Skeletal muscle tissue composition ratio in patients with hip fracture: Comparison of fractured side and non-fractured side

Abstract

BACKGROUND:

The extent of asymmetry in the muscle tissue composition ratios with hip fractures has not been clarified.

OBJECTIVE:

To determine whether there is a difference in the muscle tissue composition ratios between the fractured and non-fractured sides of the trunk and thighs immediate measurement.

METHODS:

Forty-four patients (84.6 $\pm$ 7.0 years) were included. Computed tomography images were used for measurements. The muscle tissue composition ratio was measured using muscle cross-sectional area (CSA) and attenuation coefficient (Hounsfield units; HU). Defined each HU attenuation range as follows: low-density muscle (LDM), low-quality muscle tissue with fat infiltration, normal-density muscle (NDM), muscle contractor tissue, and intramuscular adipose tissue (IMAT), fat infiltration tissue. The CSA of each muscle tissue was expressed as a percentage: %LDM, %NDM, and %IMAT. A paired $t$ -test was performed for comparison.

RESULTS:

The %LDM on the fractured side was higher in the thigh and erector spinae. The %NDM on the fractured side was lower in the thigh. There was no significant difference in the %IMAT for all muscles.

CONCLUSION:

The thigh on the fractured side showed asymmetry with low %NDM and high %LDM. This characteristic captures a characteristic of muscle tissue that may have importance in hip fracture etiology.

Keywords

Hip fractures muscle tissue adipose tissue aged computed tomography

1. Introduction

Hip fractures in older adults are directly linked to life expectancy. Previous studies reported mortality rates of 10.1% and 14.1% within one year of surgery [1, 2]. Hip fracture in older adults was caused by a fall [3, 4], and lower extremity muscle strength and imbalance in muscle mass were associated with falls [5, 6]. The association between falls and lower limb explosive power asymmetry in the elderly was reported to be 24% weaker than in non-fallers [7]. In addition, the muscle mass of the trunk was also considered to be a factor influencing dynamic posture related to standing balance [8]. Thus, to prevent falls in older adults, healthcare providers should focus on improving muscle strength, mass, and imbalance of the trunk and lower limbs.

In the past decade, research on asymmetry of fat infiltration in skeletal muscle has focused on factors related to falls. Previous studies indicated that there was asymmetry in patients with hip fractures, and that the proportion of fat infiltration in the gluteus medius and gluteus minimus muscles on the fractured side was higher than that on the non-fractured side [9]. This asymmetry was observed even after the surgery. It was reported that the adipose tissue-to-muscle ratio in the gluteus medius and the fat area of the quadriceps muscle was higher on the fractured side than on the non-fractured side [10, 11]. Therefore, it important to compare the muscle quality on the fractured and non-fractured sides.

The muscle quality was assessed using intramuscular fat (IMAT). IMAT was reported to increase with age [12] and was associated with a decrease in muscle strength, motor function, and walking ability in older adults [13, 14]. Furthermore, older inpatients with high levels of IMAT in the quadriceps muscle at the time of hospitalization showed poor improvement in activities of daily living at discharge [15]. In a previous study [11], IMAT of the thigh was higher on the fractured side than on the non-fractured side after a hip fracture. However, in the same study, IMAT in the thigh was measured two months after surgery; hence, the effects of postoperative disuse syndrome cannot be ruled out. To determine whether IMAT in the thigh is associated with hip fractures due to falls, it is important to evaluate the muscle immediately after injury. Understanding the nature of a patient’s muscle composition immediately after a hip fracture may help provide specific recommendations for the prevention of falls and the effectiveness of exercise programs for patients with hip fracture.

Computed tomography (CT) is one of the gold standards for measuring skeletal muscle mass and IMAT. Each tissue in the CT image has a CT value (Hounsfield unit: HU) determined by X-ray absorption. CT images can show not only IMAT and muscle tissue but also low-density muscle (LDM) with fat infiltration and fat-free normal density muscle (NDM) [16, 17, 18]. It has been reported that LDM with fat infiltration is positively correlated with IMAT ( $r=$ 0.46, $P=$ 0.007) [19]. LDM was reported to increase after the age of 60, when the decline in thigh CSA due to aging was less, offsetting the decrease in thigh CSA [20]. LDM with fat infiltration can adversely affect motor function. The CT values in these CT images can be used to evaluate more detailed muscle tissue changes.

The purpose of this study was to quantitatively measure muscle mass and tissue in the trunk and thigh using CT in older adults immediately after hip fracture and to confirm asymmetry between the fractured and non-fracture sides. It has been hypothesized that muscle mass and muscle tissue asymmetry in the trunk and thighs are observed immediately after injury in patients with hip fracture due to falls.

2. Methods

We designed an observational study to investigate professionally whether asymmetry is observed in the trunk and thigh muscle tissue composition ratio of elderly patients of hip fracture, by immediate measuring the muscle tissue immediately after hip fracture.

2.1 Ethical considerations

The study was conducted on patients admitted in a hospital in Maniwa City between April 2015 and December 2017. The study was approved by the Kaneda Hospital Ethics Review Committee (approval number: 0403). The patients received a verbal explanation of the study and provided written informed consent prior to participation.

2.2 Study participants

The inclusion criteria were as follows (Fig. 1): 1) patients aged $\geqslant$ 75 years; 2) patient’s level of physical activity had some disability, but was almost completely independent in everyday activities, and could go outside unassisted, or was mostly independent in daily living activities at home, but cannot go out without assistance (with or without a cane or other assistive device); 3) An orthopedic surgeon and a diagnostic radiologist diagnosed with intertrochanteric fracture or a femoral neck fracture and confirmed that it was a first fracture; 4) those with fracture caused by falls, defined as a falls ingress on the ground or a low surface against intention; and 5) underwent a CT scan within 3 days of injury, and CT images of the trunk and both thighs were confirmed. The exclusion criteria were as follows: 1) patients who had fractures other than intertrochanteric fracture or femoral neck fracture; 2) history of neuromuscular, or pelvic or lower extremity fractures due to falls or trauma; 3) joint replacement surgery anywhere in the hip, knee, or ankle; 4) patient’s level of physical activity was to stay in bed even during the day, and used a wheelchair mainly for mobility; 5) dementia; 6) patients who had a history of falls more than 3 days prior to diagnosis by CT images; and 7) When records covered by this study are missing or have missing data.

Figure 1.

Target selection criteria.

2.3 Measurements of sociodemographic factors

Patients’ age, height, weight, body mass index (BMI), albumin (ALB), and geriatric nutritional risk index (GNRI) at the time of hospitalization were measured and reported from their electronic medical records. GNRI has been reported as a predictive factor of the life expectancy of older adults and a concise and accurate nutritional assessment method [21, 22]. The GNRI was calculated as follows: GNRI $=$ [14.89 $\times$ ALB (g/dL)] $+$ [41.7 (weight/ideal weight in kg)]. The authors defined four grades of nutrition-related risk: major risk (GNRI $<$ 82), moderate risk (GNRI 82–92), low risk (GNRI 92–98), and no risk (GNRI $>$ 98) [21].

2.4 Measurement of skeletal muscle CSA and muscle tissue on CT imaging

CT images were 120 kVp, 280 mA, 512 $\times$ 512 matrix and a field of view (FOV) adjusted to capture the entire trunk and both thigh of legs. Each patient was supine. They underwent a continuous CT scan from upper part of abdomen to the patella. A single 10 mm thick CT image each was obtained in trunk muscle (middle of 4th and 5th lumbar vertebrae or upper border of 5th lumbar vertebrae) and thigh muscle (the midline area between the greater trochanter and the lateral femoral epicondyle) were selected for this analysis. It was hypothesized that fractures could cause bleeding and hematomas in the surrounding muscles and other tissues, which could affect CT values. In this study, we excluded the hip, which could affect muscle tissues measures. Thigh and trunk muscle cross-sectional area (CSA) and muscle composition was quantified using ImageJ (1.48v). ImageJ supports many file formats, including Digital Imaging and Communication in Medicine (DICOM). Long et al. [18] reported the validity of the measured skeletal muscle CSA using ImageJ and muscle composition analysis of the thigh using CT. This study was conducted according to the method described by Long et al. [18]. Measurements were taken by a trained physical therapist. Muscle composition were expressed as a CSA of tissue (cm ${}^{2}$ ) and using Hounsfield units (HU) for 35 to 100 HU; normal-density muscle (NDM), 0–34 HU; low-density muscle (LDM), and $-$ 150 to $-$ 30 HU; IMAT (Fig. 2) [18, 23, 24, 25]. %NDM, %LDM and %IMAT were quantified for the respective muscle’s size by calculating percentage of each measure relative in the muscle CSA. The CSA of the skeletal muscle tissues of the trunk and thighs were used as a measure of muscle quality. LDM, a low-quality muscle tissue with fat infiltration, has a higher lipid concentration than NDM [19]. IMAT is the fat infiltration in muscle tissue. The target trunk muscles included quadratus lumborum, erector spinae, multifidus, psoas major, oblique (transversus abdominis, internal oblique, and external oblique) and rectus abdominis. The target thigh muscles were divided into extensor muscle (rectus femoris, lateral vastus, medial vastus, and intermediate vastus) and flexor muscle (biceps femoris, semitendinosus, and semimembranosus).

Table 1
Baseline demographics characteristics of patients with hip fracture in study ( $n=$ 44)

Age (years)	84.6 $\pm$ 7.0
Heigh (cm)	148.5 $\pm$ 7.7
Body weight (kg)	45.7 $\pm$ 8.9
BMI (kg/m ${}^{2}$ )	20.7 $\pm$ 3.7
ALB (g/dl)	3.5 $\pm$ 0.8
GNRI	91.5 $\pm$ 13.7
	Major risk $=$ 7, moderate risk $=$ 16, low risk $=$ 11, no risk $=$ 10
Types of fracture	Cervical fracture $=$ 25, Transduction fracture $=$ 19
The level of physical	Some disability, but was almost completely independent in everyday activities, and could go outside unassisted $=$ 25
activity	Mostly independent in daily living activities at home, but cannot go out. without assistance $=$ 19

BMI; body mass index. GNRI; Geriatric Nutritional Risk Index $=$ [14.8 9 $\times$ ALB (g/dL)] $+$ [41.7 $\times$ (weight/height(m) ${}^{2}$ $\times$ 22)]. risk: major risk (GNRI $<$ 82), moderate risk (GNRI: 82 to $<$ 92), low risk (GNRI: 92 to $<$ 98), and no risk (GNRI: $>$ 98).

Figure 2.

Graphical representation of various Hounsfield Unit ranges used for determining intramuscular adipose tissue and skeletal muscle in the quadriceps. Visual output from ImageJ when assessing intra-muscular adipose tissue, low density muscle, and normal density muscle.

2.5 Statistical analyses

Descriptive data for the fractured and non-fractured sides were presented. The CSA of trunk and thighs or %LDM, %NDM, and %IMAT measured on the fractured and nonfractured sides of 44 patients with hip fracture were compared. After performing the Shapiro-Wilk test to check the normality of the data, a paired $t$ -test as a parametric test or the Mann-Whitney $U$ test as a non-parametric test was performed. All statistical analyses were performed using Easy R (ver1.24). The level of significance was set at $P<$ 0.05.

3. Results

Of the 293 patients admitted to the orthopedic department during the period, 124 patients had hip fractures. Of these, 44 patients (9 males, 35 females) were indicated for this study (Fig. 1). The mean age of included patients was 84.6 $\pm$ 7.0 years. The baseline demographic characteristics of patients with hip fracture were shown in Table 1.

Table 2
Comparison results between the fracture side and non-fracture side for each muscle CSA and muscle tissue composition ratio ( $n=$ 44)

		Fracture side		Non-fracture side		Difference		$P$ -value
Quadratus lumborum	CSA (cm ${}^{2}$ )	3.6	$\pm$ 1.4	3.4	$\pm$ 1.3	0.2	$\pm$ 1.4	0.449
	%LDM (%)	30.4	$\pm$ 13.1	31.4	$\pm$ 12.3	$-$ 1.0	$\pm$ 8.0	0.427
	%NDM (%)	38.9	$\pm$ 16.3	38.6	$\pm$ 17.5	0.3	$\pm$ 14.8	0.878
	%IMAT (%)	7.2	$\pm$ 6.9	6.6	$\pm$ 8.4	0.6	$\pm$ 10.4	0.697
Erecter spinae	CSA (cm ${}^{2}$ )	8.5	$\pm$ 2.7	8.3	$\pm$ 2.5	0.2	$\pm$ 2.0	0.548
	%LDM (%)	30.6	$\pm$ 11.4	28.1	$\pm$ 10.4	2.5	$\pm$ 8.0	0.044 ${}^{*}$
	%NDM (%)	33.9	$\pm$ 17.6	36.8	$\pm$ 20.0	$-$ 2.9	$\pm$ 11.9	0.112
	%IMAT (%)	7.2	$\pm$ 7.6	7.8	$\pm$ 6.7	$-$ 0.6	$\pm$ 5.2	0.414
Multifidus	CSA (cm ${}^{2}$ )	3.9	$\pm$ 1.5	4.1	$\pm$ 1.7	$-$ 0.2	$\pm$ 1.4	0.480
	%LDM (%)	28.0	$\pm$ 11.9	27.1	$\pm$ 12.2	0.9	$\pm$ 7.2	0.418
	%NDM (%)	34.1	$\pm$ 19.0	35.4	$\pm$ 18.1	$-$ 1.3	$\pm$ 16.9	0.609
	%IMAT (%)	10.8	$\pm$ 11.2	9.2	$\pm$ 8.7	1.6	$\pm$ 9.6	0.279
Psoas major	CSA (cm ${}^{2}$ )	6.4	$\pm$ 2.1	7.0	$\pm$ 2.8	$-$ 0.5	$\pm$ 1.6	0.030 ${}^{*}$
	%LDM (%)	24.5	$\pm$ 7.7	25.3	$\pm$ 9.8	$-$ 0.7	$\pm$ 7.8	0.531
	%NDM (%)	57.9	$\pm$ 13.7	57.7	$\pm$ 13.6	0.2	$\pm$ 13.4	0.940
	%IMAT (%)	3.8	$\pm$ 3.1	3.3	$\pm$ 2.8	0.5	$\pm$ 2.7	0.213
Oblique muscles	CSA (cm ${}^{2}$ )	13.8	$\pm$ 4.3	13.4	$\pm$ 6.6	0.3	$\pm$ 5.6	0.699
	%LDM (%)	32.0	$\pm$ 12.9	31.8	$\pm$ 11.8	0.2	$\pm$ 8.4	0.867
	%NDM (%)	47.2	$\pm$ 18.2	45.2	$\pm$ 18.1	2.0	$\pm$ 13.4	0.318
	%IMAT (%)	3.7	$\pm$ 3.6	4.4	$\pm$ 4.2	$-$ 0.7	$\pm$ 3.2	0.173
Rectus abdominis	CSA (cm ${}^{2}$ )	2.6	$\pm$ 1.2	2.7	$\pm$ 1.2	$-$ 0.2	$\pm$ 1.0	0.314
	%LDM (%)	30.0	$\pm$ 18.5	29.3	$\pm$ 14.1	0.7	$\pm$ 12.0	0.687
	%NDM (%)	35.4	$\pm$ 23.8	39.2	$\pm$ 35.6	$-$ 3.9	$\pm$ 35.8	0.479
	%IMAT (%)	14.3	$\pm$ 22.6	13.7	$\pm$ 24.9	0.6	$\pm$ 30.2	0.903
Knee extensor muscles	CSA (cm ${}^{2}$ )	28.6	$\pm$ 7.8	33.2	$\pm$ 10.6	$-$ 4.6	$\pm$ 10.7	0.006 ${}^{*}$
	%LDM (%)	20.2	$\pm$ 8.1	17.8	$\pm$ 8.9	2.4	$\pm$ 6.6	0.020 ${}^{*}$
	%NDM (%)	64.2	$\pm$ 15.4	67.9	$\pm$ 17.6	$-$ 3.7	$\pm$ 9.0	0.009 ${}^{*}$
	%IMAT (%)	2.0	$\pm$ 2.1	1.9	$\pm$ 2.1	0.1	$\pm$ 0.2	0.663
Knee flexor muscles	CSA (cm ${}^{2}$ )	39.5	$\pm$ 12.8	45.0	$\pm$ 21.9	$-$ 5.5	$\pm$ 15.9	0.026 ${}^{*}$
	%LDM (%)	22.4	$\pm$ 7.1	21.5	$\pm$ 8.3	0.9	$\pm$ 6.8	0.027 ${}^{*}$
	%NDM (%)	57.3	$\pm$ 16.1	60.2	$\pm$ 17.5	$-$ 3.0	$\pm$ 8.9	0.032 ${}^{*}$
	%IMAT (%)	3.7	$\pm$ 3.5	3.2	$\pm$ 3.3	0.5	$\pm$ 3.0	0.062

%LDM, %NDM, and %IMAT are the ratios of the muscle tissues in each muscle CSA (LDM, NDM, and IMAT, respectively). CSA, cross-sectional area; LDM, low-density muscle; NDM, normal density muscle; IMAT, intramuscular adipose tissue. ${}^{*}P<$ 0.05, compared between the fractured and non-fractured sides.

The comparison results of the muscle measurements on the fractured and non-fractured sides of the 44 patients with hip fracture are shown in Table 2. The CSA was lower in the psoas major (asymmetrical difference was $-$ 0.5 cm), extensor muscle group ( $-$ 4.6 cm), and flexor muscle group ( $-$ 5.5 cm) on the fractured side compared to the non-fractured side. The %LDM was higher in the erector spinae (2.5%), extensor muscle group (2.4%), and flexor muscle group (0.9 cm) on the fractured side compared to the non-fractured side.

The %NDM was lower in the extensor muscle group ( $-$ 3.7%) and flexor muscle group ( $-$ 3.0%) on the fractured side than on the non-fractured side. There was no significant difference in %IMAT in all target muscle groups ( $-$ 0.7%–1.6%).

4. Discussion

In this study, we immediately measured the muscle tissue of the trunk and thigh immediately after hip fracture injury in elderly patients and compared the muscle mass and muscle tissue composition ratios on the fracture and non-fracture sides to confirm the presence of asymmetry. Asymmetry was observed in the thighs, which had a low CSA value, high %LDM, and low %NDM on the fractured side compared to the non-fractured side. The erector spinae were asymmetric with a high %LDM on the fractured side. These were new findings in the qualitative assessment of patients with hip fractures.

In this study, asymmetry was observed with a high %LDM and a low %NDM on the fractured thigh compared with the non-fractured thigh. Patients with hip fractures had lower muscle mass than outpatients who did not have hip fractures [26]. The muscle mass was lower and IMAT was higher in the fractured thigh than in the non-fractured thigh [9, 10, 11]. Muscle tissue can be divided into LDM, which is a low-quality muscle tissue with fat infiltration, and NDM, which is essential for muscle contraction tissue [19]. However, asymmetry has not been confirmed. Therefore, this study investigated %IMAT, %LDM, and %NDM as measures of asymmetry in muscle tissue composition ratio in CSA. Compared to the non-fractured side, on the fractured side, a low CSA and asymmetry with high %LDM and low %NDM values in CSA were observed.

The muscle tissue composition ratio on the fractured side, which was recognized to be asymmetric in this study, was high for the non-contraction tissue. LDM is considered low quality muscle tissue containing adipose tissue [19]. The %IMAT in this study was not asymmetric, but the %IMAT values were 2–4% in the thigh and about 3–14% in the trunk muscles. The proportion of non-contractile tissue was higher in the thighs on the fractured side than in the non-fractured side when %LDM and %IMAT were combined. In the erecter spinae muscle where asymmetry was observed only in %LDM, the fractured side was 37.8% (%LDM, 30.6%, %IMAT, 7.2%), compared to the non-fractured side, 35.9% (%LDM 28.1%, %IMAT 7.8%), suggesting that the proportion of non-contraction tissue was high. This was considered an important result that could not be determined by evaluation of only IMAT and muscle tissue alone. Therefore, the results suggested that asymmetry occurred when the proportion of essential for muscle contraction on the fractured side was low.

The asymmetry in muscle tissue composition ratios observed in the thighs was not observed in the trunk muscles, except for the %LDM of erector spinae. Age-related muscle atrophy was greater in type II fibers than in type I fibers. Trunk muscles were found to have more type I fibers than limb skeletal muscles, but the degree of muscle atrophy varies muscles [27]. CT image of muscle tissue CT values was also reported to differ between muscles, with a greater decrease in CT values in the erector spinae [28]. The asymmetry in the tissue composition ratio of the erector spinae muscles in this study may have influenced the decrease in postural stability. However, it was considered necessary to be careful in interpretation due to the possibility of a type I error. In other trunk muscles, asymmetry was not observed, presumably due to age-related decline in physical activity involving trunk movements such as rotation [27]. The thigh muscles were predominantly type II fibers and were the dominant muscles during physical activity such as walking. It was susceptible to the effects of decreased physical activity with aging. It was possible that the asymmetry in this study was caused by less muscle use in the thigh on the fractured side compared to the non-fractured side. Therefore, the asymmetry in muscle tissue composition ratios could have been influenced by aging-related type fiber characteristics and decreased physical activity.

The asymmetry of the muscle tissue composition ratio in this study might further increase after surgery, thereby compromising walking ability and activities of daily living and increase the risk of falls. After surgery for hip fracture, inflammation, rest, and unloading have been reported to cause low muscle mass, high IMAT, and asymmetry on the fractured side [11]. In contrast, muscle-strengthening exercises for muscle tissue in older adults with reduced motor function were reported to increase the NDM [19] and decrease the IMAT [29]. Muscle-strengthening exercises are a valuable key for improving muscle tissue composition. Muscle training was thought to have the potential to inhibit asymmetric expansion of muscle tissue composition ratio in the lower limbs. The results of this study suggest that it is important to detailed measure the muscle and muscle tissue of each side separately in order to characterize the relationship between ability and function. It was then thought that clarifying asymmetries would help in beneficial prevention strategies to reduce the risk of fractures from falls and could be advised to the elderly as a postoperative exercise program initiative.

This study has four limitations. First, the investigations were done in a single facility, and the sample size was relatively small. Therefore, further research with a larger sample size is warranted to confirm the results of the current study. Second, the muscle tissue composition ratio was measured on the fractured and non-fracture sides and only compared. It was difficult to assess motor function immediately after the injury. Third, Asymmetry was observed in the muscle tissue composition ratio in the thigh, but it is unclear to what extent asymmetry leads to hip fractures due to falls. In the future, it would be necessary to examine the extent to which asymmetry in each muscle tissue composition ratio is associated with hip fracture due to falls. Therefore, it was deemed necessary to compare the results with those of older adults who had no history of falls. Fourth, falls and hip fractures were multifactorial processes. For example, pharmacological treatment were factors in the falls [30]. Other factors must also be considered and discussed. Future studies are needed to determine which factors, including asymmetry in muscle tissue composition ratios, are most influential.

5. Conclusions

Asymmetry was observed in patients with hip fractures due to falls, with low muscle mass as well as low %NDM, which is muscle contractile tissue, and high %LDM, which is a low-quality muscle tissue with fat infiltration, in the thigh on the fractured side. This asymmetry could be even greater after surgery. This asymmetry has direct clinical implications for designing exercises to improve muscle quality and function related to physical function. Future studies should clarify the extent to which asymmetry in each muscle tissue composition ratio is associated with hip fractures due to falls.

Funding

This study did not receive funding.

Author contributions

Conceptualization: TF; Data curation: TF, ST; Formal analysis: TF, ST; Investigation: TF; Methodology: TF, ST; Supervision: ST; Writing-original draft: TF; Writing-review & editing: TF, ST. All authors read and approved the final version of the manuscript.

Footnotes

Acknowledgments

The authors thank the patients who participated in the study.

Conflict of interest

The authors declare that they have no conflict of interest.

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Skeletal muscle tissue composition ratio in patients with hip fracture: Comparison of fractured side and non-fractured side

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSION:

Keywords

1. Introduction

2. Methods

2.1 Ethical considerations

2.2 Study participants

2.4 Measurement of skeletal muscle CSA and muscle tissue on CT imaging

Table 1 Baseline demographics characteristics of patients with hip fracture in study ( n = 44)

3. Results

Table 2 Comparison results between the fracture side and non-fracture side for each muscle CSA and muscle tissue composition ratio ( n = 44)

5. Conclusions

Funding

Author contributions

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Baseline demographics characteristics of patients with hip fracture in study ( $n=$ 44)

Table 2
Comparison results between the fracture side and non-fracture side for each muscle CSA and muscle tissue composition ratio ( $n=$ 44)