Obesity Surgery

, Volume 18, Issue 9, pp 1112–1118

Muscle Force and Force Control After Weight Loss in Obese and Morbidly Obese Men

Authors

  • Olivier Hue
    • Département des sciences de l’activité physiqueUniversité du Québec à Trois-Rivières
  • Félix Berrigan
    • Faculté de médecine, Division de kinésiologie, PEPS, Département de médecine sociale et préventiveUniversité Laval
  • Martin Simoneau
    • Faculté de médecine, Division de kinésiologie, PEPS, Département de médecine sociale et préventiveUniversité Laval
    • Centre de recherche du CHA—Axe perte d’autonomie et sciences neurologiques du QuébecCentre d’excellence sur le vieillissement—Hôpital Saint-Sacrement
  • Julie Marcotte
    • Faculté de médecine, Division de kinésiologie, PEPS, Département de médecine sociale et préventiveUniversité Laval
  • Picard Marceau
    • Faculté de médecine, Département de chirurgieUniversité Laval
    • Département de chirurgie généraleHôpital Laval
  • Simon Marceau
    • Faculté de médecine, Département de chirurgieUniversité Laval
    • Département de chirurgie généraleHôpital Laval
  • Angelo Tremblay
    • Faculté de médecine, Division de kinésiologie, PEPS, Département de médecine sociale et préventiveUniversité Laval
    • Faculté de médecine, Division de kinésiologie, PEPS, Département de médecine sociale et préventiveUniversité Laval
    • Centre de recherche du CHA—Axe perte d’autonomie et sciences neurologiques du QuébecCentre d’excellence sur le vieillissement—Hôpital Saint-Sacrement
Research Article

DOI: 10.1007/s11695-008-9597-5

Cite this article as:
Hue, O., Berrigan, F., Simoneau, M. et al. OBES SURG (2008) 18: 1112. doi:10.1007/s11695-008-9597-5

Abstract

Background

Decrease in fat mass and fat-free mass have been observed with weight loss induced by a dietary intervention or surgery. There are concerns that fat-free mass decrease could have some negative functional consequences. The aim of this study was to examine how weight loss affects strength and force control in obese and morbidly obese men.

Methods

Weight loss was obtained in obese individuals by a hypocaloric diet program until resistance to lose fat and in morbidly obese individuals by bariatric surgery. Maximal force was measured for upper and lower limb and the ability to maintain 15% and 40% of that force. These measures were taken at baseline, in those dieting once resistant to weight loss and 1 year after surgery for those operated on. Normal weight individuals used for control were evaluated twice (6 to 12 months apart).

Results

At baseline, there was no significant difference between groups for maximal forces and capabilities to maintain force levels. Weight loss averaged 11.1% of the initial body weight after dieting and 46.3% 1 year after surgery. At the same time, there was for the lower limb a loss of 10.1% in maximal force after dieting and 33.5% after surgery. For the upper limb, there was no change in maximal force after dieting whereas a decrease of 14.4% was observed after surgery. When transformed in force related to body weight, there was no change in relative force for the lower limb after dieting whereas an increased relative force after surgery. There was no significant difference for the ability for maintaining force levels.

Conclusion

Despite a large force loss, particularly for the lower limbs in morbidly obese individuals after surgery, this loss is relatively well tolerated because the relation between force and body weight is even improved and the ability to maintain that force is preserved.

Keywords

ObesityWeight lossMuscular strengthForce controlDiet restrictionBariatric surgery

Introduction

Excess of weight is considered as a critical and common health problem because overweight and obesity are associated with many physiological and psychological disorders related to high mortality and morbidity [1, 2]. Obesity is mainly characterized by an increase in fat mass (FM) and, to a lesser extent, in fat-free mass (FFM). It also changes body geometry, increases the mass of the different body segments [3, 4], and imposes limits about the biomechanics of daily living activities that may predispose obese persons to injury [5].

Many weight loss interventions are proposed to reduce obesity. Interventions based on diet, exercise, or both have been suggested for overweight and obese persons. Benefits of these programs vary according to the duration of the intervention, the diet type, and the associated physical activity modalities [68]. Surgical treatments are often adopted for morbid obesity or obesity (BMI > 35 kg/m2) in the presence of significant comorbidities. After undergoing bariatric surgery, a large weight loss (on average, 50% of the initial body weight) is achieved in morbidly obese persons [9, 10].

Several studies suggest that fat mass and fat-free mass decrease after weight loss [11, 12]. For instance, Trombetta et al. [13] showed a significant decrease in fat-free mass after weight loss by dieting. With exercise training, there was no decrease of fat-free mass. The maximal voluntary handgrip strength of their subjects, however, was not reduced (whether exercise was included or not). Kraemer et al. [12] showed similar effects for the lower limbs. After a gastroplasty and despite a decrease of 15% of muscle fiber’s surface accompanying a weight loss of 10%, Wadström et al. [11] reported no difference in eccentric and concentric strength of knee extensors and flexors. However, in these studies, weight loss was less than more recent bariatric operations with loss averaging around 50%. Decrease of FFM has been reported after biliopancreatic diversion [1416] and gastric bypass [16, 17]. For example, Benedetti et al. [14] reported an overall 35% decrease of FFM 30 months after surgery, and there are concerns that FFM decrease could have negative functional consequences [13, 18]. To our knowledge, there is no force data available to examine how this massive weight loss (and presumably FFM loss) affects force production capabilities and force control.

The aim of this study was to determine if maximal strength capacities and isometric force control in obese and morbidly obese persons are affected by a weight loss. Although there is a debate on the exact nature of the physiological mechanisms underlying the relationship that can exist between maximal strength and force variability referring to possible inaccuracy and lack of precision in force control. Force variability appears to be mediated by muscle strength with muscle weakness sometimes inducing greater variability [19]. Hence, an increased variability (that is, a less accurate and precise force control) could be noted in morbidly obese individuals if muscle strength declines.

Materials and Methods

Subjects and Weight Loss Protocols

We studied three groups of Caucasian male adults: control (n = 16; BMI < 25 kg/m2), obese (n = 17; 30 < BMI <  39.9 kg/m2) and morbidly obese (n = 10; BMI > 40 kg/m2). All individuals were tested at baseline. For those treated by hypocaloric diet, tests were repeated once they have become resistant to weight loss for four consecutive weeks (resistance). This occurred after 15 to 47 weeks. For those submitted to surgery, tests were repeated 12 months after surgery (postsurgery). Control participants were evaluated at baseline and after a period varying from 6 to 12 months after their first visit (postsurgery). Table 1 presents the physical characteristics of the participants. The research project was approved by the Laval University and the Laval Hospital Research Centre Medical Ethics Committees, and all participants gave written informed consent.
Table 1

Group characteristics for each phase of protocol

Characteristics

Control group

Obese group

Morbidly obese group

Baseline (n = 16)

Post (n = 16)

Baseline (n = 17)

Resistance (n = 17)

Baseline (n = 10)

Postsurgery (n = 10)

Age (years)

38.6 ± 9.4

 

36.9 ± 7.7

 

43.8 ± 9.0

 

Height (cm)

177 ± 5.6

 

176 ± 6.7

 

174 ± 6.2

 

Weight (kg)**

71.1 ± 7.9

71.5 ± 8.1

106.1 ± 19.6

94.3 ± 20.4*

152.8 ± 24.6

82.0 ± 14.9*

BMI (kg/m2)**

22.7 ± 2.2

22.8 ± 2.3

34.0 ± 4.7

30.2 ± 4.8*

50.2 ± 6.9

27.0 ± 5.4*

Waist cicumference (cm)a**

83.0 ± 6.1

82.4 ± 6

113.6 ± 13.9

102.1 ± 16.5*

152.4 ± 13.9

99.5 ± 17.7*

Hip cicumference (cm)**

95.2 ± 5.0

95.1 ± 5.3

113.8 ± 10.4

106.2 ± 10.2*

143.3 ± 14.6

105.1 ± 11.6*

Lower limb force measures

Maximal force (N)

693.8 ± 201.9

684 ± 176.4

795.8 ± 175.4

715.4 ± 199.9*

742.8 ± 131.3

493.9 ± 84.3*

CV (%) 15% of maximal force

4.1 ± 1.8

4.2 ± 2.4

6.1 ± 4.0

6.0 ± 3.6

4.3 ± 2.3

5.8 ± 3.7

45% of maximal force

6.1 ± 3.0

6.3 ± 3.4

7.8 ± 3.7

8.3 ± 3.7

7.0 ± 5.7

6.2 ± 4.2

Upper limb force measures

Maximal force (N)

63.7 ± 10.8

63.1 ± 11.8

71 ± 10.8

70.9 ± 11.8

71.4 ± 18.6

61.2 ± 19.6*

CV (%) 15% of maximal force

7.5 ± 5.5

9.4 ± 8.7

10.4 ± 6.0

10.9 ± 6.9

7.7 ± 5.7

10.3 ± 11.7

45% of maximal force

11.9 ± 4.5

12.1 ± 5.1

14.4 ± 5.6

14.7 ± 5.6

12.3 ± 5.7

12.3 ± 5.9

Values are means ± SD

CV = Coefficient of Variation

ameasured at mid distance between 12th rib and iliac crest

*P < 0.01 = significantly different after intervention

**P < 0.01 = significantly different between group at baseline

Dietary Intervention

An energy restriction which corresponded to a reduction in energy intake was determined for all obese subjects. The weight loss program was a hypocaloric nonmacronutrient specific diet of about 700 kcal/day. To achieve this energy restriction, the baseline resting metabolic rate, measured by indirect calorimetry, was used by extrapolating this value over a 24-h period and then multiplying it by an activity factor of 1.4 which corresponds to a sedentary state. A 3-day dietary record was used to assess macronutrient and micronutrient composition of the diet of the subjects at the onset of the program [20]. To achieve this energy restriction and to maintain macronutrient composition, a nutritionist followed each subject during the diet program. During the study, obese subjects had to come to our laboratory every other week for a control session during which they were asked to fill-out a 24-h dietary recall with a nutritionist. This served to assess compliance to the energy restriction.

Surgery Procedure

The morbidly obese patients underwent a duodenal switch procedure. It consists of 65% sleeve gastrectomy, duodenoileostomy at 250 cm from the ileocecal valve, and ileoileostomy 100 cm from the ileocecal valve, creating an alimentary channel of 250 cm including a common channel of 100 cm [21, 22]. The procedure let food going only into the distal intestine, decreases the surface of food absorption, and decreases the role of bile. This is a malabsorptive procedure.

Muscular Strength and Coefficient of Variation Procedures

Maximal forces and coefficient of force variation (CV) of lower and upper limbs were assessed with the subjects seated comfortably in an experimental chair. Figure 1 illustrates the general setup for the lower limb measurements. The subjects had to perform isometric right quadriceps contraction with the hip angle fixed at 100° and knee angle set at 90° of flexion. A padded cuff (15-cm wide) was secured above the ankle malleolus and attached to the load cell fixed to the chair. The subjects hold a rigid armchair and were asked to maintain their back and their buttock in contact with the chair. The subjects were told verbally to produce their maximal force and strongly encouraged to maintain this force level for about 3 s. For all subjects, lower limb strength measures were collected first followed by upper limb measures. For each condition, two trials were performed with a 1-min rest between trials. For the upper limb measures, the subjects were seated in the same chair and had to apply force pressure to a load cell positioned between the pulp of the thumb and the index of the dominant hand. Flexed in the palm, the other fingers were kept away from the index to prevent them from providing any support.
https://static-content.springer.com/image/art%3A10.1007%2Fs11695-008-9597-5/MediaObjects/11695_2008_9597_Fig1_HTML.gif
Fig. 1

Experimental setup for the lower limb measurements. Force output feedback was provided to the subject on an oscilloscope. Force applied on the load cells corresponds to an upward displacement of the force signal

For the CV measures, the subjects were asked to maintain a constant isometric force output at target force levels of 15% and 40% of their maximum. Visual feedback of the force was given through an oscilloscope (Hewlett-Packard 54651A) facing the subject (see Fig. 1). A target calibration for each subject and limbs was positioned on the center of the screen (dashed horizontal line on a uniform background without any grid). An upward deviation of the force signal (solid line) signalled the force pressure exceeded the target whereas a downward deviation signalled an undershoot of the target. Subjects were familiarized with the visual feedback provided on the oscilloscope and allowed to play with the visual signal until they felt comfortable. Each trial lasted 30 s. The first 5 s only served to match the target force level presented. Then, visual feedback of the force was masked and subjects were instructed to maintain their force level constant. The coefficient of variation (CV), representing the relative variation to the mean force, was measured from the remaining 25 s (standard deviation of the force signal over the 25 s times 100/mean force). The subjects performed seven trials at each force level (15% and 40% of maximal force) and for the upper and lower limbs.

After the CV measures, maximal forces for the upper and lower limbs were retaken (similar procedures, two trials per limb). This procedure served to examine the presence, if any, of fatigue.

Two load cells were used for measuring forces (InterTechnology model 9363-DI-500 for the lower limb and Omega model LC703-25 for the upper limb). Force signals were amplified and conditioned (Ectron model 563H, Intertechnology, Toronto, Canada) before digitizing at 500 Hz (12-bit A/D conversion). All data were imported into the Matlab environment for the analyses. Force signals were filtered (Butterworth low-pass filter, fourth order with 10-Hz cutt-off frequency). All maximal curves were visually inspected and maximal forces identified. The mean of the first and last two trials were taken. T tests for dependent samples were conducted for each group and each session to examine the presence of fatigue between the first and last trials. All tests were not significant (Ps > 0.05) and the mean for the first two trials for each session were used for subsequent analyses. For the CV data, all curves also were first inspected before calculating a coefficient of variation for the last 25 s of each trial. For each subject, the mean of each condition for each session was used for the statistical analyses.

Statistical Analysis

Statistica software 7.0 (Statsoft, Tulsa, OK, USA) was used for all analyses. For all variables (body anthropometric and force parameters), data were submitted to Group (Obese, Morbidly obese, Control) × Phase (Baseline/Postintervention) analysis of variance with repeated measures on the last factor. All results presented were considered significant at P < 0.05.

Results

Anthropometric Characteristics

Table 1 presents age, body weight, body mass index (BMI), waist circumference and hip circumference for the three groups for both sessions. At baseline, body weight, BMI, waist circumference, and hip circumference were different between all groups and significantly higher in morbidly obese. After weight loss, body weight, BMI, waist circumference and hip circumference decreased for obese and morbidly obese subjects. At resistance to further lose weight, obese subjects had lost, on average, 11.8 kg of body weight, 3.8 kg/m2 of BMI, 11.5 cm of waist circumference, and 7.6 cm of hip circumference. One year post-surgery, the mean decrease in anthropometric variables in morbidly obese subjects was 70.8 kg for body weight, 23.2 kg/m2 for BMI, 52.9 cm for waist circumference, and 38.2 cm for hip circumference.

Maximal Force and Coefficient of Variation After Weight Loss Interventions

The main objective of this study was to determine if maximal strength capacities and isometric force control would be affected by weight loss. Table 1 presents maximal forces and CV values before and after the weight loss interventions. For the lower limb, the ANOVA showed main effects of Group (F(2,40) = 2.35; P < 0.05) and Phase (F(1,40) = 43.42; P < 0.001) as well as a significant interaction of Group by Phase (F(2,40) = 14.37; P < 0.001). A decomposition of the interaction into its simple main effects showed that, while the control group had a stable maximum force level (P > 0.05), both the obese (P < 0.001) and the morbidly obese groups’ maximal force decreased (P < 0.001). The decrease for the morbidly obese group was greater than that noted for the obese (P < 0.001). Figure 2 shows the magnitude of the decrease for each group in percentage of the maximal force noted at baseline. While control subjects presented a stable maximal force, obese and morbidly obese individuals showed a decrease of 10.1% and 33.5%, respectively.
https://static-content.springer.com/image/art%3A10.1007%2Fs11695-008-9597-5/MediaObjects/11695_2008_9597_Fig2_HTML.gif
Fig. 2

Group changes in maximal lower limb force before and after weight loss interventions expressed in percentage of the mean (±SD). Asterisk, significantly different after weight loss (P < 0.001)

Maximal force data for the upper limb (pinch force) nearly mirrored those observed for the lower limb. The ANOVA revealed a main effect of Phase (F(1,40) = 5.76; P < 0.05) as well as a significant interaction of Group by Phase (F(2,40) = 5.45; P < 0.01). A decomposition of the interaction into its simple main effects showed the control and the obese groups generated a similar maximal force level over the two phases (Ps > 0.05) while it decreased by 14.4% for the morbidly obese group (P < 0.001). Figure 3 shows the magnitude of the decrease for each group in percentage of the maximal force level observed at baseline. We also computed a relative maximal force by dividing the maximal force by the weight at the time of testing [24]. Relative maximal force for the upper limb increased for morbidly obese and obese individuals (57.8% and 20.6%, respectively). For the lower limbs, no change was observed for the control and obese individuals whereas it increased by 27.8% for the morbidly obese individuals.
https://static-content.springer.com/image/art%3A10.1007%2Fs11695-008-9597-5/MediaObjects/11695_2008_9597_Fig3_HTML.gif
Fig. 3

Group changes in maximal upper limb force before and after weight loss interventions expressed in percentage of the mean (±SD). Asterisk, significantly different after weight loss (P < 0.001)

Table 1 presents a summary of the CV values. All effects for all ANOVAs were nonsignificant (Ps > 0.05). On average, for the lower limb, the CV were 7% and 5% for the 40% and 15% targets, respectively. For the upper limb, the CV were 9% and 12% for the two target values. Overall, these results suggest that, although weight loss yielded a decrease in maximal force (for the morbidly obese, 33.5% and 14.4% for the upper and lower limbs, respectively), force control was not affected.

Discussion

In the present study, we report several findings related to the effects of weight loss interventions in obese and morbidly obese persons on maximal force and isometric force control of lower and upper limbs. First, when massive weight loss is induced, as noted in morbidly obese individuals, there is a decrease of the absolute maximal force. For the morbidly obese individuals, this was observed both for lower limbs and upper limbs (decrease of 33.5% and 14.4%, respectively). For obese individuals, a weight loss of 11.8 kg was observed at resistance to further lose weight and yielded a decrease maximal force for the lower limbs only (10.1%). These observations contrast with previous studies that have presented no or minor loss of maximal force following a weight loss intervention. For several of these experiments, the weight loss was significantly smaller than that noted for our morbidly obese patients (for example, 10% in Trombetta et al. [13] and 9% in Kraemer et al. [12]). In addition, a physical activity program was included in previously reported weight loss interventions [23, 24]. In some studies, the physical activity program (often resistance training) did not only preserve muscle strength but even increased it [12, 23, 24].

In a recent review of changes in FFM during weight loss including 26 cohorts treated with dietary interventions and 29 cohorts of bariatric surgery, Chaston et al. [17] concluded that the rate of weight loss influences the proportion of FFM after nonsurgical interventions. For surgical interventions, FFM loss varied from 12.4% up to 52.7% of the weight loss with bariatric surgeries leading to greater FFM loss than laparoscopic gastric banding. Hence, the massive weight loss noted in our study presumably yielded a large loss of FFM which could explain the large decline in maximal force. However, it is interesting to note that our obese subjects also showed a decrease in maximal force of the lower limb. This suggests that, in absence of physical activity intervention, the decline in maximal force could be directly related to the magnitude of body weight loss. This agrees with Chaston et al. [17] who proposed the decrease of maximal force is related to the rate of body weight loss.

It is noteworthy to underline that not all force features were affected negatively by the weight loss. Firstly, when the force loss was considered in relative terms, morbidly obese showed an increased in relative force (57.8% for the upper limb and 27.8% for the lower limb). Secondly, the CV data point to an interesting observation in that the large decline in absolute muscle strength was not associated with any increase in force variability (as indexed by the force CV). Loss of force control has been associated with muscle weakness [19]. In the present study and after the weight loss intervention, the morbidly obese subjects produced smaller maximal force for the lower limb than control and obese subjects (on average, 493.9 N for the morbidly obese vs 684.0 N and 715.4 N for the control and obese, respectively). This absolute force loss presumably was not the result of a change in muscle fiber type since Gray et al. [25] showed that for morbidly obese women, there was no change in the proportion of Type I and II muscle fiber types after massive weight loss following gastric bypass surgery (weight loss of 47% of initial weight). Kern et al. [26] reported similar results for smaller weight loss (on average, 20.8% of initial body weight).

Despite the large decrease in maximal force, we reported in other studies that weight loss in morbidly obese and obese individuals improved balance and movement control [27, 28]. In a first study [27], we showed that, before weight loss, morbidly obese subjects were less stable than obese and lean subjects. It is well acknowledged that less stable individuals are at higher risk of falling. After a weight loss of 12.1% after dieting and 46.3% after surgery, balance control improved for both groups. More importantly, this improvement was directly related to the size of the weight loss. Hence, obese individuals, despite significant loss of absolute maximal force improved their balance control. Results from another study showed that a weight loss program (7.9% of the initial body weight) improved the ability to point rapidly and accurately to a target when standing upright [28]. A more stable postural platform resulting from weight loss allowed a better control of the upper-limb movements.

Overall, decrease in maximal force did not have any negative impact on force control. This should not be taken as an argument against the favorable effect of introducing physical activity program with weight loss intervention. As mentioned above, there are several indications that physical activity improves muscle strength and muscle mass and plays a key role in managing obesity [23]. Without significant FFM decrease, physical activity improves the physical performances of obese subjects, which suggests that their muscle strength can sometimes be maintained and even improved [23, 24].

Our results were obtained in middle-aged individuals and these conclusions may not be applicable to an older population. With aging, loss of body weight leads to a reduction of motor unit number and athrophy of muscle fibers, particularly the type IIa fibers [2931]. Therefore, for older subjects, the age-related changes following weight loss may need to be compensated by a more active lifestyle. In older individuals, resistance exercises enhance muscle mass [32, 33] and strength [34]. Hence, for this population, the positive impact of introducing physical activity for reducing force loss may be an essential prerequisite of the weight loss intervention [35, 36]. This point should be considered by health professionals.

In summary, despite a large decline in force, particularly for the lower limb, morbidly obese individuals maintain their ability to control various force levels and improve their maximal force when it was computed as a function of their weight.

Acknowledgements

All subjects are gratefully acknowledged. Special thanks to Paule Marceau and the surgeon team at the Department of Surgery of Laval Hospital, especially Drs. Fredéric-Simon Hould, Stéfane Lebel, Simon Biron and Odette Lescelleur. Finally, thanks to Marcel Kaszap for programming expertise and François Bégin for his help in data collection. This study was supported by a Collaborative Health Research Project (CHRP) of NSERC and NSERC Discovery grants of Canada.

Copyright information

© Springer Science + Business Media, LLC 2008