Skip to main content
Top
Published in: Langenbeck's Archives of Surgery 2/2020

01-03-2020 | Obesity | Original Article

A retrospective case control study identifies peripheral blood mononuclear cell albumin RNA expression as a biomarker for non-alcoholic fatty liver disease

Authors: Xin Chu, Kelsey Karasinski, Sean Donellan, Scott Kaniper, G. Craig Wood, Weixing Shi, Michael A. Edwards, Rohit Soans, Christopher D. Still, Glenn S. Gerhard

Published in: Langenbeck's Archives of Surgery | Issue 2/2020

Login to get access

Abstract

Purpose

Non-alcoholic fatty liver disease (NAFLD) improves after bariatric surgery. The aim of this study was to determine whether peripheral blood mononuclear cell albumin gene expression was related to NAFLD and whether albumin (ALB) and alpha fetoprotein (AFP) expression could be detected in whole blood and visceral adipose tissue.

Methods

Using a retrospective case control study design, RNA isolated from peripheral blood mononuclear cells from patients prior to undergoing bariatric surgery was used for pooled microarray analysis. Quantitative polymerase chain reaction (QPCR) was used to analyze whole blood and visceral adipose tissue. Liver histology was obtained via intra-operative biopsy and clinical data extracted from the electronic health record.

Results

The albumin (ALB) gene was the second most up-regulated found in microarray analysis of peripheral blood mononuclear cell RNA from patients with hepatic lobular inflammation versus normal liver histology. Transcript levels of ALB were significantly different across those with normal (n = 50), steatosis (n = 50), lobular inflammation (n = 50), and peri-sinusoidal fibrosis (n = 50) liver histologies, with lobular inflammation 3.9 times higher than those with normal histology (p < 0.017). Albumin expression levels decreased in 11/13 patients in paired samples obtained prior to and at 1 year after Roux-en-Y gastric bypass surgery. ALB expression could be detected in 23 visceral adipose tissue samples obtained intra-operatively and in 18/19 available paired whole blood samples. No significant correlation was found between ALB expression in visceral adipose tissue and whole blood RNA samples. Alpha fetoprotein expression as a marker of early hepatocytic differentiation was detected in 17/17 available VAT RNA samples, but in only 2/17 whole blood RNA samples.

Conclusion

Albumin RNA expression from blood cells may serve as a biomarker of NAFLD. Albumin and alpha fetoprotein appear to be ubiquitously expressed in visceral adipose tissue in patients with extreme obesity.
Literature
1.
go back to reference Neuschwander-Tetri BA, Caldwell SH (2003) Nonalcoholic steatohepatitis: summary of an AASLD single topic conference. Hepatology. 37(5):1202–1219PubMed Neuschwander-Tetri BA, Caldwell SH (2003) Nonalcoholic steatohepatitis: summary of an AASLD single topic conference. Hepatology. 37(5):1202–1219PubMed
2.
go back to reference Starley BQ, Calcagno CJ, Harrison SA (2010) Nonalcoholic fatty liver disease and hepatocellular carcinoma: a weighty connection. Hepatology. 51(5):1820–1832PubMed Starley BQ, Calcagno CJ, Harrison SA (2010) Nonalcoholic fatty liver disease and hepatocellular carcinoma: a weighty connection. Hepatology. 51(5):1820–1832PubMed
3.
go back to reference Wong RJ, Cheung R, Ahmed A (2014) Nonalcoholic steatohepatitis is the most rapidly growing indication for liver transplantation in patients with hepatocellular carcinoma in the U.S. Hepatology. 59(6):2188–2195PubMed Wong RJ, Cheung R, Ahmed A (2014) Nonalcoholic steatohepatitis is the most rapidly growing indication for liver transplantation in patients with hepatocellular carcinoma in the U.S. Hepatology. 59(6):2188–2195PubMed
4.
go back to reference Udompap P, Kim D, Kim WR (2015) Current and future burden of chronic nonmalignant liver disease. Clin Gastroenterol Hepatol 13(12):2031–2041PubMedPubMedCentral Udompap P, Kim D, Kim WR (2015) Current and future burden of chronic nonmalignant liver disease. Clin Gastroenterol Hepatol 13(12):2031–2041PubMedPubMedCentral
5.
go back to reference Allen RE, Hughes TD, Ng JL, Ortiz RD, Ghantous MA, Bouhali O et al (2013) Mechanisms behind the immediate effects of roux-en-Y gastric bypass surgery on type 2 diabetes. Theor Biol Med Model 10:45PubMedPubMedCentral Allen RE, Hughes TD, Ng JL, Ortiz RD, Ghantous MA, Bouhali O et al (2013) Mechanisms behind the immediate effects of roux-en-Y gastric bypass surgery on type 2 diabetes. Theor Biol Med Model 10:45PubMedPubMedCentral
6.
go back to reference Nguyen KT, Korner J (2014) The sum of many parts: potential mechanisms for improvement in glucose homeostasis after bariatric surgery. Curr Diab Rep 14(5):481PubMedPubMedCentral Nguyen KT, Korner J (2014) The sum of many parts: potential mechanisms for improvement in glucose homeostasis after bariatric surgery. Curr Diab Rep 14(5):481PubMedPubMedCentral
7.
go back to reference Laursen TL, Hagemann CA, Wei C, Kazankov K, Thomsen KL, Knop FK, Grønbæk H (2019) Bariatric surgery in patients with non-alcoholic fatty liver disease - from pathophysiology to clinical effects. World J Hepatol 11(2):138–149PubMedPubMedCentral Laursen TL, Hagemann CA, Wei C, Kazankov K, Thomsen KL, Knop FK, Grønbæk H (2019) Bariatric surgery in patients with non-alcoholic fatty liver disease - from pathophysiology to clinical effects. World J Hepatol 11(2):138–149PubMedPubMedCentral
8.
go back to reference Alizai PH, Wendl J, Roeth AA, Klink CD, Luedde T, Steinhoff I, Neumann UP, Schmeding M, Ulmer F (2015) Functional liver recovery after bariatric surgery--a prospective cohort study with the LiMAx test. Obes Surg 25(11):2047–2053PubMed Alizai PH, Wendl J, Roeth AA, Klink CD, Luedde T, Steinhoff I, Neumann UP, Schmeding M, Ulmer F (2015) Functional liver recovery after bariatric surgery--a prospective cohort study with the LiMAx test. Obes Surg 25(11):2047–2053PubMed
9.
go back to reference Carpino G, Renzi A, Onori P, Gaudio E (2013) Role of hepatic progenitor cells in nonalcoholic fatty liver disease development: cellular cross-talks and molecular networks. Int J Mol Sci 14(10):20112–20130PubMedPubMedCentral Carpino G, Renzi A, Onori P, Gaudio E (2013) Role of hepatic progenitor cells in nonalcoholic fatty liver disease development: cellular cross-talks and molecular networks. Int J Mol Sci 14(10):20112–20130PubMedPubMedCentral
10.
go back to reference Muller C, Petermann D, Pfeffel F, Oesterreicher C, Fugger R (1997) Lack of specificity of albumin-mRNA-positive cells as a marker of circulating hepatoma cells. Hepatology. 25(4):896–899PubMed Muller C, Petermann D, Pfeffel F, Oesterreicher C, Fugger R (1997) Lack of specificity of albumin-mRNA-positive cells as a marker of circulating hepatoma cells. Hepatology. 25(4):896–899PubMed
11.
go back to reference Gaia S, Olivero A, Smedile A, Ruella M, Abate ML, Fadda M, Rolle E, Omedè P, Bondesan P, Passera R, Risso A, Aragno M, Marzano A, Ciancio A, Rizzetto M, Tarella C (2013) Multiple courses of G-CSF in patients with decompensated cirrhosis: consistent mobilization of immature cells expressing hepatocyte markers and exploratory clinical evaluation. Hepatol Int 7(4):1075–1083PubMed Gaia S, Olivero A, Smedile A, Ruella M, Abate ML, Fadda M, Rolle E, Omedè P, Bondesan P, Passera R, Risso A, Aragno M, Marzano A, Ciancio A, Rizzetto M, Tarella C (2013) Multiple courses of G-CSF in patients with decompensated cirrhosis: consistent mobilization of immature cells expressing hepatocyte markers and exploratory clinical evaluation. Hepatol Int 7(4):1075–1083PubMed
12.
go back to reference Ghaedi M, Duan Y, Zern MA, Revzin A (2014) Hepatic differentiation of human embryonic stem cells on growth factor-containing surfaces. J Tissue Eng Regen Med 8(11):886–895PubMed Ghaedi M, Duan Y, Zern MA, Revzin A (2014) Hepatic differentiation of human embryonic stem cells on growth factor-containing surfaces. J Tissue Eng Regen Med 8(11):886–895PubMed
13.
go back to reference Zhang W, Li W, Liu B, Wang P, Li W, Zhang H (2012) Efficient generation of functional hepatocyte-like cells from human fetal hepatic progenitor cells in vitro. J Cell Physiol 227(5):2051–2058PubMed Zhang W, Li W, Liu B, Wang P, Li W, Zhang H (2012) Efficient generation of functional hepatocyte-like cells from human fetal hepatic progenitor cells in vitro. J Cell Physiol 227(5):2051–2058PubMed
14.
go back to reference Wood GC, Chu X, Manney C, Strodel W, Petrick A, Gabrielsen J et al (2012) An electronic health record-enabled obesity database. BMC Med Inform Decis Mak 12(1):45PubMedPubMedCentral Wood GC, Chu X, Manney C, Strodel W, Petrick A, Gabrielsen J et al (2012) An electronic health record-enabled obesity database. BMC Med Inform Decis Mak 12(1):45PubMedPubMedCentral
15.
go back to reference Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW et al (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 41(6):1313–1321PubMed Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW et al (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 41(6):1313–1321PubMed
16.
go back to reference Bogoslovsky T, Wang D, Maric D, Scattergood-Keepper L, Spatz M, Auh S, et al (2013) Cryopreservation and enumeration of human endothelialprogenitor and endothelial cells for clinical trials. J Blood Disord Transfus 4(5): 158 Bogoslovsky T, Wang D, Maric D, Scattergood-Keepper L, Spatz M, Auh S, et al (2013) Cryopreservation and enumeration of human endothelialprogenitor and endothelial cells for clinical trials. J Blood Disord Transfus 4(5): 158
17.
go back to reference Chu X, Jin Q, Chen H, Wood GC, Petrick A, Strodel W, Gabrielsen J, Benotti P, Mirshahi T, Carey DJ, Still CD, DiStefano J, Gerhard GS (2018) CCL20 is up-regulated in non-alcoholic fatty liver disease fibrosis and is produced by hepatic stellate cells in response to fatty acid loading. J Transl Med 16(1):108PubMedPubMedCentral Chu X, Jin Q, Chen H, Wood GC, Petrick A, Strodel W, Gabrielsen J, Benotti P, Mirshahi T, Carey DJ, Still CD, DiStefano J, Gerhard GS (2018) CCL20 is up-regulated in non-alcoholic fatty liver disease fibrosis and is produced by hepatic stellate cells in response to fatty acid loading. J Transl Med 16(1):108PubMedPubMedCentral
18.
go back to reference Ortega FJ, Vilallonga R, Xifra G, Sabater M, Ricart W, Fernandez-Real JM (2016) Bariatric surgery acutely changes the expression of inflammatory and lipogenic genes in obese adipose tissue. Surg Obes Relat Dis 12(2):357–362PubMed Ortega FJ, Vilallonga R, Xifra G, Sabater M, Ricart W, Fernandez-Real JM (2016) Bariatric surgery acutely changes the expression of inflammatory and lipogenic genes in obese adipose tissue. Surg Obes Relat Dis 12(2):357–362PubMed
19.
go back to reference Gerhard GS, Styer AM, Strodel WE, Roesch SL, Yavorek A, Carey DJ, Wood GC, Petrick AT, Gabrielsen J, Ibele A, Benotti P, Rolston DD, Still CD, Argyropoulos G (2014) Gene expression profiling in subcutaneous, visceral and epigastric adipose tissues of patients with extreme obesity. Int J Obes 38(3):371–378 Gerhard GS, Styer AM, Strodel WE, Roesch SL, Yavorek A, Carey DJ, Wood GC, Petrick AT, Gabrielsen J, Ibele A, Benotti P, Rolston DD, Still CD, Argyropoulos G (2014) Gene expression profiling in subcutaneous, visceral and epigastric adipose tissues of patients with extreme obesity. Int J Obes 38(3):371–378
20.
go back to reference Hu C, Zhao L, Li L (2019) Current understanding of adipose-derived mesenchymal stem cell-based therapies in liver diseases. Stem Cell Res Ther 10(1):199PubMedPubMedCentral Hu C, Zhao L, Li L (2019) Current understanding of adipose-derived mesenchymal stem cell-based therapies in liver diseases. Stem Cell Res Ther 10(1):199PubMedPubMedCentral
21.
go back to reference Hafeez S, Ahmed MH (2013) Bariatric surgery as potential treatment for nonalcoholic fatty liver disease: a future treatment by choice or by chance? J Obes 2013:839275PubMedPubMedCentral Hafeez S, Ahmed MH (2013) Bariatric surgery as potential treatment for nonalcoholic fatty liver disease: a future treatment by choice or by chance? J Obes 2013:839275PubMedPubMedCentral
22.
go back to reference Mattar SG, Velcu LM, Rabinovitz M, Demetris AJ, Krasinskas AM, Barinas-Mitchell E et al (2005) Surgically-induced weight loss significantly improves nonalcoholic fatty liver disease and the metabolic syndrome. Ann Surg 242(4):610–617 discussion 8-20PubMedPubMedCentral Mattar SG, Velcu LM, Rabinovitz M, Demetris AJ, Krasinskas AM, Barinas-Mitchell E et al (2005) Surgically-induced weight loss significantly improves nonalcoholic fatty liver disease and the metabolic syndrome. Ann Surg 242(4):610–617 discussion 8-20PubMedPubMedCentral
23.
go back to reference Mottin CC, Moretto M, Padoin AV, Kupski C, Swarowsky AM, Glock L, Duval V, da Silva JB (2005) Histological behavior of hepatic steatosis in morbidly obese patients after weight loss induced by bariatric surgery. Obes Surg 15(6):788–793PubMed Mottin CC, Moretto M, Padoin AV, Kupski C, Swarowsky AM, Glock L, Duval V, da Silva JB (2005) Histological behavior of hepatic steatosis in morbidly obese patients after weight loss induced by bariatric surgery. Obes Surg 15(6):788–793PubMed
24.
go back to reference Klein S, Mittendorfer B, Eagon JC, Patterson B, Grant L, Feirt N et al (2006) Gastric bypass surgery improves metabolic and hepatic abnormalities associated with nonalcoholic fatty liver disease. Gastroenterology. 130(6):1564–1572PubMed Klein S, Mittendorfer B, Eagon JC, Patterson B, Grant L, Feirt N et al (2006) Gastric bypass surgery improves metabolic and hepatic abnormalities associated with nonalcoholic fatty liver disease. Gastroenterology. 130(6):1564–1572PubMed
25.
go back to reference Barker KB, Palekar NA, Bowers SP, Goldberg JE, Pulcini JP, Harrison SA (2006 Feb) Non-alcoholic steatohepatitis: effect of roux-en-Y gastric bypass surgery. Am J Gastroenterol 101(2):368–373PubMed Barker KB, Palekar NA, Bowers SP, Goldberg JE, Pulcini JP, Harrison SA (2006 Feb) Non-alcoholic steatohepatitis: effect of roux-en-Y gastric bypass surgery. Am J Gastroenterol 101(2):368–373PubMed
26.
go back to reference Csendes A, Smok G, Burgos AM (2006) Histological findings in the liver before and after gastric bypass. Obes Surg 16(5):607–611PubMed Csendes A, Smok G, Burgos AM (2006) Histological findings in the liver before and after gastric bypass. Obes Surg 16(5):607–611PubMed
27.
go back to reference de Almeida SR, Rocha PR, Sanches MD, Leite VH, da Silva RA, Diniz MT, Diniz Mde F, Rocha AL (2006) Roux-en-Y gastric bypass improves the nonalcoholic steatohepatitis (NASH) of morbid obesity. Obes Surg 16(3):270–278PubMed de Almeida SR, Rocha PR, Sanches MD, Leite VH, da Silva RA, Diniz MT, Diniz Mde F, Rocha AL (2006) Roux-en-Y gastric bypass improves the nonalcoholic steatohepatitis (NASH) of morbid obesity. Obes Surg 16(3):270–278PubMed
28.
go back to reference Furuya CK Jr, de Oliveira CP, de Mello ES, Faintuch J, Raskovski A, Matsuda M et al (2007) Effects of bariatric surgery on nonalcoholic fatty liver disease: preliminary findings after 2 years. J Gastroenterol Hepatol 22(4):510–514PubMed Furuya CK Jr, de Oliveira CP, de Mello ES, Faintuch J, Raskovski A, Matsuda M et al (2007) Effects of bariatric surgery on nonalcoholic fatty liver disease: preliminary findings after 2 years. J Gastroenterol Hepatol 22(4):510–514PubMed
29.
go back to reference Liu X, Lazenby AJ, Clements RH, Jhala N, Abrams GA (2007) Resolution of nonalcoholic steatohepatits after gastric bypass surgery. Obes Surg 17(4):486–492PubMed Liu X, Lazenby AJ, Clements RH, Jhala N, Abrams GA (2007) Resolution of nonalcoholic steatohepatits after gastric bypass surgery. Obes Surg 17(4):486–492PubMed
30.
go back to reference Weiner RA (2010) Surgical treatment of non-alcoholic steatohepatitis and non-alcoholic fatty liver disease. Dig Dis 28(1):274–279PubMed Weiner RA (2010) Surgical treatment of non-alcoholic steatohepatitis and non-alcoholic fatty liver disease. Dig Dis 28(1):274–279PubMed
31.
go back to reference Moretto M, Kupski C, da Silva VD, Padoin AV, Mottin CC (2012) Effect of bariatric surgery on liver fibrosis. Obes Surg 22(7):1044–1049PubMed Moretto M, Kupski C, da Silva VD, Padoin AV, Mottin CC (2012) Effect of bariatric surgery on liver fibrosis. Obes Surg 22(7):1044–1049PubMed
32.
go back to reference Ranlov I, Hardt F (1990) Regression of liver steatosis following gastroplasty or gastric bypass for morbid obesity. Digestion. 47(4):208–214PubMed Ranlov I, Hardt F (1990) Regression of liver steatosis following gastroplasty or gastric bypass for morbid obesity. Digestion. 47(4):208–214PubMed
33.
go back to reference Stratopoulos C, Papakonstantinou A, Terzis I, Spiliadi C, Dimitriades G, Komesidou V, Kitsanta P, Argyrakos T, Hadjiyannakis E (2005) Changes in liver histology accompanying massive weight loss after gastroplasty for morbid obesity. Obes Surg 15(8):1154–1160PubMed Stratopoulos C, Papakonstantinou A, Terzis I, Spiliadi C, Dimitriades G, Komesidou V, Kitsanta P, Argyrakos T, Hadjiyannakis E (2005) Changes in liver histology accompanying massive weight loss after gastroplasty for morbid obesity. Obes Surg 15(8):1154–1160PubMed
34.
go back to reference Dixon JB, Bhathal PS, Hughes NR, O'Brien PE (2004) Nonalcoholic fatty liver disease: improvement in liver histological analysis with weight loss. Hepatology. 39(6):1647–1654PubMed Dixon JB, Bhathal PS, Hughes NR, O'Brien PE (2004) Nonalcoholic fatty liver disease: improvement in liver histological analysis with weight loss. Hepatology. 39(6):1647–1654PubMed
35.
go back to reference Dixon JB, Bhathal PS, O'Brien PE (2006) Weight loss and non-alcoholic fatty liver disease: falls in gamma-glutamyl transferase concentrations are associated with histologic improvement. Obes Surg 16(10):1278–1286PubMed Dixon JB, Bhathal PS, O'Brien PE (2006) Weight loss and non-alcoholic fatty liver disease: falls in gamma-glutamyl transferase concentrations are associated with histologic improvement. Obes Surg 16(10):1278–1286PubMed
36.
go back to reference Mathurin P, Hollebecque A, Arnalsteen L, Buob D, Leteurtre E, Caiazzo R, Pigeyre M, Verkindt H, Dharancy S, Louvet A, Romon M, Pattou F (2009) Prospective study of the long-term effects of bariatric surgery on liver injury in patients without advanced disease. Gastroenterology. 137(2):532–540PubMed Mathurin P, Hollebecque A, Arnalsteen L, Buob D, Leteurtre E, Caiazzo R, Pigeyre M, Verkindt H, Dharancy S, Louvet A, Romon M, Pattou F (2009) Prospective study of the long-term effects of bariatric surgery on liver injury in patients without advanced disease. Gastroenterology. 137(2):532–540PubMed
37.
go back to reference Kral JG, Thung SN, Biron S, Hould FS, Lebel S, Marceau S, Simard S, Marceau P (2004) Effects of surgical treatment of the metabolic syndrome on liver fibrosis and cirrhosis. Surgery. 135(1):48–58PubMed Kral JG, Thung SN, Biron S, Hould FS, Lebel S, Marceau S, Simard S, Marceau P (2004) Effects of surgical treatment of the metabolic syndrome on liver fibrosis and cirrhosis. Surgery. 135(1):48–58PubMed
38.
go back to reference Kucia M, Ratajczak J, Reca R, Janowska-Wieczorek A, Ratajczak MZ (2004) Tissue-specific muscle, neural and liver stem/progenitor cells reside in the bone marrow, respond to an SDF-1 gradient and are mobilized into peripheral blood during stress and tissue injury. Blood Cells Mol Dis 32(1):52–57PubMed Kucia M, Ratajczak J, Reca R, Janowska-Wieczorek A, Ratajczak MZ (2004) Tissue-specific muscle, neural and liver stem/progenitor cells reside in the bone marrow, respond to an SDF-1 gradient and are mobilized into peripheral blood during stress and tissue injury. Blood Cells Mol Dis 32(1):52–57PubMed
39.
go back to reference Chen Y, Xiang LX, Shao JZ, Pan RL, Wang YX, Dong XJ, Zhang GR (2010) Recruitment of endogenous bone marrow mesenchymal stem cells towards injured liver. J Cell Mol Med 14(6B):1494–1508PubMed Chen Y, Xiang LX, Shao JZ, Pan RL, Wang YX, Dong XJ, Zhang GR (2010) Recruitment of endogenous bone marrow mesenchymal stem cells towards injured liver. J Cell Mol Med 14(6B):1494–1508PubMed
40.
41.
go back to reference Fakhry TK, Mhaskar R, Schwitalla T, Muradova E, Gonzalvo JP, Murr MM (2019) Bariatric surgery improves nonalcoholic fatty liver disease: a contemporary systematic review and meta-analysis. Surg Obes Relat Dis 15(3):502–511PubMed Fakhry TK, Mhaskar R, Schwitalla T, Muradova E, Gonzalvo JP, Murr MM (2019) Bariatric surgery improves nonalcoholic fatty liver disease: a contemporary systematic review and meta-analysis. Surg Obes Relat Dis 15(3):502–511PubMed
42.
go back to reference Lee Y, Doumouras AG, Yu J, Brar K, Banfield L, Gmora S, Anvari M, Hong D (2019) Complete resolution of nonalcoholic fatty liver disease after bariatric surgery: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 17(6):1040–1060 e11PubMed Lee Y, Doumouras AG, Yu J, Brar K, Banfield L, Gmora S, Anvari M, Hong D (2019) Complete resolution of nonalcoholic fatty liver disease after bariatric surgery: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 17(6):1040–1060 e11PubMed
43.
go back to reference Sawitza I, Kordes C, Gotze S, Herebian D, Haussinger D (2015) Bile acids induce hepatic differentiation of mesenchymal stem cells. Sci Rep 5:13320PubMedPubMedCentral Sawitza I, Kordes C, Gotze S, Herebian D, Haussinger D (2015) Bile acids induce hepatic differentiation of mesenchymal stem cells. Sci Rep 5:13320PubMedPubMedCentral
44.
go back to reference Cho JG, Lee JH, Hong SH, Lee HN, Kim CM, Kim SY, Yoon KJ, Oh BJ, Kim JH, Jung SY, Asahara T, Kwon SM, Park SG (2015) Tauroursodeoxycholic acid, a bile acid, promotes blood vessel repair by recruiting vasculogenic progenitor cells. Stem Cells 33(3):792–805PubMed Cho JG, Lee JH, Hong SH, Lee HN, Kim CM, Kim SY, Yoon KJ, Oh BJ, Kim JH, Jung SY, Asahara T, Kwon SM, Park SG (2015) Tauroursodeoxycholic acid, a bile acid, promotes blood vessel repair by recruiting vasculogenic progenitor cells. Stem Cells 33(3):792–805PubMed
45.
go back to reference Goktas Z, Moustaid-Moussa N, Shen CL, Boylan M, Mo H, Wang S (2013) Effects of bariatric surgery on adipokine-induced inflammation and insulin resistance. Front Endocrinol (Lausanne) 4:69 Goktas Z, Moustaid-Moussa N, Shen CL, Boylan M, Mo H, Wang S (2013) Effects of bariatric surgery on adipokine-induced inflammation and insulin resistance. Front Endocrinol (Lausanne) 4:69
46.
go back to reference Jimenez LS, Mendonca Chaim FH, Mendonca Chaim FD, Utrini MP, Gestic MA, Chaim EA et al (2018) Impact of weight regain on the evolution of non-alcoholic fatty liver disease after roux-en-Y gastric bypass: a 3-year follow-up. Obes Surg 28(10):3131–3135PubMed Jimenez LS, Mendonca Chaim FH, Mendonca Chaim FD, Utrini MP, Gestic MA, Chaim EA et al (2018) Impact of weight regain on the evolution of non-alcoholic fatty liver disease after roux-en-Y gastric bypass: a 3-year follow-up. Obes Surg 28(10):3131–3135PubMed
47.
go back to reference Paek HJ, Kim C, Williams SK (2014) Adipose stem cell-based regenerative medicine for reversal of diabetic hyperglycemia. World J Diabetes 5(3):235–243PubMedPubMedCentral Paek HJ, Kim C, Williams SK (2014) Adipose stem cell-based regenerative medicine for reversal of diabetic hyperglycemia. World J Diabetes 5(3):235–243PubMedPubMedCentral
48.
go back to reference Nakao N, Nakayama T, Yahata T, Muguruma Y, Saito S, Miyata Y et al (2010) Adipose tissue-derived mesenchymal stem cells facilitate hematopoiesis in vitro and in vivo: advantages over bone marrow-derived mesenchymal stem cells. Am J Pathol 177(2):547–554PubMedPubMedCentral Nakao N, Nakayama T, Yahata T, Muguruma Y, Saito S, Miyata Y et al (2010) Adipose tissue-derived mesenchymal stem cells facilitate hematopoiesis in vitro and in vivo: advantages over bone marrow-derived mesenchymal stem cells. Am J Pathol 177(2):547–554PubMedPubMedCentral
49.
go back to reference Ong WK, Sugii S (2013) Adipose-derived stem cells: fatty potentials for therapy. Int J Biochem Cell Biol 45(6):1083–1086PubMed Ong WK, Sugii S (2013) Adipose-derived stem cells: fatty potentials for therapy. Int J Biochem Cell Biol 45(6):1083–1086PubMed
50.
go back to reference Baer PC (2014) Adipose-derived mesenchymal stromal/stem cells: an update on their phenotype in vivo and in vitro. World J Stem Cells 6(3):256–265PubMedPubMedCentral Baer PC (2014) Adipose-derived mesenchymal stromal/stem cells: an update on their phenotype in vivo and in vitro. World J Stem Cells 6(3):256–265PubMedPubMedCentral
51.
go back to reference Baer PC, Geiger H (2012) Adipose-derived mesenchymal stromal/stem cells: tissue localization, characterization, and heterogeneity. Stem Cells Int 2012:812693PubMedPubMedCentral Baer PC, Geiger H (2012) Adipose-derived mesenchymal stromal/stem cells: tissue localization, characterization, and heterogeneity. Stem Cells Int 2012:812693PubMedPubMedCentral
52.
go back to reference Zhao Y, Zhang H (2016) Update on the mechanisms of homing of adipose tissue-derived stem cells. Cytotherapy. 18(7):816–827PubMed Zhao Y, Zhang H (2016) Update on the mechanisms of homing of adipose tissue-derived stem cells. Cytotherapy. 18(7):816–827PubMed
53.
go back to reference De Francesco F, Ricci G, D'Andrea F, Nicoletti GF, Ferraro GA (2015) Human adipose stem cells: from bench to bedside. Tissue Eng Part B Rev 21(6):572–584PubMed De Francesco F, Ricci G, D'Andrea F, Nicoletti GF, Ferraro GA (2015) Human adipose stem cells: from bench to bedside. Tissue Eng Part B Rev 21(6):572–584PubMed
54.
go back to reference Lee SW, Chong JU, Min SO, Bak SY, Kim KS (2017) Are adipose-derived stem cells from liver Falciform ligaments another possible source of Mesenchymal stem cells? Cell Transplant 26(5):855–866PubMedPubMedCentral Lee SW, Chong JU, Min SO, Bak SY, Kim KS (2017) Are adipose-derived stem cells from liver Falciform ligaments another possible source of Mesenchymal stem cells? Cell Transplant 26(5):855–866PubMedPubMedCentral
55.
go back to reference Schwartz RE, Fleming HE, Khetani SR, Bhatia SN (2014) Pluripotent stem cell-derived hepatocyte-like cells. Biotechnol Adv 32(2):504–513PubMedPubMedCentral Schwartz RE, Fleming HE, Khetani SR, Bhatia SN (2014) Pluripotent stem cell-derived hepatocyte-like cells. Biotechnol Adv 32(2):504–513PubMedPubMedCentral
56.
go back to reference Eguchi A, Feldstein AE (2018) Extracellular vesicles in non-alcoholic and alcoholic fatty liver diseases. Liver Res 2(1):30–34PubMedPubMedCentral Eguchi A, Feldstein AE (2018) Extracellular vesicles in non-alcoholic and alcoholic fatty liver diseases. Liver Res 2(1):30–34PubMedPubMedCentral
Metadata
Title
A retrospective case control study identifies peripheral blood mononuclear cell albumin RNA expression as a biomarker for non-alcoholic fatty liver disease
Authors
Xin Chu
Kelsey Karasinski
Sean Donellan
Scott Kaniper
G. Craig Wood
Weixing Shi
Michael A. Edwards
Rohit Soans
Christopher D. Still
Glenn S. Gerhard
Publication date
01-03-2020
Publisher
Springer Berlin Heidelberg
Published in
Langenbeck's Archives of Surgery / Issue 2/2020
Print ISSN: 1435-2443
Electronic ISSN: 1435-2451
DOI
https://doi.org/10.1007/s00423-019-01848-0

Other articles of this Issue 2/2020

Langenbeck's Archives of Surgery 2/2020 Go to the issue