International Journal of Obesity (2004) 28, 1097–1104 & 2004 Nature Publishing Group All rights reserved 0307-0565/04 $30.00 www.nature.com/ijo PAPER Elderly obese women display the greatest improvement in stair climbing performance after a 3-week body mass reduction program A Sartorio1,2*, CL Lafortuna3, F Agosti2, M Proietti2 and NA Maffiuletti2,4 1 Division of Metabolic Diseases III, Istituto Auxologico Italiano, IRCCS, Piancavallo (VB), Italy; 2Experimental Laboratory for Endocrinological Research, Istituto Auxologico Italiano, IRCCS, Milan, Italy; 3Institute of Molecular Bioimaging and Physiology, CNR, Segrate (MI), Italy; and 4INSERM/ERIT-M 0207 Laboratory, University of Burgundy, Dijon, France OBJECTIVE: To investigate whether stair climbing performance and body composition are similarly affected by a body mass reduction (BMR) program in obese individuals of different gender, age and body mass index (BMI) level. DESIGN: Longitudinal, clinical intervention study entailing energy-restricted diet (5023–7535 kJ/day), nutritional education, psychological counselling and moderate physical activity (indoor cycling, outdoor walking, gymnastics routines, five sessions/ week) during a 3-week period. SUBJECTS: A total of 466 male and 807 female subjects categorized as a function of gender, age (o vs Z50 y) and BMI (o vs Z40 kg/m2). MEASUREMENTS: Body mass, stair climbing time and power before and after the BMR program. Fat-free mass and fat mass were also evaluated by bioimpedance analysis, in a representative subgroup of 160 patients, to evaluate the relation between fat-free mass and power output. RESULTS: Body mass, fat-free mass and fat mass significantly decreased following the BMR program (Po0.001), with male subjects reducing body mass and fat-free mass more than and fat mass less than the female subjects. Stair climbing time decreased (Po0.001) and therefore anaerobic power significantly increased 9.7% after the treatment. The greatest improvement in stair climbing performance was observed in obese women aged Z50 y. Significant inverse correlations were found between initial power or fat-free mass level and respective percent increases (R ¼ 0.35/0.37, Po0.001) and between BMR-induced percent changes in body mass and power (R ¼ 0.13, Po0.001). CONCLUSION: Subjects with the lowest baseline level in stair climbing performance (and probably with the lowest amount of fatfree mass), that is, obese women aged more than 50 y, obtained the largest enhancement after the 3-week BMR program, likely improving overall functional capacities and resulting in greater independence during daily-living activities in such a population. International Journal of Obesity (2004) 28, 1097–1104. doi:10.1038/sj.ijo.0802702 Published online 22 June 2004 Keywords: muscle power; stair climbing; BMI; sarcopenia Introduction Several activities of daily living (eg, stair climbing, walking, chair rise, etc.) and brisk postural adjustments associated to body equilibrium maintenance involve dynamic movements, where power is generated by the lower limb muscles. *Correspondence: Dr A Sartorio, Laboratorio Sperimentale di Ricerche Endocrinologiche (LSRE), Istituto Auxologico Italiano, IRCCS, Via Ariosto, 13, 20145 Milano, Italy. E-mail: [email protected] Received 25 November 2003; revised 22 February 2004; accepted 14 March 2004; published online 22 June 2004 Aging and obesity are both accompanied by a significant decline in anaerobic muscular power,1–3 which in turn affects life quality and maintenance of independent living in these particular populations. Muscle power losses are more pronounced in the aged obese (particularly in female subjects) due to cumulative effects of sarcopenia (ie, the agerelated decline in muscle mass, strength and power4,5) and obesity. It was indeed suggested, based on anaerobic power estimation during stair climbing, that severely obese (body mass index (BMI) Z40 kg/m2) women over 50 y can be circumscribed as the most ‘disabled’ category as a consequence of obesity and aging.6 Stair climbing power in obese patients A Sartorio et al 1098 However, it is now well recognized that sarcopenia is partly reversible with a number of intervention strategies, including both endurance7 and strength training.8 Similarly, it has recently been shown that maximum strength and power of the lower limb muscles increased significantly in severely obese male and female subjects following a body mass reduction (BMR) program, entailing physical activity in combination with energy-restricted diet.9 Therefore, it appears that anaerobic muscular power can be easily modified in both aged and obese subjects of both sexes. However, it is still not clear whether power increases associated to a BMR program are comparable between obese subjects of different gender, age and BMI classes. According to the principle of initial values recently demonstrated in nonobese women (ie, women with lower initial power values benefited more from resistance and impact-training than those with higher values),10 it could be hypothesized that elderly obese women would obtain the greatest increases in anaerobic power of the lower limb muscles, as compared to their young and male counterparts. Therefore, the main aim of this paper was to compare the changes in stair climbing performance (stair climbing time and power) induced by a BMR program entailing diet caloric restriction and moderate physical activity between obese individuals of different gender, age and BMI level. A total of 1273 subjects were thus categorized according to previously established classification,6 based on gender, age (o vs Z50 y) and BMI level (o vs Z40 kg/m2). A secondary aim was to study, in a representative subgroup of 160 subjects, body composition changes between these categories of obese individuals and their potential influence on stair climbing performance. disease contraindicating or interfering with the execution of the stair climbing test, both before and after the completion of the BMR program. All the patients gave their informed consent to participate in the study, which was approved by the Ethics Committee of the Istituto Auxologico Italiano. All the procedures were conducted according to the principles expressed in the Declaration of Helsinki. Stair climbing test (N ¼ 1273) Stair climbing test (SCT), which allows measuring the maximal anaerobic power of the involved muscles, was performed before and immediately after the completion of the BMR program. At the moment of the first execution, 2–3 practice trials were allowed so that the subjects gained a good control of the performing technique. SCT consists in a modification of the test proposed by Margaria et al,11 recently applied in severely obese subjects.3,12 In brief, subjects were invited to climb up ordinary stairs at the highest possible speed, according to their capabilities. The stairs consisted of 13 steps of 15.3 cm each, thus covering a total vertical distance of 1.99 m. An experimenter measured the time employed to cover the test with a digital stopwatch. In line with Margaria et al11 assumptions, anaerobic power (in W) was calculated by using the following formula: ðbody mass9:81vertical distanceÞ=time where body mass, vertical distance (ie, 1.99 m) and time are expressed in kg, m and s, respectively, and 9.81 m/s2 represents the acceleration of gravity. SCT repeatability in obese individuals with BMI and age range similar to the present subjects has been previously assessed in our laboratory and the coefficient of variation between measurements has been found to be lower than 5%.13 Methods Subjects The study population for stair climbing test consisted of 1273 Italian subjects (466 males and 807 females) comprised within a wide range of age (18–80 y; mean7s.d.: 45.3715.4 y) and BMI (30–66.1 kg/m2; mean7s.d.: 41.275.8 kg/m2), which were categorized according to gender (male vs female subjects), age (younger: o50 y vs older: Z50 y) and BMI level (lower: BMI o40 kg/m2 vs higher: BMI Z40 kg/m2, ie, extreme or class III obesity). This classification has recently been adopted by Sartorio et al6 to study the influence of gender, age and obesity degree on muscular power. A subgroup of 160 patients (80 male and 80 female subjects) of comparable age (mean7s.d.: 47.1716.1 y) and BMI (mean7s.d.: 41.175.3 kg/m2) was considered for the additional assessment of body composition. All the subjects were followed at the 3rd Division of Metabolic Diseases (Istituto Auxologico Italiano, Piancavallo, Italy), where they had been admitted for a BMR program (see below). None of the individuals had signs or symptoms referable to overt cardiovascular, respiratory or orthopaedic International Journal of Obesity Body composition (N ¼ 160) Fat-free mass and fat mass were assessed by bioelectric impedance analysis, performed in the early morning after an overnight fast, according to a conventional standard technique.14 Whole-body resistance to an applied current (at 1, 5, 10, 50 and 100 kHz, 0.8 mA) was measured with a tetrapolar device (Human IM, Dietosystem, Milan, Italy). The electrodes were placed on the right wrist and ankle of the subjects while lying comfortably supine in a bed with the limbs abducted from the body. Fat-free mass was calculated with the fat-specific equations derived by Gray et al15 Fat mass was derived as the difference between total body mass and fatfree mass. BMR program The BMR program combined an energy-restricted diet, nutritional education, psychological counselling and moderate physical activity during a 3-week period. Stair climbing power in obese patients A Sartorio et al 1099 Caloric intake was restricted by means of a diet (5023– 7535 kJ/day, ie, 1200–1800 kcal/day) containing 21% proteins, 53% carbohydrates and 26% lipids. The amount of energy to be given with diet was calculated by subtracting approximately 2093 kJ (500 kcal)16 from the measurement of basal energy expenditure, as assessed by indirect calorimetry (Vmax 29; SensorMedics Corporation, Yorba Linda, CA, USA) for a total duration of 20 min, while the subjects rested in bed. The estimated H2O content of the food was 1000 ml/day and the estimated salt content was 1560 mg/day of Na þ , 3600 mg/day of K þ and 900 mg/day of Ca2 þ . A fluid intake of at least 2000 ml/day was encouraged. Dietary compliance was evaluated every day by a dietician. Nutritional education consisted of lectures, demonstrations and group discussions with and without a supervisor, which took place every day throughout the experimental period. Psychological counselling sessions were conducted by clinical psychologists 2–3 times/week and were based on individual or cognitivebehavioral strategies, for example, stimulus control procedures, problem solving training, stress management skills, development of healthy eating habits, assertiveness training, facilitation of social supports, cognitive restructuring of negative maladaptive thoughts and relapse prevention training. Physical activity consisted of five training sessions/week including indoor light jogging, dynamic exercises of the upper and lower limbs (standing and floor gymnastics routines focalized on muscle strength-power development by using body mass as movement resistance) at moderate intensity under the guide of a therapist (B1 h), and either 20–30 min aerobic exercise on an ergocycle at B60 W (Technogym, Gambettola, Italy), or 3–4 km outdoor walking on a predetermined track, according to individual capabilities and clinical status. Heart rate was monitored during typical training sessions in the majority of the experimental subjects by means of a telemetric system (Polar, Kempele, Finland) and, as a general observation, it was comprised between 110 and 160 beats/min, that is, between 55 and 75% of the individual maximal heart rate estimated as 220age (y). of SCT power or time or fat-free mass and respective percent changes. In each case, the level of significance was established at Pr0.05. Statistical analyses were performed using Statistica software (StatSoft, Tulsa, OK, USA). Results The present BMR program resulted in significant body mass (and BMI) reductions for the entire subject group (Po0.001, Table 1). A significant main effect was found for gender, age and BMI level (Table 2), and body mass percent decreases were significantly higher in male (4.8%) vs female subjects (3.9%), young (4.5%) vs old (4.2%) and in subjects with lower (4.4%) vs higher BMI (4.2%). Moreover, a significant gender BMI interaction (Po0.001) was observed, with males BMI o40 kg/m2 and female subjects BMI o40 kg/m2 obtaining the largest (5.1%) and the smallest (3.8%) body mass reduction, respectively. In the subgroup of 160 individuals, body mass reductions were almost identical to those obtained with the whole group (Table 3). Both fat-free mass and fat mass significantly decreased after the BMR program (Po0.001), with male subjects demonstrating significant larger reductions in fatfree mass (Figure 1a, Po0.001) but smaller changes in fat mass compared to female subjects (Figure 1b, Po0.01). SCT time significantly decreased following the BMR program (Po0.001) and, as a consequence, SCT power significantly increased (Po0.001, Table 1). A significant gender age BMI interaction was found for SCT time Table 1 Body mass, SCT time and power before and after the BMR program and respective absolute and percent changes in the whole study population (N ¼ 1273) Pre-BMR Absolute changes Percent changes Body mass (kg)a 110.6719.4 105.8718.4b 4.7272.23 4.2271.68 5.0072.60 4.3772.03b 0.6371.32 9.42716.36 SCT time (s)a SCT power (W)a 5037191 534.37191.0b 31.0790.1 9.73724.00 a Statistical procedures Wilcoxon test for nonparametric values were performed to compare means obtained before and after the BMR program for dependent variables (body mass, BMI, SCT time and power for N ¼ 1273 and body mass, fat-free and fat mass for N ¼ 160). The associated percent changes, calculated as: ((prepost)/pre) 100, were analyzed for significant differences using a three-way analysis of variance (gender age BMI level). The F-ratios were considered significant at Po0.05. A LSD post hoc test was conducted if significant main effects or interactions were present. Spearman rank order correlations were used to assess the significance of relations between BMR-induced percent changes in power and body mass and between initial values Post-BMR Mean values7s.d. bSignificantly different than prevalues (Po0.001). Table 2 ANOVA results associated to body mass, SCT time and power percent changes Gender effect Body mass a F ¼ 93.91 M4F b Age effect c BMI effect d Interaction F ¼ 8.31 Young 4old F ¼ 4.11 Low4high F ¼ 13.44b Gender BMI SCT timea F F F F ¼ 3.84d Gender age BMI SCT powera F ¼ 7.94c MoF F F F ¼ 5.97d Gender age a Mean values7s.d. bSignificant main effect or interaction (Po0.001). Significant main effect or interaction (Po0.01). dSignificant main effect or interaction (Po0.05). Note: N ¼ 1273. c International Journal of Obesity Stair climbing power in obese patients A Sartorio et al 1100 Table 3 Body mass, fat-free and fat mass before and after the BMR program and respective absolute and percent changes in the subgroup of 160 subjects Body mass (kg)a Fat-free mass (kg)a Fat mass (%)a Pre-BMR Post-BMR Absolute changes Percent changes 111.8719.9 60.8714.6 45.877.4 107.5719.0b 59.1713.7b 45.177.3b 4.3771.96 1.7272.17 0.6971.69 3.8871.46c 2.5573.47c 1.4273.82d,e a Mean values7s.d. bSignificantly lower than prevalues (Po0.001). cSignificant main gender effect (Po0.001). dSignificant main gender effect (Po0.01). eSignificant main age effect (Po0.01). Note: significant main effects are associated to three-way ANOVA on percent changes. elderly women compared to young men and women (Po0.01) and to elderly men (Po0.001, Figure 2b). Percent changes in SCT time and power obtained after the treatment were also plotted as a function of initial respective values for all the experimental subjects, to study whether the principle of initial values is also valid for obese populations.10 A significant inverse correlation was found for both SCT time (R ¼ 0.433, Po0.001) and power (Po0.001, Figure 3a), indicating that obese patients with high SCT time and low SCT power at baseline benefited more from the BMR program than faster and more powerful subjects. The same result was then obtained when considering initial fatfree mass values (Figure 3b), therefore suggesting that those subjects with higher fat-free mass (and consequently higher power) at baseline obtained the greatest fat-free mass losses (and thus the lowest power enhancement) after the treatment, according to the principle of initial values. These assumptions were then confirmed by the significant (inverse) correlation that was found between percent changes in body mass and SCT power (N ¼ 1273, R ¼ 0.127, Po0.001). Discussion Figure 1 Percent changes in fat-free mass (a) and fat mass (b) after the BMR program as a function of gender. Vertical bars represent s.e.m. and N ¼ 160. LSD post hoc tests showed the following differences: **: significantly different than males (Po0.01); ***: significantly different than males (Po0.001). changes (Table 2) and female subjects aged Z50 y with BMI Z40 kg/m2 obtained the largest improvements (Figure 2a). Muscle power increased more in female ( þ 11.2%) compared to male subjects ( þ 7.3%, Po0.01), and the same was true for International Journal of Obesity The present investigation demonstrated that a 4.2% body mass reduction, obtained after an integrated BMR program lasting 3 weeks was accompanied by enhanced stair climbing performance, that is, shorter time of execution and higher power output, in 1273 obese men and women aged 18–80 y. The main finding of this study is that greater BMR-induced power increases were observed in those subjects displaying lower initial values, that is, elderly obese women, even though body mass losses in female subjects were significantly smaller as compared to their male counterparts. Maximal muscle power, which depends on the product of muscular force and velocity of shortening, declines more precipitously than strength with advancing age.17,18 Reduced muscle power (ie, reduced muscle strength and/or movement velocity) is associated with a reduction in the ability to perform activities of daily living in older individuals, more particularly in obese subjects. Sartorio et al6,12 have indeed provided experimental evidence that aged obese of both genders produce lower stair climbing power as compared to their younger counterparts. However, although a number of studies have shown that muscle power can be Stair climbing power in obese patients A Sartorio et al 1101 Figure 2 Percent changes in SCT time (a) and power (b) after the BMR program as a function of gender, age (o vs Z50 y) and BMI level (o vs Z40 kg/m2). Vertical bars represent s.e.m. and N ¼ 1273. LSD post hoc tests showed the following differences: *: significantly lower than female subjects Z50 y BMI Z40 (Po0.05); **: significantly lower than female subjects Z50 y BMI Z40 (Po0.01); ww: significantly lower than female subjects Z50 y (Po0.01); www: significantly lower than female subjects Z50 y (Po0.001). improved in nonobese older individuals using standardized physical training protocols (eg, resistance training19–22), it is unclear whether this is also possible in the case of the aged obese. The present study clearly demonstrated that elderly obese of both genders and with different degrees of obesity positively benefited from the BMR program, since stair climbing time and power were both enhanced after the 3week treatment, especially in female subjects. This is noteworthy, since power and strength increases in elderly seem to be directly in relation with improvements of some functional capacities, such as stepping up and rising from the kneeling position on the floor19 and also gait velocity.23 Unfortunately, walking speed changes were not measured in this study, but, since power was quantified during a typical activity of daily living, we conclude that overall functional capacity of elderly obese is enhanced by a 3-week BMR program, entailing diet caloric restriction and physical activity. Stair climbing power increases obtained here are consistent with those previously reported for nonobese older men and women after physical training (for a review, see Pu and Nelson24), but a systematic comparison of the plasticity of muscle power to training between old obese and nonobese is necessary. The extremely obese (ie, BMI higher than 40 kg/m2) women over 50 y tested in the present study have been previously identified as the most ‘disabled’ category on International Journal of Obesity Stair climbing power in obese patients A Sartorio et al 1102 Figure 3 Correlations between initial levels of SCT power and respective BMR-induced percent changes in the whole study population (a, N ¼ 1273) and between baseline fat-free mass and percent changes in the subgroup of 160 subjects (b). R- and P-values associated to Spearman rank order correlations are shown. account of the low power output during stair climbing.6 However, BMR-induced stair climbing time reductions were higher in this group and power increased more in elderly female subjects with respect to the other subjects, therefore indicating that the adaptive capacity of stair climbing performance was superior in individuals with low initial values (see also below). Previous research demonstrated similar improvements in whole muscle characteristics among elderly men and women25,26 and among young and old nonobese subjects27,28 following resistance training protocols. However, little is known on the differential adaptability of elderly male vs female or young vs old obese subject and for the first time, the present study demonstrated that older obese women increased power more than their male and young counterparts. These findings are unique and require further investigation, in order to understand the basic mechanisms modulating muscle power adaptability with gender, aging and physical activity. International Journal of Obesity In our study, male subjects generally displayed larger body mass reductions than female subjects at the completion of the BMR program, in line with earlier studies performed with smaller populations.12,29 An intriguing finding comes from the inverse correlation between BMR-induced changes in body mass and SCT power, that is to say, large body mass losses in obese males were associated with small increases of stair climbing power and vice versa for female subjects. Even though fat mass and fat-free mass were measured only in a representative subgroup of 160 subjects, it is concluded that the present BMR program resulted in different body composition changes between genders, where women mainly reduced the proportion of fat mass and only to a lesser extent fat-free mass, while the opposite outcome was observed in males. Assuming that neural adaptations (ie, changes within the nervous system30) explaining the majority of the present BMR-induced power improvements were comparable between male and female subjects,8 sizeable reductions in fat-free mass in the former subjects inevitably minimized the magnitude of power increases. It is important to note that, in obese children, such an alteration during a 3-week BMR program similar to that adopted here has been recognized as a major factor for later regain in body mass.31 However, the same authors later demonstrated that fat-free reductions could be minimized by standardized resistance training program combined with caloric restriction,32 also in line with the recent review of Donnelly et al33 (see also below). The principle of initial values states that subjects with lower initial values of a physiological variable will exhibit the greatest improvement in response to specific exercise training. Winters-Stone and Snow10 have recently shown that initial levels of bone mass density, stability, strength and power were significantly correlated with training-induced percent changes in 31 premenopausal nonobese women, thus initial values predicted the response of the musculoskeletal system to training. In the current investigation, a significant inverse relation was found between baseline SCT time or power and the associated BMR-induced changes, that is, obese subjects with lower initial levels (elderly obese females) benefited more from the treatment than those with higher values. Therefore, the present findings confirm that the principle of initial values is also applicable in a large population of obese subjects of different gender, age and BMI level. The data in Figure 3a enable the estimation of the expected increase in SCT power that an obese individual would obtain as a result of a BMR program entailing diet caloric restriction and moderate physical activity, by including baseline SCT power in the following equation: Percent D SCT power ¼ ð0:05baseline SCT powerÞ þ 34:44 Based on these theoretical calculations, subjects with baseline SCT power equal to or higher than 700 W would obtain no changes or even reductions of the muscle power following the present BMR program. This suggests that for Stair climbing power in obese patients A Sartorio et al 1103 obese subjects with high baseline power levels (mainly men aged o50 y), 3 weeks of physical activity performed at moderate intensity with five sessions per week may have been too light and not sufficient enough to increase stair climbing power. Therefore, it is recommended that the physical training considered in the present study must be implemented, at least for the most fit obese individuals, with specific exercises for the development of power and/or strength of the lower limb muscles, in order to maintain fat-free mass during BMR. In conclusion, we have completed a 3-week BMR program in a large population of obese individuals, and studied the effects of gender, age and BMI level on the muscular power estimated during a simple functional test. Body mass reductions of B4% were accompanied by a substantial enhancement (B9%) of the stair climbing performance (stair climbing time and power) and these changes were related together (ie, low power increases were associated to high body mass reductions, eg, in male subjects). In the same way, a significant inverse correlation was found between initial values at the stair climbing test or fat-free mass and respective percent changes. These findings indicate that subjects with the lowest baseline muscle power (and probably with the lowest amount of muscle mass), namely obese women aged Z50 y, obtained the largest power enhancement after the treatment, therefore confirming that the principle of initial values is also valid for obese individuals. These positive effects could allow elderly obese female subjects to perform common daily activities better (previously precluded) and possibly to maintain better compliance to regular exercise activity at home. Further studies are requested to ascertain whether the short-term effects observed here are similarly maintained in obese subjects of different gender, age and BMI during long-term follow-up. Acknowledgements This study is partially supported by Progetto di Ricerca Corrente, Istituto Auxologico Italiano, IRCCS, Milan, Italy. The technical assistance of Mr S Ottolini was greatly appreciated. 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