ORIGINAL ARTICLE
Chronic Liver Disease Among Two American Indian
Patient Populations in the Southwestern United States,
2000-2003
Stephanie R. Bialek, MD,* John T. Redd, MD,* Audrey Lynch, BSc,w Tara Vogt, PhD,*
Sharon Lewis, PhD,z Charlton Wilson, MD,w and Beth P. Bell, MD*
Goals: To determine the etiologies of chronic liver disease
among American Indians.
Background: American Indians are disproportionately affected
by chronic liver disease, yet little is known about its underlying
etiologies in this group.
Study: We conducted a cross-sectional prevalence study at
medical centers serving American Indian populations in Arizona
and California. Patients’ records were reviewed to identify those
with chronic liver disease (ICD-9 code for chronic liver disease
or 2 abnormal liver tests Z6 mo apart). ICD-9 codes and
laboratory findings were abstracted to determine etiologies.
Results: Of the 30,698 American Indian patients seen at the
Arizona center during 2000 to 2002, 1496 (4.9%) had chronic
liver disease, including 268/1496 (17.9%) with decompensated
cirrhosis. Etiologies included alcohol (621; 41.5%), hepatitis C
(103; 6.9%), both (136; 9.1%), or nonalcoholic fatty liver disease
(191; 12.8%). Among alcohol-related liver disease patients
tested for hepatitis C, 32.2% were positive. Of the 6074
American Indian patients seen at the California center during
2002 to 2003, 344 (5.7%) had chronic liver disease, including
45/344 (13.1%) with decompensated cirrhosis. Etiologies included
alcohol (57; 16.6%) hepatitis C (83; 24.1%), and both
(42; 12.2%). In one-third of chronic liver disease patient at the
2 centers, no etiology could be identified; 30% to 45% had not
been tested for hepatitis C.
Conclusions: Alcohol-related liver disease and hepatitis C were
the most commonly identified etiologies among these American
Indian patients with chronic liver disease in clinical care.
Identifying American Indian and Alaska Native patients with
chronic liver disease and providing treatment are critical for
reducing disease burden.
Received for publication December 19, 2006; accepted February 28,
2007.
From the *Division of Viral Hepatitis, Centers for Disease Control and
Prevention, Atlanta, GA; wPhoenix Indian Medical Center, Centers
of Excellence, Phoenix, AZ; and zRiverside San Bernadino County
Indian Health, Inc, Banning, CA.
The authors declare no conflict of interest.
There was no outside financial support used for this study.
Reprints: Stephanie R. Bialek, MD, Division of Viral Hepatitis, Centers
for Disease Control and Prevention, Mailstop G-37, 1600 Clifton
Road, Atlanta, GA 30333 (e-mail: zqg7@cdc.gov).
Copyright r 2008 by Lippincott Williams & Wilkins
J Clin Gastroenterol  Volume 42, Number 7, August 2008
Key Words: chronic liver disease, American Indians, hepatitis C,
alcohol-related liver disease, nonalcoholic fatty liver disease,
cirrhosis
(J Clin Gastroenterol 2008;42:849–854)
I n 2002, the proportion of deaths attributable to chronic
liver disease was more than 4 times greater among
American Indians and Alaska Natives than among the
overall US population.1,2 Chronic liver disease was the
6th leading cause of death in this group, with a mortality
burden similar to that due to diabetes, a well-recognized
health concern in American Indian and Alaska Native
populations.1 Despite a disproportionately high mortality
burden from chronic liver disease, none of the popula-
tion-based studies of this disease in the United States have
included large numbers of American Indians or Alaska
Natives3,4 and little is known about the distribution of
chronic liver disease etiologies in these populations.
Primary and secondary prevention measures exist to
forestall the development and progression of chronic liver
disease. Historically, resources for the evaluation and
treatment of chronic liver disease at medical centers that
served American Indians were extremely limited. The size
of the American Indian population with chronic liver
disease and the candidate population for preventive
measures such as hepatitis C treatment are unknown.
Better characterization of this patient population is
needed to identify the necessary resources to provide
optimal care for American Indian patients with chronic
liver disease.
We report the findings of a cross-sectional chronic
liver disease prevalence study at 2 medical centers that
serve predominantly American Indian populations in the
southwestern United States. The objectives of this study
were to describe the underlying etiologies and scope of
morbidity associated with chronic liver disease among
American Indian patients at these medical centers.
MATERIALS AND METHODS
This study was conducted at Phoenix Indian
Medical Center (PIMC) and Riverside San Bernardino
County Indian Health Incorporated (RSBCIHI). PIMC,
administered by the Indian Health Service (IHS),
849
Bialek et al J Clin Gastroenterol  Volume 42, Number 7, August 2008

provides comprehensive medical care to American Indian
and Alaska Native inhabitants of the Phoenix metropo-
litan area, including 6 reservation communities, and
specialty services to people from over 125 tribes from
the southwestern United States. RSBCIHI, a tribally
managed healthcare organization comprised of a con-
sortium of 10 tribes is funded through an IHS contract.
Six outpatient clinics serve American Indians residing in
small cities and rural areas on reservation and nonreser-
vation lands in San Bernardino and Riverside Counties in
California.
Chronic liver disease was defined as persistently
elevated liver tests, in accordance with existing guide-
lines,5,6 or the assignment of an International Classifica-
tion of Diseases, 9th Revision (ICD-9) code consistent
with chronic liver disease, or both, in an American Indian
or Alaska Native adult aged 18 years or older who was
eligible for primary medical care services from PIMC or
RSBCIHI during the study period. Persistently elevated
liver tests were defined as either 2 serum alanine
aminotransferase (ALT), serum aspartate aminotransfer-
ase, or total bilirubin levels greater than the laboratory-
determined upper limits of normal at each site (ALT
>65 U/L at PIMC, ALT >47 U/L at RSBCIHI,
aspartate aminotransferase>37 U/L at both sites). The
study period was October 2000 to September 2002 at
PIMC and January 2002 to December 2003 at RSBCIHI.
Data were abstracted from the medical records for the
study period and the 3 years preceding it. A combination
of laboratory test results and ICD-9 codes were used to
determine underlying chronic liver disease etiologies and
conditions (Table 1).
SAS version 9.1 (Cary, NC) was used for all
analyses. Because the range of medical services available
at the 2 sites differed, it is likely that the completeness of
diagnosis of chronic liver disease varied by site. For this
reason, the data were analyzed separately by site.
This protocol was reviewed by the institutional
review boards of the Centers for Disease Control and
Prevention, PIMC, and RSBCIHI.
RESULTS
Phoenix Indian Medical Center
Of the 30,698 American Indian and Alaska Native
adults who received care at PIMC during October 2000
to September 2002, 1496 (4.9%) had chronic liver disease.
The majority of patients had been assigned an ICD-9
code consistent with chronic liver disease, but a quarter
had persistently elevated liver tests in the absence of
any ICD-9 codes for chronic liver disease (Table 2). The
median age of chronic liver disease patients was 41 years
and 774 (51.7%) were male, whereas the median age of all
PIMC patients was 32 years and 41.5% were male.
Alcohol-related liver disease and chronic hepatitis C
were the most common etiologies of chronic liver disease;
621/1496 (41.5%) patients had alcohol-related liver disease
alone, 136/1496 (9.1%) had chronic hepatitis C and
alcohol-related liver disease, 103/1496 (6.9%) had chronic
hepatitis C alone and 191/1496 (12.8%) had nonalcoholic
fatty liver disease (Table 2). Screening for chronic hepatitis
C was incomplete among 232 (37.4%) of the 621 patients
with alcohol-related liver disease alone and 71 (37.2%) of
the 191 with nonalcoholic fatty liver disease.

TABLE 1. Criteria Used to Assign Etiologies of Chronic Liver Disease and Define Clinically Recognized Cirrhosis
Etiology or Condition Criteria Used to Assign Etiology or Condition
Chronic hepatitis C (1) Positive hepatitis C virus RNA test with elevated ALT or AST tests
or
(2) In the absence of HCV RNA testing, positive HCV RIBA test with elevated ALT or AST tests
or
(3) In absence of HCV RNA or RIBA testing, positive HCV EIA tests and elevated ALT or AST tests
or
(4) In the absence of any HCV test, assignment of an ICD-9 for hepatitis C
Alcohol-related liver disease (1) Any alcohol-related liver disease ICD-9 code
or
(2) Assignment an ICD-9 code consistent with alcohol abuse and an elevated ALT or AST test
Nonalcoholic fatty liver disease Persistently elevated liver enzyme tests and obesity (body mass index >28) and diabetes mellitus
(hemoglobin A1c >7% or an ICD-9 code consistent with diabetes mellitus) and the absence of criteria for
chronic hepatitis C or alcohol-related liver disease
Chronic hepatitis B Positive test for hepatitis B surface antigen and negative test for IgM antibody to hepatitis B core antigen
(IgM anti-HBc)
Hemochromatosis (1) ICD-9 code for hemochromatosis
or
(2) Ferritin >900 ng/mL and an elevated ALT or AST, and the absence of criteria consistent with chronic
hepatitis C or alcohol-related liver disease
Autoimmune hepatitis Antinuclear antibody Z1:80 or antismooth muscle antibody Z1:40 and elevated AST or ALT tests and
absence of criteria consistent with chronic hepatitis C or alcohol-related liver disease
Undetermined etiology Did not meet criteria for any of the etiologies above
Clinically recognized cirrhosis Assignment of an ICD-9 code for cirrhosis, ascites, encephalopathy, esophageal varices, hepatorenal
syndrome, or portal hypertension
ALT indicates alanine aminotransferase; AST, aspartate aminotransferase; EIA, enzyme immunoassay; RIBA, recombinant immunoblot assay.

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J Clin Gastroenterol  Volume 42, Number 7, August 2008 Chronic Liver Disease Among American Indians

more likely to be female compared with those who had an

TABLE 2. Characteristics of Patients With Chronic Liver
Disease identified etiology (62.7% vs. 43.2%, P<0.0001). Many
of those with no etiology met at least some of the criteria
PIMC RSBCIHI
N = 1496 N = 344 for nonalcoholic fatty liver disease, including 136 (34.8%)
Characteristics of Patients With CLD n (%) n (%) with diabetes and 233 (59.6%) who were obese. One
CLD criteria
hundred seventy-two (44.0%) had not been screened for
2 abnormal liver tests, no CLD ICD-9 383 (25.6) 69 (20.1) hepatitis C virus (HCV) infection. Seventy-one (18.1%)
2 abnormal liver tests with CLD ICD-9 598 (40.0) 78 (22.7) had been assigned an ICD-9 code of noninfectious
CLD ICD-9 only 515 (34.4) 197 (57.3) chronic hepatitis due to a toxin. Data on use of
Etiologies of CLD potentially hepatotoxic medications such as HMG CoA
Alcohol-related liver disease 621 (41.5) 57 (16.6)
Alcohol-related liver disease and chronic 136 (9.1) 42 (12.2) reductase inhibitors, or statins, were unavailable;
hepatitis C however, only 7 of these 71 patients had a diagnosis of
Chronic hepatitis C 103 (6.9) 83 (24.1) hyperlipidemia.
Nonalcoholic fatty liver disease 191 (12.8) 43 (12.5) There were 268 (17.9%) chronic liver disease
Other etiologies 54 (3.6) 0
No identifiable etiology 391 (26.1) 119 (34.6)
patients with clinically recognized cirrhosis (Table 2),
Complications of cirrhosis including 181 (29.1%) of the patients with alcohol-related
Ascites 102 (6.8) 13 (3.8) chronic liver disease. Eleven patients with chronic liver
Encephalopathy 74 (5.0) 4 (1.2) disease had hepatocellular carcinoma. Fifty-nine (3.8%)
Esophageal Varices 72 (4.8) 5 (1.5) chronic liver disease patients died during October 2000
Hepatorenal syndrome 10 (0.7) 0
Portal hypertension 46 (3.1) 11 (3.2) to December 2003, 39 (66.1%) of whom had clinically
At least 1 ICD-9 code for a complication 268 (17.9) 45 (13.1) recognized cirrhosis.
of cirrhosis
Complications of cirrhosis, by etiology Riverside San Bernardino County
Alcohol-related liver disease 181/621 (29.1) 16/57 (28.1) Indian Health Inc
Alcohol-related liver disease and hepatitis 34/136 (25.0) 12/42 (28.6)
C Of the 6074 American Indian adult patients who
Hepatitis C 7/103 (6.8) 5/83 (6.0) received medical care at RSBCIHI during 2002 to 2003,
Nonalcoholic fatty liver disease 6/191 (3.1) 1/43 (2.3) 344 (5.7%) had chronic liver disease (Table 2). The
No identified etiology 34/391 (8.7) 11/119 (9.2) median age of chronic liver disease patients was 48 years
Underwent liver biopsy 43 (2.9) 11 (3.2)
Stage 2 or higher fibrosis 25/43 (58.1) 7/11 (63.6) (range 20 to 86) and 183 (53.2%) were male. The median
Cirrhosis on biopsy 7/43 (16.3) 1/11 (9.1) age among all patients who received care at RSBCIHI
Underlying etiology of hepatitis C 21/43 (48.8) 7/11 (63.6) was 43 years and 43.4% were male. Chronic hepatitis C,
Deaths 59 (3.9) Not alone or in conjunction with alcohol-related liver disease,
available
Hospitalizations for CLD 127 (8.5) Not
was the most common underlying etiology, present in
available 125/344 (36.3%) patients. Screening for hepatitis C was
incomplete among patients with chronic liver disease,
Phoenix Indian Medical Center (PIMC), Phoenix, AZ, 2000-2002, n = 1469. with 15 (26.3%) of those with alcohol-related liver disease
Riverside San Bernardino County Indian Health, Inc (RSBCIHI), Riverside, CA,
2002-2003, n = 344. and 17 (34.7%) of those with nonalcoholic fatty liver
CLD indicates chronic liver disease. disease unscreened. Overall, 45 (13.1%) of the 344
chronic liver disease patients had clinically recognized
cirrhosis, including 16 (28.1%) of the 57 with alcohol-
related liver disease alone.
The prevalence of chronic liver disease, alcohol- The prevalence of chronic liver disease, alcohol-
related liver disease, and chronic hepatitis C was higher related liver disease, and chronic hepatitis C was higher
among males than females, whereas nonalcoholic fatty among males than females, while nonalcoholic fatty liver
liver disease was more prevalent among females than disease was more prevalent among females. Among men,
males (Fig. 1). Among men, those aged 40 to 49 had those aged 60 to 69 had the highest prevalence of chronic
the highest prevalence of chronic liver disease (110/1000 liver disease (138/1000 patients), chronic hepatitis C
patients), chronic hepatitis C (29/1000 patients), and (71/1000 patients), and alcohol-related chronic liver
alcohol-related chronic liver disease (73/1000 patients). disease (47/1000 patients). Among women, the highest
Among women, the highest prevalence of chronic liver prevalence of chronic liver disease (81/1000 patients) and
disease (93/1000 patients) and nonalcoholic fatty liver chronic hepatitis C (34/1000 patients) was seen among
disease (21/1000 patients) was seen among those aged those aged 40 to 49, whereas the highest prevalence of
50 to 59. The highest prevalence of chronic hepatitis C nonalcoholic fatty liver disease (20/1000 patients) was
(10/1000 patients) was in those aged 30 to 49 years. The among those aged 50 to 59. The highest prevalence of
peak prevalence of alcohol-related chronic liver disease alcohol-related chronic liver disease among women (20/
among women (31/1000 patients) occurred in those aged 1000 patients) was in those aged 40 to 49 years.
40 to 49 years. Of the 119 (34.6%) chronic liver disease patients for
The 391 (26.1%) chronic liver disease patients for whom no etiology could be determined, 37 (31.1%) had
whom no underlying etiology could be determined were not been screened for hepatitis C. Many of the patients

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Bialek et al J Clin Gastroenterol  Volume 42, Number 7, August 2008

CLD Hepatitis C-related CLD

120
80
100
80 60
60 40
40
Prevalence/1000 patients

20
20
0 0
20-29 30-39 40-49 50-59 60-69 70+ 20-29 30-39 40-49 50-59 60-69 70+

Alcohol-related liver disease Non-alcoholic fatty liver disease

80 80

60 60

40 40

20 20

0 0
20-29 30-39 40-49 50-59 60-69 70+ 20-29 30-39 40-49 50-59 60-69 70+
Age categories (years)

female male

FIGURE 1. Prevalence per 1000 patients of CLD, hepatitis C-related CLD, alcohol-related CLD, and nonalcoholic fatty liver disease
among American Indian patients, Phoenix Indian Medical Center, Phoenix, AZ, September 2001 to October 2002, by sex and
years of age. Solid line represents males and dashed line represents females.

whose etiology was undetermined had risk factors for
nonalcoholic fatty liver disease; 39 (32.8%) had diabetes
and 69 (82.1%) of the 84 for whom body mass index data
were available were obese.
DISCUSSION
This is one of the first studies to provide data on
the prevalence of chronic liver disease and its etiologies
among a well-defined population of American Indians.
We documented substantial morbidity from sequelae of
chronic liver disease among American Indian patients in
this study. Consistent with findings for the overall US
population,3,4 alcohol-related liver disease and chronic
hepatitis C were the most common etiologies among
American Indian patients.
Hepatitis C was the first or second most common
etiology among American Indian patients in the 2 sites in
this study. As nearly one-third of the patients with
chronic liver disease had not been screened for HCV
infection, the true prevalence of chronic hepatitis C
among those with chronic liver disease was probably
higher. It is unclear why the prevalence at the 2 sites
ranged from 16% to 36%. There were no apparent
differences in formal outreach efforts or access to testing
during the study period. The prevalence of underlying
risk factors for HCV infection among the populations
served at these sites has not been well characterized.
The prominence of alcohol-related liver disease as
an underlying etiology was not unexpected. At the 2 sites,
28% and 50% of the patients with chronic liver disease
met the study criteria for alcohol-related liver disease.
Alcohol-related conditions may have been more readily
detected at the site with inpatient and emergency
department services and could have resulted in greater
ascertainment of alcohol-related liver disease, or there
may be true differences in the prevalence of this etiology
in these sites. Alcohol-related morbidity varies across
American Indian and Alaska Native communities but
remains a significant health concern for many tribal
groups.7,8 Alcohol-related liver disease was the most
commonly identified etiology among all persons who died
of chronic liver disease in the United States during 1990
to 1998, with alcohol-related liver disease mortality rates
at least 2-fold higher among American Indians and
Alaska Natives compared with all other groups in the
United States.9
There was substantial overlap in diagnoses of
alcohol-related liver disease and chronic hepatitis C at
both sites. Identifying the subgroup of patients with both
hepatitis C and alcohol-related liver disease is particularly
important because patients with chronic hepatitis C who
continue to consume alcohol are at increased risk for
progression to end stage liver disease.10–12 Many patients
with alcohol-related liver disease in this study had not
been tested for hepatitis C. When evaluating patients with
chronic liver disease, providers should consider multiple
etiologies and perform a complete diagnostic work-up.
Among American Indians and Alaska Natives, the
prevalence of obesity (24%) and diabetes (10%), 2 of
the clinical correlates of nonalcoholic fatty liver disease,
exceeded that reported by all other racial groups during
1997 to 2000.8 Confirming a diagnosis of nonalcoholic
fatty liver disease requires liver biopsy or radiologic

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J Clin Gastroenterol  Volume 42, Number 7, August 2008
evidence of steatohepatitis. Because these procedures
were not widely available at the sites during the study
period, we relied on a case definition of nonalcoholic fatty
liver disease on the basis of the presence of obesity and
diabetes that was specific but not sensitive. Hence, it is
likely that we underestimated the prevalence of nonalco-
holic fatty liver disease.
Nearly a quarter of study patients with persistently
elevated liver enzymes had not been assigned a diagnosis
of chronic liver disease, which may have resulted in an
underestimation of the prevalence of the various under-
lying etiologies of chronic liver disease in the study
population. Evaluation for chronic liver disease may have
been incomplete among patients who received care in
urgent care settings, obtained medical care from outside
providers, or had liver enzyme elevations attributed to
hepatotoxic medications, such as the patients taking
cholesterol-lowering drugs. It is concerning, however, if
medical providers did not recognize persistently elevated
liver enzymes as a marker of possible chronic liver
disease.5,6 Mildly but persistently elevated liver enzymes
are frequently seen among patients with chronic hepatitis
C and nonalcoholic fatty liver disease. Patients in whom
chronic liver disease is not diagnosed miss the opportu-
nity for treatment and preventive measures such as viral
hepatitis immunization and counseling to avoid alcohol
and other hepatotoxic substances.
Previously reported population-based data on
chronic liver disease etiology among American Indians
have been drawn primarily from death certificates.9
Mortality rates from alcohol-related chronic liver disease
were substantially higher than those from hepatitis C-
related chronic liver disease among American Indians and
Alaska Natives during 1990 to 1998.9 Data from death
certificates have been shown to substantially under-
estimate the presence of viral hepatitis among patients
with chronic liver disease because standard methods to
identify chronic liver disease deaths do not include all
relevant diagnostic codes and because contributing causes
useful for identifying etiology are not consistently
recorded on death certificates. Studies of chronic liver
disease deaths comparing data from death certificates
with information available in medical records found that
death certificates documented only 5% to 64% of deaths
associated with chronic hepatitis C.13,14
There are several limitations to this study. Although
the large subset of American Indians who met IHS
eligibility criteria for medical services were included, there
may be limitations in the generalizability of the findings
because the study did not include all American Indians
living in the study areas and only 2 sites were studied. One
of the strengths of the study is that the sites chosen had
characteristics of a spectrum of medical centers that serve
American Indians in that they included urban and rural
areas, reservation and nonreservation lands, and IHS-and
also tribally administered healthcare systems. Use of
existing clinical data in this study could have resulted in
an underestimate of the prevalence of chronic liver
disease, especially early disease, because not all patients
r 2008 Lippincott Williams & Wilkins
Chronic Liver Disease Among American Indians
with the condition would have had it detected through
routine medical care. Alternatively, because the study
population was drawn from a clinical setting, the results
could have overestimated the prevalence of severe disease.
Differences in clinical services available at the 2 sites
probably resulted in differences in the ascertainment of
chronic liver disease. For example, there may have
been more opportunity for recognition and diagnosis of
alcohol dependence at the site with inpatient and
emergency department services resulting in greater
ascertainment of alcohol-related liver disease at that site.
Despite these limitations, medical records are the only
existing data source currently available for estimating
chronic liver disease prevalence among American Indians
and Alaska Natives. Other studies have validated the use
of electronic medical records data from managed care and
government settings such as the Veterans Administration
and Indian Health Service to estimate prevalence of a
variety of conditions.15–20
In conclusion, our findings indicate that chronic
liver disease is prevalent among American Indian patients
in clinical care. Hepatitis C and alcohol-related liver
disease were the 2 most common etiologies. Morbidity
and mortality from chronic liver disease are likely to
increase in the future as the large number of patients
infected with HCV during the 1980s begin to develop the
clinical manifestations of cirrhosis.21 Increasingly effec-
tive treatments for hepatitis C are the standard of care,
but do not seem to have been widely instituted at many of
the facilities that serve large American Indian patient
populations.8 Increasing the availability of these treat-
ments for American Indian and Alaska Native patient
populations could reduce future morbidity from cirrhosis
and end stage liver disease.
REFERENCES
1. Anderson RN, Smith BL. Deaths: Leading Causes for 2002.
Hyattsville, Maryland: National Center for Health Statistics; 2005.
Report nr 53:17.
2. Kochanek KD, Murphy SL, Anderson RN, et al. Deaths: Final data
for 2002. Hyattsville, Maryland: National Center for Health
Statistics; 2004. Report nr 53:5.
3. Frieden TR, Ozick L, McCord C, et al. Chronic liver disease in
central Harlem: the role of alcohol and viral hepatitis. Hepatology.
1999;29:883–888.
4. Bell BP, Navarro VJ, Manos MM, et al. The epidemiology of newly-
diagnosed chronic liver disease in the United States: findings of
population-based sentinel surveillance. Hepatology. 2001;34:468A.
5. Dufour DR, Lott JA, Nolte FS, et al. Diagnosis and monitoring
of hepatic injury. II. Recommendations for use of laboratory tests
in screening, diagnosis, and monitoring. Clin Chem. 2000;46:
2050–2068.
6. American Gastroenterological Association medical position state-
ment. Evaluation of liver chemistry tests. Gastroenterology.
2002;123:1364–1366.
7. Indian Health Service. Trends in Indian Health, 1998-99. Rockville,
Maryland: US Department of Health and Human Services, Indian
Health Service; 2000.
8. Denny CH, Holtzman D, Cobb N. Surveillance for health behaviors
of American Indians and Alaska Natives. Findings from the
Behavioral Risk Factor Surveillance System, 1997-2000. MMWR
Surveill Summ. 2003;52:1–13.
9. Vong S, Bell BP. Chronic liver disease mortality in the United
States, 1990-1998. Hepatology. 2004;39:476–483.
853
Bialek et al
10. Poynard T, Bedossa P, Opolon P. Natural history of liver fibrosis
progression in patients with chronic hepatitis C. The OBSVIRC,
METAVIR, CLINIVIR, and DOSVIRC groups. Lancet. 1997;349:
825–832.
11. Roudot-Thoraval F, Bastie A, Pawlotsky JM, et al. Epidemiological
factors affecting the severity of hepatitis C virus-related liver disease:
a French survey of 6,664 patients. The Study Group for the
Prevalence and the Epidemiology of Hepatitis C Virus. Hepatology.
1997;26:485–490.
12. Harris DR, Gonin R, Alter HJ, et al. The relationship of acute
transfusion-associated hepatitis to the development of cirrhosis in
the presence of alcohol abuse. Ann Intern Med. 2001;134:120–124.
13. Wu C, Chang HG, McNutt LA, et al. Estimating the mortality rate
of hepatitis C using multiple data sources. Epidemiol Infect. 2005;
133:121–125.
14. Leydon WA, Murphy RC, Bell BP, et al. A Comprehensive
assessment of chronic liver disease deaths reveals limitations
of statistics based on standard methods. Hepatology. 2004;40
(4, suppl 1):176A.
15. Wilson C, Susan L, Lynch A, et al. Patients with diagnosed diabetes
mellitus can be accurately identified in an Indian Health Service
854
J Clin Gastroenterol  Volume 42, Number 7, August 2008
patient registration database. Public Health Reports. 2001;116:
45–50.
16. Newton KM, Wagner EH, Ramsey SD, et al. The use of automated
data to identify complications and comorbidities of diabetes:
a validation study. J Clin Epidemiol. 1999;52:199–207.
17. Ives DG, Fitzpatrick AL, Bild DE, et al. Surveillance and
ascertainment of cardiovascular events. The Cardiovascular Health
Study. Ann Epidemiol. 1995;5:278–285.
18. Selby JV. Linking automated databases for research in managed
care settings. Ann Intern Med. 1997;127(8 Pt 2):719–724.
19. Pogach LM, Hawley G, Weinstock R, et al. Diabetes prevalence and
hospital and pharmacy use in the Veterans Health Administration
(1994). Use of an ambulatory care pharmacy-derived database.
Diabetes Care. 1998;21:368–373.
20. Engelgau MM, Geiss LS, Manninen DL, et al. Use of services by
diabetes patients in managed care organizations. Development of a
diabetes surveillance system. CDC Diabetes in Managed Care Work
Group. Diabetes Care. 1998;21:2062–2068.
21. Armstrong GL, Alter MJ, McQuillan GM, et al. The past incidence of
hepatitis C virus infection: implications for the future burden of chronic
liver disease in the United States. Hepatology. 2000;31:777–782.
r 2008 Lippincott Williams & Wilkins