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Published in: Obesity Surgery 9/2017

01-09-2017 | Original Contributions

Impact of Bariatric Surgery on Heme Oxygenase-1, Inflammation, and Insulin Resistance in Morbid Obesity with Obstructive Sleep Apnea

Authors: Raquel Tirado, Maria José Masdeu, Laura Vigil, Mercedes Rigla, Alexis Luna, Pere Rebasa, Rocío Pareja, Marta Hurtado, Assumpta Caixàs

Published in: Obesity Surgery | Issue 9/2017

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Abstract

Introduction

Morbid obesity and obstructive sleep apnea (OSA) interact at an inflammatory level. Bariatric surgery reduces inflammatory responses associated with obesity. Heme oxygenase-1 (HO-1) is an enzyme with anti-inflammatory properties, which might be increased in morbid obesity or OSA. We studied morbidly obese patients with OSA to determine: (a) HO-1 plasma concentrations according to OSA severity and their relationship with insulin resistance and inflammation and (b) the impact of bariatric surgery on HO-1 and parameters of insulin resistance and inflammation.

Material and Methods

We analyzed the homeostasis model insulin resistance index (HOMA) and plasma concentrations of HO-1, tumor necrosis factor alpha, interleukin-6, interleukin-1-beta, C reactive protein (CRP), and adiponectin according to polysomnography findings in 66 morbidly obese patients before bariatric surgery and 12 months after surgery.

Results

Before surgery, HO-1 plasma concentrations were similar in three groups of patients with mild, moderate, and severe OSA, and correlated with HOMA (r = 0.27, p = 0.02). Twelve months after surgery, low-grade inflammation and insulin resistance had decreased in all the groups, but HO-1 plasma concentration had decreased only in the severe OSA group (p = 0.02). In this group, the reduction in HO-1 correlated with a reduction in CRP concentrations (r = 0.43, p = 0.04) and with improved HOMA score (r = 0.37, p = 0.03).

Conclusions

Bariatric surgery decreases HO-1 concentrations in morbid obesity with severe OSA, and this decrease is associated with decreases in insulin resistance and in inflammation.
Literature
1.
go back to reference Leiter JC. Upper airway shape: is it important in the pathogenesis of obstructive sleep apnea? Am J Respir Crit Care Med. 1996;153(3):894–8.PubMedCrossRef Leiter JC. Upper airway shape: is it important in the pathogenesis of obstructive sleep apnea? Am J Respir Crit Care Med. 1996;153(3):894–8.PubMedCrossRef
2.
go back to reference Brander PE, Mortimore IL, Douglas NJ. Effect of obesity and erect/supine posture on lateral cephalometry: relationship to sleep-disordered breathing. Eur Respir J. 1999;13(2):398–402.PubMedCrossRef Brander PE, Mortimore IL, Douglas NJ. Effect of obesity and erect/supine posture on lateral cephalometry: relationship to sleep-disordered breathing. Eur Respir J. 1999;13(2):398–402.PubMedCrossRef
3.
go back to reference Schwab RJ. Genetic determinants of upper airway structures that predispose to obstructive sleep apnea. Respir Physiol Neurobiol. 2005;147(2–3):289–98.PubMedCrossRef Schwab RJ. Genetic determinants of upper airway structures that predispose to obstructive sleep apnea. Respir Physiol Neurobiol. 2005;147(2–3):289–98.PubMedCrossRef
4.
go back to reference Borel AL, Leblanc X, Alméras N, et al. Sleep apnoea attenuates the effects of a lifestyle intervention programme in men with visceral obesity. Thorax. 2012;67(8):735–41.PubMedCrossRef Borel AL, Leblanc X, Alméras N, et al. Sleep apnoea attenuates the effects of a lifestyle intervention programme in men with visceral obesity. Thorax. 2012;67(8):735–41.PubMedCrossRef
5.
go back to reference Kim NH, Cho NH, Yun CH, et al. Association of obstructive sleep apnea and glucose metabolism in subjects with or without obesity. Diabetes Care. 2013;36(12):3909–15.PubMedPubMedCentralCrossRef Kim NH, Cho NH, Yun CH, et al. Association of obstructive sleep apnea and glucose metabolism in subjects with or without obesity. Diabetes Care. 2013;36(12):3909–15.PubMedPubMedCentralCrossRef
6.
go back to reference Togeiro SM, Carneiro G, Ribeiro Filho FF, et al. Consequences of obstructive sleep apnea on metabolic profile: a population-based survey. Obesity (Silver Spring). 2013;21(4):847–51.CrossRef Togeiro SM, Carneiro G, Ribeiro Filho FF, et al. Consequences of obstructive sleep apnea on metabolic profile: a population-based survey. Obesity (Silver Spring). 2013;21(4):847–51.CrossRef
7.
go back to reference Tzanavari T, Giannogonas P, Karalis KP. TNF-alpha and obesity. Curr Dir Autoimmun. 2010;11:145–56.PubMedCrossRef Tzanavari T, Giannogonas P, Karalis KP. TNF-alpha and obesity. Curr Dir Autoimmun. 2010;11:145–56.PubMedCrossRef
8.
go back to reference Illán-Gómez F, Gonzálvez-Ortega M, Orea-Soler I, et al. Obesity and inflammation: change in adiponectin, C-reactive protein, tumour necrosis factor-alpha and interleukin-6 after bariatric surgery. Obes Surg. 2012;22(6):950–5.PubMedCrossRef Illán-Gómez F, Gonzálvez-Ortega M, Orea-Soler I, et al. Obesity and inflammation: change in adiponectin, C-reactive protein, tumour necrosis factor-alpha and interleukin-6 after bariatric surgery. Obes Surg. 2012;22(6):950–5.PubMedCrossRef
9.
go back to reference Terra X, Quintero Y, Auguet T, et al. FABP 4 is associated with inflammatory markers and metabolic syndrome in morbidly obese women. Eur J Endocrinol. 2011;164(4):539–47.PubMedCrossRef Terra X, Quintero Y, Auguet T, et al. FABP 4 is associated with inflammatory markers and metabolic syndrome in morbidly obese women. Eur J Endocrinol. 2011;164(4):539–47.PubMedCrossRef
10.
go back to reference Ciftci TU, Kokturk O, Bukan N, et al. The relationship between serum cytokine levels with obesity and obstructive sleep apnea syndrome. Cytokine. 2004;28(2):87–91.PubMedCrossRef Ciftci TU, Kokturk O, Bukan N, et al. The relationship between serum cytokine levels with obesity and obstructive sleep apnea syndrome. Cytokine. 2004;28(2):87–91.PubMedCrossRef
11.
go back to reference Sahlman J, Miettinen K, Peuhkurinen K, et al. The activation of the inflammatory cytokines in overweight patients with mild obstructive sleep apnoea. J Sleep Res. 2010;19(2):341–8.PubMedCrossRef Sahlman J, Miettinen K, Peuhkurinen K, et al. The activation of the inflammatory cytokines in overweight patients with mild obstructive sleep apnoea. J Sleep Res. 2010;19(2):341–8.PubMedCrossRef
12.
go back to reference Vgontzas AN, Zoumakis E, Bixler EO, et al. Selective effects of CPAP on sleep apnoea-associated manifestations. Eur J Clin Investig. 2008;38(8):585–95.CrossRef Vgontzas AN, Zoumakis E, Bixler EO, et al. Selective effects of CPAP on sleep apnoea-associated manifestations. Eur J Clin Investig. 2008;38(8):585–95.CrossRef
13.
go back to reference Vgontzas AN, Papanicolaou DA, Bixler EO, et al. Sleep apnea and daytime sleepiness and fatigue: relation to visceral obesity, insulin resistance, and hypercytokinemia. J Clin Endocrinol Metab. 2000;85(3):1151–8.PubMedCrossRef Vgontzas AN, Papanicolaou DA, Bixler EO, et al. Sleep apnea and daytime sleepiness and fatigue: relation to visceral obesity, insulin resistance, and hypercytokinemia. J Clin Endocrinol Metab. 2000;85(3):1151–8.PubMedCrossRef
14.
go back to reference Constantinidis J, Ereliadis S, Angouridakis N, et al. Cytokine changes after surgical treatment of obstructive sleep apnoea syndrome. Eur Arch Otorhinolaryngol. 2008;265(10):1275–9.PubMedCrossRef Constantinidis J, Ereliadis S, Angouridakis N, et al. Cytokine changes after surgical treatment of obstructive sleep apnoea syndrome. Eur Arch Otorhinolaryngol. 2008;265(10):1275–9.PubMedCrossRef
15.
go back to reference Auguet T, Terra X, Hernández M, et al. Clinical and adipocytokine changes after bariatric surgery in morbidly obese women. Obesity (Silver Spring). 2014;22(1):188–94.CrossRef Auguet T, Terra X, Hernández M, et al. Clinical and adipocytokine changes after bariatric surgery in morbidly obese women. Obesity (Silver Spring). 2014;22(1):188–94.CrossRef
16.
go back to reference Guven SF, Turkkani MH, Ciftci B, et al. The relationship between high-sensitivity C-reactive protein levels and the severity of obstructive sleep apnea. Sleep Breath. 2012;16(1):217–21.PubMedCrossRef Guven SF, Turkkani MH, Ciftci B, et al. The relationship between high-sensitivity C-reactive protein levels and the severity of obstructive sleep apnea. Sleep Breath. 2012;16(1):217–21.PubMedCrossRef
17.
go back to reference Drager LF, Lopes HF, Maki-Nunes C, et al. The impact of obstructive sleep apnea on metabolic and inflammatory markers in consecutive patients with metabolic syndrome. PLoS One. 2010;5(8):e12065.PubMedPubMedCentralCrossRef Drager LF, Lopes HF, Maki-Nunes C, et al. The impact of obstructive sleep apnea on metabolic and inflammatory markers in consecutive patients with metabolic syndrome. PLoS One. 2010;5(8):e12065.PubMedPubMedCentralCrossRef
18.
19.
go back to reference García de la Torre N, Rubio MA, Bordiú E, et al. Effects of weight loss after bariatric surgery for morbid obesity on vascular endothelial growth factor-A, adipocytokines, and insulin. J Clin Endocrinol Metab. 2008;93(11):4276–81.PubMedCrossRef García de la Torre N, Rubio MA, Bordiú E, et al. Effects of weight loss after bariatric surgery for morbid obesity on vascular endothelial growth factor-A, adipocytokines, and insulin. J Clin Endocrinol Metab. 2008;93(11):4276–81.PubMedCrossRef
20.
go back to reference Lam JC, Xu A, Tam S, et al. Hypoadiponectinemia is related to sympathetic activation and severity of obstructive sleep apnea. Sleep. 2008;31(12):1721–7.PubMedPubMedCentralCrossRef Lam JC, Xu A, Tam S, et al. Hypoadiponectinemia is related to sympathetic activation and severity of obstructive sleep apnea. Sleep. 2008;31(12):1721–7.PubMedPubMedCentralCrossRef
21.
go back to reference Nakagawa Y, Kishida K, Kihara S, et al. Nocturnal falls of adiponectin levels in sleep apnea with abdominal obesity and impact of hypoxia-induced dysregulated adiponectin production in obese murine mesenteric adipose tissue. J Atheroscler Thromb. 2011;18(3):240–7.PubMedCrossRef Nakagawa Y, Kishida K, Kihara S, et al. Nocturnal falls of adiponectin levels in sleep apnea with abdominal obesity and impact of hypoxia-induced dysregulated adiponectin production in obese murine mesenteric adipose tissue. J Atheroscler Thromb. 2011;18(3):240–7.PubMedCrossRef
22.
go back to reference Yin J, Gao Z, He Q, et al. Role of hypoxia in obesity-induced disorders of glucose and lipid metabolism in adipose tissue. Am J Physiol Endocrinol Metab. 2009;296(2):E333–42.PubMedCrossRef Yin J, Gao Z, He Q, et al. Role of hypoxia in obesity-induced disorders of glucose and lipid metabolism in adipose tissue. Am J Physiol Endocrinol Metab. 2009;296(2):E333–42.PubMedCrossRef
23.
go back to reference Bonsignore MR, McNicholas WT, Montserrat JM, et al. Adipose tissue in obesity and obstructive sleep apnoea. Eur Respir J. 2012;39(3):746–67.PubMedCrossRef Bonsignore MR, McNicholas WT, Montserrat JM, et al. Adipose tissue in obesity and obstructive sleep apnoea. Eur Respir J. 2012;39(3):746–67.PubMedCrossRef
24.
go back to reference Sjöström L. Review of the key results from the Swedish Obese Subjects (SOS) trial—a prospective controlled intervention study of bariatric surgery. J Intern Med. 2013;273(3):219–34.PubMedCrossRef Sjöström L. Review of the key results from the Swedish Obese Subjects (SOS) trial—a prospective controlled intervention study of bariatric surgery. J Intern Med. 2013;273(3):219–34.PubMedCrossRef
25.
go back to reference Compher C, Badellino KO. Obesity and inflammation: lessons from bariatric surgery. JPEN J Parenter Enteral Nutr. 2008;32(6):645–7.PubMedCrossRef Compher C, Badellino KO. Obesity and inflammation: lessons from bariatric surgery. JPEN J Parenter Enteral Nutr. 2008;32(6):645–7.PubMedCrossRef
26.
go back to reference Fredheim JM, Rollheim J, Sandbu R, et al. Obstructive sleep apnea after weight loss: a clinical trial comparing gastric bypass and intensive lifestyle intervention. J Clin Sleep Med. 2013;9(5):427–32.PubMedPubMedCentral Fredheim JM, Rollheim J, Sandbu R, et al. Obstructive sleep apnea after weight loss: a clinical trial comparing gastric bypass and intensive lifestyle intervention. J Clin Sleep Med. 2013;9(5):427–32.PubMedPubMedCentral
27.
go back to reference West SD, Nicoll DJ, Wallace TM, et al. Effect of CPAP on insulin resistance and HbA1c in men with obstructive sleep apnoea and type 2 diabetes. Thorax. 2007;62(11):969–74.PubMedPubMedCentralCrossRef West SD, Nicoll DJ, Wallace TM, et al. Effect of CPAP on insulin resistance and HbA1c in men with obstructive sleep apnoea and type 2 diabetes. Thorax. 2007;62(11):969–74.PubMedPubMedCentralCrossRef
29.
go back to reference Ndisang JF, Lane N, Jadhav A. The heme oxygenase system abates hyperglycemia in Zucker diabetic fatty rats by potentiating insulin-sensitizing pathways. Endocrinology. 2009a;150(5):2098–108.PubMedCrossRef Ndisang JF, Lane N, Jadhav A. The heme oxygenase system abates hyperglycemia in Zucker diabetic fatty rats by potentiating insulin-sensitizing pathways. Endocrinology. 2009a;150(5):2098–108.PubMedCrossRef
30.
go back to reference Burgess A, Li M, Vanella L, et al. Adipocyte heme oxygenase-1 induction attenuates metabolic syndrome in both male and female obese mice. Hypertension. 2010;56(6):1124–30.PubMedPubMedCentralCrossRef Burgess A, Li M, Vanella L, et al. Adipocyte heme oxygenase-1 induction attenuates metabolic syndrome in both male and female obese mice. Hypertension. 2010;56(6):1124–30.PubMedPubMedCentralCrossRef
31.
go back to reference Peterson SJ, Drummond G, Kim DH, et al. L-4F treatment reduces adiposity, increases adiponectin levels, and improves insulin sensitivity in obese mice. J Lipid Res. 2008;49(8):1658–69.PubMedPubMedCentralCrossRef Peterson SJ, Drummond G, Kim DH, et al. L-4F treatment reduces adiposity, increases adiponectin levels, and improves insulin sensitivity in obese mice. J Lipid Res. 2008;49(8):1658–69.PubMedPubMedCentralCrossRef
32.
go back to reference Nicolai A, Li M, Kim DH, et al. Heme oxygenase-1 induction remodels adipose tissue and improves insulin sensitivity in obesity-induced diabetic rats. Hypertension. 2009;53(3):508–15.PubMedPubMedCentralCrossRef Nicolai A, Li M, Kim DH, et al. Heme oxygenase-1 induction remodels adipose tissue and improves insulin sensitivity in obesity-induced diabetic rats. Hypertension. 2009;53(3):508–15.PubMedPubMedCentralCrossRef
33.
go back to reference Lehr S, Hartwig S, Lamers D, et al. Identification and validation of novel adipokines released from primary human adipocytes. Mol Cell Proteomics. 2012;11(1):M111.010504.PubMedCrossRef Lehr S, Hartwig S, Lamers D, et al. Identification and validation of novel adipokines released from primary human adipocytes. Mol Cell Proteomics. 2012;11(1):M111.010504.PubMedCrossRef
34.
go back to reference Shakeri-Manesch S, Zeyda M, Huber J, et al. Diminished upregulation of visceral adipose heme oxygenase-1 correlates with waist-to-hip ratio and insulin resistance. Int J Obes. 2009;33(11):1257–64.CrossRef Shakeri-Manesch S, Zeyda M, Huber J, et al. Diminished upregulation of visceral adipose heme oxygenase-1 correlates with waist-to-hip ratio and insulin resistance. Int J Obes. 2009;33(11):1257–64.CrossRef
35.
go back to reference Jais A, Einwallner E, Sharif O, et al. Heme oxygenase-1 drives metaflammation and insulin resistance in mouse and man. Cell. 2014;158(1):25–40.PubMedCrossRef Jais A, Einwallner E, Sharif O, et al. Heme oxygenase-1 drives metaflammation and insulin resistance in mouse and man. Cell. 2014;158(1):25–40.PubMedCrossRef
36.
go back to reference Kobayashi M, Miyazawa N, Takeno M, et al. Circulating carbon monoxide level is elevated after sleep in patients with obstructive sleep apnea. Chest. 2008;134(5):904–10.PubMedCrossRef Kobayashi M, Miyazawa N, Takeno M, et al. Circulating carbon monoxide level is elevated after sleep in patients with obstructive sleep apnea. Chest. 2008;134(5):904–10.PubMedCrossRef
37.
go back to reference Hoffmann MS, Singh P, Wolk R, et al. Microarray studies of genomic oxidative stress and cell cycle responses in obstructive sleep apnea. Antioxid Redox Signal. 2007;9(6):661–9.PubMedCrossRef Hoffmann MS, Singh P, Wolk R, et al. Microarray studies of genomic oxidative stress and cell cycle responses in obstructive sleep apnea. Antioxid Redox Signal. 2007;9(6):661–9.PubMedCrossRef
38.
go back to reference Fried M, Yumuk V, Oppert JM, et al. Interdisciplinary European guidelines on metabolic and bariatric surgery. Rozhl Chir. 2014;93(7):366–78.PubMed Fried M, Yumuk V, Oppert JM, et al. Interdisciplinary European guidelines on metabolic and bariatric surgery. Rozhl Chir. 2014;93(7):366–78.PubMed
39.
go back to reference Baltasar A, Perez N, Serra C, et al. Weight loss reporting: predicted body mass index after bariatric surgery. Obes Surg. 2011;21(3):367–72.PubMedCrossRef Baltasar A, Perez N, Serra C, et al. Weight loss reporting: predicted body mass index after bariatric surgery. Obes Surg. 2011;21(3):367–72.PubMedCrossRef
40.
go back to reference Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–9.PubMedCrossRef Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–9.PubMedCrossRef
41.
go back to reference Sleep-related breathing disorders in adults: recommendations for syndrome definition and measurement techniques in clinical research. The report of an American Academy of Sleep Medicine Task Force. Sleep. 1999;22(5):667–89.CrossRef Sleep-related breathing disorders in adults: recommendations for syndrome definition and measurement techniques in clinical research. The report of an American Academy of Sleep Medicine Task Force. Sleep. 1999;22(5):667–89.CrossRef
42.
go back to reference Berry RB, Budhiraja R, Gottlieb DJ, et al. Rules for scoring respiratory events in sleep: update of the 2007 AASM Manual for the Scoring of Sleep and Associated Events. Deliberations of the Sleep Apnea Definitions Task Force of the American Academy of Sleep Medicine. J Clin Sleep Med. 2012;8(5):597–619.PubMedPubMedCentral Berry RB, Budhiraja R, Gottlieb DJ, et al. Rules for scoring respiratory events in sleep: update of the 2007 AASM Manual for the Scoring of Sleep and Associated Events. Deliberations of the Sleep Apnea Definitions Task Force of the American Academy of Sleep Medicine. J Clin Sleep Med. 2012;8(5):597–619.PubMedPubMedCentral
43.
go back to reference Ndisang JF, Jadhav A. Up-regulating the hemeoxygenase system enhances insulin sensitivity and improves glucose metabolism in insulin-resistant diabetes in Goto-Kakizaki rats. Endocrinology. 2009;150(6):2627–36.PubMedCrossRef Ndisang JF, Jadhav A. Up-regulating the hemeoxygenase system enhances insulin sensitivity and improves glucose metabolism in insulin-resistant diabetes in Goto-Kakizaki rats. Endocrinology. 2009;150(6):2627–36.PubMedCrossRef
44.
go back to reference Yang L, Quan S, Nasjletti A, et al. Heme oxygenase-1 gene expression modulates angiotensin II-induced increase in blood pressure. Hypertension. 2004;43(6):1221–6.PubMedCrossRef Yang L, Quan S, Nasjletti A, et al. Heme oxygenase-1 gene expression modulates angiotensin II-induced increase in blood pressure. Hypertension. 2004;43(6):1221–6.PubMedCrossRef
45.
go back to reference Li M, Kim DH, Tsenovoy PL, et al. Treatment of obese diabetic mice with a heme oxygenase inducer reduces visceral and subcutaneous adiposity, increases adiponectin levels, and improves insulin sensitivity and glucose tolerance. Diabetes. 2008;57(6):1526–35.PubMedCrossRef Li M, Kim DH, Tsenovoy PL, et al. Treatment of obese diabetic mice with a heme oxygenase inducer reduces visceral and subcutaneous adiposity, increases adiponectin levels, and improves insulin sensitivity and glucose tolerance. Diabetes. 2008;57(6):1526–35.PubMedCrossRef
46.
go back to reference Peterson SJ, Kim DH, Li M, et al. The L-4F mimetic peptide prevents insulin resistance through increased levels of HO-1, pAMPK, and pAKT in obese mice. J Lipid Res. 2009;50(7):1293–304.PubMedPubMedCentralCrossRef Peterson SJ, Kim DH, Li M, et al. The L-4F mimetic peptide prevents insulin resistance through increased levels of HO-1, pAMPK, and pAKT in obese mice. J Lipid Res. 2009;50(7):1293–304.PubMedPubMedCentralCrossRef
47.
go back to reference Cao J, Peterson SJ, Sodhi K, et al. Heme oxygenase gene targeting to adipocytes attenuates adiposity and vascular dysfunction in mice fed a high-fat diet. Hypertension. 2012;60(2):467–75.PubMedPubMedCentralCrossRef Cao J, Peterson SJ, Sodhi K, et al. Heme oxygenase gene targeting to adipocytes attenuates adiposity and vascular dysfunction in mice fed a high-fat diet. Hypertension. 2012;60(2):467–75.PubMedPubMedCentralCrossRef
48.
go back to reference Ndisang JF, Lane N, Jadhav A. Upregulation of the heme oxygenase system ameliorates postprandial and fasting hyperglycemia in type 2 diabetes. Am J Physiol Endocrinol Metab. 2009b;296(5):E1029–41.PubMedCrossRef Ndisang JF, Lane N, Jadhav A. Upregulation of the heme oxygenase system ameliorates postprandial and fasting hyperglycemia in type 2 diabetes. Am J Physiol Endocrinol Metab. 2009b;296(5):E1029–41.PubMedCrossRef
49.
go back to reference Wang XQ, Luo NS, Salah ZQ, et al. Atorvastatin attenuates TNF-alpha production via heme oxygenase-1 pathway in LPS-stimulated RAW264.7 macrophages. Biomed Environ Sci. 2014;27(10):786–93.PubMed Wang XQ, Luo NS, Salah ZQ, et al. Atorvastatin attenuates TNF-alpha production via heme oxygenase-1 pathway in LPS-stimulated RAW264.7 macrophages. Biomed Environ Sci. 2014;27(10):786–93.PubMed
50.
go back to reference Bao W, Song F, Li X, et al. Plasma heme oxygenase-1 concentration is elevated in individuals with type 2 diabetes mellitus. PLoS One. 2010;5(8):e12371.PubMedPubMedCentralCrossRef Bao W, Song F, Li X, et al. Plasma heme oxygenase-1 concentration is elevated in individuals with type 2 diabetes mellitus. PLoS One. 2010;5(8):e12371.PubMedPubMedCentralCrossRef
51.
go back to reference Di Raimondo D, Tuttolomondo A, Buttà C, et al. Effects of ACE-inhibitors and angiotensin receptor blockers on inflammation. Curr Pharm Des. 2012;18(28):4385–413.PubMedCrossRef Di Raimondo D, Tuttolomondo A, Buttà C, et al. Effects of ACE-inhibitors and angiotensin receptor blockers on inflammation. Curr Pharm Des. 2012;18(28):4385–413.PubMedCrossRef
52.
go back to reference Krysiak R, Zmuda W, Okopien B. The effect of simvastatin-ezetimibe combination therapy on adipose tissue hormones and systemic inflammation in patients with isolated hypercholesterolemia. Cardiovasc Ther. 2014;32(2):40–6.PubMedCrossRef Krysiak R, Zmuda W, Okopien B. The effect of simvastatin-ezetimibe combination therapy on adipose tissue hormones and systemic inflammation in patients with isolated hypercholesterolemia. Cardiovasc Ther. 2014;32(2):40–6.PubMedCrossRef
53.
go back to reference Leung PO, Wang SH, Lu SH, et al. Simvastatin inhibits pro-inflammatory mediators through induction of heme oxygenase-1 expression in lipopolysaccharide-stimulated RAW264.7 macrophages. Toxicol Lett. 2011;207(2):159–66.PubMedCrossRef Leung PO, Wang SH, Lu SH, et al. Simvastatin inhibits pro-inflammatory mediators through induction of heme oxygenase-1 expression in lipopolysaccharide-stimulated RAW264.7 macrophages. Toxicol Lett. 2011;207(2):159–66.PubMedCrossRef
54.
go back to reference Arnardottir ES, Maislin G, Schwab RJ, et al. The interaction of obstructive sleep apnea and obesity on the inflammatory markers C-reactive protein and interleukin-6: the Icelandic Sleep Apnea Cohort. Sleep. 2012;35(7):921–32.PubMedPubMedCentral Arnardottir ES, Maislin G, Schwab RJ, et al. The interaction of obstructive sleep apnea and obesity on the inflammatory markers C-reactive protein and interleukin-6: the Icelandic Sleep Apnea Cohort. Sleep. 2012;35(7):921–32.PubMedPubMedCentral
55.
go back to reference Ekstedt M, Akerstedt T, Söderström M. Microarousals during sleep are associated with increased levels of lipids, cortisol, and blood pressure. Psychosom Med. 2004;66(6):925–31.PubMedCrossRef Ekstedt M, Akerstedt T, Söderström M. Microarousals during sleep are associated with increased levels of lipids, cortisol, and blood pressure. Psychosom Med. 2004;66(6):925–31.PubMedCrossRef
Metadata
Title
Impact of Bariatric Surgery on Heme Oxygenase-1, Inflammation, and Insulin Resistance in Morbid Obesity with Obstructive Sleep Apnea
Authors
Raquel Tirado
Maria José Masdeu
Laura Vigil
Mercedes Rigla
Alexis Luna
Pere Rebasa
Rocío Pareja
Marta Hurtado
Assumpta Caixàs
Publication date
01-09-2017
Publisher
Springer US
Published in
Obesity Surgery / Issue 9/2017
Print ISSN: 0960-8923
Electronic ISSN: 1708-0428
DOI
https://doi.org/10.1007/s11695-017-2635-4

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