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Original Article |

Plasma Levels of MCP-1 and Adiponectin in Obstructive Sleep Apnea Syndrome FREE

Joohwan Kim, MD; Chang Hoon Lee, MD; Chan Soon Park, MD; Byung Guk Kim, MD; Soo Whan Kim, MD; Jin Hee Cho, MD
[+] Author Affiliations

Author Affiliations: Departments of Otorhinolaryngology–Head and Neck Surgery, College of Medicine, The Catholic University of Korea, Seoul (Drs J. Kim, Park, B. G. Kim, S. W. Kim, and Cho), and Woori Medical Clinic, Pyeongtaek-si, Gyeonggi-do, Korea (Dr Lee).


Arch Otolaryngol Head Neck Surg. 2010;136(9):896-899. doi:10.1001/archoto.2010.142.
Text Size: A A A
Published online

Objectives  To evaluate the correlation between concentrations of the proinflammatory cytokines monocyte chemotactic protein 1 (MCP-1), adiponectin, interleukin 6 (IL-6), interleukin 8 (IL-8), and tumor necrosis factor (TNF) and patients with obstructive sleep apnea syndrome (OSAS). Repeated apnea attacks in patients with OSAS constitute a hypoxic condition, which induces tissue inflammation by mediation of these proinflammatory cytokines.

Design  Radioimmunoassay analyses of nonrandomized controlled trial.

Setting  University-affiliated tertiary care hospital.

Patients  The study population comprised 59 patients who underwent the polysomnography.

Main Outcome Measures  Serum concentrations of MCP-1, adiponectin, IL-6, IL-8, and TNF, as well as body mass index and polysomnographic data, including apnea-hypopnea index (AHI) and lowest oxygen saturation.

Results  The mean (SD) plasma level of MCP-1 in serum was increased in all patients with OSAS (P < .001), while adiponectin level was decreased in the patients with severe OSAS (6.88 [1.78] μg/mL) compared with normal controls (8.90 [2.63] μg/mL) (P = .006). Serum concentrations of IL-6, IL-8, and TNF did not exhibit any differences between patients with OSAS and normal controls. The correlation coefficient between plasma MCP-1 level and AHI was 0.62 and between adiponectin level and AHI was 0.66.

Conclusions  Our results suggest that plasma MCP-1 and adiponectin levels were different between patients with OSAS and normal controls. Adiponectin and MCP-1 may be prognostic factors for comparing patients with OSAS before and after treatment.

Figures in this Article

Obstructive sleep apnea (OSA) repeatedly causes low oxygen (O2) saturation during sleep. This causes functional abnormality in vascular endothelial cells and increases the risk of cardiovascular diseases such as artherosclerosis.13 Hypoxia is known to be associated with a series of inflammatory responses through the induction of adhesion molecules and C-reactive protein in vascular endothelial cells and leukocytes.4,5 Obstructive sleep apnea is also involved in various metabolic dysfunctions such as insulin resistance with or without obesity.6,7 Despite an increased heart rate, circulating blood flow, O2 consumption, and overall blood flow in patients with severe obesity do not change and the O2 level in the arterial blood is relatively decreased. Moreover, enlarged adipose cells need more O2, hypoxic condition gradually induces tissue inflammation, and adipose tissues release materials to overcome cardiovascular disease.

Monocyte chemotactic protein 1 (MCP-1) is the cytokine that integrates the migration of leukocytes or monocytes to inflammatory tissue. A transient or repeated hypoxia induced by OSA increases the cellular adhesion of inflammatory cells and results in the atherosclerosis by the mediation of this proinflammatory cytokine in vascular endothelial cells.8 Adiponectin, one of the materials released from adipose cells, has an anti-inflammatory effect. Its plasma concentration is low in patients with obesity compared with healthy individuals. This has been known to affect the increased prevalence of cardiovascular diseases.9 Chronic hypoxic condition also contributes to the low level of adiponectin. Serum adiponectin has been reported to be decreased in patients with sleep apnea with a high apnea-hypopnea index (AHI).9,10 Some famous proinflammatory cytokines such as interleukin 6 (IL-6), interleukin 8 (IL-8), and tumor necrosis factor (TNF) were proven to raise the risk of developing cardiovascular disease.

Although there have been so many studies that deal with cytokines, especially adiponectin, the studies on other hypoxia-sensitive molecules such as MCP-1, IL-6, and TNF are hard to find. The purpose of the present study was to examine proinflammatory cytokines such as MCP-1, IL-6, IL-8, and TNF, as well as adiponectin in patients with OSA syndrome (OSAS) and define the correlation between such cytokines and the severity of OSAS.

Among the patients who had visited the department of otorhinolaryngology clinic for evaluation of sleep problems, 59 were selected. Polysomnography (PSG) was performed in all the patients, and 37 patients were diagnosed as having OSAS, with an AHI exceeding 5. History of diabetes, hypertension, or chronic pulmonary disease was checked by blood test and radiologic evaluation, and those with any of these conditions were excluded. The patients with other cardiovascular disease and metabolic disorders were excluded as well.

Apnea was defined as a complete lack of air flow for at least 10 seconds. Hypopnea was defined as a decreased O2 saturation by more than 4% for at least 10 seconds. Apnea-hypopnea index was defined as the frequency of apnea and hypopnea per 1 hour. We defined OSAS as cases in which AHI exceeded 5. Moderate severity was classified in patients whose AHI ranged between 5 and 20. Severe OSAS was defined when AHI exceeded 20. Patients in the normal control group consisted of those who had an AHI lower than 5 and no complaint of sleep apnea. Body mass index (BMI), a statistical measurement that compares a person's weight and height, was calculated as weight in kilograms divided by the height in meters squared.

Blood sampling was performed prior to PSG at 8 to 10 PM. After 10 minutes of centrifugation, plasma was isolated. For measurement of the concentrations of MCP-1, adiponectin, IL-6, IL-8, and TNF in plasma, a radioimmunoassay was performed using Human Adipokine Kit (Linco Research Inc, St Charles, Missouri). Each specimen was diluted 1-, 2-, and 4-fold. Assay buffer and mixed beads were added in a microwell whose surface was coated with antibodies against antihuman MCP-1, adiponectin, IL-6, IL-8, and TNF. The reaction was performed at room temperature for 2 hours. After rinsing, each antibody was added for conjugation to the enzyme. This reaction was performed at room temperature for more than 1 hour. By adding enzyme substrate solution, the reaction was performed at room temperature for approximately 30 minutes. After adding the stopping solution, the absorbance was measured using an enzyme-linked immunosorbent assay (ELISA) plate reader at a wavelength of 450 nm.

Statistical analysis was carried out using SPSS version 12.0 software program (SPSS Inc, Chicago, Illinois) and bivariates correlation test was used to determine the relation between each cytokine and sleep apnea. A coefficient of correlation was obtained with the same program. Statistical significance was set at a P value of .01. Informed consent was obtained from all participants, and our institutional review board approved this study.

A total of 48 male and 11 female patients were analyzed. The mean age was 36 years. The normal control group consisted of 21 patients with normal findings on PSG. Among 37 patients, 28 with an AHI exceeding 20 on PSG were classified as the severe OSAS group and 9 with an AHI less than 20 as the moderate OSAS group.

The mean (SD) BMI of the normal control, moderate, and severe OSAS groups were 23.88 (2.30), 24.43 (2.45), and 28.69 (4.05), respectively. There were no statistical differences among the groups. The mean (SD) minimal O2 saturation of the moderate OSAS group was 85.67% (3.30%) compared with 74.79% (6.86%) in the severe group (Table). The serum concentration of MCP-1, adiponectin, IL-6, IL-8, and TNF are also given in the Table.

Table Graphic Jump LocationTable. Mean (SD) Measurements in Each Group

The serum concentration of MCP-1 of the normal control group was lower than that of the OSAS groups (P < .001), and the difference between the 2 OSAS groups was statistically significant (P < .001). The mean (SD) adiponectin level of normal control was 8.90 (2.63) μg/mL, which was higher than that of the severe OSAS group with a statistical significance (P = .006). However, there was no difference between normal controls and the moderate OSAS group (P = .25). There were no differences among groups in serum concentrations of IL-6, IL-8, and TNF (P = .21, .38, and .18, respectively).

Between the 2 OSAS groups, serum concentration of MCP-1 was positively correlated with BMI (r = 0.59) and AHI (r = 0.62) after bivariates analysis (Figure 1). Serum adiponectin was positively correlated with BMI (r = 0.44) and AHI (r = 0.66) (Figure 2).

Place holder to copy figure label and caption
Figure 1.

A, Scatterplot of correlation between the plasma level of MCP-1 and AHI in the patients with obstructive sleep apnea syndrome; B, correlation between MCP-1 and BMI. AHI indicates apnea-hypopnea index; BMI, body mass index (calculated as weight in kilograms divided by height in meters squared); MCP-1, monocyte chemotactic protein 1.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

A, Scatterplot of correlation between the plasma level of adiponectin and AHI in the patients with obstructive sleep apnea syndrome; B, correlation between adiponectin and BMI. AHI indicates apnea-hypopnea index; BMI, body mass index (calculated as weight in kilograms divided by height in meters squared).

Graphic Jump Location

Repeated hypoxic condition in the patients with OSAS resulted in a change of plasma concentration of TH1-type cytokine originating from immune cells in peripheral blood.11,12 It is also proved that hypoxia increases the expression of proinflammatory molecules such as IL-1β, IL-6, and TNF.13,14 The patients with metabolic disorder, including obesity, showed increased expression of IL-6, IL-8, and TNF, and elevated levels of these cytokines increase the possibility of cardiovascular diseases.15,16 The repeated OSA attacks aggravate hypoxia, especially in enlarged adipose tissue, and this induces more proinflammatory cytokines in plasma. Obese patients are usually exposed to the hypoxic condition without any increased blood flow, although they need more O2 consumption because of increased body mass. It has been reported that hyperventilation, which increases the level of O2 saturation, or the use of continuous positive airway pressure for the management of OSAS will decrease the plasma level of these cytokines in several months.1719 Moreover, the change of serum level of proinflammatory cytokines will be helpful in monitoring the efficacy of treatment of OSAS.

Monocyte chemotactic protein 1 is one of the proinflammatory cytokines that facilitates leukocyte migration to inflamed tissue by leukocyte's ability to adhere to microvascular endothelium.20 It is upregulated in human atherosclerotic plaques, suggesting a role in the development of atherosclerotic lesions. Monocyte chemotactic protein 1 is also known to have a strong correlation in the patients with diabetes or obesity.8 Ohga et al20 showed that MCP-1 levels were increased in patients with OSAS compared with normal controls. These authors also noted that MCP-1 levels were decreased after the use of continuous positive airway pressure. Hayashi et al21 reported on its close relationship with AHI, although there was no significant correlation between MCP-1 and BMI. Our series showed a correlation coefficient of 0.62 between the MCP-1 and AHI, which is similar to their result of the positive correlation with BMI (r = 0.59) and age (r = 0.37).21

Adiponectin, one of the various adipocyte-derived biologically active peptides, has received considerable attention owing to its association with several cardiovascular risk factors.22 Some diseases such as coronary heart disease, dyslipidemia, insulin resistance, and type 2 diabetes mellitus were shown to be related to reduced plasma adiponectin levels. The presence of adiponectin might have an effect on obesity or metabolic diseases in patients with OSAS. Wolk et al22 reported that adiponectin had a higher correlation to AHI compared with various factors associated with obesity (eg, BMI).23,24 According to Tokuda et al25 and Shand et al,26 there was no significant difference in the concentration of serum adiponectin between patients with OSA and the normal control group. These authors also noted that there was a significant correlation between serum adiponectin level and age. Controversial opinions still exist regarding adiponectin in patients with OSAS. In our series, adiponectin had a stronger correlation with AHI (r = 0.66) compared with age and AHI (r = 0.35) or BMI and AHI (r = 0.44). These results indicate that adiponectin has more influence on AHI compared with other factors in patients with OSAS.

Interleukin 6, IL-8, and TNF are well-known proinflammatory cytokines that are proven to be elevated in patients with OSAS and have been proposed as the mediators of muscle weakness.27 Interestingly, there were no significant correlations between their concentrations and AHI. Presumably, this might be the result of their short half-life and instability to the stimulation.

There were some differences in plasma concentration between the OSAS groups. The serum level of MCP-1 in the normal control group was lower than in the OSAS groups, and the less severe patients had lower serum MCP-1 levels compared with the more severe ones (P < .001). There was no difference in the serum level of adiponectin between the moderate and severe OSAS groups (P = .10), whereas that of the normal control group was higher than in the severe group (P = .006). There were also no differences between groups in serum levels of IL-6, IL-8, and TNF.

Generally, Asian people have more frequent hypoxic events compared with white people with comparable BMIs because of their physical characteristics.28,29 According to Li et al,28 Asian people had a mean (SD) AHI of 56.6 (34.9), with a BMI of 26.6 (3.7), whereas white people had an AHI of 55.6 (26.9), with BMI of 30.7 (5.9). That is to say, compared with whites, Asians with a lower BMI had approximately the same AHI. Scharf et al29 reported that the mean (SD) BMI was 33.4 (9.2) and mean (SD) AHI was 33.4 (26.8) in whites. In our series, mean (SD) AHI was 52.71 (22.23), with a mean (SD) BMI of 28.69 (4.05) in the severe OSAS group, a result that is similar to Asians in the report by Li et al.28 The population who were diagnosed as having severe OSAS without a high degree of obesity is relatively greater compared with that of whites without a high degree of obesity. A greater number of patients with higher AHIs and the same BMI as whites suggests that the diagnosis and treatment should be performed based on the different criteria from whites in the Asian clinical setting.

Recently, PSG became a first choice for the diagnosis of sleep disorder. However, its use is limited because it is expensive and inconvenient and needs special facilities and a specialist for analysis. Adiponectin and MCP-1 can be more reasonable alternatives to PSG for predicting the prognosis and confirming the effect of treatment because of their convenience and cost-effectiveness. The concentration of serum MCP-1 had a greater change in measurement according to the severity of OSAS than adiponectin. Accordingly, MCP-1 might be more useful as an indicator for predicting the occurrence of OSA than adiponectin.

Body mass index, our primary measure of obesity, usually does not fully characterize the distribution of body fat, and the distribution of BMI is not homogenized in each subgroup. This makes it difficult to confirm the independent effects of obesity or AHI in each group. For the clinical application, a systematized investigation to identify the correlations between obesity and proinflammatory molecules, and a larger-scale study with quantitative measurements is warranted.

In conclusion, patients with OSAS had a relatively higher serum MCP-1 level and a lower adiponectin level compared with the normal control group. Adiponectin and MCP-1 are associated with OSAS and might be useful indicators for comparing the postoperative and preoperative status and estimating the prognosis.

Correspondence: Jin Hee Cho, MD, Department of Otorhinolaryngology–Head and Neck Surgery, College of Medicine, The Catholic University of Korea, 62 Yeuido-dong, Yeongdeungpo-gu, Seoul 150-713, Korea (entcho@catholic.ac.kr).

Submitted for Publication: December 31, 2009; accepted April 29, 2010.

Author Contributions: Drs J. Kim, Lee, and Cho had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: J. Kim, Lee, and Cho. Acquisition of data: Lee and S. W. Kim. Analysis and interpretation of data: Park and B. G. Kim. Drafting of the manuscript: J. Kim, Lee, Park, B. G. Kim, S. W. Kim, and Cho. Critical revision of the manuscript for important intellectual content: J. Kim, S. W. Kim, and Cho. Statistical analysis: Park and B. G. Kim. Administrative, technical, and material support: Lee. Study supervision: J. Kim, S. W. Kim, and Cho.

Financial Disclosure: None reported.

Shahar  EWhitney  CWRedline  S  et al.  Sleep-disordered breathing and cardiovascular disease: cross-sectional results of the Sleep Heart Health Study. Am J Respir Crit Care Med 2001;163 (1) 19- 25
PubMed Link to Article
Peters  RW Obstructive sleep apnea and cardiovascular disease. Chest 2005;127 (1) 1- 3
PubMed Link to Article
Shamsuzzaman  ASGersh  BJSomers  VK Obstructive sleep apnea: implications for cardiac and vascular disease. JAMA 2003;290 (14) 1906- 1914
PubMed Link to Article
El-Solh  AAMador  MJSikka  PDhillon  RSAmsterdam  DGrant  BJ Adhesion molecules in patients with coronary artery disease and moderate-to-severe obstructive sleep apnea. Chest 2002;121 (5) 1541- 1547
PubMed Link to Article
Yokoe  TMinoguchi  KMatsuo  H  et al.  Elevated levels of C-reactive protein and interleukin-6 in patients with obstructive sleep apnea syndrome are decreased by nasal continuous positive airway pressure. Circulation 2003;107 (8) 1129- 1134
PubMed Link to Article
Makino  SHanda  HSuzukawa  K  et al.  Obstructive sleep apnoea syndrome, plasma adiponectin levels, and insulin resistance. Clin Endocrinol (Oxf) 2006;64 (1) 12- 19
PubMed Link to Article
Punjabi  NMSorkin  JDKatzel  LIGoldberg  APSchwartz  ARSmith  PL Sleep-disordered breathing and insulin resistance in middle-aged and overweight men. Am J Respir Crit Care Med 2002;165 (5) 677- 682
PubMed Link to Article
Hojo  YIkeda  UTakahashi  MShimada  K Increased levels of monocyte-related cytokines in patients with unstable angina. Atherosclerosis 2002;161 (2) 403- 408
PubMed Link to Article
Kabon  BNagele  AReddy  D  et al.  Obesity decreases perioperative tissue oxygenation. Anesthesiology 2004;100 (2) 274- 280
PubMed Link to Article
Wajchenberg  BL Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev 2000;21 (6) 697- 738
PubMed Link to Article
Dimitrov  SLange  TTieken  SFehm  HLBorn  J Sleep associated regulation of T helper 1/T helper 2 cytokine balance in humans. Brain Behav Immun 2004;18 (4) 341- 348
PubMed Link to Article
Redwine  LDang  JHall  MIrwin  M Disordered sleep, nocturnal cytokines, and immunity in alcoholics. Psychosom Med 2003;65 (1) 75- 85
PubMed Link to Article
Naldini  ACarraro  FSilvestri  SBocci  V Hypoxia affects cytokine production and proliferative responses by human peripheral mononuclear cells. J Cell Physiol 1997;173 (3) 335- 342
PubMed Link to Article
Hempel  SLMonick  MMHunninghake  GW Effect of hypoxia on release of IL-1 and TNF by human alveolar macrophages. Am J Respir Cell Mol Biol 1996;14 (2) 170- 176
PubMed Link to Article
Cancello  RTounian  APoitou  ChClément  K Adiposity signals, genetic and body weight regulation in humans. Diabetes Metab 2004;30 (3) 215- 227
PubMed Link to Article
Trayhurn  PWood  IS Adipokines: inflammation and the pleiotropic role of white adipose tissue. Br J Nutr 2004;92 (3) 347- 355
PubMed Link to Article
Enoz  MInancli  HM CPAP and measures of cardiovascular risks in patients with OSAS. Eur Respir J 2009;33 (6) 1520
PubMed Link to Article
Zhang  XLYin  KSLi  CJia  EZLi  YQGao  ZF Effect of continuous positive airway pressure treatment on serum adiponectin level and mean arterial pressure in male patients with obstructive sleep apnea syndrome. Chin Med J (Engl) 2007;120 (17) 1477- 1481
PubMed
Tam  CSWong  MTam  KAouad  LWaters  KA The effect of acute intermittent hypercapnic hypoxia treatment on IL-6, TNF-alpha, and CRP levels in piglets. Sleep 2007;30 (6) 723- 727
PubMed
Ohga  ETomita  TWada  HYamamoto  HNagase  TOuchi  Y Effects of obstructive sleep apnea on circulating ICAM-1, IL-8, and MCP-1. J Appl Physiol 2003;94 (1) 179- 184
PubMed
Hayashi  MFujimoto  KUrushibata  KTakamizawa  AKinoshita  OKubo  K Hypoxia-sensitive molecules may modulate the development of atherosclerosis in sleep apnoea syndrome. Respirology 2006;11 (1) 24- 31
PubMed Link to Article
Wolk  RSvatikova  ANelson  CA  et al.  Plasma levels of adiponectin, a novel adipocyte-derived hormone, in sleep apnea. Obes Res 2005;13 (1) 186- 190
PubMed Link to Article
Masserini  BMorpurgo  PSDonadio  F  et al.  Reduced levels of adiponectin in sleep apnea syndrome. J Endocrinol Invest 2006;29 (8) 700- 705
PubMed Link to Article
Zhang  XLYin  KSWang  HSu  S Serum adiponectin levels in adult male patients with obstructive sleep apnea hypopnea syndrome. Respiration 2006;73 (1) 73- 77
PubMed Link to Article
Tokuda  FSando  YMatsui  HKoike  HYokoyama  T Serum levels of adipocytokines, adiponectin and leptin, in patients with obstructive sleep apnea syndrome. Intern Med 2008;47 (21) 1843- 1849
PubMed Link to Article
Shand  BIScott  RSElder  PAGeorge  PM Plasma adiponectin in overweight, nondiabetic individuals with or without insulin resistance. Diabetes Obes Metab 2003;5 (5) 349- 353
PubMed Link to Article
Marais  J The value of sedation nasendoscopy: a comparison between snoring and non-snoring patients. Clin Otolaryngol Allied Sci 1998;23 (1) 74- 76
PubMed Link to Article
Li  KKPowell  NBKushida  CRiley  RWAdornato  BGuilleminault  C A comparison of Asian and white patients with obstructive sleep apnea syndrome. Laryngoscope 1999;109 (12) 1937- 1940
PubMed Link to Article
Scharf  SMSeiden  LDeMore  JCarter-Pokras  O Racial differences in clinical presentation of patients with sleep-disordered breathing. Sleep Breath 2004;8 (4) 173- 183
PubMed Link to Article

Figures

Place holder to copy figure label and caption
Figure 1.

A, Scatterplot of correlation between the plasma level of MCP-1 and AHI in the patients with obstructive sleep apnea syndrome; B, correlation between MCP-1 and BMI. AHI indicates apnea-hypopnea index; BMI, body mass index (calculated as weight in kilograms divided by height in meters squared); MCP-1, monocyte chemotactic protein 1.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

A, Scatterplot of correlation between the plasma level of adiponectin and AHI in the patients with obstructive sleep apnea syndrome; B, correlation between adiponectin and BMI. AHI indicates apnea-hypopnea index; BMI, body mass index (calculated as weight in kilograms divided by height in meters squared).

Graphic Jump Location

Tables

Table Graphic Jump LocationTable. Mean (SD) Measurements in Each Group

References

Shahar  EWhitney  CWRedline  S  et al.  Sleep-disordered breathing and cardiovascular disease: cross-sectional results of the Sleep Heart Health Study. Am J Respir Crit Care Med 2001;163 (1) 19- 25
PubMed Link to Article
Peters  RW Obstructive sleep apnea and cardiovascular disease. Chest 2005;127 (1) 1- 3
PubMed Link to Article
Shamsuzzaman  ASGersh  BJSomers  VK Obstructive sleep apnea: implications for cardiac and vascular disease. JAMA 2003;290 (14) 1906- 1914
PubMed Link to Article
El-Solh  AAMador  MJSikka  PDhillon  RSAmsterdam  DGrant  BJ Adhesion molecules in patients with coronary artery disease and moderate-to-severe obstructive sleep apnea. Chest 2002;121 (5) 1541- 1547
PubMed Link to Article
Yokoe  TMinoguchi  KMatsuo  H  et al.  Elevated levels of C-reactive protein and interleukin-6 in patients with obstructive sleep apnea syndrome are decreased by nasal continuous positive airway pressure. Circulation 2003;107 (8) 1129- 1134
PubMed Link to Article
Makino  SHanda  HSuzukawa  K  et al.  Obstructive sleep apnoea syndrome, plasma adiponectin levels, and insulin resistance. Clin Endocrinol (Oxf) 2006;64 (1) 12- 19
PubMed Link to Article
Punjabi  NMSorkin  JDKatzel  LIGoldberg  APSchwartz  ARSmith  PL Sleep-disordered breathing and insulin resistance in middle-aged and overweight men. Am J Respir Crit Care Med 2002;165 (5) 677- 682
PubMed Link to Article
Hojo  YIkeda  UTakahashi  MShimada  K Increased levels of monocyte-related cytokines in patients with unstable angina. Atherosclerosis 2002;161 (2) 403- 408
PubMed Link to Article
Kabon  BNagele  AReddy  D  et al.  Obesity decreases perioperative tissue oxygenation. Anesthesiology 2004;100 (2) 274- 280
PubMed Link to Article
Wajchenberg  BL Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev 2000;21 (6) 697- 738
PubMed Link to Article
Dimitrov  SLange  TTieken  SFehm  HLBorn  J Sleep associated regulation of T helper 1/T helper 2 cytokine balance in humans. Brain Behav Immun 2004;18 (4) 341- 348
PubMed Link to Article
Redwine  LDang  JHall  MIrwin  M Disordered sleep, nocturnal cytokines, and immunity in alcoholics. Psychosom Med 2003;65 (1) 75- 85
PubMed Link to Article
Naldini  ACarraro  FSilvestri  SBocci  V Hypoxia affects cytokine production and proliferative responses by human peripheral mononuclear cells. J Cell Physiol 1997;173 (3) 335- 342
PubMed Link to Article
Hempel  SLMonick  MMHunninghake  GW Effect of hypoxia on release of IL-1 and TNF by human alveolar macrophages. Am J Respir Cell Mol Biol 1996;14 (2) 170- 176
PubMed Link to Article
Cancello  RTounian  APoitou  ChClément  K Adiposity signals, genetic and body weight regulation in humans. Diabetes Metab 2004;30 (3) 215- 227
PubMed Link to Article
Trayhurn  PWood  IS Adipokines: inflammation and the pleiotropic role of white adipose tissue. Br J Nutr 2004;92 (3) 347- 355
PubMed Link to Article
Enoz  MInancli  HM CPAP and measures of cardiovascular risks in patients with OSAS. Eur Respir J 2009;33 (6) 1520
PubMed Link to Article
Zhang  XLYin  KSLi  CJia  EZLi  YQGao  ZF Effect of continuous positive airway pressure treatment on serum adiponectin level and mean arterial pressure in male patients with obstructive sleep apnea syndrome. Chin Med J (Engl) 2007;120 (17) 1477- 1481
PubMed
Tam  CSWong  MTam  KAouad  LWaters  KA The effect of acute intermittent hypercapnic hypoxia treatment on IL-6, TNF-alpha, and CRP levels in piglets. Sleep 2007;30 (6) 723- 727
PubMed
Ohga  ETomita  TWada  HYamamoto  HNagase  TOuchi  Y Effects of obstructive sleep apnea on circulating ICAM-1, IL-8, and MCP-1. J Appl Physiol 2003;94 (1) 179- 184
PubMed
Hayashi  MFujimoto  KUrushibata  KTakamizawa  AKinoshita  OKubo  K Hypoxia-sensitive molecules may modulate the development of atherosclerosis in sleep apnoea syndrome. Respirology 2006;11 (1) 24- 31
PubMed Link to Article
Wolk  RSvatikova  ANelson  CA  et al.  Plasma levels of adiponectin, a novel adipocyte-derived hormone, in sleep apnea. Obes Res 2005;13 (1) 186- 190
PubMed Link to Article
Masserini  BMorpurgo  PSDonadio  F  et al.  Reduced levels of adiponectin in sleep apnea syndrome. J Endocrinol Invest 2006;29 (8) 700- 705
PubMed Link to Article
Zhang  XLYin  KSWang  HSu  S Serum adiponectin levels in adult male patients with obstructive sleep apnea hypopnea syndrome. Respiration 2006;73 (1) 73- 77
PubMed Link to Article
Tokuda  FSando  YMatsui  HKoike  HYokoyama  T Serum levels of adipocytokines, adiponectin and leptin, in patients with obstructive sleep apnea syndrome. Intern Med 2008;47 (21) 1843- 1849
PubMed Link to Article
Shand  BIScott  RSElder  PAGeorge  PM Plasma adiponectin in overweight, nondiabetic individuals with or without insulin resistance. Diabetes Obes Metab 2003;5 (5) 349- 353
PubMed Link to Article
Marais  J The value of sedation nasendoscopy: a comparison between snoring and non-snoring patients. Clin Otolaryngol Allied Sci 1998;23 (1) 74- 76
PubMed Link to Article
Li  KKPowell  NBKushida  CRiley  RWAdornato  BGuilleminault  C A comparison of Asian and white patients with obstructive sleep apnea syndrome. Laryngoscope 1999;109 (12) 1937- 1940
PubMed Link to Article
Scharf  SMSeiden  LDeMore  JCarter-Pokras  O Racial differences in clinical presentation of patients with sleep-disordered breathing. Sleep Breath 2004;8 (4) 173- 183
PubMed Link to Article

Correspondence

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The American Medical Association is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. The AMA designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 CreditTM per course. Physicians should claim only the credit commensurate with the extent of their participation in the activity. Physicians who complete the CME course and score at least 80% correct on the quiz are eligible for AMA PRA Category 1 CreditTM.
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For CME Course: A Proposed Model for Initial Assessment and Management of Acute Heart Failure Syndromes
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