Associations of artificially sweetened beverage intake with disease recurrence and mortality in stage III colon cancer: Results from CALGB 89803 (Alliance)

Brendan J. Guercio; Sui Zhang; Donna Niedzwiecki; Yanping Li; Ana Babic; Vicente Morales-Oyarvide; Leonard B. Saltz; Robert J. Mayer; Rex B. Mowat; Renaud Whittom; Alexander Hantel; Al Benson; Daniel Atienza; Michael Messino; Hedy Kindler; Alan Venook; Shuji Ogino; Emilie S. Zoltick; Meir Stampfer; Kimmie Ng; Kana Wu; Walter C. Willett; Edward L. Giovannucci; Jeffrey A. Meyerhardt; Charles S. Fuchs

doi:10.1371/journal.pone.0199244

Associations of artificially sweetened beverage intake with disease recurrence and mortality in stage III colon cancer: Results from CALGB 89803 (Alliance)

Brendan J. Guercio, Sui Zhang, Donna Niedzwiecki, Yanping Li, Ana Babic, Vicente Morales-Oyarvide, Leonard B. Saltz, Robert J. Mayer, Rex B. Mowat, Renaud Whittom, Alexander Hantel, Al Benson, Daniel Atienza, Michael Messino, Hedy Kindler, Alan Venook, Shuji Ogino, Emilie S. Zoltick, Meir Stampfer, Kimmie NgKana Wu, Walter C. Willett, Edward L. Giovannucci, Jeffrey A. Meyerhardt, Charles S. Fuchs^*

^*Corresponding author for this work

Medicine, Hematology Oncology Division

Research output: Contribution to journal › Article › peer-review

31 Scopus citations

Abstract

Purpose Observational studies have demonstrated increased colon cancer recurrence and mortality in states of excess energy balance, as denoted by factors including sedentary lifestyle, diabetes, increased dietary glycemic load, and increased intake of sugar-sweetened beverages. Nonetheless, the relation between artificially sweetened beverages, a popular alternative for sugar-sweetened beverages, and colon cancer recurrence and survival is unknown. Methods We analyzed data from 1,018 patients with stage III colon cancer who prospectively reported dietary intake during and after chemotherapy while enrolled in a National Cancer Institute-sponsored trial of adjuvant chemotherapy. Using Cox proportional hazards regressions, we assessed associations of artificially sweetened beverage intake with cancer recurrence and mortality. Results Patients consuming one or more 12-ounce servings of artificially sweetened beverages per day experienced an adjusted hazard ratio for cancer recurrence or mortality of 0.54 (95% confidence interval, 0.36 to 0.80) when compared to those who largely abstained (P_trend = .004). Similarly, increasing artificially sweetened beverage intake was also associated with a significant improvement in both recurrence-free survival (P_trend = .005) and overall survival (P_trend = .02). Substitution models demonstrated that replacing a 12-ounce serving of a sugar-sweetened beverage with an isovolumetric serving of an artificially sweetened beverage per day was associated with a 23% lower risk of cancer recurrence and mortality (relative risk, 0.77; 95% confidence interval, 0.63 to 0.95; P = .02). Conclusion Higher artificially sweetened beverage consumption may be associated with significantly reduced cancer recurrence and death in patients with stage III colon cancer. This association may be mediated by substitution for sugar-sweetened alternatives. Further studies are needed to confirm these findings.

Original language	English (US)
Article number	e0199244
Journal	PloS one
Volume	13
Issue number	7
DOIs	https://doi.org/10.1371/journal.pone.0199244
State	Published - Jul 2018

Funding

Research reported in this publication was supported by the National Cancer Institute of the National Institutes of Health (https://www.cancer. gov) under Award Numbers U10CA180821 and U10CA180882 (to the Alliance for Clinical Trials in Oncology), U10CA180820 (to ECOG-ACRIN), and U10A80888 (to SWOG). Additional support from the National Cancer Institute was provided under U10CA060138 (to University of California San Francisco and AV), U10CA180791 (to Memorial Sloan-Kettering Cancer Center), U10CA180836 (to the University of Chicago Comprehensive Cancer Center and HK), U10CA180867 (to Dana-Farber/ Partners Cancer Care), and UG1CA189858 (to Southeast Clinical Oncology Research Consortium, Inc., [SCOR]). Support for the trial was also provided by Pharmacia & Upjohn Company, now Pfizer Oncology (https://www.pfizer.com/science/ oncology-cancer). CF, KN, and JM are supported in part by grants from the National Cancer Institute (K07 CA148894, R01 CA118553, R01 CA149222, R01 CA169141, and P50 CA127003). DN is supported in part by grant R01 CA149222 from the National Cancer Institute. SO is supported by R35 CA197735 from the National Cancer Institute. KW is supported by a grant from the American Institute for Cancer Research (http://www.aicr.org). EZ is supported by the National Institutes of Health National Heart, Lung, and Blood Institute grant T32HL125232 (https://www.nhlbi.nih.gov). Support was also provided by the National Cancer Institute P30 Cancer Center Support Grant (CCSG) (P30 CA008748) to Memorial Sloan-Kettering. The National Institutes for Health participated in the design of the study as well as review and approval of the manuscript. Non-federal funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors would like to thank Sherry Breaux, Alliance Publications Operations Manager, and Dr. William Barry, Alliance faculty statistician, for their review of this manuscript prior to publication.

ASJC Scopus subject areas

General Agricultural and Biological Sciences
General
General Biochemistry, Genetics and Molecular Biology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1371/journal.pone.0199244

Cite this

Guercio, B. J., Zhang, S., Niedzwiecki, D., Li, Y., Babic, A., Morales-Oyarvide, V., Saltz, L. B., Mayer, R. J., Mowat, R. B., Whittom, R., Hantel, A., Benson, A., Atienza, D., Messino, M., Kindler, H., Venook, A., Ogino, S., Zoltick, E. S., Stampfer, M., ... Fuchs, C. S. (2018). Associations of artificially sweetened beverage intake with disease recurrence and mortality in stage III colon cancer: Results from CALGB 89803 (Alliance). PloS one, 13(7), Article e0199244. https://doi.org/10.1371/journal.pone.0199244

@article{a4fa8c0c730c4a1b8bbeae72f17ebeb3,

title = "Associations of artificially sweetened beverage intake with disease recurrence and mortality in stage III colon cancer: Results from CALGB 89803 (Alliance)",

abstract = "Purpose Observational studies have demonstrated increased colon cancer recurrence and mortality in states of excess energy balance, as denoted by factors including sedentary lifestyle, diabetes, increased dietary glycemic load, and increased intake of sugar-sweetened beverages. Nonetheless, the relation between artificially sweetened beverages, a popular alternative for sugar-sweetened beverages, and colon cancer recurrence and survival is unknown. Methods We analyzed data from 1,018 patients with stage III colon cancer who prospectively reported dietary intake during and after chemotherapy while enrolled in a National Cancer Institute-sponsored trial of adjuvant chemotherapy. Using Cox proportional hazards regressions, we assessed associations of artificially sweetened beverage intake with cancer recurrence and mortality. Results Patients consuming one or more 12-ounce servings of artificially sweetened beverages per day experienced an adjusted hazard ratio for cancer recurrence or mortality of 0.54 (95\% confidence interval, 0.36 to 0.80) when compared to those who largely abstained (Ptrend = .004). Similarly, increasing artificially sweetened beverage intake was also associated with a significant improvement in both recurrence-free survival (Ptrend = .005) and overall survival (Ptrend = .02). Substitution models demonstrated that replacing a 12-ounce serving of a sugar-sweetened beverage with an isovolumetric serving of an artificially sweetened beverage per day was associated with a 23\% lower risk of cancer recurrence and mortality (relative risk, 0.77; 95\% confidence interval, 0.63 to 0.95; P = .02). Conclusion Higher artificially sweetened beverage consumption may be associated with significantly reduced cancer recurrence and death in patients with stage III colon cancer. This association may be mediated by substitution for sugar-sweetened alternatives. Further studies are needed to confirm these findings.",

author = "Guercio, \{Brendan J.\} and Sui Zhang and Donna Niedzwiecki and Yanping Li and Ana Babic and Vicente Morales-Oyarvide and Saltz, \{Leonard B.\} and Mayer, \{Robert J.\} and Mowat, \{Rex B.\} and Renaud Whittom and Alexander Hantel and Al Benson and Daniel Atienza and Michael Messino and Hedy Kindler and Alan Venook and Shuji Ogino and Zoltick, \{Emilie S.\} and Meir Stampfer and Kimmie Ng and Kana Wu and Willett, \{Walter C.\} and Giovannucci, \{Edward L.\} and Meyerhardt, \{Jeffrey A.\} and Fuchs, \{Charles S.\}",

note = "Funding Information: Research reported in this publication was supported by the National Cancer Institute of the National Institutes of Health (https://www.cancer. gov) under Award Numbers U10CA180821 and U10CA180882 (to the Alliance for Clinical Trials in Oncology), U10CA180820 (to ECOG-ACRIN), and U10A80888 (to SWOG). Additional support from the National Cancer Institute was provided under U10CA060138 (to University of California San Francisco and AV), U10CA180791 (to Memorial Sloan-Kettering Cancer Center), U10CA180836 (to the University of Chicago Comprehensive Cancer Center and HK), U10CA180867 (to Dana-Farber/ Partners Cancer Care), and UG1CA189858 (to Southeast Clinical Oncology Research Consortium, Inc., [SCOR]). Support for the trial was also provided by Pharmacia \& Upjohn Company, now Pfizer Oncology (https://www.pfizer.com/science/ oncology-cancer). CF, KN, and JM are supported in part by grants from the National Cancer Institute (K07 CA148894, R01 CA118553, R01 CA149222, R01 CA169141, and P50 CA127003). DN is supported in part by grant R01 CA149222 from the National Cancer Institute. SO is supported by R35 CA197735 from the National Cancer Institute. KW is supported by a grant from the American Institute for Cancer Research (http://www.aicr.org). EZ is supported by the National Institutes of Health National Heart, Lung, and Blood Institute grant T32HL125232 (https://www.nhlbi.nih.gov). Support was also provided by the National Cancer Institute P30 Cancer Center Support Grant (CCSG) (P30 CA008748) to Memorial Sloan-Kettering. The National Institutes for Health participated in the design of the study as well as review and approval of the manuscript. Non-federal funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors would like to thank Sherry Breaux, Alliance Publications Operations Manager, and Dr. William Barry, Alliance faculty statistician, for their review of this manuscript prior to publication. Publisher Copyright: {\textcopyright} 2018 Guercio et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.",

year = "2018",

month = jul,

doi = "10.1371/journal.pone.0199244",

language = "English (US)",

volume = "13",

journal = "PloS one",

issn = "1932-6203",

publisher = "Public Library of Science",

number = "7",

}

Guercio, BJ, Zhang, S, Niedzwiecki, D, Li, Y, Babic, A, Morales-Oyarvide, V, Saltz, LB, Mayer, RJ, Mowat, RB, Whittom, R, Hantel, A, Benson, A, Atienza, D, Messino, M, Kindler, H, Venook, A, Ogino, S, Zoltick, ES, Stampfer, M, Ng, K, Wu, K, Willett, WC, Giovannucci, EL, Meyerhardt, JA & Fuchs, CS 2018, 'Associations of artificially sweetened beverage intake with disease recurrence and mortality in stage III colon cancer: Results from CALGB 89803 (Alliance)', PloS one, vol. 13, no. 7, e0199244. https://doi.org/10.1371/journal.pone.0199244

TY - JOUR

T1 - Associations of artificially sweetened beverage intake with disease recurrence and mortality in stage III colon cancer

T2 - Results from CALGB 89803 (Alliance)

AU - Guercio, Brendan J.

AU - Zhang, Sui

AU - Niedzwiecki, Donna

AU - Li, Yanping

AU - Babic, Ana

AU - Morales-Oyarvide, Vicente

AU - Saltz, Leonard B.

AU - Mayer, Robert J.

AU - Mowat, Rex B.

AU - Whittom, Renaud

AU - Hantel, Alexander

AU - Benson, Al

AU - Atienza, Daniel

AU - Messino, Michael

AU - Kindler, Hedy

AU - Venook, Alan

AU - Ogino, Shuji

AU - Zoltick, Emilie S.

AU - Stampfer, Meir

AU - Ng, Kimmie

AU - Wu, Kana

AU - Willett, Walter C.

AU - Giovannucci, Edward L.

AU - Meyerhardt, Jeffrey A.

AU - Fuchs, Charles S.

N1 - Funding Information: Research reported in this publication was supported by the National Cancer Institute of the National Institutes of Health (https://www.cancer. gov) under Award Numbers U10CA180821 and U10CA180882 (to the Alliance for Clinical Trials in Oncology), U10CA180820 (to ECOG-ACRIN), and U10A80888 (to SWOG). Additional support from the National Cancer Institute was provided under U10CA060138 (to University of California San Francisco and AV), U10CA180791 (to Memorial Sloan-Kettering Cancer Center), U10CA180836 (to the University of Chicago Comprehensive Cancer Center and HK), U10CA180867 (to Dana-Farber/ Partners Cancer Care), and UG1CA189858 (to Southeast Clinical Oncology Research Consortium, Inc., [SCOR]). Support for the trial was also provided by Pharmacia & Upjohn Company, now Pfizer Oncology (https://www.pfizer.com/science/ oncology-cancer). CF, KN, and JM are supported in part by grants from the National Cancer Institute (K07 CA148894, R01 CA118553, R01 CA149222, R01 CA169141, and P50 CA127003). DN is supported in part by grant R01 CA149222 from the National Cancer Institute. SO is supported by R35 CA197735 from the National Cancer Institute. KW is supported by a grant from the American Institute for Cancer Research (http://www.aicr.org). EZ is supported by the National Institutes of Health National Heart, Lung, and Blood Institute grant T32HL125232 (https://www.nhlbi.nih.gov). Support was also provided by the National Cancer Institute P30 Cancer Center Support Grant (CCSG) (P30 CA008748) to Memorial Sloan-Kettering. The National Institutes for Health participated in the design of the study as well as review and approval of the manuscript. Non-federal funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors would like to thank Sherry Breaux, Alliance Publications Operations Manager, and Dr. William Barry, Alliance faculty statistician, for their review of this manuscript prior to publication. Publisher Copyright: © 2018 Guercio et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

PY - 2018/7

Y1 - 2018/7

N2 - Purpose Observational studies have demonstrated increased colon cancer recurrence and mortality in states of excess energy balance, as denoted by factors including sedentary lifestyle, diabetes, increased dietary glycemic load, and increased intake of sugar-sweetened beverages. Nonetheless, the relation between artificially sweetened beverages, a popular alternative for sugar-sweetened beverages, and colon cancer recurrence and survival is unknown. Methods We analyzed data from 1,018 patients with stage III colon cancer who prospectively reported dietary intake during and after chemotherapy while enrolled in a National Cancer Institute-sponsored trial of adjuvant chemotherapy. Using Cox proportional hazards regressions, we assessed associations of artificially sweetened beverage intake with cancer recurrence and mortality. Results Patients consuming one or more 12-ounce servings of artificially sweetened beverages per day experienced an adjusted hazard ratio for cancer recurrence or mortality of 0.54 (95% confidence interval, 0.36 to 0.80) when compared to those who largely abstained (Ptrend = .004). Similarly, increasing artificially sweetened beverage intake was also associated with a significant improvement in both recurrence-free survival (Ptrend = .005) and overall survival (Ptrend = .02). Substitution models demonstrated that replacing a 12-ounce serving of a sugar-sweetened beverage with an isovolumetric serving of an artificially sweetened beverage per day was associated with a 23% lower risk of cancer recurrence and mortality (relative risk, 0.77; 95% confidence interval, 0.63 to 0.95; P = .02). Conclusion Higher artificially sweetened beverage consumption may be associated with significantly reduced cancer recurrence and death in patients with stage III colon cancer. This association may be mediated by substitution for sugar-sweetened alternatives. Further studies are needed to confirm these findings.

AB - Purpose Observational studies have demonstrated increased colon cancer recurrence and mortality in states of excess energy balance, as denoted by factors including sedentary lifestyle, diabetes, increased dietary glycemic load, and increased intake of sugar-sweetened beverages. Nonetheless, the relation between artificially sweetened beverages, a popular alternative for sugar-sweetened beverages, and colon cancer recurrence and survival is unknown. Methods We analyzed data from 1,018 patients with stage III colon cancer who prospectively reported dietary intake during and after chemotherapy while enrolled in a National Cancer Institute-sponsored trial of adjuvant chemotherapy. Using Cox proportional hazards regressions, we assessed associations of artificially sweetened beverage intake with cancer recurrence and mortality. Results Patients consuming one or more 12-ounce servings of artificially sweetened beverages per day experienced an adjusted hazard ratio for cancer recurrence or mortality of 0.54 (95% confidence interval, 0.36 to 0.80) when compared to those who largely abstained (Ptrend = .004). Similarly, increasing artificially sweetened beverage intake was also associated with a significant improvement in both recurrence-free survival (Ptrend = .005) and overall survival (Ptrend = .02). Substitution models demonstrated that replacing a 12-ounce serving of a sugar-sweetened beverage with an isovolumetric serving of an artificially sweetened beverage per day was associated with a 23% lower risk of cancer recurrence and mortality (relative risk, 0.77; 95% confidence interval, 0.63 to 0.95; P = .02). Conclusion Higher artificially sweetened beverage consumption may be associated with significantly reduced cancer recurrence and death in patients with stage III colon cancer. This association may be mediated by substitution for sugar-sweetened alternatives. Further studies are needed to confirm these findings.

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U2 - 10.1371/journal.pone.0199244

DO - 10.1371/journal.pone.0199244

M3 - Article

C2 - 30024889

AN - SCOPUS:85050524526

SN - 1932-6203

VL - 13

JO - PloS one

JF - PloS one

IS - 7

M1 - e0199244

ER -

Associations of artificially sweetened beverage intake with disease recurrence and mortality in stage III colon cancer: Results from CALGB 89803 (Alliance)

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UN SDGs

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