FEATURE AND REVIEW PAPER
Visceral adiposity and cancer survival: a review of imaging studies
J. Xiao MSc,,
V.C. Mazurak PhD,,
T.A. Olobatuyi MSc,,
B.J. Caan DrPH,,
C.M. Prado PhD,,
J. Xiao MSc,
PhD Candidate
Department of Agricultural, Food and Nutritional Science, Division of Human Nutrition, 4-002 Li Ka Shing Centre, University of Alberta, Edmonton, AB, Canada
Search for more papers by this authorV.C. Mazurak PhD,
Associate Professor in Nutrition and Metabolism
Department of Agricultural, Food and Nutritional Science, Division of Human Nutrition, 4-002 Li Ka Shing Centre, University of Alberta, Edmonton, AB, Canada
Search for more papers by this authorT.A. Olobatuyi MSc,
Research Assistant
Department of Agricultural, Food and Nutritional Science, Division of Human Nutrition, 4-002 Li Ka Shing Centre, University of Alberta, Edmonton, AB, Canada
Search for more papers by this authorB.J. Caan DrPH,
Senior Research Scientist and Nutritional Epidemiologist
Division of Research, Kaiser Permanente, Oakland, CA, USA
Search for more papers by this authorCorresponding Author
C.M. Prado PhD,
Assistant Professor, CAIP Chair in Nutrition, Food and Health; Director, Human Nutrition Research Unit
Department of Agricultural, Food and Nutritional Science, Division of Human Nutrition, 4-002 Li Ka Shing Centre, University of Alberta, Edmonton, AB, Canada
Correspondence
Carla M. Prado,
Department of Agricultural, Food and Nutritional Science, Human Nutrition Research Unit, 4-002 Li Ka Shing Centre, University of Alberta, Edmonton, AB, Canada.
Email: [email protected]
Search for more papers by this authorJ. Xiao MSc,,
V.C. Mazurak PhD,,
T.A. Olobatuyi MSc,,
B.J. Caan DrPH,,
C.M. Prado PhD,,
J. Xiao MSc,
PhD Candidate
Department of Agricultural, Food and Nutritional Science, Division of Human Nutrition, 4-002 Li Ka Shing Centre, University of Alberta, Edmonton, AB, Canada
Search for more papers by this authorV.C. Mazurak PhD,
Associate Professor in Nutrition and Metabolism
Department of Agricultural, Food and Nutritional Science, Division of Human Nutrition, 4-002 Li Ka Shing Centre, University of Alberta, Edmonton, AB, Canada
Search for more papers by this authorT.A. Olobatuyi MSc,
Research Assistant
Department of Agricultural, Food and Nutritional Science, Division of Human Nutrition, 4-002 Li Ka Shing Centre, University of Alberta, Edmonton, AB, Canada
Search for more papers by this authorB.J. Caan DrPH,
Senior Research Scientist and Nutritional Epidemiologist
Division of Research, Kaiser Permanente, Oakland, CA, USA
Search for more papers by this authorCorresponding Author
C.M. Prado PhD,
Assistant Professor, CAIP Chair in Nutrition, Food and Health; Director, Human Nutrition Research Unit
Department of Agricultural, Food and Nutritional Science, Division of Human Nutrition, 4-002 Li Ka Shing Centre, University of Alberta, Edmonton, AB, Canada
Correspondence
Carla M. Prado,
Department of Agricultural, Food and Nutritional Science, Human Nutrition Research Unit, 4-002 Li Ka Shing Centre, University of Alberta, Edmonton, AB, Canada.
Email: [email protected]
Search for more papers by this authorAbstract
Although obesity is a well-known risk factor for cancer, the association between obesity and cancer survival remains controversial. This is partially due to the inability of conventional obesity measures to directly assess adiposity or adipose tissue distribution. As a metabolic organ, visceral adipose tissue (VAT) secrets a variety of cytokines and cytokine-like factors, potentially affecting cancer survival. The objective of this review was to investigate the influence of imaging-assessed VAT on cancer survival. A total of 22 studies assessing the impact of visceral adiposity on survival were included. Negative associations between VAT and survival were more frequently observed among patients with colorectal (four of six studies) and pancreatic (three of five studies) cancers, compared to higher VAT predicting longer survival in most studies of renal cell carcinoma patients (four of five studies). Methodological limitations, including unstandardised VAT measurement methods, lack of other body composition measurement (i.e. muscle mass), small sample size and heterogeneous cohort characteristics, may explain controversial findings related to the impact of VAT on cancer survival.
References
- Aune, D., Navarro Rosenblatt, D. A., Chan, D. S., Abar, L., Vingeliene, S., Vieira, A. R., & Norat, T. (2015). Anthropometric factors and ovarian cancer risk: A systematic review and nonlinear dose-response meta-analysis of prospective studies. International Journal of Cancer, 136, 1888–1898.
- Balentine, C. J., Enriquez, J., Fisher, W., Hodges, S., Bansal, V., Sansgiry, S., & Berger, D. H. (2010). Intra-abdominal fat predicts survival in pancreatic cancer. Journal of Gastrointestinal Surgery, 14, 1832–1837.
- Balentine, C. J., Marshall, C., Robinson, C., Wilks, J., Anaya, D., Albo, D., & Berger, D. H. (2010). Validating quantitative obesity measurements in colorectal cancer patients. Journal of Surgical Research, 164, 18–22.
- Clark, W., Siegel, E. M., Chen, Y. A., Zhao, X., Parsons, C. M., Hernandez, J. M., & Shibata, D. (2013). Quantitative measures of visceral adiposity and body mass index in predicting rectal cancer outcomes after neoadjuvant chemoradiation. Journal of the American College of Surgeons, 216, 1070–1081.
- Coe, P. O., O'Reilly, D. A., & Renehan, A. G. (2014). Excess adiposity and gastrointestinal cancer. British Journal of Surgery, 101, 1518–1531; discussion 1531.
- Demerath, E. W., Shen, W., Lee, M., Choh, A. C., Czerwinski, S. A., Siervogel, R. M., & Towne, B. (2007). Approximation of total visceral adipose tissue with a single magnetic resonance image. American Journal of Clinical Nutrition, 85, 362–368.
- Donohoe, C. L., Doyle, S. L., & Reynolds, J. V. (2011). Visceral adiposity, insulin resistance and cancer risk. Diabetology and Metabolic Syndrome, 3, 12.
- Gaujoux, S., Torres, J., Olson, S., Winston, C., Gonen, M., Brennan, M. F., & Allen, P. J. (2012). Impact of obesity and body fat distribution on survival after pancreaticoduodenectomy for pancreatic adenocarcinoma. Annals of Surgical Oncology, 19, 2908–2916.
- Gonzalez, M. C., Pastore, C. A., Orlandi, S. P., & Heymsfield, S. B. (2014). Obesity paradox in cancer: New insights provided by body composition. American Journal of Clinical Nutrition, 99, 999–1005.
- Guiu, B., Petit, J. M., Bonnetain, F., Ladoire, S., Guiu, S., Cercueil, J. P., & Ghiringhelli, F. (2010). Visceral fat area is an independent predictive biomarker of outcome after first-line bevacizumab-based treatment in metastatic colorectal cancer. Gut, 59, 341–347.
- Hakimi, A. A., Furberg, H., Zabor, E. C., Jacobsen, A., Schultz, N., Ciriello, G., & Russo, P. (2013). An epidemiologic and genomic investigation into the obesity paradox in renal cell carcinoma. Journal of the National Cancer Institute, 105, 1862–1870.
- Howard, J. M., Beddy, P., Ennis, D., Keogan, M., Pidgeon, G. P., & Reynolds, J. V. (2010). Associations between leptin and adiponectin receptor upregulation, visceral obesity and tumour stage in oesophageal and junctional adenocarcinoma. British Journal of Surgery, 97, 1020–1027.
- Ibrahim, M. M. (2010). Subcutaneous and visceral adipose tissue: Structural and functional differences. Obesity Reviews, 11, 11–18.
- Kaneko, G., Miyajima, A., Yuge, K., Yazawa, S., Mizuno, R., Kikuchi, E., & Oya, M. (2015). Visceral obesity is associated with better recurrence-free survival after curative surgery for Japanese patients with localized clear cell renal cell carcinoma. Japanese Journal of Clinical Oncology, 45, 210–216.
- Kang, J., Baek, S. E., Kim, T., Hur, H., Min, B. S., Lim, J. S., … & Lee, K. Y. (2012). Impact of fat obesity on laparoscopic total mesorectal excision: More reliable indicator than body mass index. International Journal of Colorectal Disease, 27, 497–505.
- Kasenda, B., Bass, A., Koeberle, D., Pestalozzi, B., Borner, M., Herrmann, R., & Hess, V. (2014). Survival in overweight patients with advanced pancreatic carcinoma: A multicentre cohort study. BMC Cancer, 14, 728.
- Kazemi-Bajestani, S. M., Mazurak, V. C., & Baracos, V. (2016). Computed tomography-defined muscle and fat wasting are associated with cancer clinical outcomes. Seminars in Cell and Developmental Biology, 54, 2–10.
- Kershaw, E., & Flier, J. (2004). Adipose tissue as an endocrine organ. The Journal of Clinical Endocrinology and Metabolism, 89, 2548–2556.
- Kim, J. H., Chin, H. M., Hwang, S. S., & Jun, K. H. (2014). Impact of intra-abdominal fat on surgical outcome and overall survival of patients with gastric cancer. International Journal of Surgery, 12, 346–352.
- Kobayashi, J., Tadokoro, N., Watanabe, M., & Shinomiya, M. (2002). A novel method of measuring intra-abdominal fat volume using helical computed tomography. International Journal of Obesity and Related Metabolic Disorders, 26, 398–402.
- Ladoire, S., Bonnetain, F., Gauthier, M., Zanetta, S., Petit, J. M., Guiu, S., & Guiu, B. (2011). Visceral fat area as a new independent predictive factor of survival in patients with metastatic renal cell carcinoma treated with antiangiogenic agents. Oncologist, 16, 71–81.
- Lee, H. W., Jeong, B. C., Seo, S. I., Jeon, S. S., Lee, H. M., Choi, H. Y., & Jeon, H. G. (2015). Prognostic significance of visceral obesity in patients with advanced renal cell carcinoma undergoing nephrectomy. International Journal of Urology, 22, 455–461.
- Lee, C. S., Murphy, D. J., McMahon, C., Nolan, B., Cullen, G., Mulcahy, H., & Doherty, G. A. (2015). Visceral adiposity is a risk factor for poor prognosis in colorectal cancer patients receiving adjuvant chemotherapy. Journal of Gastrointestinal Cancer, 46, 243–250.
- Li, X. T., Tang, L., Chen, Y., Li, Y. L., Zhang, X. P., & Sun, Y. S. (2015). Visceral and subcutaneous fat as new independent predictive factors of survival in locally advanced gastric carcinoma patients treated with neo-adjuvant chemotherapy. Journal of Cancer Research and Clinical Oncology, 141, 1237–1247.
- Martin, L., Birdsell, L., Macdonald, N., Reiman, T., Clandinin, M. T., McCargar, L. J., & Baracos, V. E. (2013). Cancer cachexia in the age of obesity: Skeletal muscle depletion is a powerful prognostic factor, independent of body mass index. Journal of Clinical Oncology, 31, 1539–1547.
- Mathur, A., Hernandez, J., Shaheen, F., Shroff, M., Dahal, S., Morton, C., & Rosemurgy, A. (2011). Preoperative computed tomography measurements of pancreatic steatosis and visceral fat: Prognostic markers for dissemination and lethality of pancreatic adenocarcinoma. HPB, 13, 404–410.
- Miller, B. S., Ignatoski, K. M., Daignault, S., Lindland, C., Doherty, M., Gauger, P. G., & Doherty, G. M. (2012). Worsening central sarcopenia and increasing intra-abdominal fat correlate with decreased survival in patients with adrenocortical carcinoma. World Journal of Surgery, 36, 1509–1516.
- Mitsiopoulos, N., Baumgartner, R. N., Heymsfield, S. B., Lyons, W., Gallagher, D., & Ross, R. (1998). Cadaver validation of skeletal muscle measurement by magnetic resonance imaging and computerized tomography. Journal of Applied Physiology (1985), 85, 115–122.
- Mourtzakis, M., Prado, C. M., Lieffers, J. R., Reiman, T., McCargar, L. J., & Baracos, V. E. (2008). A practical and precise approach to quantification of body composition in cancer patients using computed tomography images acquired during routine care. Applied Physiology, Nutrition and Metabolism, 33, 997–1006.
- Nault, J. C., Pigneur, F., Nelson, A. C., Costentin, C., Tselikas, L., Katsahian, S., & Decaens, T. (2015). Visceral fat area predicts survival in patients with advanced hepatocellular carcinoma treated with tyrosine kinase inhibitors. Digestive and Liver Disease, 47, 869–876.
- Naya, Y., Zenbutsu, S., Araki, K., Nakamura, K., Kobayashi, M., Kamijima, S., & Igarashi, T. (2010). Influence of visceral obesity on oncologic outcome in patients with renal cell carcinoma. Urologia Internationalis, 85, 30–36.
- Oka, R., Kobayashi, J., Yagi, K., Tanii, H., Miyamoto, S., Asano, A., & Yamagishi, M. (2008). Reassessment of the cutoff values of waist circumference and visceral fat area for identifying Japanese subjects at risk for the metabolic syndrome. Diabetes Research and Clinical Practice, 79, 474–481.
- Papoulas, M., Weiser, R., Rosen, G., Gerstenhaber, F., Merimsky, O., Lubezky, N., & Lahat, G. (2015). Visceral fat content correlates with retroperitoneal soft tissue sarcoma (STS) local recurrence and survival. World Journal of Surgery, 39, 1895–1901.
- Parsons, H. A., Baracos, V. E., Dhillon, N., Hong, D. S., & Kurzrock, R. (2012). Body composition, symptoms, and survival in advanced cancer patients referred to a phase I service. PLoS ONE, 7, e29330.
- Pausch, T., Hartwig, W., Hinz, U., Swolana, T., Bundy, B. D., Hackert, T., & Werner, J. (2012). Cachexia but not obesity worsens the postoperative outcome after pancreatoduodenectomy in pancreatic cancer. Surgery, 152(3 Suppl 1), S81–S88.
- Pecorelli, N., Carrara, G., De Cobelli, F., Cristel, G., Damascelli, A., Balzano, G., & Braga, M. (2016). Effect of sarcopenia and visceral obesity on mortality and pancreatic fistula following pancreatic cancer surgery. British Journal of Surgery, 103, 434–442.
- Prado, C. M. (2013). Body composition in chemotherapy: The promising role of CT scans. Current Opinion in Clinical Nutrition and Metabolic Care, 16, 525–533.
- Prado, C. M., Baracos, V. E., McCargar, L. J., Mourtzakis, M., Mulder, K. E., Reiman, T., & Sawyer, M. B. (2007). Body composition as an independent determinant of 5-fluorouracil-based chemotherapy toxicity. Clinical Cancer Research, 13, 3264–3268.
- Prado, C. M., Birdsell, L. A., & Baracos, V. E. (2009). The emerging role of computerized tomography in assessing cancer cachexia. Current Opinion in Supportive and Palliative Care, 3, 269–275.
- Prado, C. M., Cushen, S. J., Orsso, C. E., & Ryan, A. M. (2016). Sarcopenia and cachexia in the era of obesity: clinical and nutritional impact. Proceedings of the Nutrition Society, 75, 188–198.
- Prado, C. M., Gonzalez, M. C., & Heymsfield, S. B. (2015). Body composition phenotypes and obesity paradox. Current Opinion in Clinical Nutrition and Metabolic Care, 18, 535–551
- Prado, C. M., & Heymsfield, S. B. (2014). Lean tissue imaging: A new era for nutritional assessment and intervention. JPEN, 38, 940–953.
- Prado, C. M., Lieffers, J. R., McCargar, L. J., Reiman, T., Sawyer, M. B., Martin, L., & Baracos, V. E. (2008). Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: A population-based study. Lancet Oncology, 9, 629–635.
- Renehan, A. G., Flood, A., Adams, K. F., Olden, M., Hollenbeck, A. R., Cross, A. J., & Leitzmann, M. F. (2012). Body mass index at different adult ages, weight change, and colorectal cancer risk in the National Institutes of Health-AARP Cohort. American Journal of Epidemiology, 176, 1130–1140.
- Rickles, A. S., Iannuzzi, J. C., Mironov, O., Deeb, A. P., Sharma, A., Fleming, F. J., & Monson, J. R. (2013). Visceral obesity and colorectal cancer: Are we missing the boat with BMI? Journal of Gastrointestinal Surgery, 17, 133–143; discussion p. 143.
- Schlesinger, S., Siegert, S., Koch, M., Walter, J., Heits, N., Hinz, S., & Nothlings, U. (2014). Postdiagnosis body mass index and risk of mortality in colorectal cancer survivors: A prospective study and meta-analysis. Cancer Causes and Control, 25, 1407–1418.
- Shen, W., Punyanitya, M., Wang, Z., Gallagher, D., St-Onge, M. P., Albu, J., & Heshka, S. (2004a). Total body skeletal muscle and adipose tissue volumes: Estimation from a single abdominal cross-sectional image. Journal of Applied Physiology (1985), 97, 2333–2338.
- Shen, W., Punyanitya, M., Wang, Z., Gallagher, D., St-Onge, M. P., Albu, J., & Heshka, S. (2004b). Visceral adipose tissue: Relations between single-slice areas and total volume. American Journal of Clinical Nutrition, 80, 271–278.
- Shuster, A., Patlas, M., Pinthus, J. H., & Mourtzakis, M. (2012). The clinical importance of visceral adiposity: A critical review of methods for visceral adipose tissue analysis. British Journal of Radiology, 85, 1–10.
- Slaughter, K. N., Thai, T., Penaroza, S., Benbrook, D. M., Thavathiru, E., Ding, K., & Moore, K. N. (2014). Measurements of adiposity as clinical biomarkers for first-line bevacizumab-based chemotherapy in epithelial ovarian cancer. Gynecologic Oncology, 133, 11–15.
- Steffens, S., Grunwald, V., Ringe, K. I., Seidel, C., Eggers, H., Schrader, M., & Schrader, A. J. (2011). Does obesity influence the prognosis of metastatic renal cell carcinoma in patients treated with vascular endothelial growth factor-targeted therapy? Oncologist, 16, 1565–1571.
- Stolzenberg-Solomon, R. Z., Adams, K., Leitzmann, M., Schairer, C., Michaud, D. S., Hollenbeck, A., & Silverman, D. T. (2008). Adiposity, physical activity, and pancreatic cancer in the National Institutes of Health-AARP Diet and Health Cohort. American Journal of Epidemiology, 167, 586–597.
- Swede, H., Hajduk, A. M., Sharma, J., Rawal, S., Rasool, H., Vella, A. T., & Stevens, R. G. (2014). Baseline serum C-reactive protein and death from colorectal cancer in the NHANES III cohort. International Journal of Cancer, 134, 1862–1870.
- Tilg, H., & Moschen, A. R. (2006). Adipocytokines: Mediators linking adipose tissue, inflammation and immunity. Nature Reviews Immunology, 6, 772–783.
- Trayhurn, P. (2005). Endocrine and signalling role of adipose tissue: New perspectives on fat. Acta Physiologica Scandinavica, 184, 285–293.
- Tsujinaka, S., Konishi, F., Kawamura, Y. J., Saito, M., Tajima, N., Tanaka, O., & Lefor, A. T. (2008). Visceral obesity predicts surgical outcomes after laparoscopic colectomy for sigmoid colon cancer. Diseases of the Colon and Rectum, 51, 1757–1765; discussion 1765-1757.
- Vrieling, A., & Kampman, E. (2010). The role of body mass index, physical activity, and diet in colorectal cancer recurrence and survival: A review of the literature. American Journal of Clinical Nutrition, 92, 471–490.
- Wang, F., & Xu, Y. (2014). Body mass index and risk of renal cell cancer: A dose-response meta-analysis of published cohort studies. International Journal of Cancer, 135, 1673–1686.
- Yamamoto, N., Fujii, S., Sato, T., Oshima, T., Rino, Y., Kunisaki, C., & Imada, T. (2012). Impact of body mass index and visceral adiposity on outcomes in colorectal cancer. Asia-Pacific Journal of Clinical Oncology, 8, 337–345.
