Strength normalized to muscle volume rather than body weight is more accurate for assessing knee strength following anterior cruciate ligament reconstruction

Abstract

BACKGROUND:

Knee strength weakness is a major problem frequently observed in patients during postoperative rehabilitation following anterior cruciate ligament reconstruction (ACLR).

OBJECTIVE:

To investigate whether knee strength normalized to muscle volume could better detect side-to-side differences than that normalized to body weight following ACLR.

METHOD:

This study included 17 patients who had undergone primary ACLR (11.6 $\pm$ 2.3 months). Body weight and total muscle volume were measured using a bioelectrical impedance analysis composition scale. Isokinetic knee extension and flexion moment were measured at 60 ${}^{\circ}$ /s and 180 ${}^{\circ}$ /s, respectively. Bivariate correlation analysis was used to examine correlations between body composition and knee strength. Differences in knee strength between the operated and unoperated legs were analyzed using a paired $t$ -test, which calculated the effect size.

RESULTS:

There was a significant correlation between knee strength and body weight ( $r=$ 0.53–0.67); however, a stronger correlation was observed between knee strength and total muscle volume ( $\rho=$ 0.80–0.87). The effect size was larger for knee strength expressed as % total muscle volume than for knee strength expressed as % body weight.

CONCLUSION:

Strength expressed as % total muscle volume may be more accurate than that expressed as % body weight for detecting side-to-side differences in knee strength following ACLR.

Keywords

ACL reconstruction isokinetic moment isokinetic strength muscle mass

1. Introduction

Knee strength weakness is a major problem frequently observed in patients during postoperative rehabilitation following anterior cruciate ligament reconstruction (ACLR) [1]. Knee strength weakness following ACLR is associated with functional impairments, such as loss of motion [2] and movement abnormalities [3], which can lead to worse outcomes, such as failure to return to sports [4] and increased risk of re-injury and osteoarthritis [5, 6]. A meta-analysis showed that knee extension weakness persisted for 2 years after ACLR [7]. Therefore, it is important to measure knee strength during rehabilitation after ACLR.

As muscle strength is dependent on body size, it is often normalized by body weight and other body size variables [8]. When assessing knee strength in post-ACLR patients, strength is most often normalized by body weight [4, 6, 9]. In isokinetic dynamometry, which is the standard method for assessing knee strength in post-ACLR patients [10], the value normalized by body weight is known as the normalized moment (in Nm/kgbw). In clinical settings, the degrees of weakness and recovery of the operated leg relative to the unoperated leg are monitored based on these values.

The method of normalizing knee strength by body weight is easy but has theoretical problems. Physiologically, muscle strength is influenced by muscle volume [11, 12, 13]. As body weight includes the weight of fat and other body composition components in addition to muscle volume, there can be differences in muscle volume for the same body weight [14]. In a study that showed normative data for knee strength and body composition in healthy individuals, the association between body weight and isokinetic knee extension strength in women was low ( $r^{2}=$ 0.14) [15]. In healthy athletes, lean body mass ( $r=$ 0.84–0.89) was correlated more strongly with lower extremity muscle strength than body weight ( $r=$ 0.45–0.51) [16]. Therefore, it is necessary to consider how to normalize knee strength using variables other than body weight.

Body composition scales using bioelectrical impedance analysis (BIA) can accurately measure muscle volume and have become commonplace in clinical settings [17]. In post-ACLR patients, normalization of isokinetic knee strength by muscle volume measured with body composition scales may yield different results from those normalized by body weight. However, no previous reports have examined the relationship between muscle volume and knee strength in post-ACLR patients.

Therefore, this study aimed to determine the relationship between isokinetic knee strength and body weight, and those between isokinetic knee strength and muscle volume in post-ACLR patients. Similarly, we aimed to determine the characteristics of the side-to-side differences in knee strength normalized to body weight and muscle volume. We established the following hypotheses: first, muscle volume is more correlated with knee strength compared to body weight; second, knee strength normalized to muscle volume could be more accurate in detecting side-to-side differences between the operated and unoperated legs compared to knee strength normalized to body weight.

2. Methods

2.1 Participants

Patients who underwent primary unilateral ACLR between March 2018 and November 2019 were included if they met the following criteria: (1) age, 16–45 years at the time of measurements [18, 19]; (2) participation in sports with modified Tegner activity scale score [20] $\geqslant$ 5 before ACL injury; (3) autografts sourced from the hamstrings and bone-patellar tendon-bone; and (4) a period of 8–24 months having passed since surgery. This period was established with reference to a previous study [7] wherein knee strength weakness in post-ACLR patients persisted for 24 months after surgery. The sample size was calculated using G*power software (Universität Düsseldorf, Düsseldorf, Germany) [21]. Based on a previous study [22] that analyzed the correlation between knee strength and body composition, the minimum sample size was 17 (effect size $=$ 0.60, alpha $=$ 0.05, power $=$ 0.80, two-tailed). All surgeries were performed by orthopedic surgeons who specialize in knee surgery.

2.2 Procedure

This was a single-center, cross-sectional study. Demographic, injury, and surgical information was collected from medical records and questionnaires. The participants’ knee strength and body composition were measured on the same day. The study was reviewed and approved by the review board of Tokyo Medical and Dental University (approval number: M2019-158) and was performed in accordance with the ethical standards of the Declaration of Helsinki. All participants provided written informed consent prior to participation.

2.3 Postoperative rehabilitation

The postoperative rehabilitation protocol was based on a previous research [23]. Range of motion and quadriceps isometric contraction exercises were started 3 days after surgery. Crutches and a straight-position knee-joint immobilizer (Knee brace, ALCARE Co., Ltd., Tokyo, Japan) were used and, then, gradually phased out from 4 weeks post-ACLR. Closed kinetic chain exercises, such as squatting and lunge, began at 1–2 weeks post-ACLR. Jogging started at least 3 months post-ACLR, and running speed was gradually increased. After 80% of full-speed running was achieved, athletic exercises related to their sports activities started. Sports participation was allowed by a physician when the following criteria were met: at least 7 months after ACLR had passed; the limb symmetry index (LSI) on the single-leg hop distance was $>$ 90%; and the LSI of isokinetic knee extension and flexion moment was $>$ 85%, as measured with a BIODEX System 4 Isokinetic Dynamometer (BIODEX Medical Inc., Shirley, NY) at 60 ${}^{\circ}$ /s and 180 ${}^{\circ}$ /s. The LSI was calculated as the ratio of the value in the operated leg to that in the unoperated leg [24]. The postoperative rehabilitation protocol was the same for all patients. However, patients who underwent repair of the middle-posterior segment of the meniscus were prohibited from deep squatting or bending the knee more than 90 ${}^{\circ}$ until 3 months after ACLR.

2.4 Body composition measurement

Body weight, body fat, and total muscle volume were measured in this study. Body composition was measured using BIA with a Tanita dual-body composition scale (DC-430A; Tanita, Tokyo, Japan). BIA estimates body composition by applying harmless low-frequency electric current to the body based on the principle that electric current flows faster through tissues with a higher water and electrolyte content (such as muscles) than less hydrated tissues (such as fat) [25]. DC-430A is a dual-frequency (6.25 and 50 kHz) BIA device that uses four electrodes and is based on reactance technology [26], a method that measures the body composition more accurately than conventional BIA method by adopting reactance values together with impedance values. As the algorithm was based on substantial data, the body composition measured by this system is highly correlated with measurements obtained by dual energy X-ray absorptiometry (DXA) [27, 28]. Participants were dressed in standard sports clothes with only shorts and $t$ -shirts and were barefoot during measurements.

To ensure normal hydration status for BIA testing, the participants were asked to adhere to the following pretest requirements, as described in previous studies [17, 25]: at least 2 h should have passed since consuming the last meal; they should have completed urination and defecation before measurement; and no excessive alcohol or caffeine should have been consumed at least 12 h prior to the measurement. Body composition measurements were taken before muscle strength measurements.

2.5 Knee strength measurement

Knee strength was assessed using an isokinetic dynamometer (Biodex System 4). Isokinetic knee extension and flexion moment were measured concentrically at angular velocities of 60 ${}^{\circ}$ /s and 180 ${}^{\circ}$ /s (Ext 60 and Ext 180, Flex 60, and Flex 180, respectively) based on the previous studies [29, 30, 31].

A no-load ergometer pedaling for 5 minutes preceded the test as a warm-up. All participants performed at least two practice repetitions to become familiar with the task, followed by six maximum repetitions. The measurements were taken in the following order: 180 ${}^{\circ}$ /s, 60 ${}^{\circ}$ /s for the non-operated leg, then 180 ${}^{\circ}$ /s, 60 ${}^{\circ}$ /s for the operated leg. The inter-velocity break was set for 1 minute, and the inter-side break was set for 5 minutes. Peak moment within the six repetitions was extracted and normalized by body weight (% body weight) and total muscle volume (% total muscle volume), respectively. High intra-rater reliability was previously reported with this method [32].

2.6 Statistical analyses

The histogram and Shapiro-Wilk normality tests were used to determine the normality of each variable’s distribution. Medians (quartile range) were calculated for variables that were not normally distributed, whereas means and standard deviations were calculated for normally distributed variables.

For the first hypothesis, bivariate correlation analysis was used to examine bivariate simple linear correlations (Pearson’s $r$ and Spearman’s $\rho$ ) between knee strength and body composition. Correlations were classified as very weak (correlation coefficient [ $r$ or $\rho$ ] $<$ 0.20), weak (0.20–0.39), moderate (0.40–0.59), strong (0.60–0.79), and very strong ( $>$ 0.80). For the second hypothesis, side-to-side differences between the operated and unoperated legs in knee strength, % body weight, and % total muscle volume were analyzed using paired $t$ -tests. The coefficient of variation (CV, %) was calculated for each variable. Effect size (Cohen’s d) was calculated using the paired $t$ -tests, and Cohen’s d was classified as small (0.20–0.50), medium (0.50–0.80), or large ( $>$ 0.8) effects [33]. The a priori $\alpha$ level was set at 0.05. Data were analyzed using SPSS version 21.0 (IBM Corp, Armonk, NY, USA).

3. Results

Overall, 17 patients (sex, six women and 11 men; age, median [interquartile range]: 21.0 [6.5] years; period since ACLR [mean $\pm$ standard deviation], 11.6 $\pm$ 2.3 months; pre-surgery modified Tegner activity scale: 7.9 $\pm$ 1.5) were included in the analysis. The body weight and total muscle volume were 69.4 $\pm$ 15.3 kg and 56.5 [24.0] kg, respectively. The descriptive data are presented in Table 1.

Table 1
Distributions of demographic variables among participants

Sex (female/male), $n$	6/11
Age, years*	21.0 (6.5)
Height, cm	167.9 $\pm$ 9.6
Body weight, kg	69.4 $\pm$ 15.3
Body mass index, kg/m ${}^{2}$	24.4 $\pm$ 3.8
Body fat, %*	16.1 (11.9)
Total muscle volume, kg*	56.5 (24.0)
Months from ACLR	11.6 $\pm$ 2.3
Pre-operated modified Tegner activity scale	7.9 $\pm$ 1.5
Graft type (HT/BTB), $n$	15/2
Meniscus repair (yes/no), $n$	13/4

*The values are presented as medians (interquartile ranges). ACLR, anterior cruciate ligament reconstruction; HT, hamstrings; BTB, bone-patellar tendon-bone. Ext and Flex 60/180 represent the isokinetic knee extension and flexion moment at 60 ${}^{\circ}$ /s or 180 ${}^{\circ}$ /s, respectively.

The correlation coefficients for the correlation between body composition and knee strength in the operated leg appear in Table 2. There were moderate-to-strong positive correlations between body weight and knee strength ( $r=$ 0.53–0.67, $P<$ 0.05), whereas there were strong-to-very strong positive correlations between the total muscle volume and knee strength ( $\rho=$ 0.80–0.87, $P<$ 0.01).

Table 2

Correlation between body composition and knee strength in the operated leg

	Operated leg
	Extension		Flexion
	60 ${}^{\circ}$ /s (Nm)	180 ${}^{\circ}$ /s (Nm)	60 ${}^{\circ}$ /s (Nm)	180 ${}^{\circ}$ /s (Nm)
Body weight	0.64 (0.23–0.86)†	0.62 (0.20–0.85)†	0.67 (0.28–0.87)†	0.53 (0.07–0.81)‡
Body mass index	0.41 ( $-$ 0.09–0.74)	0.36 ( $-$ 0.15–0.72)	0.42 ( $-$ 0.01–0.75)	0.23 ( $-$ 0.28–0.64)
Body fat*	$-$ 0.34 ( $-$ 0.74–0.10)	$-$ 0.47 ( $-$ 0.76–0.01)	$-$ 0.54 ( $-$ 0.81– $-$ 0.08)‡	$-$ 0.66 ( $-$ 0.87– $-$ 0.26)‡
Total muscle volume*	0.82 (0.56–0.93)†	0.81 (0.54–0.93)†	0.87 (0.67–0.95)†	0.80 (0.52–0.93)†

Correlation coefficients (95% confidence interval). ‡: $P<$ 0.05; †: $P<$ 0.01. *Spearman’s rho.

The results of side-to-side differences in each test appear in Table 3. Whether normalized by body weight or total muscle volume, knee strength values in unoperated leg were significantly higher than those in operated leg for all variables ( $P<$ 0.05), excluding Ext 60. For knee strength expressed as % body weight, all effect sizes were small, whereas, for knee strength expressed as % total muscle volume, the effect sizes for Ext 180 and Flex 180 were medium. All CV values were smaller for knee strength expressed as % total muscle volume than for those expressed as % body weight.

Table 3

The side-to-side differences in knee strength due to differences in normalization

	% body weight
	Operated leg		Unoperated leg
	Knee strength	CV	Knee strength	CV	$P$ -value	Effect size
Ext 60	239.7 $\pm$ 59.6	25%	254.8 $\pm$ 43.2	17%	0.140	0.29, small
Ext 180	163.0 $\pm$ 40.9	25%	177.3 $\pm$ 28.3	16%	0.012	0.41, small
Flex 60	116.5 $\pm$ 26.2	22%	124.9 $\pm$ 25.8	21%	0.018	0.32, small
Flex 180	91.9 $\pm$ 26.4	29%	102.1 $\pm$ 22.5	22%	$<$ 0.001	0.43, small
	% total muscle volume
	Operated leg		Unoperated leg
	Knee strength	CV	Knee strength	CV	$P$ -value	Effect size
Ext 60	316.3 $\pm$ 69.5	22%	336.6 $\pm$ 40.7	12%	0.134	0.36, small
Ext 180	215.0 $\pm$ 46.7	22%	234.8 $\pm$ 29.7	13%	0.011	0.51, medium
Flex 60	153.7 $\pm$ 27.0	18%	164.6 $\pm$ 25.5	16%	0.022	0.42, small
Flex 180	120.6 $\pm$ 28.0	23%	134.8 $\pm$ 24.2	18%	0.001	0.54, medium

The values are presented as means $\pm$ standard deviations. CV, coefficient of variation. Ext and Flex 60/180 represent the isokinetic knee extension and flexion moment at 60 ${}^{\circ}$ /s or 180 ${}^{\circ}$ /s, respectively. % total muscle volume and % body weight represents the knee strength normalized to total muscle volume and body weight, respectively.

4. Discussion

In this study, the correlation coefficient between total muscle volume ( $\rho=$ 0.80–0.87) and knee strength was greater than that of body weight and knee strength ( $r=$ 0.53–0.67). Thus, although knee strength is related to body size in post-ACLR patients, the relationship was greater for total muscle volume than for body weight. Physiologically, strength is proportional to the cross-sectional area or muscle volume [11, 12, 13]. Therefore, the study results can be explained theoretically.

Our results showed the effect sizes for side-to-side differences were larger for knee strength expressed as % total muscle volume than for knee strength expressed as % body weight. The effect size, Cohen’s d, is a standardized measure of the difference between the means and standard deviations for each group and indicates the degree of effect independent of the sample size. The study results indicated that knee strength % total muscle volume may be more sensitive than % body weight in detecting side-to-side differences in post-ACLR patients.

Although not statistically analyzable, the CV of knee strength % total muscle volume (12–23%) was smaller than that of knee strength % body weight (16–29%) in this study. The CV compares the degree of variability of data with different units, and a smaller CV indicates less variability. Thus, in this study, knee strength expressed as % total muscle volume showed less variability in distribution than knee strength expressed as % body weight. These results suggested that normalization by total muscle volume can more accurately correct for knee strength in post-ACLR patients.

Kim et al. [34] compared knee strength deficits (Ext and Flex at 60 and 180 ${}^{\circ}$ /s) in primary and revision post-ACLR patients and found no difference between the groups. Knee strength expressed as % body weight deficit ([unoperated leg-operated leg] * 100%) was used in this study. Lentz et al. [35] analyzed the relationship between the return to sports status and extensor strength (60 ${}^{\circ}$ /s) expressed as % body weight in 1-year post-ACLR patients. In this study [35], there was no significant association between the return-to-sports status and extensor strength on the operative side. Based on the results of this study, normalizing strength by physiologically relevant muscle volume rather than by body weight may lead to different results from those obtained in these studies.

4.1 Clinical implications

To accurately assess muscle volume, it is desirable to use DXA [22] or magnetic resonance imaging (MRI) [11, 13]. Although these methods are highly accurate for measurements, they are time-consuming, expensive, require expertise (should be performed by a trained technician), and are generally performed in a laboratory or hospital most times [25]. Therefore, a more simplified technique, such as BIA, is needed for therapists and trainers who cannot use DXA or MRI to measure body composition in athletes. Based on the current study’s results, BIA can be used to normalize knee strength in post-ACLR patients.

4.2 Limitations of this study

This study had several limitations. Patients who participated in sports for more than 8 months were included in the study, and it is unclear whether the method can be adapted to patients in earlier phases with greater muscle weakness. Although the calculated sample size was met, it was not sufficient to generalize the results. Post-ACLR patients are more likely to develop long-term residual muscle atrophy on the operative leg [36]. The method used in this study measures the total muscle volume and, therefore, it cannot capture this feature. As muscle atrophy was not measured in this study, this effect cannot be excluded. However, total muscle volume would be a better normalization of muscle strength than body weight, which includes the weight of fat and other body composition components in addition to the muscle volume. Finally, knee strength is affected by the neuromuscular system and fiber type [37] in addition to muscle volume; however, this study did not examine these factors.

5. Conclusions

In this study, both knee extension and flexion strength were more strongly correlated with total muscle volume than with body weight in post-ACLR patients. The side-to-side differences between knee strength expressed as % body weight and % total muscle volume had the same statistical trend; however, the effect size for strength expressed as % total muscle volume was larger than that expressed as % body weight. Knee strength expressed as % total muscle volume had a smaller CV and lower data variability than that expressed as % body weight. Hence, knee strength expressed as % total muscle volume may be more accurate in detecting side-to-side differences to assess knee strength than strength expressed as % body weight in post-ACLR patients.

Author contributions

CONCEPTION: Shunsuke Ohji.

PERFORMANCE OF WORK: Shunsuke Ohji, Junya Aizawa, Kenji Hirohata, Takehiro Ohmi and Sho Mitomo.

INTERPRETATION OR ANALYSIS OF DATA: Shunsuke Ohji, Junya Aizawa, Kenji Hirohata, Takehiro Ohmi and Sho Mitomo.

PREPARATION OF THE MANUSCRIPT: Shunsuke Ohji, Junya Aizawa, Kenji Hirohata, Takehiro Ohmi and Sho Mitomo.

REVISION FOR IMPORTANT INTELLECTUAL CONTENT: Junya Aizawa, Hideyuki Koga and Kazuyoshi Yagishita.

SUPERVISION: Hideyuki Koga and Kazuyoshi Yagishita.

Ethical considerations

The study was reviewed and approved by the review board of Tokyo Medical and Dental University (approval number: M2019-158, approval date: October 8th, 2019). All participants provided a written informed consent prior to participation.

Funding

This work was supported by the Japanese Physical Therapy Association (JPTA1-B17).

Footnotes

Acknowledgments

We would like to thank Editage (www.editage.com) for English language editing.

Conflict of interest

The authors have no conflicts of interest to report.

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