Skip to main content
Top
Published in: Cancer Causes & Control 11/2014

01-11-2014 | Original paper

Obesity and non-Hodgkin lymphoma survival in an ethnically diverse population: the Multiethnic Cohort study

Authors: Qi Jie Nicholas Leo, Nicholas J. Ollberding, Lynne R. Wilkens, Laurence N. Kolonel, Brian E. Henderson, Loic Le Marchand, Gertraud Maskarinec

Published in: Cancer Causes & Control | Issue 11/2014

Login to get access

Abstract

Purpose

Obesity increases mortality for several malignancies, but for non-Hodgkin lymphoma (NHL), the association between body mass index (BMI) and survival is unclear. We examined the association of pre-diagnostic BMI with overall and NHL-specific survival in the multiethnic cohort (MEC) study of African Americans, Native Hawaiians, Japanese Americans, Latinos, and Caucasians.

Methods

MEC participants free of NHL at cohort entry and diagnosed with NHL during follow-up were included in the analyses (n = 1,331). BMI was based on self-reported weight and height at cohort entry and after 6.1 years of cohort entry. Cox proportional hazards regression was used to calculate hazard ratios (HR) and 95 % confidence intervals (CI) with BMI as time-varying exposure in relation to all-cause and NHL-specific mortality while adjusting for known confounders.

Results

The mean age at NHL diagnosis was 70.5 (range 45–89) years. After a mean follow-up of 4.3 ± 3.5 years, 667 deaths including 450 NHL-specific deaths occurred. In multivariable models, obese patients (BMI ≥30.0 kg/m2) had higher all-cause (HR 1.46, 95 % CI 1.13–1.87) and NHL-specific (HR 1.77, 95 % CI 1.30–2.41) mortality compared with patients with high-normal BMI (22.5–24.9 kg/m2). For overweight patients (BMI = 25.0–29.9 kg/m2), the respective HRs were 1.21 (95 % CI 0.99–1.49) and 1.36 (95 % CI 1.06–1.75). Cases with low-normal BMI (<22.5 kg/m2) experienced a significant 45 % higher all-cause and a 40 % higher NHL-specific mortality. After stratification by NHL type, the adverse effect of BMI was stronger for chronic lymphocytic leukemia/small lymphocytic lymphoma than for diffuse large B cell lymphoma and follicular lymphoma.

Conclusions

Pre-diagnostic BMI may be a suitable prognostic marker for NHL patients.
Literature
1.
go back to reference Society AC (2013) Cancer Facts & Figures 2013. American Cancer Society, Atlanta Society AC (2013) Cancer Facts & Figures 2013. American Cancer Society, Atlanta
2.
go back to reference Molina A (2008) A decade of rituximab: improving survival outcomes in non-Hodgkin’s lymphoma. Annu Rev Med 59:237–250PubMedCrossRef Molina A (2008) A decade of rituximab: improving survival outcomes in non-Hodgkin’s lymphoma. Annu Rev Med 59:237–250PubMedCrossRef
3.
go back to reference Howlader NNA, Krapcho M, Garshell J, Neyman N, Altekruse SF, et al SEER Cancer Statistics Review, 1975–2010, National Cancer Institute. Bethesda. http://seer.cancer.gov/csr/1975_2010/. Based on November 2012 SEER data submission, posted to the SEER web site, April 2013 Howlader NNA, Krapcho M, Garshell J, Neyman N, Altekruse SF, et al SEER Cancer Statistics Review, 1975–2010, National Cancer Institute. Bethesda. http://​seer.​cancer.​gov/​csr/​1975_​2010/​. Based on November 2012 SEER data submission, posted to the SEER web site, April 2013
4.
go back to reference No authors listed (1993) A predictive model for aggressive non-Hodgkin’s lymphoma. The international non-Hodgkin’s lymphoma prognostic factors project. N Engl J Med 329:987–94 No authors listed (1993) A predictive model for aggressive non-Hodgkin’s lymphoma. The international non-Hodgkin’s lymphoma prognostic factors project. N Engl J Med 329:987–94
5.
go back to reference Solal-Celigny P, Roy P, Colombat P et al (2004) Follicular lymphoma international prognostic index. Blood 104:1258–1265PubMedCrossRef Solal-Celigny P, Roy P, Colombat P et al (2004) Follicular lymphoma international prognostic index. Blood 104:1258–1265PubMedCrossRef
6.
go back to reference Larsson SC, Wolk A (2011) Body mass index and risk of non-Hodgkin’s and Hodgkin’s lymphoma: a meta-analysis of prospective studies. Eur J Cancer 47:2422–2430PubMedCrossRef Larsson SC, Wolk A (2011) Body mass index and risk of non-Hodgkin’s and Hodgkin’s lymphoma: a meta-analysis of prospective studies. Eur J Cancer 47:2422–2430PubMedCrossRef
7.
go back to reference Maskarinec G, Erber E, Gill J, Cozen W, Kolonel LN (2008) Overweight and obesity at different times in life as risk factors for non-Hodgkin’s lymphoma: the multiethnic cohort. Cancer Epidemiol Biomark Prev 17:196–203CrossRef Maskarinec G, Erber E, Gill J, Cozen W, Kolonel LN (2008) Overweight and obesity at different times in life as risk factors for non-Hodgkin’s lymphoma: the multiethnic cohort. Cancer Epidemiol Biomark Prev 17:196–203CrossRef
8.
go back to reference Larsson SC, Wolk A (2011) Body mass index and risk of non-Hodgkin’s and Hodgkin’s lymphoma: a meta-analysis of prospective studies. Eur J Cancer 47:2422–2430PubMedCrossRef Larsson SC, Wolk A (2011) Body mass index and risk of non-Hodgkin’s and Hodgkin’s lymphoma: a meta-analysis of prospective studies. Eur J Cancer 47:2422–2430PubMedCrossRef
9.
go back to reference Protani M, Coory M, Martin JH (2010) Effect of obesity on survival of women with breast cancer: systematic review and meta-analysis. Breast Cancer Res Treat 123:627–635PubMedCrossRef Protani M, Coory M, Martin JH (2010) Effect of obesity on survival of women with breast cancer: systematic review and meta-analysis. Breast Cancer Res Treat 123:627–635PubMedCrossRef
10.
go back to reference Geyer SM, Morton LM, Habermann TM et al (2010) Smoking, alcohol use, obesity, and overall survival from non-Hodgkin lymphoma: a population-based study. Cancer 116:2993–3000PubMedCrossRefPubMedCentral Geyer SM, Morton LM, Habermann TM et al (2010) Smoking, alcohol use, obesity, and overall survival from non-Hodgkin lymphoma: a population-based study. Cancer 116:2993–3000PubMedCrossRefPubMedCentral
11.
go back to reference Simard JF, Baecklund F, Chang ET et al (2013) Lifestyle factors, autoimmune disease and family history in prognosis of non-hodgkin lymphoma overall and subtypes. Int J Cancer 132:2659–2666PubMedCrossRef Simard JF, Baecklund F, Chang ET et al (2013) Lifestyle factors, autoimmune disease and family history in prognosis of non-hodgkin lymphoma overall and subtypes. Int J Cancer 132:2659–2666PubMedCrossRef
12.
go back to reference Chu DM, Wahlqvist ML, Lee MS, Chang HY (2011) Central obesity predicts non-Hodgkin’s lymphoma mortality and overall obesity predicts leukemia mortality in adult Taiwanese. J Am Coll Nutr 30:310–319PubMedCrossRef Chu DM, Wahlqvist ML, Lee MS, Chang HY (2011) Central obesity predicts non-Hodgkin’s lymphoma mortality and overall obesity predicts leukemia mortality in adult Taiwanese. J Am Coll Nutr 30:310–319PubMedCrossRef
13.
go back to reference Jones JA, Fayad LE, Elting LS, Rodriguez MA (2010) Body mass index and outcomes in patients receiving chemotherapy for intermediate-grade B-cell non-Hodgkin lymphoma. Leuk Lymphoma 51:1649–1657PubMedCrossRef Jones JA, Fayad LE, Elting LS, Rodriguez MA (2010) Body mass index and outcomes in patients receiving chemotherapy for intermediate-grade B-cell non-Hodgkin lymphoma. Leuk Lymphoma 51:1649–1657PubMedCrossRef
14.
go back to reference Carson KR, Bartlett NL, McDonald JR et al (2012) Increased body mass index is associated with improved survival in United States veterans with diffuse large B-cell lymphoma. J Clin Oncol 30:3217–3222PubMedCrossRefPubMedCentral Carson KR, Bartlett NL, McDonald JR et al (2012) Increased body mass index is associated with improved survival in United States veterans with diffuse large B-cell lymphoma. J Clin Oncol 30:3217–3222PubMedCrossRefPubMedCentral
15.
go back to reference Parr CL, Batty GD, Lam TH et al (2010) Body-mass index and cancer mortality in the Asia-Pacific Cohort Studies Collaboration: pooled analyses of 424,519 participants. Lancet Oncol 11:741–752PubMedCrossRefPubMedCentral Parr CL, Batty GD, Lam TH et al (2010) Body-mass index and cancer mortality in the Asia-Pacific Cohort Studies Collaboration: pooled analyses of 424,519 participants. Lancet Oncol 11:741–752PubMedCrossRefPubMedCentral
16.
go back to reference Reeves GK, Pirie K, Beral V, Green J, Spencer E, Bull D (2007) Cancer incidence and mortality in relation to body mass index in the Million Women Study: cohort study. BMJ 335:1134PubMedCrossRefPubMedCentral Reeves GK, Pirie K, Beral V, Green J, Spencer E, Bull D (2007) Cancer incidence and mortality in relation to body mass index in the Million Women Study: cohort study. BMJ 335:1134PubMedCrossRefPubMedCentral
17.
go back to reference Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ (2003) Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 348:1625–1638PubMedCrossRef Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ (2003) Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 348:1625–1638PubMedCrossRef
18.
go back to reference Kolonel LN, Henderson BE, Hankin JH et al (2000) A multiethnic cohort in Hawaii and Los Angeles: baseline characteristics. Am J Epidemiol 151:346–357PubMedCrossRef Kolonel LN, Henderson BE, Hankin JH et al (2000) A multiethnic cohort in Hawaii and Los Angeles: baseline characteristics. Am J Epidemiol 151:346–357PubMedCrossRef
19.
go back to reference Stram DO, Hankin JH, Wilkens LR et al (2000) Calibration of the dietary questionnaire for a multiethnic cohort in Hawaii and Los Angeles. Am J Epidemiol 151:358–370PubMedCrossRef Stram DO, Hankin JH, Wilkens LR et al (2000) Calibration of the dietary questionnaire for a multiethnic cohort in Hawaii and Los Angeles. Am J Epidemiol 151:358–370PubMedCrossRef
20.
go back to reference Hankey BF, Ries LA, Edwards BK (1999) The surveillance, epidemiology, and end results program: a national resource. Cancer Epidemiol Biomark Prev 8:1117–1121 Hankey BF, Ries LA, Edwards BK (1999) The surveillance, epidemiology, and end results program: a national resource. Cancer Epidemiol Biomark Prev 8:1117–1121
21.
go back to reference Turner JJ, Morton LM, Linet MS et al (2010) InterLymph hierarchical classification of lymphoid neoplasms for epidemiologic research based on the WHO classification (2008): update and future directions. Blood 116:e90–e98PubMedCrossRefPubMedCentral Turner JJ, Morton LM, Linet MS et al (2010) InterLymph hierarchical classification of lymphoid neoplasms for epidemiologic research based on the WHO classification (2008): update and future directions. Blood 116:e90–e98PubMedCrossRefPubMedCentral
22.
go back to reference Morton LM, Turner JJ, Cerhan JR et al (2007) Proposed classification of lymphoid neoplasms for epidemiologic research from the Pathology Working Group of the International Lymphoma Epidemiology Consortium (InterLymph). Blood 110:695–708PubMedCrossRefPubMedCentral Morton LM, Turner JJ, Cerhan JR et al (2007) Proposed classification of lymphoid neoplasms for epidemiologic research from the Pathology Working Group of the International Lymphoma Epidemiology Consortium (InterLymph). Blood 110:695–708PubMedCrossRefPubMedCentral
23.
go back to reference Johnson C (2004) SEER Program Coding and Staging Manual 2004, Revision 1. National Cancer Institute, NIH Publication number 04-5581, Bethesda Johnson C (2004) SEER Program Coding and Staging Manual 2004, Revision 1. National Cancer Institute, NIH Publication number 04-5581, Bethesda
24.
go back to reference Henderson SO, Haiman CA, Wilkens LR, Kolonel LN, Wan P, Pike MC (2007) Established risk factors account for most of the racial differences in cardiovascular disease mortality. PLoS ONE 2:e377PubMedCrossRefPubMedCentral Henderson SO, Haiman CA, Wilkens LR, Kolonel LN, Wan P, Pike MC (2007) Established risk factors account for most of the racial differences in cardiovascular disease mortality. PLoS ONE 2:e377PubMedCrossRefPubMedCentral
25.
go back to reference Coiffier B, Lepage E, Briere J et al (2002) CHOP chemotherapy plus rituximab compared with CHOP alone in elderly patients with diffuse large-B-cell lymphoma. N Engl J Med 346:235–242PubMedCrossRef Coiffier B, Lepage E, Briere J et al (2002) CHOP chemotherapy plus rituximab compared with CHOP alone in elderly patients with diffuse large-B-cell lymphoma. N Engl J Med 346:235–242PubMedCrossRef
26.
go back to reference Carmienke S, Freitag MH, Pischon T et al (2013) General and abdominal obesity parameters and their combination in relation to mortality: a systematic review and meta-regression analysis. Eur J Clin Nutr 67:573–585PubMedCrossRef Carmienke S, Freitag MH, Pischon T et al (2013) General and abdominal obesity parameters and their combination in relation to mortality: a systematic review and meta-regression analysis. Eur J Clin Nutr 67:573–585PubMedCrossRef
27.
go back to reference Ollberding NJ, Evens AM, Aschebrook-Kilfoy B et al (2013) Pre-diagnosis cigarette smoking and overall survival in non-Hodgkin lymphoma. Br J Haematol 163:352–356PubMedCrossRef Ollberding NJ, Evens AM, Aschebrook-Kilfoy B et al (2013) Pre-diagnosis cigarette smoking and overall survival in non-Hodgkin lymphoma. Br J Haematol 163:352–356PubMedCrossRef
28.
go back to reference Talamini R, Polesel J, Spina M et al (2008) The impact of tobacco smoking and alcohol drinking on survival of patients with non-Hodgkin lymphoma. Int J Cancer 122:1624–1629PubMedCrossRef Talamini R, Polesel J, Spina M et al (2008) The impact of tobacco smoking and alcohol drinking on survival of patients with non-Hodgkin lymphoma. Int J Cancer 122:1624–1629PubMedCrossRef
29.
go back to reference Han X, Stevens J, Bradshaw PT (2013) Body mass index, weight change, and survival in non-Hodgkin lymphoma patients in Connecticut women. Nutr Cancer 65:43–50PubMedCrossRef Han X, Stevens J, Bradshaw PT (2013) Body mass index, weight change, and survival in non-Hodgkin lymphoma patients in Connecticut women. Nutr Cancer 65:43–50PubMedCrossRef
30.
go back to reference Ezzati M, Riboli E (2013) Behavioral and dietary risk factors for noncommunicable diseases. N Engl J Med 369:954–964PubMedCrossRef Ezzati M, Riboli E (2013) Behavioral and dietary risk factors for noncommunicable diseases. N Engl J Med 369:954–964PubMedCrossRef
31.
go back to reference Calle EE, Kaaks R (2004) Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer 4:579–591PubMedCrossRef Calle EE, Kaaks R (2004) Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer 4:579–591PubMedCrossRef
32.
go back to reference Gregor MF, Hotamisligil GS (2011) Inflammatory mechanisms in obesity. Annu Rev Immunol 29:415–445PubMedCrossRef Gregor MF, Hotamisligil GS (2011) Inflammatory mechanisms in obesity. Annu Rev Immunol 29:415–445PubMedCrossRef
33.
34.
go back to reference Barb D, Williams CJ, Neuwirth AK, Mantzoros CS (2007) Adiponectin in relation to malignancies: a review of existing basic research and clinical evidence. Am J Clin Nutr 86:s858–s866PubMed Barb D, Williams CJ, Neuwirth AK, Mantzoros CS (2007) Adiponectin in relation to malignancies: a review of existing basic research and clinical evidence. Am J Clin Nutr 86:s858–s866PubMed
35.
go back to reference 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 109:1346–1353PubMedCrossRefPubMedCentral 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 109:1346–1353PubMedCrossRefPubMedCentral
36.
go back to reference Griggs JJ, Sabel MS (2008) Obesity and cancer treatment: weighing the evidence. J Clin Oncol 26:4060–4062PubMedCrossRef Griggs JJ, Sabel MS (2008) Obesity and cancer treatment: weighing the evidence. J Clin Oncol 26:4060–4062PubMedCrossRef
37.
go back to reference Berrington de Gonzalez A, Hartge P, Cerhan JR et al (2010) Body-mass index and mortality among 1.46 million white adults. N Engl J Med 363:2211–2219PubMedCrossRef Berrington de Gonzalez A, Hartge P, Cerhan JR et al (2010) Body-mass index and mortality among 1.46 million white adults. N Engl J Med 363:2211–2219PubMedCrossRef
38.
go back to reference Park SY, Wilkens LR, Murphy SP, Monroe KR, Henderson BE, Kolonel LN (2012) Body mass index and mortality in an ethnically diverse population: the Multiethnic Cohort Study. Eur J Epidemiol 27:489–497PubMedCrossRef Park SY, Wilkens LR, Murphy SP, Monroe KR, Henderson BE, Kolonel LN (2012) Body mass index and mortality in an ethnically diverse population: the Multiethnic Cohort Study. Eur J Epidemiol 27:489–497PubMedCrossRef
39.
go back to reference Whitlock G, Lewington S, Sherliker P et al (2009) Body-mass index and cause-specific mortality in 900 000 adults: collaborative analyses of 57 prospective studies. Lancet 373:1083–1096PubMedCrossRef Whitlock G, Lewington S, Sherliker P et al (2009) Body-mass index and cause-specific mortality in 900 000 adults: collaborative analyses of 57 prospective studies. Lancet 373:1083–1096PubMedCrossRef
40.
go back to reference Moon HG, Han W, Noh DY (2009) Underweight and breast cancer recurrence and death: a report from the Korean Breast Cancer Society. J Clin Oncol 27:5899–5905PubMedCrossRef Moon HG, Han W, Noh DY (2009) Underweight and breast cancer recurrence and death: a report from the Korean Breast Cancer Society. J Clin Oncol 27:5899–5905PubMedCrossRef
41.
go back to reference Field KM, Kosmider S, Jefford M et al (2008) Chemotherapy dosing strategies in the obese, elderly, and thin patient: results of a nationwide survey. J Oncol Pract 4:108–113PubMedCrossRefPubMedCentral Field KM, Kosmider S, Jefford M et al (2008) Chemotherapy dosing strategies in the obese, elderly, and thin patient: results of a nationwide survey. J Oncol Pract 4:108–113PubMedCrossRefPubMedCentral
42.
go back to reference Stevens J, Bradshaw PT, Truesdale KP, Jensen MD (2014) Obesity Paradox should not interfere with public health efforts. Int J Obes (Lond) Stevens J, Bradshaw PT, Truesdale KP, Jensen MD (2014) Obesity Paradox should not interfere with public health efforts. Int J Obes (Lond)
43.
go back to reference Kobayashi T, Kita K, Ohno T, Shirakawa S (1990) Chronic lymphocytic leukemia in Japan. Rinsho Ketsueki 31:554–563PubMed Kobayashi T, Kita K, Ohno T, Shirakawa S (1990) Chronic lymphocytic leukemia in Japan. Rinsho Ketsueki 31:554–563PubMed
44.
go back to reference Navarro WH, Loberiza FR Jr, Bajorunaite R et al (2006) Effect of body mass index on mortality of patients with lymphoma undergoing autologous hematopoietic cell transplantation. Biol Blood Marrow Transplant 12:541–551PubMedCrossRef Navarro WH, Loberiza FR Jr, Bajorunaite R et al (2006) Effect of body mass index on mortality of patients with lymphoma undergoing autologous hematopoietic cell transplantation. Biol Blood Marrow Transplant 12:541–551PubMedCrossRef
45.
go back to reference Tarella C, Caracciolo D, Gavarotti P et al (2000) Overweight as an adverse prognostic factor for non-Hodgkin’s lymphoma patients receiving high-dose chemotherapy and autograft. Bone Marrow Transplant 26:1185–1191PubMedCrossRef Tarella C, Caracciolo D, Gavarotti P et al (2000) Overweight as an adverse prognostic factor for non-Hodgkin’s lymphoma patients receiving high-dose chemotherapy and autograft. Bone Marrow Transplant 26:1185–1191PubMedCrossRef
46.
go back to reference German RR, Fink AK, Heron M et al (2011) The accuracy of cancer mortality statistics based on death certificates in the United States. Cancer Epidemiol 35:126–131PubMedCrossRef German RR, Fink AK, Heron M et al (2011) The accuracy of cancer mortality statistics based on death certificates in the United States. Cancer Epidemiol 35:126–131PubMedCrossRef
Metadata
Title
Obesity and non-Hodgkin lymphoma survival in an ethnically diverse population: the Multiethnic Cohort study
Authors
Qi Jie Nicholas Leo
Nicholas J. Ollberding
Lynne R. Wilkens
Laurence N. Kolonel
Brian E. Henderson
Loic Le Marchand
Gertraud Maskarinec
Publication date
01-11-2014
Publisher
Springer International Publishing
Published in
Cancer Causes & Control / Issue 11/2014
Print ISSN: 0957-5243
Electronic ISSN: 1573-7225
DOI
https://doi.org/10.1007/s10552-014-0447-6

Other articles of this Issue 11/2014

Cancer Causes & Control 11/2014 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine