Skip to main content
SpringerLink
Log in

Cardiopulmonary fitness, adiponectin, chemerin associated fasting insulin level in colorectal cancer patients

  • Original Article
  • Published:
Supportive Care in Cancer Aims and scope Submit manuscript

Abstract

Purpose

Since circulating level of insulin is associated with colorectal cancer prognosis, it is important to identify factors contributing to fasting insulin level in colorectal cancer patients. The purpose of the current study is to investigate the association of physical fitness, adiponectin, and chemerin levels with circulating level of insulin in colorectal cancer patients.

Methods

A total of 123 stage II-III colorectal cancer patients who completed standard cancer treatment were recruited. Anthropometric characteristics, fitness measurements, fasting insulin level, homeostasis model assessment of insulin resistance, lipid profiles, and adiponectin and chemerin levels were analyzed.

Result

Cardiopulmonary fitness level inversely associated with fasting insulin levels (the least fit (1st tertile): 8.11 ± 0.64, moderately fit (2nd tertile): 6.02 ± 0.63, and highly fit (3rd tertile): 5.58 ± 0.66 μU/ml, unfit vs. moderately fit, p < 0.01; unfit vs. highly fit, p < 0.05) after adjustment for gender, age, stage, and BMI. In addition, fasting adiponectin and chemerin levels were associated with fasting insulin levels after adjustment for gender, age, stage, and BMI. In our combined analyses, participants with high adiponectin and low chemerin levels showed significantly lower fasting insulin levels (4.92 ± 0.75 vs. 8.07 ± 0.80 μU/ml, p < 0.01) compared with participants with low adiponectin and high chemerin levels. Multiple linear regression analysis confirmed that cardiopulmonary fitness and adiponectin levels (β = −0.299, p = 0.002; β = −0.201, p = 0.033) were independently associated with fasting insulin level.

Conclusion

Our results suggest that physical fitness and adiponectin and chemerin levels may contribute to circulating levels of insulin. These results suggest that exercise may influence the prognosis of colorectal cancer patients by influencing physical fitness level, circulating levels of adiponectin and chemerin.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Giovannucci E (2001) Insulin, insulin-like growth factors and colon cancer: a review of the evidence. J Nutr 131:3109S–3120S

    CAS  PubMed  Google Scholar 

  2. Gonullu G, Kahraman H, Bedir A, Bektas A, Yucel I (2010) Association between adiponectin, resistin, insulin resistance, and colorectal tumors. Int J Color Dis 25:205–212

    Article  Google Scholar 

  3. Goodwin PJ, Ennis M, Pritchard KI, Trudeau ME, Koo J, Madarnas Y, Hartwick W, Hoffman B, Hood N (2002) Fasting insulin and outcome in early-stage breast cancer: results of a prospective cohort study. J Clin Oncol 20:42–51

    Article  CAS  PubMed  Google Scholar 

  4. Pasanisi P, Berrino F, De Petris M, Venturelli E, Mastroianni A, Panico S (2006) Metabolic syndrome as a prognostic factor for breast cancer recurrences. Int J Cancer 119:236–238

    Article  CAS  PubMed  Google Scholar 

  5. Wolpin BM, Meyerhardt JA, Chan AT, Ng K, Chan JA, Wu K, Pollak MN, Giovannucci EL, Fuchs CS (2009) Insulin, the insulin-like growth factor axis, and mortality in patients with nonmetastatic colorectal cancer. J Clin Oncol 27:176–185

    Article  PubMed  PubMed Central  Google Scholar 

  6. Hivert MF, Sullivan LM, Fox CS, Nathan DM, D’Agostino RB Sr, Wilson PW, Meigs JB (2008) Associations of adiponectin, resistin, and tumor necrosis factor-alpha with insulin resistance. J Clin Endocrinol Metab 93:3165–3172

  7. Lee MK, Chu SH, Lee DC, An KY, Park JH, Kim DI, Kim J, Hong S, Im JA, Lee JW, JY J (2013) The association between chemerin and homeostasis assessment of insulin resistance at baseline and after weight reduction via lifestyle modifications in young obese adults. Clin Chim Acta 421:109–115

    Article  CAS  PubMed  Google Scholar 

  8. Rabe K, Lehrke M, Parhofer KG, UC B (2008) Adipokines and insulin resistance. Mol Med 14:741–751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Scheid MP, Sweeney G (2014) The role of adiponectin signaling in metabolic syndrome and cancer. Rev Endocr Metab Disord 15:157–167

    Article  CAS  PubMed  Google Scholar 

  10. Chu SH, Lee MK, Ahn KY, Im JA, Park MS, Lee DC, Jeon JY, Lee JW (2012) Chemerin and adiponectin contribute reciprocally to metabolic syndrome. PLoS One 7:e34710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Yadav A, Kataria MA, Saini V, Yadav A (2013) Role of leptin and adiponectin in insulin resistance. Clin Chim Acta 417:80–84

    Article  CAS  PubMed  Google Scholar 

  12. Barb D, Williams CJ, Neuwirth AK, CS M (2007) Adiponectin in relation to malignancies: a review of existing bbasic research and clinical evidence. Am J Clin Nutr 86:s858–s866

    PubMed  Google Scholar 

  13. Parekh N, Okada T, Lu-Yao GL (2009) Obesity, insulin resistance, and cancer prognosis: implications for practice for providing care among cancer survivors. J Am Diet Assoc 109:1346–1353

    Article  PubMed  PubMed Central  Google Scholar 

  14. Kutzleb C, Busmann A, Wendland M, Maronde E (2005) Discovery of novel regulatory peptides by reverse pharmacology: spotlight on chemerin and the RF-amide peptides metastin and QRFP. Curr Protein Pept Sci 6:265–278

    Article  CAS  PubMed  Google Scholar 

  15. Bozaoglu K, Bolton K, McMillan J, Zimmet P, Jowett J, Collier G, Walder K, Segal D (2007) Chemerin is a novel adipokine associated with obesity and metabolic syndrome. Endocrinology 148:4687–4694

    Article  CAS  PubMed  Google Scholar 

  16. Bozaoglu K, Segal D, Shields KA, Cummings N, Curran JE, Comuzzie AG, Mahaney MC, Rainwater DL, VandeBerg JL, MacCluer JW, Collier G, Blangero J, Walder K, Jowett JB (2009) Chemerin is associated with metabolic syndrome phenotypes in a Mexican-American population. J Clin Endocrinol Metab 94:3085–3088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Yilmaz Y, Yonal O, Kurt R, Alahdab YO, Eren F, Ozdogan O, Celikel CA, Imeryuz N, Kalayci C, Avsar E (2011) Serum levels of omentin, chemerin and adipsin in patients with biopsy-proven nonalcoholic fatty liver disease. Scand J Gastroenterol 46:91–97

    Article  CAS  PubMed  Google Scholar 

  18. Chen LW, Wang J (2012) Detection of serum chemerin levels and its clinical significance in patients with gastric cancer Laboratory Medicine and Clinic 8: 022

  19. Zhang J, Jin HC, Zhu AK, Ying RC, Wei W, FJ Z (2014) Prognostic significance of plasma chemerin levels in patients with gastric cancer. Peptides 61:7–11

    Article  CAS  PubMed  Google Scholar 

  20. Pachynski RK, Zabel BA, Kohrt HE, Tejeda NM, Monnier J, Swanson CD, Holzer AK, Gentles AJ, Sperinde GV, Edalati A, Hadeiba HA, Alizadeh AA, Butcher EC (2012) The chemoattractant chemerin suppresses melanoma by recruiting natural killer cell antitumor defenses. J Exp Med 209:1427–1435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Rama D, Esendagli G, Guc D (2011) Expression of chemokine-like receptor 1 (CMKLR1) on J744A.1 macrophages co-cultured with fibroblast and/or tumor cells: modeling the influence of microenvironment. Cell Immunol 271:134–140

    Article  CAS  PubMed  Google Scholar 

  22. Wittamer V, Bondue B, Guillabert A, Vassart G, Parmentier M, Communi D (2005) Neutrophil-mediated maturation of chemerin: a link between innate and adaptive immunity. J Immunol 175:487–493

    Article  CAS  PubMed  Google Scholar 

  23. Je Y, Jeon JY, Giovannucci EL, JA M (2013) Association between physical activity and mortality in colorectal cancer: a meta-analysis of prospective cohort studies. Int J Cancer 133:1905–1913

    Article  CAS  PubMed  Google Scholar 

  24. Kuiper JG, Phipps AI, Neuhouser ML, Chlebowski RT, Thomson CA, Irwin ML, Lane DS, Wactawski-Wende J, Hou L, Jackson RD, Kampman E, Newcomb PA (2012) Recreational physical activity, body mass index, and survival in women with colorectal cancer cancer causes control 23: 1939-1948

  25. Meyerhardt JA, Giovannucci EL, Holmes MD, Chan AT, Chan JA, Colditz GA, Fuchs CS (2006) Physical activity and survival after colorectal cancer diagnosis. J Clin Oncol 24:3527–3534

    Article  PubMed  Google Scholar 

  26. Meyerhardt JA, Heseltine D, Niedzwiecki D, Hollis D, Saltz LB, Mayer RJ, Thomas J, Nelson H, Whittom R, Hantel A, Schilsky RL, Fuchs CS (2006) Impact of physical activity on cancer recurrence and survival in patients with stage III colon cancer: findings from CALGB 89803. J Clin Oncol 24:3535–3541

    Article  PubMed  Google Scholar 

  27. Irwin ML, Mayer-Davis EJ, Addy CL, Pate RR, Durstine JL, Stolarczyk LM, BE A (2000) Moderate-intensity physical activity and fasting insulin levels in women: the Cross-Cultural Activity Participation Study. Diabetes Care 23:449–454

    Article  CAS  PubMed  Google Scholar 

  28. Irwin ML, McTiernan A, Bernstein L, Gilliland FD, Baumgartner R, Baumgartner K, Ballard-Barbash R (2005) Relationship of obesity and physical activity with C-peptide, leptin, and insulin-like growth factors in breast cancer survivors. Cancer Epidemiol Biomark Prev 14:2881–2888

    Article  CAS  Google Scholar 

  29. Lee DH, Kim JY, Lee MK, Lee C, Min JH, Jeong DH, Lee JW, Chu SH, Meyerhardt JA, Ligibel J, Jones LW, Kim NK, Jeon JY (2013) Effects of a 12-week home-based exercise program on the level of physical activity, insulin, and cytokines in colorectal cancer survivors: a pilot study. Support Care Cancer 21:2537–2545

    Article  PubMed  Google Scholar 

  30. Kim M, Kim H (2013) Accuracy of segmental multi-frequency bioelectrical impedance analysis for assessing whole-body and appendicular fat mass and lean soft tissue mass in frail women aged 75 years and older. Eur J Clin Nutr 67:395–400

    Article  CAS  PubMed  Google Scholar 

  31. Kushner RF, Kunigk A, Alspaugh M, Andronis PT, Leitch CA, DA S (1990) Validation of bioelectrical-impedance analysis as a measurement of change in body composition in obesity Am. J Clin Nutr 52:219–223

    CAS  Google Scholar 

  32. WHO (2008) Waist circumference and waist-hip ratio. In: Editor (ed)^(eds) Book waist circumference and waist-hip ratio. World Health Organization, City.

  33. Lee DC, Koh MY, Kim YS, Gang HJ (2006) Correlation between cardiorespiratory fitness measured by step test and Hba1C, blood pressure and blood lipids in type II diabetic patients. Kor J Sport Sci 17:28–36

    Google Scholar 

  34. R RE, J CJ (1999) Development and validation of a functional fitness test for community-residing older adults. J Aging Phys Act 7:129–161

    Google Scholar 

  35. B JA (1987) Assessment of physical fitness of female physical therapy students. J Orthop Sports Phys Ther 8:525–532

    Article  Google Scholar 

  36. Mann S, Beedie C, Balducci S, Zanuso S, Allgrove J, Bertiato F, Jimenez A (2014) Changes in insulin sensitivity in response to different modalities of exercise: a review of the evidence. Diabetes Metab Res Rev 30:257–268

    Article  CAS  PubMed  Google Scholar 

  37. Li S, Shin HJ, Ding EL, van Dam RM (2009) Adiponectin levels and risk of type 2 diabetes: a systematic review and meta-analysis. Jama 302:179–188

    Article  CAS  PubMed  Google Scholar 

  38. Allen DB, Nemeth BA, Clark RR, Peterson SE, Eickhoff J, AL C (2007) Fitness is a stronger predictor of fasting insulin levels than fatness in overweight male middle-school children. J Pediatr 150:383–387

    Article  CAS  PubMed  Google Scholar 

  39. Brufani C, Grossi A, Fintini D, Fiori R, Ubertini G, Colabianchi D, Ciampalini P, Tozzi A, Barbetti F, Cappa M (2008) Cardiovascular fitness, insulin resistance and metabolic syndrome in severely obese prepubertal Italian children. Horm Res 70:349–356

    Article  CAS  PubMed  Google Scholar 

  40. Imperatore G, Cheng YJ, Williams DE, Fulton J, Gregg EW (2006) Physical activity, cardiovascular fitness, and insulin sensitivity among U.S. adolescents: the National Health and Nutrition Examination Survey, 1999–2002. Diabetes Care 29:1567–1572

    Article  PubMed  Google Scholar 

  41. Nyholm B, Mengel A, Nielsen S, Skjaerbaek C, Moller N, Alberti KG, Schmitz O (1996) Insulin resistance in relatives of NIDDM patients: the role of physical fitness and muscle metabolism. Diabetologia 39:813–822

    Article  CAS  PubMed  Google Scholar 

  42. Kim S, Kim JY, Lee DC, Lee HS, Lee JW, Jeon JY (2014) Distribution of abdominal obesity and fitness level in overweight and obese Korean adults. Int J Endocrinol 2014:854392

    PubMed  PubMed Central  Google Scholar 

  43. Kim ES, Im JA, Kim KC, Park JH, Suh SH, Kang ES, Kim SH, Jekal Y, Lee CW, Yoon YJ, Lee HC, JY J (2007) Improved insulin sensitivity and adiponectin level after exercise training in obese Korean youth. Obesity 15:3023–3030

    Article  CAS  PubMed  Google Scholar 

  44. Lee JY, Lee HS, Lee DC, Chu SH, Jeon JY, Kim NK, Lee JW (2014) Visceral fat accumulation is associated with colorectal cancer in postmenopausal women. PloS one 9:e110587

    Article  PubMed  PubMed Central  Google Scholar 

  45. Shin HY, Lee DC, Chu SH, Jeon JY, Lee MK, Im JA, JW L (2012) Chemerin levels are positively correlated with abdominal visceral fat accumulation. Clin Endocrinol (Oxf) 77:47–50

    Article  CAS  Google Scholar 

  46. Lee J, Jeon JY, Meyerhardt JA (2015) Diet and lifestyle in survivors of colorectal cancer. Hematol Oncol Clin North Am 29:1–27

    Article  PubMed  PubMed Central  Google Scholar 

  47. Kim SH, Lee SH, Ahn KY, Lee DH, Suh YJ, Cho SG, Choi YJ, Lee DH, Lee SY, Hong SB, Kim YS, Jeon JY, Nam M (2014) Effect of lifestyle modification on serum chemerin concentration and its association with insulin sensitivity in overweight and obese adults with type 2 diabetes. Clin Endocrinol 80:825–833

    Article  CAS  Google Scholar 

  48. Barzilay JI, Cotsonis GA, Walston J, Schwartz AV, Satterfield S, Miljkovic I, Harris TB, Health ABCS (2009) Insulin resistance is associated with decreased quadriceps muscle strength in nondiabetic adults aged >or = 70 years. Diabetes Care 32:736–738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Benson AC, Torode ME, MA S (2006) Muscular strength and cardiorespiratory fitness is associated with higher insulin sensitivity in children and adolescents. Int J Pediatr Obes 1:222–231

    Article  PubMed  Google Scholar 

  50. Brooks N, Layne JE, Gordon PL, Roubenoff R, Nelson ME, Castaneda-Sceppa C (2007) Strength training improves muscle quality and insulin sensitivity in Hispanic older adults with type 2 diabetes. Int J Med Sci 4:19–27

    Article  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Research Foundation of Korea (NRF-2010-0009048) and the National R&D Program for Cancer Control, Ministry of Health and Welfare, Republic of Korea (1120230).

Author contributions

Conception and design were done by Jeon JY, Kim NK, Chu SH, and Lee JW. Provision of study materials or patients was done by Lee MK, Jeon JY, Kim NK. Collection and assembly of data were administered by Ahn KY, Lee MK, Lee JW, Kim DI, Jihye Park, Hyuna Park, Minsuk Oh, and Junga Lee. Manuscript writing was performed by Ahn KY, Lee MK, Meyerhardt JA, Junga Lee, Hyuk In Yang, Jungbae An, and Jeon JY. All authors approved the final manuscript.

Author information

Authors and Affiliations

  1. Cancer Prevention Center, Yonsei Cancer Canter, Department of Medicine, Yonsei Unversity College of Medicine, Yonsei University, Seoul, Republic of Korea

    Ki-Yong Ahn, Mi Kyung Lee, Dong-Il Kim, Jihye Park, Jihee Min, Hyuk In Yang, Junga Lee, Minsuk Oh & Justin Y. Jeon

  2. Department of Internal Medicine, Yonsei University, College of Medicine, Seoul, Republic of Korea

    Joongbae An

  3. Department of Family Medicine, Yonsei University, College of Medicine, Seoul, Republic of Korea

    Ji-Won Lee

  4. Department of Clinical Nursing Science, Yonsei University, College of Nursing, Nursing Policy Research Institute, Biobehavioral Research Center, Seoul, Republic of Korea

    Sang Hui Chu

  5. Department of Medical Oncology, Dana-Farber Cancer Institute, 450 Brookline Avenue, Boston, MA, USA

    Jeffrey A. Meyerhardt

  6. Department of Surgery, Yonsei University College of Medicine, 250 Seongsan-ro, Seodaemun-gu, Seoul, 120-752, South Korea

    Nam-Kyu Kim

  7. Department of Sport and Leisure Studies, Exercise Medicine Center for Diabetes and Cancer Patients, Yonsei University, Shinchon-dong, Seodaemun-gu, Seoul, 120-749, South Korea

    Nam-Kyu Kim & Justin Y. Jeon

Authors
  1. Ki-Yong Ahn
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mi Kyung Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dong-Il Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jihye Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jihee Min
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hyuk In Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Junga Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Minsuk Oh
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Joongbae An
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Ji-Won Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Sang Hui Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Jeffrey A. Meyerhardt
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Nam-Kyu Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Justin Y. Jeon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Nam-Kyu Kim or Justin Y. Jeon.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ahn, KY., Lee, M.K., Kim, DI. et al. Cardiopulmonary fitness, adiponectin, chemerin associated fasting insulin level in colorectal cancer patients. Support Care Cancer 24, 2927–2935 (2016). https://doi.org/10.1007/s00520-016-3095-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00520-016-3095-4

Keywords

Search

Navigation