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Journal of Clinical Oncology, Vol 25, No 30 (October 20), 2007: pp. 4835-4843 © 2007 American Society of Clinical Oncology. DOI: 10.1200/JCO.2006.10.3416 Prediagnosis Smoking, Obesity, Insulin Resistance, and Second Primary Cancer Risk in Male Cancer Survivors: National Health Insurance Corporation Study
From the National Cancer Center, Goyang, Gyeonggi; National Health Insurance Corporation; and Department of Preventive Medicine and Department of Family Medicine, Seoul National University, Seoul, Korea Address reprint requests to Young Ho Yun, MD, PhD, Division of Cancer Control, National Cancer Center, 809 Madu-dong, Ilsan-gu, Goyang-si, Gyeonggi-do, 411-769 Korea; e-mail: lawyun08{at}ncc.re.kr or Bong Yul Huh, MD, PhD, National Cancer Center, 809 Madu-dong, Ilsan-gu, Goyang-si, Gyeonggi-do, 411-769 Korea
Purpose Smoking, obesity, and insulin resistance are well-known risk factors for cancer, yet few epidemiology studies evaluate their role as risk factors for a second primary cancer (SPC). Patients and Methods We identified 14,181 men with a first cancer from the National Health Insurance Corporation Study cohort. We obtained data on fasting glucose level, body mass index (BMI), and smoking history from an enrollment interview (1996). We obtained SPC incidence data for 1996 through 2002 from the Korean Central Cancer Registry. We used the standard Poisson regression model to estimate the age- and multivariate-adjusted relative risk (RR) for SPCs in relation to smoking history, BMI, and insulin resistance before diagnosis.
Results We observed 204 patients with SPC. The overall age-standardized incidence rate of SPC was 603.2 occurrences per 100,000 person-years, which was about 2.3 times higher than that of first cancer in the general male population. Multivariate regression revealed that lung (RR, 3.69; 95% CI, 1.35 to 10.09) and smoking-related (RR, 2.02; 95% CI, 1.02 to 4.03) SPCs were significantly associated with smoking. Obese patients (BMI Conclusion Prediagnosis smoking history, obesity, and insulin resistance were risk factors for several SPCs. These findings suggest that more thorough surveillance and screening for SPCs is needed for the cancer survivors with these risk factors.
Continuous advances in cancer treatment have led to a marked improvement in cure rates, and thus an increased population of long-term cancer survivors.1,2 As a result of both original and treatment-related risk factors, however, survivors are at increased risk for second primary cancers (SPCs), not only at the original site but also at other sites.3,4 Although many large population-based studies demonstrate that smoking,5,6 obesity,7-10 and insulin resistance11-13 are risk factors for first cancers, few studies evaluate the role of known risk factors in the development of SPCs in cancer survivors. Previously, we conducted a prospective cohort investigation,5,6,14 and during the 7 years of follow-up, more than 14,900 men were diagnosed with a first cancer. Drawing from that male survivor cohort, we identified the role of the baseline risk factors that existed before the first cancer diagnosis in the development of SPCs.
Study Population and Data Collection The National Health Insurance Corporation Study, which enrolled 1,216,041 (901,979 male and 314,062 female) government employees and teachers  20 years old who participated in a national health examination program begun in 1996, includes the results of biennial health examinations and a self-administered questionnaire survey regarding medical history, current health status, family history, tobacco and alcohol consumption, dietary preferences, and leisure-time physical activity. Serum glucose was measured under fasting conditions, and body mass index (BMI) was calculated as kilograms per square meters at enrollment. Data for the incident cancer occurrences were obtained from the Korea Central Cancer Registry. The details of this cohort study, including outcome measures, were reported previously.5,6,14 We restricted our analyses to men because the women generally were younger and the number of female cancer patients was too small for detailed analysis. We retrieved data on 14,944 men with a first cancer. We excluded patients who were dying or diagnosed with multiple primary cancers within the first 30 days of follow-up (n = 763). This left 14,181 patients in the study (Fig 1).
A cancer was identified as an SPC if it was diagnosed at least 1 month later than the first cancer and was of a different topology, using the four-digit International Classification of Diseases code when available. We observed patients up to December 31, 2002. During the follow-up period of 28,235.22 person-years, we identified 204 SPC occurrences (Fig 1).
Statistical Methods
To compare cancer incidence between the general population and the cancer survivors, we calculated the age-standardized incidence rate by a direct method. We used the standard Poisson regression model to estimate the relative risk (RR) for development of an SPC in relation to smoking history, obesity, and insulin resistance before the first primary tumor. For multivariate analyses, we used the following categories: smoking status (current, former, or never smoker), BMI (< 23, 23 to 24.9,
The mean age of the 14,181 patients was 50.8 years. Table 1 lists the baseline characteristics. The mean duration of follow-up was 2.0 years, during which we observed 204 occurrences of SPC. There were 5,653 deaths among the patients who did not have an SPC (Fig 1), most of which were due to cancer. Only 23 (11.3%) of the SPCs occurred at the same site as the first cancer.
Age-Standardized Incidence Rates of First Primary Cancers and SPCs Table 2 lists the number of occurrences and the age-standardized incidence rate of first primary cancers and SPCs. The overall age-standardized incidence SPC rate was 603.2 occurrences per 100,000 person-years, which was about 2.3 times higher than that of first primary cancers (259.9 occurrences per 100,000 person-years). For every site except the stomach, the age-standardized incidence rate was higher in cancer survivors than in the general population.
Among those with an unfavorable risk factor such as smoking or obesity, the overall age-standardized cancer incidence rates for SPCs were more than twice those for first primary cancers. In smokers, the age-standardized incidence rates of head and neck, colorectal, lung, hepatopancreatobiliary, genitourinary, and smoking-related cancers were higher in the survivors than in the general population. In men with a BMI 25 kg/m2, the age-standardized incidence rate of colorectal and genitourinary cancers was about 5 times higher for second than for first primary cancers. Because of the small number of SPC occurrences in cancer survivors with fasting serum glucose levels 126 mg/dL (n = 22), we could not compare the age-standardized cancer incidence rate for each site, but the rate for all cancers was 1.6 times higher for SPCs (856.6 occurrences per 100,000 person-years) than for first primary cancers (544.4 occurrences per 100,000 person-years).
Age at First Primary Cancer and Risk of SPC
Prediagnosis Smoking and SPC Age- and multivariate-adjusted analyses showed a significant relationship between smoking status before the first cancer diagnosis and SPC incidence for lung and smoking-related cancers (Table 4). Second primary lung cancers were not found in survivors who had never smoked. Furthermore, second primary lung cancers were more likely to develop in current smokers than in former smokers (RR, 3.69; 95% CI, 1.35 to 10.09). As in smoking-related cancer incidence, we observed positive linear trends with smoking status in age-adjusted analysis (P < .01). The effect persisted in multivariate analysis, with current smokers having a higher RR for smoking-related SPCs (RR, 2.02; 95% CI, 1.02 to 4.03) than those who had never smoked.
Prediagnosis BMI and SPC Compared with the reference category (BMI < 23 kg/m2), survivors with a prediagnosis BMI 25 kg/m2 had a significantly elevated RR for colorectal SPC (RR, 3.45; 95% CI, 1.50 to 7.93) with dose-dependent relationships in multivariate analysis (Table 5). We also found that patients with BMI 25 kg/m2 had a higher RR for genitourinary SPC (RR, 3.61; 95% CI, 1.36 to 9.54) than those with BMI less than 25 kg/m2 (Table 5).
When we stratified the patients based on smoking history, the survivors with prediagnosis obesity had a significant high risk of second primary colorectal cancer in both current smokers (RR, 3.17; 95% CI, 1.06 to 9.51) and former/nonsmokers (RR, 3.90; 95% CI, 1.07 to 14.21).
Prediagnosis Fasting Serum Glucose Level and SPC
When we repeated Poisson regression analysis with different time frames of SPC, such as 3 or 6 months, the impact of prediagnosis smoking history and obesity on SPC risk was similar to those with a 1-month time frame. Only the association between insulin resistance and SPCs was attenuated and not statistically significant in different time frames (data not shown).
In this large population-based cohort study, we found that among male cancer survivors, prediagnosis risk factors (a history of smoking, obesity, and elevated fasting serum glucose levels) were independent risk factors for several SPCs after adjusting for confounders such as physical activity, alcohol consumption, and age at first cancer diagnosis. The overall age-standardized incidence rate was 2.3 times higher for an SPC than for a first cancer in the general male population. When we compared the age-standardized cancer incidence rates for male cancer survivors and the general male population, we found similar results for most cancer sites except the stomach. We also found that in smokers, the age-standardized incidence rate of smoking-related cancers was higher in the survivors than in the general population. A previous study showed that the risk of a smoking-related SPC after laryngeal cancer was elevated; although laryngeal cancer is usually smoking-related, data on smoking were not given.22 Little is known about the incidence of secondary nonsmoking-related cancers in smokers. In this study, we found that in smokers, the age-standardized incidence rate was about 5 times higher for second than for first primary colorectal cancers. The age-standardized incidence rate was also higher for second than for first primary cancers in several sites among those with a different unfavorable risk factor, such as obesity or insulin resistance. We also showed positive linear trends in SPC incidence with increasing age at first cancer diagnosis for head and neck, stomach, lung, and smoking-related cancers, and all cancer combined. Although advancing age is known to be associated with an increased risk of a first cancer in the general population,23 the relationship between age at first cancer diagnosis and the risk of an SPC is controversial.24-26 Our results suggest that physicians should monitor not only for recurrence of a first cancer, but also for new primary cancers, especially in the elderly. Our finding that prediagnosis smoking was an independent risk factor for secondary lung and other smoking-related cancers is consistent with other studies suggesting that smoking increases the risk of SPCs, especially lung cancers.27,28 Current smokers who have a nonrespiratory cancer are also at increased risk for SPCs. In Japan, smoking significantly increases the risk for SPC in esophageal25 and gastric cancer29 patients. In aerodigestive cancers, a history of smoking, particularly heavy smoking, is a universally recognized risk factor for SPCs,30-32 and prediagnosis smoking is an independent poor prognostic factor in cancer patients.14 Together with previous findings, our results suggest that groups with a high cancer risk need to be educated continually not to smoke—not only to prevent a first cancer, but also to prevent a second cancer. We also found significant dose-dependent relationships between prediagnosis BMI and the risk of colorectal and genitourinary SPCs, as has been reported for first cancers.7-10 Although few prospective studies have investigated the association between SPCs and obesity, some studies have shown obesity to be a risk factor for recurrent colorectal, prostate, or breast cancer.33-35 Those studies, however, did not consider the SPCs in discordant sites. Only one case-control study showed obesity to be a risk factor for colorectal cancer in breast cancer patients.36 In our study, the proportion of concordant SPCs was 11.3%, confirming that obesity is a risk factor for several SPCs at discordant as well as concordant sites. Smoking and other confounding risk factors for SPC may distort the link between BMI and SPC risk. Smoking is associated inversely with body weight,37,38 and that must be considered when examining the effect of BMI on SPC risk. In our study, the associations between obesity and the risk of second primary colorectal cancer were statistically significant in both current smokers and former/nonsmokers. The mechanisms underlying the association between obesity and cancer are still uncertain. Individuals in the obese population are known to have increased blood levels of sex steroids, insulin, insulinlike growth factor (IGF), leptin, and adipocytokine, and these could influence cancer development or growth.10,39 Recent studies had revealed that weight gain after the diagnosis of some cancers is a common occurrence, and the prevalence of elevated BMIs is high.39,40 Because excess weight could increase the risk of several SPCs, clinician involvement to reduce the impact of excess weight in cancer patients will continue to be important.
Glucose intolerance is another risk factor for cancer, both overall and for particular sites,11-13 but few prospective studies have identified its relationship to SPC risk. One study showed that colon cancer patients with diabetes experience a significantly elevated recurrence rate.41 Another showed that an elevated IGF level is a risk factor for second primary head and neck cancers.42 We found no studies, however, that considered the effects of other important risk factors, such as BMI, exercise, and alcohol consumption. In the National Health Insurance Corporation Study, we found that the increased SPC risk associated with high serum glucose was unchanged when adjusted for BMI and other known risk factors. To our knowledge, this is the first study to demonstrate positive linear trends in SPC incidence with increasing fasting serum glucose levels for hepatopancreatobiliary and smoking-related cancers. The multicancer effect is consistent with postulated mechanisms of systemic consequences of hyperinsulinemia.11-13,43 Given that IGF-1 and insulin receptors are overexpressed in cancer cells, high insulin levels could lead to a selective growth advantage.11-13,43 IGF-1 has been shown to be an important regulator of angiogenesis, and it could increase vascular endothelial growth factor production in cancer cells.44,45 In addition, insulin resistance is associated with the elevation in proinflammatory markers such as C-reactive protein, interleukin-6, and tumor necrosis factor The strengths of this study include its prospective, population-based design, reliable assessment of cancer incidence, and detailed assessment of the health risk factors that preceded the first cancer diagnosis. Many other population-based cohort studies, in contrast, rely on national linkage registries that do not have this type of information, thereby limiting the ability to adjust for potential confounders.3,51 In addition, most studies that identify SPC risk factors collect health behavior information after the diagnosis,30,38 and those data may not accurately represent long-term exposure because body weight and behaviors such as smoking, alcohol consumption, and exercise are influenced by the experience of cancer.52,53 Some studies do collect information about health behaviors that preceded the cancer diagnosis at the time of patient enrollment,25,29 but those are subject to recall bias. Another advantage of our study is that height and weight measurements were made by trained personnel. This is preferable to self-reported data (which have been used frequently in large-scale cohort studies) because heavier individuals tend to under-report their weight.54 Our study has several limitations. First, our sample might not represent cancer patients in the general population because cancer registration is not yet complete throughout Korea, although it includes approximately 90% of patients,55 and the patients held stable, secure jobs. This population, however, was relatively easy to observe and offered a relatively reliable source of information. Second, because we did not include information about first cancer treatment, we could not consider its effect. The carcinogenic effects of cancer-related treatment, however, are usually delayed,3 and the follow-up period of our study was relatively short (mean, 2.0 years). Third, our adjustment for the small number of SPC occurrences by combining some risk factor categories into a single stratum could have masked real associations between prediagnosis environmental factors and SPC risk. Despite this technique, however, we found statistically meaningful associations between smoking history and lung cancer and between obesity and genitourinary cancer. Fourth, although we excluded individuals whose follow-up was less than 1 month (the same time frame used in other SPC studies3,56) to avoid uncertainty as to which was the first cancer, there were some chances of an SPC misclassification bias. However, when we compared analyses with different time frames, such as 3 or 6 months, the results were similar to those with a 1-month time frame. Our study showed that male cancer survivors had a higher primary cancer incidence than the general male population. We also showed that prediagnosis smoking, obesity, and elevated fasting serum glucose levels, which are well-known risk factors for cancer in the general population, seemed to increase the risk of several SPCs. Our findings suggest that more thorough surveillance and screening for SPCs is needed for cancer survivors, especially those patients with these risk factors. Additional study is needed to examine whether discontinuing smoking and reducing weight or insulin resistance might decrease the incidence of SPCs.
The author(s) indicated no potential conflicts of interest.
Conception and design: Sang Min Park, Min Kyung Lim, Kyu Won Jung, Soon Ae Shin, Keun-Young Yoo, Young Ho Yun, Bong Yul Huh Administrative support: Soon Ae Shin, Bong Yul Huh Provision of study materials or patients: Soon Ae Shin, Bong Yul Huh Collection and assembly of data: Sang Min Park, Min Kyung Lim, Kyu Won Jung, Soon Ae Shin, Keun-Young Yoo, Young Ho Yun, Bong Yul Huh Data analysis and interpretation: Sang Min Park, Min Kyung Lim, Kyu Won Jung, Keun-Young Yoo, Young Ho Yun Manuscript writing: Sang Min Park, Young Ho Yun, Bong Yul Huh Final approval of manuscript: Sang Min Park, Min Kyung Lim, Kyu Won Jung, Soon Ae Shin, Keun-Young Yoo, Young Ho Yun, Bong Yul Huh
We thank the staff of the Korean National Health Insurance Corporation for their cooperation. We also thank Hai-Rim Shin, Byung Ho Nam, and Si Won Huh for their excellent comments and assistance.
Supported by National Cancer Center Grant No. 04101502 and National Cancer Center Grant No. 07104221. Y.H.Y. and B.Y.H. contributed equally to this work. Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.
1. National Cancer Institute: Surveillance, epidemiology, and end results (SEER). http://www.seer.cancer.gov 2. National Cancer Institute: Living beyond cancer: Finding a new balance: President's Cancer Panel 2003-2004 annual report. Bethesda, MD, President's Cancer Panel, National Cancer Institute, National Institutes of Health, US Dept. of Health and Human Services, 2004 3. Dong C, Hemminki K: Second primary neoplasms in 633,964 cancer patients in Sweden, 1958-1996. Int J Cancer 93:155-161, 2001[CrossRef][Medline] 4. Dikshit RP, Boffetta P, Bouchardy C, et al: Risk factors for the development of second primary tumors among men after laryngeal and hypopharyngeal carcinoma. Cancer 103:2326-2333, 2005[CrossRef][Medline] 5. Yun YH, Jung KW, Bae JM, et al: Cigarette smoking and cancer incidence risk in adult men: National Health Insurance Corporation Study. Cancer Detect Prev 29:15-24, 2005[CrossRef][Medline] 6. Yun YH, Lim MK, Jung KW, et al: Relative and absolute risks of cigarette smoking on major histologic types of lung cancer in Korean Men. Cancer Epidemiol Biomarkers Prev 14:2125-2130, 2005 7. Samanic C, Gridley G, Chow WH, et al: Obesity and cancer risk among white and black United States veterans. Cancer Causes Control 15:35-43, 2004[CrossRef][Medline] 8. Kuriyama S, Tsubono Y, Hozawa A, et al: Obesity and risk of cancer in Japan. Int J Cancer 113:148-157, 2005[CrossRef][Medline] 9. International Agency for Research on Cancer: Handbooks of Cancer Prevention. Vol 6: Weight Control and Physical Activity. Lyons, France, IARC, 2002 10. Oh SW, Yoon YS, Shin SA: Effects of excess weight on cancer incidences depending on cancer sites and histologic findings among men: Korea national health insurance corporation study. J Clin Oncol 23:4742-4754, 2005 11. Jee SH, Ohrr H, Sull JW, et al: Fasting serum glucose level and cancer risk in Korean men and women. JAMA 293:194-202, 2005 12. Dawson SI: Long-term risk of malignant neoplasm associated with gestational glucose intolerance. Cancer 100:149-155, 2004[CrossRef][Medline] 13. Hsing AW, Gao YT, Chua S Jr, et al: Insulin resistance and prostate cancer risk. J Natl Cancer Inst 95:67-71, 2003 14. Park SM, Lim MK, Shin SA, et al: Impact of pre-diagnosis smoking, alcohol, obesity, and insulin resistance on survival in male cancer patients: National Health Insurance Corporation Study. J Clin Oncol 24:5017-5024, 2006 15. Kahn HA: The Dorn study of smoking and mortality among US veterans: Report on eight and one-half years of observation. In: W. Haenszel (ed): Epidemiological Approaches to the Study of Cancer and Other Chronic Diseases, Vol 19. US Department of Health, Education, and Welfare, Rockville, MD. Natl Cancer Inst Monogr 1-125, 1966 16. Doll R, Peto R, Wheatley K, et al: Mortality in relation to smoking: 40 years' observations on male British doctors. BMJ 309:901-911, 1994 17. Pasanen PA, Eskelinen M, Partanen K, et al: Multivariate analysis of six serum tumor markers (CEA, CA 50, CA 242, TPA, TPS, TATI) and conventional laboratory tests in the diagnosis of hepatopancreatobiliary malignancy. Anticancer Res 15:2731-2737, 1995[Medline] 18. Sheth H, Javed SS, Hilson AJ, et al: Radioisotope bone scans in the preoperative staging of hepatopancreatobiliary cancer. Br J Surg 92:203-207, 2005[CrossRef][Medline] 19. Sommer F, Klotz T, Schmitz-Drager BJ: Lifestyle issues and genitourinary tumours. World J Urol 21:402-413, 2004[CrossRef][Medline] 20. WHO Western Pacific Region, International Association for the Study of Obesity, and International Obesity Taskforce: The Asian-Pacific Perspective: Redefining Obesity and Its Treatment. Geneva, Switzerland, WHO Western Pacific Region, 2000 21. World Health Organization: Definition, Diagnosis and Classification of Diabetes Mellitus and its Complications: Report of a WHO Consultation: Part 1: Diagnosis and Classification of Diabetes Mellitus. Geneva, Switzerland: World Health Organization; 1999 22. Gao X, Fisher SG, Mohideen N, Emami B: Second primary cancers in patients with laryngeal cancer: A population-based study. Int J Radiat Oncol Biol Phys 56:427-435, 2003[CrossRef][Medline] 23. Shin HR, Ahn YO, Bae JM, et al: Cancer incidence in Korea. Cancer Res Treat 34:405-408, 2002 24. Lin K, Patel SG, Chu PY, et al: Second primary malignancy of the aerodigestive tract in patients treated for cancer of the oral cavity and larynx. Head Neck 27:1042-1048, 2005[CrossRef][Medline] 25. Matsubara T, Yamada K, Nakagawa A: Risk of second primary malignancy after esophagectomy for squamous cell carcinoma of the thoracic esophagus. J Clin Oncol 21:4336-4341, 2003 26. Fowble B, Hanlon A, Freedman G, et al: Second cancers after conservative surgery and radiation for stages I-II breast cancer: Identifying a subset of women at increased risk. Int J Radiat Oncol Biol Phys 51:679-690, 2001[CrossRef][Medline] 27. Obedian E, Fischer DB, Haffty BG: Second malignancies after treatment of early-stage breast cancer: Lumpectomy and RT versus mastectomy. J Clin Oncol 18:2406-2412, 2000 28. van Leeuwen FE, Klokman WJ, Stovall M, et al: Roles of radiotherapy and smoking in lung cancer following Hodgkin's disease. J Natl Cancer Inst 87:1530-1537, 1995 29. Kinoshita Y, Tsukuma H, Ajiki W, et al: The risk for second primaries in gastric cancer patients: Adjuvant therapy and habitual smoking and drinking. J Epidemiol 10:300-304, 2000[Medline] 30. Do KA, Johnson MM, Doherty DA, et al: Second primary tumors in patients with upper aerodigestive tract cancers: Joint effects of smoking and alcohol (United States). Cancer Causes Control 14:131-138, 2003[CrossRef][Medline] 31. Wynder EL, Mushinski MH, Spivak JC: Tobacco and alcohol consumption in relation to the development of multiple primary cancers. Cancer 40:1872-1878, 1977[CrossRef][Medline] 32. Day GL, Blot WJ, Shore RE, et al: Second cancers following oral and pharyngeal cancers: Role of tobacco and alcohol. J Natl Cancer Inst 86:131-137, 1994 33. Goodwin PJ, Ennis M, Pritchard KI, et al: Fasting insulin and outcome in early-stage breast cancer: Results of a prospective cohort study. J Clin Oncol 20:42-51, 2002 34. Meyerhardt JA, Catalano PJ, Haller DG, et al: Influence of body mass index on outcomes and treatment-related toxicity in patients with colon carcinoma. Cancer 98:484-495, 2003[CrossRef][Medline] 35. Freedland SJ, Aronson WJ, Kane CJ, et al: Impact of obesity on biochemical control after radical prostatectomy for clinically localized prostate cancer: A report by the Shared Equal Access Regional Cancer Hospital database study group. J Clin Oncol 22:446-453, 2004 36. Kmet LM, Cook LS, Weiss NS, et al: Risk factors for colorectal cancer following breast cancer. Breast Cancer Res Treat 79:143-147, 2003[CrossRef][Medline] 37. Hafron J, Mitra N, Dalbagni G, et al: Does body mass index affect survival of patients undergoing radical or partial cystectomy for bladder cancer? J Urol 173:1513-1517, 2005[CrossRef][Medline] 38. Molarius A, Seidell JC, Kuulasmaa K, et al: Smoking and relative body weight: An international perspective from the WHO MONICA Project. J Epidemiol Community Health 51:252-260, 1997 39. Chlebowski RT, Aiello E, McTiernan A: Weight loss in breast cancer patient management. J Clin Oncol 20:1128-1143, 2002 40. Tayek JA, Heber D, Byerley LO, et al: Nutritional and metabolic effects of gonadotropin-releasing hormone agonist treatment for prostate cancer. Metabolism 39:1314-1319, 1990[CrossRef][Medline] 41. Meyerhardt JA, Catalano PJ, Haller DG, et al: Impact of diabetes mellitus on outcomes in patients with colon cancer. J Clin Oncol 21:433-440, 2003 42. Wu X, Zhao H, Do KA, et al: Serum levels of insulin growth factor (IGF-I) and IGF-binding protein predict risk of second primary tumors in patients with head and neck cancer. Clin Cancer Res 10:3988-3995, 2004 43. Gapstur SM, Gann PH, Lowe W, et al: Abnormal glucose metabolism and pancreatic cancer mortality. JAMA 283:2552-2558, 2000 44. O'Byrne KJ, Dalgleish AG, Browning MJ, et al: The relationship between angiogenesis and the immune response in carcinogenesis and the progression of malignant disease. Eur J Cancer 36:151-169, 2000[CrossRef][Medline] 45. Cowey S, Hardy RW: The metabolic syndrome: A high-risk state for cancer? Am J Pathol 169:1505-1522, 2006 46. Festa A, Hanley AJ, Tracy RP, et al: Inflammation in the prediabetic state is related to increased insulin resistance rather than decreased insulin secretion. Circulation 108:1822-1830, 2003 47. Lee WY, Park JS, Noh SY, et al: C-reactive protein concentrations are related to insulin resistance and metabolic syndrome as defined by the ATP III report. Int J Cardiol 97:101-106, 2004[CrossRef][Medline] 48. Helzlsouer KJ, Erlinger TP, Platz EA: C-reactive protein levels and subsequent cancer outcomes: Results from a prospective cohort study. Eur J Cancer 42:704-707, 2006[CrossRef][Medline] 49. Gunter MJ, Stolzenberg-Solomon R, Cross AJ, et al: A prospective study of serum C-reactive protein and colorectal cancer risk in men. Cancer Res 66:2483-2487, 2006 50. Siemes C, Visser LE, Coebergh JW, et al: C-reactive protein levels, variation in the C-reactive protein gene, and cancer risk: The Rotterdam Study. J Clin Oncol 24:5216-5222, 2006 51. Travis LB, Fossa SD, Schonfeld SJ, et al: Second cancers among 40,576 testicular cancer patients: Focus on long-term survivors. J Natl Cancer Inst 97:1354-1365, 2005 52. Satia JA, Campbell MK, Galanko JA, et al: Longitudinal changes in lifestyle behaviors and health status in colon cancer survivors. Cancer Epidemiol Biomarkers Prev 13:1022-1031, 2004 53. Patterson RE, Neuhouser ML, Hedderson MM, et al: Changes in diet, physical activity, and supplement use among adults diagnosed with cancer. J Am Diet Assoc 103:323-328, 2003[Medline] 54. Hill A, Roberts J: Body mass index: A comparison between self-reported and measured height and weight. J Public Health Med 20:206-210, 1998 55. International Agency for Research on Cancer: Cancer Incidence in Five Continents. Lyons, France, IARC, 2002 56. Levi F, Randimbison L, Te VC, et al: Second primary cancers in laryngeal cancer patients. Eur J Cancer 39:265-267, 2003[CrossRef][Medline] Submitted December 10, 2006; accepted June 28, 2007.
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Copyright © 2007 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
,
