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Diet-derived metabolites and mucus link the gut microbiome to fever after cytotoxic cancer treatment.

ABSTRACT: Not all patients with cancer and severe neutropenia develop fever, and the fecal microbiome may play a role. In a single-center study of patients undergoing hematopoietic cell transplant (n = 119), the fecal microbiome was characterized at onset of severe neutropenia. A total of 63 patients (53%) developed a subsequent fever, and their fecal microbiome displayed increased relative abundances of Akkermansia muciniphila, a species of mucin-degrading bacteria (P = 0.006, corrected for multiple comparisons). Two therapies that induce neutropenia, irradiation and melphalan, similarly expanded A. muciniphila and additionally thinned the colonic mucus layer in mice. Caloric restriction of unirradiated mice also expanded A. muciniphila and thinned the colonic mucus layer. Antibiotic treatment to eradicate A. muciniphila before caloric restriction preserved colonic mucus, whereas A. muciniphila reintroduction restored mucus thinning. Caloric restriction of unirradiated mice raised colonic luminal pH and reduced acetate, propionate, and butyrate. Culturing A. muciniphila in vitro with propionate reduced utilization of mucin as well as of fucose. Treating irradiated mice with an antibiotic targeting A. muciniphila or propionate preserved the mucus layer, suppressed translocation of flagellin, reduced inflammatory cytokines in the colon, and improved thermoregulation. These results suggest that diet, metabolites, and colonic mucus link the microbiome to neutropenic fever and may guide future microbiome-based preventive strategies.

SUBMITTER: Schwabkey ZI

PROVIDER: S-EPMC10028729 | biostudies-literature | 2022 Nov

REPOSITORIES: biostudies-literature

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Diet-derived metabolites and mucus link the gut microbiome to fever after cytotoxic cancer treatment.

Schwabkey Zaker I ZI Wiesnoski Diana H DH Chang Chia-Chi CC Tsai Wen-Bin WB Pham Dung D Ahmed Saira S SS Hayase Tomo T Ortega Turrubiates Miriam R MR El-Himri Rawan K RK Sanchez Christopher A CA Hayase Eiko E Frenk Oquendo Annette C AC Miyama Takahiko T Halsey Taylor M TM Heckel Brooke E BE Brown Alexandria N AN Jin Yimei Y Raybaud Mathilde M Prasad Rishika R Flores Ivonne I McDaniel Lauren L Chapa Valerie V Lorenzi Philip L PL Warmoes Marc O MO Tan Lin L Swennes Alton G AG Fowler Stephanie S Conner Margaret M McHugh Kevin K Graf Tyler T Jensen Vanessa B VB Peterson Christine B CB Do Kim-Anh KA Zhang Liangliang L Shi Yushu Y Wang Yinghong Y Galloway-Pena Jessica R JR Okhuysen Pablo C PC Daniel-MacDougall Carrie R CR Shono Yusuke Y Burgos da Silva Marina M Peled Jonathan U JU van den Brink Marcel R M MRM Ajami Nadim N Wargo Jennifer A JA Reddy Pavan P Valdivia Raphael H RH Davey Lauren L Rondon Gabriela G Srour Samer A SA Mehta Rohtesh S RS Alousi Amin M AM Shpall Elizabeth J EJ Champlin Richard E RE Shelburne Samuel A SA Molldrem Jeffrey J JJ Jamal Mohamed A MA Karmouch Jennifer L JL Jenq Robert R RR

Science translational medicine 20221116 671

Not all patients with cancer and severe neutropenia develop fever, and the fecal microbiome may play a role. In a single-center study of patients undergoing hematopoietic cell transplant (n = 119), the fecal microbiome was characterized at onset of severe neutropenia. A total of 63 patients (53%) developed a subsequent fever, and their fecal microbiome displayed increased relative abundances of Akkermansia muciniphila, a species of mucin-degrading bacteria (P = 0.006, correc ...[more]

PMID: 36383683

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Project description:Both crude protein (CP) and probiotics can modulate the gut microbiome of the host, thus conferring beneficial effects. However, the benefits of low CP diet supplemented with multispecies probiotics on gut microbiome and its metabolites have not been investigated in pigs. Thus, we investigated the combinatory effects of low CP diet supplemented with multispecies probiotics on gut microbiome composition, function, and microbial metabolites in growing pigs. In total, 140 6 week-old piglets (Landrace × Yorkshire × Duroc) were used in this study. The pigs were divided into four groups with a 2 × 2 factorial design based on their diets: normal-level protein diet (16% CP; NP), low-level protein diet (14% CP; LP), NP with multispecies probiotics (NP-P), and LP with multispecies probiotics (LP-P). After the feeding trial, the fecal samples of the pigs were analyzed. The fecal scores were improved by the probiotic supplementation, especially in LP-P group. We also observed a probiotic-mediated alteration in the gut microbiome of pigs. In addition, LP-P group showed higher species richness and diversity compared with other groups. The addition of multispecies probiotics in low CP diet also enhanced gut microbiota metabolites production, such as short-chain fatty acids (SCFAs) and polyamines. Correlation analysis revealed that Oscillospiraceae UCG-002, Eubacterium coprostanoligenes, Lachnospiraceae NK4A136 group, and Muribaculaceae were positively associated with SCFAs; and Prevotella, Eubacterium ruminantium, Catenibacterium, Alloprevotella, Prevotellaceae NK3B31 group, Roseburia, Butyrivibrio, and Dialister were positively correlated with polyamines. Supplementation with multispecies probiotics modulated the function of the gut microbiome by upregulating the pathways for protein digestion and utilization, potentially contributing to enriched metabolite production in the gut. The results of this study demonstrate that supplementation with multispecies probiotics may complement the beneficial effects of low CP levels in pig feed. These findings may help formulate sustainable feeding strategies for swine production.

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Diet-derived metabolites and mucus link the gut microbiome to fever after cytotoxic cancer treatment.

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Diet-derived metabolites and mucus link the gut microbiome to fever after cytotoxic cancer treatment.

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