Sarcopenia, sarcopenic obesity, myosteatosis as factors of poor prognosis in gastrointestinal tract tumors: review

Cover Page

Cite item

Full Text

Abstract

Over the past decade, there has been a noticeable increase in the number of publications devoted to the analysis of body composition in the treatment of gastrointestinal malignancies. Sarcopenia (skeletal muscle depletion), sarcopenic obesity and myosteatosis are shown to have a negative impact on the results of surgical and chemotherapeutic treatment of patients with gastrointestinal tumors. The review presents in detail data on clinical value of sarcopenia, sarcopenic obesity and myosteatosis along with methodological aspects of body composition analysis. Different cut-offs and diagnostic criteria exist between “Western” and “Eastern” patient populations which makes any comparison or meta-analysis not possible right now. The review presents data from Russian and foreign studies on the influence of body composition on postoperative outcomes and survival in patients with gastrointestinal tumors. The article also discusses the influence of body composition on dose-limiting toxicity of chemotherapy. We aimed at raising awareness of clinicians regarding the high prevalence of cancer cachexia and, precisely, sarcopenia, sarcopenic obesity and myosteatosis in patients with GI tract tumors. Deeper understanding of these syndromes is the key to developing measures for prevention as well as correcting the treatment of patients with gastrointestinal tumors.

About the authors

Tatyana S. Dikova

Sechenov First Moscow State Medical University (Sechenov University)

Email: dikovatatyanasergeevna@gmail.com
SPIN-code: 7597-3600

Student

Russian Federation, Moscow

Alina Y. Zatsepina

Sechenov First Moscow State Medical University (Sechenov University)

Email: zatsepina.alina@gmail.com
SPIN-code: 8495-8418

Student

Russian Federation, Moscow

Denis S. Fedorinov

Russian Medical Academy of Continuous Professional Education

Email: Deni_fe@mail.com
SPIN-code: 1079-8460

Senior Laboratory Assistant

Russian Federation, Moscow

Vladimir K. Lyadov

Russian Medical Academy of Continuous Professional Education; Novokuznetsk State Institute for Postgraduate Medical Education – branch of Russian Medical Academy of Continuous Professional Education; City Clinical Oncological Hospital №1

Author for correspondence.
Email: vlyadov@gmail.com
ORCID iD: 0000-0002-7281-3591
SPIN-code: 5385-7889

D. Sci. (Med.), Russian Medical Academy of Continuous Professional Education, Novokuznetsk State Institute for Postgraduate Medical Education – Branch of Russian Medical Academy of Continuous Professional Education, City Clinical Oncology Hospital №1

Russian Federation, Moscow; Novokuznetsk; Moscow

References

  1. Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68 (6): 394–424. Erratum: CA Cancer J Clin. 2020; 70 (4): 313.
  2. Каприн А.Д., Старинский В.В., Петрова Г.В. Злокачественные новообразования в России в 2018 году (заболеваемость и смертность). М.: МНИОИ им. П.А. Герцена – филиал ФГБУ «НМИЦ радиологии» Минздрава России, 2019 [Kaprin AD, Starinskiy VV, Petrova GV. Malignant tumors of Russia in 2018 (morbidity and mortality). Moscow: Herzen Moscow Scientific and Research Oncological Institute, 2019 (in Russian)].
  3. Prado CM, Lieffers JR, McCargar LJ, et al. Prevalence and clinical implications of sarcopenic obesity in patients with solid tumours of the respiratory and gastrointestinal tracts: a population-based study. Lancet Oncol 2008; 9 (7): 629–35.
  4. Cespedes Feliciano EM, Chen WY, Lee V, et al. Body Composition, Adherence to Anthracycline and Taxane-Based Chemotherapy, and Survival After Nonmetastatic Breast Cancer. JAMA Oncol 2020; 6 (2): 264–70.
  5. Peterson SJ, Mozer M. Differentiating Sarcopenia and Cachexia Among Patients With Cancer. Nutr Clin Pract 2017; 32 (1): 30–9.
  6. Sadeghi M, Keshavarz-Fathi M, Baracos V, et al. Cancer cachexia: Diagnosis, assessment, and treatment. Crit Rev Oncol Hematol 2018; 127: 91–104.
  7. Fearon K, Strasser F, Anker SD, et al. Definition and classification of cancer cachexia: an international consensus. Lancet Oncol 2011; 12 (5): 489–95.
  8. Blum D, Stene GB, Solheim TS, et al. Validation of the Consensus-Definition for cancer cachexia and evaluation of a classification model – a study based on data from an international multicenter project (EPCRC-CSA). Ann Oncol 2014; 25: 1635–42.
  9. Cruz-Jentoft AJ, Bahat G, Bauer J, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019; 48 (1): 16–31.
  10. Obesity and overweight. Available at: http://www.who.int/en/news-room/fact-sheets/detail/obesity-and-overweight. Accessed: 15.06.2020.
  11. Zhang WT, Lin J, Chen WS, et al. Sarcopenic Obesity Is Associated with Severe Postoperative Complications in Gastric Cancer Patients Undergoing Gastrectomy: a Prospective Study. J Gastrointest Surg 2018; 22 (11): 1861–9.
  12. Hopkins JJ, Reif RL, Bigam DL, et al. The Impact of Muscle and Adipose Tissue on Long-term Survival in Patients With Stage I to III Colorectal Cancer. Dis Colon Rectum 2019; 62 (5): 549–60.
  13. Dodds RM, Syddall HE, Cooper R, et al. Grip strength across the life course: normative data from twelve British studies. PLoS One 2014; 9: e113637.
  14. Cesari M, Kritchevsky SB, Newman AB, et al. Added value of physical performance measures in predicting adverse health-related events: results from the Health, Aging And Body Composition Study. J Am Geriatr Soc 2009; 57: 251–9.
  15. Maggio M, Ceda GP, Ticinesi A, et al. Instrumental and Non-Instrumental Evaluation of 4-Meter Walking Speed in Older Individuals. PLoS One 2016; 11 (4): e0153583.
  16. Mourtzakis M, Prado CMM, Lieffers JR, et al. A practical and precise approach to quantification of body composition in cancer patients using computed tomography images acquired during routine care. Appl Physiol Nutr Metab 2008; 33 (5): 997–1006.
  17. Касаткина Е.А., Лядов В.К., Мершина Е.А., и др. Методы лучевой диагностики в оценке состава тела человека. Вестник рентгенологии и радиологии. 2013; 2: 59–64 [Kasatkina EA, Lyadov VK, Mershina EA, et al. Radiodiagnostic methods in the assessment of human body composition. Vestnik rentgenologii i radiologii. 2013; 2: 59–64 (in Russian)].
  18. Wu CH, Chang MC, Lyadov VK, et al. Comparing Western and Eastern criteria for sarcopenia and their association with survival in patients with pancreatic cancer. Clin Nutr 2019; 38 (2): 862–9.
  19. Auyeung TW, Lee SW, Leung J, et al. Age-associated decline of muscle mass, grip strength and gait speed: a 4-year longitudinal study of 3018 community-dwelling older Chinese. Geriatr Gerontol Int 2014; 14 Suppl. 1: 76–84.
  20. Chen LK, Liu LK, Woo J, et al. Sarcopenia in Asia: consensus report of the Asian Working Group for Sarcopenia. J Am Med Dir Assoc 2014; 15 (2): 95–101.
  21. Miljkovic I, Zmuda JM. Epidemiology of myosteatosis. Curr Opin Clin Nutr Metab Care 2010; 13: 260–4.
  22. Malietzis G, Johns N, Al-Hassi HO, et al. Low muscularity and myosteatosis is related to the host systemic inflammatory response in patients undergoing surgery for colorectal cancer. Ann Surg 2016; 263 (2): 320–5.
  23. Correa-de-Araujo R, Addison O, Miljkovic I, et al. Myosteatosis in the Context of Skeletal Muscle Function Deficit: An Interdisciplinary Workshop at the National Institute on Aging. Front Physiol 2020; 11: 963.
  24. Gabiatti CTB, Martins MCL, Miyazaki DL, et al. Myosteatosis in a systemic inflammation-dependent manner predicts favorable survival outcomes in locally advanced esophageal cancer. Cancer Med 2019; 8 (16): 6967–76.
  25. Sueda T, Takahasi H, Nishimura J, et al. Impact of Low Muscularity and Myosteatosis on Long-term Outcome After Curative Colorectal Cancer Surgery: A Propensity Score-Matched Analysis. Dis Colon Rectum 2018; 61 (3): v364–74.
  26. Aro R, Mäkäräinen-Uhlbäck E, Ämmälä N, et al. The impact of sarcopenia and myosteatosis on postoperative outcomes and 5-year survival in curatively operated colorectal cancer patients – A retrospective register study. Eur J Surg Oncol 2020; 46 (9): 1656–62.
  27. Srpcic M, Jordan T, Popuri K, et al. Sarcopenia and myosteatosis at presentation adversely affect survival after esophagectomy for esophageal cancer. Radiol Oncol 2020; 54 (2): 237–46.
  28. Stretch C, Aubin JM, Mickiewicz B, et al. Sarcopenia and myosteatosis are accompanied by distinct biological profiles in patients with pancreatic and periampullary adenocarcinomas. PLoS One. 2018; 13 (5): e0196235.
  29. van Dijk DPJ, Bakers FCH, Sanduleanu S, et al. Myosteatosis predicts survival after surgery for periampullary cancer: a novel method using MRI. HPB (Oxford) 2018; 20 (8): 715–20.
  30. Pamoukdjian F, Bouillet T, Lévy V, et al. Prevalence and predictive value of pre-therapeutic sarcopenia in cancer patients: A systematic review. Clin Nutr 2018; 37 (4): 1101–13.
  31. Ida S, Watanabe M, Yoshida N, et al. Sarcopenia is a predictor of postoperative respiratory complications in patients with esophageal cancer. Ann Surg Oncol 2015; 22 (13): 4432e7.
  32. Nishigori T, Okabe H, Tanaka E, et al. Sarcopenia as a predictor of pulmonary complications after esophagectomy for thoracic esophageal cancer. J Surg Oncol 2016; 113 (6): 678e84.
  33. Wang SL, Zhuang CL, Huang DD, et al. Sarcopenia Adversely Impacts Postoperative Clinical Outcomes Following Gastrectomy in Patients with Gastric Cancer: A Prospective Study. Ann Surg Oncol 2016; 23 (2): 556–64.
  34. Huang DD, Wang SL, Zhuang CL, et al. Sarcopenia, as defined by low muscle mass, strength and physical performance, predicts complications after surgery for colorectal cancer. Colorectal Dis 2015; 17 (11): O256–64.
  35. van Vugt JLA, Braam HJ, van Oudheusden TR, et al. Skeletal muscle depletion is associated with severe post-operative complications in patients undergoing cytoreductive surgery with hyperthermic intraperitoneal chemotherapy for peritoneal carcinomatosis of colorectal cancer. Ann Surg Oncol 2015; 22 (11): 3625e31.
  36. Reisinger KW, van Vugt JLA, Tegels JJW, et al. Functional compromise reflected by sarcopenia, frailty and nutritional depletion predicts adverse postoperative outcome after colorectal cancer surgery. Ann Surg 2015; 261: 345–52.
  37. van Vledder MG, Levolger S, Ayez N, et al. Body composition and outcome in patients undergoing resection of colorectal liver metastases. Br J Surg 2012; 99 (4): 550e7.
  38. Harimoto N, Shirabe K, Yamashita Y-I, et al. Sarcopenia as a predictor of prognosis in patients following hepatectomy for hepatocellular carcinoma. Br J Surg 2013; 100 (11): 1523e30.
  39. Voron T, Tselikas L, Pietrasz D, et al. Sarcopenia impacts on short- and long-term results of hepatectomy for hepatocellular carcinoma. Ann Surg 2015; 261 (6): 1173e83.
  40. Levolger S, van Vledder MG, Muslem R, et al. Sarcopenia impairs survival in patients with potentially curable hepatocellular carcinoma. J Surg Oncol 2015; 112 (2): 208e13.
  41. Peng P, Hyder O, Firoozmand A, et al. Impact of sarcopenia on outcomes following resection of pancreatic adenocarcinoma. J Gastrointest Surg 2012; 16 (8): 1478–86.
  42. Buettner S, Wagner D, Kim Y, et al. Inclusion of sarcopenia outperforms the modified frailty index in predicting 1-year mortality among 1,326 patients undergoing gastrointestinal surgery for a malignant indication. J Am Coll Surg 2015; 222 (4): 397e407.e2.
  43. Malietzis G, Currie AC, Athanasiou T, et al. Influence of body composition profiles on outcomes following colorectal cancer surgery. BJS 2016; 103: 572–80.
  44. Лядов В.К., Егиев В.Н., Серяков А.П., и др. Саркопения и распределение жировой ткани у пациентов с колоректальным раком. Российский журнал гастроэнтерологии, гепатологии, колопроктологии. 2012; 3: 33–7 [Lyadov VK, Egiev VN, Seryakov АP, et al. Sarkopeniya i raspredelenie zhirovoj tkani u patsientov s kolorektalnim rakom Rossiiskii zhurnal gastroenterologii, gepatologii, koloproktologii. 2012; 22 (3): 33–7 (In Russian)].
  45. Tegels JJ, van Vugt JL, Reisinger KW, et al. Sarcopenia is highly prevalent in patients under-going surgery for gastric cancer but not associated with worse outcomes. J Surg Oncol 2015; 112 (4): 403–7.
  46. Tan BH, Birdsell LA, Martin L, et al. Sarcopenia in an overweight or obese patient is an adverse prognostic factor in pancreatic cancer. Clin Cancer Res 2009; 15 (22): 6973–9.
  47. Lodewick TM, van Nijnatten TJ, van Dam RM, et al. Are sarcopenia, obesity and sarcopenic obesity predictive of outcome in patients with colorectal liver metastases? HPB (Oxford). 2015; 17 (5): 438–46.
  48. Rodrigues V, Landi F, Castro S, et al. Is sarcopenic obesity an indicator of poor prognosis in gastric cancer surgery? A cohort study in a western population. J Gastrointest Surg 2020. doi: 10.1007/s11605-020-04716-1
  49. Gruber ES, Jomrich G, Tamandl D, et al. Sarcopenia and sarcopenic obesity are independent adverse prognostic factors in resectable pancreatic ductal adenocarcinoma. PLoS One 2019; 14 (5): e0215915.
  50. Caan BJ, Meyerhardt JA, Kroenke CH, et al. Explaining the Obesity Paradox: The Association between Body Composition and Colorectal Cancer Survival (C-SCANS Study). Cancer Epidemiol Biomarkers Prev 2017; 26 (7): 1008–15.
  51. Han JS, Ryu H, Park IJ, et al. Association of Body Composition with Long-Term Survival in Non-metastatic Rectal Cancer Patients. Cancer Res Treat 2020; 52 (2): 563–72.
  52. Aleixo GFP, Shachar SS, Nyrop KA, et al. Myosteatosis and prognosis in cancer: Systematic review and meta-analysis. Crit Rev Oncol Hematol 2020; 145: 102839.
  53. Lee CM, Kang J. Prognostic impact of myosteatosis in patients with colorectal cancer: a systematic review and meta-analysis. J Cachexia Sarcopenia Muscle 2020; 11 (5): 1270–82.
  54. Zhuang CL, Shen X, Huang YY, et al. Myosteatosis predicts prognosis after radical gastrectomy for gastric cancer: A propensity score-matched analysis from a large-scale cohort. Surgery 2019; 166 (3): 297–304.
  55. Rollins KE, Tewari N, Ackner A, et al. The impact of sarcopenia and myosteatosis on outcomes of unresectable pancreatic cancer or distal cholangiocarcinoma. Clin Nutr 2016; 35: 1103–9.
  56. Antoun S, Baracos VE, Birdsell L, et al. Low body mass index and sarcopenia associated with dose-limiting toxicity of sorafenib in patients with renal cell carcinoma. Ann Oncol 2010; 21 (8): 1594–8.
  57. Martin D, von der Grün J, Rödel C, et al. Sarcopenia Is Associated With Hematologic Toxicity During Chemoradiotherapy in Patients With Anal Carcinoma. Front Oncol 2020; 10: 1576.
  58. Palmela C, Velho S, Agostinho L, et al. Body Composition as a Prognostic Factor of Neoadjuvant Chemotherapy Toxicity and Outcome in Patients with Locally Advanced Gastric Cancer. J Gastric Cancer 2017; 17 (1): 74–87.
  59. Dijksterhuis WPM, Pruijt MJ, van der Woude SO, et al. Association between body composition, survival, and toxicity in advanced esophagogastric cancer patients receiving palliative chemotherapy. J Cachexia Sarcopenia Muscle 2019; 10 (1): 199–206.

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2021 Consilium Medicum

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
 


Согласие на обработку персональных данных с помощью сервиса «Яндекс.Метрика»

1. Я (далее – «Пользователь» или «Субъект персональных данных»), осуществляя использование сайта https://journals.rcsi.science/ (далее – «Сайт»), подтверждая свою полную дееспособность даю согласие на обработку персональных данных с использованием средств автоматизации Оператору - федеральному государственному бюджетному учреждению «Российский центр научной информации» (РЦНИ), далее – «Оператор», расположенному по адресу: 119991, г. Москва, Ленинский просп., д.32А, со следующими условиями.

2. Категории обрабатываемых данных: файлы «cookies» (куки-файлы). Файлы «cookie» – это небольшой текстовый файл, который веб-сервер может хранить в браузере Пользователя. Данные файлы веб-сервер загружает на устройство Пользователя при посещении им Сайта. При каждом следующем посещении Пользователем Сайта «cookie» файлы отправляются на Сайт Оператора. Данные файлы позволяют Сайту распознавать устройство Пользователя. Содержимое такого файла может как относиться, так и не относиться к персональным данным, в зависимости от того, содержит ли такой файл персональные данные или содержит обезличенные технические данные.

3. Цель обработки персональных данных: анализ пользовательской активности с помощью сервиса «Яндекс.Метрика».

4. Категории субъектов персональных данных: все Пользователи Сайта, которые дали согласие на обработку файлов «cookie».

5. Способы обработки: сбор, запись, систематизация, накопление, хранение, уточнение (обновление, изменение), извлечение, использование, передача (доступ, предоставление), блокирование, удаление, уничтожение персональных данных.

6. Срок обработки и хранения: до получения от Субъекта персональных данных требования о прекращении обработки/отзыва согласия.

7. Способ отзыва: заявление об отзыве в письменном виде путём его направления на адрес электронной почты Оператора: info@rcsi.science или путем письменного обращения по юридическому адресу: 119991, г. Москва, Ленинский просп., д.32А

8. Субъект персональных данных вправе запретить своему оборудованию прием этих данных или ограничить прием этих данных. При отказе от получения таких данных или при ограничении приема данных некоторые функции Сайта могут работать некорректно. Субъект персональных данных обязуется сам настроить свое оборудование таким способом, чтобы оно обеспечивало адекватный его желаниям режим работы и уровень защиты данных файлов «cookie», Оператор не предоставляет технологических и правовых консультаций на темы подобного характера.

9. Порядок уничтожения персональных данных при достижении цели их обработки или при наступлении иных законных оснований определяется Оператором в соответствии с законодательством Российской Федерации.

10. Я согласен/согласна квалифицировать в качестве своей простой электронной подписи под настоящим Согласием и под Политикой обработки персональных данных выполнение мною следующего действия на сайте: https://journals.rcsi.science/ нажатие мною на интерфейсе с текстом: «Сайт использует сервис «Яндекс.Метрика» (который использует файлы «cookie») на элемент с текстом «Принять и продолжить».