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Epidemiologic studies of serum uric acid levels among micronesians.

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Epidemiologic Studies of Serum Uric Acid Levels Among
Micronesians
Dwayne Reed, Darwin Labarthe and Reuel Stallones
Data f r o m epidemiologic studies of Chamorro and Palauan populations
of Micronesia were analyzed for associations of serum uric acid levels
with other characteristics of the populations. The mean serum uric acid
levels for those groups were significantly higher than those reported for
Western populations, but the frequency distribution patterns were similar,
being unimodal and slightly skewed toward higher values. Analysis by geographic subgroups showed differences in mean serum uric acid levels, but
those differences did not follow any pattern of association with sociocultural indices. There was a general association of serum uric acid levels
with total daily caloric intakes. Correlation analysis of individual characteristics indicated that serum uric acid levels were positively associated
with measures of blood pressure, obesity and serum triglyceride levels.
There was no consistent association with serum cholesterol or glucose
levels, electrocardiogram abnormalities, smoking habits or measures of
occupation, education or sociocultural attitudes. The overall impression
was that, except for a possible dietary influence, the risk of hyperuricemia
was more strongly associated with being a Micronesian than with geographic residence or life style.
Burch and co-workers reported
that
Chamorros and Carolinians in the Mariana
Islands have a high prevalence of hyperuricemia and gout (1). This situation offered an unusual opportunity for epidemiologic analysis of
hyperuricemia; for there are subgroups of these
From the Epidemiology Branch, C&FR, NINDS, National Institutes of Health, Bethesda, Md.
This study was supported by the National Institute of
Neurological Diseases and Stroke (NINDS), Contract PH43-68-36.
DWAYNE REED, MD, PHD: Formerly University of
Texas School of Public Health at Houston, currently Epidemiology Branch. C&FR, NINDS, Building 36, Room
4A-05. National Institutes of Health, Bethesda Md 20014;
DARWIN LABARTHE, MD, MPH: T h e University of Texas
School of Public Health at Houston, Texas: REUEL STALLONES, MD, MPH: T h e University of Texas School of
Public Health at Houston, Texas.
Reprint requests should be addressed to: Dr. Dwayne
Reed.
Submitted for publication Dec 20, 1971; accepted March
7, 1972.
Micronesian populations which have similar
genetic backgrounds, but are presently living
under different environmental conditions. This
is a report of studies in Micronesia of three
subgroups of Chamorros of the Mariana
Islands and three subgroups of Palauans of the
Western Caroline Islands. T h e data used for
the analyses were collected as part of two
larger studies of the health effects of culture
change (2, 3).
Background
T h e Chamorros and the Palauans reportedly
have common ancestry in the Malay Archipelago (4, 5). T h e first known European
contacts were made by the Spanish in the early
Sixteenth century. During the next 300 years
the Spanish actively occupied G u a m and imported large groups of laborers and soldiers so
that by the end of the Nineteenth Century the
Althritis and Rheumatism,Vol. 15, No. 4 (July-August 1972)
381
REED ET
AL
Chamorro population was mixed with Chamorros in Rota, Guam and California, and the
Palauans in Ngerchelong were examined between DecemFilipinos, Spanish and Mexicans.
During this 300-year period, contact with the ber 1967 and June 1968. T h e Palauans in Koror and Peleliu were examined in March and April of 1970. T h e examWestern Caroline Islands was limited to occa- ining physicians and equipment were the same throughout
sional trading and whaling voyages. In 1898, the study, but a few interview items were changed for the
the United States acquired Guam and the second phase.
T h e sampling procedure was based upon household
Spanish sold the rest of their interests in Micronesia to Germany. While the United States units. Where the population was small (Rota, California
and Ngerchelong) we included the total available populamaintained a military administration in Guam,
tion. Where the population was large we selected a random
first Germany then Japan developed commer- sample of households. Only persons 20 years of age and
cial interests in the rest of the Caroline and older in the selected households were examined.
Upon arrival at the examination site, each examinee was
Mariana Islands. After World W a r 11, administration of the Mariana and Caroline Islands served a carbonated drink containing 50 g of dextrose
(Dextrose 50, USPHS) and was interviewed concerning
was turned over to the United States as part of symptoms and illnesses, personal habits, sociocultural attithe Trust Territory of the Pacific Islands, and tudes and residential mobility. A nurse then took body
Guam became a United States Territory.
measurements and recorded a 12-lead electrocardiogram
T h e extent of interbreeding between for- (EKG). T h e EKG was checked by an examining physician
eigners and natives can only be surmised from a who then completed a screening physical examination and
determined the casual sitting blood pressure.
few available records, however, the different
A 15 ml blood specimen was taken for all examinees apdegrees of exposure to modern cultural influ- proximately 1 hour after the administration of the dextrose.
ence are evident among subgroups of these two Serum was separated approximately 2 hours after bleeding
populations. Among the Chamorros, the people and kept frozen until shipment on dry ice to the laboratory
of the island of Rota have most nearly retained of the Heart Disease and Stroke Control Program in San
Francisco, California. T h e laboratory used Tecnicon Autotheir traditional forms of social organization
‘4nalyzer methods to determine serum uric acid.
and agricultural economy. T h e natives of G u a m
have undergone a rapid change from their traditional way of life, especially following the es- Dietary Survey
tablishment of United States military bases at
T o describe the dietary patterns of the geographic
the end of World W a r 11. A third group of subgroups we selected random subsamples of approxirnateC h a m o r r o s h a s experienced even g r e a t e r ly 9 0 persons in each of the six areas. A standard interview
was developed to obtain a 24-hour dietary recall from each
change in migrating to California.
person. Our nutritionist compiled composition values of
In the Palau District, the inhabitants of food items in terms of total calories, protein, carbohydrate
Ngerchelong, an isolated village, still live a and both saturated and polyunsaturated fat. as previously
traditional subsistence way of life. T h e people described (6). T h e 24-hour dietary history provides an acof Koror, the District Center, have experienced rurate estimate of intakes for population groups, but not for
individuals.
modern influence during both the Japanese and
the United States Trust Territory administration. In between these two extremes were the Computation and Scores
In order to examine the association between serum uric
inhabitants of Peleliu. While still dependent
upon agriculture and fishing for subsistence, acid values and other study variables a number of scores
were calculated. T h e estimation of percent body fat was
they often visited and worked part time in the derived from an average of triceps and subscapular skinDistrict Center.
folds, as proposed by Damon and Goldman (7). A “symp-
MATERIALS AND METHODS
Detailed methods were described in previous reports (2,
3). Briefly. the study was completed in two phases. The
382
toms score” was derived from the number of positive answers to interview questions for histories of high blood
pressure, paralysis, joint disease. numbness, angina pectoris, present health problems, limited activities due to a
physical problem, hospitalization within the prior year and
Arthritis and Rheumatism,Vol. 15, No. 4 (July-August 1972)
SERUM URIC ACID LEVELS
Table 1. Study Population by Age, Sex and Area
~
~~~
~
~
Charnorros
Males
Females
Age group
Calif
Guam
Rota
Calif
Guam
Rota
20-29
30-39
40-49
50-59
60
21
44
57
33
9
61
56
59
50
47
24
29
23
26
20
31
38
50
21
11
94
61
72
68
60
38
33
25
32
21
164
273
122
151
355
149
+
Total
Palauans
FemaIes
Males
Age group
~~~
20-29
30-39
40-49
50-59
60
+
Total
Koror
~
Peleliu
~~
~~~
Nger
~~
~~
Koror
Peleliu
Nger
~
23
23
32
18
13
9
5
4
7
16
4
5
18
18
24
28
45
38
20
14
8
6
12
12
19
11
17
23
22
16
109
41
69
145
57
89
current medications.
Measures of socioculture attitudes included a “food
preference score” which measured the usual preference for
traditional island foods, and a “traditional attitude score”
based upon attitudes concerning child rearing. Occupations
were categorized as subsistence, blue collar and white collar
and scored from high to low in that order.
Geographic mobility was recorded in terms of the number of residential changes during the previous 5 years and
the number of years a person has lived away from his village
of birth. For the second phase of this study (Palau) we included a “cultural mobility score” to represent a combination of occupational geographic and generational mobility.
RESULTS
Table 1 shows the examined populations by
age, sex and area. We completed the examinations for 1214 Chamorros and 510 Palauans.
Of the people available for examination, the
response ratios were 44% in California, 74% in
Guam, 81% in Rota, 81% in Koror, 85% in
Peleliu and 9 1 70 in Ngerchelong. Because of the
different age distributions, all group rates were
age-adjusted to the 1968 Micronesian Trust
Territory population (8).
Because of the low response in California, we
asked the nonrespondents to complete the
questionnaire part of the examination. An agespecific comparison of questionnaire items for
100 nonrespondents and the examined group
showed no meaningful differences. T h e great
majority of nonrespondents in California lived
more than 25 miles from the examination centers.
Figure 1 shows the frequency distribution
curves of serum uric acid levels for all Chamorros and Palauans by sex. T h e mean serum uric
acid levels, plus or minus one standard deviation, were 6.9 +1.45 for Chamorro males, 5.3
+1.37 for Chamorro females, 6.7 &1.62 for
Palauan males and 5.3 +1.35 for Palauan females. Separately by sex, the patterns of the
distribution curves were similar for the
Chamorros and Palauans being unimodal with
slight skewing towards the higher values.
Arthritis and Rheumatism, Vol. 15, No. 4 (July-August 1972)
383
REED ET AL
I
y-
Males
H
k
3020 -
10-
0
0
I
1
2
4
I
SERUM URIC ACID
I
6
a
(w/ioo.m l )
1
I
10
12
F i g l . Frequency distribution curves of serum uric acid levels for all Chamorros (-)
and Palauans (-) by sex.
Table 2 shows the mean serum uric acid
values by age, sex and geographic subgroup.
For all subgroups the males had higher mean
384
serum uric acid levels than females. There was
slight tendency for the values to increase with
age, however, the pattern was inconsistent.
Arthritis and Rheumatism,Vol. 15, No. 4 (JulyAugust 1972)
SERUM URIC ACID LEVELS
Table 2. Mean Serum Uric Acid Levels (mg/100 ml) by Age, Sex and Area
Chamorros
Males
Females
Age groups
Calif
Guam
Rota
Calif
Guam
Rota
20-29
30-39
40-49
50-59
5.7
6.1
6.4
6.9
7.5
6.7
7.2
7.4
6.8
7.5
7.2
6.9
7.1
7.5
7.3
4.3
4.3
5.0
5.6
6.0
5.0
5.1
5.3
5.7
6.1
5.3
5.1
5.3
5.7
5.9
60+
Total”
+ 1 SD
6.4 + 1.4
7.1
f
1.5
*
7.2
1.4
4.9
L
1.3
5.4
+
1.4
5.4 + 1.2
Pa la uans
Males
Females
Age groups
Koror
Peleliu
Nger
Koror
Peleliu
Nger
20-29
30-39
40-49
50-59
60
6.7
6.7
6.3
7.6
7.0
6.3
5.8
6.3
6.5
6.4
6.6
6.6
6.8
7.0
6.9
5.2
5.3
4.9
5.3
5.2
5.9
4.8
5.3
5.6
5.8
4.6
4.5
5.0
5.5
5.5
+
Total”
i
1 SD
6.8 + 1.4
6.2
i
1.3
6.7
*
1.3
5.2
i
1.3
5.5
i
1.2
4.9 + 1.4
“Age-adjusted to the 1968 Trust Territory population.
Among the Chamorro subgroups, the mean
serum uric acid values were significantly lower
for the people in California than for those in
Guam and Rota, especially in the younger age
groups, (tests of differences between means had
probability values of less than 0.05). Among the
Palauans, differences among the subgroups
were inconsistent. T h e mean values were significantly lower for Peleliu males and Ngerchelong females.
Hyperuricemia was defined as a serum uric
acid level of 7 mg/ 100 ml or greater for males
and 6 mg/100 ml or greater for females. Table 3
shows the prevalence of hyperuricemia by age,
sex and geographic subgroup. T h e males had a
higher prevalence of hyperuricemia than females for all subgroups, except in Peleliu.
There was a tendency for the prevalence of hyperuricemia to increase with age, but the pattern was not consistent. T h e age-adjusted pre-
valence of hyperuricemia was 44% for
Chamorro males, 28% for Chamorro females,
37% for Palauan males and 22% for Palauan
females. Among the Chamorro subgroups, the
people in California had a lower prevalence of
hyperuricemia than those in G u a m and Rota.
Among the Palauans, the Peleliu males and
Ngerchelong females had the lowest prevalence
ratios.
Dietary Survey
Table 4 shows the mean total daily caloric
intakes by age, sex and geographic subgroups.
For comparison, mean serum uric acid levels
were included. T h e Chamorros of California
and Guam reported intakes similar to the typical “Western type” diet being relatively high in
animal and saturated fat and low in carbohydrate. In contrast, the Chamorros of Rota and
Palauans reported intakes which were relative-
Arthritis and Rheumatism, Vol. 15, No. 4 (July-August 1972)
385
REED ET AL
Table 3. Percentages of Subjects With Hyperuricemia by Age, Sex and Area
Chamorros
FemaIes
Males
Age groups
Calif
Guam
Rota
Calif
Guam
Rota
20-29
30-39
40-49
'50-59
60
+
14
23
28
47
56
39
53
53
40
59
58
52
39
54
55
7
8
19
37
40
18
29
28
39
48
21
24
32
38
52
Mean*
30
48
52
19
30
31
~~
Pa la ua ns
Males
Age groups
Females
Koror
Peleliu
Nger
Koror
Pelel i u
Nger
20-29
30-39
40-49
50-59
60
+
30
39
38
61
46
22
20
25
29
33
25
40
50
44
50
25
22
16
20
27
38
33
17
25
28
0
6
26
41
37
Mean*
40
25
40
22
30
18
*Age-adjusted t o the 1958 Trust Territory population
ly high in carbohydrate and low in fat. T h e
sources of calories derived from protein, were
generally meat in California and Guam, and
fish in Rota and Palau (6).
For the geographic subgroups of Chamorros
and Palauans, there was a general pattern of
association of mean serum uric acid levels with
total caloric intake. This pattern was further
reflected in an association of serum uric acid
levels with calories derived from protein and
carbohydrate sources, but not with calories
dervied from fat. T h e Palauan female
subgroups were the only ones which did not
show this pattern. In terms of nutrients as percentages of total calories, there was no consistent association with mean serum uric acid levels. Separate analysis showed no association of
serum uric acid levels with calories derived from
saturated or polyunsaturated fats.
386
Clinical Features
Interview questions indicated positive histories of joint disease for 10% of the examined
males and 14% of the females. Histories were
positive for gout in 5% of Chamorro males and
2% of the Chamorro females (there was no
Palauan term for gout). T h e mean serum uric
acid levels were higher for persons with positive
histories, than for those without, but the differences were statistically significant at the 0.05
level for females only.
Physical examination findings indicating arthritic disease were found for 16 (1.3%) of the
Chamorros and 7 (1.3%) of the Palauans. T h e
mean serum uric acid levels for these persons
with arthritic changes were similar to the mean
level for persons without such findings.
Separate analysis of the frequencies of positive
Arthritis and Rheumatism, Vol. 15, No. 4 (July-August 1972)
SERUM URIC ACID LEVELS
Table 4. Comparison of Mean Daily Caloric Intakes With Mean Serum Uric Acid Levels by Sex and Area*
(Nutrients as Percentages of Total Daily Calories are Shown in Parentheses)
Males
Subjects
Mean serum
uric acid
Meantotal
daily calories
Calories f r o m
protein
Calories from
carbohydrate
~
Chamorro
Calif
Guam
Rota
Pa la ua n
Koror
Pelel i u
Nger
Calories from
fat
~~
6.4
7.1
7.2
242 1
2619
2905
363( 15)
393( 15)
436( 15)
1041(43)
1310(50)
1743(60)
1017(42)
9 16(35)
726(25)
6.8
6.2
6.7
2203
1836
2262
441(20)
349(19)
362(16)
1432(65)
1102(60)
1312(58)
330( 15)
385(21)
588(26)
Females
Chamorro
Calif
Guam
Rota
Palauan
Koror
Peleliu
Nger
4.9
5.4
5.4
1611
1807
1963
258( 16)
289( 16)
295( 15)
661(41)
885(49)
1080(56)
692(43)
633(35)
588(30)
5.2
5.5
4.9
1651
1637
1853
281( 17)
327(20)
278( 15)
1007(61)
1048(64)
1056(57)
363(22)
262(16)
519(28)
"'All values have been age-adjusted to the 1968 Micronesian Trust Territory population
histories a n d a r t h r i t i c disease a m o n g t h e
subgroups showed no meaningful differences.
Correlation Analysis
Associations between serum uric acid values
and other variables tabulated by geographic
subgroupings are difficult to interpret because
group characteristics may not reflect individual
experience. W e therefore examined the relations of serum uric acid levels and other variables as characteristics of individuals by means
of correlation analysis. Table 5 shows the resulting correlation coefficients for all Chamorros and Palauans by sex. T h e effect of age upon
all variable pairs, except the age and serum uric
acid pair, has been removed by partial correlation. Those correlations which were significantly different from 0 at the 0.05 level were
starred.
Serum uric acid levels were positively associated with measures of blood pressure and
obesity (weight, skinfolds and calculated percent body fat) for most groups. There were also
significant associations with serum triglyceride,
but not for serum cholesterol levels. T h e association with age was significant only for the
Chamorros. There was no consistent association with EKG abnormalities, symptom score,
serum glucose levels, smoking habits or any of
the measures of education, occupation, sociocultural attitudes or residential mobility.
DISCUSSION
Studies of Western populations indicate that
serum uric acid has a unimodal distribution
with slight skewing toward higher values. T h e
mean value is generally about 5.0 mg/100 ml
for males and 4.0 mg/100 ml for females (9-1 1).
T h e mean serum uric acid levels we found
among Chamorros and Palauans, in agreement
with the values reported by Burch et a1 ( l ) ,
were significantly higher than the values re-
Arthritis and Rheumatism, Vol. 15, No. 4 (July-August 1972)
387
REED ET AL
ported among Western populations. W e did not
find a bimodal frequency distribution, as reported by Burch et a l ( l ) , but rather a unimodal distribution, with slight skewing towards
higher values as generally reported for large
population surveys. T h e larger number of
people in our study probably accounts for this
difference.
A basic question is whether the high serum
uric acid levels are due to genetic or environmental factors. Kellgren has suggested that the
people of the Pacific belong to one large gouty
family (1 1). Indeed, high serum uric acid levels
have been reported for Maori, Cook Island and
Samoan Polynesians (1 2, 13), Filipinos (14,
15), Indonesian Malayans (16) and Chamorro
and Carolinian Micronesians (1).
Detailed analyses of blood group variations
have shown that both the Chamorros and
Palauans have blood group gene frequencies
similar to those found among Filipinos and Indonesian Malays (5, 17). T h e C a r o l i n i a n s
studied by Burch on Saipan and T r u k have
blood group gene frequencies favoring an intermediate pattern of both Indonesian and
Polynesian influence (5); the Polynesians
studied by Prior et a/ (12) have blood group
gene frequencies which are quite different from
Indonesian patterns (18). Thus, while the prevalence of hyperuricemia among Chamorros,
Palauans, Filipinos and Malayans could be
linked to a common ancestral influence, the
similarly high prevalence among mixed Carolinian and pure Polynesian subgroups cannot.
O n the other hand, the only evidence of environmental influence upon the Pacific pattern
of hyperuricemia comes from studies of
Filipinos living in different areas. Several investigators have reported that serum uric acid
levels were high among Filipinos living in the
Table 5. Age Partialed Correlation Coefficients for Serum Uric Acid by Study Groups and Sex
Chamorros
Variables
Age
Weight
Triceps skinfold
Subscapular skinfold
Percent bodyfat
Systolic BP
Diastolic BP
Serum glucose
Serum cholesterol
Serum triglyceride
EKG abnormal it ies
Symptom score
Cigarettes per day
Years of school
Years away birthplace
Number of places lived
Traditional attitudes
Traditional food score
Occupation
Mobility score
Male
.16"
17::.
.09
,16::
,13::
.16"'
,20"
Palauans
Female
.13
17::
,17"
.oo
-.02
.08
.ll
.05
.04
.22+
-.14:::
.03
.08
12'3
.04
,134
.01
.01
-.08
-.09
-.02
-.06
23:;
-.08
.05
-.08
.07
.06
.02
-
.01
-
Male
,30"
,214
,17+
16::
,17::
16::
.10
.ll
,24
.13
,18:2
-t
.08
-.04
.05
-.05
.04
-.06
-.01
.02
.08
Female
.ll
,23^
.22"
.25*
24"
,23"
.20"
.06
.06
.14"
.07
.10
.00
.05
.07
.04
.02
.05
-.11
"The magnitude of these coefficients in relation to the sample size have P < 0.05.
+Not available
388
Arfhritir and Rheumatism, Vol. 15, No. 4 (July-August 1972)
SERUM URIC ACID LEVELS
United States and Hawaii (14, 15) but not
among those in the Philippine Islands (19).
Healey et a1 have suggested that this difference
may be due to an inherited defect in renal excretion of uric acid which becomes manifest
when the Filipinos change to a high purine
Western diet (1 9).
It is difficult to evaluate the importance of
diet among the groups we studied. In terms of
“type” of diet, the Chamorros in California,
reporting a Western diet relatively high in animal protein and fat, had lower serum uric acid
levels than both Chamorros on Rota, who reported a typical island type diet, and Chamorros on Guam, who reported a Western type
diet.
Among most subgroups, however, there was
an association of serum uric acid levels and
quantity of daily caloric intakes, especially calories derived from protein and carbohydrate. As
the dietary survey information was obtained
only for subsamples and could only be used to
describe groups rather than individuals, these
associations should be viewed cautiously.
While there were differences in serum uric
acid levels among the geographic subgroups we
studied, analysis both by area and individual
characteristics showed no obvious association of
uric acid levels with sociocultural factors, including education, occupation, geographic mobility, cultural attitudes and exposure to modernization.
Thus, from an overall evaluation of serum
uric acid levels between and within the study
groups, we were impressed with the similarity
of values regardless of environmental conditions. This suggested that, except for a possible
dietary influence, the risk of hyperuricemia was
more strongly associated with being a Micronesian than with geographic residence or life
style.
ACKNOWLEDGMENTS
Dr. Milton Nichaman, Nutrition Program, CDC, Atlanta, Ga, directed the laboratory studies. Dr. Jean Hankin, University of Hawaii School of Public Health, con-
ducted the dietary survey. Paul Callen assisted with the
computer analyses. Dr. William Peck, Commissioner of
Health, Trust Territory of the Pacific Islands and his staff,
members of the NlNDS Research Center of Guam, and the
members of The University of Texas School of Public
Health greatly assisted the examinations.
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Ann Rheum Dis 25:114-116, 1966
2. Reed D M , Labarthe D R , Stallones RA: Health
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REED ET AL
hyperuricemia. Bull Rheum Dis 20:600-603,
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DR-MORRIS ZlFF HONORED BY NEW YORK UNIVERSITY
Dr. Morris Ziff, professor of internal medicine a t T h e University of Texas Southwestern
Medical School, Dallas, Texas, received the Medical Alumni Achievement Award of the New
York University School of Medicine Alumni Association on April 22, 1972. Dr. Ziff was
honored for his contributions to the understanding of connective tissue disease in man. H e
received a BS, a PhD in chemistry and an M D from NYU and was on the faculty of the School
of Medicine. D r . Ziff was president of the AMERICAN RHEUMATISM ASSOCIATION and Chairman of the Medical Administrative Committee of T h e Arthritis Foundation in 1965-1966.
390
Arthritis and Rheumatism,Vol. 15, No. 4 (July-August 1972)
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