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ARTICLE Comparison of bilateral and unilateral contractions between swimmers and nonathletes during leg press and hand grip exercises Monica MacDonald, Danielle Losier, Victoria L. Chester, and Usha Kuruganti
Abstract: The bilateral limb deficit (BLD) is defined as the reduction in force production during bilateral compared with summed unilateral contractions of homologous muscles. The underlying mechanism for the BLD has been elusive to determine. The purpose of this study was to examine the presence of the BLD during maximal isometric leg press and handgrip exercises in female swimmers (n = 9, mean age = 20.1 ± 1.3 years) and nonathletes (n = 9, mean age = 21.7 ± 1.3 years) to gain further insight into this phenomenon. Force and electromyography (EMG) measures were collected from participants under bilateral and unilateral conditions for handgrip and leg press exercises. Bilateral limb ratios (BLR) were calculated for swimmers (BLRS) and nonathletes (BLRNA). A deficit was found for swimmers and nonathletes in leg force (BLRS = 79.84% ± 13.09% and BLRNA = 81.44% ± 19.23%) and leg EMG (BLRS = 88.45% ± 15.41% and BLRNA = 94.66% ± 13.62%); however, no BLD was seen in hand force (BLRS = 98.30% ± 11.21% and BLRNA = 95.91% ± 11.04%) and hand EMG (BLRS = 102.42% ± 11.20% and BLRNA = 103.30% ± 16.50%). Furthermore, no significant differences were found between groups for leg force, leg EMG, hand force, and hand EMG. In conclusion, a BLD was detected for both groups during bilateral isometric leg press. This suggests that while the BLD may be affected by neural influences, there may other factors involved such as postural stability requirements to perform the exercise. Key words: athletes, skeletal muscle function, exercise performance, human performance, muscle physiology. Résumé : Le déficit segmentaire bilatéral (« BLD ») se définit par la diminution de la force produite bilatéralement en comparaison a` la somme des forces produites unilatéralement par les mêmes muscles. Les mécanismes a` la base du BLD ne sont pas connus. Cette étude se propose d’examiner la présence du BLD au cours d’efforts maximaux dans un développé des jambes et d’exercices de préhension manuelle en condition isométrique chez des nageuses (n = 9, âge moyen= 20,1 ± 1,3 ans) et des non-athlètes (n = 9, âge moyen = 21,7 ± 1,3 ans), et ce, afin de comprendre davantage ce phénomène. On évalue la force et l’activité myoélectrique (« EMG ») des participants au cours d’exercices de préhension et de développé des jambes en condition bilatérale et unilatérale. On calcule les ratios segmentaires bilatéraux (« BLR ») des nageuses (« BLRS ») et des non-athlètes (« BLRNA »). On observe un déficit chez les nageuses et les non-athlètes aux plans de la force des jambes (BLRS = 79,84 ± 13,09 % et BLRNA = 81,44 ± 19,23 %) et de l’EMG des jambes (BLRS = 88,45 ± 15,41 % et BLRNA = 94,66 ± 13,62 %); cependant, on n’observe pas de BLD dans la force des mains (BLRS = 98,30 ± 11,21 % et BLRNA = 95,91 ± 11,04 %) et l’EMG de la préhension (BLRS = 102,42 ± 11,20 % et BLRNA = 103,30 ± 16,50 %). En outre, on n’observe pas de différence significative entre les groupes en ce qui concerne la force des jambes, l’EMG des jambes, la force des mains et l’EMG de la préhension. En conclusion, on note dans les deux groupes la présence d’un BLD au cours d’un développé bilatéral isométrique des jambes. Ces résultats suggèrent que des influences nerveuses probables agissent sur le BLD en même temps que d’autres facteurs impliqués dans la stabilisation de la posture pour la réalisation des exercices. [Traduit par la Rédaction] Mots-clés : athlètes, fonction du muscle squelettique, performance kinésique, performance humaine, physiologie humaine.
Introduction Bilateral limb deficit (BLD) is the reduction in force that accompanies maximal 2-limb efforts relative to single-limb performances (Howard and Enoka 1991). BLD is found in both large and small muscle groups (Howard and Enoka 1991; Oda and Moritani 1995; Schantz et al. 1989; Secher et al. 1988) and athletic and nonathletic populations (Secher et al. 1988; Schantz et al. 1989; Kuruganti and Murphy 2008). The underlying mechanism of the deficit has been elusive to determine. There have been suggestions that the decline in force during bilateral contractions could be due to some form of neural inhibition (Archontides and Fazey 1993; Howard and Enoka 1991); however, there have been mixed results in the literature (Jakobi and Chilibeck 2001).
Electromyography (EMG) has been used in past studies to examine the source of the deficit. The signal resulting from EMG, the myoelectric signal (MES), measures the neural commands sent to the muscle and provides evidence of the neural mechanisms causing the deficit. However, studies to date have been mixed regarding the relationship between the force and EMG deficits, with some studies suggesting that amplitude of the MES is lower under bilateral conditions versus unilateral conditions (Kuruganti and Murphy 2008; Cresswell and Ovendal 2002; Kawakami et al. 1998; Koh et al. 1993; Oda and Moritani 1995; Ohtsuki 1981b, 1983; Rube and Secher 1990; Steger and Denoth 1996; Van Soest et al. 1985; Vandervoort et al. 1984), while others show no deficit in the EMG data (Howard and Enoka 1991; Owings and Grabiner 1998; Schantz et al. 1989). Because studies have shown varying results, it has
Received 7 February 2014. Accepted 11 June 2014. M. MacDonald, D. Losier, V.L. Chester, and U. Kuruganti. Andrew and Marjorie McCain Human Performance Laboratory, Faculty of Kinesiology, University of New Brunswick, Fredericton, NB E3B 5A3, Canada. Corresponding author: Usha Kuruganti (e-mail: [email protected]). Appl. Physiol. Nutr. Metab. 39: 1–5 (2014) dx.doi.org/10.1139/apnm-2014-0040
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been difficult to identify the mechanism of the deficit; however, 2 primary theories that have been proposed are the neural inhibition theory and the postural stability theory. Several researchers have cited neural inhibition as the cause of the BLD (Magnus and Farthing 2008; Ohtsuki 1983; Post et al. 2007; Van Dieen et al. 2003). Ohtsuki (1983) proposed that the deficit could be related to inhibitory spinal reflexes, which occurs when the neural control for 1 limb is affected when the opposite limb is simultaneously activated. Others attributed the BLD to reduced motor neuron excitability during bilateral contraction (Kawakami et al. 1998). Most evidence points towards interhemispheric inhibition as a potential cause of the deficit, where the activity in 1 hemisphere can affect the activity in the opposite hemisphere when they are concurrently activated, thereby decreasing neural drive to the muscles (Oda and Moritani 1995; Taniguchi et al. 2001; Van Dieen et al. 2003). Another possible explanation for the BLD is the postural stability requirements of the exercise (Herbert and Gandevia 1996; Magnus and Farthing 2008). While the BLD has been shown to be present in both upper and lower body movements, its presence has been more evident during dynamic contractions (Kuruganti and Seaman 2006). Multi-jointed lower body exercises involving large muscles and high force generation may require more postural stability than upper body exercises and therefore sustain a greater deficit (Lan 2002). Exercises involving multiple muscle groups and higher ground reaction forces, such as the leg press, might exhibit larger bilateral deficits because it is more difficult to maintain postural stability under the bilateral condition (Magnus and Farthing 2008). Studying these types of movements could provide a better understanding of the cause of the BLD and the impact of stability on the BLD. Interestingly, it has been shown that the BLD can be improved with targeted training. Several bilateral training programs have been shown to decrease the BLD (Janzen et al. 2006; Kuruganti et al. 2005; Taniguchi 1998). Janzen et al. (2006) implemented a 26-week bilateral training program. Initially, they found a BLD for both leg press and lateral pull-down exercises. They found that bilateral training decreased the deficit. Kuruganti et al. (2005) found similar results after a 6-week knee extension training program. Taniguchi (1998) also implemented a 6-week training program and found that BLD decreased with bilateral training and increased with unilateral training in both arm and leg extensions. Other studies have shown that sport-specific training can eliminate the bilateral limb deficit and even result in bilateral facilitation (Howard and Enoka 1991; Secher 1975). Secher (1975) found that oarsmen had bilateral leg strength comparable with their summed unilateral leg strength and that more experienced rowers showed no deficit. While studies of specific athletes have been conducted to study the BLD, no studies to date have examined swimmers and compared them with nonathletes. Swimmers are a group of interest because they are bilaterally trained and could provide evidence towards the training theory. A better understanding of the BLD and its underlying mechanisms can be used to improve training programs in populations where maximal bilateral force output is required. The present study examined BLD in swimmers and nonathletes for both leg press and handgrip exercises. Along with force output, EMG data was collected to provide insight into the underlying mechanism of the deficit. It was hypothesized that swimmers would exhibit a smaller BLD or even bilateral facilitation compared with nonathletes for both exercises because of their bilateral training background. Because of the postural stability requirements of the leg press, it was expected that this exercise would show a larger BLD than the handgrip exercise across both groups (Magnus and Farthing 2008).
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Materials and methods Eighteen female participants volunteered for this study, comprising 9 women from the university varsity swimming team (mean age, 20.1 ± 1.3 years; mean height, 1.70 ± 0.04 m; mean body mass, 68.3 ± 5.4 kg) and 9 women who were untrained controls (mean age, 21.7 ± 1.3 years; mean height, 1.70 ± 0.07 m; mean weight, 69.7 ± 4.5 kg). The participants were considered to be untrained if they exercised less than 3 times per week. Trained participants were involved in a swimming program at least 7 times per week. Of the 9 swimmers, 6 regularly practiced strokes involving bilateral movements (fly, breast), while the remaining swimmers regularly practiced free style and backstroke. Participants were required to complete the Canadian Society for Exercise Physiology’s Physical Activity Readiness Questionnaire as well as an informed consent form before participating in the study. This study was approved by the University of New Brunswick Research Ethics Board. Instrumentation A Cybex Humac Norm (CSMI Inc., USA) isokinetic dynamometer fitted with a closed kinetic chain adaptor was used to collect isometric leg press data both unilaterally and bilaterally. Handgrip strength was collected using custom-made force transducers. Surface EMG was used to examine muscle activity during all contractions. A 16-channel wireless EMG system (Aurion Inc., Italy) was used to collect muscle activity data. This system has an input impedance of 20 MOhm, a common mode rejection ratio of 90 dB, and a signal to noise ratio >50 dB. The gain of each channel was 1000. The system has an analog resistor-capacitor DC filter for both high pass (to remove the DC component) and low pass filtering (as an anti-alias). The bandwidth of the signal was 10–500 Hz and the slopes of the cut-offs were 6 dB/octave. Force and EMG data were sampled at a frequency of 1500 Hz for 5 s using personalcomputer– based software and a 16-bit A/D board (Tektronix, TM 5006, Lake Mary, Fla., USA), interfaced to a personal computer. Further processing was performed off-line using a custom-built Labview 6.1 program (National Instruments, Tex., USA). EMG data collection During all strength tests, bipolar surface electrodes (Duotrode silver–silver chloride electrodes (Myo-tronics Inc.); interlelectrode spacing = 21.0 ± 1.0 mm) were placed over the muscles of interest. Prior to application of the electrodes, the participant’s skin was abraded and cleaned with alcohol. Electrodes were placed bilaterally (right and left) over the belly of the muscles of interest according to standardized procedures (Criswell 2010). For the leg press exercise, electrodes were placed over the rectus femoris at half the distance between the knee (superior part of the patella) and the iliac spine. Electrodes were placed over the right and left vastus medialis at an oblique angle (55°), 2 cm medially from the superior rim of the patella. Electrodes were then placed over the biceps femoris parallel to the muscle fibers on the lateral aspect of the thigh at two-thirds of the distance between the trochanter and the back of the knee crease (midpoint between the lateral and medial femoral condyles). For the handgrip exercise, similar to Magnus and Farthing (2008), electrodes were placed bilaterally over the flexor carpi ulnaris (FCU) on the medial aspect of the forearm, 2% of the distance from the elbow (midpoint between the lateral and medial epicondyles) to the wrist (midpoint between the ulnar and radial styloids). To examine other possible contributions from surrounding muscles, electrodes were also placed bilaterally on the flexor digitorum superficialis in the midline of the forearm three-fourths of the distance from the elbow to the. Electrodes were then placed on the flexor carpi radialis (FCR) on the ventral aspect of the forearm near the elbow on the medial side of the arm. Published by NRC Research Press
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Table 1. Mean values for leg force and handgrip force for both swimmers and nonathletes.
Swimmers Nonathletes Total
Bilateral leg force (Nm)
Unilateral left leg force (Nm)
Unilateral right leg force (Nm)
Bilateral hand force (N)
Unilateral left hand force (N)
Unilateral right hand force (N)
402.52±155.62 463.99±137.29 433.25±145.83
254.29±83.86 286.83±90.12 270.56±86.09
245.85±69.24 288.03±70.31 266.94±71.09
348.76±77.32 336.96±44.09 342.86±61.36
194.27±38.55 198.73±25.44 196.50±31.76
159.38±21.49 154.28±21.10 156.83±20.36
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Note: Values are means ± SD. No statistical significant difference was detected in leg force or hand force between the 2 groups (swimmers and nonathletes).
Table 2. Mean values for bilateral limb ratio (BLR) leg force, BLR leg electromyography (EMG), BLR hand force, and BLR hand EMG for both swimmers and nonathletes.
Swimmers Nonathletes Total
BLR leg force (%)
BLR leg EMG (%)
BLR hand force (%)
BLR hand EMG (%)
79.84±13.09 81.44±19.23 80.64±15.98*
88.45±15.41 94.66±13.62 91.55±14.47*
98.30±11.21 95.91±11.04 97.10±10.86
102.42±11.20 103.30±16.50 102.86±13.69
Note: Values are means ± SD. The BLR was calculated as BLR (%) = (peak bilateral force)/(sum of peak unilateral forces) × 100 (Ohtsuki 1983). No significant differences were found between swimmers and nonathletes. *Significant difference from 100% (p < 0.05) and therefore a deficit.
Isometric strength testing For the leg press exercise, participants were seated upright at a self-selected seat back angle and horizontal translation to assure comfort. The dynamometer was adjusted so that the participant’s knees were at a 90° angle. Generally, hip angle was maintained at 90°; however, to ensure that the participant’s back was resting comfortably against the dynamometer chair this resulted in the hip angle varying for each participant (85–100°). Participants were instructed to cross their arms during the trials to ensure that there was no force being generated by the upper body. Participants were asked to perform 3 maximal voluntary contractions (MVCs) unilaterally for the right and left leg, as well as 3 MVCs bilaterally. Participants held the contraction for 5 s to allow them to reach their maximal force. Two-minute rest periods were given in between trials to ensure participants were able to adequately recover. The order of the testing conditions (i.e., unilateral, bilateral) was randomized. For the handgrip exercise, participants were in a standing position with their hands by their sides. Participants were asked to perform 3 MVCs with each their right and left hand, and 3 MVCs bilaterally. Again, 2-min rest periods were given between all trials to avoid fatigue. During all contractions, participants were provided with verbal encouragement to “push as hard” as they could. Finally, the order of the exercises (leg press and handgrip) was randomized and all tests were completed in 1 session. Data analysis For each activity (leg press and handgrip), the trial with the highest peak force was chosen for further analysis. The amplitude of the EMG signal was estimated using the root mean square (RMS) calculation. A 0.5-s window of EMG data, centred at the peak force was used for all calculations similar to previous studies (Kuruganti and Murphy 2008, Kuruganti et al. 2011). The bilateral limb ratio (BLRForce) was calculated as in previous studies (Howard and Enoka 1991; Jakobi and Chilibeck 2001; Ohtsuki 1983). The BLR was calculated for both leg press and handgrip using the peak force data from unilateral left (ULL), unilateral right (ULR), and bilateral (BL) contractions as: BLRForce (%) = [(peak force BL)/(peak force ULL + peak force ULR)] × 100 (Ohtsuki 1983). A BLR was also calculated from the EMG data (BLREMG) similar to previous studies (Kuruganti and Murphy 2008). The RMS values of each agonist muscle were summed for each limb and the corresponding antagonist activity was then subtracted to better reflect the net activity. These values were then used in all of the BLREMG calculations. A series of 1-way ANOVAs were used to test for mean differences in the dependent variables between swimmers and nonathletes. The ␣ level was set to 0.05. Student’s t tests were run to determine
if the BLR values were significantly different than 100%, thereby identifying the presence of a BLD.
Results Mean force data for the leg press and handgrip are shown in Table 1. BLD data (BLRLegForce, BLRLegEMG, BLRHandForce, and BLRHandEMG) for each group and both groups combined are listed in Table 2. One-way ANOVAs showed no significant differences in mean values between groups in any of the dependant variables (p > 0.05). Results of the t tests showed that the BLRLegForce and the BLRLegEMG were significantly different from 100 (p < 0.001 and p = 0.024, respectively), indicating a bilateral deficit; however, the results varied according to group (swimmers vs. nonathletes). The BLRLegForce was significantly different from 100 for both swimmers (p = 0.002) and nonathletes (p = 0.020). The BLRLegEMG was not significantly different from 100 for swimmers (p = 0.055) or nonathletes (p = 0.27). BLRHandForce and BLRHandEMG were not significantly different from 100 (p > 0.05).
Discussion The BLD phenomenon has been studied in several populations; however, to our knowledge this is the first study to examine swimmers. It was hypothesized that swimmers would have a lower bilateral deficit because of their bilateral training. Contrary to our hypothesis, the results of the present study showed no significant differences between swimmers and nonathletes for BLRLegForce, BLRLegEMG, BLRHandForce, and BLRHandEMG. While BLRLegForce and BLRLegEMG showed a deficit across both groups, there was no evidence of a deficit in BLRHandForce and BLRHandEMG. The lack of difference between the 2 groups may have been due to the training status of the swimmers. While all swimmers that participated in this study were recruited from the university varsity swim team, the participants were not categorized according to their stroke. It is possible that differences in their individual training backgrounds could have affected the findings. Of the 9 swimmers who participated in this study, 6 practiced bilateral movements. Increased sample size of swimmers who train bilaterally may provide more insight into the BLD. Similar to the present study, Secher et al. (1988) and Schantz et al. (1989) found no differences between groups of trained and untrained participants. Secher et al. (1988) compared unilateral and bilateral leg extension strength between cyclists, weightlifters, and untrained participants. Their results showed no significant differences; however, there were large differences in population size between groups. Schantz et al. (1989) performed a cross-sectional study between untrained participants, physical education students, ballet dancers, volleyball players, and strength-trained participants. They compared bilateral and unilateral leg extensions between Published by NRC Research Press
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groups and found no significant differences. Contrary to these studies, Howard and Enoka (1991) examined isometric knee extensions in weightlifters, cyclists, and untrained participants. They found a deficit for untrained participants, no deficit for cyclists, and a bilateral facilitation for weightlifters. Intensity and duration of training as well as population size could have caused discrepancies between studies. While the BLD has been shown in both males and females, the previously mentioned training studies examined predominantly male participants between the ages of 20–39 years. Specifics were not provided concerning frequency of training, making it difficult to compare across studies. The present study examined only a small sample of swimmers and did not control for individual techniques. This factor, along with individual differences in training methods, could explain why no significant differences were found. Future studies should carefully examine prior training status of individuals involved. The nonathletes were asked about their exercise participation prior to the study and all indicated that they exercised less than 3 times per week. Unfortunately, the specific type of exercises this group participated in was not recorded and it is possible that the nonathletic group may have trained bilaterally and thus been less prone to a deficit than this particular group of swimmers. In the future, the background of the nonathletic group should be carefully monitored to avoid this. The isometric leg press showed a BLD in both swimmers and nonathletes, while the handgrip exercise did not reveal a BLD in either group. This is consistent with other studies in the literature (Matkowski et al. 2010; Secher et al. 1988; Hay et al. 2006; Cresswell and Ovendal 2002; Kuruganti and Murphy 2008; Kuruganti and Seaman 2006). The BLD is more evident in dynamic exercises (e.g., isokinetic knee extension) than isometric contractions (Jakobi and Chilibeck 2001). Handgrip exercises have shown varied results across studies. Ohtsuki (1981a, 1981b) reported BLD in handgrip; however, Seki and Ohtsuki (1990) did not detect a BLD in the same exercise. The differences in the studies may have been due to the differences in the instrumentation used to measure the contractions (Jakobi and Chilibeck 2001). Seki and Ohtsuki (1990) used an apparatus that was also used to study isometric elbow extension. Participants were required to sit on a chair with their eyes closed and their forearms on a table at approximately 90° of flexion. Ohstuki (1981a, 1981b) examined handgrip in a similar position (seated with elbow flexed); however, they examined individual finger forces by using plaster to limit movement in the various digits. In addition, they used fine wire EMG rather than surface EMG to monitor muscle activity. In the present study, participants were asked to stand with their arms lowered (sides of body) with their eyes open and surface EMG was used to monitor activity. It is not surprising in this work that no differences were detected in the handgrip EMG as no BLD was detected in this exercise. In addition, while 2 wrist flexors were examined with EMG in this work (FCR and FCU), no antagonist muscle activity was recorded for the wrist. This may have provided further evidence of the neural mechanisms during the handgrip exercise. Magnus and Farthing (2008) investigated isometric handgrip and dynamic leg press and showed that muscle activation of the agonist muscles were not significantly different between unilateral and bilateral conditions for either exercise. They did find that the BLD for leg press that was larger than the BLD for handgrip. These provide evidence that lower body exercises involving multiple large muscle groups exhibit a larger BLD. This could be due to larger postural stability requirements (Magnus and Farthing 2008) or a larger involvement of the nervous system during contractions that involve movement at multiple joints (Chilibeck et al. 1998). Janzen et al. (2006) also found that movements involving multiple joints, such as leg press and lateral pull-down exercises, exhibited a larger deficit than movements involving a single joint, such as a knee extension exercise. While a deficit was detected overall for individual groups in the torque data, the results from the EMG data varied. A deficit was detected overall (swim-
Appl. Physiol. Nutr. Metab. Vol. 39, 2014
mers and nonathletes); however, when the individual groups were analyzed a deficit in the EMG data was not significantly different from 100%. This suggests that neural mechanisms could be the source of the deficit; however, it is also possible that other factors may have contributed to the deficit, such as the postural stability requirements of the leg press. Cresswell and Ovendal (2002) found a deficit in torque and EMG for the quadriceps group during isokinetic knee extensions. Kuruganti and Murphy (2008) found a similar BLD in torque and EMG data during isometric knee extensions. Oda and Moritani (1995) and Ohtsuki (1983) also found a simultaneous bilateral deficit for force and EMG activity. However, other studies did not report a correlation between BLD force and EMG activity (Howard and Enoka 1991; Shantz et al. 1989). Despite a lack of consistency between studies, the majority of evidence indicates that the bilateral deficit does have a neural influence.
Conclusions This study found that a BLD is present during bilateral isometric leg press and not present during bilateral handgrip exercises for both female swimmers and female nonathletes. There were no significant differences between the bilaterally trained swimmers and nonathletes. These results suggest that the training status of the individual may have little influence on the BLD. It is also possible that the training status between our 2 groups was not different enough to influence the BLD. In addition, the definition of a bilaterally trained group may need to be re-examined and more specifically defined. Studies have examined cyclists and figure skaters and have claimed that these individuals are bilaterally trained (Howard and Enoka 1991; Kuruganti and Chester 2009). However, these groups as well as swimmers do repetitive out-ofphase motions. It has been found that flexion in 1 arm and extension in the other showed no evidence of a bilateral deficit (Ohtsuki 1983). Howard and Enoka (1991) did an arm–leg task that demonstrated that the bilateral deficit affects only homologous contralateral muscles. Since most movements in swimming are repeated patterns with the contralateral limbs doing opposing motions (in-phase–out-of-phase motion), this may not be considered a bilateral activity. While every effort was made to maintain a 90° hip flexion angle, it is possible that there were individual variations that may have affected maximal force and should be considered in future studies. This study was the first to examine swimmers and compare them with nonathletes. While a BLD was detected in both groups, future studies should examine individuals bilaterally trained in-phase (rowers, weightlifters) and bilaterally trained out-of-phase (swimmers, speed skaters, cyclists) to compare the extent of the BLD in these populations.
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ARTICLE Comparison of bilateral and unilateral contractions between swimmers and nonathletes during leg press and hand grip exercises Monica MacDonald, Danielle Losier, Victoria L. Chester, and Usha Kuruganti
Abstract: The bilateral limb deficit (BLD) is defined as the reduction in force production during bilateral compared with summed unilateral contractions of homologous muscles. The underlying mechanism for the BLD has been elusive to determine. The purpose of this study was to examine the presence of the BLD during maximal isometric leg press and handgrip exercises in female swimmers (n = 9, mean age = 20.1 ± 1.3 years) and nonathletes (n = 9, mean age = 21.7 ± 1.3 years) to gain further insight into this phenomenon. Force and electromyography (EMG) measures were collected from participants under bilateral and unilateral conditions for handgrip and leg press exercises. Bilateral limb ratios (BLR) were calculated for swimmers (BLRS) and nonathletes (BLRNA). A deficit was found for swimmers and nonathletes in leg force (BLRS = 79.84% ± 13.09% and BLRNA = 81.44% ± 19.23%) and leg EMG (BLRS = 88.45% ± 15.41% and BLRNA = 94.66% ± 13.62%); however, no BLD was seen in hand force (BLRS = 98.30% ± 11.21% and BLRNA = 95.91% ± 11.04%) and hand EMG (BLRS = 102.42% ± 11.20% and BLRNA = 103.30% ± 16.50%). Furthermore, no significant differences were found between groups for leg force, leg EMG, hand force, and hand EMG. In conclusion, a BLD was detected for both groups during bilateral isometric leg press. This suggests that while the BLD may be affected by neural influences, there may other factors involved such as postural stability requirements to perform the exercise. Key words: athletes, skeletal muscle function, exercise performance, human performance, muscle physiology. Résumé : Le déficit segmentaire bilatéral (« BLD ») se définit par la diminution de la force produite bilatéralement en comparaison a` la somme des forces produites unilatéralement par les mêmes muscles. Les mécanismes a` la base du BLD ne sont pas connus. Cette étude se propose d’examiner la présence du BLD au cours d’efforts maximaux dans un développé des jambes et d’exercices de préhension manuelle en condition isométrique chez des nageuses (n = 9, âge moyen= 20,1 ± 1,3 ans) et des non-athlètes (n = 9, âge moyen = 21,7 ± 1,3 ans), et ce, afin de comprendre davantage ce phénomène. On évalue la force et l’activité myoélectrique (« EMG ») des participants au cours d’exercices de préhension et de développé des jambes en condition bilatérale et unilatérale. On calcule les ratios segmentaires bilatéraux (« BLR ») des nageuses (« BLRS ») et des non-athlètes (« BLRNA »). On observe un déficit chez les nageuses et les non-athlètes aux plans de la force des jambes (BLRS = 79,84 ± 13,09 % et BLRNA = 81,44 ± 19,23 %) et de l’EMG des jambes (BLRS = 88,45 ± 15,41 % et BLRNA = 94,66 ± 13,62 %); cependant, on n’observe pas de BLD dans la force des mains (BLRS = 98,30 ± 11,21 % et BLRNA = 95,91 ± 11,04 %) et l’EMG de la préhension (BLRS = 102,42 ± 11,20 % et BLRNA = 103,30 ± 16,50 %). En outre, on n’observe pas de différence significative entre les groupes en ce qui concerne la force des jambes, l’EMG des jambes, la force des mains et l’EMG de la préhension. En conclusion, on note dans les deux groupes la présence d’un BLD au cours d’un développé bilatéral isométrique des jambes. Ces résultats suggèrent que des influences nerveuses probables agissent sur le BLD en même temps que d’autres facteurs impliqués dans la stabilisation de la posture pour la réalisation des exercices. [Traduit par la Rédaction] Mots-clés : athlètes, fonction du muscle squelettique, performance kinésique, performance humaine, physiologie humaine.
Introduction Bilateral limb deficit (BLD) is the reduction in force that accompanies maximal 2-limb efforts relative to single-limb performances (Howard and Enoka 1991). BLD is found in both large and small muscle groups (Howard and Enoka 1991; Oda and Moritani 1995; Schantz et al. 1989; Secher et al. 1988) and athletic and nonathletic populations (Secher et al. 1988; Schantz et al. 1989; Kuruganti and Murphy 2008). The underlying mechanism of the deficit has been elusive to determine. There have been suggestions that the decline in force during bilateral contractions could be due to some form of neural inhibition (Archontides and Fazey 1993; Howard and Enoka 1991); however, there have been mixed results in the literature (Jakobi and Chilibeck 2001).
Electromyography (EMG) has been used in past studies to examine the source of the deficit. The signal resulting from EMG, the myoelectric signal (MES), measures the neural commands sent to the muscle and provides evidence of the neural mechanisms causing the deficit. However, studies to date have been mixed regarding the relationship between the force and EMG deficits, with some studies suggesting that amplitude of the MES is lower under bilateral conditions versus unilateral conditions (Kuruganti and Murphy 2008; Cresswell and Ovendal 2002; Kawakami et al. 1998; Koh et al. 1993; Oda and Moritani 1995; Ohtsuki 1981b, 1983; Rube and Secher 1990; Steger and Denoth 1996; Van Soest et al. 1985; Vandervoort et al. 1984), while others show no deficit in the EMG data (Howard and Enoka 1991; Owings and Grabiner 1998; Schantz et al. 1989). Because studies have shown varying results, it has
Received 7 February 2014. Accepted 11 June 2014. M. MacDonald, D. Losier, V.L. Chester, and U. Kuruganti. Andrew and Marjorie McCain Human Performance Laboratory, Faculty of Kinesiology, University of New Brunswick, Fredericton, NB E3B 5A3, Canada. Corresponding author: Usha Kuruganti (e-mail: [email protected]). Appl. Physiol. Nutr. Metab. 39: 1–5 (2014) dx.doi.org/10.1139/apnm-2014-0040
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been difficult to identify the mechanism of the deficit; however, 2 primary theories that have been proposed are the neural inhibition theory and the postural stability theory. Several researchers have cited neural inhibition as the cause of the BLD (Magnus and Farthing 2008; Ohtsuki 1983; Post et al. 2007; Van Dieen et al. 2003). Ohtsuki (1983) proposed that the deficit could be related to inhibitory spinal reflexes, which occurs when the neural control for 1 limb is affected when the opposite limb is simultaneously activated. Others attributed the BLD to reduced motor neuron excitability during bilateral contraction (Kawakami et al. 1998). Most evidence points towards interhemispheric inhibition as a potential cause of the deficit, where the activity in 1 hemisphere can affect the activity in the opposite hemisphere when they are concurrently activated, thereby decreasing neural drive to the muscles (Oda and Moritani 1995; Taniguchi et al. 2001; Van Dieen et al. 2003). Another possible explanation for the BLD is the postural stability requirements of the exercise (Herbert and Gandevia 1996; Magnus and Farthing 2008). While the BLD has been shown to be present in both upper and lower body movements, its presence has been more evident during dynamic contractions (Kuruganti and Seaman 2006). Multi-jointed lower body exercises involving large muscles and high force generation may require more postural stability than upper body exercises and therefore sustain a greater deficit (Lan 2002). Exercises involving multiple muscle groups and higher ground reaction forces, such as the leg press, might exhibit larger bilateral deficits because it is more difficult to maintain postural stability under the bilateral condition (Magnus and Farthing 2008). Studying these types of movements could provide a better understanding of the cause of the BLD and the impact of stability on the BLD. Interestingly, it has been shown that the BLD can be improved with targeted training. Several bilateral training programs have been shown to decrease the BLD (Janzen et al. 2006; Kuruganti et al. 2005; Taniguchi 1998). Janzen et al. (2006) implemented a 26-week bilateral training program. Initially, they found a BLD for both leg press and lateral pull-down exercises. They found that bilateral training decreased the deficit. Kuruganti et al. (2005) found similar results after a 6-week knee extension training program. Taniguchi (1998) also implemented a 6-week training program and found that BLD decreased with bilateral training and increased with unilateral training in both arm and leg extensions. Other studies have shown that sport-specific training can eliminate the bilateral limb deficit and even result in bilateral facilitation (Howard and Enoka 1991; Secher 1975). Secher (1975) found that oarsmen had bilateral leg strength comparable with their summed unilateral leg strength and that more experienced rowers showed no deficit. While studies of specific athletes have been conducted to study the BLD, no studies to date have examined swimmers and compared them with nonathletes. Swimmers are a group of interest because they are bilaterally trained and could provide evidence towards the training theory. A better understanding of the BLD and its underlying mechanisms can be used to improve training programs in populations where maximal bilateral force output is required. The present study examined BLD in swimmers and nonathletes for both leg press and handgrip exercises. Along with force output, EMG data was collected to provide insight into the underlying mechanism of the deficit. It was hypothesized that swimmers would exhibit a smaller BLD or even bilateral facilitation compared with nonathletes for both exercises because of their bilateral training background. Because of the postural stability requirements of the leg press, it was expected that this exercise would show a larger BLD than the handgrip exercise across both groups (Magnus and Farthing 2008).
Appl. Physiol. Nutr. Metab. Vol. 39, 2014
Materials and methods Eighteen female participants volunteered for this study, comprising 9 women from the university varsity swimming team (mean age, 20.1 ± 1.3 years; mean height, 1.70 ± 0.04 m; mean body mass, 68.3 ± 5.4 kg) and 9 women who were untrained controls (mean age, 21.7 ± 1.3 years; mean height, 1.70 ± 0.07 m; mean weight, 69.7 ± 4.5 kg). The participants were considered to be untrained if they exercised less than 3 times per week. Trained participants were involved in a swimming program at least 7 times per week. Of the 9 swimmers, 6 regularly practiced strokes involving bilateral movements (fly, breast), while the remaining swimmers regularly practiced free style and backstroke. Participants were required to complete the Canadian Society for Exercise Physiology’s Physical Activity Readiness Questionnaire as well as an informed consent form before participating in the study. This study was approved by the University of New Brunswick Research Ethics Board. Instrumentation A Cybex Humac Norm (CSMI Inc., USA) isokinetic dynamometer fitted with a closed kinetic chain adaptor was used to collect isometric leg press data both unilaterally and bilaterally. Handgrip strength was collected using custom-made force transducers. Surface EMG was used to examine muscle activity during all contractions. A 16-channel wireless EMG system (Aurion Inc., Italy) was used to collect muscle activity data. This system has an input impedance of 20 MOhm, a common mode rejection ratio of 90 dB, and a signal to noise ratio >50 dB. The gain of each channel was 1000. The system has an analog resistor-capacitor DC filter for both high pass (to remove the DC component) and low pass filtering (as an anti-alias). The bandwidth of the signal was 10–500 Hz and the slopes of the cut-offs were 6 dB/octave. Force and EMG data were sampled at a frequency of 1500 Hz for 5 s using personalcomputer– based software and a 16-bit A/D board (Tektronix, TM 5006, Lake Mary, Fla., USA), interfaced to a personal computer. Further processing was performed off-line using a custom-built Labview 6.1 program (National Instruments, Tex., USA). EMG data collection During all strength tests, bipolar surface electrodes (Duotrode silver–silver chloride electrodes (Myo-tronics Inc.); interlelectrode spacing = 21.0 ± 1.0 mm) were placed over the muscles of interest. Prior to application of the electrodes, the participant’s skin was abraded and cleaned with alcohol. Electrodes were placed bilaterally (right and left) over the belly of the muscles of interest according to standardized procedures (Criswell 2010). For the leg press exercise, electrodes were placed over the rectus femoris at half the distance between the knee (superior part of the patella) and the iliac spine. Electrodes were placed over the right and left vastus medialis at an oblique angle (55°), 2 cm medially from the superior rim of the patella. Electrodes were then placed over the biceps femoris parallel to the muscle fibers on the lateral aspect of the thigh at two-thirds of the distance between the trochanter and the back of the knee crease (midpoint between the lateral and medial femoral condyles). For the handgrip exercise, similar to Magnus and Farthing (2008), electrodes were placed bilaterally over the flexor carpi ulnaris (FCU) on the medial aspect of the forearm, 2% of the distance from the elbow (midpoint between the lateral and medial epicondyles) to the wrist (midpoint between the ulnar and radial styloids). To examine other possible contributions from surrounding muscles, electrodes were also placed bilaterally on the flexor digitorum superficialis in the midline of the forearm three-fourths of the distance from the elbow to the. Electrodes were then placed on the flexor carpi radialis (FCR) on the ventral aspect of the forearm near the elbow on the medial side of the arm. Published by NRC Research Press
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Table 1. Mean values for leg force and handgrip force for both swimmers and nonathletes.
Swimmers Nonathletes Total
Bilateral leg force (Nm)
Unilateral left leg force (Nm)
Unilateral right leg force (Nm)
Bilateral hand force (N)
Unilateral left hand force (N)
Unilateral right hand force (N)
402.52±155.62 463.99±137.29 433.25±145.83
254.29±83.86 286.83±90.12 270.56±86.09
245.85±69.24 288.03±70.31 266.94±71.09
348.76±77.32 336.96±44.09 342.86±61.36
194.27±38.55 198.73±25.44 196.50±31.76
159.38±21.49 154.28±21.10 156.83±20.36
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Note: Values are means ± SD. No statistical significant difference was detected in leg force or hand force between the 2 groups (swimmers and nonathletes).
Table 2. Mean values for bilateral limb ratio (BLR) leg force, BLR leg electromyography (EMG), BLR hand force, and BLR hand EMG for both swimmers and nonathletes.
Swimmers Nonathletes Total
BLR leg force (%)
BLR leg EMG (%)
BLR hand force (%)
BLR hand EMG (%)
79.84±13.09 81.44±19.23 80.64±15.98*
88.45±15.41 94.66±13.62 91.55±14.47*
98.30±11.21 95.91±11.04 97.10±10.86
102.42±11.20 103.30±16.50 102.86±13.69
Note: Values are means ± SD. The BLR was calculated as BLR (%) = (peak bilateral force)/(sum of peak unilateral forces) × 100 (Ohtsuki 1983). No significant differences were found between swimmers and nonathletes. *Significant difference from 100% (p < 0.05) and therefore a deficit.
Isometric strength testing For the leg press exercise, participants were seated upright at a self-selected seat back angle and horizontal translation to assure comfort. The dynamometer was adjusted so that the participant’s knees were at a 90° angle. Generally, hip angle was maintained at 90°; however, to ensure that the participant’s back was resting comfortably against the dynamometer chair this resulted in the hip angle varying for each participant (85–100°). Participants were instructed to cross their arms during the trials to ensure that there was no force being generated by the upper body. Participants were asked to perform 3 maximal voluntary contractions (MVCs) unilaterally for the right and left leg, as well as 3 MVCs bilaterally. Participants held the contraction for 5 s to allow them to reach their maximal force. Two-minute rest periods were given in between trials to ensure participants were able to adequately recover. The order of the testing conditions (i.e., unilateral, bilateral) was randomized. For the handgrip exercise, participants were in a standing position with their hands by their sides. Participants were asked to perform 3 MVCs with each their right and left hand, and 3 MVCs bilaterally. Again, 2-min rest periods were given between all trials to avoid fatigue. During all contractions, participants were provided with verbal encouragement to “push as hard” as they could. Finally, the order of the exercises (leg press and handgrip) was randomized and all tests were completed in 1 session. Data analysis For each activity (leg press and handgrip), the trial with the highest peak force was chosen for further analysis. The amplitude of the EMG signal was estimated using the root mean square (RMS) calculation. A 0.5-s window of EMG data, centred at the peak force was used for all calculations similar to previous studies (Kuruganti and Murphy 2008, Kuruganti et al. 2011). The bilateral limb ratio (BLRForce) was calculated as in previous studies (Howard and Enoka 1991; Jakobi and Chilibeck 2001; Ohtsuki 1983). The BLR was calculated for both leg press and handgrip using the peak force data from unilateral left (ULL), unilateral right (ULR), and bilateral (BL) contractions as: BLRForce (%) = [(peak force BL)/(peak force ULL + peak force ULR)] × 100 (Ohtsuki 1983). A BLR was also calculated from the EMG data (BLREMG) similar to previous studies (Kuruganti and Murphy 2008). The RMS values of each agonist muscle were summed for each limb and the corresponding antagonist activity was then subtracted to better reflect the net activity. These values were then used in all of the BLREMG calculations. A series of 1-way ANOVAs were used to test for mean differences in the dependent variables between swimmers and nonathletes. The ␣ level was set to 0.05. Student’s t tests were run to determine
if the BLR values were significantly different than 100%, thereby identifying the presence of a BLD.
Results Mean force data for the leg press and handgrip are shown in Table 1. BLD data (BLRLegForce, BLRLegEMG, BLRHandForce, and BLRHandEMG) for each group and both groups combined are listed in Table 2. One-way ANOVAs showed no significant differences in mean values between groups in any of the dependant variables (p > 0.05). Results of the t tests showed that the BLRLegForce and the BLRLegEMG were significantly different from 100 (p < 0.001 and p = 0.024, respectively), indicating a bilateral deficit; however, the results varied according to group (swimmers vs. nonathletes). The BLRLegForce was significantly different from 100 for both swimmers (p = 0.002) and nonathletes (p = 0.020). The BLRLegEMG was not significantly different from 100 for swimmers (p = 0.055) or nonathletes (p = 0.27). BLRHandForce and BLRHandEMG were not significantly different from 100 (p > 0.05).
Discussion The BLD phenomenon has been studied in several populations; however, to our knowledge this is the first study to examine swimmers. It was hypothesized that swimmers would have a lower bilateral deficit because of their bilateral training. Contrary to our hypothesis, the results of the present study showed no significant differences between swimmers and nonathletes for BLRLegForce, BLRLegEMG, BLRHandForce, and BLRHandEMG. While BLRLegForce and BLRLegEMG showed a deficit across both groups, there was no evidence of a deficit in BLRHandForce and BLRHandEMG. The lack of difference between the 2 groups may have been due to the training status of the swimmers. While all swimmers that participated in this study were recruited from the university varsity swim team, the participants were not categorized according to their stroke. It is possible that differences in their individual training backgrounds could have affected the findings. Of the 9 swimmers who participated in this study, 6 practiced bilateral movements. Increased sample size of swimmers who train bilaterally may provide more insight into the BLD. Similar to the present study, Secher et al. (1988) and Schantz et al. (1989) found no differences between groups of trained and untrained participants. Secher et al. (1988) compared unilateral and bilateral leg extension strength between cyclists, weightlifters, and untrained participants. Their results showed no significant differences; however, there were large differences in population size between groups. Schantz et al. (1989) performed a cross-sectional study between untrained participants, physical education students, ballet dancers, volleyball players, and strength-trained participants. They compared bilateral and unilateral leg extensions between Published by NRC Research Press
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groups and found no significant differences. Contrary to these studies, Howard and Enoka (1991) examined isometric knee extensions in weightlifters, cyclists, and untrained participants. They found a deficit for untrained participants, no deficit for cyclists, and a bilateral facilitation for weightlifters. Intensity and duration of training as well as population size could have caused discrepancies between studies. While the BLD has been shown in both males and females, the previously mentioned training studies examined predominantly male participants between the ages of 20–39 years. Specifics were not provided concerning frequency of training, making it difficult to compare across studies. The present study examined only a small sample of swimmers and did not control for individual techniques. This factor, along with individual differences in training methods, could explain why no significant differences were found. Future studies should carefully examine prior training status of individuals involved. The nonathletes were asked about their exercise participation prior to the study and all indicated that they exercised less than 3 times per week. Unfortunately, the specific type of exercises this group participated in was not recorded and it is possible that the nonathletic group may have trained bilaterally and thus been less prone to a deficit than this particular group of swimmers. In the future, the background of the nonathletic group should be carefully monitored to avoid this. The isometric leg press showed a BLD in both swimmers and nonathletes, while the handgrip exercise did not reveal a BLD in either group. This is consistent with other studies in the literature (Matkowski et al. 2010; Secher et al. 1988; Hay et al. 2006; Cresswell and Ovendal 2002; Kuruganti and Murphy 2008; Kuruganti and Seaman 2006). The BLD is more evident in dynamic exercises (e.g., isokinetic knee extension) than isometric contractions (Jakobi and Chilibeck 2001). Handgrip exercises have shown varied results across studies. Ohtsuki (1981a, 1981b) reported BLD in handgrip; however, Seki and Ohtsuki (1990) did not detect a BLD in the same exercise. The differences in the studies may have been due to the differences in the instrumentation used to measure the contractions (Jakobi and Chilibeck 2001). Seki and Ohtsuki (1990) used an apparatus that was also used to study isometric elbow extension. Participants were required to sit on a chair with their eyes closed and their forearms on a table at approximately 90° of flexion. Ohstuki (1981a, 1981b) examined handgrip in a similar position (seated with elbow flexed); however, they examined individual finger forces by using plaster to limit movement in the various digits. In addition, they used fine wire EMG rather than surface EMG to monitor muscle activity. In the present study, participants were asked to stand with their arms lowered (sides of body) with their eyes open and surface EMG was used to monitor activity. It is not surprising in this work that no differences were detected in the handgrip EMG as no BLD was detected in this exercise. In addition, while 2 wrist flexors were examined with EMG in this work (FCR and FCU), no antagonist muscle activity was recorded for the wrist. This may have provided further evidence of the neural mechanisms during the handgrip exercise. Magnus and Farthing (2008) investigated isometric handgrip and dynamic leg press and showed that muscle activation of the agonist muscles were not significantly different between unilateral and bilateral conditions for either exercise. They did find that the BLD for leg press that was larger than the BLD for handgrip. These provide evidence that lower body exercises involving multiple large muscle groups exhibit a larger BLD. This could be due to larger postural stability requirements (Magnus and Farthing 2008) or a larger involvement of the nervous system during contractions that involve movement at multiple joints (Chilibeck et al. 1998). Janzen et al. (2006) also found that movements involving multiple joints, such as leg press and lateral pull-down exercises, exhibited a larger deficit than movements involving a single joint, such as a knee extension exercise. While a deficit was detected overall for individual groups in the torque data, the results from the EMG data varied. A deficit was detected overall (swim-
Appl. Physiol. Nutr. Metab. Vol. 39, 2014
mers and nonathletes); however, when the individual groups were analyzed a deficit in the EMG data was not significantly different from 100%. This suggests that neural mechanisms could be the source of the deficit; however, it is also possible that other factors may have contributed to the deficit, such as the postural stability requirements of the leg press. Cresswell and Ovendal (2002) found a deficit in torque and EMG for the quadriceps group during isokinetic knee extensions. Kuruganti and Murphy (2008) found a similar BLD in torque and EMG data during isometric knee extensions. Oda and Moritani (1995) and Ohtsuki (1983) also found a simultaneous bilateral deficit for force and EMG activity. However, other studies did not report a correlation between BLD force and EMG activity (Howard and Enoka 1991; Shantz et al. 1989). Despite a lack of consistency between studies, the majority of evidence indicates that the bilateral deficit does have a neural influence.
Conclusions This study found that a BLD is present during bilateral isometric leg press and not present during bilateral handgrip exercises for both female swimmers and female nonathletes. There were no significant differences between the bilaterally trained swimmers and nonathletes. These results suggest that the training status of the individual may have little influence on the BLD. It is also possible that the training status between our 2 groups was not different enough to influence the BLD. In addition, the definition of a bilaterally trained group may need to be re-examined and more specifically defined. Studies have examined cyclists and figure skaters and have claimed that these individuals are bilaterally trained (Howard and Enoka 1991; Kuruganti and Chester 2009). However, these groups as well as swimmers do repetitive out-ofphase motions. It has been found that flexion in 1 arm and extension in the other showed no evidence of a bilateral deficit (Ohtsuki 1983). Howard and Enoka (1991) did an arm–leg task that demonstrated that the bilateral deficit affects only homologous contralateral muscles. Since most movements in swimming are repeated patterns with the contralateral limbs doing opposing motions (in-phase–out-of-phase motion), this may not be considered a bilateral activity. While every effort was made to maintain a 90° hip flexion angle, it is possible that there were individual variations that may have affected maximal force and should be considered in future studies. This study was the first to examine swimmers and compare them with nonathletes. While a BLD was detected in both groups, future studies should examine individuals bilaterally trained in-phase (rowers, weightlifters) and bilaterally trained out-of-phase (swimmers, speed skaters, cyclists) to compare the extent of the BLD in these populations.
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