antioxidants
Article
Associations between Coenzyme Q10 Status,
Oxidative Stress, and Muscle Strength and Endurance
in Patients with Osteoarthritis
Po-Sheng Chang 1,2 , Chi-Hua Yen 3,4 , Yu-Yun Huang 1 , Ching-Ju Chiu 1 and Ping-Ting Lin 1,5, *
1
2
3
4
5
*
Department of Nutrition, Chung Shan Medical University, Taichung 402367, Taiwan;
s0746002@gm.csmu.edu.tw (P.-S.C.); s0745011@gm.csmu.edu.tw (Y.-Y.H.);
s0745018@gm.csmu.edu.tw (C.-J.C.)
Graduate Program in Nutrition, Chung Shan Medical University, Taichung 402367, Taiwan
School of Medicine, Chung Shan Medical University, Taichung 402367, Taiwan; cshy352@csh.org.tw
Department of Family and Community Medicine, Chung Shan Medical University Hospital,
Taichung 402367, Taiwan
Department of Nutrition, Chung Shan Medical University Hospital, Taichung 402367, Taiwan
Correspondence: apt810@csmu.edu.tw; Tel.: +886-4-24730022 (ext. 12187); Fax: +886-4-2324-8175
Received: 11 November 2020; Accepted: 12 December 2020; Published: 14 December 2020
Abstract: Osteoarthritis (OA) causes oxidative stress. Coenzyme Q10 is an antioxidant that participates
in energy production in the human body. The purpose of this study was to investigate the relationships
among coenzyme Q10 status, oxidative stress, antioxidant capacity, and muscle function in patients
with OA. This case-control study recruited 100 patients with OA and 100 without OA. The coenzyme
Q10 status, oxidative stress, antioxidant capacity, muscle mass (by dual-energy X-ray absorptiometry),
muscle strength (hand-grip and leg-back strength), and muscle endurance (dumbbell curls, gait speed,
chair-stand test, and short physical performance battery) were measured. The results showed that both
OA and elderly subjects had a low coenzyme Q10 status (<0.5 µM). Oxidative stress was significantly
negatively correlated with muscle function (protein carbonyl, p < 0.05). Coenzyme Q10 level was
positively associated with antioxidant capacity, muscle mass, muscle strength and muscle endurance
in patients with OA (p < 0.05). Since OA is an age-related disease, coenzyme Q10 may be consumed
by oxidative stress and thereby affect muscle function. Raising coenzyme Q10 in patients with OA
could be suggested, which may benefit their antioxidant capacity and muscle function.
Keywords: coenzyme Q10; oxidative stress; muscle mass; muscle function; osteoarthritis; aging
1. Introduction
Osteoarthritis (OA) is an age-related chronic disease that leads to joint pain, stiffness, and physical
impairment [1]. Genetic susceptibility, obesity, and aging are risk factors for OA [2]. In addition to
risk factors (obesity or aging), the progression of OA is related to the accumulation of reactive oxygen
species (ROS), which may regulate the secretion of cytokines and apoptosis to affect intracellular
metabolism in chondrocytes [3]. The excessive production of ROS in patients with OA may cause
cartilage matrix degradation and exacerbate the OA process [4,5]. The increased oxidative stress
molecules may attack proteins and affect skeletal muscle function in elderly individuals [6,7], and it may
increase the risk of sarcopenia in patients with OA [8]. Some studies have shown that the antioxidant
status is decreased in patients with OA [5,9]. Antioxidant status or antioxidant capacity can protect
cells from oxidative stress damage caused by diseases. However, the association of antioxidant status
and muscle function is not clear, especially for patients with OA who have a high risk of limited
Antioxidants 2020, 9, 1275; doi:10.3390/antiox9121275
www.mdpi.com/journal/antioxidants
Antioxidants 2020, 9, 1275
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mobility. Therefore, we investigated the relationships between oxidative stress, antioxidant capacity,
muscle mass and muscle strength in patients with OA in this study.
Coenzyme Q10 is an antioxidant nutrient that can act as a free radical scavenger [10].
Coenzyme Q10 also participates in adenosine triphosphate synthesis in the mitochondrial respiratory
chain [11], which is important for organs with high energy demands, such as skeletal muscle [12].
Aging decreased cellular bioenergy capacity and may result in a depletion of coenzyme Q10 levels [13].
It is well known that chronic diseases such as cardiac diseases, diabetes, and neurodegenerative
diseases may influence the coenzyme Q10 status [14–17]. To date, no clinical study has investigated the
level of coenzyme Q10 in patients with OA. The aim of the present study was to examine coenzyme Q10
status, oxidative stress, antioxidant capacity, and their correlations with muscle function in patients
with OA.
2. Materials and Methods
2.1. Participants and Study Design
The present study was designed as a case-control study. We recruited patients with OA and
subjects without OA as the control group. The included participants were ≥40 years old and received
standing anterior-to-posterior knee X-ray examination. The diagnosis of OA was made according to
the Kellgren and Lawrence (K/L) grade [18]. Participants whose K/L grade was ≥2 were OA, and those
whose K/L grade was 0 or 1 were without OA (Non-OA group). The exclusion criteria for both OA and
Non-OA groups were as follows: (1) patients with rheumatoid arthritis; (2) the use of glucosamine
sulfate, a nonsteroidal anti-inflammatory drug, or hyaluronic acid injection therapy in the past month;
(3) the use of other antioxidants or coenzyme Q10 supplements, statins, or warfarin medications;
and (4) knee replacement surgery. This study was approved by the Institutional Review Board of
Chung Shan Medical University Hospital, Taiwan (CSMUH No: CS2−17095). Each subject provided
written informed consent to participate in the study.
2.2. Data Collection and Biochemical Analysis
The characteristics of the subjects were recorded from a questionnaire containing age and gender.
Height and weight were measured, and body mass index (BMI) was calculated. Muscle mass,
including whole and trunk muscle mass, whole skeletal muscle mass index (WSMI), and appendicular
skeletal muscle mass index (ASMI), was measured by dual-energy X-ray absorptiometry (Hologic,
ASY−05119, Marlborough, MA, USA). Fasting venous blood specimens were collected in vacutainers
with K2-EDTA anticoagulant (Becton Dickinson, Franklin Lakes, NJ, USA) or without anticoagulant.
Plasma, serum, and red blood cell (RBC) samples were prepared after centrifugation at 4 ◦ C and
3000 rpm for 15 min. The biochemical data, including albumin, blood urea nitrogen (BUN), creatinine,
glutamic oxaloacetic transaminase (GOT), glutamic pyruvic transaminase (GPT), high-sensitivity
C-reactive protein (hs-CRP), and total cholesterol (TC) were measured by an automated chemistry
analyzer (Beckman Coulter, DxC 800, Brea, CA, USA; Hitachi 7600−110, Tokyo, Japan).
2.3. Oxidative Stress and Antioxidant Capacity Measurements
Malondialdehyde (MDA) in plasma was analyzed by the thiobarbituric acid reactive substance
method [19]. Protein carbonyl groups in plasma were measured by condensation reaction with
2,4-dinitrophenylhydrazine [20]. The protein content in plasma was analyzed with a bicinchoninic
acid protein assay reagent kit (Thermo Scientific, Rockford, IL, USA). Protein carbonyl is expressed
as nmol/mg protein. Total antioxidant capacity (TAC) in serum and RBC was measured by a Trolox
equivalent antioxidant capacity assay, and the wavelength was set at 730 nm [21].
Antioxidants 2020, 9, 1275
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2.4. Coenzyme Q10 Status Measurement
The level of coenzyme Q10 was measured by high-performance liquid chromatography (HPLC)
with an ultraviolet detector [22]. The protein in plasma was precipitated by propanol after centrifugation,
and methanol was added to the supernatant at the same ratio. After mixing, the liquid was filtered for
analysis by HPLC. Mixed methanol and ethanol were the mobile phase. The analysis column was
a LiChroCART® RP-18 (Merck, Germany), and the wavelength of the ultraviolet detector was set at
275 nm.
2.5. Muscle Strength and Endurance Assessments
The upper and lower limb muscle strength was evaluated as the handgrip and leg-back strength,
respectively. Handgrip was assessed by a handgrip dynamometer (TAKEI, TKK-5401, Niigata, Japan).
The subjects were asked to stand with the dominant hand hanging down and then grip the apparatus
as tightly as they could. Leg-back strength was assessed by a back dynamometer (TAKEI, TKK-5402,
Niigata, Japan). The subjects were asked to stand straight on the platform of the dynamometer and
grasp a bar that was attached to a chain and dynamometer and then lift up with maximal effort.
Both the handgrip and leg-back strength tests were performed in duplicated for one minute, and the
best value was recorded. For the muscle endurance tests, upper limb endurance was assessed by
dumbbell curls of the left hand. Subjects were instructed to flex and extend the elbow to lift a 5 lb
dumbbell for 30 s. Lower limb endurance was assessed by the chair-stand test. We recorded the
number of times in 30 s that the subjects could stand from a chair and then return to sit in it. The gait
speed was assessed by the 6-min walk test. Subjects were asked to walk on a flat road for 6 min to
record the distance that the subjects walked. Furthermore, we used the short physical performance
battery (SPPB) to assess the physical performance of these subjects, which included a balance test,
gait speed test, and chair-stand test [23,24]. Higher SPPB scores mean that subjects have better physical
performance. Sarcopenia was defined according to the Asian Working Group for Sarcopenia [23],
which was assessed by appendicular skeletal muscle mass index and muscle strength and endurance.
2.6. Statistical Analysis
SigmaPlot software (version 12.0, Systat, San Jose, CA, USA) was used for all statistical
tests in the present study. The normality of each distribution was analyzed by the Shapiro–Wilk
test. The mean ± standard deviation (median) or percentages are shown for descriptive statistics.
Student’s t-Test or the Mann–Whitney rank sum test was used to understand the differences in
demographic data, coenzyme Q10 status, oxidative stress, and antioxidant capacity between the
two groups. The differences in categorical variables were examined by using the Chi-square test or
Fisher’s exact test. Pearson’s correlation coefficient or Spearman’s rank order correlation coefficient was
calculated to examine the correlations between coenzyme Q10 status and oxidative stress, antioxidant
capacity, muscle mass, muscle strength, and muscle endurance. The results were considered statistically
significant at p-value < 0.05.
3. Results
3.1. Subjects’ Characteristics
Table 2 shows the characteristics of the subjects. Patients with OA had significantly higher values
of age and BUN and lower GPT than the Non-OA group (p < 0.01). Male OA patients had significantly
lower muscle strength and endurance than Non-OA (p < 0.05); female OA patients showed significantly
lower values of gait speed (p < 0.01) and SPPB scores (p = 0.01). Because the patients with OA had
a significantly higher age than Non-OA patients, we stratified the subjects by age: ≥65 years as the
elderly group and 40−64 years as the middle-aged group. Elderly patients with OA had significantly
higher values of BMI (p = 0.02) and significantly lower levels of GOT (p < 0.01) and GPT (p = 0.02)
than the Non-OA group. Both OA and Non-OA subjects in the elderly group had significantly lower
Antioxidants 2020, 9, 1275
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level of albumin (p < 0.01), muscle mass (p ≤ 0.01), muscle strength (p < 0.05), and muscle endurance
(p < 0.05) than those in the middle-aged group. In addition, elderly OA patients had a significantly
higher level of hs-CRP than the middle-aged group (p = 0.04). Regarding the level of muscle mass,
muscle strength, and muscle endurance stratified by age, patients with OA in the elderly (p = 0.07) and
middle-aged groups (p = 0.01) had significantly lower gait speed than Non-OA.
Male OA patients in the elderly group showed lower handgrip strength (p = 0.09), leg-back strength
(p < 0.01), and gait speed (p = 0.07) than their Non-OA counterparts, as did the middle-aged OA
males for dumbbell curls (p = 0.06) and gait speed (p = 0.09). Female OA patients in the elderly group
showed a higher value of whole-body muscle mass and WSMI than the Non-OA subjects (p = 0.03).
However, there was no significant difference in muscle strength or endurance between the OA and
Non-OA groups of elderly.
3.2. The Coenzyme Q10 Status, Oxidative Stress, and Antioxidant Capacity of the Subjects
The coenzyme Q10 status, oxidative stress, and antioxidant capacity of the subjects are shown in
Table 1. Elderly patients with OA had a slightly significantly lower level of coenzyme Q10 than Non-OA
subjects (coenzyme Q10/TC, p = 0.06). With regard to oxidative stress, middle-aged patients with OA
had a significantly higher level of protein carbonyl than Non-OA subjects (p = 0.02). After stratification
by age, Non-OA subjects in the elderly group had a significantly higher level of protein carbonyl than
those in the middle-aged group (p < 0.01). Regarding the level of antioxidant capacity, both elderly
and middle-aged patients with OA had a significantly higher level of serum TAC than the Non-OA
group (p < 0.01). After stratification by age, the level of RBC TAC was significantly lower in elderly
patients with OA than middle-aged patients with OA (p = 0.02).
Table 1. Coenzyme Q10 status, oxidative stress, and antioxidant capacity of the subjects.
Elderly 2
OA (N = 74)
1
Coenzyme Q10 (µM)
Coenzyme Q10/TC
(µmol/mmol)
Oxidative stress
MDA (µM)
Protein carbonyl
(nmole/mg protein)
Antioxidant capacity
Serum TAC (mM Trolox)
RBC TAC (mM Trolox)
Non-OA (N = 33)
Middle-Age 2
p Value
3
OA (N = 26)
Non-OA (N = 67)
p Value 3
0.41 ± 0.15 (0.41)
0.47 ± 0.22 (0.46)
0.18
0.44 ± 0.13 (0.42)
0.47 ± 0.18 (0.43)
0.44
0.08 ± 0.03 (0.08)
0.10 ± 0.04 (0.09)
0.06
0.09 ± 0.03 (0.09)
0.09 ± 0.03 (0.09)
0.99
2.6 ± 0.5 (2.5)
2.7 ± 0.6 (2.6)
0.29
2.5 ± 0.4 (2.5)
2.7 ± 0.5 (2.7)
0.09
0.38 ± 0.06 (0.37)
0.38 ± 0.07 (0.38) *
0.96
0.36 ± 0.05 (0.37)
0.34 ± 0.07 (0.33)
0.02
5.8 ± 0.5 (5.7)
10.2 ± 0.7 (10.1) *
5.4 ± 0.3 (5.4)
10.0 ± 0.5 (10.0)
<0.01
0.16
5.9 ± 0.4 (6.0)
10.6 ± 0.7 (10.4)
5.4 ± 0.3 (5.5)
10.1 ± 0.5 (10.0)
<0.01
<0.01
1
Means ± SD (medians). 2 Elderly: ≥65 y; middle-age: 40–64 y. 3 Comparison between OA and non-OA in the same
age group. * Comparison between different age groups with OA or without OA, p < 0.05. MDA, malondialdehyde;
OA, osteoarthritis; RBC, red blood cell; TAC, total antioxidant capacity; TC, total cholesterol.
3.3. The Correlations between Coenzyme Q10 Status, Oxidative Stress, Antioxidant Capacity, Muscle Mass,
and Muscle Strength and Endurance
Figure 1 shows the correlations between coenzyme Q10 status and oxidative stress and antioxidant
capacity. Coenzyme Q10 status was significantly negatively correlated with oxidative stress (protein
carbonyl, r = −0.18, p < 0.01) and positively correlated with the level of RBC TAC (r = 0.15, p = 0.03).
Additionally, significantly positive correlations were found between coenzyme Q10 status and the
levels of serum TAC (r = 0.21, p = 0.04) and RBC TAC (r = 0.27, p < 0.01) in the patients with OA.
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Table 2. Characteristics of the subjects.
Characteristics
OA (N = 100)
Non-OA (N = 100)
p Value 2
Age (y)
BMI (kg/m2 )
Albumin (g/L)
BUN (mmol/L)
Creatinine (µmol/L)
GOT (U/L)
GPT (U/L)
hs-CRP (mg/L)
69.5 ± 9.4 (71.0) 1
25.3 ± 3.8 (25.6)
45.0 ± 2.7 (45.0)
6.0 ± 2.4 (5.4)
76.0 ± 23.9 (71.6)
24.0 ± 5.0 (23.0)
20.9 ± 7.9 (19.0)
2.4 ± 7.2 (1.2)
60.5 ± 9.6 (60.0)
24.3 ± 4.3 (24.2)
45.2 ± 3.1 (45.0)
5.1 ± 2.1 (4.6)
74.3 ± 23.9 (71.6)
27.1 ± 10.9 (25.0)
27.3 ± 20.7 (22.0)
2.2 ± 3.8 (1.0)
<0.01
0.10
0.31
<0.01
0.58
0.06
<0.01
0.36
Muscle mass
Whole body muscle mass (kg)
Trunk muscle mass (kg)
WSMI (kg/m2 )
ASMI (kg/m2 )
Muscle strength and endurance
Handgrip strength (kg)
Dumbbells curls (reps)
Leg-back strength (kg)
Chair-stand test (reps)
Gait speed (m/s)
SPPB (scores)
Sarcopenia (n, %) 6
Male (n = 27)
Female (n = 73)
p Value 3
Male (n = 40)
Female (n = 60)
p Value 3
50.5 ± 9.0 (49.5)
25.4 ± 4.6 (24.9)
18.6 ± 2.8 (18.9)
7.9 ± 1.3 (7.9)
38.6 ± 6.4 (38.6)
19.9 ± 3.5 (19.5)
16.3 ± 2.3 (16.4)
6.6 ± 1.0 (6.7)
<0.01
<0.01
<0.01
<0.01
51.5 ± 10.6 (50.9)
25.5 ± 5.2 (25.6)
18.6 ± 2.9 (18.6)
8.1 ± 1.5 (8.1)
38.3 ± 7.4 (36.8)
19.3 ± 3.6 (18.7)
15.8 ± 2.5 (15.7))
6.6 ± 1.3 (6.4)
<0.01
<0.01
<0.01
<0.01
29.3 ± 6.7 (28.7) †
16.8 ± 6.5 (17.0) †
65.2 ± 23.8 (61.5) †
11.5 ± 4.9 (11.0) †
0.9 ± 0.3 (1.0) †
9.7 ± 2.1 (10.0) †
7 (25.9%)
20.2 ± 4.4 (20.1)
15.5 ± 4.3 (15.0)
38.3 ± 14.0 (38.5)
11.1 ± 4.0 (11.0)
0.9 ± 0.3 (0.9) †
9.5 ± 2.2 (10.0) †
10 (13.7%)
<0.01
0.18
<0.01
0.65
0.26
0.75
0.23
35.1 ± 7.2 (35.5)
21.2 ± 6.1 (20.0)
80.0 ± 29.3 (79.3)
13.1 ± 3.8 (13.5)
1.2 ± 0.3 (1.3)
10.9 ± 1.4 (11.5)
6 (15.0%)
21.2 ± 4.6 (21.5)
16.1 ± 4.4 (16.0)
42.7 ± 14.8 (44.0)
12.4 ± 4.0 (12.0)
1.0 ± 0.2 (1.0)
10.5 ± 1.5 (11.0)
10 (16.7%)
<0.01
<0.01
<0.01
0.14
<0.01
0.11
0.96
Elderly 4
BMI (kg/m2 )
Albumin (g/L)
BUN (mmol/L)
Creatinine (µmol/L)
GOT (U/L)
GPT (U/L)
hs-CRP (mg/L)
Middle-age 4
OA (N = 74)
Non-OA (N = 33)
p Value 5
OA (N = 26)
Non-OA (N = 67)
p Value 5
24.9 ± 3.7 (25.1)
44.5 ± 2.3 (44.5) *
6.2 ± 2.6 (5.4)
77.8 ± 24.8 (72.5)
24.1 ± 4.9 (23.0)
19.9 ± 7.3 (18.0) *
2.9 ± 8.3 (1.3) *
22.9 ± 4.0 (23.2)
43.4 ± 3.2 (44.0) *
6.1 ± 2.9 (5.4) *
84.9 ± 31.8 (81.3) *
29.8 ± 12.4 (27.0) *
27.5 ± 19.5 (22.0)
2.0 ± 2.3 (1.1)
0.02
0.20
0.63
0.18
<0.01
0.02
0.41
26.5 ± 3.8 (26.3)
46.5 ± 3.4 (46.5)
5.5 ± 1.5 (5.4)
73.4 ± 19.4 (67.2)
23.8 ± 5.3 (23.0)
23.7 ± 8.9 (22.0)
1.2 ± 1.0 (0.9)
25.0 ± 4.2 (24.8)
46.0 ± 2.6 (46.0)
4.5 ± 1.2 (4.6)
69.0 ± 16.8 (66.3)
25.7 ± 9.9 (24.0)
27.2 ± 21.4 (22.0)
2.3 ± 4.4 (0.9)
0.12
0.53
<0.01
0.47
0.53
0.80
0.56
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Table 2. Cont.
Characteristics
OA (N = 100)
Non-OA (N = 100)
Elderly 4
Muscle mass
Whole body muscle mass (kg)
Trunk muscle mass (kg)
WSMI (kg/m2 )
ASMI (kg/m2 )
Muscle strength and endurance
Handgrip strength (kg)
Dumbbells curls (reps)
Leg-back strength (kg)
Chair-stand test (reps)
Gait speed (m/s)
SPPB (scores)
Sarcopenia (n, %) 6
p Value 2
Middle-age 4
OA (N = 74)
Non-OA (N = 33)
p Value 5
OA (N = 26)
Non-OA (N = 67)
p Value 5
40.1 ± 8.0 (38.7) *
20.5 ± 4.2 (19.9) *
16.5 ± 2.4 (16.4) *
6.8 ± 1.1 (6.7) *
38.8 ± 8.3 (36.5) *
19.5 ± 3.9 (18.6) *
15.8 ± 2.5 (15.6) *
6.6 ± 1.4 (6.3) *
0.24
0.17
0.19
0.25
46.7 ± 9.8 (45.1)
23.9 ± 4.8 (23.2)
18.2 ± 2.9 (17.8)
7.6 ± 1.4 (7.2)
45.9 ± 11.3 (45.7)
23.0 ± 5.5 (23.2)
17.4 ± 3.1 (17.6)
7.5 ± 1.6 (7.4)
0.75
0.46
0.26
0.79
21.2 ± 5.5 (20.6) *
14.9 ± 5.0 (15.0) *
41.4 ± 16.6 (38.8) *
10.5 ± 4.3 (10.0) *
0.85 ± 0.29 (0.90) *
9.1 ± 2.2 (9.0) *
14 (18.9%)
23.1 ± 7.1 (23.9) *
15.5 ± 5.2 (16.0) *
49.3 ± 25.8 (44.0) *
10.6 ± 3.6 (10.0) *
0.96 ± 0.27 (1.02) *
9.8 ± 1.7 (10.0) *
9 (27.3%)
0.19
0.49
0.21
0.67
0.07
0.14
0.47
26.8 ± 7.5 (26.3)
18.3 ± 4.2 (18.0)
57.5 ± 26.8 (53.3)
13.2 ± 3.7 (13.5)
1.00 ± 0.21 (1.04)
10.8 ± 1.5 (11.0)
3 (11.5%)
28.6 ± 9.2 (26.7)
19.5 ± 5.6 (19.0)
61.7 ± 28.9 (58.5)
13.7 ± 3.7 (14.0)
1.15 ± 0.25 (1.17)
11.1 ± 1.1 (11.0)
7 (10.4%)
0.55
0.57
0.61
0.64
0.01
0.48
1.00
Male
Elderly
Muscle mass
Whole body muscle mass (kg)
Trunk muscle mass (kg)
WSMI (kg/m2 )
ASMI (kg/m2 )
Muscle strength and endurance
Handgrip strength (kg)
Dumbbells curls (reps)
Leg-back strength (kg)
Chair-stand test (reps)
Gait speed (m/s)
SPPB (scores)
Sarcopenia (n, %) 6
4
Middle-Age 4
OA (N = 18)
Non-OA (N = 10)
p Value 5
OA (N = 9)
Non-OA (N = 30)
p Value 5
48.3 ± 8.5 (47.0)
24.4 ± 4.4 (23.6)
17.7 ± 2.6 (17.7) *
7.5 ± 1.3 (7.6) *
46.8 ± 6.9 (45.8)
23.6 ± 3.3 (23.9)
17.9 ± 2.4 (18.3)
7.6 ± 1.3 (7.5)
0.63
0.60
0.87
0.92
54.8 ± 8.7 (53.7)
27.5 ± 4.7 (26.9)
20.4 ± 2.5 (20.4)
8.7 ± 1.1 (8.7)
53.0 ± 11.2 (53.2)
26.2 ± 5.6 (26.0)
18.8 ± 3.1 (19.0)
8.3 ± 1.5 (8.2)
0.56
0.52
0.19
0.19
27.0 ± 5.5 (25.8) *
16.2 ± 7.6 (16.5)
57.7 ± 16.7 (57.8)
10.7 ± 5.6 (10.0)
0.9 ± 0.4 (0.9)
9.1 ± 2.3 (10.0)
6 (33.3%)
30.5 ± 4.4 (29.8) *
17.7 ± 3.9 (17.0) *
79.8 ± 20.1 (78.0)
10.7 ± 2.5 (10.0) *
1.1 ± 0.3 (1.2)
10.1 ± 1.2 (10.0) *
3 (30.0%)
0.09
0.41
< 0.01
0.77
0.07
0.41
1.00
34.0 ± 6.8 (36.0)
18.0 ± 3.0 (18.0)
80.3 ± 29.5 (88.0)
13.1 ± 2.8 (13.0)
1.0 ± 0.2 (1.1)
10.8 ± 1.1 (11.0)
1 (11.1%)
36.6 ± 7.3 (38.3)
22.4 ± 6.4 (22.0)
80.1 ± 32.1 (79.8)
13.9 ± 3.9 (14.0)
1.2 ± 0.3 (1.3)
11.2 ± 1.3 (12.0)
3 (10.0%)
0.34
0.06
0.99
0.34
0.09
0.21
1.00
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Table 2. Cont.
Characteristics
OA (N = 100)
p Value 2
Non-OA (N = 100)
Female
Elderly
Muscle mass
Whole body muscle mass (kg)
Trunk muscle mass (kg)
WSMI (kg/m2 )
ASMI (kg/m2 )
Muscle strength and endurance
Handgrip strength (kg)
Dumbbells curls (reps)
Leg-back strength (kg)
Chair-stand test (reps)
Gait speed (m/s)
SPPB (scores)
Sarcopenia (n, %) 6
1
4
Middle-Age 4
OA (N = 56)
Non-OA (N = 23)
p Value 5
OA (N = 17)
Non-OA (N = 37)
p Value 5
37.4 ± 5.6 (38.1) *
19.2 ± 3.2 (19.2) *
16.1 ± 2.2 (16.2)
6.5 ± 1.0 (6.6)
35.3 ± 6.3 (34.2) *
17.7 ± 2.6 (17.4) *
14.9 ± 2.0 (14.9) *
6.2 ± 1.3 (6.0)*
0.03
0.05
0.03
0.06
42.4 ± 7.4 (40.6)
22.0 ± 3.7 (22.3)
17.1 ± 2.5 (17.2)
6.9 ± 1.2 (7.2)
40.2 ± 7.4 (39.3)
20.4 ± 3.7 (19.7)
16.3 ± 2.6 (16.2)
6.8 ± 1.2 (6.7)
0.32
0.13
0.29
0.69
19.3 ± 4.1 (19.4) *
14.5 ± 3.7 (15.0) *
36.2 ± 12.8 (34.8) *
10.4 ± 3.8 (10.0) *
0.8 ± 0.3 (0.9) *
9.1 ± 2.2 (9.0) *
8 (14.3%)
19.8 ± 5.5 (19.8)
14.5 ± 5.4 (13.5) *
36.1 ± 14.0 (35.0) *
10.6 ± 4.0 (10.0) *
0.9 ± 0.2 (1.0) *
9.6 ± 1.9 (9.0) *
6 (26.1%)
0.83
0.95
0.92
0.79
0.40
0.25
0.33
23.0 ± 4.5 (23.9)
18.5 ± 4.8 (18.0)
45.4 ± 15.7 (48.5)
13.2 ± 4.1 (14.0)
1.0 ± 0.2 (1.0)
10.8 ± 1.7 (11.0)
2 (11.8%)
22.0 ± 3.8 (21.9)
17.1 ± 3.4 (17.0)
46.7 ± 13.9 (48.0)
13.5 ± 3.7 (13.0)
1.1 ± 0.2 (1.1)
11.0 ± 1.0 (11.0)
4 (10.8%)
0.43
0.25
0.76
0.93
0.10
0.85
1.00
Means ± SD (medians). 2 Comparison between OA and Non-OA groups. 3 Comparison between gender in the OA or Non-OA group. † Comparison between OA or Non-OA in the same
gender group, p < 0.05. 4 Elderly: ≥65 y; middle-age: 40–64 y. 5 Comparison between OA or Non-OA in the same age group. * Comparison between different age groups with OA or
without OA, p < 0.05. 6 Sarcopenia was defined according to the Asian Working Group. ASMI, appendicular skeletal muscle mass index; BMI, body mass index; BUN, blood urea nitrogen;
GOT, glutamic-oxaloacetic transaminase; GPT, glutamate-pyruvate transaminase; hs-CRP, high sensitivity-C reactive protein; OA, osteoarthritis; SPPB, short physical performance battery;
WSMI, whole skeletal muscle mass index.
Figure 1 shows the correlations between coenzyme Q10 status and oxidative stress and
antioxidant capacity. Coenzyme Q10 status was significantly negatively correlated with oxidative
stress (protein carbonyl, r = −0.18, p < 0.01) and positively correlated with the level of RBC TAC (r =
0.15, p = 0.03). Additionally, significantly positive correlations were found between coenzyme Q10
Antioxidants 2020, 9, 1275
8 of 16
status and the levels of serum TAC (r = 0.21, p = 0.04) and RBC TAC (r = 0.27, p < 0.01) in the patients
with OA.
Next, the
the correlations
correlations between
between coenzyme
coenzyme Q10
muscle mass
mass (Figure
(Figure 2),
2), and
and muscle
muscle
Next,
Q10 status
status and
and muscle
strength and
and endurance
endurance (Figure
(Figure 3)
3) were
were analyzed.
analyzed. In
whole sample,
sample, the
the level
level of
of coenzyme
coenzyme Q10
Q10
In the
the whole
strength
was significantly
significantly positively
positively correlated
correlated with
with whole
whole body
body muscle
muscle mass
mass (Figure
(Figure 2A,
2A, rr =
= 0.24,
0.24, pp <
< 0.01),
0.01),
was
trunk muscle
musclemass
mass(Figure
(Figure2B,
2B,r =
r =0.24,
0.24,p <
p <0.01),
0.01),
WSMI
(Figure
= 0.26,
< 0.01),
ASMI
(Figure
trunk
WSMI
(Figure
2C,2C,
r =r0.26,
p <p0.01),
ASMI
(Figure
2D,
r = 0.24,
p < 0.01),
handgrip
strength
(Figure
r = 0.20,
p < 0.01),
repetitions
of hand
dumbbell
r2D,
= 0.24,
p < 0.01),
handgrip
strength
(Figure
3A, r3A,
= 0.20,
p < 0.01),
repetitions
of hand
dumbbell
curls
curls (Figure
r =p0.22,
p < 0.01),
leg-back
strength
(Figure
r =p0.28,
p < repetitions
0.01), repetitions
of chair(Figure
3B, r =3B,
0.22,
< 0.01),
leg-back
strength
(Figure
3C, r =3C,
0.28,
< 0.01),
of chair-stands
stands (Figure
r =p0.15,
p = 0.03),
gait speed
(Figure
r = 0.24,
p < 0.01),
SPPB
scores
(Figure
(Figure
3D, r =3D,
0.15,
= 0.03),
gait speed
(Figure
3E, r 3E,
= 0.24,
p < 0.01),
andand
SPPB
scores
(Figure
3F,
r = 0.20,
< 0.01).
Similar
trends
were
also
found
in the
patients
with
OA.
r3F,
= 0.20,
p <p0.01).
Similar
trends
were
also
found
in the
patients
with
OA.
Figure 1. Correlations between coenzyme Q10 status and oxidative stress and total antioxidant
Figure 1. Correlations between coenzyme Q10 status and oxidative stress and total antioxidant
capacity. (A) Correlation between coenzyme Q10 status and MDA. OA group: r = −0.16, p = 0.11;
capacity. (A) Correlation between coenzyme Q10 status and MDA. OA group: r = −0.16, p = 0.11; OA
OA + non-OA group: r = 0.02, p = 0.74; (B) Correlation between coenzyme Q10 status and protein
+ non-OA group: r = 0.02, p = 0.74; (B) Correlation between coenzyme Q10 status and protein carbonyl.
carbonyl. OA group: r = −0.13, p = 0.21; OA + non-OA group: r = −0.18, p < 0.01; (C) Correlation
OA group: r = −0.13, p = 0.21; OA + non-OA group: r = −0.18, p < 0.01; (C) Correlation between
between coenzyme Q10 status and serum TAC. OA group: r = 0.21, p = 0.04; OA + non-OA group:
coenzyme Q10 status and serum TAC. OA group: r = 0.21, p = 0.04; OA + non-OA group: r = 0.05, p =
r = 0.05, p = 0.47; (D) Correlation between coenzyme Q10 status and RBC TAC. OA group: r = 0.27,
0.47; (D) Correlation between coenzyme Q10 status and RBC TAC. OA group: r = 0.27, p < 0.01; OA +
p < 0.01; OA + non-OA group: r = 0.15, p = 0.03. MDA, malondialdehyde; OA, osteoarthritis;
non-OA group: r = 0.15, p = 0.03. MDA, malondialdehyde; OA, osteoarthritis; RBC, red blood cell;
RBC, red blood cell; TAC, total antioxidant capacity; TC, total cholesterol.
TAC, total antioxidant capacity; TC, total cholesterol.
We further examined the correlations between coenzyme Q10 status and oxidative stress, muscle
mass, muscle strength, and muscle endurance after stratification by age (Table 3). Coenzyme Q10
status was significantly negatively correlated with oxidative stress (MDA, r = −0.21, p = 0.07),
and positively correlated with antioxidant capacity (serum TAC, r = 0.20, p = 0.08; RBC TAC, r = 0.26,
p < 0.05), muscle mass (whole body muscle mass, r = 0.21, p = 0.08; WSMI, r = 0.22, p = 0.07;
ASMI, mboxr = 0.26, p < 0.05), and muscle strength and endurance (dumbbell curls, r = 0.24, p < 0.05;
leg-back strength, r = 0.29, p < 0.05; gait speed, r = 0.33, p < 0.01) in the elderly OA patients. In addition,
coenzyme Q10 status was significantly positively correlated with muscle mass in the middle-aged
Non-OA group (p < 0.05).
Antioxidants 2020, 9, 1275
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11 of 18
Figure 2. Correlations between coenzyme Q10 status and muscle mass. (A) Correlation between
Figure 2. Correlations between coenzyme Q10 status and muscle mass. (A) Correlation between
coenzyme Q10 status and whole-body muscle mass. OA group: r = 0.27, p < 0.01; OA + non-OA group:
coenzyme Q10 status and whole-body muscle mass. OA group: r = 0.27, p < 0.01; OA + non-OA group:
r = 0.24, p < 0.01; (B) Correlation between coenzyme Q10 status and trunk muscle mass. OA group:
r = 0.24, p < 0.01; (B) Correlation between coenzyme Q10 status and trunk muscle mass. OA group: r
r = 0.24, p = 0.02; OA + non-OA group: r = 0.24, p < 0.01; (C) Correlation between coenzyme Q10
= 0.24, p = 0.02; OA + non-OA group: r = 0.24, p < 0.01; (C) Correlation between coenzyme Q10 status
status and WSMI. OA group: r = 0.26, p < 0.01; OA + non-OA group: r = 0.26, p < 0.01; (D) Correlation
and WSMI. OA group: r = 0.26, p < 0.01; OA + non-OA group: r =0.26, p < 0.01; (D) Correlation between
between coenzyme Q10 status and ASMI. OA group: r = 0.24, p = 0.02; OA + non-OA group: r = 0.24,
coenzyme Q10 status and ASMI. OA group: r = 0.24, p = 0.02; OA + non-OA group: r = 0.24, p < 0.01.
p < 0.01. ASMI, appendicular skeletal muscle mass index; OA, osteoarthritis; TC, total cholesterol;
ASMI, appendicular skeletal muscle mass index; OA, osteoarthritis; TC, total cholesterol; WSMI,
WSMI, whole skeletal muscle mass index.
whole skeletal muscle mass index.
3.4. The Correlations between Oxidative Stress and Antioxidant Capacity, Muscle Mass, Muscle Strength,
and Muscle Endurance
Table 4 shows the correlations between oxidative stress and antioxidant capacity, muscle mass,
muscle strength, and muscle endurance. There was a significantly negative correlation between
oxidative stress (protein carbonyl) and muscle mass (whole body muscle mass, r = −0.23, p < 0.01;
trunk muscle mass, r = −0.26, p < 0.01; WSMI, r = −0.25, p < 0.01; ASMI, r = −0.22, p < 0.01) and
muscle strength and endurance (leg-back strength, r = −0.15, p = 0.03; gait speed, r = −0.33, p < 0.01;
SPPB, r = −0.26, p < 0.01). Similar trends were also found in the middle-aged group. On the other
hand, antioxidant capacity (RBC TAC) was significantly positively correlated with muscle mass
(WSMI, r = 0.15, p < 0.05) and muscle endurance (gait speed, r = 0.27, p < 0.01).
Antioxidants 2020, 9, 1275
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12 of 18
Figure 3.
3. Correlations
Correlationsbetween
betweencoenzyme
coenzyme
Q10
status
and
muscle
strength
muscle
endurance.
Figure
Q10
status
and
muscle
strength
andand
muscle
endurance.
(A)
between
coenzyme
status
and handgrip
strength.
OA group:
r =p0.24,
p =OA
0.01;
(A) Correlation
Correlation
between
coenzyme
Q10 Q10
status
and handgrip
strength.
OA group:
r = 0.24,
= 0.01;
+
OA
+
non-OA
group:
r
=
0.20,
p
<
0.01;
(B)
Correlation
between
coenzyme
Q10
status
and
dumbbells
non-OA group: r = 0.20, p < 0.01; (B) Correlation between coenzyme Q10 status and dumbbells curls.
curls.
OA group:
= 0.02;
OA + non-OA
0.22,(C)
p <Correlation
0.01; (C) Correlation
between
OA
group:
r = 0.24,r p==0.24,
0.02;pOA
+ non-OA
group: r =group:
0.22, pr<=0.01;
between coenzyme
coenzyme
Q10
status
and
leg-back
strength.
OA
group:
r
=
0.34,
p
<
0.01;
OA
+
non-OA
group:
0.28,
Q10 status and leg-back strength. OA group: r = 0.34, p < 0.01; OA + non-OA group: r =0.28, pr <= 0.01;
p
<
0.01;
(D)
Correlation
between
coenzyme
Q10
status
and
chairstand
test.
OA
group:
r
=
0.13,
(D) Correlation between coenzyme Q10 status and chair- stand test. OA group: r = 0.13, p = 0.20; OA
= 0.20; OA
+ non-OA
group:
r = 0.15,
p = 0.03; (E)between
Correlation
betweenQ10
coenzyme
Q10gait
status
and gait
+p non-OA
group:
r = 0.15,
p = 0.03;
(E) Correlation
coenzyme
status and
speed.
OA
speed. OA group: r = 0.35, p < 0.01; OA + non-OA group: r = 0.24, p < 0.01; (F) Correlation between
group: r = 0.35, p < 0.01; OA + non-OA group: r = 0.24, p < 0.01; (F) Correlation between coenzyme Q10
coenzyme Q10 status and SPPB. OA group: r = 0.21, p = 0.04; OA + non-OA group: r = 0.20, p < 0.01.
status and SPPB. OA group: r = 0.21, p = 0.04; OA + non-OA group: r = 0.20, p < 0.01. OA, osteoarthritis;
OA, osteoarthritis; SPPB, short physical performance battery; TC, total cholesterol.
SPPB, short physical performance battery; TC, total cholesterol.
We further examined the correlations between coenzyme Q10 status and oxidative stress, muscle
mass, muscle strength, and muscle endurance after stratification by age (Table 3). Coenzyme Q10
status was significantly negatively correlated with oxidative stress (MDA, r = −0.21, p = 0.07), and
positively correlated with antioxidant capacity (serum TAC, r = 0.20, p = 0.08; RBC TAC, r = 0.26, p <
0.05), muscle mass (whole body muscle mass, r = 0.21, p = 0.08; WSMI, r = 0.22, p = 0.07; ASMI, r = 0.26,
p < 0.05), and muscle strength and endurance (dumbbell curls, r = 0.24, p < 0.05; leg-back strength, r =
0.29, p < 0.05; gait speed, r = 0.33, p < 0.01) in the elderly OA patients. In addition, coenzyme Q10
status was significantly positively correlated with muscle mass in the middle-aged Non-OA group (p
< 0.05).
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Table 3. Correlation between coenzyme Q10 status and oxidative stress, muscle mass, muscle strength,
and muscle endurance stratified by age.
Coenzyme Q10/TC (µmol/mmol)
Elderly 2
Oxidative stress
MDA (µM)
Protein carbonyl (nmole/mg protein)
Antioxidant capacity
Serum TAC (mM Trolox)
RBC TAC (mM Trolox)
Muscle mass
Whole body muscle mass (kg)
Trunk muscle mass (kg)
WSMI (kg/m2 )
ASMI (kg/m2 )
Muscle strength and endurance
Handgrip strength (kg)
Dumbbells curls (reps)
Leg-back strength (kg)
Chair-stand test (reps)
Gait speed (m/s)
SPPB (scores)
Middle-Age 2
OA (N = 74)
Non-OA (N = 33)
OA (N = 26)
Non-OA (N = 67)
−0.21 1,#
−0.12
0.18
−0.27
−0.07
−0.08
0.09
−0.11
0.20 †
0.26 *
−0.10
−0.19
0.19
0.20
−0.02
0.13
0.21 †
0.15
0.22 #
0.26 *
0.15
0.25
0.15
0.08
0.20
0.30
0.27
0.10
0.30 *
0.28 *
0.36 **
0.38 **
0.19
0.24 *
0.29 *
0.03
0.33 **
0.16
0.04
0.24
0.19
0.33 ‡
0.17
0.28
0.17
−0.01
0.25
0.17
0.31
0.12
0.18
0.20
0.27 *
0.12
0.05
0.15
1 Correlation coefficients. * p < 0.05, ** p < 0.01, ‡ p = 0.06, # p = 0.07, † p = 0.08. 2 Elderly: ≥65 y; middle-age: 40–64 y.
ASMI, appendicular skeletal muscle mass index; MDA, malondialdehyde; OA, osteoarthritis; SPPB, short physical
performance battery; TAC, total antioxidant capacity; TC, total cholesterol; WSMI, whole skeletal muscle mass index.
Table 4. Correlations between oxidative stress, antioxidant capacity, muscle mass, muscle strength, and
muscle endurance of the subjects.
Oxidative Stress
OA + Non-OA (N = 200)
Whole body muscle mass (kg)
Trunk muscle mass (kg)
WSMI (kg/m2 )
ASMI (kg/m2 )
Handgrip strength (kg)
Dumbbells curls (reps)
Leg-back strength (kg)
Chair-stand test (reps)
Gait speed (m/s)
SPPB (scores)
Elderly 2 OA + Non-OA (N = 107)
Whole body muscle mass (kg)
Trunk muscle mass (kg)
WSMI (kg/m2 )
ASMI (kg/m2 )
Handgrip strength (kg)
Dumbbells curls (reps)
Leg-back strength (kg)
Chair-stand test (reps)
Gait speed (m/s)
SPPB (scores)
Middle-age 2 OA + Non-OA (N = 93)
Whole body muscle mass (kg)
Trunk muscle mass (kg)
WSMI (kg/m2 )
Antioxidant Capacity
MDA
(µM)
Protein Carbonyl
(nmole/mg protein)
Serum TAC
(mM Trolox)
RBC TAC
(mM Trolox)
0.11 1
0.08
0.08
0.13
0.13
−0.04
0.10
−0.01
0.14
0.01
−0.23 **
−0.26 **
−0.25 **
−0.22 **
−0.07
−0.13
−0.15 *
−0.13
−0.33 **
−0.26 **
0.01
0.04
0.07
0.04
−0.13
−0.06
−0.03
−0.03
0.12
0.01
0.09
0.10
0.15 *
0.10
−0.03
−0.02
0.04
−0.00
0.27 **
0.11
0.12
0.13
0.08
0.09
0.06
−0.03
−0.00
−0.03
0.09
0.00
−0.12
−0.14
−0.17
−0.14
0.04
−0.02
0.01
−0.04
−0.10
−0.10
0.02
0.04
0.09
0.10
−0.17
−0.06
−0.04
−0.05
0.17
−0.02
0.08
0.09
0.14
0.10
−0.03
−0.00
0.09
−0.02
0.38 **
0.08
0.08
0.02
0.07
−0.23 *
−0.26 *
−0.23 *
0.03
0.08
0.07
0.01
0.05
0.11
Antioxidants 2020, 9, 1275
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Table 4. Cont.
Oxidative Stress
ASMI (kg/m2 )
Handgrip strength (kg)
Dumbbells curls (reps)
Leg-back strength (kg)
Chair-stand test (reps)
Gait speed (m/s)
SPPB (scores)
Antioxidant Capacity
MDA
(µM)
Protein Carbonyl
(nmole/mg protein)
Serum TAC
(mM Trolox)
RBC TAC
(mM Trolox)
0.17
0.17
−0.12
0.21*
−0.04
0.15
−0.04
−0.20
0.01
−0.08
−0.17
−0.02
−0.42 **
−0.23 *
−0.01
−0.08
−0.08
−0.03
−0.01
0.12
0.10
0.04
−0.11
−0.12
−0.09
−0.10
0.12
0.07
1
Correlation coefficients. * p < 0.05 and ** p < 0.01. 2 Elderly: ≥65 y; middle-age: 40–64 y. ASMI, appendicular
skeletal muscle mass index; MDA, malondialdehyde; OA, osteoarthritis; SPPB, short physical performance battery;
TAC, total antioxidant capacity; WSMI, whole skeletal muscle mass index.
4. Discussion
This is the first study to investigate the association of coenzyme Q10 status and muscle mass,
strength and endurance in patients with OA. In this study, we successfully detected a significantly
positive correlation between coenzyme Q10 status and muscle mass, muscle strength, and muscle
endurance in patients with OA. OA is an age-related disease that mostly occurs in middle-aged and
elderly individuals that may prompt them to face loss of muscle mass and physical function [25,26].
In addition to the level of coenzyme Q10, coenzyme Q10 status may be depleted during aging [27].
Elderly subjects were characterized by impaired coenzyme Q10 status due to a low coenzyme Q10
redox capacity [13]. Indeed, patients with OA had lower coenzyme Q10 status than the Non-OA
group, particularly those in the elderly group (Table 1). We also noticed that both the middle-aged
and elderly groups suffered from coenzyme Q10 deficiency (plasma coenzyme Q10 < 0.5 µM) [10] in
this study. There was a significantly higher proportion of coenzyme Q10 status deficiency in patients
with OA than Non-OA (OA, 75% vs. Non-OA, 59%, p = 0.02), and the level of coenzyme Q10 dropped
with the severity of joint degeneration (K/L grade =2 vs. ≥3, median level of coenzyme Q10: 0.44 vs.
0.39 µM, p = 0.04). Previous studies have demonstrated that patients with OA had significantly lower
antioxidants such as vitamin C and vitamin E [28–30]. Since evidence has indicated that patients with
OA suffer from higher oxidative stress [5,31], to neutralize the higher oxidative stress caused by OA,
we speculate that coenzyme Q10 may be consumed to slow the progression of OA.
Oxidative stress damage in patients with OA may limit their physical function [6,32]. A result from
the FORMoSA project (Bavarian Research Association—Sarcopenia and Osteoporosis) indicated that
patients with OA exhibited a higher rate of sarcopenia (OA vs. Non-OA, 9.1% and 3.5%, respectively) [8].
Recently, a Korean report from the Dong-gu study also indicated that joint space narrowing was
positively correlated with the muscle strength of OA in both genders [33]. In this study, 17% of patients
with OA suffered from sarcopenia, and the prevalence increased with the degree of joint degeneration
(data not shown, K/L grade =2 vs. ≥3, prevalence: 12% vs. 23%). Patients with OA may exhibit a
decrease in collagen metabolism, mitochondrial impairment in the pathology of sarcopenia, and muscle
fiber atrophy, which are associated with oxidative stress caused by the disease [5,34]. As a result,
patients with OA in the middle-aged group in this study exhibited significantly higher oxidative stress
(protein carbonyl, Table 1), and the level of protein carbonyl was significantly negatively associated
with muscle mass, muscle strength, and muscle endurance (Table 4). However, we did not detect
a significantly lower antioxidant capacity in patients with OA, except in the elderly OA (Table 1).
A decreasing level of antioxidant capacity with joint degeneration was found in the patients with OA
(data not shown, K/L grade =2 vs. ≥3, median level of serum TAC: 5.90 vs. 5.57 mM Trolox, p = 0.07;
median level of RBC TAC: 10.20 vs. 10.00 mM Trolox, p = 0.01). The oxidative changes during the
progression of OA are complicated. Most patients with OA in the present study were newly diagnosed;
we speculated that their higher antioxidant capacity may be caused by compensatory responses to
Antioxidants 2020, 9, 1275
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oxidative stress [35,36]. This may also be a reason that the patients with OA did not show a significantly
low value of muscle mass in this study (Table 2), but their muscle strength and endurance worsened
with the severity of joint degeneration (K/L grade =2 vs. ≥3, p < 0.05). Even so, the antioxidant
capacity was significantly positively correlated with muscle mass and muscle endurance (Table 4).
Thus, increasing the antioxidant capacity of patients with OA may benefit their muscle function as
well as decrease oxidative stress during disease progression.
Recent data from two independent population-based cohorts (PopGen control cohort and FoCus
cohort) pointed out that coenzyme Q10 status could be a determinant of muscle strength [37].
Del Pozo-Cruz et al. [38] found that coenzyme Q10 status was correlated with functional capacity at
an advanced age in community-dwelling people. In the present study, patients with OA had lower
muscle mass, muscle strength, and muscle endurance, particularly in the elderly group (Table 2).
In addition, significantly positive correlations were found between coenzyme Q10 status and muscle
mass, muscle strength, and muscle endurance (Figures 2 and 3). We used the post hoc tests to examine
the statistical power of the sample size for the data, and the values for the statistical power of the sample
size were 0.8–0.9. It is worth noting that subjects who showed a low muscle strength and endurance
score had insufficient coenzyme Q10 status (Figure 3B–E). Since both age and gender are related to
muscle function, we examined the correlations between coenzyme Q10 status and muscle mass, muscle
strength, and muscle endurance by performing multiple linear regression analyses. After adjusting for
age and gender, coenzyme Q10 status was still positively correlated with muscle mass, muscle strength,
and muscle endurance (data not shown, p < 0.05). The physiological function of coenzyme Q10 is not
only to act as an antioxidant, but also to participate in energy production [11]. In this study, we detected
a positive correlation between coenzyme Q10 status and antioxidant capacity, particularly in the OA
group (Figure 1). As OA patients’ coenzyme Q10 levels went up, they seemed to exhibit a better muscle
mass status or muscle performance (Figures 2 and 3). OA is an age- and oxidative-related disease that
may contribute to mitochondrial dysfunction [3]. Using mitochondria-targeted antioxidants such as
coenzyme Q10 to increase antioxidant capacity may be able to attenuate the progression of OA [39]
and further exert beneficial effects on muscle mass and physical performance.
The current paradigm of OA has changed from the concept of a “wear and tear” disease to an
inflammation-mediated disease [40]. Coenzyme Q10 has been demonstrated to play a role in OA
pathogenesis via pain suppression and cartilage degeneration by inhibiting inflammatory mediators [41].
Although we did not find a relationship between coenzyme Q10 status and inflammation in these
OA patients, this might be because our subjects were outpatients who had a stable status. Elderly
patients with OA should pay attention their inflammatory status due to their higher level of hs-CRP
than middle-aged patients (Table 2).
5. Conclusions
In conclusion, patients with OA and elderly subjects suffered from coenzyme Q10 deficiency.
Since coenzyme Q10 status was significantly positively associated with antioxidant capacity, muscle
mass, muscle strength, and muscle endurance in the present study, we suggest that OA and elderly
patients fortify their coenzyme Q10 status, which may benefit their muscle function. Further intervention
studies should confirm the causal effects of coenzyme Q10 supplementation on antioxidant capacity
and muscle function in patients with OA. Increasing research interest has been focused on myokines
such as irisin and myostatin, which may relate to regulate muscle protein synthesis [42,43];
therefore, further study should explore how coenzyme Q10 involved in muscle synthesis.
Author Contributions: P.-S.C. and C.-H.Y. performed the study and recruited the subjects. P.-S.C. performed
the data analyses. C.-J.C. and Y.-Y.H. helped perform the study and analyzed sample. P.-T.L. conceived the
study, participated in its design, and coordinated the study. P.-S.C., C.-H.Y., and P.-T.L. drafted the manuscript.
All authors read and approved the final manuscript.
Funding: This study was supported by a grant from the Ministry of Science and Technology, Taiwan (MOST 1072320-B-040-011).
Antioxidants 2020, 9, 1275
14 of 16
Acknowledgments: We would like to express our sincere appreciation to the subjects for their participation.
Conflicts of Interest: The authors declare no conflict of interest.
Abbreviations
ASMI
BMI
BUN
GOT
GPT
HPLC
Hs-CRP
K/L
MDA
OA
RBC
ROS
SPPB
TAC
TC
WSMI
appendicular skeletal muscle mass index
body mass index
blood urea nitrogen
glutamic oxaloacetic transaminase
glutamic pyruvic transaminase
high-performance liquid chromatography
high-sensitivity C-reactive protein
Kellgren and Lawrence
Malondialdehyde
Osteoarthritis
red blood cell
reactive oxygen species
short physical performance battery
Total antioxidant capacity
total cholesterol
whole skeletal muscle mass index
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