Hypertension, hyperinsulinaemia and obesity in middle-aged Finns with impaired glucose tolerance

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1 Journl of Humn Hypertension (1998) 12, Stockton Press. All rights reserved /98 $12.00 ORIGINAL ARTICLE Hypertension, hyperinsulinemi nd obesity in middle-ged Finns with impired glucose tolernce Q Qio, U Rjl nd S Keinänen-Kiuknniemi Deprtment of Public Helth Science nd Generl Prctice, University of Oulu, Oulu University Hospitl, Oulu, Finlnd The im of the study ws to nlyse the dt obtined from 2-yer follow-up study of middle-ged Finnish subjects (n = 183) with previous history of impired glucose tolernce (IGT) in order to elucidte the longitudinl reltionships between hypertension, fsting hyperinsulinemi nd obesity. Hypertension ws defined s either systolic blood pressure (BP) of 160 mm Hg or distolic BP of 95 mm Hg or being on ntihypertensive mediction regrdless of the BP vlue. Multiple logistic regression nlysis djusted for glucose tolernce sttus, serum lipids, exercise behviour nd lcohol consumption shows tht the odds rtios of one unit (mu/l) increse in the bseline fsting insulin concentrtion were 1.13 (95% confidence intervl ) for the 2-yer incidence of hypertension in subjects with IGT t bseline. Bseline body mss index (BMI) lso predicted the 2-yer incidence of hypertension, with n odds rtio of 1.20 (95% CI ). BMI correlted positively with fsting insulin level (r = 0.54, P 0.001). It is concluded tht n elevted fsting insulin concentrtion s well s n incresed BMI preceded the onset of hypertension in subjects with IGT. It my suggest cusl reltionship between hypertension nd hyperinsulinemi. Keywords: hypertension; fsting hyperinsulinemi; obesity; impired glucose tolernce Introduction Hypertension, obesity, nd glucose intolernce (impired glucose tolernce nd non-insulin-dependent dibetes) re so commonly ssocited 1 6 s to suggest common pthogenic mechnisms. There is strong belief tht hyperinsulinemi is directly linked to hypertension, 1,2 nd insulin resistnce hs been observed mong len hypertensive ptients. 6 8 However, some studies hve filed to confirm these observtions. 9,10 Most of these studies were crosssectionl in nture, nd cuse nd effect were thus difficult to demonstrte. Longitudinl nd prospective studies on this issue re scrce. One prospective study reveled tht fter djustment for overweight nd body ft distribution, fsting insulin ws n independent risk fctor for hypertension only in subjects with norml body weight nd normoglycemi, 11 wheres nother study showed tht chnges in blood pressure (BP) preceded bnorml glucose tolernce, but not hyperinsulinemi. 4 A study mde on non-obese young dult blck men with the euglycemic hyperinsulinemic clmp technique suggested tht insulin resistnce might precede the onset of estblished essentil hypertension. 12 Correspondence: Qing Qio, Deprtment of Public Helth Science nd Generl Prctice, University of Oulu, Apistie 1, SF-90220, Oulu, Finlnd Received 20 July 1997; revised nd ccepted 23 Jnury 1998 The im of this study ws to nlyse the dt obtined from 2-yer follow-up study of middleged Finnish subjects with impired glucose tolernce (IGT) nd try to elucidte the longitudinl reltionships between hypertension, fsting hyperinsulinemi nd obesity. Subjects nd methods A screening survey for dibetes nd the resons for erly retirement mong the subjects born in 1935 nd living in Oulu, city of inhbitnts in northern Finlnd on 1 October 1990, ws conducted from 15 October 1990 to 5 My In this survey, 207 subjects were defined s hving IGT ccording to 2-h 75 g orl glucose tolernce tests (OGTTs) recommended by the WHO in 1985, 13 ie, 2-h postlod cpillry whole blood glucose vlue of 7.8 to 11.1 mmol/l. A follow-up study of the subjects with bseline IGT ws crried out between 14 Februry nd 9 June 1994, n verge of 2.1 yers (rnge 1.9 to 2.4) fter the initil 2-h OGTTs. Of the 207 IGT subjects, 183 (84 men nd 99 women) corresponding to 88.4% of the originl group prticipted in the retest, two persons hd died, one ws in hospitl due to ctrct, two hd moved nd 19 did not ttend. There were no significnt differences in sex, in nti-hypertensive mediction nd in the men vlues of 2-h OGTT between the prticipnts nd the non-prticipnts. However, higher men fsting insulin level (13.7

2 266 vs 11.1 mu/l) nd higher men body mss index (BMI) (28.8 vs 27.1) were observed in the non-prticipnts. The detils of the initil survey nd the follow-up study hve been reported previously A postl questionnire concerning the previous history of dibetes, hypertension, nti-hypertensive mediction nd other questions ws sent to ech of the prticipnts, nd the nswers to the questions nd the nti-hypertensive gents used previously were checked during the interviews. Systolic (1st phse of Korotkoff sounds) nd distolic (5th phse) blood pressures were recorded using stndrd mercury sphygmomnometers fter the subjects hd rested for more thn 30 min in the sitting position. A single BP reding ws tken for the subjects with norml BP. A repeted BP mesurement ws mde whenever the first reding ws bove the defined norml limit, nd the second reding ws recorded. For every subject, two BP mesurements were mde seprtely on the dy of interview nd when the subject ws coming in for blood glucose test. The men vlue of the two mesurements ws used in this nlysis. Drug tretment for hypertension ws verified t both the initil survey nd t follow-up. If subject reported tking nti-hypertensive mediction t the initil survey, but not t follow-up, the reson ws investigted by checking the ptient s previous records in the helth centre, nd dignosis of hypertension ws mde on the bsis of the history of the disese. Hypertension ws defined s either systolic BP of 160 mm Hg, or distolic BP of 95 mm Hg, or being on nti-hypertensive mediction regrdless of the BP vlues. 17 The BMI ws clculted by dividing the weight (kg) by the height (m) squred. Chnges in the weight between the initil nd follow-up surveys were clculted by subtrcting the weight t bseline from the weight t follow-up. A positive chnge mens n increse in the weight t follow-up nd negtive chnge mens decrese. The sme principle ws used in clculting the chnges in fsting insulin levels between the two exmintions. A person ws defined s smoker if he/she smoked currently or hd quitted smoking during the follow-up period, but hd smoked for t lest 10 yers before. Exercise behviour ws determined by sking the subjects bout the frequency, intensity nd durtion of exercise tken in their leisure time. A sum vrible with three scles for exercise behviour ws then formed. Physicl inctivity mens tht exercise ws tken once week or less. Moderte ctivity mens tht exercise ws tken twice week or more for hlf n hour or longer t time, but without swet or brethlessness. Vigorous ctivity indictes tht the person did more thn moderte exercise with hevy swet nd brethlessness every time. Alcohol consumption ws ctegorised into three groups ccording to the mount of lcohol consumed within 2-week period, ie, no drink, drinks 56 cl nd 56 cl. Lbortory tests The procedures of lbortory mesurements hve been described in detil elsewhere. 15 In brief, stndrd 75-g OGTT ws mde ccording to the 1985 WHO 13 recommendtion. After fst of h, venous blood smple ws drwn between m to obtin fsting vlue nd vlues for serum insulin, totl cholesterol, serum high-density lipoprotein (HDL) cholesterol nd triglycerides. After tht, 75-g glucose lod (Glucodyn/Leirs) ws given to the prticipnts. At 2 h, single cpillry blood smple ws collected for the 2-h vlue. The concentrtion of blood glucose ws determined with the hexokinse-glucose-6-phosphte dehydrogense method (Merck Dignostic, Drmstdt, Germny). The coefficients of vrition (CV) for within-run studies were between 1.7 nd 2.8% depending on the glucose concentrtion. For dy-tody studies, the CV ws 2.8% t the upper end of the reference rnge. The times when the blood smples were tken were registered, nd the 2-h postlod smple ws not ccepted if it hd been drwn more thn 5 min too erly or too lte. The serum smples for insulin nd lipids were deep-frozen ( 74 C) until mesurement. The serum insulin concentrtion ws mesured by rdioimmunossy using Phdeseph Insulin RIA100 (Phrmci Dignostics AB, Uppsl, Sweden), which lso detects proinsulin nd proinsulin conversion products with considerble sensitivity. The cross-rectivity of proinsulin in this ssy is bout 41%. Sttisticl nlysis The sttisticl nlyses were crried out using the SPSS for Windows progrm version Student s t-tests nd descriptive cross-tbultions were employed to compre the men vlues of selected chrcteristics nd to nlyse the ssocition of the outcome (hypertension vs normotension) with ech ctegoricl vrible. In cse of skewed vribles the geometric mens of insulin concentrtion were presented, bsed on logrithmic trnsformtions. Multiple logistic regression nlyses were performed to investigte the ssocition of hypertension t follow-up (outcome) with bseline fsting insulin level nd bseline BMI in forwrd stepwise mnner seprtely for subjects with normotension t bseline nd for ll of the subjects. Glucose tolernce sttus, sex, BMI, weight chnge during the follow-up, smoking, exercise behviour nd lcohol consumption were djusted in ech regression model. Results Sixteen (18%) of the 91 subjects who were normotensive t bseline hd developed hypertension by follow-up. The highest incidence of hypertension ws seen mong dibetic subjects t follow-up. One dibetic (50%), four (22%) IGT nd 11 (16%) norml glucose tolernce subjects developed hypertension during the follow-up. The bseline chrcteristics of the subjects ccording to the incidence of hypertension t follow-up re presented in Tble 1. Subjects who developed hypertension t follow-up hd

3 Tble 1 Chrcteristics of the subjects t the initil survey ccording to the incidence of hypertension t follow-up 267 Normotension Hypertension P vlue (n = 75) (n = 16) Sex (%) men women Body mss index (kg/m 2 ) b 26.0 (3.0) 28.1 (4.4) 0.02 Increse in weight (kg) b 2.8 (3.5) 3.0 (3.0) 0.82 Fsting insulin (mu/l) c 8.9 (1.6) 11.0 (1.6) 0.04 Increse in fsting insulin c 1.0 (1.3) 1.0 (1.3) 0.86 Fsting blood glucose (mmol/l) 5.2 (0.8) 5.3 (0.8) h postlod blood glucose (mmol/l) 8.8 (0.8) 9.0 (0.9) 0.49 Totl cholesterol (mmol/l) 5.6 (1.4) 6.2 (1.3) 0.13 HDL-cholesterol (mmol/l) 1.4 (0.4) 1.3 (0.4) 0.26 Triglycerides (mmol/l) 1.1 (0.8) 1.4 (0.8) 0.09 Alcohol drink (cl) per 2 weeks (%) No Smoker (%) No Yes Physicl exercise (%) Low Moderte Vigorous Dt expressed s men (s.d.) except noted. By chi-squre test or by Student s t-test. b Two missing vlues from BMI. c Geometric mens. higher fsting insulin level nd higher BMI t bseline. Tble 2 shows the djusted odds rtios of the ssocition between hypertension nd hyperinsulinemi for subjects normotensive t bseline nd for ll of the IGT subjects. Elevted fsting insulin concentrtion t bseline ws n independent predictor for the incidence of hypertension t follow-up. Elevted bseline BMI ws lso risk for hypertension (Tble 3). The bseline fsting insulin concentrtion ws higher in subjects who developed hypertension compred to subjects who were normotensive, nd the highest fsting insulin level ws seen in obese hypertensive subjects (Tble 4). Tble 2 Adjusted odds rtios for the ssocition between hypertension t follow-up (outcome) nd fsting insulin concentrtion (mu/l) t bseline. The odds rtios corresponding to one unit increse in the fsting insulin level Odds rtios 95% confidence intervl (1) Subjects normotensive t bseline (n = 91) (2) Normotensive t bseline nd norml glucose tolernce t follow-up (n = 71) (3) All subjects normotensive or hypertensive t bseline (n = 183) Sex, 2-h blood glucose, totl cholesterol, HDL-cholesterol, triglycerides, lcohol consumption, nd smoking nd exercise behviour t bseline djusted ech model. Tble 3 Adjusted odds rtios for the ssocition of hypertension t follow-up (outcome) with body mss index (BMI, kg/m 2 )t bseline. The odds rtios corresponding to one unit increse in BMI Odds rtios 95% confidence intervl (1) Subjects normotensive t bseline (n = 89) (2) All subjects normotensive or hypertensive t bseline (n = 173) Sex, 2-h blood glucose, totl cholesterol, HDL-cholesterol, triglycerides, lcohol consumption, nd smoking nd exercise behviour t bseline djusted ech model. There re missing vlues from BMI. Tble 4 Geometric men (s.d.) of bseline fsting insulin concentrtion strtified by body mss index (BMI, kg/m 2 ) nd hypertension No. Hypertension Normotension P vlue Normotensive 89 t bseline BMI (1.4) 10.5 (1.4) 0.04 BMI (1.3) 7.9 (1.4) 0.57 All subjects BMI (1.5) 10.6 (1.4) BMI (1.4) 7.9 (1.4) 0.03 There re missing vlues from BMI.

4 268 Discussion In spite of the high respondent rte for this study, the smll smple size nd the short period of followup my obscure the observtion of interest. And, becuse the subjects who did not ttend the followup survey were more obese nd hd higher bseline fsting insulin levels thn the prticipnts, the risk of hypertension nd the observed ssocition between hyperinsulinemi nd hypertension would hve been stronger if ll subjects hd ttended the study. In ddition, becuse wist nd hip circumferences were not mesured t bseline, the ssocition of centrl obesity with hypertension could not be evluted nd djusted for. However, the ssessment of hypertension sttus is quite relible. Firstly, BP ws mesured two times on different dys nd the men of the two mesurements ws used in the dt nlysis. Secondly, we rechecked the disese history from cse records for ll those with inconsistent nswers on nti-hypertensive medictions nd excluded the ptients who took drugs with BP-lowering effect for diseses other thn hypertension. Subjects with IGT provide good opportunity to study the ssocition between hypertension nd hyperinsulinemi, since hyperinsulinemi nd insulin resistnce re bsic chrcteristics of ptients with IGT, nd the incidence of IGT is higher in hypertensive ptients. 21 In this study, the incidence of hypertension ws higher in the subjects with dibetes nd IGT compred to the subjects with norml glucose tolernce t follow-up. This suggested the coexistence of hypertension nd glucose intolernce, which hs been observed in mny other studies. 1 6 An independent ssocition of hyperinsulinemi with hypertension hs lso been reported in mny other studies. 5,22 26 However, most of the studies hve been cross-sectionl, nd thus the presence of hyperinsulinemi could be consequence of hypertension or hyperlipidemi rther thn cuse of these disorders. Longitudinl studies to verify the etiologic role of hyperinsulinemi in the development of hypertension re still scrce. Christlieb et l 5 found cusl reltionship between the level of circulting insulin nd distolic BP t the first-yer follow-up of subjects with impired glucose tolernce. Hffner et l 11 observed n independent ssocition in subjects with norml body weight nd normoglycemi. A cusl reltionship between the elevted fsting insulin concentrtion nd the development of hypertension ws found in this study. But, the presence of this ssocition in the generl popultion remins to be demonstrted since the popultion studied here hd previous history of IGT. Insulin resistnce hs been thought to rise the BP by incresing renl sodium retention or stimulting the sympthetic nervous system, or both. 27 But the biologicl plusibility of insulin s hypertensive gent seems slender. 28 An independent ssocition of obesity nd weight gin with hypertension hs been observed in mny cross-sectionl nd prospective studies, nd severl studies hve shown tht body ft distribution is more powerful determinnt of BP thn overll mesures of obesity, 32,33 In this study, the incresed BMI preceded the development of hypertension, nd correlted positively with the fsting insulin concentrtion (r = 0.54, P 0.001). This my suggest tht hyperinsulinemi is link between hypertension nd obesity nd tht the ssocition of hypertension with obesity is medited by hyperinsulinemi. 1,5 It is concluded tht n elevted fsting insulin concentrtion s well s n incresed BMI preceded the onset of hypertension in subjects with IGT t bseline. It my suggest cusl reltionship between hypertension nd hyperinsulinemi. References 1 Modn M et l. Hyperinsulinemi link between hypertension obesity nd glucose intolernce. J Clin Invest 1985; 75: Donhue RP, Skyler JS, Schneidermn N, Prines RJ. Hyperinsulinemi nd elevted blood pressure: cuse, confounder, or coincidence? Am J Epidemiol 1990; 132: Mbny J-CN et l. Hypertension nd hyperinsulinemi: reltion in dibetes but not essentil hypertension. Lncet 1988; 2 April: Feskens EJM et l. Hypertension nd overweight ssocited with hyperinsulinemi nd glucose tolernce: longitudinl study of the Finnish nd Dutch cohorts of the Seven Countries Study. Dibetologi 1995; 38: Christlieb AR, Krolewski AS, Wrrm JH, Soeldner JS. Is insulin the link between hypertension nd obesity? Hypertension 1985; 7 (Suppl II): II-54 II Ferrnnini E et l. Insulin resistnce in essentil hypertension. N Engl J Med 1987; 317: Lkso M, Srlund M, Mykkänen L. Essentil hypertension nd insulin resistnce in non-insulin-dependent dibetes. Eur J Clin Invest 1989; 19: Zvroni I et l. Risk fctors for coronry rtery disese in helth persons with hyperinsulinemi nd norml glucose tolernce. N Engl J Med 1989; 320: Muller DC et l. An epidemiologicl test of the hyperinsulinemi hypertension hypothesis. J Clin Endocrinol Metb 1993; 76: Collins VR, Dowse GK, Finch CF, Zimmet PZ. An inconsistent reltionship between insulin nd blood pressure in three pcific islnd popultions. J Clin Epidemiol 1990; 43: Hffner SM et l. Prospective nlysis of the insulinresistnce syndrome (Syndrome X). Dibetes 1992; 41: Flkner B, Hulmn S, Tnnenbum J, Kushner H. Insulin resistnce nd blood pressure in young blck men. Hypertension 1990; 16: WHO Study Group. Dibetes Mellitus. World Helth Orgniztion, Genev (Tech Rep Ser No. 727), Rjl U, Keinänen-Kiuknniemi S, Uusimäki A, Kivelä S-L. Prevlence of dibetes mellitus nd impired glucose tolernce in middle-ged Finnish popultion. Scnd J Prim Helth Cre 1995; 13: Qio Q et l. Risk for dibetes nd persistent glucose tolernce mong middle-ged Finns. Dibet Res Clin Prct 1996; 33: Qio Q et l. Rndom cpillry whole blood glucose test s screening test for dibetes mellitus in middle-ged popultion. Scnd J Clin Lb Invest 1995; 55: 3 8.

5 17 WHO: Arteril hypertension. Technicl Report Series no Genev, Reven GM, Hollenbeck CB, Chen Y-DI. Reltionship between glucose tolernce, insulin secretion, nd insulin ction in non-obese individuls with vrying degrees of glucose tolernce. Dibetologi 1989; 32: Lillioj S et l. Impired glucose tolernce s disorder of insulin ction: longitudinl nd crosssectionl studies in Pim Indins. N Engl J Med 1988; 318: Sd MF et l. Sequentil chnges in serum insulin concentrtion during development of non-insulindependent dibetes. Lncet 1989; I: Morles PA et l. Incidence of NIDDM nd impired glucose tolernce in hypertensive subjects. Dibetes 1993; 42: Welborn TA et l. Serum-insulin in essentil hypertension nd in peripherl vsculr disese. Lncet 1966; 1: Berglund G et l. Body composition nd glucose metbolism in hypertensive middle-ged mles. Act Med Scnd 1976; 200: Donhue RP et l. Sex differences in the coronry hert disese risk profile: possible role for insulin. The Bever County Study. Am J Epidemiol 1987; 125: Fournier AM et l. Blood pressure, insulin, nd glycemi in nondibetic subjects. Am J Med 1986; 80: Wing RR, Bunker CH, Kuller LH, Mtthews KA. Insulin body mss index, nd crdiovsculr risk fctors in premenopusl women. Arteriosclerosis 1989; 9: Reven GM, Hoffmn BB. A role for insulin in the etiology nd course of hypertension? Lncet 1987; 1: Jrrett RJ. In defence of insulin: critique of syndrome X. Lncet 1992; 340: Sims EAH. Mechnisms of hypertension in the overweight. Hypertension 1982; 4 (Suppl 3): III Hvlik RJ, Hubert HB, Fbsitz RR. Weight nd hypertension. Ann Intern Med 1983; 98 (Prt 3): Ashley RW, Knnel WB. Reltion of weight chnges to chnges in therogenic trits: The Frminghm Study. J Chronic Dis 1974, 27: Blir D et l. Evidence for n incresed risk for hypertension with centrlly locted body ft nd the effect of rce nd sex on this risk. Am J Epidemiol 1984; 119: Selby JV, Friedmn GD, Quesenberry CP Jr. Precursors of essentil hypertension: the role of body ft distribution pttern. Am J Epidemiol 1989; 129:

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