Role of physical activity in cancer survival and recurrence: A narrative review from relationship evidence to crucial research perspectives
Article Sidebar
Main Article Content
Abstract
Purpose: The benefits of Physical Activity (PA) considered as a major supportive care in cancer patients, on survival, and recurrence risk is largely disseminated in public communication. However, these data must be taken with caution. The main objectives were to review the evidence and limits of studies reported regarding the post-diagnosis PA role on cancer survival and recurrence risk to secondly discuss of research perspectives on PA programs.
Method: The narrative review included all published or ongoing studies in English during the last 20 years related to PA, survival and recurrence risk with a systematic search on main databases.
Results and discussion: The current evidences regarding the PA role on survival and recurrence risk were only based on cohort studies, mainly in breast cancer. The major methodological limits identified as the lack of PA change assessment, PA level assessed largely by self-reported methods and the significant inter- but also intra- variability make the interpretation of data very. Beyond the use of rigorous RCT, the major issue is to develop adapted and personalized interventions to progressively increase PA level overtime in cancer survivors.
Conclusion: Despite the lack of causal relationship between post-diagnosis PA, survival and recurrence risk, the review underlines several interesting research perspectives. The future PA interventions, using innovative tools and integrated to the “real-life” will argued for the potential antitumoral PA role growing in literature.
Article Details
Copyright (c) 2018 Maury J, et al.
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Global Burden of Disease Cancer Collaboration, Fitzmaurice C1, Allen C2, Barber RM2, Barregard L. et al. Global, Regional, and National Cancer Incidence, Mortality, Years of Life Lost, Years Lived With Disability, and Disability-Adjusted Life-years for 32 Cancer Groups, 1990 to 2015: A Systematic Analysis for the Global Burden of Disease Study. JAMA Oncol. 2017; 3: 524-528. Ref.: https://goo.gl/qt1GT9
Lowy DR, Collins FS. Aiming High — Changing the Trajectory for Cancer. N Engl J Med. 2016; 374: 1901–1904. Ref.: https://goo.gl/iom4XT
Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018: Cancer Statistics, 2018. CA Cancer J Clin. 2018; 68: 7–30. Ref.: https://goo.gl/ocDvFd
Courneya KS, Friedenreich CM. Physical exercise and quality of life following cancer diagnosis: A literature review. Ann Behav Med. 1999; 21: 171–179. Ref.: https://goo.gl/apsLpN
Cramp F, Daniel J. Exercise for the management of cancer-related fatigue in adults. Cochrane Database Syst Rev. 2008; CD006145. Ref.: https://goo.gl/DasDop
Mishra SI, Scherer RW, Snyder C, Geigle PM, Berlanstein DR, et al. Exercise interventions on health-related quality of life for people with cancer during active treatment. Clinical Otolaryngology. 2012; CD008465. Ref.: https://goo.gl/DGLyUi
Speck RM, Courneya KS, Mâsse LC, Duval S, Schmitz KH. An update of controlled physical activity trials in cancer survivors: a systematic review and meta-analysis. J Cancer Surviv. 2010; 4: 87–100. Ref.: https://goo.gl/KU9xPT
Fong DY, Ho JW, Hui BP, Lee AM, Macfarlane DJ, et al. Physical activity for cancer survivors: meta-analysis of randomised controlled trials. BMJ. 2012; 344: e70–e70. Ref.: https://goo.gl/wFfLdU
Jones LW, Liang Y, Pituskin EN, Battaglini CL, Scott JM, et al. Effect of Exercise Training on Peak Oxygen Consumption in Patients with Cancer: A Meta-Analysis. Oncologist. 2011; 16: 112–120. Ref.: https://goo.gl/qHWiPM
Strasser B, Steindorf K, Wiskemann J, Ulrich CM. Impact of Resistance Training in Cancer Survivors: A Meta-Analysis. Med Sci Sports Exerc. 2013; 45: 2080–2090. Ref.: https://goo.gl/ZdKaSX
Ballard-Barbash R, Friedenreich CM, Courneya KS, Siddiqi SM, McTiernan A, et al. Physical Activity, Biomarkers, and Disease Outcomes in Cancer Survivors: A Systematic Review. J Natl Cancer Inst. 2012; 104: 815–840. Ref.: https://goo.gl/Y6kkfW
Hojman P. Exercise protects from cancer through regulation of immune function and inflammation. Biochem Soc Trans. 2017; 45: 905–911. Ref.: https://goo.gl/KfXfQT
Löf M1, Bergström K, Weiderpass E. Physical activity and biomarkers in breast cancer survivors: A systematic review. Maturitas. 2012; 73: 134–142. Ref.: https://goo.gl/BeQVRA
Ancellin R, Gaillot-de Saintignon J. Bénéfices de l’activité physique pendant et après cancer : des connaissances scientifiques aux repères pratiques. Oncologie. 2017; 19: 95–107. Ref.: https://goo.gl/Njr7mx
Kohler LN, Garcia DO, Harris RB, Oren E, Roe DJ, et al. Adherence to Diet and Physical Activity Cancer Prevention Guidelines and Cancer Outcomes: A Systematic Review. Cancer Epidemiol Biomarkers Prev. 2016; 25: 1018–1028. Ref.: https://goo.gl/sKFPCE
Stout NL, Baima J, Swisher AK, Winters-Stone KM, Welsh J. A Systematic Review of Exercise Systematic Reviews in the Cancer Literature (2005-2017). PM R. 2017; 9: S347–S384 Ref.: https://goo.gl/JYc7P3
Hojman P, Gehl J, Christensen JF, Pedersen BK. Molecular Mechanisms Linking Exercise to Cancer Prevention and Treatment. Cell Metab. 2018; 27: 10–21. Ref.: https://goo.gl/RQcngm
Moore SC, Lee IM, Weiderpass E, Campbell PT, Sampson JN, et al. Association of Leisure-Time Physical Activity With Risk of 26 Types of Cancer in 1.44 Million Adults. JAMA Intern Med. 2016; 176: 816. Ref.: https://goo.gl/NRjCwU
Rezende LFM, Sá TH, Markozannes G, Rey-López JP, Lee IM, et al. Physical activity and cancer: an umbrella review of the literature including 22 major anatomical sites and 770 000 cancer cases. Br J Sports Med. 2017; 52: 826-833. Ref.: https://goo.gl/xiJCb9
Ormel HL, van der Schoot GGF, Sluiter WJ, Jalving M, Gietema JA, et al. Predictors of adherence to exercise interventions during and after cancer treatment: A systematic review. Psychooncology. 2018; 27: 713–724. Ref.: https://goo.gl/248swz
Benke IN, Leitzmann MF, Behrens G, Schmid D. Physical activity in relation to risk of prostate cancer: a systematic review and meta-analysis. Ann Oncol. 2018; 29: 1154–1179. Ref.: https://goo.gl/Vf37Zn
Kerr J, Anderson C, Lippman SM. Physical activity, sedentary behaviour, diet, and cancer: an update and emerging new evidence. The Lancet Oncol. 2017; 18: e457–e471. Ref.: https://goo.gl/KYe7ch
Lahart IM, Metsios GS, Nevill AM, Carmichael AR. Physical activity for women with breast cancer after adjuvant therapy. Cochrane Database Syst Rev. 2018; CD011292. Ref.: https://goo.gl/p6tHhv
Schmid D, Leitzmann MF. Association between physical activity and mortality among breast cancer and colorectal cancer survivors: a systematic review and meta-analysis. Ann Oncol. 2014; 25: 1293–1311. Ref.: https://goo.gl/MvWPb7
Wu W, Guo F, Ye J, Li Y, Shi D. Pre- and post-diagnosis physical activity is associated with survival benefits of colorectal cancer patients: a systematic review and meta-analysis. Oncotarget. 2016; 7: 52095-52103. Ref.: https://goo.gl/VrtrqL
Bourke L, Homer KE, Thaha MA, Steed L, Rosario DJ, et al. Interventions to improve exercise behaviour in sedentary people living with and beyond cancer: a systematic review. Br J Cancer. 2014; 110: 831–841. Ref.: https://goo.gl/pmF7Kt
Courneya KS, Segal RJ, McKenzie DC, Dong H, Gelmon K, et al. Effects of Exercise during Adjuvant Chemotherapy on Breast Cancer Outcomes: Med Sci Sports Exerc. 2014; 46: 1744–1751. Ref.: https://goo.gl/5iSzPu
Courneya KS, Friedenreich CM, Franco-Villalobos C, Crawford J4, Chua N, et al. Effects of supervised exercise on progression-free survival in lymphoma patients: an exploratory follow-up of the HELP Trial. Cancer Causes & Control. 2015; 26: 269–276. Ref.: https://goo.gl/ipGiWr
Wiskemann J, Kleindienst N, Kuehl R, Dreger P, Schwerdtfeger R, et al. Effects of physical exercise on survival after allogeneic stem cell transplantation: Effects of exercise on survival after transplant. Int J Cancer. 2015; 137: 2749–2756. Ref.: https://goo.gl/2KCGaV
Friedenreich CM, Gregory J, Kopciuk KA, Mackey JR, Courneya KS. Prospective cohort study of lifetime physical activity and breast cancer survival. Int J Cancer. 2009; 124: 1954–1962. Ref.: https://goo.gl/ABV2hp
Holmes MD, Chen WY, Feskanich D, Kroenke CH, Colditz GA. Physical Activity and Survival after Breast Cancer Diagnosis. JAMA. 2005; 293: 2479-2486. Ref.: https://goo.gl/hNEXdM
Meyerhardt JA, Giovannucci EL, Holmes MD, Chan AT, Chan JA, et al. Physical Activity and Survival after Colorectal Cancer Diagnosis. J Clin Oncol. 2006; 24: 3527–3534. Ref.: https://goo.gl/moCiYp
Richman EL, Kenfield SA, Stampfer MJ, Paciorek A, Carroll PR, et al. Physical Activity after Diagnosis and Risk of Prostate Cancer Progression: Data from the Cancer of the Prostate Strategic Urologic Research Endeavor. Cancer Res. 2011; 71: 3889–3895. Ref.: https://goo.gl/bRNhgr
Ibrahim EM, Al-Homaidh A. Physical activity and survival after breast cancer diagnosis: meta-analysis of published studies. Med Oncol. 2011; 28: 753–765. Ref.: https://goo.gl/PYZjca
Je Y, Jeon JY, Giovannucci EL, Meyerhardt JA. Association between physical activity and mortality in colorectal cancer: A meta-analysis of prospective cohort studies: Physical activity and colorectal cancer mortality. Int J Cancer. 2013; 133: 1905–1913. Ref.: https://goo.gl/wV2LLZ
Lahart IM, Metsios GS, Nevill AM, Carmichael AR. Physical activity, risk of death and recurrence in breast cancer survivors: A systematic review and meta-analysis of epidemiological studies. Acta Oncologica. 2015; 54: 635–654. Ref.: https://goo.gl/FqTDsT
Lee CHA, Kong JC, Ismail H, Riedel B, Heriot A. Systematic Review and Meta-analysis of Objective Assessment of Physical Fitness in Patients Undergoing Colorectal Cancer Surgery. Dis Colon Rectum. 2018; 1. Ref.: https://goo.gl/Z2uZ5u
Otto SJ, Korfage IJ, Polinder S, van der Heide A, de Vries E, et al. Association of change in physical activity and body weight with quality of life and mortality in colorectal cancer: a systematic review and meta-analysis. Support Care Cancer. 2015; 23: 1237–1250. Ref.: https://goo.gl/4S2RhS
Soares Falcetta F, de Araújo Vianna Träsel H, de Almeida FK, Rangel Ribeiro Falcetta M, Falavigna M, et al. Effects of physical exercise after treatment of early breast cancer: systematic review and meta-analysis. Breast Cancer Res Treat. 2018; 170: 455–476. Ref.: https://goo.gl/VNMdoX
Zhong S, Jiang T, Ma T, Zhang X, Tang J, et al. Association between physical activity and mortality in breast cancer: a meta-analysis of cohort studies. Eur J Epidemiol. 2014; 29: 391–404. Ref.: https://goo.gl/zccZaa
Cormie P, Zopf EM, Zhang X, Schmitz KH. The Impact of Exercise on Cancer Mortality, Recurrence, and Treatment-Related Adverse Effects. Epidemiol Rev. 2017; 39: 71–92. Ref.: https://goo.gl/STh3Vb
Bertram LA, Stefanick ML, Saquib N, Natarajan L, Patterson RE, et al. Physical activity, additional breast cancer events, and mortality among early-stage breast cancer survivors: findings from the WHEL Study. Cancer Causes Control. 2011; 22: 427–435. Ref.: https://goo.gl/tA5f4N
Matthews CE, Moore SC, George SM, Sampson J, Bowles HR. Improving Self-reports of Active and Sedentary Behaviors in Large Epidemiologic Studies. Exerc Sport Sci Rev. 2012; 40: 118-126. Ref.: https://goo.gl/ZHpMWa
Neilson HK, Robson PJ, Friedenreich CM, Csizmadi I. Estimating activity energy expenditure: how valid are physical activity questionnaires? Am J Clin Nutr. 2008; 87: 279–291. Ref.: https://goo.gl/wkxx7h
Beasley JM, Kwan ML, Chen WY, Weltzien EK, Kroenke CH, et al. Meeting the physical activity guidelines and survival after breast cancer: findings from the after breast cancer pooling project. Breast Cancer Res Treat. 2012; 131: 637–643. Ref.: https://goo.gl/DQNaqk
Holick CN, Newcomb PA, Trentham-Dietz A, Titus-Ernstoff L, Bersch AJ, et al. Physical Activity and Survival after Diagnosis of Invasive Breast Cancer. Cancer Epidemiology Biomarkers & Prevention. 2008; 17: 379–386. Ref.: https://goo.gl/Cx6zyr
Meyerhardt JA, Heseltine D, Niedzwiecki D, Hollis D, Saltz LB, et al. Impact of Physical Activity on Cancer Recurrence and Survival in Patients With Stage III Colon Cancer: Findings From CALGB 89803. J Clin Oncol. 2006; 24: 3535–3541. Ref.: https://goo.gl/sSGf5J
Hoffmann TC, Maher CG, Briffa T, Sherrington C, Bennell K, et al. Prescribing exercise interventions for patients with chronic conditions. CMAJ. 2016; 188: 510–518. Ref.: https://goo.gl/cR2MNz
Persson G, Brorsson A, Ekvall Hansson E, Troein M, Strandberg EL. Physical activity on prescription (PAP) from the general practitioner’s perspective – a qualitative study. BMC Fam Pract. 2013; 14: Ref.: https://goo.gl/7XXgEf
Rock CL, Doyle C, Demark-Wahnefried W, Meyerhardt J, Courneya KS, et al. (2012). Nutrition and physical activity guidelines for cancer survivors. CA Cancer J Clin. 2012; 62: 242–274. Ref.: https://goo.gl/WuSLJ7
Schmitz KH, Courneya KS, Matthews C, Demark-Wahnefried W, Galvão DA, et al. American College of Sports Medicine Roundtable on Exercise Guidelines for Cancer Survivors. Med Sci Sports Exerc. 2010; 42: 1409–1426. Ref.: https://goo.gl/Wk8p4S
Sedentary Behaviour Research Network. Letter to the Editor: Standardized use of the terms “sedentary” and “sedentary behaviours.” Appl Physiol Nutr Metab. 2012; 37: 540–542. Ref.: https://goo.gl/5RsutP
Coups EJ, Ostroff JS. A population-based estimate of the prevalence of behavioral risk factors among adult cancer survivors and noncancer controls. Prev Med. 2005; 40: 702–711. Ref.: https://goo.gl/qBH9jG
Mowls DS, Brame LS, Martinez SA, Beebe LA. Lifestyle behaviors among US cancer survivors. J Cancer Surviv. 2016; 10: 692–698. Ref.: https://goo.gl/rXAN2e
La vie cinq ans après un diagnostic de cancer. 2018; 364. Ref.: https://goo.gl/p1xTbh
Buffart LM, Galvão DA, Brug J, Chinapaw MJ, Newton RU. Evidence-based physical activity guidelines for cancer survivors: Current guidelines, knowledge gaps and future research directions. Cancer Treat Rev. 2014; 40: 327–340. Ref.: https://goo.gl/1oepk9
Hoffmann TC, Erueti C, Glasziou PP. Poor description of non-pharmacological interventions: analysis of consecutive sample of randomized trials. BMJ. 2013; 347: f3755–f3755. Ref.: https://goo.gl/9TYXJK
Jones LW, Alfano CM. Exercise-oncology research: Past, present, and future. Acta Oncologica. 2013; 52: 195–215. Ref.: https://goo.gl/YKn8Lf
Hudis CA, Jones L. Promoting exercise after a cancer diagnosis: easier said than done. Br J Cancer. 2014; 110: 829–830. Ref.: https://goo.gl/qqqupY
Courneya KS, Segal RJ, Gelmon K, Reid RD, Mackey JR, et al. Predictors of Supervised Exercise Adherence during Breast Cancer Chemotherapy. Med Sci Sports Exerc. 2008; 40: 1180–1187. Ref.: https://goo.gl/tVt4aM
Bluethmann SM, Vernon SW, Gabriel KP, Murphy CC, Bartholomew LK. Taking the next step: a systematic review and meta-analysis of physical activity and behavior change interventions in recent post-treatment breast cancer survivors. Breast Cancer Res Treat. 2015; 149: 331–342. Ref.: https://goo.gl/AkLHxd
Clifford BK, Mizrahi D, Sandler CX, Barry BK, Simar D, et al. Barriers and facilitators of exercise experienced by cancer survivors: a mixed methods systematic review. Support Care Cancer. 2018; 26: 685–700. Ref.: https://goo.gl/Z3XDMS
Demark-Wahnefried W, Rogers LQ, Alfano CM, Thomson CA, Courneya KS, et al. Practical clinical interventions for diet, physical activity, and weight control in cancer survivors: Clinical Interventions for Weight Loss, Diet, and Physical Activity. CA Cancer J Clin. 2015; 65: 167–189. Ref.: https://goo.gl/y6nnwC
Goode AD, Lawler SP, Brakenridge CL, Reeves MM, Eakin EG. Telephone, print, and Web-based interventions for physical activity, diet, and weight control among cancer survivors: a systematic review. J Cancer Surviv. 2015; 9: 660–682. Ref.: https://goo.gl/F62f7t
Groen WG, van Harten WH, Vallance JK. Systematic review and meta-analysis of distance-based physical activity interventions for cancer survivors (2013–2018): We still haven’t found what we’re looking for. Cancer Treat Rev. 2018; 69: 188–203. Ref.: https://goo.gl/nRRu78
Wong JN, McAuley E, Trinh L. Physical activity programming and counseling preferences among cancer survivors: a systematic review. Int J Behav Nutr Phys Act. 2018; 15: Ref.: https://goo.gl/N9JLYu
Eakin EG, Hayes SC, Haas MR, Reeves MM, Vardy JL, et al. Healthy Living after Cancer: a dissemination and implementation study evaluating a telephone-delivered healthy lifestyle program for cancer survivors. BMC Cancer. 2015; 15: Ref.: https://goo.gl/NrHyVZ
Liss MA, White M, Natarajan L, Parsons JK. Exercise Decreases and Smoking Increases Bladder Cancer Mortality. Clin Genitourin Cancer. 2017; 15: 391–395. Ref.: https://goo.gl/h2XyVr
Spence RR, Heesch KC, Brown WJ. Colorectal cancer survivors’ exercise experiences and preferences: qualitative findings from an exercise rehabilitation programme immediately after chemotherapy: Exercise rehabilitation study: qualitative findings. Eur J Cancer Care (Engl). 2011; 20: 257–266. Ref.: https://goo.gl/TCfN2o
Arem H, Pfeiffer RM, Engels EA, Alfano CM, Hollenbeck A, et al. Pre- and Postdiagnosis Physical Activity, Television Viewing, and Mortality Among Patients With Colorectal Cancer in the National Institutes of Health–AARP Diet and Health Study. J Clin Oncol. 2015; 33: 180–188. Ref.: https://goo.gl/inrcpK
Baade PD, Meng X, Youl PH, Aitken JF, Dunn J, et al. The Impact of Body Mass Index and Physical Activity on Mortality among Patients with Colorectal Cancer in Queensland, Australia. Cancer Epidemiol Biomarkers Prev. 2011; 20: 1410–1420. Ref.: https://goo.gl/4Ds5Uh
Bonn SE, Sjölander A, Lagerros YT, Wiklund F, Stattin P, et al. Physical Activity and Survival among Men Diagnosed with Prostate Cancer. Cancer Epidemiol Biomarkers Prev. 2015; 24: 57–64. Ref.: https://goo.gl/EUsoRh
Bradshaw PT, Ibrahim JG, Khankari N, Cleveland RJ, Abrahamson PE, et al. Post-diagnosis physical activity and survival after breast cancer diagnosis: the Long Island Breast Cancer Study. Breast Cancer Res Treat. 2014; 145: 735–742. Ref.: https://goo.gl/8WobnQ
Campbell PT, Patel AV, Newton CC, Jacobs EJ, Gapstur SM. Associations of Recreational Physical Activity and Leisure Time Spent Sitting with Colorectal Cancer Survival. J Clin Oncol. 2013; 31: 876–885. Ref.: https://goo.gl/uuiKYz
Chen X, Lu W, Zheng W, Gu K, Matthews CE, et al. Exercise after Diagnosis of Breast Cancer in Association with Survival. Cancer Prev Res (Phila). 2011; 4: 1409–1418. Ref.: https://goo.gl/Rf25Tv
de Glas NA, Fontein DB, Bastiaannet E, Pijpe A, De Craen AJ, et al. Physical activity and survival of postmenopausal, hormone receptor-positive breast cancer patients: Results of the Tamoxifen Exemestane Adjuvant Multicenter Lifestyle study: Physical Activity in Breast Cancer. Cancer. 2014; 120: 2847–2854. Ref.: https://goo.gl/5ZcUsJ
Friedenreich CM, Wang Q, Neilson HK, Kopciuk KA, McGregor SE, et al. Physical Activity and Survival After Prostate Cancer. Eur Urol. 2016; 70: 576–585. Ref.: https://goo.gl/2YE3u8
Hellmann SS, Thygesen LC, Tolstrup JS, Grønbaek M. Modifiable risk factors and survival in women diagnosed with primary breast cancer: results from a prospective cohort study. Eur J Cancer Prev. 2010; 19: 366–373. Ref.: https://goo.gl/xXVNqg
Irwin ML, McTiernan A, Manson JE, Thomson CA, Sternfeld B. et al. Physical Activity and Survival in Postmenopausal Women with Breast Cancer: Results from the Women’s Health Initiative. Irwin ML1, McTiernan A, Manson JE, Thomson CA, Sternfeld B. 2011; 4: 522–529. Ref.: https://goo.gl/U38mPY
Kenfield SA, Stampfer MJ, Giovannucci E, Chan JM. Physical Activity and Survival After Prostate Cancer Diagnosis in the Health Professionals Follow-Up Study. J Clin Oncol. 2011; 29: 726–732. Ref.: https://goo.gl/r326eN
Meyerhardt JA, Giovannucci EL, Ogino S, Kirkner GJ, Chan AT. et al. Physical Activity and Male Colorectal Cancer Survival. Arch Intern Med. 2011; 169: 2102. Ref.: https://goo.gl/jd9tba
Nechuta S, Chen WY, Cai H, Poole EM, Kwan ML, et al. A pooled analysis of post-diagnosis lifestyle factors in association with late estrogen-receptor-positive breast cancer prognosis. Int J Cancer. 2016; 138: 2088–2097. https://goo.gl/yXc1QL
Schmid D, Behrens G, Arem H, Hart C, Herr W, et al. Pre- and post-diagnosis physical activity, television viewing, and mortality among hematologic cancer survivors. PLOS ONE. 2018; 13: e0192078. Ref.: https://goo.gl/PCD8uC
Sternfeld B, Weltzien E, Quesenberry CP Jr, Castillo AL, Kwan M, et al. Physical Activity and Risk of Recurrence and Mortality in Breast Cancer Survivors: Findings from the LACE Study. Cancer Epidemiol Biomarkers Prev. 2009; 18: 87–95. Ref.: https://goo.gl/4eVv2B
Wang Y, Jacobs EJ, Gapstur SM, Maliniak ML, Gansler T, et al. Recreational Physical Activity in Relation to Prostate Cancer–specific Mortality Among Men with Nonmetastatic Prostate Cancer. Eur Urol. 2017; 72: 931–939. Ref.: https://goo.gl/nL1kD7
Williams PT. Significantly greater reduction in breast cancer mortality from post-diagnosis running than walking: Post-diagnosis exercise vs breast cancer mortality. Int J Cancer. 2014; 135: 1195–1202. Ref.: https://goo.gl/zRmgNj