Skip to main content
Top
Published in: BMC Infectious Diseases 1/2021

Open Access 01-12-2021 | Obesity | Research

Impact of visceral fat on the prognosis of coronavirus disease 2019: an observational cohort study

Authors: Hiroaki Ogata, Masahiro Mori, Yujiro Jingushi, Hiroshi Matsuzaki, Katsuyuki Katahira, Akiko Ishimatsu, Aimi Enokizu-Ogawa, Kazuhito Taguchi, Atsushi Moriwaki, Makoto Yoshida

Published in: BMC Infectious Diseases | Issue 1/2021

Login to get access

Abstract

Background

Clarification of the risk factors for coronavirus disease 2019 (COVID-19) severity is strongly warranted for global health. Recent studies have indicated that elevated body mass index (BMI) is associated with unfavorable progression of COVID-19. This is assumed to be due to excessive deposition of visceral adipose tissue (VAT); however, the evidence investigating the association between intra-abdominal fat and COVID-19 prognosis is sparse. We therefore investigated whether measuring the amount of intra-abdominal fat is useful to predict the prognosis of COVID-19.

Methods

The present study enrolled 53 consecutive cases of COVID-19 patients aged ≥ 20 years with chest computed tomography (CT) scans. The VAT area, total adipose tissue (TAT) area, and VAT/TAT ratio were estimated using axial CT images at the level of the upper pole of the right kidney. Severe COVID-19 was defined as death or acute respiratory failure demanding oxygen at ≥ 6 L per minute, a high-flow nasal cannula, or mechanical ventilation. The association of VAT/TAT with the incidence of progression to a severe state was estimated as a hazard ratio (HR) using Cox regression analysis. To compare the prediction ability for COVID-19 disease progression between BMI and VAT/TAT, the area under the receiver operating characteristic curve (AUC) of each was assessed.

Results

A total of 15 cases (28.3% of the whole study subjects) progressed to severe stages. The incidence of developing severe COVID-19 increased significantly with VAT/TAT (HR per 1% increase = 1.040 (95% CI 1.008–1.074), P = 0.01). After adjustment for potential confounders, the positive association of VAT/TAT with COVID-19 aggravation remained significant (multivariable-adjusted HR = 1.055 (95% CI 1.000–1.112) per 1% increase, P = 0.049). The predictive ability of VAT/TAT for COVID-19 becoming severe was significantly better than that of BMI (AUC of 0.73 for VAT/TAT and 0.50 for BMI; P = 0.0495 for the difference).

Conclusions

A higher ratio of VAT/TAT was an independent risk factor for disease progression among COVID-19 patients. VAT/TAT was superior to BMI in predicting COVID-19 morbidity. COVID-19 patients with high VAT/TAT levels should be carefully observed as high-risk individuals for morbidity and mortality.
Appendix
Available only for authorised users
Literature
1.
go back to reference Guan W, Ni Z, Hu Y, Liang W, Ou C, He J, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med. 2020;382:1708–20.CrossRef Guan W, Ni Z, Hu Y, Liang W, Ou C, He J, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med. 2020;382:1708–20.CrossRef
2.
go back to reference Lipsitch M, Swerdlow DL, Finelli L. Defining the epidemiology of Covid-19—studies needed. N Engl J Med. 2020;382:1194–6.CrossRef Lipsitch M, Swerdlow DL, Finelli L. Defining the epidemiology of Covid-19—studies needed. N Engl J Med. 2020;382:1194–6.CrossRef
4.
go back to reference Fontana L, Eagon JC, Trujillo ME, Scherer PE, Klein S. Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes. 2007;56:1010–3.CrossRef Fontana L, Eagon JC, Trujillo ME, Scherer PE, Klein S. Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes. 2007;56:1010–3.CrossRef
5.
go back to reference Anderson MR, Geleris J, Anderson DR, Zucker J, Nobel YR, Freedberg D, et al. Body mass index and risk for intubation or death in SARS-CoV-2 infection: a retrospective cohort study. Ann Intern Med. 2020;173:782–90.CrossRef Anderson MR, Geleris J, Anderson DR, Zucker J, Nobel YR, Freedberg D, et al. Body mass index and risk for intubation or death in SARS-CoV-2 infection: a retrospective cohort study. Ann Intern Med. 2020;173:782–90.CrossRef
6.
go back to reference Kim TS, Roslin M, Wang JJ, Kane J, Hirsch JS, Kim EJ. BMI as a risk factor for clinical outcomes in patients hospitalized with COVID-19 in New York. Obesity. 2021;29:279–84.CrossRef Kim TS, Roslin M, Wang JJ, Kane J, Hirsch JS, Kim EJ. BMI as a risk factor for clinical outcomes in patients hospitalized with COVID-19 in New York. Obesity. 2021;29:279–84.CrossRef
9.
go back to reference Leidman E, Duca LM, Omura JD, Proia K, Stephens JW, Sauber-Schatz EK. COVID-19 trends among persons aged 0–24 years—United States, March 1–December 12, 2020. MMWR Morb Mortal Wkly Rep. 2021;70:88–94.CrossRef Leidman E, Duca LM, Omura JD, Proia K, Stephens JW, Sauber-Schatz EK. COVID-19 trends among persons aged 0–24 years—United States, March 1–December 12, 2020. MMWR Morb Mortal Wkly Rep. 2021;70:88–94.CrossRef
11.
go back to reference DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics. 1988;44:837–45.CrossRef DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics. 1988;44:837–45.CrossRef
12.
go back to reference Watanabe M, Caruso D, Tuccinardi D, Risi R, Zerunian M, Polici M, et al. Visceral fat shows the strongest association with the need of intensive care in patients with COVID-19. Metab Clin Exp. 2020;111:154319.CrossRef Watanabe M, Caruso D, Tuccinardi D, Risi R, Zerunian M, Polici M, et al. Visceral fat shows the strongest association with the need of intensive care in patients with COVID-19. Metab Clin Exp. 2020;111:154319.CrossRef
13.
go back to reference Battisti S, Pedone C, Napoli N, Russo E, Agnoletti V, Nigra SG, et al. Computed tomography highlights increased visceral adiposity associated with critical illness in COVID-19. Diabetes Care. 2020;43:e129–30.CrossRef Battisti S, Pedone C, Napoli N, Russo E, Agnoletti V, Nigra SG, et al. Computed tomography highlights increased visceral adiposity associated with critical illness in COVID-19. Diabetes Care. 2020;43:e129–30.CrossRef
14.
go back to reference Chandarana H, Dane B, Mikheev A, Taffel MT, Feng Y, Rusinek H. Visceral adipose tissue in patients with COVID-19: risk stratification for severity. Abdom Radiol. 2021;46:818–25.CrossRef Chandarana H, Dane B, Mikheev A, Taffel MT, Feng Y, Rusinek H. Visceral adipose tissue in patients with COVID-19: risk stratification for severity. Abdom Radiol. 2021;46:818–25.CrossRef
15.
go back to reference Pediconi F, Rizzo V, Schiaffino S, Cozzi A, Pepa G, Galati F, et al. Visceral adipose tissue area predicts intensive care unit admission in COVID-19 patients. Obes Res Clin Pract. 2021;15:89–92.CrossRef Pediconi F, Rizzo V, Schiaffino S, Cozzi A, Pepa G, Galati F, et al. Visceral adipose tissue area predicts intensive care unit admission in COVID-19 patients. Obes Res Clin Pract. 2021;15:89–92.CrossRef
16.
go back to reference Xu L, Zhang J, Shen S, Hong X, Zeng X, Yang Y, et al. Association between body composition and frailty in elder inpatients. Clin Interv Aging. 2020;15:313–20.CrossRef Xu L, Zhang J, Shen S, Hong X, Zeng X, Yang Y, et al. Association between body composition and frailty in elder inpatients. Clin Interv Aging. 2020;15:313–20.CrossRef
17.
go back to reference Hoffmann M, Kleine-Weber H, Schroeder S, Krüger N, Herrler T, Erichsen S, et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell. 2020;181:271–80.CrossRef Hoffmann M, Kleine-Weber H, Schroeder S, Krüger N, Herrler T, Erichsen S, et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell. 2020;181:271–80.CrossRef
18.
go back to reference Al Heialy S, Hachim MY, Senok A, Gaudet M, Tayoun AA, Hamoudi R, et al. Regulation of angiotensin-converting enzyme 2 in obesity: implications for COVID-19. Front Physiol. 2020;11:555039.CrossRef Al Heialy S, Hachim MY, Senok A, Gaudet M, Tayoun AA, Hamoudi R, et al. Regulation of angiotensin-converting enzyme 2 in obesity: implications for COVID-19. Front Physiol. 2020;11:555039.CrossRef
19.
go back to reference Gregor MF, Hotamisligil GS. Adipocyte stress: the endoplasmic reticulum and metabolic disease. J Lipid Res. 2007;48:1905–14.CrossRef Gregor MF, Hotamisligil GS. Adipocyte stress: the endoplasmic reticulum and metabolic disease. J Lipid Res. 2007;48:1905–14.CrossRef
20.
go back to reference Ha DP, Van Krieken R, Carlos AJ, Lee AS. The stress-inducible molecular chaperone GRP78 as potential therapeutic target for coronavirus infection. J Infect. 2020;81:478–80.CrossRef Ha DP, Van Krieken R, Carlos AJ, Lee AS. The stress-inducible molecular chaperone GRP78 as potential therapeutic target for coronavirus infection. J Infect. 2020;81:478–80.CrossRef
21.
go back to reference Hudák A, Letoha A, Szilák L, Letoha T. Contribution of syndecans to the cellular entry of SARS-CoV-2. Int J Mol Sci. 2021;22:5336.CrossRef Hudák A, Letoha A, Szilák L, Letoha T. Contribution of syndecans to the cellular entry of SARS-CoV-2. Int J Mol Sci. 2021;22:5336.CrossRef
22.
go back to reference Gordts PLSM, Esko JD. The heparan sulfate proteoglycan grip on hyperlipidemia and atherosclerosis. Matrix Biol. 2018;71–72:262–82.CrossRef Gordts PLSM, Esko JD. The heparan sulfate proteoglycan grip on hyperlipidemia and atherosclerosis. Matrix Biol. 2018;71–72:262–82.CrossRef
23.
go back to reference Cantuti-Castelvetri L, Ojha R, Pedro LD, Djannatian M, Franz J, Kuivanen S, et al. Neuropilin-1 facilitates SARS-CoV-2 cell entry and infectivity. Science. 2020;370:856–60.CrossRef Cantuti-Castelvetri L, Ojha R, Pedro LD, Djannatian M, Franz J, Kuivanen S, et al. Neuropilin-1 facilitates SARS-CoV-2 cell entry and infectivity. Science. 2020;370:856–60.CrossRef
24.
go back to reference Ceccarelli S, Nodale C, Vescarelli E, Pontecorvi P, Manganelli V, Casella G, et al. Neuropilin 1 mediates keratinocyte growth factor signaling in adipose-derived stem cells: potential involvement in adipogenesis. Stem Cells Int. 2018;2018:1075156.CrossRef Ceccarelli S, Nodale C, Vescarelli E, Pontecorvi P, Manganelli V, Casella G, et al. Neuropilin 1 mediates keratinocyte growth factor signaling in adipose-derived stem cells: potential involvement in adipogenesis. Stem Cells Int. 2018;2018:1075156.CrossRef
25.
go back to reference Lecube A, Hernández C, Pelegrí D, Simó R. Factors accounting for high ferritin levels in obesity. Int J Obes. 2008;32:1665–9.CrossRef Lecube A, Hernández C, Pelegrí D, Simó R. Factors accounting for high ferritin levels in obesity. Int J Obes. 2008;32:1665–9.CrossRef
26.
go back to reference Shoenfeld Y. Corona (COVID-19) time musings: our involvement in COVID-19 pathogenesis, diagnosis, treatment and vaccine planning. Autoimmun Rev. 2020;19:102538.CrossRef Shoenfeld Y. Corona (COVID-19) time musings: our involvement in COVID-19 pathogenesis, diagnosis, treatment and vaccine planning. Autoimmun Rev. 2020;19:102538.CrossRef
27.
go back to reference Martin SS, Qasim A, Reilly MP. Leptin resistance: a possible interface of inflammation and metabolism in obesity-related cardiovascular disease. J Am Coll Cardiol. 2008;52:1201–10.CrossRef Martin SS, Qasim A, Reilly MP. Leptin resistance: a possible interface of inflammation and metabolism in obesity-related cardiovascular disease. J Am Coll Cardiol. 2008;52:1201–10.CrossRef
28.
go back to reference Morange PE, Lijnen HR, Alessi MC, Kopp F, Collen D, Juhan-Vague I. Influence of PAI-1 on adipose tissue growth and metabolic parameters in a murine model of diet-induced obesity. Arterioscler Thromb Vasc Biol. 2000;20:1150–4.CrossRef Morange PE, Lijnen HR, Alessi MC, Kopp F, Collen D, Juhan-Vague I. Influence of PAI-1 on adipose tissue growth and metabolic parameters in a murine model of diet-induced obesity. Arterioscler Thromb Vasc Biol. 2000;20:1150–4.CrossRef
29.
go back to reference Nascimento GP, de Melo HA, Faria SS, Santos I, Kobinger GP, Magalhães KG. Hypercoagulopathy and adipose tissue exacerbated inflammation may explain higher mortality in COVID-19 patients with obesity. Front Endocrinol. 2020;11:530.CrossRef Nascimento GP, de Melo HA, Faria SS, Santos I, Kobinger GP, Magalhães KG. Hypercoagulopathy and adipose tissue exacerbated inflammation may explain higher mortality in COVID-19 patients with obesity. Front Endocrinol. 2020;11:530.CrossRef
30.
go back to reference Li C, Li J, He F, Li K, Li X, Zhang Y. Matrix Gla protein regulates adipogenesis and is serum marker of visceral adiposity. Adipocyte. 2020;9:68–76.CrossRef Li C, Li J, He F, Li K, Li X, Zhang Y. Matrix Gla protein regulates adipogenesis and is serum marker of visceral adiposity. Adipocyte. 2020;9:68–76.CrossRef
31.
go back to reference Morley JE, Vellas B, van Kan GA, Anker SD, Bauer JM, Bernabei R, et al. Frailty consensus: a call to action. J Am Med Dir Assoc. 2013;14:392–7.CrossRef Morley JE, Vellas B, van Kan GA, Anker SD, Bauer JM, Bernabei R, et al. Frailty consensus: a call to action. J Am Med Dir Assoc. 2013;14:392–7.CrossRef
32.
go back to reference Hewitt J, Carter B, Vilches-Moraga A, Quinn TJ, Braude P, Verduri A, et al. The effect of frailty on survival in patients with COVID-19 (COPE): a multicentre, European, observational cohort study. Lancet Public Heal. 2020;5:e444–51.CrossRef Hewitt J, Carter B, Vilches-Moraga A, Quinn TJ, Braude P, Verduri A, et al. The effect of frailty on survival in patients with COVID-19 (COPE): a multicentre, European, observational cohort study. Lancet Public Heal. 2020;5:e444–51.CrossRef
33.
go back to reference Demeulemeester F, de Punder K, van Heijningen M, van Doesburg F. Obesity as a risk factor for severe COVID-19 and complications: a review. Cells. 2021;10:933.CrossRef Demeulemeester F, de Punder K, van Heijningen M, van Doesburg F. Obesity as a risk factor for severe COVID-19 and complications: a review. Cells. 2021;10:933.CrossRef
34.
go back to reference Irlbeck T, Massaro JM, Bamberg F, O’Donnell CJ, Hoffmann U, Fox CS. Association between single-slice measurements of visceral and abdominal subcutaneous adipose tissue with volumetric measurements: the Framingham Heart Study. Int J Obes. 2010;34:781–7.CrossRef Irlbeck T, Massaro JM, Bamberg F, O’Donnell CJ, Hoffmann U, Fox CS. Association between single-slice measurements of visceral and abdominal subcutaneous adipose tissue with volumetric measurements: the Framingham Heart Study. Int J Obes. 2010;34:781–7.CrossRef
35.
go back to reference Idoate F, Cadore EL, Casas-Herrero A, Zambom-Ferraresi F, Marcellán T, de Gordoa AR, et al. Adipose tissue compartments, muscle mass, muscle fat infiltration, and coronary calcium in institutionalized frail nonagenarians. Eur Radiol. 2015;25:2163–75.CrossRef Idoate F, Cadore EL, Casas-Herrero A, Zambom-Ferraresi F, Marcellán T, de Gordoa AR, et al. Adipose tissue compartments, muscle mass, muscle fat infiltration, and coronary calcium in institutionalized frail nonagenarians. Eur Radiol. 2015;25:2163–75.CrossRef
36.
go back to reference Gorber SC, Tremblay M, Moher D, Gorber B. A comparison of direct vs. self-report measures for assessing height, weight and body mass index: a systematic review. Obes Rev. 2007;8:307–26.CrossRef Gorber SC, Tremblay M, Moher D, Gorber B. A comparison of direct vs. self-report measures for assessing height, weight and body mass index: a systematic review. Obes Rev. 2007;8:307–26.CrossRef
Metadata
Title
Impact of visceral fat on the prognosis of coronavirus disease 2019: an observational cohort study
Authors
Hiroaki Ogata
Masahiro Mori
Yujiro Jingushi
Hiroshi Matsuzaki
Katsuyuki Katahira
Akiko Ishimatsu
Aimi Enokizu-Ogawa
Kazuhito Taguchi
Atsushi Moriwaki
Makoto Yoshida
Publication date
01-12-2021
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2021
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-021-06958-z

Other articles of this Issue 1/2021

BMC Infectious Diseases 1/2021 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.