Physical Inactivity is Correlated With Levels of Quantitative C-Reactive Protein in Serum, Independent of Obesity Results of the National Surveillance of Risk Factors of Non-Communicable Diseases in Iran | C Reactive Protein

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J HEALTH POPUL NUTR 2012 Mar;30(1):66-72 ISSN 1606-0997 | $ 5.00+0.20 ©INTERNATIONAL CENTRE FOR DIARRHOEAL DISEASE RESEARCH, BANGLADESH Physical Inactivity Is Correlated with Levels of Quantitative C-reactive Protein in Serum, Independent of Obesity: Results of the National Surveillance of Risk Factors of Non-communicable Diseases in Iran Alireza Esteghamati, Afsaneh Morteza, Omid Khalilzadeh, Mehdi Anvari, Sina Noshad, Ali Zandieh, and Manouchehr Nakhjavani Endocrinology and Metabolism Resea
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  ©INTERNATIONAL CENTRE FOR DIARRHOEALDISEASE RESEARCH, BANGLADESH J HEALTH POPUL NUTR 2012 Mar;30(1):66-72ISSN 1606-0997|$ 5.00+0.20 Correspondence and reprint requests should beaddressed to:Dr. Alireza EsteghamatiProfessor of Endocrinology and MetabolismEndocrinology and Metabolism Research CenterVali-Asr Hospital, School of MedicineTehran University of Medical SciencesPO Box 13145-784, TehranIranEmail: esteghamati@tums.ac.irFax: +9821 64432466 Physical Inactivity Is Correlated with Levels of Quantitative C-reactive Protein in Serum, Independentof Obesity: Results of the National Surveillance of Risk Factors of Non-communicable Diseases in Iran Alireza Esteghamati, Afsaneh Morteza, Omid Khalilzadeh, Mehdi Anvari,Sina Noshad, Ali Zandieh, and Manouchehr Nakhjavani Endocrinology and Metabolism Research Center, Vali-Asr Hospital,School of Medicine, Tehran University of Medical Sciences, Tehran, Iran ABSTRACT Increased C-reactive protein (CRP) levels are associated with coronary heart disease, stroke, and mortality.Physical activity prevents cardiovascular disorders, which can be partly mediated through reducing inflam-mation, including serum CRP levels. The association of different intensities of physical activity, sedentarybehaviours, and C-reactive protein (CRP) levels in serum was examined after adjustment for markers of adiposity, including waist-circumference and body mass index (BMI), in a large population-based study.Using data of the SuRFNCD-2007 study, a large national representative population-based study in Iran, therelationship between quantitative CRP concentrations in serum and physical activity was examined in asample of 3,001 Iranian adults. The global physical activity questionnaire (GPAQ) was used for evaluatingthe duration and intensity of physical activity. Total physical activity (TPA) was calculated using metabolicequivalents for the intensity of physical activity. Quantitative CRP concentrations in serum were meas-ured with high-sensitivity enzyme immunoassay. The CRP levels in serum significantly correlated withTPA (r=-0.103, p=0.021 in men and r=-0.114, p=0.017 in women), duration of vigorous-intensity activity(r=-0.122, p=0.019 in men and r=-0.109, p=0.026 in women), duration of moderate-intensity activity (r=-0.107, p=0.031 in men and r=-0.118, p=0.020 in women), and duration of sedentary behaviours (r=0.092,p=0.029 in men and r=0.101, p=0.022 in women) after multiple adjustments for age, area of residence,BMI, waist-circumference, smoking, and diabetes mellitus. Physical activity (of both moderate and vigor-ous intensity) is inversely associated with the quantitative CRP levels in serum, independent of diabetesand body adiposity. Key words: Cardiovascular diseases; C-reactive protein; Physical activity; Physical exercise; Risk factors;Iran INTRODUCTION Adipose tissue in obesity, diabetes, and metabolicsyndrome is in a state of chronic inflammation(1-5). Quantitative C-reactive protein (CRP), anacute-phase reactant produced dominantly by liv-er, is a plasma protein that circulates in increasedamounts during inflammation and often damagesthe tissue (6,7). Results of studies showed that theincreased CRP levels were associated with func-tional impairment, coronary heart disease, stroke,and mortality (8). So, reducing the CRP levels canreduce mortality and morbidity due to cardiovas-cular disorders.Physical activity can prevent cardiovascular disor-ders (9). This effect can be partly mediated throughreducing inflammation, including serum CRP lev-els (10). Results of some population-based studiesshowed a negative association between physicalactivity and the circulating levels of CRP (7,10-14).However, the pattern of this association with res-pect to different intensities and metabolic equiva-  Esteghamati A et al. Volume 30|Number 1|March 2012 67 C-reactive protein and physical activity  lents (METs) of physical activity and several terti-ary factors, such as adiposity and glycaemic status,is not well-understood. Results of some studiesshowed that the impact of physical activity is me-diated through its weight-lowering effect (15,16).A study reported that the circulating levels of CRPcan be markedly suppressed, independent of totaladiposity or fat mass, by intense regular physicalexercise (17).The present study was carried out to examine theassociation among different intensities of physicalactivity (moderate and severe), total physical activi-ty (using METs for the intensity of activities), dura-tion of sedentary behaviours, and the serum CRPlevels after adjustment for glycaemic status andmarkers of adiposity, including waist-circumferenceand body mass index (BMI) in a large population-based sample of Iranian adults. Physical activitywas defined by an international standard question-naire, named global physical activity questionnaire(GPAQ). MATERIALS AND METHODSParticipants The study was based on data collected in the thirdnational surveillance of risk factors of non-com-municable diseases (SuRFNCD-2007). Details of the survey were reported elsewhere (18). In brief, acluster-sampling scheme was applied to randomlyselect a representative sample of Iranian adults aged25-64 years. The number of clusters selected fromeach province was proportional to the urban/ruralsize of that province. Trained healthcare profes-sionals conducted household interviews and physi-cal examinations. All interviews were conducted inPersian. Data were recorded in standardized sets of questionnaire. Blood sampling was done within afew days of the interview.The survey received ethical approval from the Cent-er for Disease Control of Iran, and written informedconsent was obtained from all the participants. Assessment of physical activity The second version of the GPAQ was used in thesurvey (19). This questionnaire, developed by theWorld Health Organization (WHO), contains 16questions about physical activity in a typical weekand assesses physical activity in three domains:work, transportation, and recreational activities.The evaluation of physical activity in these do-mains is one of the factors that make the GPAQ dis-tinct from other sets of questionnaire, such as theless-sophisticated, short version of the internation-al physical activity questionnaire (IPAQ) (http://www.ipaq.ki.se). It also determines the intensity of activity (i.e. vigorous or moderate) in each domainand the time spent on sedentary behaviours, suchas watching TV. Sedentary behaviours were definedas activities, such as sitting at a desk, travelling incar/bus/train, reading, working with computer, andwatching television.To measure energy expenditure, the concept of METs was used (19). MET is the ratio of a person’sworking metabolic rate and the resting metabolicrate (19). One MET is defined as the energy cost of sitting quietly and is equivalent to a caloric con-sumption of 1 kcal/kg/hour. It is estimated that aperson’s caloric consumption is four times highwhen moderately active and eight times highwhen vigorously active. Therefore, to calculate aperson’s overall energy expenditure, four METs areassigned to the time spent on moderate activities,and eight METs are assigned to the time spent onvigorous activities. The total physical activity (TPA)score was calculated as the sum of all METs × min-utes for moderate- or vigorous-intensity physicalactivity performed in work, commuting, and rec-reation.Based on the GPAQ analysis framework (19), ourparticipants were classified into three groups of high, moderate and low physical activity catego-ries. More details on these definitions were reportedelsewhere (20,21). Physical examination and biochemicalmeasurements Weight and height were measured in light clothingand without shoes. A portable calibrated electronicweighing scale (Omron Corp., Tokyo, Japan) andportable measuring inflexible bars (Seca, Hamburg,Germany) were used for this purpose. A constanttension tape (Seca, Hamburg, Germany) was usedfor measuring waist-circumference at the end of anormal expiration, with arms relaxed at the sides,at the midpoint between the lower margin of thelowest rib and the highest point of the hip on themid-axillary line. The BMI (kg/m 2 ) was calculatedaccording to the Quetelet formula. Five mL of ve-nous blood was taken in sitting position, centri-fuged, and transferred under cold-chain conditionto the laboratory. Quantitative CRP concentrationsin serum were measured in the endocrine labora-tory of the Vali-Asr Hospital (Tehran University of Medical Sciences) using the quantitative CRP kit(Parsazmoon, Karaj, Iran), with an intra-assay coef-ficient of variation of 2.6%. Diabetes was diagnosedfollowing the criteria of the American Diabetes As-sociation as described in our previous report (22).  Esteghamati A et al. C-reactive protein and physical activity   JHPN 68 Statistical analysis Complex analysis of the sample survey was per-formed using the SPSS software for Windows (ver-sion 17) (Chicago, IL, USA). Data were weighted forsex, age, and residential area (urban/rural) strata, ac-cording to the population of Iran (national census,2006). Kolmogorov Smirnov analysis was employedto study the normality of variables. CRP concentra-tions in serum were log-transformed to change thedistribution to normal; the log-transformed valuesof CRP were used in analyses. Continuous variableswere expressed as mean±standard error of mean(SEM). Partial correlation coefficients were calculat-ed between quantitative CRP and features of physi-cal activity after adjustment for various variables.The adjusted values of quantitative CRP were com-pared between the categories of physical activity,using the general linear modelling method. The pvalue of <0.05 was considered significant. RESULTS After excluding the participants with missing datain laboratory results (n=396), analyses were per-formed for the remaining 3,001 individuals. Thedemographic data (age, sex, and residential area) of the excluded subjects were not different from theremaining participants. Table 1 shows the baselinecharacteristics of the study participants. Forty-sixpercent of men were in the category of high physi-cal activity while 40% of women fell into the cate-gory of low physical activity. There was no signifi-cant difference in the serum CRP levels betweenmen and women.The serum CRP levels correlated with age (r=0.058,p=0.024 in men and r=0.065, p=0.44 in women), BMI (r=0.029, p=0.026 in men and r=0.030, p=0.023 in women), and waist-circumference (r=0.59,p=0.021 in men and r=0.047, p=0.046 in women).Current smokers had higher levels of quantitativeCRP vs ex-smokers or never-smokers (5.64±3.06vs 5.19±2.73, p=0.139 in men and 5.60±2.68 vs5.41±2.93, p=0.69 in women). TPA was inverselyassociated with age (r=-0.212, p=p.002 in menand r=-0.173, p=0.005 in women), BMI (r=-0.338,p<0.001 in men and r=-0.198, p=0.001 in wom-en), and waist-circumference (r=-0.357, p<0.001 inmen and r=-0.239, p<0.001 in women).CRP significantly correlated with TPA (r=-0.103,p=0.021 in men and r=-0.114, p=0.017 in wom-en), duration of vigorous-intensity activity (r=-0.122, p=0.019 in men and r=-0.109, p=0.026 inwomen), duration of moderate-intensity activity(r=-0.107, p=0.031 in men and r=-0.118, p=0.020in women), and duration of sedentary behaviours(r=0.092, p=0.029 in men and r=0.101, p=0.022 inwomen) after multiple adjustments for age, area of residence, BMI, waist-circumference, smoking, anddiabetes mellitus using partial correlation (Table 2).  Table 1. Characteristics of study participants (SuRFNCD-2007, Iran)CharacteristicsMale(n=1,494)Female(n=1,507)Total(n=3,001)Age (year) * 39.42±0.7539.76±0.7839.59±0.54Area of residenceUrban (%)1,011 (67.7)1,004 (66.6)2,015 (67.1)Rural (%)483 (32.3)503 (33.4)986 (32.9)BMI (kg/m 2 ) *   25.4±0.227.6±0.226.5±0.2Waist-circumference (cm) * 88.6±0.488.8±0.688.7±0.4Physical activity categoryLow (%)31.6±1.148.6±1.340.0±1.0Moderate (%)22.3±0.127.1±1.224.7±0.8High (%)46.1±1.324.3±1.235.4±1.1Total physical activity (MET-min/day)909.2±47.3327.9±13.8623.2±31.9Duration of vigorous activity (min/day)58.1±5.74.9±0.931.9±3.9Duration of moderate activity (min/day)111.1±4.472.2±2.391.9±3.2Duration of sedentary behaviours (min/day)240.2±4.2238.0±4.6239.2±3.8Current smoking (%±SE)26.1±1.61.8±0.314.1±1.1Diabetes mellitusQuantitative CRP (mg/L) * 6.6±0.45.6±0.19.1±0.45.6±0.17.8±0.45.6±0.1Variables, except age, sex, and area of residence, were standardized for age, sex, and residentialarea of the 2006 population of Iran. * Mean±SE; BMI=Body mass index; CRP=C-reactive protein;MET=Metabolic equivalent; min=Minute; SE=Standard error  Esteghamati A et al. Volume 30|Number 1|March 2012 69 C-reactive protein and physical activity  The correlation between quantitative CRP and TPAwas independent of the duration of sedentary be-haviours (r=-0.084, p=0.035 in men and r=-0.104,p=0.030 in women) (Table 2).Considering the different categories of physicalactivity, there was a significant inverse correlationbetween quantitative CRP and higher physical ac-tivity in both men and women after multiple ad-justments for age, residential area, BMI, waist-cir-cumference, smoking, and diabetes mellitus (Fig.).Serum CRP concentrations of ≥10 mg/L are fre-quently observed in subjects with inflammatoryconditions (23); therefore, in a separate analysis,we excluded these patients (n=70) and repeated theassociation analyses once more. This change couldnot considerably change the level of associations (r)in different models. DISCUSSION In this study, the duration and the intensity (vigo-rous and moderate) of physical activity in threedomains of work, transportation, and leisure timewere evaluated using the GPAQ. Our findings clear-ly demonstrated that physical activities of bothmoderate and vigorous intensity were associatedwith lower levels of quantitative CRP. Furthermore,we showed that this correlation was independentof several potential confounders, including BMI,waist-circumference, smoking status, diabetes mel-litus, age, and sex. Note that our study, in a largepopulation-based sample, could show a mild butsignificant and independent inverse association be-tween physical activity and CRP. The mild degreeof this association is expected because, in a generalpopulation, the level of CRP does not have a largevariation, and the majority of people have normal  Table 2. Association between several features of physical activity and serum quantitative CRP after mul-tiple adjustments (SuRFNCD-2007, Iran) Total physical activity (MET-min/day)MaleFemalerprpAdjustment forAge and area of residence-0.1270.011-0.1290.010Age, area of residence, BMI, WC, and smoking-0.1030.021-0.1140.017Age, area of residence, BMI, WC,smoking, diabetes mellitus, andduration of sedentary behaviours-0.0840.035-0.1040.030Duration of vigorous activity (min/day)Adjustment forAge and area of residence-0.1310.008-0.1170.021Age, area of residence, BMI, WC, and smoking-0.1220.019-0.1090.026Age, area of residence, BMI, WC,smoking, diabetes mellitus, durationof moderate activity, and sedentarybehaviours-0.1160.027-0.1060.029Duration of moderate activity (min/day)Adjustment forAge and area of residence-0.1230.018-0.1250.012Age, area of residence, BMI, WC, and smoking-0.1070.031-0.1180.020Age, area of residence, BMI, WC,smoking, diabetes mellitus, durationof vigorous activity, and sedentarybehaviours-0.0710.052-0.1020.032Duration of sedentary behaviours (min/day)Adjustment forAge and area of residence0.1080.0130.1190.008Age, area of residence, BMI, WC, and smoking0.0920.0290.1010.022Age, area of residence, BMI, WC,smoking, diabetes mellitus, and TPA0.0810.0410.0780.047BMI=Body mass index; CRP=C-reactive protein; MET=Metabolic equivalent; min=Minute; SE=Standarderror; TPA=Total physical activity; WC=Waist-circumference
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