Dynamics of hepatic steatosis resolution and changes in gut microbiome with weight loss in nonalcoholic fatty liver disease

Jaideep Behari; Lisa Graham; Renwei Wang; Claudiu Schirda; Amir A. Borhani; Barbara A. Methé; Kelvin Li; Alison Morris; Hung N. Luu; Sabrina Palmieri; Jian Min Yuan

doi:10.1002/osp4.476

Dynamics of hepatic steatosis resolution and changes in gut microbiome with weight loss in nonalcoholic fatty liver disease

Jaideep Behari^*, Lisa Graham, Renwei Wang, Claudiu Schirda, Amir A. Borhani, Barbara A. Methé, Kelvin Li, Alison Morris, Hung N. Luu, Sabrina Palmieri, Jian Min Yuan

^*Corresponding author for this work

Radiology

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Abstract

Background: Weight loss is recommended as the primary treatment for nonalcoholic fatty liver disease (NAFLD). However, the magnitude and velocity of hepatic steatosis resolution with weight loss is unclear, making it difficult to counsel patients seeking weight loss for treatment of NAFLD. The aim of this study was to determine the rate of hepatic steatosis improvement and stool microbiome changes associated with rapid diet-induced weight loss in NAFLD. Methods: Fourteen NAFLD patients (mean ± standard deviation, body mass index [BMI] 36.4 ± 4 kg/m²) enrolled in a 12-week meal replacement program underwent frequent measurement of Fibroscan-controlled attenuation parameter (CAP). Magnetic resonance imaging (MRI-Dixon method) for hepatic fat quantitation and stool microbiome analysis (16S rRNA gene sequencing) were completed in 11 subjects at baseline and Week 12. Results: At Week 12, mean (95% confidence interval) weight loss was −13.4 (−15.2, −11.5)% and CAP score −26.6 (−35.6, −17.6)% (both Ps < 0.001). CAP scores changed at a rate of −4.9 dB/m/kg (−30.1 dB/m per unit BMI) in Weeks 1–4 and −0.6 dB/m/kg (−2.4 dB/m per unit BMI) in Weeks 8–12. MRI-determined hepatic fat fraction decreased by −74.1% (p < 0.001) at a rate of −0.51%/kg (−3.19% per unit BMI), with complete steatosis resolution in 90% patients. BMI change was associated with decreased stool microbial diversity (coefficient = 0.17; Shannon Index), increased abundance of Prevotella_9 (Bacteroidetes; coefficient = 0.96) and decreased abundance of Phascolarctobacterium (Firmicutes; coefficient = −0.42) (both Ps < 0.05). Conclusions: Diet-induced intensive weight loss is associated with rapid improvement and complete resolution of hepatic steatosis and decreased stool microbial diversity. These findings highlight the dynamic nature of hepatic fat and may help clinicians to develop evidence-based treatment goals for patients with NAFLD and obesity who undertake weight loss interventions. Further research is warranted to understand the effects of intensive weight loss and gut microbiome changes on long-term NAFLD resolution.

Original language	English (US)
Pages (from-to)	217-225
Number of pages	9
Journal	Obesity Science and Practice
Volume	7
Issue number	2
DOIs	https://doi.org/10.1002/osp4.476
State	Published - Apr 2021

Keywords

liver disease
microbiome
obesity
weight loss

ASJC Scopus subject areas

Endocrinology, Diabetes and Metabolism
Nutrition and Dietetics

UN SDGs

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

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10.1002/osp4.476

Cite this

@article{5a967e56a99e4a7493e45fe15efb9e60,

title = "Dynamics of hepatic steatosis resolution and changes in gut microbiome with weight loss in nonalcoholic fatty liver disease",

abstract = "Background: Weight loss is recommended as the primary treatment for nonalcoholic fatty liver disease (NAFLD). However, the magnitude and velocity of hepatic steatosis resolution with weight loss is unclear, making it difficult to counsel patients seeking weight loss for treatment of NAFLD. The aim of this study was to determine the rate of hepatic steatosis improvement and stool microbiome changes associated with rapid diet-induced weight loss in NAFLD. Methods: Fourteen NAFLD patients (mean ± standard deviation, body mass index [BMI] 36.4 ± 4 kg/m2) enrolled in a 12-week meal replacement program underwent frequent measurement of Fibroscan-controlled attenuation parameter (CAP). Magnetic resonance imaging (MRI-Dixon method) for hepatic fat quantitation and stool microbiome analysis (16S rRNA gene sequencing) were completed in 11 subjects at baseline and Week 12. Results: At Week 12, mean (95% confidence interval) weight loss was −13.4 (−15.2, −11.5)% and CAP score −26.6 (−35.6, −17.6)% (both Ps < 0.001). CAP scores changed at a rate of −4.9 dB/m/kg (−30.1 dB/m per unit BMI) in Weeks 1–4 and −0.6 dB/m/kg (−2.4 dB/m per unit BMI) in Weeks 8–12. MRI-determined hepatic fat fraction decreased by −74.1% (p < 0.001) at a rate of −0.51%/kg (−3.19% per unit BMI), with complete steatosis resolution in 90% patients. BMI change was associated with decreased stool microbial diversity (coefficient = 0.17; Shannon Index), increased abundance of Prevotella_9 (Bacteroidetes; coefficient = 0.96) and decreased abundance of Phascolarctobacterium (Firmicutes; coefficient = −0.42) (both Ps < 0.05). Conclusions: Diet-induced intensive weight loss is associated with rapid improvement and complete resolution of hepatic steatosis and decreased stool microbial diversity. These findings highlight the dynamic nature of hepatic fat and may help clinicians to develop evidence-based treatment goals for patients with NAFLD and obesity who undertake weight loss interventions. Further research is warranted to understand the effects of intensive weight loss and gut microbiome changes on long-term NAFLD resolution.",

keywords = "liver disease, microbiome, obesity, weight loss",

author = "Jaideep Behari and Lisa Graham and Renwei Wang and Claudiu Schirda and Borhani, {Amir A.} and Meth{\'e}, {Barbara A.} and Kelvin Li and Alison Morris and Luu, {Hung N.} and Sabrina Palmieri and Yuan, {Jian Min}",

note = "Funding Information: The authors would like to thank all the study participants. We also acknowledge the generous support of the Pittsburgh Liver Research Center Pilot and Feasibility Grant Program for this study. This study was funded by a pilot grant from the Pittsburgh Liver Research Institute, which is supported by the NIH/NIDDK Digestive Disease Research Core Center grant P30DK120531. Publisher Copyright: {\textcopyright} 2021 The Authors. Obesity Science & Practice published by World Obesity and The Obesity Society and John Wiley & Sons Ltd.",

year = "2021",

month = apr,

doi = "10.1002/osp4.476",

language = "English (US)",

volume = "7",

pages = "217--225",

journal = "Obesity Science and Practice",

issn = "2055-2238",

publisher = "Wiley-Blackwell",

number = "2",

}

TY - JOUR

T1 - Dynamics of hepatic steatosis resolution and changes in gut microbiome with weight loss in nonalcoholic fatty liver disease

AU - Behari, Jaideep

AU - Graham, Lisa

AU - Wang, Renwei

AU - Schirda, Claudiu

AU - Borhani, Amir A.

AU - Methé, Barbara A.

AU - Li, Kelvin

AU - Morris, Alison

AU - Luu, Hung N.

AU - Palmieri, Sabrina

AU - Yuan, Jian Min

N1 - Funding Information: The authors would like to thank all the study participants. We also acknowledge the generous support of the Pittsburgh Liver Research Center Pilot and Feasibility Grant Program for this study. This study was funded by a pilot grant from the Pittsburgh Liver Research Institute, which is supported by the NIH/NIDDK Digestive Disease Research Core Center grant P30DK120531. Publisher Copyright: © 2021 The Authors. Obesity Science & Practice published by World Obesity and The Obesity Society and John Wiley & Sons Ltd.

PY - 2021/4

Y1 - 2021/4

N2 - Background: Weight loss is recommended as the primary treatment for nonalcoholic fatty liver disease (NAFLD). However, the magnitude and velocity of hepatic steatosis resolution with weight loss is unclear, making it difficult to counsel patients seeking weight loss for treatment of NAFLD. The aim of this study was to determine the rate of hepatic steatosis improvement and stool microbiome changes associated with rapid diet-induced weight loss in NAFLD. Methods: Fourteen NAFLD patients (mean ± standard deviation, body mass index [BMI] 36.4 ± 4 kg/m2) enrolled in a 12-week meal replacement program underwent frequent measurement of Fibroscan-controlled attenuation parameter (CAP). Magnetic resonance imaging (MRI-Dixon method) for hepatic fat quantitation and stool microbiome analysis (16S rRNA gene sequencing) were completed in 11 subjects at baseline and Week 12. Results: At Week 12, mean (95% confidence interval) weight loss was −13.4 (−15.2, −11.5)% and CAP score −26.6 (−35.6, −17.6)% (both Ps < 0.001). CAP scores changed at a rate of −4.9 dB/m/kg (−30.1 dB/m per unit BMI) in Weeks 1–4 and −0.6 dB/m/kg (−2.4 dB/m per unit BMI) in Weeks 8–12. MRI-determined hepatic fat fraction decreased by −74.1% (p < 0.001) at a rate of −0.51%/kg (−3.19% per unit BMI), with complete steatosis resolution in 90% patients. BMI change was associated with decreased stool microbial diversity (coefficient = 0.17; Shannon Index), increased abundance of Prevotella_9 (Bacteroidetes; coefficient = 0.96) and decreased abundance of Phascolarctobacterium (Firmicutes; coefficient = −0.42) (both Ps < 0.05). Conclusions: Diet-induced intensive weight loss is associated with rapid improvement and complete resolution of hepatic steatosis and decreased stool microbial diversity. These findings highlight the dynamic nature of hepatic fat and may help clinicians to develop evidence-based treatment goals for patients with NAFLD and obesity who undertake weight loss interventions. Further research is warranted to understand the effects of intensive weight loss and gut microbiome changes on long-term NAFLD resolution.

AB - Background: Weight loss is recommended as the primary treatment for nonalcoholic fatty liver disease (NAFLD). However, the magnitude and velocity of hepatic steatosis resolution with weight loss is unclear, making it difficult to counsel patients seeking weight loss for treatment of NAFLD. The aim of this study was to determine the rate of hepatic steatosis improvement and stool microbiome changes associated with rapid diet-induced weight loss in NAFLD. Methods: Fourteen NAFLD patients (mean ± standard deviation, body mass index [BMI] 36.4 ± 4 kg/m2) enrolled in a 12-week meal replacement program underwent frequent measurement of Fibroscan-controlled attenuation parameter (CAP). Magnetic resonance imaging (MRI-Dixon method) for hepatic fat quantitation and stool microbiome analysis (16S rRNA gene sequencing) were completed in 11 subjects at baseline and Week 12. Results: At Week 12, mean (95% confidence interval) weight loss was −13.4 (−15.2, −11.5)% and CAP score −26.6 (−35.6, −17.6)% (both Ps < 0.001). CAP scores changed at a rate of −4.9 dB/m/kg (−30.1 dB/m per unit BMI) in Weeks 1–4 and −0.6 dB/m/kg (−2.4 dB/m per unit BMI) in Weeks 8–12. MRI-determined hepatic fat fraction decreased by −74.1% (p < 0.001) at a rate of −0.51%/kg (−3.19% per unit BMI), with complete steatosis resolution in 90% patients. BMI change was associated with decreased stool microbial diversity (coefficient = 0.17; Shannon Index), increased abundance of Prevotella_9 (Bacteroidetes; coefficient = 0.96) and decreased abundance of Phascolarctobacterium (Firmicutes; coefficient = −0.42) (both Ps < 0.05). Conclusions: Diet-induced intensive weight loss is associated with rapid improvement and complete resolution of hepatic steatosis and decreased stool microbial diversity. These findings highlight the dynamic nature of hepatic fat and may help clinicians to develop evidence-based treatment goals for patients with NAFLD and obesity who undertake weight loss interventions. Further research is warranted to understand the effects of intensive weight loss and gut microbiome changes on long-term NAFLD resolution.

KW - liver disease

KW - microbiome

KW - obesity

KW - weight loss

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UR - http://www.scopus.com/inward/citedby.url?scp=85099013139&partnerID=8YFLogxK

U2 - 10.1002/osp4.476

DO - 10.1002/osp4.476

M3 - Article

C2 - 33841891

AN - SCOPUS:85099013139

SN - 2055-2238

VL - 7

SP - 217

EP - 225

JO - Obesity Science and Practice

JF - Obesity Science and Practice

IS - 2

ER -

Dynamics of hepatic steatosis resolution and changes in gut microbiome with weight loss in nonalcoholic fatty liver disease

Abstract

Keywords

ASJC Scopus subject areas

UN SDGs

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