Skip to main content
Top
Published in: Cardiovascular Diabetology 1/2012

Open Access 01-12-2012 | Original investigation

Hyperinsulinemia correlates with low levels of plasma B-type natriuretic peptide in Japanese men irrespective of fat distribution

Authors: Hideaki Nakatsuji, Ken Kishida, Tohru Funahashi, Tohru Nakagawa, Iichiro Shimomura

Published in: Cardiovascular Diabetology | Issue 1/2012

Login to get access

Abstract

Background

B-type natriuretic peptide (BNP), a member of the natriuretic peptide family, is a cardiac-derived secretory hormone with natriuretic, diuretic, and vasorelaxant activities. Intraabdominal fat accumulation is associated with atherosclerotic cardiovascular diseases and cardiac dysfunction. Circulating BNP levels are relatively low (within the normal limits) in obesity and the metabolic syndrome. However, the relationship between plasma BNP levels and visceral fat accumulation in general population has not been reported. The present study analyzed the relationships between plasma BNP levels and various clinical variables, including insulin, visceral and subcutaneous fat area (VFA and SFA, respectively), in normal Japanese men.

Methods

The study (Victor-J study) subjects were consecutive 500 Japanese male workers, who underwent a health checkup and were measured VFA and SFA by computed tomography.

Results

Age-adjusted simple linear regression analysis showed that log-BNP correlated positively with HDL-cholesterol, and negatively with VFA, log-immunoreactive insulin (IRI), log-triglyceride, and LDL-cholesterol, but not body mass index or SFA. Stepwise multiple regression analysis identified log-IRI and HDL-cholesterol as significant determinants of log-BNP. Subjects with IRI ≥5.5 μIU/mL had lower plasma BNP levels than those with IRI < 5.5 μIU/mL, irrespective of obesity (body mass index, cutoff value 25 kg/m2), visceral fat accumulation (VFA, cutoff value 100 cm2) and subcutaneous fat accumulation (SFA, cutoff value 128 cm2).

Conclusions

Our study showed that hyperinsulinemia correlated with low levels of plasma BNP in general men, irrespective of fat distribution.

Trial registration

UMIN 000004318.
Appendix
Available only for authorised users
Literature
1.
go back to reference Mukoyama M, Nakao K, Hosoda K, Suga S, Saito Y, Ogawa Y, Shirakami G, Jougasaki M, Obata K, Yasue H, Kambayashi Y, Inoue K, Imura H: Brain natriuretic peptide as a novel cardiac hormone in humans. Evidence for an exquisite dual natriuretic peptide system, atrial natriuretic peptide and brain natriuretic peptide. J Clin Invest. 1991, 87: 1402-1412. 10.1172/JCI115146.PubMedCentralCrossRefPubMed Mukoyama M, Nakao K, Hosoda K, Suga S, Saito Y, Ogawa Y, Shirakami G, Jougasaki M, Obata K, Yasue H, Kambayashi Y, Inoue K, Imura H: Brain natriuretic peptide as a novel cardiac hormone in humans. Evidence for an exquisite dual natriuretic peptide system, atrial natriuretic peptide and brain natriuretic peptide. J Clin Invest. 1991, 87: 1402-1412. 10.1172/JCI115146.PubMedCentralCrossRefPubMed
2.
go back to reference Levin ER, Gardner DG, Samson WK: Natriuretic peptides. N Engl J Med. 1998, 339: 321-328. 10.1056/NEJM199807303390507.CrossRefPubMed Levin ER, Gardner DG, Samson WK: Natriuretic peptides. N Engl J Med. 1998, 339: 321-328. 10.1056/NEJM199807303390507.CrossRefPubMed
3.
go back to reference Nakamura M, Endo H, Nasu M, Arakawa N, Segawa T, Hiramori K: Value of plasma B type natriuretic peptide measurement for heart disease screening in a Japanese population. Heart. 2002, 87: 131-135. 10.1136/heart.87.2.131.PubMedCentralCrossRefPubMed Nakamura M, Endo H, Nasu M, Arakawa N, Segawa T, Hiramori K: Value of plasma B type natriuretic peptide measurement for heart disease screening in a Japanese population. Heart. 2002, 87: 131-135. 10.1136/heart.87.2.131.PubMedCentralCrossRefPubMed
4.
go back to reference Kanai H, Matsuzawa Y, Kotani K, Keno Y, Kobatake T, Nagai Y, Fujioka S, Tokunaga K, Tarui S: Close correlation of intra-abdominal fat accumulation to hypertension in obese women. Hypertension. 1990, 16: 484-490.CrossRefPubMed Kanai H, Matsuzawa Y, Kotani K, Keno Y, Kobatake T, Nagai Y, Fujioka S, Tokunaga K, Tarui S: Close correlation of intra-abdominal fat accumulation to hypertension in obese women. Hypertension. 1990, 16: 484-490.CrossRefPubMed
5.
go back to reference Nakajima T, Fujioka S, Tokunaga K, Matsuzawa Y, Tarui S: Correlation of intraabdominal fat accumulation and left ventricular performance in obesity. Am J Cardiol. 1989, 64: 369-373. 10.1016/0002-9149(89)90537-7.CrossRefPubMed Nakajima T, Fujioka S, Tokunaga K, Matsuzawa Y, Tarui S: Correlation of intraabdominal fat accumulation and left ventricular performance in obesity. Am J Cardiol. 1989, 64: 369-373. 10.1016/0002-9149(89)90537-7.CrossRefPubMed
6.
go back to reference Sugisawa T, Kishimoto I, Kokubo Y, Makino H, Miyamoto Y, Yoshimasa Y: Association of plasma B-type natriuretic peptide levels with obesity in a general urban Japanese population: the Suita study. Endocr J. 2010, 57: 727-733. 10.1507/endocrj.K10E-067.CrossRefPubMed Sugisawa T, Kishimoto I, Kokubo Y, Makino H, Miyamoto Y, Yoshimasa Y: Association of plasma B-type natriuretic peptide levels with obesity in a general urban Japanese population: the Suita study. Endocr J. 2010, 57: 727-733. 10.1507/endocrj.K10E-067.CrossRefPubMed
7.
go back to reference Horwich TB, Hamilton MA, Fonarow GC: B-type natriuretic peptide levels in obese patients with advanced heart failure. J Am Coll Cardiol. 2006, 47: 85-90. 10.1016/j.jacc.2005.08.050.CrossRefPubMed Horwich TB, Hamilton MA, Fonarow GC: B-type natriuretic peptide levels in obese patients with advanced heart failure. J Am Coll Cardiol. 2006, 47: 85-90. 10.1016/j.jacc.2005.08.050.CrossRefPubMed
8.
go back to reference McCord J, Mundy BJ, Hudson MP, Maisel AS, Hollander JE, Abraham WT, Steg PG, Omland T, Knudsen CW, Sandberg KR, McCullough PA: Breathing not properly multinational study investigators: relationship between obesity and B-type natriuretic peptide levels. Arch Intern Med. 2004, 164: 2247-2252. 10.1001/archinte.164.20.2247.CrossRefPubMed McCord J, Mundy BJ, Hudson MP, Maisel AS, Hollander JE, Abraham WT, Steg PG, Omland T, Knudsen CW, Sandberg KR, McCullough PA: Breathing not properly multinational study investigators: relationship between obesity and B-type natriuretic peptide levels. Arch Intern Med. 2004, 164: 2247-2252. 10.1001/archinte.164.20.2247.CrossRefPubMed
9.
go back to reference Wang TJ, Larson MG, Levy D, Benjamin EJ, Leip EP, Wilson PW, Vasan RS: Impact of obesity on plasma natriuretic peptide levels. Circulation. 2004, 109: 594-600. 10.1161/01.CIR.0000112582.16683.EA.CrossRefPubMed Wang TJ, Larson MG, Levy D, Benjamin EJ, Leip EP, Wilson PW, Vasan RS: Impact of obesity on plasma natriuretic peptide levels. Circulation. 2004, 109: 594-600. 10.1161/01.CIR.0000112582.16683.EA.CrossRefPubMed
10.
go back to reference Khan AM, Cheng S, Magnusson M, Larson MG, Newton-Cheh C, McCabe EL, Coviello AD, Florez JC, Fox CS, Levy D, Robins SJ, Arora P, Bhasin S, Lam CS, Vasan RS, Melander O, Wang TJ: Cardiac natriuretic peptides, obesity, and insulin resistance: evidence from two community-based studies. J Clin Endocrinol Metab. 2011, 96: 3242-3249. 10.1210/jc.2011-1182.PubMedCentralCrossRefPubMed Khan AM, Cheng S, Magnusson M, Larson MG, Newton-Cheh C, McCabe EL, Coviello AD, Florez JC, Fox CS, Levy D, Robins SJ, Arora P, Bhasin S, Lam CS, Vasan RS, Melander O, Wang TJ: Cardiac natriuretic peptides, obesity, and insulin resistance: evidence from two community-based studies. J Clin Endocrinol Metab. 2011, 96: 3242-3249. 10.1210/jc.2011-1182.PubMedCentralCrossRefPubMed
11.
go back to reference Cheng S, Fox CS, Larson MG, Massaro JM, McCabe EL, Khan AM, Levy D, Hoffmann U, O'Donnell CJ, Miller KK, Newton-Cheh C, Coviello AD, Bhasin S, Vasan RS, Wang TJ: Relation of visceral adiposity to circulating natriuretic peptides in ambulatory individuals. Am J Cardiol. 2011, 108: 979-984. 10.1016/j.amjcard.2011.05.033.PubMedCentralCrossRefPubMed Cheng S, Fox CS, Larson MG, Massaro JM, McCabe EL, Khan AM, Levy D, Hoffmann U, O'Donnell CJ, Miller KK, Newton-Cheh C, Coviello AD, Bhasin S, Vasan RS, Wang TJ: Relation of visceral adiposity to circulating natriuretic peptides in ambulatory individuals. Am J Cardiol. 2011, 108: 979-984. 10.1016/j.amjcard.2011.05.033.PubMedCentralCrossRefPubMed
12.
go back to reference Wang TJ, Larson MG, Keyes MJ, Levy D, Benjamin EJ, Vasan RS: Association of plasma natriuretic peptide levels with metabolic risk factors in ambulatory individuals. Circulation. 2007, 115: 1345-1353. 10.1161/CIRCULATIONAHA.106.655142.CrossRefPubMed Wang TJ, Larson MG, Keyes MJ, Levy D, Benjamin EJ, Vasan RS: Association of plasma natriuretic peptide levels with metabolic risk factors in ambulatory individuals. Circulation. 2007, 115: 1345-1353. 10.1161/CIRCULATIONAHA.106.655142.CrossRefPubMed
13.
go back to reference Tanabe A, Naruse M, Wasada T, Naruse K, Yoshimoto T, Omori Y, Demura H: Effects of acute hyperinsulinemia on plasma atrial and brain natriuretic peptide concentrations. Eur J Endocrinol. 1995, 132: 693-698. 10.1530/eje.0.1320693.CrossRefPubMed Tanabe A, Naruse M, Wasada T, Naruse K, Yoshimoto T, Omori Y, Demura H: Effects of acute hyperinsulinemia on plasma atrial and brain natriuretic peptide concentrations. Eur J Endocrinol. 1995, 132: 693-698. 10.1530/eje.0.1320693.CrossRefPubMed
14.
go back to reference Halbirk M, Nørrelund H, Møller N, Schmitz O, Bøtker HE, Wiggers H: Short-term changes in circulating insulin and free fatty acids affect Nt-pro-BNP levels in heart failure patients. Int J Cardiol. 2010, 144: 140-142. 10.1016/j.ijcard.2008.12.152.CrossRefPubMed Halbirk M, Nørrelund H, Møller N, Schmitz O, Bøtker HE, Wiggers H: Short-term changes in circulating insulin and free fatty acids affect Nt-pro-BNP levels in heart failure patients. Int J Cardiol. 2010, 144: 140-142. 10.1016/j.ijcard.2008.12.152.CrossRefPubMed
15.
go back to reference Sengenes C, Bouloumie A, Hauner H, Berlan M, Busse R, Lafontan M, Galitzky J: Involvement of a cGMP-dependent pathway in the natriuretic peptide-mediated hormone-sensitive lipase phosphorylation in human adipocytes. J Biol Chem. 2003, 278: 48617-48626. 10.1074/jbc.M303713200.CrossRefPubMed Sengenes C, Bouloumie A, Hauner H, Berlan M, Busse R, Lafontan M, Galitzky J: Involvement of a cGMP-dependent pathway in the natriuretic peptide-mediated hormone-sensitive lipase phosphorylation in human adipocytes. J Biol Chem. 2003, 278: 48617-48626. 10.1074/jbc.M303713200.CrossRefPubMed
16.
go back to reference Birkenfeld AL, Boschmann M, Moro C, Adams F, Heusser K, Franke G, Berlan M, Luft FC, Lafontan M, Jordan J: Lipid mobilization with physiological atrial natriuretic peptide concentrations in humans. J Clin Endocrinol Metab. 2005, 90: 3622-3628. 10.1210/jc.2004-1953.CrossRefPubMed Birkenfeld AL, Boschmann M, Moro C, Adams F, Heusser K, Franke G, Berlan M, Luft FC, Lafontan M, Jordan J: Lipid mobilization with physiological atrial natriuretic peptide concentrations in humans. J Clin Endocrinol Metab. 2005, 90: 3622-3628. 10.1210/jc.2004-1953.CrossRefPubMed
17.
go back to reference Savoia C, Volpe M, Alonzo A, Rossi C, Rubattu S: Natriuretic peptides and cardiovascular damage in the metabolic syndrome: molecular mechanisms and clinical implications. Clin Sci (Lond). 2009, 118: 231-240. 10.1042/CS20090204.CrossRef Savoia C, Volpe M, Alonzo A, Rossi C, Rubattu S: Natriuretic peptides and cardiovascular damage in the metabolic syndrome: molecular mechanisms and clinical implications. Clin Sci (Lond). 2009, 118: 231-240. 10.1042/CS20090204.CrossRef
18.
go back to reference Kenny AJ, Bourne A, Ingram J: Hydrolysis of human and pig brain natriuretic peptides, urodilatin, C-type natriuretic peptide and some C-receptor ligands by endopeptidase-24.11. Biochem J. 1993, 291: 83-88.PubMedCentralCrossRefPubMed Kenny AJ, Bourne A, Ingram J: Hydrolysis of human and pig brain natriuretic peptides, urodilatin, C-type natriuretic peptide and some C-receptor ligands by endopeptidase-24.11. Biochem J. 1993, 291: 83-88.PubMedCentralCrossRefPubMed
19.
go back to reference Nakatsuji H, Maeda N, Hibuse T, Hiuge A, Hirata A, Kuroda Y, Kishida K, Kihara S, Funahashi T, Shimomura I: Reciprocal regulation of natriuretic peptide receptors by insulin in adipose cells. Biochem Biophys Res Commun. 2010, 392: 100-105. 10.1016/j.bbrc.2010.01.008.CrossRefPubMed Nakatsuji H, Maeda N, Hibuse T, Hiuge A, Hirata A, Kuroda Y, Kishida K, Kihara S, Funahashi T, Shimomura I: Reciprocal regulation of natriuretic peptide receptors by insulin in adipose cells. Biochem Biophys Res Commun. 2010, 392: 100-105. 10.1016/j.bbrc.2010.01.008.CrossRefPubMed
20.
go back to reference Miyashita K, Itoh H, Tsujimoto H, Tamura N, Fukunaga Y, Sone M, Yamahara K, Taura D, Inuzuka M, Sonoyama T, Nakao K: Natriuretic peptides/cGMP/cGMP -dependent protein kinase cascades promote muscle mitochondrial biogenesis and prevent obesity. Diabetes. 2009, 58: 2880-2892. 10.2337/db09-0393.PubMedCentralCrossRefPubMed Miyashita K, Itoh H, Tsujimoto H, Tamura N, Fukunaga Y, Sone M, Yamahara K, Taura D, Inuzuka M, Sonoyama T, Nakao K: Natriuretic peptides/cGMP/cGMP -dependent protein kinase cascades promote muscle mitochondrial biogenesis and prevent obesity. Diabetes. 2009, 58: 2880-2892. 10.2337/db09-0393.PubMedCentralCrossRefPubMed
21.
go back to reference Standeven KF, Hess K, Carter AM, Rice GI, Cordell PA, Balmforth AJ, Lu B, Scott DJ, Turner AJ, Hooper NM, Grant PJ: Neprilysin, obesity and the metabolic syndrome. Int J Obes (Lond). 2011, 35: 1031-1040. 10.1038/ijo.2010.227.CrossRef Standeven KF, Hess K, Carter AM, Rice GI, Cordell PA, Balmforth AJ, Lu B, Scott DJ, Turner AJ, Hooper NM, Grant PJ: Neprilysin, obesity and the metabolic syndrome. Int J Obes (Lond). 2011, 35: 1031-1040. 10.1038/ijo.2010.227.CrossRef
22.
go back to reference McCullough PA, Nowak RM, McCord J, Hollander JE, Herrmann HC, Steg PG, Duc P, Westheim A, Omland T, Knudsen CW, Storrow AB, Abraham WT, Lamba S, Wu AH, Perez A, Clopton P, Krishnaswamy P, Kazanegra R, Maisel AS: B-type natriuretic peptide and clinical judgment in emergency diagnosis of heart failure: analysis from Breathing Not Properly (BNP) multinational study. Circulation. 2002, 106: 416-422. 10.1161/01.CIR.0000025242.79963.4C.CrossRefPubMed McCullough PA, Nowak RM, McCord J, Hollander JE, Herrmann HC, Steg PG, Duc P, Westheim A, Omland T, Knudsen CW, Storrow AB, Abraham WT, Lamba S, Wu AH, Perez A, Clopton P, Krishnaswamy P, Kazanegra R, Maisel AS: B-type natriuretic peptide and clinical judgment in emergency diagnosis of heart failure: analysis from Breathing Not Properly (BNP) multinational study. Circulation. 2002, 106: 416-422. 10.1161/01.CIR.0000025242.79963.4C.CrossRefPubMed
23.
go back to reference Kim HN, Januzzi JL: Natriuretic peptide testing in heart failure. Circulation. 2011, 123: 2015-2019. 10.1161/CIRCULATIONAHA.110.979500.CrossRefPubMed Kim HN, Januzzi JL: Natriuretic peptide testing in heart failure. Circulation. 2011, 123: 2015-2019. 10.1161/CIRCULATIONAHA.110.979500.CrossRefPubMed
24.
go back to reference Chen-Tournoux A, Khan AM, Baggish AL, Castro VM, Semigran MJ, McCabe EL, Moukarbel G, Reingold J, Durrani S, Lewis GD, Newton-Cheh C, Scherrer-Crosbie M, Kaplan LM, Wang TJ: Effect of weight loss after weight loss surgery on plasma N-terminal pro-B-type natriuretic peptide levels. Am J Cardiol. 2010, 106: 1450-1455. 10.1016/j.amjcard.2010.06.076.PubMedCentralCrossRefPubMed Chen-Tournoux A, Khan AM, Baggish AL, Castro VM, Semigran MJ, McCabe EL, Moukarbel G, Reingold J, Durrani S, Lewis GD, Newton-Cheh C, Scherrer-Crosbie M, Kaplan LM, Wang TJ: Effect of weight loss after weight loss surgery on plasma N-terminal pro-B-type natriuretic peptide levels. Am J Cardiol. 2010, 106: 1450-1455. 10.1016/j.amjcard.2010.06.076.PubMedCentralCrossRefPubMed
25.
go back to reference Andreas M, Zeisler H, Handisurya A, Franz MB, Gottsauner-Wolf M, Wolzt M, Kautzky-Willer A: N-terminal-pro-brain natriuretic peptide is decreased in insulin dependent gestational diabetes mellitus: a prospective cohort trial. Cardiovasc Diabetol. 2011, 10: 28-10.1186/1475-2840-10-28.PubMedCentralCrossRefPubMed Andreas M, Zeisler H, Handisurya A, Franz MB, Gottsauner-Wolf M, Wolzt M, Kautzky-Willer A: N-terminal-pro-brain natriuretic peptide is decreased in insulin dependent gestational diabetes mellitus: a prospective cohort trial. Cardiovasc Diabetol. 2011, 10: 28-10.1186/1475-2840-10-28.PubMedCentralCrossRefPubMed
26.
go back to reference Palmer SC, Yandle TG, Nicholls MG, Frampton CM, Richards AM: Regional clearance of amino-terminal pro-brain natriuretic peptide from human plasma. Eur J Heart Fail. 2009, 11: 832-839. 10.1093/eurjhf/hfp099.CrossRefPubMed Palmer SC, Yandle TG, Nicholls MG, Frampton CM, Richards AM: Regional clearance of amino-terminal pro-brain natriuretic peptide from human plasma. Eur J Heart Fail. 2009, 11: 832-839. 10.1093/eurjhf/hfp099.CrossRefPubMed
Metadata
Title
Hyperinsulinemia correlates with low levels of plasma B-type natriuretic peptide in Japanese men irrespective of fat distribution
Authors
Hideaki Nakatsuji
Ken Kishida
Tohru Funahashi
Tohru Nakagawa
Iichiro Shimomura
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2012
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/1475-2840-11-22

Other articles of this Issue 1/2012

Cardiovascular Diabetology 1/2012 Go to the issue