Authors: Serdar Kesikburun, MD O¨zlem Ko¨rog˘lu, MD Evren Yas$ ar, MD U¨mu¨t Gu¨zelku¨c¸u¨k, MD Kamil YazNcNog˘lu, MD Arif Kenan Tan, MD
Amputation
ORIGINAL RESEARCH ARTICLE
Affiliations: From the Department of Physical Medicine and Rehabilitation, Gu¨lhane Military Medical Academy, Turkish Armed Forces Rehabilitation Center, Ankara (SK, EY, U¨G, KY, AKT); and Military Hospital of ElazNg˘, The Clinics of Physical Medicine and Rehabilitation, ElazNg˘, Turkey (O¨K).
Correspondence: All correspondence and requests for reprints should be addressed to: Serdar Kesikburun, MD, TSK Rehabilitasyon Merkezi, 06800, Lodumlu Yolu, Bilkent, Ankara, Turkey.
Disclosures: Financial disclosure statements have been obtained, and no conflicts of interest have been reported by the authors or by any individuals in control of the content of this article.
0894-9115/15/9408-0602 American Journal of Physical Medicine & Rehabilitation Copyright * 2014 Wolters Kluwer Health, Inc. All rights reserved. DOI: 10.1097/PHM.0000000000000216
Comparison of Intact Knee Cartilage Thickness in Patients with Traumatic Lower Extremity Amputation and Nonimpaired Individuals ABSTRACT ¨ , Yas$ ar E, Gu¨zelku¨çu¨k U¨, YazNcNog˘lu K, Tan AK: Kesikburun S, Ko¨rog˘lu O Comparison of intact knee cartilage thickness in patients with traumatic lower extremity amputation and nonimpaired individuals. Am J Phys Med Rehabil 2015;94:602Y608.
Objective:
The aim of this study was to assess the femoral articular cartilage thickness of the intact knee in patients with traumatic lower extremity amputation compared with nonimpaired individuals.
Design: A total of 30 male patients with traumatic lower extremity amputation (mean [SD] age, 31.2 [6.3] yrs) and a random sample of 53 age-matched and body mass indexYmatched male nonimpaired individuals (mean [SD] age, 29.8 [6.3] yrs) participated in the study. Exclusion criteria were age younger than 18 yrs, history of significant knee injury, previous knee surgery, or rheumatic disease. The femoral articular cartilage thickness was measured using ultrasound at the midpoints of the medial condyle, the intercondylar notch, and the lateral condyle. Ultrasonographic cartilage measurement was performed on the intact side of the patients with amputation and on both sides of the nonimpaired individuals.
Results: The femoral articular cartilage thickness of the intact knees of the patients with amputation was significantly decreased at the lateral and medial condyles compared with the nonimpaired individuals (P G 0.05). There was no significant difference in the measurements at the intercondylar notch between the patients with amputation and the nonimpaired individuals (P 9 0.05).
Conclusions: There was a premature cartilage loss in the intact limb knee of the patients with traumatic amputation. This result supports the view that patients with traumatic lower extremity amputation are at increased risk for developing knee osteoarthritis in the intact limb. Key Words:
602
Amputation, Osteoarthritis, Cartilage Thickness, Ultrasonography
Am. J. Phys. Med. Rehabil. & Vol. 94, No. 8, August 2015 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
I
t has been suggested that patients with lower extremity amputation are predisposed to knee osteoarthritis especially in the intact limb, which has been attributed to alteration in gait biomechanics and abnormal joint loading.1,2 Knee osteoarthritis in the intact limb of patients with lower extremity amputation has been found to be more prevalent than in age-matched nonimpaired individuals.3Y5 There have also been imaging studies with plain radiography supporting the increased prevalence of knee osteoarthritis in the intact limb of amputees compared with the nonimpaired population.6,7 These findings support the presence of early cartilage damage in the knee of the intact limb of patients with amputation. Plain radiographs have been used for the assessment of knee cartilage from measurement of the tibiofemoral joint space width. However, problems resulting from positioning of the knee, misalignment of the x-ray beams, and radiographic magnification have been postulated to impact the reproducibility of tibiofemoral joint space width measurement.8 Magnetic resonance imaging is the criterion standard but not a cost-effective imaging technique for knee cartilage evaluation. Ultrasonography is a quick, inexpensive, and valid technique for the assessment of femoral articular cartilage.9Y12 The aim of this study was to investigate the femoral articular cartilage thickness of the intact knee in patients with traumatic lower extremity amputation, compared with nonimpaired individuals, and its relationship with various clinical features of the patients with amputation.
MATERIALS AND METHODS Study Design and Participants A cross-sectional experimental design was applied to compare the ultrasound measurements of the intact knee cartilage thickness of patients with traumatic lower extremity amputation with nonimpaired individuals. A total of 30 male patients with traumatic lower extremity amputation (mean [SD] age, 31.2 [6.3] yrs) and a random sample of 53 agematched and body mass indexYmatched male nonimpaired individuals (mean [SD] age, 29.8 [6.3] yrs) participated in the study. Inclusion criteria for the study were (1) unilateral traumatic amputation including the amputation levels of transtibial, knee disarticulation, and transfemoral as well as (2) ability to walk with a prosthesis for at least 6 mos. Participants were excluded if they were (1) younger than 18 yrs, (2) had a history of significant knee injury, (3) www.ajpmr.com
had previous knee surgery, or (4) had a connective tissue disease. Given their higher life expectancy resulting in better ambulatory capacity and more participation in sports and work, patients with traumatic amputation were selected for the study because of their higher chance of developing premature knee cartilage damage. All participants provided written informed consent. The study protocol was approved by the Local Ethics Committee of Gu¨lhane Military Medical Academy.
Clinical Assessment The baseline data for all participants including age, sex, body height/weight, side of amputation, level of amputation, time since amputation, and time since receiving a prosthesis were noted. Body mass index was calculated. Using a 5-point Likert scale from very easy to very difficult, the patients were asked about duration of standing or walking with a prosthesis in a day, participation in regular sports activities with risk for knee cartilage damage, and working conditions related to risk for knee cartilage damage. The functional abilities of the patients were assessed using the K classification system,13 which uses code modifiers (K0, K1, K2, K3, K4) as a fivelevel functional classification system related to the functional abilities of patients with lower limb amputation. The lower the activity potential of the patients is, the lower the K-level is and vice versa. The K-levels are explained as follows: K0, nonambulatory and no mobility; K1, household ambulatory and having ability or potential to use a prosthesis for transfers or ambulation on level surfaces; K2, limited community ambulatory and having ability or potential to use a prosthesis for ambulation and ability to adjust for low-level environmental barriers such as curbs, stairs, and uneven surfaces; K3, unlimited community ambulatory and having ability or potential to use a prosthesis for basic ambulation and ability to adjust for most environmental barriers; and K4, very active and exceeding basic mobility and applying high impact and stress to the prosthetic leg. The patients were examined to determine the presence of clinical knee osteoarthritis on the intact side according to the American College of Rheumatology classification criteria.14 The patients were designated as having knee osteoarthritis if they had pain in the knee and three of the following six criteria: (1) older than 50 yrs, (2) less than 30 mins of morning stiffness, (3) crepitus on active motion, (4) bony tenderness, (5) bony enlargement, and (6) no palpable warmth of synovium. Intact Knee Cartilage Thickness in Amputation
Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
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Ultrasonographic Cartilage Measurement
Statistical Analysis
Ultrasonographic examinations were performed by the same investigator using the same machine with a 7.5- to 12-MHz linear transducer (LOGIQ 7 Pro; GE Yokogawa Medical System, Tokyo, Japan). While the subjects were lying supine on the examination table with their knees in maximum flexion (at a knee flexion of 135 degrees), the transducer was placed transversely to the leg above the superior margin of the patella and perpendicular to the femoral articular surface. The femoral articular cartilage was imaged as an anechoic line between the bony cortex and suprapatellar fat tissue. Femoral articular cartilage thickness was measured by drawing a straight line from the bone-cartilage interface to the cartilageYfat tissue interface at the midpoints of the medial condyle, the intercondylar notch, and the lateral condyle (Fig. 1). Ultrasonographic cartilage measurement was performed on the intact side of the patients with amputation (30 knees) and on both sides of the nonimpaired individuals (106 knees). To test the intrarater reliability, the ultrasonographic cartilage measurements at the medial condyle, the intercondylar notch, and the lateral condyle were taken according to the study methodology in 15 nonimpaired individuals (30 knees). After 1 day, all the measurements were repeated, blinded to the first measurements. The intrarater reliability was found to be moderate to good (1.84%Y9.2% coefficient of variation) for the ultrasonographic femoral cartilage thickness measurements.
All statistical tests were performed using the IBM SPSS Statistics software program (Chicago, IL) for Mac version 20.0. The results were expressed as mean (standard deviation). For between-group comparisons of patient imaging findings, the independent sample t test was used. The relationship between clinical features and ultrasonographic femoral cartilage thickness measures was assessed using the Pearson correlation coefficient. The significance level was determined at P G 0.05.
RESULTS The amputations of the patients in the study were 26 transtibial, 3 knee disarticulation, and 1 transfemoral, on the left side in 24 cases and the right side in 26. The mean (SD) time since amputation and the mean (SD) time since receiving a prosthesis were 7.6 (7.0) and 7.2 (6.9) yrs, respectively. The patients with traumatic amputation in this study generally had a high functional level, with all but one patient higher than K3. The mean (SD) daily walking or standing time with prosthesis was 8 (4.2) hrs. Onethird of the patients with amputation participated in a regular sports activity. Very few of the patients with amputation (10%) identified their working conditions as hard. Although none of the patients met the American College of Rheumatology knee osteoarthritis criteria, nine of the patients with amputation (30%) had pain and crepitus in the knee of the intact side. The demographics and clinical features of the subjects are presented in Table 1.
FIGURE 1 Femoral cartilage measures at the lateral condyle, the intercondylar notch, and the medial condyle in an ultrasound transverse image.
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Am. J. Phys. Med. Rehabil. & Vol. 94, No. 8, August 2015 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
TABLE 1 Demographics and clinical characteristics of the patients with amputation and the nonimpaired individuals
Sex Male Female Age,a yrs Body mass index,a kg/m2 Side of amputation Right Left Level of amputation Below knee Knee disarticulation Above knee Time since amputation,a yrs Time since receiving a prosthesis,a yrs Daily standing/walking time with prosthesis,a hrs K-levels K0: nonambulatory K1: household ambulatory K2: limited community ambulatory K3: unlimited community ambulatory K4: very active Sports Yes No Working conditions Very easy Easy Moderate Hard Very hard Pain and crepitus in the intact knee Osteoarthritis in the intact knee a
Patients with Amputation (n = 30)
Nonimpaired Individuals (n = 53)
P
30 (100.0%) 0 (0.0%) 31.2 (6.3) [22Y41] 25.1 (3.3) [18.1Y32.2]
53 (100.0%) 0 (0.0%) 29.8 (6.3) [24Y40] 24.5 (3.8) [17.6Y33.2]
0.603 0.459
16 (53.3%) 14 (46.7%) 26 (86.7%) 3 (10.0%) 1 (3.3%) 7.6 (7.0) [1Y20] 7.2 (6.9) [0.75Y19] 8.5 (4.2) [1Y15] 0 (0.0%) 0 (0.0%) 1 (3.3%) 21 (70.0%) 8 (26.7%) 10 (33.3%) 20 (66.7%) 10 (33.3%) 9 (30.0%) 8 (26.7%) 3 (10.0%) 0 (0.0%) 9 (30.0%) 0 (0.0%)
Mean (standard deviation) [range].
The femoral articular cartilage thickness in the intact knees of the patients with amputation was significantly decreased at the lateral and medial condyles compared with the nonimpaired individuals (P G 0.05). There was no significant difference in the measurements at the intercondylar notch between the patients with amputation and
the nonimpaired individuals (P 9 0.05) (Table 2). No significant correlation was found between the ultrasonographic measurements of femoral cartilage thickness and the patients’ clinical features including age, body mass index, time since amputation, time since receiving a prosthesis, daily standing/walking time with prosthesis, and K-levels (P 9 0.05).
TABLE 2 Ultrasonographic femoral cartilage thickness measures in the patients with amputation and the nonimpaired individuals
a
LFCCT, cm ICCT,a cm MFCCT,a cm
Patients with Amputation (n = 30)
Nonimpaired Individuals (n = 53)
P
0.185 (0.043) 0.207 (0.055) 0.187 (0.051)
0.203 (0.037) 0.207 (0.038) 0.205 (0.036)
0.041b 0.928 0.047b
a
Mean (standard deviation). Statistically significant. INCT, intercondylar notch cartilage thickness; LFCCT, lateral femoral condylar cartilage thickness; MFCCT, medial femoral condylar cartilage thickness. b
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DISCUSSION The knee cartilage in the intact limb knees of the patients with traumatic amputation was found to be thinner than in the knees of the nonimpaired individuals. Ultrasonographic measurement showed early femoral articular cartilage loss at the lateral and medial condyles in the intact limb knees of the patients with amputation. There was no correlation between knee cartilage thickness and the clinical features of the patients. The primary mechanism of premature joint degeneration in patients with amputation has been attributed to increased load on the intact limb and gait asymmetry.1,2 Patients with lower extremity amputation tend to use the intact limb to compensate for the amputated side, resulting in a greater load through the intact limb knee during walking.15 Reduced prosthetic limb push-off power leading to increased effort of the intact limb for walking balance is another explanation for the increased intact limb loading.16,17 A larger ground reaction force, as measured with force plates during walking, was found on the intact side compared with the prosthetic side and also in nonimpaired individuals.18,19 Bone mineral density at the proximal tibia of the intact side was also found to be larger than that of the amputated side, indicating a greater mechanical loading on the intact limb.20 Knee external adduction moment during load bearing is another potential biomechanical factor contributing to the onset and progression of knee osteoarthritis.21 Knee adduction moment describes the distribution of medial and lateral tibiofemoral compartment joint contact forces and correlates well with medial compartment loading.22 In the general population, knee osteoarthritis most commonly affects the medial compartment because of greater medial contact forces and knee adduction moment during normal gait.23,24 Knee external adduction moment in the intact knees of patients with transtibial amputation was found to be higher than in the amputated knee.18,25 This asymmetry in gait mechanics contributes to a predisposition to knee osteoarthritis in patients with amputation. There is only a single radiographic study concerning patterns of compartment involvement in intact knee osteoarthritis of patients with amputation compared with nonimpaired individuals. It showed a tendency to medial narrowing of the tibiofemoral joint space and patellofemoral degeneration in patients with amputation.6 This study demonstrated a significant cartilage loss at both the medial and lateral condyles of the femur. Compartment involvement in the intact limb knee osteoarthritis and its
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potential biomechanical explanations should be investigated in future research, which may help to develop rehabilitative strategies for the prevention and treatment of osteoarthritis in patients with amputation. An amputee with traumatic etiology probably has an increased risk for developing intact knee osteoarthritis in comparison with patients with amputation as a result of dysvascular etiology.1 Injury in these individuals often happens at a younger age, and they usually live longer compared with patients with amputation as a result of dysvascular etiology. In addition, they have a better ambulatory capacity as well as more participation in sports and work. These factors increase the exposure to abnormal gait mechanics over time. A previous ultrasound study in patients with amputation found increased cartilage loss on the amputated side compared with the intact side.26 Most of the participants in that study had amputation secondary to dysvascular disease, which may account for the confounding results. The lack of a control group in the study did not allow comparison with nonimpaired individuals. Research into osteoarthritis associated with amputation to show the increased risk in the intact limb could be better performed in subjects of traumatic origin. In the current study, despite the presence of significant cartilage loss, none of the participants matched the osteoarthritis criteria of the American College of Rheumatology. However, 30% reported pain and crepitus in the intact knee. There may be two explanations for this. First, the American College of Rheumatology clinical criteria have been suggested to reflect later signs in advanced disease and fail to identify early, mild osteoarthritis.27 Second, ultrasonography may be sensitive to reveal early cartilage damage before the clinical symptoms of the disease are seen. In addition, the mean of 7 yrs since amputation is a relatively shorter time compared with previous observational studies that have reported results from more than 25 yrs since amputation.2 It may take time for clinical osteoarthritis to show in the current study subjects. This short duration may also account for why the results did not show a correlation between cartilage thickness and time since amputation and receiving a prosthesis. This correlation may be found in a study group during a longer period. A limitation of this study is that the physical activity of the subjects was not measured with a more objective scale or test than K-levels. However, the mean age of the subjects in the study was 31 yrs, ranging from 22 to 41 yrs. None were older or assumed to be in bad physical condition. Another limitation is that no investigation was made into whether there was a difference in knee cartilage
Am. J. Phys. Med. Rehabil. & Vol. 94, No. 8, August 2015 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
thickness between the patients with transtibial and transfemoral amputation. A previous study found that patients with transfemoral amputation were at higher risk for knee pain than patients with transtibial amputation,4 although the number of patients with transfemoral amputation was not sufficient for statistical comparison. Whether the level of amputation may have an impact on knee cartilage thickness could be a topic for further investigations. There was also a technical limitation because ultrasonography can image only femoral articular cartilage. However, knee joint degeneration may also affect tibial and patellar articular cartilage, which were not assessed in this study. Finally, a limitation regarding the measurement technique is the challenge of controlling the exact obliquity angle of the transducer in relation to the femoral cartilage across the subjects. The transducer might be somewhat oblique to the trochlear groove, and so the cartilage thickness measurements might appear falsely large. Therefore, there might have been inaccuracies of measurements across the subjects. Naredo et al.9 showed good intrarater and interrater reliability for ultrasonographic knee cartilage measurement in their study comparing ultrasonographic and anatomic measurements in cadaver specimens. They found that ultrasound measurements were accurate in normal to moderately damaged cartilage but not in severely damaged cartilage. Moderate to substantial agreement was found between the ultrasound observers in femoral cartilage thickness measurements in the study of Abraham et al.28 Yoon et al.29 found no correlation between the transverse suprapatellar ultrasound scan and magnetic resonance imaging in the medial condyle, and that study showed high overall intrarater and interrater agreement in the ultrasound scan. It was concluded that ultrasound scan in the longitudinal plane is more feasible than suprapatellar transverse scan for cartilage measurement in the medial condyle. In the current study, the intrarater reliability was also found to be moderate to good for the measurements. Although the described ultrasound technique in this study has been widely used in previous studies,30Y35 considering the abovementioned concerns about the measurements, future studies with quantitative analysis of femoral articular cartilage using magnetic resonance imaging could be beneficial to confirm the result of this ultrasound study.
healthy subjects. This result supports the view that patients with traumatic lower extremity amputation are at increased risk for developing early knee degeneration in the intact limb. Clinicians should be aware of the importance of rehabilitation strategies aimed at decreasing onset and progression of knee osteoarthritis in patients with traumatic amputation. REFERENCES 1. Morgenroth DC, Gellhorn AC, Suri P: Osteoarthritis in the disabled population: A mechanical perspective. PM R 2012;4:20Y7 2. Gailey R, Allen K, Castles J, et al: Review of secondary physical conditions associated with lower-limb amputation and long-term prosthesis use. J Rehabil Res Dev 2008;45:15Y29 3. Hungerford D, Cockin J: Fate of the retained lower limb joints in second World War amputees. J Bone Joint Surg 1975;57:111 4. Norvell DC, Czerniecki JM, Reiber GE, et al: The prevalence of knee pain and symptomatic knee osteoarthritis among veteran traumatic amputees and nonamputees. Arch Phys Med Rehabil 2005;86:487Y93 5. Struyf PA, van Heugten CM, Hitters MW, et al: The prevalence of osteoarthritis of the intact hip and knee among traumatic leg amputees. Arch Phys Med Rehabil 2009;90:440Y6 6. Melzer I, Yekutiel M, Sukenik S: Comparative study of osteoarthritis of the contralateral knee joint of male amputees who do and do not play volleyball. J Rheumatol 2001;28:169Y72 7. Lemaire ED, Fisher FR: Osteoarthritis and elderly amputee gait. Arch Phys Med Rehabil 1994;75:1094Y9 8. Mazzuca SA, Brandt KD, Katz BP: Is conventional radiography suitable for evaluation of a diseasemodifying drug in patients with knee osteoarthritis? Osteoarthritis Cartilage 1997;5:217Y26 9. Naredo E, Acebes C, Mo¨ller I, et al: Ultrasound validity in the measurement of knee cartilage thickness. Ann Rheum Dis 2009;68:1322Y7 10. Saarakkala S, Waris P, Waris V, et al: Diagnostic performance of knee ultrasonography for detecting degenerative changes of articular cartilage. Osteoarthritis Cartilage 2012;20:376Y81 11. Liukkonen J, Hirvasniemi J, Joukainen A, et al: Arthroscopic ultrasound technique for simultaneous quantitative assessment of articular cartilage and subchondral bone: An in vitro and in vivo feasibility study. Ultrasound Med Biol 2013;39:1460Y8
CONCLUSIONS
12. Ozc¸akar L, Tunc¸ H, Oken O, et al: Femoral cartilage thickness measurements in healthy individuals learning, practicing and publishing with TURKMUSCULUS. J Back Musculoskelet Rehabil 2014; 27:117Y24. doi:10.3233/BMR-130441
This study showed that there was cartilage loss in the intact limb knee of the patients with traumatic amputation compared with the age-matched
13. HCFA Common Procedure Coding System HCPCS 2001. Washington, DC, US Government Printing Office, 2001. Ch 5.3
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14. Altman R, Asch E, Bloch D, et al: Development of criteria for the classification and reporting of osteoarthritis. Classification of osteoarthritis of the knee. Diagnostic and Therapeutic Criteria Committee of the American Rheumatism Association. Arthritis Rheum 1986;29:1039Y49 15. Mussman M, Altwerger W, Eisenstein J, et al: Contralateral lower extremity evaluation with a lower limb prosthesis. J Am Podiatry Assoc 1983; 73:344Y6 16. Winter DA, Sienko SE: Biomechanics of below-knee amputee gait. J Biomech 1988;21:361Y7
26. Akkaya N, Akkaya S, O¨zc¸akar L, et al: Ultrasonographic measurement of the distal femoral cartilage thickness in patients with unilateral transtibial amputation. Prosthet Orthot Int 2013;37:268Y74 27. Peat G, Thomas E, Duncan R, et al: Clinical classification criteria for knee osteoarthritis: Performance in the general population and primary care. Ann Rheum Dis 2006;65:1363Y7
17. Houdijk H, Pollmann E, Groenewold M, et al: The energy cost for the step-to-step transition in amputee walking. Gait Posture 2009;30:35Y40
28. Abraham AM, Goff I, Pearce MS, et al: Reliability and validity of ultrasound imaging of features of knee osteoarthritis in the community. BMC Musculoskelet Disord 2011;12:70
18. Lloyd CH, Stanhope SJ, Davis IS, et al: Strength asymmetry and osteoarthritis risk factors in unilateral trans-tibial, amputee gait. Gait Posture 2010; 32:296Y300
29. Yoon CH, Kim HS, Ju JH, et al: Validity of the sonographic longitudinal sagittal image for assessment of the cartilage thickness in the knee osteoarthritis. Clin Rheumatol 2008;27:1507Y16
19. Engsberg JR, Lee AG, Patterson JL, et al: External loading comparisons between able-bodied and belowknee-amputee children during walking. Arch Phys Med Rehabil 1991;72:657Y61
30. Kara M, Tiftik T, O¨ken O¨, et al: Ultrasonographic measurement of femoral cartilage thickness in patients with spinal cord injury. J Rehabil Med 2013;45:145Y8
20. Royer T, Koenig M: Joint loading and bone mineral density in persons with unilateral, trans-tibial amputation. Clin Biomech 2005;20:1119Y25 21. Vincent KR, Conrad BP, Fregly BJ, et al: The pathophysiology of osteoarthritis: A mechanical perspective on the knee joint. PM R 2012;4:3Y9 22. Zhao D, Banks SA, Mitchell KH, et al: Correlation between the knee adduction torque and medial contact force for a variety of gait patterns. J Orthopaed Res 2007;25:789Y97 23. Wise BL, Niu J, Yang M, et al; Multicenter Osteoarthritis (MOST) Group: Patterns of compartment involvement in tibiofemoral osteoarthritis in men and women and in whites and African Americans. Arthritis Care Res 2012;64:847Y52 24. Schipplein OD, Andriacchi TP: Interaction between active and passive knee stabilizers during level walking. J Orthop Res 1991;9:113Y9
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25. Royer T, Wasilewski C: Hip and knee frontal plane moments in persons with unilateral, trans-tibial amputation. Gait Posture 2006;23:303Y6
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31. Akkaya S, Akkaya N, Ozcakar L, et al: Ultrasonographic evaluation of the femoral cartilage thickness after unilateral arthroscopic partial meniscectomy. Knee Surg Sports Traumatol Arthrosc 2013;21:1104Y10 32. Tunc¸ H, Oken O, Kara M, et al: Ultrasonographic measurement of the femoral cartilage thickness in hemiparetic patients after stroke. Int J Rehabil Res 2012;35:203Y7 33. O¨zgu¨l A, Gu¨nendi Z, Kesikburun S, et al: The association between patellar alignments features and tibiofemoral joint osteoarthritis. Clin Rheumatol 2013;32:1017Y20 34. CarlN AB, Akarsu S, Tekin L, et al: Ultrasonographic assessment of the femoral cartilage in osteoarthritis patients with and without osteoporosis. Aging Clin Exp Res 2014;26:411Y5 35. Kilic G, Kilic E, Akgul O, et al: Decreased femoral cartilage thickness in patients with systemic sclerosis. Am J Med Sci 2014;347:382Y6
Am. J. Phys. Med. Rehabil. & Vol. 94, No. 8, August 2015 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
Amputation
ORIGINAL RESEARCH ARTICLE
Affiliations: From the Department of Physical Medicine and Rehabilitation, Gu¨lhane Military Medical Academy, Turkish Armed Forces Rehabilitation Center, Ankara (SK, EY, U¨G, KY, AKT); and Military Hospital of ElazNg˘, The Clinics of Physical Medicine and Rehabilitation, ElazNg˘, Turkey (O¨K).
Correspondence: All correspondence and requests for reprints should be addressed to: Serdar Kesikburun, MD, TSK Rehabilitasyon Merkezi, 06800, Lodumlu Yolu, Bilkent, Ankara, Turkey.
Disclosures: Financial disclosure statements have been obtained, and no conflicts of interest have been reported by the authors or by any individuals in control of the content of this article.
0894-9115/15/9408-0602 American Journal of Physical Medicine & Rehabilitation Copyright * 2014 Wolters Kluwer Health, Inc. All rights reserved. DOI: 10.1097/PHM.0000000000000216
Comparison of Intact Knee Cartilage Thickness in Patients with Traumatic Lower Extremity Amputation and Nonimpaired Individuals ABSTRACT ¨ , Yas$ ar E, Gu¨zelku¨çu¨k U¨, YazNcNog˘lu K, Tan AK: Kesikburun S, Ko¨rog˘lu O Comparison of intact knee cartilage thickness in patients with traumatic lower extremity amputation and nonimpaired individuals. Am J Phys Med Rehabil 2015;94:602Y608.
Objective:
The aim of this study was to assess the femoral articular cartilage thickness of the intact knee in patients with traumatic lower extremity amputation compared with nonimpaired individuals.
Design: A total of 30 male patients with traumatic lower extremity amputation (mean [SD] age, 31.2 [6.3] yrs) and a random sample of 53 age-matched and body mass indexYmatched male nonimpaired individuals (mean [SD] age, 29.8 [6.3] yrs) participated in the study. Exclusion criteria were age younger than 18 yrs, history of significant knee injury, previous knee surgery, or rheumatic disease. The femoral articular cartilage thickness was measured using ultrasound at the midpoints of the medial condyle, the intercondylar notch, and the lateral condyle. Ultrasonographic cartilage measurement was performed on the intact side of the patients with amputation and on both sides of the nonimpaired individuals.
Results: The femoral articular cartilage thickness of the intact knees of the patients with amputation was significantly decreased at the lateral and medial condyles compared with the nonimpaired individuals (P G 0.05). There was no significant difference in the measurements at the intercondylar notch between the patients with amputation and the nonimpaired individuals (P 9 0.05).
Conclusions: There was a premature cartilage loss in the intact limb knee of the patients with traumatic amputation. This result supports the view that patients with traumatic lower extremity amputation are at increased risk for developing knee osteoarthritis in the intact limb. Key Words:
602
Amputation, Osteoarthritis, Cartilage Thickness, Ultrasonography
Am. J. Phys. Med. Rehabil. & Vol. 94, No. 8, August 2015 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
I
t has been suggested that patients with lower extremity amputation are predisposed to knee osteoarthritis especially in the intact limb, which has been attributed to alteration in gait biomechanics and abnormal joint loading.1,2 Knee osteoarthritis in the intact limb of patients with lower extremity amputation has been found to be more prevalent than in age-matched nonimpaired individuals.3Y5 There have also been imaging studies with plain radiography supporting the increased prevalence of knee osteoarthritis in the intact limb of amputees compared with the nonimpaired population.6,7 These findings support the presence of early cartilage damage in the knee of the intact limb of patients with amputation. Plain radiographs have been used for the assessment of knee cartilage from measurement of the tibiofemoral joint space width. However, problems resulting from positioning of the knee, misalignment of the x-ray beams, and radiographic magnification have been postulated to impact the reproducibility of tibiofemoral joint space width measurement.8 Magnetic resonance imaging is the criterion standard but not a cost-effective imaging technique for knee cartilage evaluation. Ultrasonography is a quick, inexpensive, and valid technique for the assessment of femoral articular cartilage.9Y12 The aim of this study was to investigate the femoral articular cartilage thickness of the intact knee in patients with traumatic lower extremity amputation, compared with nonimpaired individuals, and its relationship with various clinical features of the patients with amputation.
MATERIALS AND METHODS Study Design and Participants A cross-sectional experimental design was applied to compare the ultrasound measurements of the intact knee cartilage thickness of patients with traumatic lower extremity amputation with nonimpaired individuals. A total of 30 male patients with traumatic lower extremity amputation (mean [SD] age, 31.2 [6.3] yrs) and a random sample of 53 agematched and body mass indexYmatched male nonimpaired individuals (mean [SD] age, 29.8 [6.3] yrs) participated in the study. Inclusion criteria for the study were (1) unilateral traumatic amputation including the amputation levels of transtibial, knee disarticulation, and transfemoral as well as (2) ability to walk with a prosthesis for at least 6 mos. Participants were excluded if they were (1) younger than 18 yrs, (2) had a history of significant knee injury, (3) www.ajpmr.com
had previous knee surgery, or (4) had a connective tissue disease. Given their higher life expectancy resulting in better ambulatory capacity and more participation in sports and work, patients with traumatic amputation were selected for the study because of their higher chance of developing premature knee cartilage damage. All participants provided written informed consent. The study protocol was approved by the Local Ethics Committee of Gu¨lhane Military Medical Academy.
Clinical Assessment The baseline data for all participants including age, sex, body height/weight, side of amputation, level of amputation, time since amputation, and time since receiving a prosthesis were noted. Body mass index was calculated. Using a 5-point Likert scale from very easy to very difficult, the patients were asked about duration of standing or walking with a prosthesis in a day, participation in regular sports activities with risk for knee cartilage damage, and working conditions related to risk for knee cartilage damage. The functional abilities of the patients were assessed using the K classification system,13 which uses code modifiers (K0, K1, K2, K3, K4) as a fivelevel functional classification system related to the functional abilities of patients with lower limb amputation. The lower the activity potential of the patients is, the lower the K-level is and vice versa. The K-levels are explained as follows: K0, nonambulatory and no mobility; K1, household ambulatory and having ability or potential to use a prosthesis for transfers or ambulation on level surfaces; K2, limited community ambulatory and having ability or potential to use a prosthesis for ambulation and ability to adjust for low-level environmental barriers such as curbs, stairs, and uneven surfaces; K3, unlimited community ambulatory and having ability or potential to use a prosthesis for basic ambulation and ability to adjust for most environmental barriers; and K4, very active and exceeding basic mobility and applying high impact and stress to the prosthetic leg. The patients were examined to determine the presence of clinical knee osteoarthritis on the intact side according to the American College of Rheumatology classification criteria.14 The patients were designated as having knee osteoarthritis if they had pain in the knee and three of the following six criteria: (1) older than 50 yrs, (2) less than 30 mins of morning stiffness, (3) crepitus on active motion, (4) bony tenderness, (5) bony enlargement, and (6) no palpable warmth of synovium. Intact Knee Cartilage Thickness in Amputation
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Ultrasonographic Cartilage Measurement
Statistical Analysis
Ultrasonographic examinations were performed by the same investigator using the same machine with a 7.5- to 12-MHz linear transducer (LOGIQ 7 Pro; GE Yokogawa Medical System, Tokyo, Japan). While the subjects were lying supine on the examination table with their knees in maximum flexion (at a knee flexion of 135 degrees), the transducer was placed transversely to the leg above the superior margin of the patella and perpendicular to the femoral articular surface. The femoral articular cartilage was imaged as an anechoic line between the bony cortex and suprapatellar fat tissue. Femoral articular cartilage thickness was measured by drawing a straight line from the bone-cartilage interface to the cartilageYfat tissue interface at the midpoints of the medial condyle, the intercondylar notch, and the lateral condyle (Fig. 1). Ultrasonographic cartilage measurement was performed on the intact side of the patients with amputation (30 knees) and on both sides of the nonimpaired individuals (106 knees). To test the intrarater reliability, the ultrasonographic cartilage measurements at the medial condyle, the intercondylar notch, and the lateral condyle were taken according to the study methodology in 15 nonimpaired individuals (30 knees). After 1 day, all the measurements were repeated, blinded to the first measurements. The intrarater reliability was found to be moderate to good (1.84%Y9.2% coefficient of variation) for the ultrasonographic femoral cartilage thickness measurements.
All statistical tests were performed using the IBM SPSS Statistics software program (Chicago, IL) for Mac version 20.0. The results were expressed as mean (standard deviation). For between-group comparisons of patient imaging findings, the independent sample t test was used. The relationship between clinical features and ultrasonographic femoral cartilage thickness measures was assessed using the Pearson correlation coefficient. The significance level was determined at P G 0.05.
RESULTS The amputations of the patients in the study were 26 transtibial, 3 knee disarticulation, and 1 transfemoral, on the left side in 24 cases and the right side in 26. The mean (SD) time since amputation and the mean (SD) time since receiving a prosthesis were 7.6 (7.0) and 7.2 (6.9) yrs, respectively. The patients with traumatic amputation in this study generally had a high functional level, with all but one patient higher than K3. The mean (SD) daily walking or standing time with prosthesis was 8 (4.2) hrs. Onethird of the patients with amputation participated in a regular sports activity. Very few of the patients with amputation (10%) identified their working conditions as hard. Although none of the patients met the American College of Rheumatology knee osteoarthritis criteria, nine of the patients with amputation (30%) had pain and crepitus in the knee of the intact side. The demographics and clinical features of the subjects are presented in Table 1.
FIGURE 1 Femoral cartilage measures at the lateral condyle, the intercondylar notch, and the medial condyle in an ultrasound transverse image.
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Am. J. Phys. Med. Rehabil. & Vol. 94, No. 8, August 2015 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
TABLE 1 Demographics and clinical characteristics of the patients with amputation and the nonimpaired individuals
Sex Male Female Age,a yrs Body mass index,a kg/m2 Side of amputation Right Left Level of amputation Below knee Knee disarticulation Above knee Time since amputation,a yrs Time since receiving a prosthesis,a yrs Daily standing/walking time with prosthesis,a hrs K-levels K0: nonambulatory K1: household ambulatory K2: limited community ambulatory K3: unlimited community ambulatory K4: very active Sports Yes No Working conditions Very easy Easy Moderate Hard Very hard Pain and crepitus in the intact knee Osteoarthritis in the intact knee a
Patients with Amputation (n = 30)
Nonimpaired Individuals (n = 53)
P
30 (100.0%) 0 (0.0%) 31.2 (6.3) [22Y41] 25.1 (3.3) [18.1Y32.2]
53 (100.0%) 0 (0.0%) 29.8 (6.3) [24Y40] 24.5 (3.8) [17.6Y33.2]
0.603 0.459
16 (53.3%) 14 (46.7%) 26 (86.7%) 3 (10.0%) 1 (3.3%) 7.6 (7.0) [1Y20] 7.2 (6.9) [0.75Y19] 8.5 (4.2) [1Y15] 0 (0.0%) 0 (0.0%) 1 (3.3%) 21 (70.0%) 8 (26.7%) 10 (33.3%) 20 (66.7%) 10 (33.3%) 9 (30.0%) 8 (26.7%) 3 (10.0%) 0 (0.0%) 9 (30.0%) 0 (0.0%)
Mean (standard deviation) [range].
The femoral articular cartilage thickness in the intact knees of the patients with amputation was significantly decreased at the lateral and medial condyles compared with the nonimpaired individuals (P G 0.05). There was no significant difference in the measurements at the intercondylar notch between the patients with amputation and
the nonimpaired individuals (P 9 0.05) (Table 2). No significant correlation was found between the ultrasonographic measurements of femoral cartilage thickness and the patients’ clinical features including age, body mass index, time since amputation, time since receiving a prosthesis, daily standing/walking time with prosthesis, and K-levels (P 9 0.05).
TABLE 2 Ultrasonographic femoral cartilage thickness measures in the patients with amputation and the nonimpaired individuals
a
LFCCT, cm ICCT,a cm MFCCT,a cm
Patients with Amputation (n = 30)
Nonimpaired Individuals (n = 53)
P
0.185 (0.043) 0.207 (0.055) 0.187 (0.051)
0.203 (0.037) 0.207 (0.038) 0.205 (0.036)
0.041b 0.928 0.047b
a
Mean (standard deviation). Statistically significant. INCT, intercondylar notch cartilage thickness; LFCCT, lateral femoral condylar cartilage thickness; MFCCT, medial femoral condylar cartilage thickness. b
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DISCUSSION The knee cartilage in the intact limb knees of the patients with traumatic amputation was found to be thinner than in the knees of the nonimpaired individuals. Ultrasonographic measurement showed early femoral articular cartilage loss at the lateral and medial condyles in the intact limb knees of the patients with amputation. There was no correlation between knee cartilage thickness and the clinical features of the patients. The primary mechanism of premature joint degeneration in patients with amputation has been attributed to increased load on the intact limb and gait asymmetry.1,2 Patients with lower extremity amputation tend to use the intact limb to compensate for the amputated side, resulting in a greater load through the intact limb knee during walking.15 Reduced prosthetic limb push-off power leading to increased effort of the intact limb for walking balance is another explanation for the increased intact limb loading.16,17 A larger ground reaction force, as measured with force plates during walking, was found on the intact side compared with the prosthetic side and also in nonimpaired individuals.18,19 Bone mineral density at the proximal tibia of the intact side was also found to be larger than that of the amputated side, indicating a greater mechanical loading on the intact limb.20 Knee external adduction moment during load bearing is another potential biomechanical factor contributing to the onset and progression of knee osteoarthritis.21 Knee adduction moment describes the distribution of medial and lateral tibiofemoral compartment joint contact forces and correlates well with medial compartment loading.22 In the general population, knee osteoarthritis most commonly affects the medial compartment because of greater medial contact forces and knee adduction moment during normal gait.23,24 Knee external adduction moment in the intact knees of patients with transtibial amputation was found to be higher than in the amputated knee.18,25 This asymmetry in gait mechanics contributes to a predisposition to knee osteoarthritis in patients with amputation. There is only a single radiographic study concerning patterns of compartment involvement in intact knee osteoarthritis of patients with amputation compared with nonimpaired individuals. It showed a tendency to medial narrowing of the tibiofemoral joint space and patellofemoral degeneration in patients with amputation.6 This study demonstrated a significant cartilage loss at both the medial and lateral condyles of the femur. Compartment involvement in the intact limb knee osteoarthritis and its
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potential biomechanical explanations should be investigated in future research, which may help to develop rehabilitative strategies for the prevention and treatment of osteoarthritis in patients with amputation. An amputee with traumatic etiology probably has an increased risk for developing intact knee osteoarthritis in comparison with patients with amputation as a result of dysvascular etiology.1 Injury in these individuals often happens at a younger age, and they usually live longer compared with patients with amputation as a result of dysvascular etiology. In addition, they have a better ambulatory capacity as well as more participation in sports and work. These factors increase the exposure to abnormal gait mechanics over time. A previous ultrasound study in patients with amputation found increased cartilage loss on the amputated side compared with the intact side.26 Most of the participants in that study had amputation secondary to dysvascular disease, which may account for the confounding results. The lack of a control group in the study did not allow comparison with nonimpaired individuals. Research into osteoarthritis associated with amputation to show the increased risk in the intact limb could be better performed in subjects of traumatic origin. In the current study, despite the presence of significant cartilage loss, none of the participants matched the osteoarthritis criteria of the American College of Rheumatology. However, 30% reported pain and crepitus in the intact knee. There may be two explanations for this. First, the American College of Rheumatology clinical criteria have been suggested to reflect later signs in advanced disease and fail to identify early, mild osteoarthritis.27 Second, ultrasonography may be sensitive to reveal early cartilage damage before the clinical symptoms of the disease are seen. In addition, the mean of 7 yrs since amputation is a relatively shorter time compared with previous observational studies that have reported results from more than 25 yrs since amputation.2 It may take time for clinical osteoarthritis to show in the current study subjects. This short duration may also account for why the results did not show a correlation between cartilage thickness and time since amputation and receiving a prosthesis. This correlation may be found in a study group during a longer period. A limitation of this study is that the physical activity of the subjects was not measured with a more objective scale or test than K-levels. However, the mean age of the subjects in the study was 31 yrs, ranging from 22 to 41 yrs. None were older or assumed to be in bad physical condition. Another limitation is that no investigation was made into whether there was a difference in knee cartilage
Am. J. Phys. Med. Rehabil. & Vol. 94, No. 8, August 2015 Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.
thickness between the patients with transtibial and transfemoral amputation. A previous study found that patients with transfemoral amputation were at higher risk for knee pain than patients with transtibial amputation,4 although the number of patients with transfemoral amputation was not sufficient for statistical comparison. Whether the level of amputation may have an impact on knee cartilage thickness could be a topic for further investigations. There was also a technical limitation because ultrasonography can image only femoral articular cartilage. However, knee joint degeneration may also affect tibial and patellar articular cartilage, which were not assessed in this study. Finally, a limitation regarding the measurement technique is the challenge of controlling the exact obliquity angle of the transducer in relation to the femoral cartilage across the subjects. The transducer might be somewhat oblique to the trochlear groove, and so the cartilage thickness measurements might appear falsely large. Therefore, there might have been inaccuracies of measurements across the subjects. Naredo et al.9 showed good intrarater and interrater reliability for ultrasonographic knee cartilage measurement in their study comparing ultrasonographic and anatomic measurements in cadaver specimens. They found that ultrasound measurements were accurate in normal to moderately damaged cartilage but not in severely damaged cartilage. Moderate to substantial agreement was found between the ultrasound observers in femoral cartilage thickness measurements in the study of Abraham et al.28 Yoon et al.29 found no correlation between the transverse suprapatellar ultrasound scan and magnetic resonance imaging in the medial condyle, and that study showed high overall intrarater and interrater agreement in the ultrasound scan. It was concluded that ultrasound scan in the longitudinal plane is more feasible than suprapatellar transverse scan for cartilage measurement in the medial condyle. In the current study, the intrarater reliability was also found to be moderate to good for the measurements. Although the described ultrasound technique in this study has been widely used in previous studies,30Y35 considering the abovementioned concerns about the measurements, future studies with quantitative analysis of femoral articular cartilage using magnetic resonance imaging could be beneficial to confirm the result of this ultrasound study.
healthy subjects. This result supports the view that patients with traumatic lower extremity amputation are at increased risk for developing early knee degeneration in the intact limb. Clinicians should be aware of the importance of rehabilitation strategies aimed at decreasing onset and progression of knee osteoarthritis in patients with traumatic amputation. REFERENCES 1. Morgenroth DC, Gellhorn AC, Suri P: Osteoarthritis in the disabled population: A mechanical perspective. PM R 2012;4:20Y7 2. Gailey R, Allen K, Castles J, et al: Review of secondary physical conditions associated with lower-limb amputation and long-term prosthesis use. J Rehabil Res Dev 2008;45:15Y29 3. Hungerford D, Cockin J: Fate of the retained lower limb joints in second World War amputees. J Bone Joint Surg 1975;57:111 4. Norvell DC, Czerniecki JM, Reiber GE, et al: The prevalence of knee pain and symptomatic knee osteoarthritis among veteran traumatic amputees and nonamputees. Arch Phys Med Rehabil 2005;86:487Y93 5. Struyf PA, van Heugten CM, Hitters MW, et al: The prevalence of osteoarthritis of the intact hip and knee among traumatic leg amputees. Arch Phys Med Rehabil 2009;90:440Y6 6. Melzer I, Yekutiel M, Sukenik S: Comparative study of osteoarthritis of the contralateral knee joint of male amputees who do and do not play volleyball. J Rheumatol 2001;28:169Y72 7. Lemaire ED, Fisher FR: Osteoarthritis and elderly amputee gait. Arch Phys Med Rehabil 1994;75:1094Y9 8. Mazzuca SA, Brandt KD, Katz BP: Is conventional radiography suitable for evaluation of a diseasemodifying drug in patients with knee osteoarthritis? Osteoarthritis Cartilage 1997;5:217Y26 9. Naredo E, Acebes C, Mo¨ller I, et al: Ultrasound validity in the measurement of knee cartilage thickness. Ann Rheum Dis 2009;68:1322Y7 10. Saarakkala S, Waris P, Waris V, et al: Diagnostic performance of knee ultrasonography for detecting degenerative changes of articular cartilage. Osteoarthritis Cartilage 2012;20:376Y81 11. Liukkonen J, Hirvasniemi J, Joukainen A, et al: Arthroscopic ultrasound technique for simultaneous quantitative assessment of articular cartilage and subchondral bone: An in vitro and in vivo feasibility study. Ultrasound Med Biol 2013;39:1460Y8
CONCLUSIONS
12. Ozc¸akar L, Tunc¸ H, Oken O, et al: Femoral cartilage thickness measurements in healthy individuals learning, practicing and publishing with TURKMUSCULUS. J Back Musculoskelet Rehabil 2014; 27:117Y24. doi:10.3233/BMR-130441
This study showed that there was cartilage loss in the intact limb knee of the patients with traumatic amputation compared with the age-matched
13. HCFA Common Procedure Coding System HCPCS 2001. Washington, DC, US Government Printing Office, 2001. Ch 5.3
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14. Altman R, Asch E, Bloch D, et al: Development of criteria for the classification and reporting of osteoarthritis. Classification of osteoarthritis of the knee. Diagnostic and Therapeutic Criteria Committee of the American Rheumatism Association. Arthritis Rheum 1986;29:1039Y49 15. Mussman M, Altwerger W, Eisenstein J, et al: Contralateral lower extremity evaluation with a lower limb prosthesis. J Am Podiatry Assoc 1983; 73:344Y6 16. Winter DA, Sienko SE: Biomechanics of below-knee amputee gait. J Biomech 1988;21:361Y7
26. Akkaya N, Akkaya S, O¨zc¸akar L, et al: Ultrasonographic measurement of the distal femoral cartilage thickness in patients with unilateral transtibial amputation. Prosthet Orthot Int 2013;37:268Y74 27. Peat G, Thomas E, Duncan R, et al: Clinical classification criteria for knee osteoarthritis: Performance in the general population and primary care. Ann Rheum Dis 2006;65:1363Y7
17. Houdijk H, Pollmann E, Groenewold M, et al: The energy cost for the step-to-step transition in amputee walking. Gait Posture 2009;30:35Y40
28. Abraham AM, Goff I, Pearce MS, et al: Reliability and validity of ultrasound imaging of features of knee osteoarthritis in the community. BMC Musculoskelet Disord 2011;12:70
18. Lloyd CH, Stanhope SJ, Davis IS, et al: Strength asymmetry and osteoarthritis risk factors in unilateral trans-tibial, amputee gait. Gait Posture 2010; 32:296Y300
29. Yoon CH, Kim HS, Ju JH, et al: Validity of the sonographic longitudinal sagittal image for assessment of the cartilage thickness in the knee osteoarthritis. Clin Rheumatol 2008;27:1507Y16
19. Engsberg JR, Lee AG, Patterson JL, et al: External loading comparisons between able-bodied and belowknee-amputee children during walking. Arch Phys Med Rehabil 1991;72:657Y61
30. Kara M, Tiftik T, O¨ken O¨, et al: Ultrasonographic measurement of femoral cartilage thickness in patients with spinal cord injury. J Rehabil Med 2013;45:145Y8
20. Royer T, Koenig M: Joint loading and bone mineral density in persons with unilateral, trans-tibial amputation. Clin Biomech 2005;20:1119Y25 21. Vincent KR, Conrad BP, Fregly BJ, et al: The pathophysiology of osteoarthritis: A mechanical perspective on the knee joint. PM R 2012;4:3Y9 22. Zhao D, Banks SA, Mitchell KH, et al: Correlation between the knee adduction torque and medial contact force for a variety of gait patterns. J Orthopaed Res 2007;25:789Y97 23. Wise BL, Niu J, Yang M, et al; Multicenter Osteoarthritis (MOST) Group: Patterns of compartment involvement in tibiofemoral osteoarthritis in men and women and in whites and African Americans. Arthritis Care Res 2012;64:847Y52 24. Schipplein OD, Andriacchi TP: Interaction between active and passive knee stabilizers during level walking. J Orthop Res 1991;9:113Y9
608
25. Royer T, Wasilewski C: Hip and knee frontal plane moments in persons with unilateral, trans-tibial amputation. Gait Posture 2006;23:303Y6
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31. Akkaya S, Akkaya N, Ozcakar L, et al: Ultrasonographic evaluation of the femoral cartilage thickness after unilateral arthroscopic partial meniscectomy. Knee Surg Sports Traumatol Arthrosc 2013;21:1104Y10 32. Tunc¸ H, Oken O, Kara M, et al: Ultrasonographic measurement of the femoral cartilage thickness in hemiparetic patients after stroke. Int J Rehabil Res 2012;35:203Y7 33. O¨zgu¨l A, Gu¨nendi Z, Kesikburun S, et al: The association between patellar alignments features and tibiofemoral joint osteoarthritis. Clin Rheumatol 2013;32:1017Y20 34. CarlN AB, Akarsu S, Tekin L, et al: Ultrasonographic assessment of the femoral cartilage in osteoarthritis patients with and without osteoporosis. Aging Clin Exp Res 2014;26:411Y5 35. Kilic G, Kilic E, Akgul O, et al: Decreased femoral cartilage thickness in patients with systemic sclerosis. Am J Med Sci 2014;347:382Y6
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