Reported Family History of Cancer in the Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial

Paul F. Pinsky1,, Barnett S. Kramer2, Douglas Reding3 and Saundra Buys4

1 Division of Cancer Prevention, National Cancer Institute, Bethesda, MD.
2 Office of Disease Prevention, Office of the Director, National Institutes of Health, Bethesda, MD.
3 Marshfield Medical Research and Education Foundation, Marshfield, WI.
4 Division of Hematology-Oncology, Department of Internal Medicine, University of Utah School of Medicine, Salt Lake City, UT.

Received for publication June 19, 2002; accepted for publication November 4, 2002.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 
The authors analyzed data from almost 150,000 subjects aged 55–74 years enrolled in the Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial who completed a self-administered baseline questionnaire (1993–2001) that included items about family history of cancer. Male respondents reported significantly less family history of cancer than females. The relative underreporting by male respondents relative to females was greater for female family members (28% lower for sisters and 21% lower for mothers) than for male family members (13% lower for brothers and 9% lower for fathers). Black, Hispanic, and Asian respondents reported significantly less family history of cancer than Whites. Reported family history prevalences for parents decreased with respondents’ age, while those for siblings increased with respondents’ age. The four most commonly reported cancers in families were breast (11.8%), lung (10.1%), colorectal (9.4%), and prostate (7.3%) cancer. Expected prevalences in family members of history of cancer overall and history of specific types of cancer were calculated using incidence rates and life table data obtained from the Surveillance, Epidemiology, and End Results Program. Overall, the ratio of reported cancer rates to expected cancer rates in family members was approximately 0.7. Liver, bone, stomach, and brain cancer had greater-than-average reported:expected ratios, while lymphoma, bladder cancer, melanoma, and testicular cancer had lower-than-average ratios.

ethnic groups; family characteristics; genetic predisposition to disease; neoplasms; questionnaires; sex factors

Abbreviations: Abbreviations: CI, confidence interval; PLCO, Prostate, Lung, Colorectal, and Ovarian; SEER, Surveillance, Epidemiology, and End Results.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 
Interest in the contribution of genetic factors to cancer etiology is strong and has been growing in recent years. One of the most common methods of exploring the impact of genetic factors is ascertainment of family history of cancer. Frequently, such family history data are obtained through the use of questionnaires. It is therefore essential that the validity of family history data obtained in this manner be assessed. A number of small-scale studies have been performed in which researchers attempted to directly verify reports of family cancer history through cancer registries or other means (13). These studies have been useful in the estimation of false-negative and false-positive rates (i.e., errors of omission or commission) for overall cancer in family members and for some of the more common types of cancer (e.g., breast cancer, colon cancer). However, the modest size of these studies has limited investigators’ ability to detect differences in validity by demographic factors or to assess the relative validity of reports of less common cancer types.

The Prostate, Lung, Colorectal, and Ovarian (PLCO) Cancer Screening Trial is a large, ongoing, national, multicenter cancer screening trial which includes a baseline questionnaire component with a family cancer history section (4). Data from this study provide us with an opportunity to assess reported family history of cancer in a large group of volunteers in a cancer-related study and to indirectly assess the validity of such data. Although we do not have direct verification of reported cancers, the large size of this study allows us to examine with great precision the effects of factors such as age, sex, and race/ethnicity on reported family history of cancer. The study’s size also makes it feasible to compare the reported rates of various cancers with the rates expected on the basis of national population-based registries, and thus to help identify which cancers may be absolutely or relatively under- or overreported. Internal analysis of the family history data reported, together with analysis of the corresponding expected rates, may provide clues to assessing the validity of these data and may help us determine whether any systematic biases are present. Assessment of the validity of these data is important not only for future studies based on PLCO data but also for performing and examining family history studies based on similar questionnaire data.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 
Randomization of subjects aged 55–74 years to the screened or control arm of the PLCO Trial began in 1993 and was completed in July 2001. Subjects with a personal history of one of the four PLCO cancers or who were currently undergoing treatment for any cancer, except basal- or squamous-cell skin cancer, were excluded from the trial, as were subjects who had a recent history of certain screening procedures (4).

Around the time of randomization, study subjects were asked to complete a written, self-administered baseline questionnaire that included questions on demographic factors, medical history, history of smoking and other health-related behaviors, and familial and personal history of cancer. The family history section of the questionnaire (questions 18–21) is displayed in figure 1. Respondents were asked to list each parent, sibling, or child with a history of cancer (not including basal-cell skin cancer) and to specify the type(s) of cancer and the age(s) of diagnosis; respondents were also asked about the total numbers of sisters and brothers that they had. The open-ended responses on cancer type were coded at each screening center according to a standardized protocol.



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FIGURE 1. Questions on the baseline questionnaire (1993–2001) of the Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial that were related to family history of cancer.

 
We calculated the expected prevalence in family members of a history of various cancer types and of overall cancer based on life tables and on cancer incidence rates as derived from the National Cancer Institute’s Surveillance, Epidemiology, and End Results (SEER) database (see Appendix for details). The method also allowed for calculation of the expected age distribution at diagnosis. We limited this analysis to siblings’ cancers, because a large percentage of parents’ cancers would have occurred prior to 1973, the year the SEER Program was initiated. Expected probabilities were created for the overall population and separately for family members of Whites and Blacks (for the latter, we assumed that first-degree relatives were of the same race as the respondent). Individual cancer types were defined according to International Classification of Diseases for Oncology, Second Edition, site and morphology codes, as defined by the SEER Program (5). In-situ cancers were excluded.

Logistic regression was used to model the odds that a family member had a history of cancer as a function of various covariates. Confidence intervals for the ratio of reported rates of cancer to expected rates were calculated assuming fixed expected rates and a Poisson distribution for the reported rates.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 
The PLCO Trial randomized almost 155,000 subjects. The current analysis was based on the 149,332 subjects (96 percent) who completed the family history section of the baseline questionnaire. The age and sex distributions of the study participants are given in table . Approximately 88 percent of the cohort was (non-Hispanic) White, 5.1 percent was (non-Hispanic) Black, 1.9 percent was Hispanic, 3.7 percent was Asian, and 1 percent was of unknown or other ethnicity. The average number of siblings was 3.5 for both male and female respondents, with 7 percent of both sexes reporting no siblings. The population was relatively well educated; almost 93 percent had completed high school, and 35 percent had completed college.


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TABLE 1. Age and sex distributions of respondents in the Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial, 1993–2001
 
Results for overall cancer
A family history of cancer (defined as a history of any cancer, except basal-cell skin cancer, in parents, siblings or half-siblings, or offspring) was reported by 57.1 percent of respondents. Of all reported cancers, 57 percent were reported in parents, 40 percent in siblings, and 3 percent in offspring. The prevalence of a family history of cancer showed relatively little geographic variation; all 10 PLCO centers had prevalences of 55–60 percent.

As table shows, male respondents reported a significantly lower family history prevalence (53.1 percent) than females (61.0 percent) (difference = 7.9 percent, 95 percent confidence interval (CI): 7.4, 8.4). Table also displays the percentages of mothers, fathers, brothers, and sisters with a reported history of cancer, by the sex of the respondent. Male respondents reported significantly lower prevalences than females for all four types of relatives (p < 0.0001). Logistic modeling also demonstrated a significant interaction between the sex of the respondent and the sex of the relative (p < 0.0001); specifically, the underreporting of family history by male respondents as compared with females was lower for male relatives than for female relatives. This can be seen in table , where this underreporting was 28 percent for sisters (i.e., 100 x [1 – 8.6/11.9]) and 21 percent for mothers, as compared with 13 percent and 9 percent for brothers and fathers, respectively. The proportion of cancers reported to be of unknown type was significantly greater for male respondents (5.8 percent) than for female respondents (2.7 percent); as above, there was a significant interaction in that the differential between male and female respondents’ unknown percentages was significantly greater for female relatives than for males. Among relatives reported to have had cancer, the proportion reported to have had multiple types of cancer was significantly lower for male respondents (6.5 percent) than for female respondents (9.2 percent).


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TABLE 2. Prevalence (%) of a reported history of cancer among family members in the Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial, 1993–2001
 
For siblings, reported cancer history prevalence was compared with expected prevalence. The ratios of reported prevalence to expected prevalence were closer to 1.0 for female respondents than for male respondents for both brothers and sisters; females had reported:expected ratios of 0.88 (95 percent CI: 0.86, 0.89) and 0.70 (95 percent CI: 0.69, 0.72) for sisters and brothers, respectively, while male respondents had corresponding ratios of 0.63 (95 percent CI: 0.62, 0.65) and 0.60 (95 percent CI: 0.59, 0.62).

Cancer history rates are displayed in table by the race/ethnicity of the respondent. Logistic modeling, which controlled for the age and sex of respondents, showed that Black, Hispanic, and Asian respondents each reported significantly (p < 0.0001) lower overall family history rates and lower rates for mothers, fathers, sisters, and brothers than did non-Hispanic White respondents. Blacks also had significantly (p < 0.0001) lower ratios of reported rates to expected rates in brothers and sisters (0.40 and 0.53, respectively) than did Whites (0.68 and 0.79, respectively). Brothers of Blacks had 25 percent higher expected rates than did brothers of Whites, while sisters of Whites had expected rates similar to those of sisters of Blacks. All four racial/ethnic groups demonstrated significantly lower reported rates for male versus female respondents, with the male:female ratio being lower among Blacks, Hispanics, and Asians than among Whites (data not shown).


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TABLE 3. Prevalence (%) of a family history of cancer by race/ethnicity in the Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial, 1993–2001
 
Respondents with very little education (<8 years) reported family history rates that were significantly lower than average (48.5 percent for males and 48.8 percent for females); however, this group comprised only 1 percent of the population. Among persons with 8 or more years of education, there was relatively little effect of education on reported family history rates. Reported rates for females decreased slightly with educational level, ranging from 62.7 percent for 8–11 years of schooling to 58.4 percent for postgraduate education. There was no clear trend with educational level in males; the rate was lowest (51.7 percent) for college graduates and highest (54.1 percent) for post-high-school (vocational or technical) training.

As table shows, the reported family history rates for siblings increased significantly with the age of the respondent, while the reported rates for parents decreased significantly with the age of the respondent (p < 0.0001 for both trends). These age trends for siblings and parents were seen for both male and female respondents and male and female relatives (not shown in the table). The percentage of reported parental cancers that were of unknown type significantly increased with the respondent’s age (p < 0.0001); for siblings, there was no linear trend with age, although the rates in the oldest age group were elevated (table ).


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TABLE 4. Prevalence (%) of a family history of cancer and percentage of cancers of unknown type, by the age of the respondent, Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial, 1993–2001
 
There was a modest but statistically significant relation between the number of siblings and the proportion reported to have a history of cancer. The proportion of respondents’ siblings reported to have had cancer decreased 1.7 percent (95 percent CI: 1.3, 2.0), on average, with each additional sibling up to 12 siblings, and it decreased 3.1 percent (95 percent CI: 2.7, 3.4) for each additional sibling from 13 through 20.

Results by cancer type
Table displays the percentage of respondents reporting any family history for various types of cancer. The four cancers most commonly reported in families were breast (11.8 percent), lung (10.1 percent), colorectal (9.4 percent), and prostate (7.3 percent) cancer. Breast, lung, and colorectal cancers each had approximately 1 percent of respondents reporting two or more relatives with the given cancer (table ). A total of 26 respondents (0.02 percent) had families meeting the Amsterdam criteria for hereditary nonpolyposis colon cancer—that is, three or more relatives of at least two generations with colorectal cancer, at least two of whom are first-degree relatives of the third and at least one of whom was diagnosed by age 50 (6). A total of 250 respondents (0.2 percent) had a family history consistent with breast-ovarian syndrome—that is, three or more cases of breast or ovarian cancer in first-degree relatives. For most cancer types, parents and siblings comprised more than 90 percent of the reported cases; types for which offspring accounted for at least 10 percent of cases were testicular cancer (35 percent), cervical cancer (17 percent), lymphoma (14 percent), and melanoma (12 percent). Of cancers diagnosed in childhood (age <20 years) among any type of relative, the four most commonly reported types were leukemia (32 percent), brain tumors (13 percent), Hodgkin’s disease (10 percent), and bone cancer (8 percent).


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TABLE 5. Rates of a family history of cancer, by cancer type, Prostate, Lung, Colorectal, and Ovarian Cancer Screening Trial, 1993–2001
 
Table shows reported rates in siblings and the ratios of reported rates to expected rates for various types of cancer, by the sex of the respondent. Most cancers fell into the range of reported (by females) versus expected ratios of 0.6–1.4, with a few notable exceptions. Respondents (of both sexes) reported much higher than expected rates of liver and bone cancer. Cancers with reported (by both sexes) rates that were much lower than expected included testicular cancer, lymphoma, bladder cancer, and melanoma. For lymphoma, approximately 30 percent of respondents did not specify the type (i.e., Hodgkin’s vs. non-Hodgkin’s), so we only report here the combined reported (and expected) rates for lymphoma.

Blacks reported significantly lower family history rates than did Whites for all cancers listed except prostate, lung, and stomach cancer, for which the rates were essentially identical. Asians and Hispanics reported 3.0- and 1.5-fold higher rates, respectively, of a family history of stomach cancer than did Whites, and Asians also reported significantly higher rates of liver, pancreatic, and esophageal cancer than did Whites. All other cancers were reported at significantly lower rates by Hispanics and Asians than by Whites, with the exception of vaginal and uterine cancer, which Hispanics and Whites reported at essentially the same rates.

Age of diagnosis was reported for approximately 90 percent of sibling cancer cases (the other 10 percent included instances where no age was given and instances of multiple cancers where the age of diagnosis of each cancer type was not distinguished). The age distributions did not differ appreciably by the sex of the respondent. The reported median age at diagnosis was close to that expected for most cancer types, as was the reported percentage diagnosed before age 50. The reported and expected medians were within 3 years except for uterine cancer (6 years younger than expected), leukemia in females (4 years younger than expected), esophageal cancer in females (5 years older than expected), and bone cancer in males and females, where the reported medians (and percentages over 50) were much greater than expected. The percentage of cases diagnosed after age 50 also differed appreciably for uterine cancer (53 percent reported vs. 76 percent expected) and testicular cancer (33 percent reported vs. 17 percent expected).


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 
A major finding here is that males reported substantially less family history of cancer than did females, with this difference being greater for female relatives than for male relatives. Since we have no direct verification of the cancer events, we cannot say definitively which sex’s responses (on average) were more accurate. In a verification study using cancer registries, Kerber and Slattery (3) showed slightly increased accuracy of family history reports for female respondents. However, Winter et al. (7) showed no difference in male versus female awareness of relatives’ actual breast cancer history. In the current study, it seems likely that most of the differential was made up by males’ omitting cancer events rather than by females’ inventing them. Several validation studies using registries have shown that overreporting—that is, the percentage of reported cancers that could not be documented—is relatively low, ranging from 3 percent to 12 percent in several US studies (1, 3, 8). Rates of underreporting—that is, the percentage of actual cases not reported—have been estimated to be in the range of 20–30 percent (3, 9). In addition, the rates reported by females were closer to expected rates than those reported by males. Reported rates for siblings were 12–30 percent lower than expected for female respondents and approximately 40 percent lower for male respondents. The overall average underreporting was approximately 30 percent, which is consistent with the above-reported rates from the literature.

Rates of reported family history of cancer for other racial/ethnic groups were substantially lower than those for Whites. Blacks also had considerably lower reported:expected ratios than did Whites (expected rates were not calculated for Asians and Hispanics). Note that Hispanics and Asians are very heterogeneous groups, and this study population is not representative of these groups in the United States as a whole. Most of the Asians included in this study came from the PLCO center in Hawaii.

The 2000 National Health Interview Survey contained questions on family history of cancer; we obtained the raw data tapes and conducted basic analyses of data from this survey (10). The family history rates in the age group 55–74 years (n = 7,120) were generally similar to though slightly lower than those found here. The structure of the family history questions was different in the National Health Interview Survey than in the PLCO Trial (e.g., individual questions were asked about the cancer history of the respondent’s mother, father, sisters, and brothers), and the National Health Interview Survey was a telephone survey, so it would not be expected to produce identical results. The National Health Interview Survey data showed a sex-specific trend, with males reporting approximately 20 percent lower rates of a sibling history of cancer than females and 7 percent lower rates for a mother’s history of cancer (the reported rates for fathers were similar). The National Health Interview Survey also found that Blacks and Hispanics had 30–40 percent lower rates than did Whites. There were too few Asians for a meaningful comparison.

Expected rates were not computed for respondents’ parents, because a large fraction of parents’ cancers would have occurred before 1973, the earliest year for which SEER registries have data. However, we can estimate expected rates of overall cancer utilizing two different scenarios. Data from the Connecticut cancer registry showed overall age-adjusted cancer rates increasing by an average of 1.7 percent per year in males and by 0.55 percent per year in females from the late 1930s to the late 1960s (11). We calculated expected values under this (increasing) scenario by assuming that the rate in each age group increased by the above amounts each year. We also calculated expected values under the constant scenario of pre-1973 rates set equal to 1973 rates. The expected rates for fathers were 31.5 and 33.6 under the increasing and constant scenarios, respectively. Corresponding expected rates for mothers were 29.3 and 30.1. With these expected rates, the reported:expected ratio for fathers was similar to that for brothers, and the ratio for mothers was similar to that for sisters.

The expected cancer history rate in parents (under either scenario) was essentially constant with the respondent’s age; however, the reported rates decreased 22 percent from the lowest respondent age groups to the highest, as seen in table . Thus, this decrease in reported rates for parents with the age of the respondent may be partly due to recall bias. The calculations for expected rates also produce the expected average time remoteness of the cancer events (i.e., the time between the event and the respondent’s filling out the questionnaire). The expected average time remoteness increased from 19 years for the youngest age group to 29 years for the oldest age group, which may have contributed to the decrease in reported rates. The recall bias hypothesis is strengthened by the fact that the unknown cancer-type rate for parents’ cancers also significantly increased with the respondent’s age. Kerber and Slattery (3) found that the sensitivity of family history reports was lower for older respondents than for younger respondents.

Reported rates in siblings increased with the age of the respondent, though at a rate that was somewhat lower than expected. The expected average time remoteness of sibling events was fairly constant with the respondent’s age, with the overall average being about 11 years. There was no clear trend with respondent’s age in the rate of siblings’ cancers being reported to be of unknown type; this may relate to the fact that, unlike the case with parents, the time remoteness of the events was not increasing with the respondent’s age.

Reported:expected ratios of well under 1 for a given cancer could be caused by actual underreporting (i.e., not reporting events that truly did occur) or by the actual rates in this population being lower than SEER rates, or some combination of the above. A similar argument holds for ratios above 1. However, it is unlikely that the true rates in this population differ from SEER rates by more than 20–40 percent for any given type of cancer. In fact, most individual cancer types were reported at rates reasonably close to those expected and with the expected age distribution, with a few important exceptions.

Reported:expected ratios greatly above 1 for liver and bone cancer and somewhat above 1 for brain cancer were probably due to the fact that respondents mistakenly reported sites of metastasis as the primary tumor site. Thirty-one percent of siblings reported to have had liver or bone cancer had multiple reported cancers; in contrast, overall only 8 percent of siblings with reported cancer had multiple reported cancers. However, even if multiple cancers were removed from the liver and bone cancer totals, the reported:expected ratios would still be well over 1. Stomach cancer also had reported:expected ratios significantly above 1, which may be indicative of misclassification by the respondent.

Cancers with reported rates much lower than expected included lymphoma, melanoma, bladder cancer, and testicular cancer. Respondents may have underreported melanoma because they mistook it for basal-cell skin cancer, a cancer that was not supposed to be reported according to the baseline questionnaire. Testicular cancer is one of the most curable cancers, so this may be a factor in its underreportage; in addition, this cancer was likely to have occurred a long time in the past because of its young age distribution (5). There were a number of instances in which respondents specified "lymph nodes" as the cancer site. According to SEER data, almost all (>99 percent) primary cancers at this anatomic site are classified morphologically under lymphoma (12). If these were all added to the reported lymphomas, the (female-) reported:expected ratio would increase from 0.40 to 0.60. However, since many cancers spread to the lymph nodes, some respondents may have denoted a primary cancer at another site that spread to the lymph nodes as "lymph node" cancer. A large proportion of bladder cancers are low-grade and treated with periodic local excision, so family members may not report these lesions as cancers (13).

Airewele et al. (1), in a direct verification study, found that liver and bone cancer, along with stomach cancer and gynecologic cancers, tended to be reported less accurately than other cancers. Kerber and Slattery (3) showed decreased validity for reports of uterine cancer in comparison with breast, colon, and prostate cancer.

In conclusion, this study shows important differences in rates of reporting of a family history of cancer by the sex, race/ethnicity, and age of the respondent. For the most part, these differences appear to be due to relative underreporting according to the above factors, as opposed to true differences in family rates. Most individual cancer types were reported by females at rates 10–40 percent below the rates expected, although a few appeared greatly over- or underreported. These findings should be taken into consideration when performing epidemiologic or other analyses based on these or similar family history data obtained from questionnaires.


    APPENDIX
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 
Generating Expected Cancer Rates

We used age-, sex-, and calendar-year-specific Surveillance, Epidemiology, and End Results (SEER) cancer incidence rates, cancer mortality rates, and life tables to compute the probability of ever getting cancer (overall or type-specific) for a given birth year, end year (i.e., the year of the baseline questionnaire), and sex, employing the method of Feuer et al. (14). The SEER data begin in 1973 and are current (as of this writing) through 1998, and the life table data cover 1900–2000 (12, 15). We applied the 1973 rates for years prior to 1973 and the 1998 rates for years after 1998. For most cancers, we estimated that the majority of cases in siblings (>=85 percent) were diagnosed from 1973 onward; and for all cancers, only a small proportion would have been diagnosed after 1998. For cancers for which a large percentage of cases would be expected to have been diagnosed before 1973 (e.g., testicular cancer), we performed sensitivity analyses using the Connecticut cancer registry rates, which go back to 1935. The only cancer for which the expected rates would have changed appreciably was testicular cancer, and here the expected rate decreased by only 10 percent.

The final step was to compute, for each sex of respondent and sibling, the weighted average of the above probabilities of ever getting cancer over the distribution of birth year and end year in the sibling population, in order to obtain expected probabilities for the siblings. Data were not collected on the ages of the siblings, so we assumed a 0 mean distribution on the age difference between siblings and the respondent (the final results were quite robust to the exact nature of the distribution). The age of the respondent, the age difference, and the end year then specified the birth year of the sibling.


    NOTES
 
Correspondence to Dr. Paul F. Pinsky, Division of Cancer Prevention, National Cancer Institute, 6130 Executive Blvd., EPN 3064, Bethesda, MD 20892 (e-mail: pinskyp{at}mail.nih.gov). Back


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 REFERENCES
 

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