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Association of knee osteoarthritis grade with one-leg standing balance and quadriceps strength in male independent ambulators aged ≥80 years
Journal of Orthopaedics 21 (2020) 79–83
Contents lists available at ScienceDirect
Journal of Orthopaedics journal homepage: www.elsevier.com/locate/jor
Association of knee osteoarthritis grade with one-leg standing balance and quadriceps strength in male independent ambulators aged ≥80 years
T
Yoshinori Ishiia,∗, Hideo Noguchia, Junko Satoa, Hana Ishiib, Ryo Ishiic, Shin-ichi Toyabed a
Ishii Orthopaedic & Rehabilitation Clinic, 1089 Shimo-Oshi, Gyoda, Saitama, 361-0037, Japan Kanazawa Medical University, School of Plastic Surgery, 1-1 Daigaku Uchinada, Ishikawa, 920-0253, Japan c Sado General Hospital, 161 Chikusa Sado, Niigata, 952-1209, Japan d Niigata University Crisis Management Office, Niigata University Hospital, Niigata University Graduate School of Medical and Dental Sciences, 1 Asahimachi Dori Niigata, Niigata, 951-8520, Japan b
A R T I C LE I N FO
A B S T R A C T
Keywords: One-leg-standing balance Quadriceps strength Kellgren–lawrence grade Knee osteoarthritis
Background: One-leg standing (OLS) balance is an important predictor of falls in people of advanced age. In this population, muscle weakness and knee osteoarthritis also contribute to falls and resultant fractures and thereby affect mortality rates. The Kellgren–Lawrence (KL) classification is widely used in the radiographic evaluation of knee osteoarthritis. This study was performed to evaluate OLS balance and the quadriceps strength (QS) for each KL grade and to clarify the impact of the knee osteoarthritis grade on OLS balance and QS. Hypothesis: OLS balance shows results compatible with those of previous reports when independent walking is possible because of maintenance of QS regardless of the OA grade. Methods: This single-center prospective cross-sectional study included data on 106 male orthopedic patients (106 knees) aged ≥80 years who could walk independently. OLS balance with eyes open was assessed using the patient's preferred leg. A handheld dynamometer was used to measure QS. The ratio of muscle strength to body weight (QS/BW ratio) was used to evaluate outcomes. Weight-bearing standing knee radiographs were evaluated using the KL classification. OLS balance and the QS/BW ratio were evaluated for each KL grade, and the correlations of the KL grade with OLS balance and the QS/BW ratio were assessed simultaneously. Results: For each KL grade, the number of participants (n), median OLS balance (seconds), and QS/BW ratio (N/ kg) were as follows: grade I: 24, 12, and 4.9; grade II: 51, 14, and 5.2; grade III: 22, 14, and 4.9; and grade IV: 9, 26, and 5.7, respectively. There were no significant differences in either OLS balance or the QS/BW ratio among the four grades. Conclusions: Participants exhibited good OLS balance and QS/BW ratio regardless of their KL grade. This study demonstrated an absence of correlations of the KL grade with OLS balance and the QS/BW ratio, as was previously reported for the KL grade and pain. Level of evidence: Level II prospective study.
1. Introduction A fall is the most significant risk factor for hip fracture, and 90% of fractures are associated with a fall.1 Hip fracture leads to the deterioration of walking ability, which is associated with cognitive impairment2 and reflects the survival rate of older people.3 Therefore, prevention of falls in the advanced-age population is an urgent issue that must be addressed to expand the healthy life span (the period during which there is no restriction on daily life caused by mobility limitations) of older people. One-leg standing (OLS) balance is an
important predictor of injurious falls in older persons.4 In addition, a systematic review demonstrated that OLS can also be a predictive tool for frailty among community-dwelling older adult populations.5 Besides OLS balance, quadriceps strength (QS) was recently reported to be highly correlated with walking ability in both native6 and artificial7 knee joints. In addition, QS is reported to be a discriminant predictor of dependence in daily activities in nursing home residents (mean age of 85.6 ± 7.1 years).8 To the best of our knowledge, however, no such study has focused on people of advanced age. One study of active postmenopausal women reported a correlation between
∗
Corresponding author. Ishii Orthopaedic and Rehabilitation Clinic, 1089 Shimo-Oshi, Gyoda, Saitama, 361-0037, Japan. E-mail addresses: [email protected] (Y. Ishii), [email protected] (J. Sato), [email protected] (H. Ishii), [email protected] (R. Ishii), [email protected] (S.-i. Toyabe). https://doi.org/10.1016/j.jor.2020.03.013 Received 14 February 2020; Accepted 23 March 2020 Available online 24 March 2020 0972-978X/ © 2020 Published by Elsevier B.V. on behalf of Professor P K Surendran Memorial Education Foundation.
Journal of Orthopaedics 21 (2020) 79–83
Y. Ishii, et al.
Fig. 1. Measurement of quadriceps strength using the Locomo Scan. With the knee positioned over the force sensor at 20° of flexion, the participant extended the knee with maximum force. The load pressure applied to the sensor was measured and displayed as the isometric knee extension quadriceps strength.
QS and OLS balance.9 Knee osteoarthritis (OA) is a major public health issue causing disability of advanced-age people in most developed countries.10,11 It is characterized by pathological features including joint space narrowing and the presence or absence of osteophytes and is graded by the Kellgren–Lawrence (KL) classification,12 which has been widely used as a research tool in epidemiological studies of knee OA.11,13,14 In addition, previous studies have focused on the associations of clinical symptoms such as muscle strength around the knee13–17 and knee pain11,18,19 with each KL grade. However, among these studies, there is no consensus on the association of the KL grade with muscle strength and knee pain in patients with knee OA. Currently, only 11 countries have an average male life expectancy of ≥80 years; this is much fewer than the number of countries with such a female life expectancy.20 Analyses of OLS balance in men aged > 80 years who can walk independently may help to provide target values to facilitate the maintenance of independent walking in older adults who have not yet reached the age of 80 years. Furthermore, considering the significant correlation between walking level and mortality,3 achieving or exceeding these values may expand these men's healthy life span and increase their life expectancy to approach that of women because of fall prevention. To the best of our knowledge, however, no reports have focused on men aged > 80 years with various KL grades who can walk independently. Previous reports were mainly focused on communitydwelling older adults in variously functioning cohorts.5,21 Therefore, this study was performed to compare OLS balance in men aged ≥80 years who can walk independently and the association with QS and the knee OA grade as influencing factors with those of previous studies. The hypothesis of this study was that OLS balance shows results compatible with those of previous reports when independent walking is possible because of maintenance of QS regardless of the OA grade.
was 24 (22, 25) kg/m2. All 106 patients received diagnoses of degenerative joint and/or cartilage disease. More specifically, the diagnoses were spine-related for 51 patients, upper limb-related for 14 patients, lower limb-related for 39 patients, and related to other areas for 2 patients. All participants were men aged ≥80 years who were able to walk independently with or without a T-cane but without support from other people. That is, all participants had no restrictions on daily life caused by mobility limitations. The exclusion criteria were neurological abnormalities, such as motor paralysis; cognitive or mental dysfunction requiring medication; and skeletal dysfunction that had a negative impact on walking. This study was conducted based on the guidelines laid down in the Helsinki Declaration and in the ethical guidelines of our institution. This research has been approved by the IRB of the authors. All patients provided written informed consent for participation.
3. Measurements 3.1. Physical performance measure: OLS body balance The OLS balance with eyes open was assessed using the participant's preferred leg. The participants were asked to place their hands on their waists while staring at a mark on the wall, raise one leg, and stand for as long as possible. They were timed until they lost their balance or reached the maximum time of 60 s. The participants performed two trials, and the longer time (to the nearest 0.1 s) was used in the analysis.
3.2. Muscle strength measure: QS To assess QS, the isometric knee extension muscle strength in Newtons was measured with the knee at approximately 20° of flexion using a Locomo Scan dynamometer (Alcare Corp., Tokyo, Japan), following a standard protocol13 (Fig. 1). The correlation between the maximum measured value using this arthrometer and the value obtained using the Biodex System 3 (Biodex Medical Systems Inc., Shirley, NY, USA) was r = 0.69 (p < 0.01) for the first measurement and r = 0.82 (p < 0.01) for the second measurement conducted 1 week later. Moreover, a good correlation (r = 0.92, p < 0.01) was observed between the first and second measurements obtained using the Locomo Scan arthrometer.13 The QS was measured twice, and the highest value on each side was used in the analysis. These values were divided by BW to eliminate the effect of physique. These QS values normalized by BW (i.e., the QS/BW ratio in N/kg) were used in the analysis.
2. Methods 2.1. Participants This prospective cross-sectional study was conducted from September 2018 to August 2019. The study included data on 106 Japanese men (106 knees) who visited an orthopedic specialty outpatient clinic (median age, 83 years; 25th percentile, 81 years; 75th percentile, 86 years; range, 80–94 years). Their median (25th percentile, 75th percentile) body weight (BW) was 59 (56, 66) kg, and their median height was 159 (156, 164) cm. Their median body mass index 80
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Y. Ishii, et al.
Additionally, OLS balance is reportedly an important predictor of injurious falls4 and a predictive tool for frailty in the older population.5 For individuals aged > 75 years, Seichi et al. [27] proposed a cutoff of 6 s for the average OLS balance time to screen older adults for medical interventions or training programs. Seino et al.21 reported mean OLS balance values of 26.0 s for those aged 80–84 years and 21.9 s for those aged ≥85 years. Even for individuals in their 80s, the deterioration of OLS balance with aging is consistent with our results. Harato et al.23 reported a mean OLS balance of 8.7 s among patients with KL grade IV knee OA12 before total knee arthroplasty (TKA). OLS balance clearly showed a non-normal distribution by the Kolmogorov–Smirnov test and in the histogram in this study. For this reason, we used the median, 25th percentile, and 75th percentile. However, the mean and standard deviation (SD) for OLS balance were used as representative values in previous reports [21,23,27]. When OLS balance was expressed as mean (SD) for comparison with our data, the mean (SD) OLS balance in each KL grade (I–IV) was 21 (21), 24 (23), 21 (19), and 26 (27) seconds, respectively, which are equivalent to previous reports [21,23,27]. Taking these results into account, the participants in the present study can be considered to have maintained relatively good OLS balance and to be at low risk of falls. Both QS and knee OA severity were reported as factors that influence OLS balance [28–30]. QS reportedly declines with aging [21,25], which is consistent with our results. The decline of QS may lead to poor OLS because the quadriceps muscles function to maintain the upright stance [29,30]. The significant positive correlation between OLS balance and the QS/BW ratio in this study may confirm the association of poor OLS balance and a decline in the QS/BW ratio. A few previous studies [24,25] have evaluated QS using the same arthrometer used in the present study. Ishii et al.24 reported that the median QS/BW ratio was 3.3 N/kg for patients who had undergone posterior cruciate ligament-retaining TKA, 3.4 N/kg for patients who had undergone posterior cruciate ligament-substituting TKA (median age, 81 years), and 4.6 N/kg for controls (median age, 83 years). In another study of Japanese men aged 80–89 years (n = 86), the median QS/BW ratio was 5.9 N/kg.25 The values found in the present study were compatible with these previous findings. We believe that the index QS/BW ratio reported in the present study can be used as a target for adults aged < 80 years to maintain independent walking ability as they age. Conversely, the impact of the severity of knee OA on OLS balance is inconclusive. Birmingham et al. [28] found a significant deterioration of OLS balance with increasing radiographic severity. Meanwhile, Hunt et al. [30] reported that participants with more severe structural degeneration or reports of bilateral symptoms exhibited better OLS balance. Additionally, in their systematic review and meta-analysis, Hatfield et al. [26] identified no studies that compared balance among different radiographic disease severities of knee OA and found very little research comparing balance in different subpopulations of knee OA. The current study showed no correlations between the severity of knee OA using the KL grade and body balance evaluated by OLS when participants were aged ≥80 years and could walk unaided. We speculate that the abundant amount of mobility associated with independent walking regardless of the KL grade might result in a good QS/BW ratio. As a result, the OLS balance is maintained. The positive correlation between OLS balance and the QS/BW ratio in this study might support this speculation. This study had several limitations. First, all patients who took part in this study had some type of skeletal dysfunction that induced pain due to degenerative joints and/or cartilage. However, because they did not need the support of others to ambulate, the impact of their diseases on their OLS balance and QS/BW measures seemed to be small or negligible. Additionally, discordances have been reported between the severity of knee OA and the degree of pain.15,16 Second, the total number of participants was less than that in previous reports on community-dwelling individuals.21 However, the number of men aged ≥80 years seems adequate for evaluation of physical performance compared
3.3. Radiographic assessment All participants underwent a Rosenberg-view anteroposterior radiographic examination of their knees during weight bearing.22 The KL grade was defined using the KL radiographic atlas for overall knee radiographic grades.12 Radiographs were scored from KL grade I to IV, with higher grades being associated with more severe OA. Each grade was defined using anteroposterior radiographs as follows: grade I, doubtful narrowing of the joint space with possible osteophyte formation; grade II, possible narrowing of the joint space with definite osteophyte formation; grade III, definite narrowing of the joint space, moderate osteophyte formation, some sclerosis, and possible deformity of bone ends; and grade IV, large osteophyte formation, severe narrowing of the joint space with marked sclerosis, and definite deformity of bone ends. To evaluate the intraobserver variability of KL grading, 100 randomly selected knee radiographs were scored by the same observer (Y.I.) more than 1 month after the first reading. Kappa analysis confirmed that the intraobserver variability evaluated for the KL grade (I to IV) was sufficient for assessment (k = 0.894). OLS balance and the QS/BW ratio for men aged ≥80 years who could walk independently were measured for each KL grade, and the correlations of the KL grade of the participant's preferred leg with OLS balance and the QS/BW ratio were evaluated simultaneously. 4. Statistical analysis Data for some variables did not pass the Kolmogorov–Smirnov test. Spearman's rank correlation coefficient was used to investigate the association between any two variables. The strength of the correlation of the rank coefficients was defined as follows: strong = 0.70–1.00, moderate = 0.40–0.69, or weak = 0.20–0.39. The effects of the KL grade on OLS balance and the QS/BW ratio were analyzed using the Kruskal–Wallis method. If necessary, Bonferroni's method was used to adjust for multiple comparisons between OLS balance and the QS/BW ratio at respective KL grades. In all tests, a p value of < 0.05 was considered statistically significant. A post hoc power analysis was performed to evaluate whether the data had sufficient verification power. The estimated power was 0.54, with an effect size of 0.25 and an alpha error of 0.05. All statistical analyses were performed using IBM SPSS Statistics, Version 23 (IBM Japan, Tokyo, Japan). All values are presented as median (25th percentile, 75th percentile). 5. Results Among all participants, the OLS was 14 (5, 40) (range, 1–60) seconds and the QS/BW ratio was 5.1 (4.0, 6.0) (range, 1.4–10.9) N/kg. OLS balance and the QS/BW ratio showed a significant positive correlation (r = 0.237, p = 0.015). Negative correlations were found between age and OLS balance (r = −0.366, p < 0.001) and between age and the QS/BW ratio (r = −0.262, p = 0.007). The numbers of participants with each KL grade were as follows: grade I, 24; grade II, 51; grade III, 22; and grade IV, 9. There were no differences among the grades for either OLS balance (p = 0.971) or weight-adjusted QS (p = 0.576) (Table 1). 6. Discussion The most important finding of this study is that all participants (men aged ≥80 years who could walk independently) showed OLS balance and QS values comparable with those in previous studies [21,23–25] regardless of the KL grade. Maintenance of mobility (independent walking) in people of advanced age seems to be important for extension of their healthy life span because it helps to prevent falls through adequate QS and thus good OLS balance. OLS balance is affected by variables such as QS, severity of radiographic knee OA, knee alignment, pain, and joint position acuity [26]. 81
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Y. Ishii, et al.
Table 1 Participants’ background characteristics and results of OLS balance and QS/BW ratio in each KL grade. KL(N)
I (24)
II (51)
III (22)
IV (9)
Age (year) Body length (cm) Body weight (kg) Body Mass Index (kg/cm2) OLS Median [25%, 75%] QS/BW Median [25%, 75%]
82 [81,85] 158 [155,162] 57 [56,62] 23 [22,25]
83 [81,86] 160 [156,164] 59 [54,66] 23 [21,25]
84 [82,86] 158 [156,163] 61 [58,64] 24 [23,26]
84 [82,85] 157 [151,159] 64 [56,69] 26 [24,28]
12[5,26]
14[5,45]
14[7,25]
14[4,60]
4.9[3.2, 6.2]
5.2 [4.0, 6.2]
4.9 [4.1, 5.9]
5.6 [5.1, 5.7]
N, number; OLS, one-leg standing; QS, quadriceps strength; BW, body weight; KL, Kellgren–Lawrence. No differences in either OLS balance or the QS/BW ratio were found among the KL grades according to the Kruskal–Wallis test (p = 0.971 for OLS and p = 0.576 for QS/BW ratio).
Ethical review committee statement
with previous studies of the number of participants [5,25,27]. Third, we did not consider other factors that may impact the OLS balance and QS measures, such as age, sex, or race. Finally, this was a single-center study, which may limit the generalizability of the results. Verification of the validity of these results at multiple facilities is expected in the future. Despite these limitations, this is a valuable study that provides reference values for an aspect of physical performance (OLS balance) and body composition (QS/BW ratio) derived from 106 men aged ≥80 years who could walk independently, unlike previous epidemiological surveys of community-dwelling individuals with various walking levels. The reference ranges found in the present study can be used as the target values for walking independently among older adults aged < 80 years or their health care providers. In addition, our research showed that in men aged ≥80 years who can walk independently, radiographic OA assessment does not necessarily impact OLS balance or the QS/BW ratio, similar to previous reports of the discordance between radiographic knee OA and pain.18,19 In conclusion, independent walking among advanced-age men (age of ≥80 years) helps to maintain OLS balance and the QS/BW ratio regardless of the OA grade as determined by the KL classification. Thus, falls among this population are expected to be prevented by good OLS balance and a good QS/BW ratio. Verification of the validity of these findings at multiple facilities and among women is expected in the future.
The local institutional review board approved this study. All patients provided informed consent. Declaration of competing interest The authors declare that they have no competing interests. Acknowledgment We would like to thank all the rehabilitation staff, all the interviewers, and most sincerely all the participating patients who visited our outpatient clinic. References 1. Grisso JA, Kelsey JL, Strom BL, et al. Risk factors for hip fracture in black women. The northeast hip fracture study group. N Engl J Med. 1994;330:1555–1559. 2. Matsueda M, Ishii Y. The relationship between dementia score and ambulatory level after hip fracture in the elderly. Am J Orthoped. 2000;29:691–693. 3. Imura K, Ishii Y, Yagisawa K, Matsueda M. Postoperative ambulatory level after hip fracture in the elderly predicts survival rate. Arch Orthop Trauma Surg. 2000;120:369–371. 4. Vellas BJ, Wayne SJ, Romero L, Baumgartner RN, Rubenstein LZ, Garry PJ. One-leg balance is an important predictor of injurious falls in older persons. J Am Geriatr Soc. 1997;45:735–738. 5. Michikawa T, Nishiwaki Y, Takebayashi T, Toyama Y. One-leg standing test for elderly populations. J Orthop Sci. 2009;14:675–685. 6. Morita Y, Ito H, Torii M, et al. Factors affecting walking ability in female patients with rheumatoid arthritis. PloS One. 2018;13:e0195059. 7. Furu M, Ito H, Nishikawa T, et al. Quadriceps strength affects patient satisfaction after total knee arthroplasty. J Orthop Sci. 2016;21:38–43. 8. Wearing J, Stokes M, de Bruin ED. Quadriceps muscle strength is a discriminant predictor of dependence in daily activities in nursing home residents. PloS One. 2019;14:e0223016. 9. Dulac MC, Carvalho LP, Aubertin-Leheudre M. Functional capacity depends on lower limb muscle strength rather than on abdominal obesity in active postmenopausal women. Menopause. 2018;25:176–181. 10. Kellgren JH, Lawrence JS. Radiographical assessment of osteoarthritis. Ann Rheum Dis. 1957;16:494–502. 11. Muraki S, Oka H, Akune T, et al. Prevalence of radiographic knee osteoarthritis and its association with knee pain in the elderly of Japanese population-based cohorts: the ROAD study. Osteoarthritis Cartilage. 2009;17:1137–1143. 12. Omori G, Koga Y, Tanaka M, et al. Quadriceps muscle strength and its relationship to radiographic knee osteoarthritis in Japanese elderly. J Orthop Sci. 2013;18:536–542. 13. Dell'isola A, Wirth W, Steultjens M, Eckstein F, Culvenor AG. Knee extensor muscle weakness and radiographic knee osteoarthritis progression. Acta Orthop. 2018;89:406–411. 14. Bedson J, Croft PR. The discordance between clinical and radiographic knee osteoarthritis: a systematic search and summary of the literature. BMC Muscoskel Disord. 2008;9:116. 15. Schiphof D, Kerkhof HJ, Damen J, et al. Factors for pain in patients with different grades of knee osteoarthritis. Arthritis Care Res (Hoboken). 2013;65:695–702. 16. Ministry of Health. Labour and welfare of Japan. https://www.mhlw.go.jp/index. html. 17. Seino S, Shinkai S, Fujiwara Y, et al. TMIG-LISA Research Group. Reference values and age and sex differences in physical performance measures for communitydwelling older Japanese: a pooled analysis of six cohort studies. PloS One. 2014;9:e99487.
Consent for publication Not applicable. Availability of data and materials The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request. Funding This work was partially supported by the Japanese Clinical Orthopedic Association under Grant 2019. The funder played no role in the design, methods, subject recruitment, data collection, analysis or preparation of the paper. Authors’ contributions YI contributed to the study conception and design, drafted the article, and ensured the accuracy of the data and analysis. HN and JS contributed to the study conception and design and to the analysis and interpretation of the data. HI and RI contributed to the data collection. ST provided statistical expertise and contributed to ensuring the accuracy of the data and analysis. All authors approved the final manuscript. 82
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22. Hatfield GL, Morrison A, Wenman M, Hammond CA, Hunt MA. Clinical tests of standing balance in the knee osteoarthritis population: systematic review and metaanalysis. Phys Ther. 2016;96(3):324–337. 23. Seichi A, Hoshino Y, Doi T, et al. Determination of the optimal cutoff time to use when screening elderly people for locomotive syndrome using the one-leg standing test (with eyes open). J Orthop Sci. 2014;19(4):620–626. 24. Birmingham T, Kramer J, Kirkley A, Inglis J, Spaulding S, Vandervoort A. Association among neuromuscular and anatomic measures for patients with knee osteoarthritis. Arch Phys Med Rehabil. 2001;82:1115–1118. 25. Hunt MA, McManus FJ, Hinman RS, Bennell KL. Predictors of single-leg standing balance in individuals with medial knee osteoarthritis. Arthritis Care Res. 2010;62:496–500.
18. Rosenberg TD, Paulos LE, Parker RD, Coward DB, Scott SM. The forty-five-degree posteroanterior flexion weight-bearing radiograph of the knee. J Bone Joint Surg Am. 1988;70:1479–1483. 19. Harato K, Kobayashi S, Kojima I, Sakurai A, Tanikawa H, Niki Y. Factors affecting one-leg standing time in patients with end-stage knee osteoarthritis and the agerelated recovery process following total knee arthroplasty. J Orthop Surg Res. 2017;12(1):21. 20. Ishii Y, Noguchi H, Sato J, Sakurai T, Toyabe SI. Quadriceps strength impairment in the mid- to long-term follow-up period after TKA. Knee Surg Sports Traumatol Arthrosc. 2017;25(11):3372–3377. 21. Narumi K, Funaki Y, Yoshimura N, et al. Quadriceps muscle strength reference value as index for functional deterioration of locomotive organs: data from 3617 men and women in Japan. J Orthop Sci. 2017;22(4):765–770.
83
Contents lists available at ScienceDirect
Journal of Orthopaedics journal homepage: www.elsevier.com/locate/jor
Association of knee osteoarthritis grade with one-leg standing balance and quadriceps strength in male independent ambulators aged ≥80 years
T
Yoshinori Ishiia,∗, Hideo Noguchia, Junko Satoa, Hana Ishiib, Ryo Ishiic, Shin-ichi Toyabed a
Ishii Orthopaedic & Rehabilitation Clinic, 1089 Shimo-Oshi, Gyoda, Saitama, 361-0037, Japan Kanazawa Medical University, School of Plastic Surgery, 1-1 Daigaku Uchinada, Ishikawa, 920-0253, Japan c Sado General Hospital, 161 Chikusa Sado, Niigata, 952-1209, Japan d Niigata University Crisis Management Office, Niigata University Hospital, Niigata University Graduate School of Medical and Dental Sciences, 1 Asahimachi Dori Niigata, Niigata, 951-8520, Japan b
A R T I C LE I N FO
A B S T R A C T
Keywords: One-leg-standing balance Quadriceps strength Kellgren–lawrence grade Knee osteoarthritis
Background: One-leg standing (OLS) balance is an important predictor of falls in people of advanced age. In this population, muscle weakness and knee osteoarthritis also contribute to falls and resultant fractures and thereby affect mortality rates. The Kellgren–Lawrence (KL) classification is widely used in the radiographic evaluation of knee osteoarthritis. This study was performed to evaluate OLS balance and the quadriceps strength (QS) for each KL grade and to clarify the impact of the knee osteoarthritis grade on OLS balance and QS. Hypothesis: OLS balance shows results compatible with those of previous reports when independent walking is possible because of maintenance of QS regardless of the OA grade. Methods: This single-center prospective cross-sectional study included data on 106 male orthopedic patients (106 knees) aged ≥80 years who could walk independently. OLS balance with eyes open was assessed using the patient's preferred leg. A handheld dynamometer was used to measure QS. The ratio of muscle strength to body weight (QS/BW ratio) was used to evaluate outcomes. Weight-bearing standing knee radiographs were evaluated using the KL classification. OLS balance and the QS/BW ratio were evaluated for each KL grade, and the correlations of the KL grade with OLS balance and the QS/BW ratio were assessed simultaneously. Results: For each KL grade, the number of participants (n), median OLS balance (seconds), and QS/BW ratio (N/ kg) were as follows: grade I: 24, 12, and 4.9; grade II: 51, 14, and 5.2; grade III: 22, 14, and 4.9; and grade IV: 9, 26, and 5.7, respectively. There were no significant differences in either OLS balance or the QS/BW ratio among the four grades. Conclusions: Participants exhibited good OLS balance and QS/BW ratio regardless of their KL grade. This study demonstrated an absence of correlations of the KL grade with OLS balance and the QS/BW ratio, as was previously reported for the KL grade and pain. Level of evidence: Level II prospective study.
1. Introduction A fall is the most significant risk factor for hip fracture, and 90% of fractures are associated with a fall.1 Hip fracture leads to the deterioration of walking ability, which is associated with cognitive impairment2 and reflects the survival rate of older people.3 Therefore, prevention of falls in the advanced-age population is an urgent issue that must be addressed to expand the healthy life span (the period during which there is no restriction on daily life caused by mobility limitations) of older people. One-leg standing (OLS) balance is an
important predictor of injurious falls in older persons.4 In addition, a systematic review demonstrated that OLS can also be a predictive tool for frailty among community-dwelling older adult populations.5 Besides OLS balance, quadriceps strength (QS) was recently reported to be highly correlated with walking ability in both native6 and artificial7 knee joints. In addition, QS is reported to be a discriminant predictor of dependence in daily activities in nursing home residents (mean age of 85.6 ± 7.1 years).8 To the best of our knowledge, however, no such study has focused on people of advanced age. One study of active postmenopausal women reported a correlation between
∗
Corresponding author. Ishii Orthopaedic and Rehabilitation Clinic, 1089 Shimo-Oshi, Gyoda, Saitama, 361-0037, Japan. E-mail addresses: [email protected] (Y. Ishii), [email protected] (J. Sato), [email protected] (H. Ishii), [email protected] (R. Ishii), [email protected] (S.-i. Toyabe). https://doi.org/10.1016/j.jor.2020.03.013 Received 14 February 2020; Accepted 23 March 2020 Available online 24 March 2020 0972-978X/ © 2020 Published by Elsevier B.V. on behalf of Professor P K Surendran Memorial Education Foundation.
Journal of Orthopaedics 21 (2020) 79–83
Y. Ishii, et al.
Fig. 1. Measurement of quadriceps strength using the Locomo Scan. With the knee positioned over the force sensor at 20° of flexion, the participant extended the knee with maximum force. The load pressure applied to the sensor was measured and displayed as the isometric knee extension quadriceps strength.
QS and OLS balance.9 Knee osteoarthritis (OA) is a major public health issue causing disability of advanced-age people in most developed countries.10,11 It is characterized by pathological features including joint space narrowing and the presence or absence of osteophytes and is graded by the Kellgren–Lawrence (KL) classification,12 which has been widely used as a research tool in epidemiological studies of knee OA.11,13,14 In addition, previous studies have focused on the associations of clinical symptoms such as muscle strength around the knee13–17 and knee pain11,18,19 with each KL grade. However, among these studies, there is no consensus on the association of the KL grade with muscle strength and knee pain in patients with knee OA. Currently, only 11 countries have an average male life expectancy of ≥80 years; this is much fewer than the number of countries with such a female life expectancy.20 Analyses of OLS balance in men aged > 80 years who can walk independently may help to provide target values to facilitate the maintenance of independent walking in older adults who have not yet reached the age of 80 years. Furthermore, considering the significant correlation between walking level and mortality,3 achieving or exceeding these values may expand these men's healthy life span and increase their life expectancy to approach that of women because of fall prevention. To the best of our knowledge, however, no reports have focused on men aged > 80 years with various KL grades who can walk independently. Previous reports were mainly focused on communitydwelling older adults in variously functioning cohorts.5,21 Therefore, this study was performed to compare OLS balance in men aged ≥80 years who can walk independently and the association with QS and the knee OA grade as influencing factors with those of previous studies. The hypothesis of this study was that OLS balance shows results compatible with those of previous reports when independent walking is possible because of maintenance of QS regardless of the OA grade.
was 24 (22, 25) kg/m2. All 106 patients received diagnoses of degenerative joint and/or cartilage disease. More specifically, the diagnoses were spine-related for 51 patients, upper limb-related for 14 patients, lower limb-related for 39 patients, and related to other areas for 2 patients. All participants were men aged ≥80 years who were able to walk independently with or without a T-cane but without support from other people. That is, all participants had no restrictions on daily life caused by mobility limitations. The exclusion criteria were neurological abnormalities, such as motor paralysis; cognitive or mental dysfunction requiring medication; and skeletal dysfunction that had a negative impact on walking. This study was conducted based on the guidelines laid down in the Helsinki Declaration and in the ethical guidelines of our institution. This research has been approved by the IRB of the authors. All patients provided written informed consent for participation.
3. Measurements 3.1. Physical performance measure: OLS body balance The OLS balance with eyes open was assessed using the participant's preferred leg. The participants were asked to place their hands on their waists while staring at a mark on the wall, raise one leg, and stand for as long as possible. They were timed until they lost their balance or reached the maximum time of 60 s. The participants performed two trials, and the longer time (to the nearest 0.1 s) was used in the analysis.
3.2. Muscle strength measure: QS To assess QS, the isometric knee extension muscle strength in Newtons was measured with the knee at approximately 20° of flexion using a Locomo Scan dynamometer (Alcare Corp., Tokyo, Japan), following a standard protocol13 (Fig. 1). The correlation between the maximum measured value using this arthrometer and the value obtained using the Biodex System 3 (Biodex Medical Systems Inc., Shirley, NY, USA) was r = 0.69 (p < 0.01) for the first measurement and r = 0.82 (p < 0.01) for the second measurement conducted 1 week later. Moreover, a good correlation (r = 0.92, p < 0.01) was observed between the first and second measurements obtained using the Locomo Scan arthrometer.13 The QS was measured twice, and the highest value on each side was used in the analysis. These values were divided by BW to eliminate the effect of physique. These QS values normalized by BW (i.e., the QS/BW ratio in N/kg) were used in the analysis.
2. Methods 2.1. Participants This prospective cross-sectional study was conducted from September 2018 to August 2019. The study included data on 106 Japanese men (106 knees) who visited an orthopedic specialty outpatient clinic (median age, 83 years; 25th percentile, 81 years; 75th percentile, 86 years; range, 80–94 years). Their median (25th percentile, 75th percentile) body weight (BW) was 59 (56, 66) kg, and their median height was 159 (156, 164) cm. Their median body mass index 80
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Additionally, OLS balance is reportedly an important predictor of injurious falls4 and a predictive tool for frailty in the older population.5 For individuals aged > 75 years, Seichi et al. [27] proposed a cutoff of 6 s for the average OLS balance time to screen older adults for medical interventions or training programs. Seino et al.21 reported mean OLS balance values of 26.0 s for those aged 80–84 years and 21.9 s for those aged ≥85 years. Even for individuals in their 80s, the deterioration of OLS balance with aging is consistent with our results. Harato et al.23 reported a mean OLS balance of 8.7 s among patients with KL grade IV knee OA12 before total knee arthroplasty (TKA). OLS balance clearly showed a non-normal distribution by the Kolmogorov–Smirnov test and in the histogram in this study. For this reason, we used the median, 25th percentile, and 75th percentile. However, the mean and standard deviation (SD) for OLS balance were used as representative values in previous reports [21,23,27]. When OLS balance was expressed as mean (SD) for comparison with our data, the mean (SD) OLS balance in each KL grade (I–IV) was 21 (21), 24 (23), 21 (19), and 26 (27) seconds, respectively, which are equivalent to previous reports [21,23,27]. Taking these results into account, the participants in the present study can be considered to have maintained relatively good OLS balance and to be at low risk of falls. Both QS and knee OA severity were reported as factors that influence OLS balance [28–30]. QS reportedly declines with aging [21,25], which is consistent with our results. The decline of QS may lead to poor OLS because the quadriceps muscles function to maintain the upright stance [29,30]. The significant positive correlation between OLS balance and the QS/BW ratio in this study may confirm the association of poor OLS balance and a decline in the QS/BW ratio. A few previous studies [24,25] have evaluated QS using the same arthrometer used in the present study. Ishii et al.24 reported that the median QS/BW ratio was 3.3 N/kg for patients who had undergone posterior cruciate ligament-retaining TKA, 3.4 N/kg for patients who had undergone posterior cruciate ligament-substituting TKA (median age, 81 years), and 4.6 N/kg for controls (median age, 83 years). In another study of Japanese men aged 80–89 years (n = 86), the median QS/BW ratio was 5.9 N/kg.25 The values found in the present study were compatible with these previous findings. We believe that the index QS/BW ratio reported in the present study can be used as a target for adults aged < 80 years to maintain independent walking ability as they age. Conversely, the impact of the severity of knee OA on OLS balance is inconclusive. Birmingham et al. [28] found a significant deterioration of OLS balance with increasing radiographic severity. Meanwhile, Hunt et al. [30] reported that participants with more severe structural degeneration or reports of bilateral symptoms exhibited better OLS balance. Additionally, in their systematic review and meta-analysis, Hatfield et al. [26] identified no studies that compared balance among different radiographic disease severities of knee OA and found very little research comparing balance in different subpopulations of knee OA. The current study showed no correlations between the severity of knee OA using the KL grade and body balance evaluated by OLS when participants were aged ≥80 years and could walk unaided. We speculate that the abundant amount of mobility associated with independent walking regardless of the KL grade might result in a good QS/BW ratio. As a result, the OLS balance is maintained. The positive correlation between OLS balance and the QS/BW ratio in this study might support this speculation. This study had several limitations. First, all patients who took part in this study had some type of skeletal dysfunction that induced pain due to degenerative joints and/or cartilage. However, because they did not need the support of others to ambulate, the impact of their diseases on their OLS balance and QS/BW measures seemed to be small or negligible. Additionally, discordances have been reported between the severity of knee OA and the degree of pain.15,16 Second, the total number of participants was less than that in previous reports on community-dwelling individuals.21 However, the number of men aged ≥80 years seems adequate for evaluation of physical performance compared
3.3. Radiographic assessment All participants underwent a Rosenberg-view anteroposterior radiographic examination of their knees during weight bearing.22 The KL grade was defined using the KL radiographic atlas for overall knee radiographic grades.12 Radiographs were scored from KL grade I to IV, with higher grades being associated with more severe OA. Each grade was defined using anteroposterior radiographs as follows: grade I, doubtful narrowing of the joint space with possible osteophyte formation; grade II, possible narrowing of the joint space with definite osteophyte formation; grade III, definite narrowing of the joint space, moderate osteophyte formation, some sclerosis, and possible deformity of bone ends; and grade IV, large osteophyte formation, severe narrowing of the joint space with marked sclerosis, and definite deformity of bone ends. To evaluate the intraobserver variability of KL grading, 100 randomly selected knee radiographs were scored by the same observer (Y.I.) more than 1 month after the first reading. Kappa analysis confirmed that the intraobserver variability evaluated for the KL grade (I to IV) was sufficient for assessment (k = 0.894). OLS balance and the QS/BW ratio for men aged ≥80 years who could walk independently were measured for each KL grade, and the correlations of the KL grade of the participant's preferred leg with OLS balance and the QS/BW ratio were evaluated simultaneously. 4. Statistical analysis Data for some variables did not pass the Kolmogorov–Smirnov test. Spearman's rank correlation coefficient was used to investigate the association between any two variables. The strength of the correlation of the rank coefficients was defined as follows: strong = 0.70–1.00, moderate = 0.40–0.69, or weak = 0.20–0.39. The effects of the KL grade on OLS balance and the QS/BW ratio were analyzed using the Kruskal–Wallis method. If necessary, Bonferroni's method was used to adjust for multiple comparisons between OLS balance and the QS/BW ratio at respective KL grades. In all tests, a p value of < 0.05 was considered statistically significant. A post hoc power analysis was performed to evaluate whether the data had sufficient verification power. The estimated power was 0.54, with an effect size of 0.25 and an alpha error of 0.05. All statistical analyses were performed using IBM SPSS Statistics, Version 23 (IBM Japan, Tokyo, Japan). All values are presented as median (25th percentile, 75th percentile). 5. Results Among all participants, the OLS was 14 (5, 40) (range, 1–60) seconds and the QS/BW ratio was 5.1 (4.0, 6.0) (range, 1.4–10.9) N/kg. OLS balance and the QS/BW ratio showed a significant positive correlation (r = 0.237, p = 0.015). Negative correlations were found between age and OLS balance (r = −0.366, p < 0.001) and between age and the QS/BW ratio (r = −0.262, p = 0.007). The numbers of participants with each KL grade were as follows: grade I, 24; grade II, 51; grade III, 22; and grade IV, 9. There were no differences among the grades for either OLS balance (p = 0.971) or weight-adjusted QS (p = 0.576) (Table 1). 6. Discussion The most important finding of this study is that all participants (men aged ≥80 years who could walk independently) showed OLS balance and QS values comparable with those in previous studies [21,23–25] regardless of the KL grade. Maintenance of mobility (independent walking) in people of advanced age seems to be important for extension of their healthy life span because it helps to prevent falls through adequate QS and thus good OLS balance. OLS balance is affected by variables such as QS, severity of radiographic knee OA, knee alignment, pain, and joint position acuity [26]. 81
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Table 1 Participants’ background characteristics and results of OLS balance and QS/BW ratio in each KL grade. KL(N)
I (24)
II (51)
III (22)
IV (9)
Age (year) Body length (cm) Body weight (kg) Body Mass Index (kg/cm2) OLS Median [25%, 75%] QS/BW Median [25%, 75%]
82 [81,85] 158 [155,162] 57 [56,62] 23 [22,25]
83 [81,86] 160 [156,164] 59 [54,66] 23 [21,25]
84 [82,86] 158 [156,163] 61 [58,64] 24 [23,26]
84 [82,85] 157 [151,159] 64 [56,69] 26 [24,28]
12[5,26]
14[5,45]
14[7,25]
14[4,60]
4.9[3.2, 6.2]
5.2 [4.0, 6.2]
4.9 [4.1, 5.9]
5.6 [5.1, 5.7]
N, number; OLS, one-leg standing; QS, quadriceps strength; BW, body weight; KL, Kellgren–Lawrence. No differences in either OLS balance or the QS/BW ratio were found among the KL grades according to the Kruskal–Wallis test (p = 0.971 for OLS and p = 0.576 for QS/BW ratio).
Ethical review committee statement
with previous studies of the number of participants [5,25,27]. Third, we did not consider other factors that may impact the OLS balance and QS measures, such as age, sex, or race. Finally, this was a single-center study, which may limit the generalizability of the results. Verification of the validity of these results at multiple facilities is expected in the future. Despite these limitations, this is a valuable study that provides reference values for an aspect of physical performance (OLS balance) and body composition (QS/BW ratio) derived from 106 men aged ≥80 years who could walk independently, unlike previous epidemiological surveys of community-dwelling individuals with various walking levels. The reference ranges found in the present study can be used as the target values for walking independently among older adults aged < 80 years or their health care providers. In addition, our research showed that in men aged ≥80 years who can walk independently, radiographic OA assessment does not necessarily impact OLS balance or the QS/BW ratio, similar to previous reports of the discordance between radiographic knee OA and pain.18,19 In conclusion, independent walking among advanced-age men (age of ≥80 years) helps to maintain OLS balance and the QS/BW ratio regardless of the OA grade as determined by the KL classification. Thus, falls among this population are expected to be prevented by good OLS balance and a good QS/BW ratio. Verification of the validity of these findings at multiple facilities and among women is expected in the future.
The local institutional review board approved this study. All patients provided informed consent. Declaration of competing interest The authors declare that they have no competing interests. Acknowledgment We would like to thank all the rehabilitation staff, all the interviewers, and most sincerely all the participating patients who visited our outpatient clinic. References 1. Grisso JA, Kelsey JL, Strom BL, et al. Risk factors for hip fracture in black women. The northeast hip fracture study group. N Engl J Med. 1994;330:1555–1559. 2. Matsueda M, Ishii Y. The relationship between dementia score and ambulatory level after hip fracture in the elderly. Am J Orthoped. 2000;29:691–693. 3. Imura K, Ishii Y, Yagisawa K, Matsueda M. Postoperative ambulatory level after hip fracture in the elderly predicts survival rate. Arch Orthop Trauma Surg. 2000;120:369–371. 4. Vellas BJ, Wayne SJ, Romero L, Baumgartner RN, Rubenstein LZ, Garry PJ. One-leg balance is an important predictor of injurious falls in older persons. J Am Geriatr Soc. 1997;45:735–738. 5. Michikawa T, Nishiwaki Y, Takebayashi T, Toyama Y. One-leg standing test for elderly populations. J Orthop Sci. 2009;14:675–685. 6. Morita Y, Ito H, Torii M, et al. Factors affecting walking ability in female patients with rheumatoid arthritis. PloS One. 2018;13:e0195059. 7. Furu M, Ito H, Nishikawa T, et al. Quadriceps strength affects patient satisfaction after total knee arthroplasty. J Orthop Sci. 2016;21:38–43. 8. Wearing J, Stokes M, de Bruin ED. Quadriceps muscle strength is a discriminant predictor of dependence in daily activities in nursing home residents. PloS One. 2019;14:e0223016. 9. Dulac MC, Carvalho LP, Aubertin-Leheudre M. Functional capacity depends on lower limb muscle strength rather than on abdominal obesity in active postmenopausal women. Menopause. 2018;25:176–181. 10. Kellgren JH, Lawrence JS. Radiographical assessment of osteoarthritis. Ann Rheum Dis. 1957;16:494–502. 11. Muraki S, Oka H, Akune T, et al. Prevalence of radiographic knee osteoarthritis and its association with knee pain in the elderly of Japanese population-based cohorts: the ROAD study. Osteoarthritis Cartilage. 2009;17:1137–1143. 12. Omori G, Koga Y, Tanaka M, et al. Quadriceps muscle strength and its relationship to radiographic knee osteoarthritis in Japanese elderly. J Orthop Sci. 2013;18:536–542. 13. Dell'isola A, Wirth W, Steultjens M, Eckstein F, Culvenor AG. Knee extensor muscle weakness and radiographic knee osteoarthritis progression. Acta Orthop. 2018;89:406–411. 14. Bedson J, Croft PR. The discordance between clinical and radiographic knee osteoarthritis: a systematic search and summary of the literature. BMC Muscoskel Disord. 2008;9:116. 15. Schiphof D, Kerkhof HJ, Damen J, et al. Factors for pain in patients with different grades of knee osteoarthritis. Arthritis Care Res (Hoboken). 2013;65:695–702. 16. Ministry of Health. Labour and welfare of Japan. https://www.mhlw.go.jp/index. html. 17. Seino S, Shinkai S, Fujiwara Y, et al. TMIG-LISA Research Group. Reference values and age and sex differences in physical performance measures for communitydwelling older Japanese: a pooled analysis of six cohort studies. PloS One. 2014;9:e99487.
Consent for publication Not applicable. Availability of data and materials The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request. Funding This work was partially supported by the Japanese Clinical Orthopedic Association under Grant 2019. The funder played no role in the design, methods, subject recruitment, data collection, analysis or preparation of the paper. Authors’ contributions YI contributed to the study conception and design, drafted the article, and ensured the accuracy of the data and analysis. HN and JS contributed to the study conception and design and to the analysis and interpretation of the data. HI and RI contributed to the data collection. ST provided statistical expertise and contributed to ensuring the accuracy of the data and analysis. All authors approved the final manuscript. 82
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22. Hatfield GL, Morrison A, Wenman M, Hammond CA, Hunt MA. Clinical tests of standing balance in the knee osteoarthritis population: systematic review and metaanalysis. Phys Ther. 2016;96(3):324–337. 23. Seichi A, Hoshino Y, Doi T, et al. Determination of the optimal cutoff time to use when screening elderly people for locomotive syndrome using the one-leg standing test (with eyes open). J Orthop Sci. 2014;19(4):620–626. 24. Birmingham T, Kramer J, Kirkley A, Inglis J, Spaulding S, Vandervoort A. Association among neuromuscular and anatomic measures for patients with knee osteoarthritis. Arch Phys Med Rehabil. 2001;82:1115–1118. 25. Hunt MA, McManus FJ, Hinman RS, Bennell KL. Predictors of single-leg standing balance in individuals with medial knee osteoarthritis. Arthritis Care Res. 2010;62:496–500.
18. Rosenberg TD, Paulos LE, Parker RD, Coward DB, Scott SM. The forty-five-degree posteroanterior flexion weight-bearing radiograph of the knee. J Bone Joint Surg Am. 1988;70:1479–1483. 19. Harato K, Kobayashi S, Kojima I, Sakurai A, Tanikawa H, Niki Y. Factors affecting one-leg standing time in patients with end-stage knee osteoarthritis and the agerelated recovery process following total knee arthroplasty. J Orthop Surg Res. 2017;12(1):21. 20. Ishii Y, Noguchi H, Sato J, Sakurai T, Toyabe SI. Quadriceps strength impairment in the mid- to long-term follow-up period after TKA. Knee Surg Sports Traumatol Arthrosc. 2017;25(11):3372–3377. 21. Narumi K, Funaki Y, Yoshimura N, et al. Quadriceps muscle strength reference value as index for functional deterioration of locomotive organs: data from 3617 men and women in Japan. J Orthop Sci. 2017;22(4):765–770.
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