increasein hospitalizationratesin males and females,
The NorthernPlains regionexperienced
respectively.
the greatestrate increase at 821% (RR=9.2, 95% CI
increases:theEast regionrose 461% (RR=5.6, 95% CI
2.9, 10.9); the SouthernPlains regionincreased349%
(RR=4.5, 95% CI 3.5,5.7); theAlaskaregionrose214%
(RR=3.1, 95% CI 2.5, 3.9); and the Southwestregion

Table 2. HepatitisB-associatedhospitalizations
in AmericanIndians/Alaska
Natives:
IndianHealthService,1995-1997 vs. 2005-2007
1995-1997 2005-2007 1995-1997vs.2005-2007
Characteristic N Rate3 (95%CI) N Ratea (95%CI) Riskratio(95%CI)

Gender
Male 69 4.6(3.6,5.9) 97 5.4 (4.4,6.6) 1.2 (0.9,1.6)
Female 41 2.5(1.8,3.5) 67 3.4(2.7,4.4) 1.4(0.9,2.0)
Agegroup(inyears)
0-4 NA NA NA NA NA
5-19 6 0.6(0.2,1.4) 1 0.1(0.0,0.6) 0.2(0.0,1.3)
20-44 69 6.1(4.8,7.7) 65 4.7 (3.7,6.1) 0.8 (0.6,1.1)
45-64 27 5.8(3.9,8.6) 80 12.2(9.7,15.2) 2.1 (1.4,3.2)
>65 8 4.3(2.0,8.9) 18 7.3 (4.5,11.8) 1.7 (0.7,3.9)
Region
East 5 5.2(1.9,12.9) 3 2.5 (0.6,7.9) 0.5(0.1,2.0)
NorthernPlains 12 1.7(0.9,3.1) 18 2.1(1.3,3.4) 1.2(0.6,2.5)
SouthernPlains 29 3.8(2.6,5.5) 51 5.5 (4.2,7.3) 1.5 (0.9,2.3)
Southwest 39 3.1(2.3,4.3) 46 3.1 (2.3,4.2) 1.0 (0.7,1.5)
Alaska 25 8.0(5.3,12.0) 46 11.7(8.7,15.8) 1.5(0.9,2.4)
Total 110 3.5(2.9,4.3) 164 4.4(3.7,5.1) 1.2(1.0,1.6)
aPer100,000
population
NA= notapplicable

Public Health Reports / November-December2011 / Volume 126

This content downloaded from 192.236.36.29 on Thu, 25 Feb 2016 17:08:06 UTC
All use subject to JSTOR Terms and Conditions
820 O Research Articles

in AmericanIndians/Alaska
Table 3. HepatitisC-associatedhospitalizations Natives:
IndianHealthService,1995-1997 vs. 2005-2007
1995-1997 2005-2007 1995-1997vs.2005-2007
Characteristic N Ratea (95%CI) N Ratea (95%CI) Riskratio(95%CI)

Gender
Male 203 13.7(11.9,15.7) 1,106 61.6(58.0,65.3) 4.5(3.9,5.2)
Female 202 12.4(10.8,14.3) 962 49.0 (46.0,52.3) 3.9 (3.4,4.6)
Agegroup(inyears)
0-4 NA NA NA NA NA
5-19 4 0.4 (0.1,1.1) 14 1.3 (0.7,2.2) 3.2 (1.0,9.6)
20-44 245 21.5(19.0,24.5) 882 64.2(60.6,68.6) 3.0(2.6,3.4)
45-64 135 29.1(24.5,34.5) 1,061 161.6(152.1,171.7) 5.6(4.6,6.6)
>65 21 11.3(7.2,17.6) 111 45.0 (37.2,54.5) 4.0 (2.5,6.4)
Region
East 10 10.4(5.3,19.9) 71 58.5 (46.0,74.2) 5.6 (2.9,10.9)
NorthernPlains 52 7.6 (5.7,10.0) 595 69.7 (64.3,75.6) 9.2 (6.9,12.2)
SouthernPlains 79 10.2(8.2,12.8) 424 45.9 (41.7,50.6) 4.5 (3.5,5.7)
Southwest 168 13.5(11.5,15.7) 599 40.8 (37.6,44.2) 3.0 (2.6,3.6)
Alaska 96 30.8 (25.1,37.8) 379 96.6(87.2,106.9) 3.1 (2.5,3.9)
Total 405 13.0(11.8,14.4) 2,065 55.0 (52.7,57.5) 4.2 (3.8,4.7)
aPer100,000
population
NA= notapplicable

increased203% (RR=3.0, 95% CI 2.6, 3.6) (Figure 2
[Panels B and C], Table 3).
Bothacute and chronichepatitisC-associatedhospi-
talizationsincreasedbetweentimeperiods.There was
an increase in acute and chronic hospitalizationsof
336% (RR=4.4, 95% CI 3.8, 5.0) and 299% (RR=4.0,
95% CI 3.3,4.8), respectively(Figure2 [Panel D]). The
acutehospitalization rateincreasedin people aged ^20
years,withthe greatestincrease (411%) seen in those
aged 45-64 years (RR=5.1, 95% CI 4.1, 6.3). Smaller
increaseswere seen in people aged ^65 years(300%,
RR=4.0, 95% CI 2.2, 7.2) and 20-44 years (240%,
RR=3.4, 95% CI 2.9, 4.1) (data not shown).
Acute hepatitis C-associated hospitalizations
increasedamong both genders- 340% and 331% in
males and females,respectively. The rate increase of
acute hospitalizationswas greatestin the Northern
Plainsregion(609%, RR=7.1, 95% CI 5.2,9.8) followed
bythe East region (545%, RR=6.5, 95% CI 2.8, 15.1);
the SouthernPlains region (378%, RR=4.8, 95% CI
3.6, 6.3); the Alaska region (281%, RR=3.8, 95% CI
2.8, 5.2); and the Southwestregion (219%, RR=3.2,
95% CI 2.6, 3.9) (data not shown).
Similartrendswereseen forchronichepatitisC-asso-
ciated hospitalizations.The chronic rate increased
in adults ^20 yearsof age, withthe greatestincrease
seen in thoseaged 45-64 yearsat 566% (RR=6.7, 95%
CI 4.8, 9.2). Smaller increases were seen in people
aged >65 years(305%, RR=4.1, 95% CI 1.9, 8.6) and
20-44 years (123%, RR=2.2, 95% CI 1.7, 2.8) (data
not shown).
Chronic hepatitis C-associated hospitalizations
increasedin both genders- 379% in males and 236%
in females.The NorthernPlains region experienced
the greatestrate increase in chronic hospitalizations
at 1,711% (RR=18.1, 95% CI 9.6, 34.1) followedby
the East region (335%, RR=4.3, 95% CI 1.5, 12.6);
the SouthernPlains region (270%, RR=3.7, 95% CI
2.2, 6.1); the Southwestregion (169%, RR=2.7, 95%
CI 2.0, 3.7); and the Alaska region (153%, RR=2.5,
95% CI 1.8, 3.5). While the overalltrendbetweenthe
two time periods increased, rates began to decrease
startingin 2003 (data not shown).
During2005-2007,thehighestriskofoverallhepati-
tisC-associatedhospitalizations
wasamongpeople aged
45-64 years(RR=2.5, 95% CI 2.3 2.8,withpatientsaged
20-44 yearsas the referencegroup); males (RR=1.3,
95% CI 1.2, 1.4); and people fromthe Alaska region
(RR=2.4, 95% CI 2.1, 2.7, withthe Southwestregion
as the referencegroup) (data not shown).
DISCUSSION
HepatitisA
Hepatitis A-associated hospitalizationsdecreased in
both genders,all age groups,and all regionsduring
the study period, although not all decreases were
statisticallysignificant.Historically,hepatitisA has

Public Health Reports / November-December2011 / Volume 126

This content downloaded from 192.236.36.29 on Thu, 25 Feb 2016 17:08:06 UTC
All use subject to JSTOR Terms and Conditions
 IHS Hepatitis Hospitalizations O 821

Figure2 (Panel A). HepatitisC-associatedannualhospitalization

rates by age group8among AI/ANs:
IndianHealthService,1995-2007

aThe
0-4-and5-19-year andtheEastregion
agegroups duetothesmall
wereexcluded number
ofhospitalizations.
AI/AN= American
Indian/Alaska
Native

Figure2 (Panel B). HepatitisC-associatedannualhospitalization

rates by gender amongAI/ANs:
IndianHealthService,1995-2007

= American
AI/AN Indian/Alaska
Native

Public Health Reports / November-December2011 / Volume 126

This content downloaded from 192.236.36.29 on Thu, 25 Feb 2016 17:08:06 UTC
All use subject to JSTOR Terms and Conditions
822 O Research Articles

Figure2 (Panel C). HepatitisC-associatedannualhospitalization

rates by region3amongAI/ANs:
IndianHealthService,1995-2007

wasexcluded
aTheEastregion duetothesmall
number
ofhospitalizations.
AI/AN= AmericanIndian/Alaska
Native

Figure2 (Panel D). Acuteand chronichepatitisC-associatedannualhospitalization

rates amongAI/ANs:
IndianHealthService,1995-2007

= American
AI/AN Indian/Alaska
Native

Public Health Reports / November-December2011 / Volume 126

This content downloaded from 192.236.36.29 on Thu, 25 Feb 2016 17:08:06 UTC
All use subject to JSTOR Terms and Conditions

been a significant burdenamong the AI/AN popula-
tion, withlarge outbreaks occurringeveryfiveto 10
years.919Seroprevalence studies performed in the
1980s showedantibodyto hepatitisA virus(anti-HAV)
in 7% of childrenand in 85% of adultsin certainAI/
AN populations.19 Since the institutionof hepatitisA
vaccinationprograms,the incidence of hepatitisA
amongtheAI/ANpopulationhas decreasedfrom>60
per 100,000populationbefore1996 to 0.5 per 100,000
populationin 2007.3
The extensivedecrease in hepatitisA-associated
hospitalizationsmay be largelyattributedto hepa-
titisA immunization.By 1995-1996, the IHS had
implementedhepatitisA immunizationprogramsfor
childrenin certainNorthernPlains reservations;by
1998,theprogramshad expanded to includemostIHS
health-care facilities.20
The declinein adulthospitaliza-
tions,which can be seen in our study,maybe explained
byhighhepatitis A vaccination coverageamongAI/AN
children,as childhood immunityto hepatitisA virus
(HAV) decreases the incidence of adult infections.21
By 2007, 86% of AI/AN childrenaged 24-35 months
had been vaccinatedforhepatitisA.22
The resultsof thisstudyare consistentwitha pre-
vious studyof hepatitisA vaccinationin a subset of
AI/AN people20 and a studyusing national data.23
Bialek et al. described the incidence of hepatitisA
among southwesternAI/AN people prior to and
after the implementationof hepatitisA immuniza-
tion programs.20 They recorded a 20-folddecrease in
incidencein the post-immunization period. Wasleyet
al. foundan overalldecrease of 76% when comparing
national incidence between 1990-1997 (pre-vaccina-
tion baseline period) and 2003.23Although neither
studydistinguishedbetweeninpatientand outpatient
cases, theyboth demonstrateda trendsimilarto that
seen in our study.
HepatitisB
WhiletheoverallhepatitisB-associatedhospitalization
ratedid notchangeduringthestudyperiod,thehospi-
talizationratein people aged 45-64 yearsdemonstrated
a twofoldincrease.
The Advisory Committeeon ImmunizationPractices
(ACIP) recommended universal infant hepatitis B
immunization in 1991 and expanded itsrecommenda-
tion to include all childrenyoungerthan 18 yearsof
age in 1999.24Vaccinationhas contributedto an 82%
nationaldeclinein hepatitisB incidencebetween1990
and 2007,mostdramatically amongthoseyoungerthan
24 yearsof age in whomincidence fellby93%-98%.3
In 2007, adults aged 25-44 yearshad the highest
hepatitisB incidencein theU.S.3Althoughthereis an
Public Health Reports / November-December2011 / Volume 126
This content downloaded from 192.236.36.29 on Thu, 25 Feb 2016 17:08:06 UTC
All use subject to JSTOR Terms and Conditions
IHS Hepatitis Hospitalizations O 823
overalldownwardnational trendforincidenthepati-
tis B, there has been a 5% increase in acute cases in
males aged 20-39 yearsand a 20%-31% increase in
adults ^40 yearsof age between 1990 and 2002.25In
our study,the increasinghepatitisB hospitalization
rate among AI/AN people aged 45-64 yearsfollowed
a similartrend.
It is difficult
to inferwhetherhepatitisB hospitaliza-
tionsin our studyrepresentedacute or chronicdisease
due to the increasein acute adult cases nationallyand
because only 37% of acute cases require hospitaliza-
tion.26Given the high rate of hepatitisB vaccination
among AI/AN children27and the age distribution
of hepatitisB hospitalizationsseen in this study,it
is possible that many of these hospitalizationsrep-
resent chronic disease, which may explain the lack
of decreased hospitalizationrates for this vaccine-
preventabledisease.
Historically, hepatitisB virus (HBV) was endemic
in ruralAlaska,althoughthiswas not the case forthe
other IHS regions. In the Yukon KuskokwimDelta
regionofAlaska,whereabout 30% oftheAlaskaNative
populationresides,data collectedbytheAlaskaNative
Medical Center (ANMC) showed that there had not
been an acute hepatitisB case in more than 10 years
(1996-2006) among Alaska Natives (Personal com-
munication,BrianMcMahon,ProgramDirector,Liver
Disease and HepatitisProgram,ANMC,June2008). It is
thereforelikelythatthehepatitisB-associatedhospital-
izationsin theAlaskaregionrepresentchronicdisease.
ACIP recommendshepatitisB vaccinationforadults
at risk,includingthosewithmultiplesexual partners,
men who have sex with men, and injection drug
users.28While approximately97% of AI/AN children
aged 19-35 monthscompletedthehepatitisB vaccina-
tion seriesduring2004-2006,27thereis no method of
systematicdocumentationof adult immunizationsin
thispopulation.However,data fromthe2004 National
Health InterviewSurveyrevealed that 45% of high-
riskadults aged 18-49 yearshad received>1 dose of
hepatitisB vaccination.Due to thesuccessofchildhood
and adolescentimmunizationprogramsand the resul-
tantdecline in national hepatitisB incidence among
young people, adults comprise the majorityof new
cases.29Declines in incidentcases willlikelycontinue
withthe ongoing success of childhood immunization
programs.To decrease the burden of HBV infection
among adults,effortsshould continue to targetvac-
cinationof high-risk adults.
HepatitisC
We found a dramatic increase in both acute and
chronic hepatitis C-associated hospitalizationrates.
824 O Research Articles
Nationally,mostchronicallyinfectedpeople wereborn
between1945 and 1964.4This age distribution is similar
to thatfoundin our study;AI/AN patients45-64 years
of age had both the highestrate of chronichepatitis
C-associated hospitalizationsand the greatest rate
increase.Adultsaged 45-64 yearsalso had the highest
rate of acute hospitalizations.Given that most acute
hepatitisC virus (HCV) infectionsare asymptomatic
or mild,30itis possiblethatsome acute diagnosesseen
in thisstudywerein actualityflaresof chronichepati-
tis.This findingcould explain the high rate of acute
hospitalizationsfor those aged 45-64 years,who are
knownto have high ratesof chronicHCV infection.4
The Alaskaregionhad the highestrate of hepatitis
C-associatedhospitalizationsamong the IHS regions.
The ANMC and the Arctic InvestigationsProgram
of the Centers for Disease Control and Prevention
(CDC) have offeredfree HCV testingto all AI/AN
people since 1989. The programhas identifiedmore
than1,200anti-HCV-positive people.31This outpatient
screening-based programhas likelyincreasedawareness
of thisdisease,whichmaytranslateto betterinpatient
coding for hepatitisdiagnoses and, consequently,to
higherratesforthisregion.In addition,the increased
ratesin theAlaskaand NorthernPlainsregionsmaybe
due to a higherprevalenceof riskbehavior.However,
prevalenceof injectiondruguse (the main riskfactor
for HCV infection)among the AI/AN population is
largelyunknown. Investigationinto the prevalence
of riskfactorswithineach IHS region is necessaryto
targetpreventionefforts.
The increasein the hepatitisC-associatedhospital-
ization rate is concerningfor severalreasons. There
is significantmorbidityand mortality associated with
HCV infection.32CDC estimates that 10%-20% of
infectedpatientswilldevelopcirrhosis, and l%-5% will
develop hepatocellularcarcinoma.30 In addition,even
in theabsence ofcirrhosis,patientshavebeen shownto
have a decreased qualityof life,withdecreased social
functioningand energy,increased fatigue,and per-
ceivedphysicallimitations.33 Substantialmedical costs
are associated withhepatitisC: futureannual direct
medical costshave been estimatedat $10.7 billionfor
2010-2019.34Given the limitedfinancialresourcesof
the IHS, increased hepatitisC hospitalizationswill
likelycause a significantburden on facilitiesserving
this population. A high prevalence of comorbidities
among this population, which can affectliver out-
comes (e.g.,alcohol abuse,35obesity,and diabetes), will
compound the futuremorbidityand mortality associ-
ated withhepatitisC.36In addition,increasesin acute
hospitalizationsare concerningbecause theyindicate
Public Health Reports / November-December2011 / Volume 126
This content downloaded from 192.236.36.29 on Thu, 25 Feb 2016 17:08:06 UTC
All use subject to JSTOR Terms and Conditions
increasingriskbehaviorfortransmissionof HCV and
otherbloodborne pathogens.
Unlike hepatitisA and B, there is no vaccine for
HCV. Preventivemeasures,therefore,should focuson
communityand patienteducation to increase aware-
ness of the disease and to reduce riskbehaviorassoci-
ated withinfection.Earlyrecognitionand treatment
with antiviralmedications can significantlyreduce
morbidity,and efforts should be made to identify
these
patientspriorto hospitalization.
Limitations
Our studyhad several limitations.First,individuals
who sought care outside of IHS health-careservices
would not be identifiedas cases in thisstudy;as such,
there may be an underestimationof hospitalizations
due to failureto captureurban-dwelling AI/AN people
who may have a higher prevalence of riskbehaviors
but may not have access to IHS health-careservices.
The unitof analysisforthestudywas a hospitalization;
therefore,an individualwho was hospitalizedforviral
hepatitismore thanonce would have each hospitaliza-
tioncounted separately.We were unable to differenti-
ate betweenacute and chronic hepatitisB-associated
hospitalizations;therefore,we were unable to draw
conclusionsabout the impact of hepatitisB vaccina-
tion in this population. This studyanalyzed hospital
dischargedata for AI/AN people who received IHS
healthcare only;as such,it maynot be representative
of all AI/AN people.
CONCLUSIONS
We observedthreedistinctpatternsin hospitalization
ratesamong AI/AN people who used IHS health-care
services from 1995-1997 to 2005-2007: a decrease
forhepatitisA, no change forhepatitisB, and a dra-
matic increase forhepatitisC. The large decrease in
hepatitisA-associatedhospitalizationrates can likely
be attributedto childhood hepatitisA immunization.
Differentiation between acute and chronic hepatitis
B-associatedhospitalizationsrequiresfurtherinvestiga-
tion to evaluate the effectof hepatitisB vaccination
programs.High-riskAI/AN adultsshould continueto
be targetedforhepatitisB immunization. Because there
is no hepatitisC vaccine, preventioneffortsshould
focuson educationto reduce riskbehaviorand identify
people withchronicinfectionto followforprogression
of liverdisease and to targetforantiviraltherapy.
Theauthors
thankDr.BrianMcMahon Native
(Alaska Tribal
HealthConsortium)
andRalphBryan forDisease
(Centers
Control
andPrevention)
fortheir
review
ofthisarticle,
andthe
 IHS Hepatitis Hospitalizations O 825

staffs
oftheparticipating Thefindings
hospitals. andconclusions 18. Kleinbaum DG,Kupper LL,Muller KE,Nizam A.Applied regression
inthisarticle
arethoseoftheauthorsanddo notnecessarily analysisandmultivariable methods. 3rded.Pacific Grove (CA):
theviews
represent ofthesponsoring Thisstudy
agencies. was Brookes/Cole PublishingCo.;1998.
19. Bulkow LR,Wainwright RB,McMahon BJ,Middaugh JP,
Jenker-
Institutional
Review
Boardexempt. sonSA,Margolis HS.Seculartrends inhepatitisAvirus infection
among Alaska Natives.
JInfectDis1993;168:1017-20.
20. BialekSR,Thoroughman DA,HuD,Simard EP,Chattin J,Cheek J,
REFERENCES etal. Hepatitis A incidence andhepatitis A vaccination among
American Indians andAlaska Natives, 1990-2001. AmJ Public
1. Surveillance
foracute viral
hepatitis- United States2007.MMWR Health 2004;94:996-1001.
Surveill
Summ 2009;58(SS-3):l-27. 21. DaganR,Leventhal A,AnisE,Slater P,Ashur Y,Shouval D. Inci-
2. Tenleadingnationallynotifiableinfectious diseases- UnitedStates, denceofhepatitis AinIsraelfollowing universal immunization of
1995.MMWR Morb Mortal Wkly Rep1996;45(41):8834. toddlers.JAMA 2005;294:202-10.
3. WasleyA,Kruszon-Moran D, Kuhnert W,Simard EP,FinelliL, 22. Hepatitis A vaccination coverage amongchildren aged24-35
McQuillan G,et al. Theprevalence ofhepatitis B virusinfec- months - United 2006and2007.
States, MMWR Morb Mortal Wkly
tionintheUnited Statesintheeraofvaccination. J InfectDis Rep2009;58 (25):689-94.
2010;202:192-201. 23. Wasley A,Samandari T,BellBP.Incidence ofhepatitis A inthe
4. Armstrong GL,Wasley A,Simard EP,McQuillan GM,Kuhnert WL, United States intheeraofvaccination. JAMA 2005;294:194-201.
AlterMJ.Theprevalence ofhepatitis Cvirus infectionintheU.S., 24. Update: recommendations toprevent hepatitisB virus transmis-
1999through 2002.AnnIntern Med2006;144:705-14. sion- United States.
MMWR Morb Mortal Wkly Rep 1999;48(2):33-4.
5. Heron MP,Smith BL.Deaths: leading causes for2003.NatlVital 25. Incidence ofacute B- United
hepatitis States,1990-2002. MMWR
StatRep2007Mar15;55:l-49. Morb Mortal Wkly Rep2004,52(51-52): 1252-4
6. HoyertDL,Heron MP,Murphy SL,Kung HC.Deaths: finaldata 26. Centers for DiseaseControlandPrevention (US). Hepatitissurveil-
for2003.NadVital StatRep2006Apr19;54:1-120. lancereport no.61.Atlanta:Department ofHealth andHuman
7. BialekSR,ReddJT,Lynch A,VogtT,Lewis S,Wilson C,etal. Services (US), CDC;2006.Alsoavailable from: URL:http://www
Chronicliverdiseaseamong two American Indian patient
popula- .wvidep.org/Portals/31/PDFs/IDEP/hepatitisA/hep_surv
tionsintheSouthwestern U.S.,2000-2003. JClinGastroenterol _61.pdf [cited 2011May31].
2008;42:849-54. 27. National, stateandlocalareavaccination coverage among children
8. Holman RC,CurnsAT,Kaufman SF,CheekJE,Pinner RW, aged19-35months - United States, 2007.MMWR MorbMortal
Schönberger LB.Trends in infectious diseasehospitalizations Wkly Rep2008;57(35):961-6.
among American IndiansandAlaska Natives. AmJPublic Health 28. Mast EE,Weinbaum CM,Fiore AE,Alter MJ, BellBP,FinelliL,etal.
2001;91:425-31. Acomprehensive immunizationstrategytoeliminate transmission
of
9. Holman RC,Curns AT,Singleton RJ,Seljvar JJ, ButlerJC,Pai- hepatitisBvirus intheUnited
infection States.Recommendations
sanoEL,etal.Infectiousdiseasehospitalizations among older
Amer- oftheAdvisory Committee onImmunization Practices (ACIP) part
icanIndiansandAlaska Natives.Public Health Rep2006;121:674-83. II:immunization ofadults[published erratum appears inMMWR
10. PreventionofhepatitisAthrough active orpassive immunization. Morb Mortal Wkly :1
Rep2007;56(42)14] 1 . MMWR Recomm Rep
MMWR Morb Mortal Wkly Rep1999;48(RR-12):l-37. 2006;55 (RR-1 6):1-25.
11. Department ofHealth andHuman Services, Indian HealthService, 29. Hepatitis B vaccination coverage among -
adultsUnited States,
OfficeofPublic Health Support (US).Regional in
differences 2004.MMWR Morb Mortal Wkly Rep2006;55(18):509-11.
Indianhealth 2002-2003. Rockville (MD):IHS;2008. 30. Recommendations forprevention andcontrol ofhepatitisC virus
12. Census Bureau(US).TheAmerican IndianandAlaska Native (HCV)infection andHCV-related chronic disease.MMWR Recomm
population:2000.Census 2000Brief (C2KBR/01-15) [cited2008 Rep1998;47 (RR-19):l-39.
Sep9].Availablefrom: URL:http://www.census.gov/population/ 31. McMahon BJ,Hennessy TW, Christensen C,Brüden D,SullivanDG,
www/cen2000/briefs.html Homan C,etal.Epidemiology andrisk factorsforhepatitis C in
13. IndianHealth Service(US).Inpatient/ CHSinpatient datafiscal Alaska Natives. Hepatology 2004;39:325-32.
years1995-2007. NationalPatient Information ReportingSystem. 32. Hoofnagle J.Course andoutcome ofhepatitis C.Hepatology 2002;
Albuquerque: IHS; 2009. 36(5Suppll):S21-9.
14. Department ofHealth andHuman Services, Indian Health Ser- 33. FosterGR,Goldin RD,Thomas HC.Chronic hepatitisCvirus infec-
vice,Office ofPublicHealth Support (US).Trends in Indian tioncauses a significant
reductioninquality oflifeintheabsence
health- 2002-2003. Rockville(MD):IHS;2009. ofcirrhosis. Hepatology 1998;27:209-12.
15. NationalCenter forHealth Statistics
(US).International classifica- 34. Wong JB,McQuillan GM,McHutchinson JG,Poynard T.Estimat-
tionofdiseases,
9threvision,clinical
modification. 6thed.Hyattsville ingfuture hepatitisC morbidity, andcosts
mortality, intheUnited
(MD):NCHS;2005. States.
AmJPublic Health2000;90:1562-9.
16. Kaufman SEUtilizationofIHSandtribal direct andcontractgeneral 35. Grant BF,Dawson DA,Stinson FS,ChouSP,Dufour MC,Picker-
FY
hospitals,1996, and US non-federal short-stay 1996.
hospitals, ingRP.The12-month prevalence andtrends inDSM-IV alcohol
Rockville(MD): Indian Health Service (US); 1998. abuseanddependence: United States,1991-1992 and2001-2002.
17. Rhoades DA,D'Angelo AJ, Rhoades ER.Datasources andsubsets Drug Alcohol Depend 2004;74:223-34.
oftheIndian population.In:Rhoades ER,editor. American Indian 36. LauerGM,Walker BD.HepatitisC virus infection. N Engl JMed
health:
innovationsinhealth care,promotion, andpolicy.Baltimore: 2001;345:41-52.
TheJohns Hopkins UniversityPress;2000.p.93-102.

Public Health Reports / November-December2011 / Volume 126

This content downloaded from 192.236.36.29 on Thu, 25 Feb 2016 17:08:06 UTC
All use subject to JSTOR Terms and Conditions