Influence of a Low-Carbohydrate High-Fat Diet on Peritoneal Inflammation, Cancer-Associated Lymphocytes, and Survival in a Murine Carcinomatous Peritonitis Model.
cytokines < research and diseases
immunosuppression
inflammation
lipids < nutrition
low-carbohydrate high-fat diet
oncology < research and diseases
peritoneal cancer
regulatory T cell
survival
Journal
JPEN. Journal of parenteral and enteral nutrition
ISSN: 1941-2444
Titre abrégé: JPEN J Parenter Enteral Nutr
Pays: United States
ID NLM: 7804134
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
revised:
08
08
2020
received:
29
06
2020
accepted:
19
08
2020
pubmed:
24
8
2020
medline:
3
11
2021
entrez:
24
8
2020
Statut:
ppublish
Résumé
Low-carbohydrate high-fat diets (LCHFDs) are thought to be beneficial for metabolic support in patients with advanced cancer. However, whether LCHFDs affect the progression of carcinomatous peritonitis (CP) remains unclear. Our study examined the influence of a lard-based LCHFD on host immunity and survival in a murine CP model. Mice were fed either a normal diet (ND) or an LCHFD ad libitum. On day 7, Panc02 cancer cells were inoculated intraperitoneally. Mice were killed on days 7, 21, and 35, and cytokine levels in the peritoneal fluid, as well as the number and phenotypes of peritoneal, splenic, and tumor-infiltrating lymphocytes were measured. Survival studies were performed with both ad libitum and isocaloric feeding in other sets of mice. The levels of all cytokines significantly increased in the LCHFD group compared with those in the ND group on day 21. The tumor necrosis factor α and interleukin-10 levels were higher in the LCHFD group than in the ND group on day 35. In the LCHFD group, the regulatory T-cell (Treg) number was significantly higher in the peritoneal cavity and tumor. The survival times were worse in the LCHFD group than in the ND group. The ad libitum, lard-based LCHFD feeding of CP mice increases the peritoneal cytokine levels, which may reduce splenic, anticancer lymphocytes and increase the number of Tregs in the peritoneal cavity and tumor. The detrimental effects of LCHFD are linked to dietary composition rather than overfeeding.
Sections du résumé
BACKGROUND
Low-carbohydrate high-fat diets (LCHFDs) are thought to be beneficial for metabolic support in patients with advanced cancer. However, whether LCHFDs affect the progression of carcinomatous peritonitis (CP) remains unclear. Our study examined the influence of a lard-based LCHFD on host immunity and survival in a murine CP model.
METHODS
Mice were fed either a normal diet (ND) or an LCHFD ad libitum. On day 7, Panc02 cancer cells were inoculated intraperitoneally. Mice were killed on days 7, 21, and 35, and cytokine levels in the peritoneal fluid, as well as the number and phenotypes of peritoneal, splenic, and tumor-infiltrating lymphocytes were measured. Survival studies were performed with both ad libitum and isocaloric feeding in other sets of mice.
RESULTS
The levels of all cytokines significantly increased in the LCHFD group compared with those in the ND group on day 21. The tumor necrosis factor α and interleukin-10 levels were higher in the LCHFD group than in the ND group on day 35. In the LCHFD group, the regulatory T-cell (Treg) number was significantly higher in the peritoneal cavity and tumor. The survival times were worse in the LCHFD group than in the ND group.
CONCLUSION
The ad libitum, lard-based LCHFD feeding of CP mice increases the peritoneal cytokine levels, which may reduce splenic, anticancer lymphocytes and increase the number of Tregs in the peritoneal cavity and tumor. The detrimental effects of LCHFD are linked to dietary composition rather than overfeeding.
Substances chimiques
Carbohydrates
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1293-1301Informations de copyright
© 2020 American Society for Parenteral and Enteral Nutrition.
Références
Caro MMM, Laviano A, Pichard C. Nutritional intervention and quality of life in adult oncology patients. Clinical Nutrition. 2007;26(3):289-301.
Soldati L, Di Renzo L, Jirillo E, Ascierto PA, Marincola FM, De Lorenzo A. The influence of diet on anti-cancer immune responsiveness. J Transl Med. 2018;16(1):75.
Balstad TR, Solheim TS, Strasser F, Kaasa S, Bye A. Dietary treatment of weight loss in patients with advanced cancer and cachexia: a systematic literature review. Crit Rev Oncol Hematol. 2014;91(2):210-221.
Wallengren O, Bosaeus I, Lundholm K. Dietary energy density, inflammation and energy balance in palliative care cancer patients. Clin Nutr. 2013;32(1):88-92.
Arends J, Bachmann P, Baracos V, et al. ESPEN guidelines on nutrition in cancer patients. Clin Nutr. 2017;36(1):11-48.
Turati F, Galeone C, Augustin LSA, La Vecchia C. Glycemic index, glycemic load and cancer risk: an updated meta-analysis. Nutrients. 2019;11(10):2342.
Heiden MGV, Cantley LC, Thompson CB. Understanding the Warburg Effect: the metabolic requirements of cell proliferation. Science. 2009;324(5930):1029-1033.
Korber J, Pricelius S, Heidrich M, Muller MJ. Increased lipid utilization in weight losing and weight stable cancer patients with normal body weight. Eur J Clin Nutr. 1999;53(9):740-745.
Trinchieri G. Cancer and inflammation: an old intuition with rapidly evolving new concepts. Annu Rev Immunol. 2012;30(1):677-706.
Caer C, Rouault C, Le Roy T, et al. Immune cell-derived cytokines contribute to obesity-related inflammation, fibrogenesis and metabolic deregulation in human adipose tissue. Sci Rep. 2017;7(1):3000.
Zitvogel L, Pietrocola F, Kroemer G. Nutrition, inflammation and cancer. Nat Immunol. 2017;18(8):843-850.
Grivennikov SI, Greten FR, Karin M. Immunity, inflammation, and cancer. Cell. 2010;140(6):883-899.
Cho HJ, Kwon GT, Park H, et al. A high-fat diet containing lard accelerates prostate cancer progression and reduces survival rate in mice: possible contribution of adipose tissue-derived cytokines. Nutrients. 2015;7(4):2539-2561.
Park H, Kim M, Kwon GT, et al. A high-fat diet increases angiogenesis, solid tumor growth, and lung metastasis of CT26 colon cancer cells in obesity-resistant BALB/c mice. Mol Carcinog. 2012;51(11):869-880.
Thomassen I, Lemmens VE, Nienhuijs SW, Luyer MD, Klaver YL, de Hingh IH. Incidence, prognosis, and possible treatment strategies of peritoneal carcinomatosis of pancreatic origin: a population-based study. Pancreas. 2013;42(1):72-75.
van Baal J, van Noorden CJF, Nieuwland R, et al. Development of peritoneal carcinomatosis in epithelial ovarian cancer: a review. J Histochem Cytochem. 2018;66(2):67-83.
Vassos N, Piso P. Metastatic colorectal cancer to the peritoneum: current treatment options. Curr Treat Options Oncol. 2018;19(10):49.
Shrihari TG. Dual role of inflammatory mediators in cancer. Ecancermedicalscience. 2017;11:721.
Vykhovanets EV, Shankar E, Vykhovanets OV, Shukla S, Gupta S. High-fat diet increases NF-kappaB signaling in the prostate of reporter mice. Prostate. 2011;71(2):147-156.
Teng KT, Chang CY, Chang LF, Nesaretnam K. Modulation of obesity-induced inflammation by dietary fats: mechanisms and clinical evidence. Nutr J. 2014;13(1):12.
Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer. 2009;9(11):798-809.
Lippitz BE. Cytokine patterns in patients with cancer: a systematic review. Lancet Oncol. 2013;14(6):e218-228.
Meza-Perez S, Randall TD. Immunological functions of the omentum. Trends Immunol. 2017;38(7):526-536.
Higashijima J, Shimada M, Chikakiyo M, et al. Effect of splenectomy on antitumor immune system in mice. Anticancer Res. 2009;29(1):385-393.
Hotta Y, Kasuya H, Bustos I, et al. Curative effect of HF10 on liver and peritoneal metastasis mediated by host antitumor immunity. Oncolytic Virother. 2017;6:31-38.
Street SE, Cretney E, Smyth MJ. Perforin and interferon-gamma activities independently control tumor initiation, growth, and metastasis. Blood. 2001;97(1):192-197.
Wang B, Sun J, Ma YH, Wu GR, Shi YH, Le GW. Increased oxidative stress and the apoptosis of regulatory T cells in obese mice but not resistant mice in response to a high-fat diet. Cell Immunol. 2014;288(1-2):39-46.
Deng G. Tumor-infiltrating regulatory T cells: origins and features. Am J Clin Exp Immunol. 2018;7(5):81-87.
Oft M. IL-10: master switch from tumor-promoting inflammation to antitumor immunity. Cancer Immunol Res. 2014;2(3):194-199.
Shevchenko I, Karakhanova S, Soltek S, et al. Low-dose gemcitabine depletes regulatory T cells and improves survival in the orthotopic Panc02 model of pancreatic cancer. Int J Cancer. 2013;133(1):98-107.
Landskron J, Helland O, Torgersen KM, et al. Activated regulatory and memory T-cells accumulate in malignant ascites from ovarian carcinoma patients. Cancer Immunol Immunother. 2015;64(3):337-347.
Michalek RD, Gerriets VA, Jacobs SR, et al. Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J Immunol. 2011;186(6):3299-3303.
Pacella I, Piconese S. immunometabolic checkpoints of Treg dynamics: adaptation to microenvironmental opportunities and challenges. Front Immunol. 2019;10:1889.
Khodadadi S, Sobhani N, Mirshekar S, et al. tumor cells growth and survival time with the ketogenic diet in animal models: a systematic review. Int J Prev Med. 2017;8:35.