American Journal of Epidemiology Advance Access originally published online on August 28, 2007
American Journal of Epidemiology 2007 166(11):1280-1287; doi:10.1093/aje/kwm201
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ORIGINAL CONTRIBUTIONS |
Coronary Artery Calcification in Japanese Men in Japan and Hawaii
1 Division of Biostatistics and Epidemiology, University of Virginia School of Medicine, Charlottesville, VA
2 Department of Health Science, Shiga University of Medical Science, Otsu, Shiga, Japan
3 Pacific Health Research Institute, Honolulu, HI
4 Honolulu Heart Program and Honolulu-Asia Aging Study, Kuakini Medical Center, Honolulu, HI
5 Department of Geriatric Medicine, John A. Burns School of Medicine, University of Hawaii, Honolulu, HI
6 Department of Epidemiology, University of Pittsburgh, Pittsburgh, PA
7 Cardiovascular Institute, University of Pittsburgh, Pittsburgh, PA
8 Department of Internal Medicine, Korea University School of Medicine, Seoul, South Korea
9 Department of Internal Medicine, Shiga University of Medical Science, Otsu, Shiga, Japan
10 Cardiovascular Epidemiology, Kyoto Women's University, Kyoto, Japan
11 Holistica Hawaii, LLC, Honolulu, HI
Correspondence to Dr. Robert D. Abbott, University of Virginia Health System, Department of Public Health Sciences, P.O. Box 800717, Charlottesville, VA 22908-0717 (e-mail: rda3e{at}virginia.edu).
Received for publication April 25, 2007. Accepted for publication June 12, 2007.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Explanations for the low prevalence of atherosclerosis in Japan versus the United States are often confounded with genetic variation. To help remove such confounding, the authors compared coronary artery calcification (CAC), a marker of subclinical atherosclerosis, between Japanese men in Japan and Japanese men in Hawaii. Findings were based on risk factors and CAC measured from 2001 to 2005 in 311 men in Japan and 300 men in Hawaii. Men were aged 40–50 years and without cardiovascular disease. After age adjustment, there was a threefold excess in the odds of prevalent CAC scores of
10 in Hawaii versus Japan (relative odds = 3.2, 95% confidence interval: 2.1, 4.9). Whereas men in Hawaii had a generally poorer risk factor profile, men in Japan were four times more likely to smoke cigarettes (49.5% vs. 12.7%, p < 0.001). In spite of marked risk factor differences between the samples, none of the risk factors explained the low amounts of CAC in Japan. After risk factor adjustment, the relative odds of CAC scores of 10 in Hawaii versus Japan was 4.0 (95% confidence interval: 2.2, 7.4). Further studies are needed to identify factors that protect against atherosclerosis in Japanese men in Japan.
atherosclerosis; cohort studies; coronary disease; Japan; men; risk factors
Abbreviations: CAC, coronary artery calcification
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Compared with men in the United States, Japanese men in Japan have a low risk of coronary heart disease. Increasing evidence further suggests that the Japanese are less prone to subclinical atherosclerosis (1, 2). In a recent study of coronary artery calcification (CAC), a marker of subclinical atherosclerosis, Japanese men in Japan had higher blood pressure levels, higher concentrations of low density lipoprotein cholesterol, and higher levels of fasting blood glucose, and they were more likely to have diabetes than Caucasian men in the United States (1, 2). Men in Japan were also three times more likely to smoke cigarettes. In spite of having a less favorable cardiovascular risk profile for several important risk factors, the men in Japan had half the prevalence of CAC of the men in the United States (1).
Unfortunately, it could not be determined whether the low levels of atherosclerosis in Japan versus the United States could be explained by genetic or environmental factors. In an attempt to remove potential explanations due to genetic differences, this study compared the prevalence and correlates of CAC between men in Japan and men in Hawaii who are entirely Japanese. For both samples, measurement of CAC and concomitant risk factors followed identical protocols.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Study samples
From 2001 to 2005, 311 Japanese men from Japan and 300 Japanese men from Hawaii were enrolled in a study of CAC and its correlated risk factors. Men were aged 40–50 years. In Japan, men were residents of Kusatsu City in Shiga prefecture and were descendents of Japanese parents (1, 2). The largely westernized men from Hawaii were second- and third-generation offspring of Japanese who migrated to Hawaii near the beginning of the 20th century. All participants were without clinical cardiovascular disease, type I diabetes, cancer (except for skin cancer in the past 2 years), renal failure, and genetic familial hyperlipidemias.
In Kusatsu City, subjects were randomly selected from a residents registry containing information on name, birth date, and address (1, 2). In Hawaii, men were randomly selected from lists of offspring of fathers who were participants in the Honolulu Heart Program (3, 4). The latter is a long-term follow-up study of coronary heart disease and stroke in Japanese-American men that began in 1965. For both samples, procedures were in accordance with institutional guidelines and were approved by an institutional review committee. Informed consent was obtained from the study participants.
CAC screening
At both sites, the same study protocol was followed. Screening for CAC was based on the use of a GE-Imatron C150 Electron Beam Tomography scanner (GE Medical Systems, South San Francisco, California), with frequent calibration by centrally trained technicians. For both scanners, measures of water density (0 Hounsfield Unit (HU)), air (–1,000 HU), and calcification (130 HU) were the same. Single scans were completed following a rigid protocol to obtain 30–40 contiguous 3-mm-thick transverse images from the level of the aortic root to the apex of the heart. Images were recorded during a maximal breath hold by using electrocardiogram-guided triggering of 100-m-per-second exposures during the same phase of the cardiac cycle. Scans were read centrally at the Cardiovascular Institute in Pittsburgh, Pennsylvania, by a trained radiology technician using a DICOM (Digital Imaging and Communications in Medicine) workstation with software from the AccuImage Diagnostic Corporation, San Francisco, California. Scoring adhered to the method of Agatston (5). The reproducibility of the scans had an intraclass correlation of 0.99 (6). Further description of the scanning procedure is provided elsewhere (1, 2, 5, 6).
Concomitant risk factors
Concomitant risk factors measured at the time of CAC screening included age, body mass index, systolic blood pressure, hypertension status, use of medications to treat hypertension, diabetes, fasting blood glucose, insulin, low density lipoprotein cholesterol, hypercholesterolemia, use of medications to treat hypercholesterolemia, high density lipoprotein cholesterol, triglycerides, C-reactive protein, fibrinogen, homocysteine, and parental history of coronary heart disease. Lifestyle factors included current and former cigarette smoking, alcohol intake, being sedentary at work, and frequent intake of fish, beef, or pork and of soy products (4 times/week). Body mass index was calculated as weight divided by height squared (kg/m2). Hypertension was diagnosed when systolic blood pressure was 140 mmHg, when diastolic blood pressure was 90 mmHg, or when a subject was being treated for high blood pressure. Diabetes was diagnosed when fasting serum glucose level was 7 mmol/liter or a subject was receiving insulin or oral hypoglycemic therapy. Hypercholesterolemia was defined when low density lipoprotein cholesterol levels were 4.14 mmol/liter or when medications were being taken for the treatment of an adverse lipid profile. A description of the methods used to measure the other risk factors is given elsewhere (1, 2, 7).
Statistical methods
The percentage of men with CAC scores above common CAC cutpoints was derived for each sample and was compared through the use of exact testing methods. The median and the 20th and 80th percentiles were also compared. Because the distribution of CAC scores was skewed (with many scores = 0), the latter comparisons were based on quantile regression models (8). Use of standard regression techniques was not considered in this study because they are often limited to modeling average values, where inference and prediction can be adversely influenced by skewness and unstable variances. While log and power transformations often provide a means for removing such influences, they are also limited to applications with nonzero CAC scores. To compare concomitant risk factors between the samples, t tests and standard procedures for comparing binomial proportions were used.
In this study, the association between a risk factor and the prevalence of a CAC score of 10 was examined by using logistic regression models. Here, a CAC cutpoint of 10 was selected because of its clinical importance (9) and because of the possibility that scores ranging from >0 to <10 could be an imaging artifact from spurious noise (10). Through the use of the logistic models, estimates of the relative odds (and 95 percent confidence interval) of having a CAC score of 10 within each sample were derived by comparing men with and without a risk factor condition. For continuous risk factors, relative odds were calculated for high versus low risk factor levels, where high versus low tended to correspond with a comparison between the 75th and 25th percentiles. The relative odds of having a CAC score of 10 was also adjusted for age and several concomitant risk factors. In addition, tests were conducted to determine whether the relative odds associated with a risk factor differed between the study samples.
To determine whether differences in the prevalence of a CAC score of 10 between Japan and Hawaii could be explained by confounding risk factors, the percentage prevalences of men with scores of 10 in the two cohorts were calculated and compared after adjusting for the effects of age and other risk factors by using logistic regression models and standard analysis of covariance methods (11). Estimated regression coefficients were used to derive the relative odds (and 95 percent confidence interval) of having a CAC score of 10 in Hawaii versus Japan. All reported p values were based on two-sided tests of significance.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The distribution of CAC scores among the Japanese men in Japan and Hawaii are shown in table 1. The percentage prevalence of scores of >0,
10, and 100 for men in Hawaii were significantly higher than for men in Japan (p < 0.001). Compared with men in Japan, men in Hawaii had a nearly threefold excess prevalence of CAC scores of 10 (32.0 percent vs. 11.6 percent) and a nearly sixfold excess of scores of 100 (13.3 percent vs. 2.3 percent).
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In Japan, the maximum CAC score was 538; in Hawaii, it was 3,170. Although the median CAC scores were identical, the 80th percentile in Hawaii was significantly higher than the 80th percentile in Japan (51.4 vs. 3.4, p < 0.001). The excess 80th percentile in Hawaii remained significant after adjustment for age, body mass index, systolic blood pressure, treatment for high blood pressure, diabetes, current and former cigarette smoking, low and high density lipoprotein cholesterol, treatment for hypercholesterolemia, and C-reactive protein (p = 0.007). For men with a CAC score of >0, the median and 80th percentile were each significantly higher in Hawaii versus Japan (p < 0.001). Findings remained significant after adjusting for age and the other risk factors (p = 0.007 for the median and p = 0.001 for the 80th percentile). For men with a CAC score of
10, only the median was significantly higher in Hawaii than in Japan (p = 0.007). After adjustment for age, however, the latter became insignificant (p = 0.195). Table 2 compares the study risk factors in the two samples. In Japan, data on body mass index were missing for two study participants and data on homocysteine were missing for 12 participants. In Hawaii, data on high density lipoprotein cholesterol were missing for one man. Except for cigarette smoking, low density lipoprotein cholesterol, homocysteine, and alcohol intake, men in Hawaii had a poorer risk factor profile. Compared with that of men in Japan, average body mass index was 4.3 kg/m2 higher for men in Hawaii (p < 0.001). For the average height of 170 cm (which was nearly identical in the two samples), this corresponds to a difference of 12.4 kg. Average weight in Japan was 68.5 kg; in Hawaii, it was 80.2 kg.
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Men in Hawaii also had a higher average systolic blood pressure than men in Japan (p = 0.033) in spite of a greater frequency of treatment for hypertension in Hawaii (p < 0.001). The frequency of diabetes in Hawaii was more than double the frequency in Japan (13.3 percent vs. 6.1 percent, p = 0.003). Men in Hawaii also had higher levels of fasting blood glucose and insulin. Whereas average levels of low density lipoprotein cholesterol were lower in Hawaii (3.15 mmol/liter vs. 3.43 mmol/liter, p < 0.001), men in Hawaii were six times more likely to be treated for an adverse lipid profile (23.0 percent vs. 3.5 percent, p < 0.001). The excess in treatment for an adverse lipid profile in Hawaii further explains the significant excess of hypercholesterolemia in Hawaii. In addition, compared with those in Japan, levels of high density lipoprotein cholesterol were lower in Hawaii (p = 0.002), whereas levels of C-reactive protein were higher (p = 0.001). Compared with men in Hawaii, Japanese men had lower levels of fibrinogen but higher levels of homocysteine. Men in Hawaii were more than twice as likely to have a parental history of coronary heart disease as men in Japan (28.7 percent vs. 13.2 percent, p < 0.001).
Regarding the lifestyle factors, men in Hawaii were six times more likely to be sedentary at work, more than twice as likely to be frequent consumers of beef or pork (4 times/week), and far less likely to be frequent consumers of fish or soy products (4 times/week). In contrast to the excess in several adverse risk factors in Hawaii, men in Japan consumed more alcohol and were four times more likely to smoke cigarettes than men in Hawaii (49.5 percent vs. 12.7 percent, p < 0.001). Men in Hawaii were also less likely to be former smokers (p = 0.001).
The relation between the risk factors shown in table 2 and prevalent CAC scores of 10 is described in table 3 within each sample after risk factor adjustment. Here, the risk-factor-adjusted relative odds of CAC scores of 10 associated with specific risk factor comparisons are shown. Compared with those from unadjusted observations, findings were largely unchanged. Although the age range for men was limited to 40–50 years, it seems noteworthy that, in each sample, a 5-year difference in age was associated with a two- to threefold excess in the odds of a CAC score of 10. The prevalence of CAC scores of 10 was also higher among men who had greater body mass index, although it was significant in Japan only. In the latter, a difference of 6 kg/m2 is associated with a 2.8-fold excess in the odds of a CAC score of 10. In both samples, the odds of an elevated CAC score increased approximately threefold for current smokers versus nonsmokers, although it was significant in Hawaii only. Of the remaining risk factors, high low density lipoprotein cholesterol levels in Japan were related to elevated CAC levels. Here, a low density lipoprotein cholesterol difference of 1.3 mmol/liter was associated with a twofold excess in the prevalence of a CAC score of 10.
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In Japan, as described in an earlier report (12), excessive intake of alcohol was also associated with a greater prevalence of elevated CAC scores, while a similar finding in Hawaii was absent. In Japan, although diabetes and treatment for hypertension and hypercholesterolemia seemed to also be associated with higher amounts of CAC, excesses were not statistically significant. The latter finding could be due, in part, to a limited sample size. Removing data for men being treated for hypercholesterolemia failed to markedly change the observations shown in table 3. Although some of the differences in table 3 in the relative odds of a prevalent CAC score of
10 between the two samples appear large (e.g., body mass index and treatment for high blood pressure), none were statistically significant.
In table 4, the possibility that the risk factors considered in this study could explain the low prevalence of CAC scores of 10 in Japan versus Hawaii is explored. After age and risk factor adjustment (including adjustment for lifestyle factors), the difference in the prevalence of scores of 10 remained unchanged (p < 0.001). In an attempt to avoid overparameterizing the statistical models used in table 4, effects of smaller subsets of risk factors and other characteristics in table 2 were also examined. Results failed to alter the findings shown in table 4. An excess of CAC scores of 10 in the sample from Hawaii versus Japan also persisted among current and noncigarette smokers and for men not being treated for hypercholesterolemia.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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In this comparison of Japanese men in Japan and Hawaii, the prevalence of CAC scores of
10 was nearly three times higher in Hawaii than in Japan. Although these men were relatively young (aged 40–50 years), there were substantial levels of CAC in Hawaii that were well over the threshold for significant obstructive atherosclerosis (13). Over 13 percent of the men in Hawaii had CAC scores of 100 compared with 2.3 percent of the men in Japan. Given the increased exposure to Western lifestyles for Japanese in Japan, these findings suggest that these men are capable of developing the same excessively high levels of atherosclerosis as in Hawaii. They are also consistent with observations from the Multi-Ethnic Study of Atherosclerosis, where increased acculturation into the United States has been associated with CAC in other ethnic samples (14, 15). In contrast to the current comparison, the Multi-Ethnic Study of Atherosclerosis includes a broad spectrum of acculturation in the United States. Here, men in Japan who have been acculturated to Japanese lifestyles in Japan were compared with Japanese men in Hawaii who have been acculturated to Western exposures in the United States through multiple generations.
No single risk factor (or set of risk factors) considered in the current study explained the low amounts of CAC in Japan versus Hawaii, and it could not be determined whether the adverse cardiovascular consequence from the generally poorer risk factor profile in Hawaii was worse than the excessive rates of smoking in Japan. When replacing the CAC cutpoint of 10 with scores of >0, it is interesting to note that each of the risk factors, except body mass index, persisted in failing to explain the excess of CAC scores of >0 in Hawaii versus Japan (49.3 percent vs. 31.2 percent, p < 0.001). When adjustments for body mass index were made, the prevalence of CAC scores of >0 became similar (38.9 percent in Japan and 41.1 percent in Hawaii, p = 0.605). The latter finding could partly be due to an exceptionally high frequency of obesity (body mass index 30 kg/m2) in the men from Hawaii with CAC scores ranging from >0 to <10. Here, 42.3 percent were obese compared with 18.4 percent of the men with CAC scores of 0 and 33.3 percent of those with CAC scores of 10. In contrast, only 4.9 percent of the men in Japan with CAC scores of >0 to <10 were obese. For those with CAC scores of 0 and 10, 1.4 percent and 8.6 percent were obese, respectively. It may be that the 1.6-fold excess of CAC scores of >0 in Hawaii versus Japan is more easily explained by a difference in body mass index compared with the three- and nearly sixfold excesses of scores of 10 and 100 observed in Hawaii.
The prevalence of high CAC scores in Japan also remained low in spite of a fourfold excess in the use of cigarettes in Japan versus Hawaii (49.5 percent vs. 12.7 percent, p < 0.001). Whether there are risk factor associations with prevalent CAC that differ between nonsmokers in Japan and those who smoke excessively warrants consideration. One possible factor might include fish intake. In the Honolulu Heart Program, risk of death was halved in heavy smokers who consumed high quantities of fish compared with those whose consumption was low (16). In the current study, high fish intake could not be shown to be associated with low amounts of CAC for either smokers or nonsmokers, although the latter could be due to limited statistical power.
Differences in intake of other dietary items such as beef or pork and soy products also failed to explain the high prevalence of CAC scores in Hawaii versus Japan. In an earlier report involving the current sample from Japan, alcohol intake was shown to have a J-shaped relation with CAC (12). In Hawaii, a similar finding was absent. Differences in the intake of ethanol and its associations with CAC between the two samples also failed to explain the excess of CAC observed in Hawaii.
Cardiovascular risk factors also failed to explain the twofold excess of CAC in a sample of Caucasian men in the United States in a comparison with the current sample in Japan (1, 2). This excess occurred in spite of the Japanese men having a more adverse cardiovascular risk profile for several risk factors, including higher blood pressures, higher concentrations of low density lipoprotein cholesterol, and higher levels of fasting blood glucose. Compared with the Caucasian men, the Japanese men in Japan were also more likely to have diabetes and to smoke cigarettes. Although genetic factors unique to the Japanese may offer some protection against this adverse risk factor profile, results of the current study imply that it is unlikely that genetic variation can provide more than a partial explanation for the low prevalence of CAC in Japanese men in Japan.
Of course, there is the assumption that gene distributions and genetic susceptibilities are similar between the Japanese samples being compared. In addition to being entirely Japanese, the two samples were also all men, were of the same age, and had identical periods of study execution. As in all populations, while genetic variation is present in Japan, the extent of this variation is likely to be considerably less than in Caucasian men in the United States, where ancestral diversity is high. As a result, it is likely that the Japanese samples in the current comparison are genetically quite similar. Even with equal frequencies of genetic susceptibility, however, genetics may still be important. An excess of nongenetic risk factors in one sample could alter disease risk by providing an environment for genetic effects to have a role in disease processes.
In addition to a comparison between samples of men who are all Japanese, other strengths of the current study are worth noting. Most important is that the study samples were examined through a common research protocol. All phases of the study were coordinated by principal investigators in Japan, in Hawaii, and at the Cardiovascular Institute in Pittsburgh, Pennsylvania. Technicians received identical training, and all CAC scans were centrally scored. The excess prevalence of CAC in the Japanese men in Hawaii versus Japan is also consistent with the excess in coronary heart disease that has been observed to occur in Japanese who migrate to the United States (3, 17–22).
Although these observations are specific to men of Japanese ancestry, it needs to be determined whether they can be generalized to include women. In addition, failure of the risk factors considered in this study to explain the excess of CAC in Hawaii versus Japan could be due to the single measurement of the risk factors at the time of CAC determination. It may be that risk factors that coexist with CAC levels are poor measures of long-term exposure to adverse risk factor profiles with origins in young adulthood. Whether this long-term exposure offers insight into the difference in CAC development between Japanese in Japan and Hawaii warrants consideration. Findings for the age range of 40–50 years may also not apply to other age groups, although having a narrow age range can increase the homogeneity of the samples being compared. It seems clear, however, that there are significant implications for the prevention of cardiovascular disease in all ethnic groups if the factors that protect against subclinical atherosclerosis can be identified, particular among Japanese men in Japan who smoke excessively. Further studies of CAC and its progression in larger samples are needed to increase the capacity to identify such factors that promote atherosclerosis or protect against its development.
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ACKNOWLEDGMENTS |
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Supported by a contract (N01-AG-4-2149) and grant (1-R01-AG17155) from the National Institute on Aging; a contract (N01-HC-05102) and grants (R01-HL068200 and R01-HL071561) from the National Heart, Lung, and Blood Institute; a grant (1-R01-NS41265-01) from the National Institute of Neurological Disorders and Stroke; a grant from the US Department of the Army (DAMD17-98-1-8621); a grant (0160512U0) from the American Heart Association; a grant-in aid for scientific research (A: 13307016) from the Japanese Ministry of Education, Culture, Sports, Science and Technology; and the Japan Society for the Promotion of Science.
The authors thank Lori Givens and Susan Simmons for their expert technical role in the scoring of coronary artery calcification.
Conflict of interest: none declared.
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