JBJS | Interrelationships of Clinical Outcome, Length of Resection, and Energy Cost of Walking after Prosthetic Knee Replacement following Resection of a Malignant Tumor of the Distal Aspect of the Femur*

The Journal of Bone & Joint Surgery, Volume 80, Issue 6

Articles | June 01, 1998

Interrelationships of Clinical Outcome, Length of Resection, and Energy Cost of Walking after Prosthetic Knee Replacement following Resection of a Malignant Tumor of the Distal Aspect of the Femur*

AKIRA KAWAI, M.D., PH.D.†; SHERRY I. BACKUS, M.A., P.T.‡; JAMES C. OTIS, PH.D.‡; JOHN H. HEALEY, M.D.†, NEW YORK, N.Y.

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Investigation performed at the Memorial Sloan-Kettering Cancer Center and The Hospital for Special Surgery, New York City

The Journal of Bone & Joint Surgery. 1998; 80:822-31

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Abstract

The relationships between the functional score according to the system of the International Society of Limb Salvage, the extent of resection, energy cost of walking, and gait characteristics were studied in thirty-six patients who had had segmental knee replacement after resection of a malignant tumor of the distal aspect of the femur. The mean free-walking velocity was 62.3 meters per minute (79 per cent of normal), which was a result of decreases in both cadence and stride length. The mean net energy cost during walking was 35 per cent greater than that of normal controls and correlated with the percentage of the femur that had been resected. All patients had decreased single-limb support time on the affected side compared with the unaffected side. There was a weak correlation between the asymmetry of the single-limb support time and the percentage of the femur that had been resected. The mean extensor torque of the affected knee was 30 per cent that of the unaffected knee when one head of the quadriceps muscle had been excised, 19 per cent when two heads had been excised, 4 per cent when three heads had been excised, and 1 per cent when four heads had been excised. The patients who had had an extra-articular resection had lower mean extensor and flexor torques at the knee compared with those who had had an intra-articular resection. The asymmetry of the single-limb support time was inversely related to the residual extensor and flexor torques. The overall score according to the system of the International Society of Limb Salvage ranged from 17 to 29 points (mean, 24.6 points; 82 per cent of normal). The net energy cost, percentage of maximum aerobic capacity, and asymmetry of the single-limb support time had significant negative correlations with the overall functional score. Multivariate analysis showed that the overall functional score and the percentage of the femur that had been resected were the two most important factors that predicted the net energy cost. To our knowledge, this is the first objective validation of the functional score according to the system of the International Society of Limb Salvage. As the net energy cost can be predicted from universally available, inexpensive measures, investigators can easily use it as a clinical and research tool to evaluate prosthetic performance and to assess operative outcome.

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Introduction

Introduction | Materials and Methods | Results | Discussion | References

Most malignant tumors of the extremities are now treated with limb-sparing procedures. At major tumor centers, more than 80 per cent of the malignant tumors of the distal aspect of the femur are treated with en bloc excision of the femur and knee followed by reconstruction of the knee^2,9. There is considerable variation in the extent of the femoral and soft-tissue resection depending on the characteristics and location of the tumor. The development of prosthetic loosening or mechanical failure is related to the extent of the resection^2,15. However, we are not aware of any report that has shown a relationship between energy cost and gait characteristics and the magnitude of the resection in patients who have a prosthetic knee replacement.

The system of the International Society of Limb Salvage (Table I) is now widely used for reporting functional outcome after prosthetic replacement³. It is a subjective non-parametric system that encompasses several functional and emotional domains. Although its reproducibility was demonstrated in a multicenter study of patients who had a tumor³, the scores failed to correlate with objective measures of function after resection of periacetabular tumors and reconstruction⁶. We therefore evaluated the relationship between the scores obtained with this system and objective measures of function after resection of malignant musculoskeletal tumors followed by total knee replacement.

The first objective of the present study was to evaluate the relationships between the functional score according to the system of the International Society of Limb Salvage, gait characteristics, energy cost, and extent of the resection. The second objective was to determine which clinical parameters could be used to predict the energy cost of walking and to enable investigators to derive a value for this important functional parameter. Our results provide an objective basis for the functional evaluation of patients who have had a limb-sparing resection with reconstruction of the knee.

*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. Funds were received in total or partial support of the research or clinical study presented in this article. The funding source was the New York Marathon Limb Preservation Fund.

†Orthopaedic Surgery Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, N.Y. 10021. E-mail address for Dr. Healey: healeyj@mskcc.org.

‡Motion Analysis Laboratory (S. I. B.) and Department of Biomechanics and Biomaterials (J. C. O.). The Hospital for Special Surgery, 535 East 70th Street, New York, N.Y. 10021.

†Orthopaedic Surgery Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, New York, N.Y. 10021. E-mail address for Dr. Healey: healeyj@mskcc.org.

‡Motion Analysis Laboratory (S. I. B.) and Department of Biomechanics and Biomaterials (J. C. O.). The Hospital for Special Surgery, 535 East 70th Street, New York, N.Y. 10021.

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TABLE I SYSTEM OF THE INTERNATIONAL SOCIETY OF LIMB SALVAGE³

Score (points)	Pain	Function	Emotional Acceptance	Supports	Walking Ability	Gait
5	None	No restrictions	Enthused	None	Unlimited	Normal
4	Intermediate	Intermediate	Intermediate	Intermediate	Intermediate	Intermediate
3	Modest	Restriction in recreational activities	Satisfied	Brace	Limited	Minor cosmetic
2	Intermediate	Intermediate	Intermediate	Intermediate	Intermediate	Intermediate
1	Moderate	Partial disability	Accepts	One cane or crutch	Household	Major cosmetic, minor handicap
0	Severe	Total disability	Dislikes	Two canes or crutches	Unable to walk unaided	Major cosmetic, major handicap

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TABLE I SYSTEM OF THE INTERNATIONAL SOCIETY OF LIMB SALVAGE³

Score (points)	Pain	Function	Emotional Acceptance	Supports	Walking Ability	Gait
5	None	No restrictions	Enthused	None	Unlimited	Normal
4	Intermediate	Intermediate	Intermediate	Intermediate	Intermediate	Intermediate
3	Modest	Restriction in recreational activities	Satisfied	Brace	Limited	Minor cosmetic
2	Intermediate	Intermediate	Intermediate	Intermediate	Intermediate	Intermediate
1	Moderate	Partial disability	Accepts	One cane or crutch	Household	Major cosmetic, minor handicap
0	Severe	Total disability	Dislikes	Two canes or crutches	Unable to walk unaided	Major cosmetic, major handicap

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TABLE II DATA ON THE PATIENTS

*The patient used a cane at the time of the examination.

Case	Gender, Age at Op. (yrs.)	Diagnosis	Side	Type of Excision	Percentage of Femur Resected	No. of Heads of Quadriceps Excised	Transfer of Sartorius	Type of Prosthesis
1	F, 16	Osteosarcoma	L	Intra-articular	58	3	No	Lane-Burstein
2	M, 17	Osteosarcoma	R	Extra-articular	55	3	Yes	Lane-Burstein
3	F, 21	Malignant fibrous histiocytoma	L	Extra-articular	39	3	No	Lane-Burstein
4	M, 17	Osteosarcoma	L	Intra-articular	42	3	Yes	Lane-Burstein
5	F, 37	Osteosarcoma	L	Extra-articular	40	1	No	Lane-Burstein
6	M, 19	Osteosarcoma	R	Extra-articular	50	2	No	Lane-Burstein
7	F, 16	Osteosarcoma	L	Intra-articular	32	1	No	Lane-Burstein
8	M, 24	Osteosarcoma	R	Extra-articular	43	3	No	Lane-Burstein
9	M, 16	Osteosarcoma	L	Extra-articular	44	1	No	Lane-Burstein
10	M, 20	Osteosarcoma	R	Extra-articular	63	3	No	Lane-Burstein
11	M, 15	Osteosarcoma	R	Extra-articular	44	3	No	Lane-Burstein
12	M, 55	Chondrosarcoma	L	Intra-articular	45	1	No	Finn
13*	F, 37	Malignant fibrous histiocytoma	L	Extra-articular	31	2	No	Lane-Burstein
14	M, 22	Osteosarcoma	L	Extra-articular	33	1	No	Lane-Burstein
15	F, 17	Osteosarcoma	L	Intra-articular	45	1	No	Lane-Burstein
16	F, 14	Osteosarcoma	R	Intra-articular	30	2	No	Lane-Burstein
17	F, 22	Osteosarcoma	L	Intra-articular	42	1	No	Lane-Burstein
18	F, 19	Osteosarcoma	R	Extra-articular	40	3	No	Lane-Burstein
19	F, 20	Osteosarcoma	L	Extra-articular	38	4	No	Lane-Burstein
20	M, 36	Ewing sarcoma	L	Intra-articular	35	1	No	Lane-Burstein
21	F, 22	Ewing sarcoma	R	Extra-articular	30	2	Yes	Lane-Burstein
22	F, 21	Osteosarcoma	L	lntra-articular	37	1	No	Lane-Burstein
23	F, 20	Osteosarcoma	L	Extra-articular	49	3	Yes	Lane-Burstein
24	M, 27	Osteosarcoma	R	Intra-articular	50	2	No	Lane-Burstein
25	M, 18	Osteosarcoma	L	Intra-articular	40	3	No	Lane-Burstein
26	F, 24	Osteosarcoma	L	Extra-articular	35	4	No	Lane-Burstein
27*	F, 17	Osteosarcoma	R	Extra-articular	45	1	No	Lane-Burstein
28	F, 18	Osteosarcoma	R	Extra-articular	52	4	Yes	Lane-Burstein
29	F, 66	Lymphoma	L	Intra-articular	30	1	No	Finn
30	F, 16	Osteosarcoma	L	Extra-articular	35	3	No	Lane-Burstein
31	M, 17	Osteosarcoma	L	Intra-articular	30	2	No	Finn
32	F, 49	Osteosarcoma	R	Intra-articular	55	2	No	Lane-Burstein
33	M, 14	Osteosarcoma	L	Intra-articular	40	2	No	Lane-Burstein
34	M, 19	Osteosarcoma	L	Extra-articular	48	3	No	Lane-Burstein
35	F, 18	Osteosarcoma	L	Intra-articular	55	1	No	Lane-Burstein
36*	M, 22	Osteosarcoma	L	Extra-articular	43	3	No	Lane-Burstein

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TABLE II DATA ON THE PATIENTS

*The patient used a cane at the time of the examination.

Case	Gender, Age at Op. (yrs.)	Diagnosis	Side	Type of Excision	Percentage of Femur Resected	No. of Heads of Quadriceps Excised	Transfer of Sartorius	Type of Prosthesis
1	F, 16	Osteosarcoma	L	Intra-articular	58	3	No	Lane-Burstein
2	M, 17	Osteosarcoma	R	Extra-articular	55	3	Yes	Lane-Burstein
3	F, 21	Malignant fibrous histiocytoma	L	Extra-articular	39	3	No	Lane-Burstein
4	M, 17	Osteosarcoma	L	Intra-articular	42	3	Yes	Lane-Burstein
5	F, 37	Osteosarcoma	L	Extra-articular	40	1	No	Lane-Burstein
6	M, 19	Osteosarcoma	R	Extra-articular	50	2	No	Lane-Burstein
7	F, 16	Osteosarcoma	L	Intra-articular	32	1	No	Lane-Burstein
8	M, 24	Osteosarcoma	R	Extra-articular	43	3	No	Lane-Burstein
9	M, 16	Osteosarcoma	L	Extra-articular	44	1	No	Lane-Burstein
10	M, 20	Osteosarcoma	R	Extra-articular	63	3	No	Lane-Burstein
11	M, 15	Osteosarcoma	R	Extra-articular	44	3	No	Lane-Burstein
12	M, 55	Chondrosarcoma	L	Intra-articular	45	1	No	Finn
13*	F, 37	Malignant fibrous histiocytoma	L	Extra-articular	31	2	No	Lane-Burstein
14	M, 22	Osteosarcoma	L	Extra-articular	33	1	No	Lane-Burstein
15	F, 17	Osteosarcoma	L	Intra-articular	45	1	No	Lane-Burstein
16	F, 14	Osteosarcoma	R	Intra-articular	30	2	No	Lane-Burstein
17	F, 22	Osteosarcoma	L	Intra-articular	42	1	No	Lane-Burstein
18	F, 19	Osteosarcoma	R	Extra-articular	40	3	No	Lane-Burstein
19	F, 20	Osteosarcoma	L	Extra-articular	38	4	No	Lane-Burstein
20	M, 36	Ewing sarcoma	L	Intra-articular	35	1	No	Lane-Burstein
21	F, 22	Ewing sarcoma	R	Extra-articular	30	2	Yes	Lane-Burstein
22	F, 21	Osteosarcoma	L	lntra-articular	37	1	No	Lane-Burstein
23	F, 20	Osteosarcoma	L	Extra-articular	49	3	Yes	Lane-Burstein
24	M, 27	Osteosarcoma	R	Intra-articular	50	2	No	Lane-Burstein
25	M, 18	Osteosarcoma	L	Intra-articular	40	3	No	Lane-Burstein
26	F, 24	Osteosarcoma	L	Extra-articular	35	4	No	Lane-Burstein
27*	F, 17	Osteosarcoma	R	Extra-articular	45	1	No	Lane-Burstein
28	F, 18	Osteosarcoma	R	Extra-articular	52	4	Yes	Lane-Burstein
29	F, 66	Lymphoma	L	Intra-articular	30	1	No	Finn
30	F, 16	Osteosarcoma	L	Extra-articular	35	3	No	Lane-Burstein
31	M, 17	Osteosarcoma	L	Intra-articular	30	2	No	Finn
32	F, 49	Osteosarcoma	R	Intra-articular	55	2	No	Lane-Burstein
33	M, 14	Osteosarcoma	L	Intra-articular	40	2	No	Lane-Burstein
34	M, 19	Osteosarcoma	L	Extra-articular	48	3	No	Lane-Burstein
35	F, 18	Osteosarcoma	L	Intra-articular	55	1	No	Lane-Burstein
36*	M, 22	Osteosarcoma	L	Extra-articular	43	3	No	Lane-Burstein

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TABLE III ENERGY COST AND STRIDE CHARACTERISTICS

*The values are given as the mean and the standard deviation.

	Patients*	Controls*	P Value
Net energy cost (ml O2/m/kg)	0.23 ± 0.04	0.17 ± 0.02	<0.0001
Percentage of maximum aerobic capacity	38.5 ± 14.7	22.9 ± 5.8	<0.0001
Free velocity (m/min.)	62.3 ± 10.8	78.8 ± 9.7	<0.0001
Cadence (steps/min.)	97.4 ± 12.6	110.8 ± 7.2	<0.0001
Stride length (m)	1.27 ± 0.17	1.42 ± 0.14	<0.0001

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TABLE III ENERGY COST AND STRIDE CHARACTERISTICS

*The values are given as the mean and the standard deviation.

	Patients*	Controls*	P Value
Net energy cost (ml O2/m/kg)	0.23 ± 0.04	0.17 ± 0.02	<0.0001
Percentage of maximum aerobic capacity	38.5 ± 14.7	22.9 ± 5.8	<0.0001
Free velocity (m/min.)	62.3 ± 10.8	78.8 ± 9.7	<0.0001
Cadence (steps/min.)	97.4 ± 12.6	110.8 ± 7.2	<0.0001
Stride length (m)	1.27 ± 0.17	1.42 ± 0.14	<0.0001

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TABLE IV CORRELATION BETWEEN EACH PARAMETER OF THE SYSTEM OF THE INTERNATIONAL SOCIETY OF LIMB SALVAGE³ AND THE OVERALL FUNCTIONAL SCORE, EXTENT OF RESECTION, AND GAIT CHARATERISTICS*

*The values are given as the p values.

Parameter	Overall Functional Score³	Percentage of Femur Resected	No. of Heads of Quadriceps Excised	Net Energy Cost	Velocity	Asymmetry of Single-Limb Support Time
Pain	0.051	0.321	0.863	0.725	0.512	0.879
Function	0.001	0.681	0.466	0.182	0.585	0.081
Acceptance	0.008	0.555	0.501	0.397	0.389	0.307
Supports	0.004	0.621	0.290	0.223	0.528	0.611
Walking ability	<0.001	0.938	0.219	0.413	0.330	0.150
Gait	0.002	0.123	0.049	<0.001	0.019	<0.001

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TABLE IV CORRELATION BETWEEN EACH PARAMETER OF THE SYSTEM OF THE INTERNATIONAL SOCIETY OF LIMB SALVAGE³ AND THE OVERALL FUNCTIONAL SCORE, EXTENT OF RESECTION, AND GAIT CHARATERISTICS*

*The values are given as the p values.

Parameter	Overall Functional Score³	Percentage of Femur Resected	No. of Heads of Quadriceps Excised	Net Energy Cost	Velocity	Asymmetry of Single-Limb Support Time
Pain	0.051	0.321	0.863	0.725	0.512	0.879
Function	0.001	0.681	0.466	0.182	0.585	0.081
Acceptance	0.008	0.555	0.501	0.397	0.389	0.307
Supports	0.004	0.621	0.290	0.223	0.528	0.611
Walking ability	<0.001	0.938	0.219	0.413	0.330	0.150
Gait	0.002	0.123	0.049	<0.001	0.019	<0.001

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Fig. 1 Graph of the relationship between the percentage of the distal aspect of the femur that was resected and the net energy cost (r = 0.504, p = 0.004). The closed circles indicate patients who used a cane at the time of the examination.

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Fig. 2 Graph of the relationship between the percentage of the distal aspect of the femur that was resected and the percentage of maximum aerobic capacity (r = 0.500, p = 0.005). The closed circles indicate patients who used a cane at the time of the examination.

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Fig. 3 Graph of the relationship between the percentage of the distal aspect of the femur that was resected and the asymmetry of the single-limb support time (r = 0.395, p = 0.020). The closed circles indicate patients who used a cane at the time of the examination.

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Fig. 4 Graph of the relationship between the asymmetry of the single-limb support time and the free-walking velocity (r = -0.697, p < 0.0001). The closed circles indicate patients who used a cane at the time of the examination.

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Fig. 5 Graph of the relationship between asymmetry of the single-limb support time and the net energy cost (r = 0.647, p < 0.0001). The closed circles indicate patients who used a cane at the time of the examination.

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Fig. 6 Graph of the relationship between the number of heads of the quadriceps muscle that were excised and the residual extensor torque (p = 0.014). The open circles indicate patients who did not have transfer of the sartorius, the closed circles indicate patients who did have transfer of the sartorius, and the bars indicate the mean torque.

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Fig. 7 Graph of the relationship between the percentage of the distal aspect of the femur that was resected and the flexor torque (r = -0.496, p = 0.009). The closed circles indicate patients who used a cane at the time of the examination.

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Fig. 8 Graph of the relationship between net energy cost and the functional score according to the system of the International Society of Limb Salvage (ISOLS) (r = -0.562, p = 0.004). The closed circles indicate patients who used a cane at the time of the examination.

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Fig. 9 Graph of the relationship between the score for the gait parameter according to the system of the International Society of Limb Salvage and the net energy cost (r = -0.759, p < 0.001). The closed circles indicate patients who used a cane at the time of the examination.

Materials and Methods

Introduction | Materials and Methods | Results | Discussion | References

Thirty-six patients who had had a prosthetic knee replacement after resection of a malignant tumor of the distal aspect of the femur were examined (Table II). Sixteen of the patients were male and twenty were female. The mean age of the patients at the time of the operation was twenty-four years (range, fourteen to sixty-six years). The interval from the operation to the examination that was performed for the present study ranged from eighteen to fifty-two months (mean, twenty-six months). The diagnosis was osteosarcoma in thirty patients, Ewing sarcoma in two, malignant fibrous histiocytoma in two, chondrosarcoma in one, and lymphoma in one. The right side was affected in twelve patients and the left, in twenty-four.

Thirty-three Lane-Burstein knee prostheses and three Finn knee prostheses (Biomet, Warsaw, Indiana) were used in the reconstructions^4,9,12. The excision was extra-articular in twenty patients and intra-articular in sixteen. The amount of femoral bone that was resected ranged from twelve to twenty-seven centimeters (mean, 20.8 centimeters). A mean of 42 per cent (range, 30 to 63 per cent) of the femur was resected, as calculated from measurements of the femoral length from the femoral head to the knee joint on anteroposterior radiographs. Total excision of the quadriceps muscles or excision of all but the rectus femoris muscle was performed in sixteen patients. Five patients had anterior transfer of the sartorius muscle to the remaining patella or patellar ligament, which was intended to provide active extension of the knee.

Three patients used a cane at the time of the examination. All patients entering the study were advised of the potential hazards, benefits, and goals of the examination, and all consented to the program.

Eighteen male individuals and sixteen female individuals who did not have a neuromuscular or skeletal disease served as normal controls. The thirty-four controls ranged in age from fourteen to sixty-seven years (mean, twenty-seven years).

The oxygen consumption was determined with a Douglas-bag technique to collect expired air in meteorological balloons. Carbon dioxide content, oxygen content, and volume of expired air were measured for ninety-second collection intervals while the subject walked around a 19.8-meter rectangular walkway at a constant, self-selected free speed and then at a speed that was 20 per cent faster¹¹. A system of pacing lights attached to the perimeter of the walkway was used to control the walking velocity. Each patient walked with the affected limb toward the center of the track. The net energy cost (milliliters of oxygen per meter traveled per kilogram of body weight) and the percentage of predicted maximum aerobic capacity were determined. The predicted maximum aerobic capacity was the maximum rate of oxygen consumption for each subject as calculated with a linear regression analysis of the heart rate and the rate of oxygen consumption¹¹. The maximum heart rate⁷ was calculated as the patient's age subtracted from 220.

Stride characteristics were measured with the VA-Rancho Footswitch Stride Analyzer (Pathokinesiology Laboratory, Rancho Los Amigos Medical Center, Downey, California)¹⁰. This instrument consists of footswitches, an automatic stop-start controller, a waistpack recorder, a microprocessor, and a printer. Each subject was instructed to walk at his or her self-selected free speed, and stride was measured over the middle six meters of a ten-meter walkway. Data were collected during two trials, and the faster-speed trial was used for analysis. The measured parameters were velocity, cadence, stride length, gait-cycle time, and right and left single-limb support times.

Torque production about the knee joint was measured with a Cybex II isokinetic dynamometer (Lumex, Ronkonkoma, New York). The maximum voluntary isometric extensor and flexor torques were measured with the subject seated and the knee in 30 degrees of flexion. The torques were measured on the affected and unaffected sides, and the strength on the affected side was presented as a percentage of that on the unaffected side.

Overall function was determined with the revised criteria of the International Society of Limb Salvage³. Six parameters—pain, function, use of supports, walking ability, gait, and emotional acceptance—were evaluated and graded from 0 to 5 points. The scores for each of the parameters were added to obtain the overall functional score, which was expressed as a percentage of the total possible score of 30 points.

Statistical Analysis

The relationships between continuous variables were assessed by inspection of scatterplots, followed by linear regression analysis. A correlation coefficient was determined to measure the correlation between the variables. Statistical analysis was performed with the Statview 4.5 statistical package (Abacus Concepts, Berkeley, California). Differences between the groups were analyzed with the Student t test. A stepwise multivariate linear regression analysis, with backward elimination, was used to determine the factors that were most predictive of net energy cost. A p value of less than 0.05 was considered significant.

Results

Introduction | Materials and Methods | Results | Discussion | References

The mean free-walking velocity of the patients was 79 per cent that of the controls (p < 0.0001). This difference was attributed to a combination of slower cadence (88 per cent of normal) and reduced stride length (89 per cent of normal) (p < 0.0001) (Table III). The mean net energy cost for the patients was 135 per cent that for the controls, and the percentage of maximum aerobic capacity was 168 per cent (p < 0.0001 for both comparisons).

The net energy cost (r = 0.504, p = 0.004) (Fig. 1) and the percentage of maximum aerobic capacity (r = 0.500, p = 0.005) (Fig. 2) for the patients correlated with the percentage of the distal aspect of the femur that had been resected. Cadence had a significant negative correlation with the percentage that had been resected (r = -0.478, p = 0.004); however, stride length did not correlate with the percentage that had been resected (r = -0.131, p = 0.453). There was a trend toward negative correlation between velocity and the percentage of the distal aspect of the femur that had been resected (r = -0.306, p = 0.073).

All patients had a shorter single-limb support time on the affected side than on the unaffected side. The asymmetry of the single-limb support time (the difference between the single-limb support time on the unaffected side [mean, 0.51 ± 0.07 second] and that on the affected side [mean, 0.42 ± 0.05 second]) ranged from 0.01 to 0.32 second. There was a weak correlation between the asymmetry of the single-limb support time and the percentage of the femur that had been resected (r = 0.395, p = 0.020) (Fig. 3). The free-walking velocity had a negative correlation with the asymmetry of the single-limb support time (r = -0.697, p < 0.0001) (Fig. 4), and the net energy cost had a significant positive correlation with the asymmetry of the single-limb support time (r = 0.647, p < 0.0001) (Fig. 5).

Excision of the quadriceps ranged from removal of only the vastus intermedius to removal of all four heads of the muscle. There was a negative relationship between the extensor torque and the number of heads that had been excised. The mean extensor torque was 30 per cent after excision of one head of the quadriceps, 19 per cent after excision of two heads, 4 per cent after excision of three heads, and 1 per cent after excision of four heads (Fig. 6). Anterior transfer of the sartorius muscle did not significantly increase extensor torque. There was a weak negative correlation between the extensor torque and the percentage of the femur that had been resected (r = -0.396, p = 0.040). The flexor torque had a significant negative correlation with the percentage of the femur that had been resected (r = -0.496, p = 0.009) (Fig. 7). The asymmetry of the single-limb support time inversely correlated with the residual extensor torque (r = -0.356, p = 0.048) and flexor torque (r = -0.405, p = 0.025). There was a weak negative correlation between the net energy cost and the residual flexor torque (r = -0.367, p = 0.046).

The mean extensor and flexor torques in the patients who had had an extra-articular resection were 10.1 ± 17.5 per cent and 30.9 ± 12.9 per cent compared with 28.3 ± 18.3 per cent and 60.2 ± 37.3 per cent in the patients who had had an intra-articular resection. These differences were significant (p = 0.03 for the extensor torque and p = 0.006 for the flexor torque).

The mean functional score according to the system of the International Society for Limb Salvage was 24.6 points (range, 17 to 29 points), which was 82 per cent of normal. The net energy cost (r = -0.562, p = 0.004) (Fig. 8), percentage of maximum aerobic capacity (r = -0.436, p = 0.041), and asymmetry of the single-limb support time (r = -0.483, p = 0.013) had significant negative correlations with the overall functional score. No significant correlation could be found between the free-walking velocity (r = 0.186, p = 0.385), the percentage of the femur that had been resected (r = -0.072, p = 0.733), or the number of heads of the quadriceps that had been excised (r = -0.298, p = 0.157) and the overall functional score. The mean functional score was 26.1 points after excision of one head, 25.3 points after excision of two heads, 23.1 points after excision of three heads, and 24.0 points after excision of four heads.

The correlations between each parameter of the system of the International Society of Limb Salvage and the overall functional score, the extent of the resection, and the gait characteristics were determined (Table IV). The overall score had the strongest correlation with walking ability (r = -0.798, p < 0.001). Function and gait also strongly correlated with the overall functional score. The number of heads of the quadriceps muscles that had been excised had a weak correlation with gait (-0.432, p = 0.049). The net energy cost (r = -0.759, p < 0.001) (Fig. 9), velocity (r = 0.455, p = 0.019), and asymmetry of the single-limb support time (r = -0.695, p < 0.001) significantly correlated with gait.

With multivariate linear regression analysis, the functional score according to the system of the International Society of Limb Salvage and the percentage of the femur that had been resected were determined to be the factors that predicted the net energy cost. It was easy to predict the energy cost with use of the equation: net energy cost = 0.33 - 0.011 x functional score + 0.004 x percentage of the femur that had been resected. With use of this equation, the net energy cost was strongly correlated with the functional score and the percentage of the femur that had been resected (r = 0.812, p < 0.0001).

Walking consumed significantly less energy when the patient had a good functional score according to the system of the International Society of Limb Salvage and more energy when he or she had had a more extensive resection of the femur.

Discussion

Introduction | Materials and Methods | Results | Discussion | References

Limb-sparing procedures that involve removal of the knee and a portion of the femur for the treatment of malignant tumors result in a wide range of femoral and soft-tissue loss. It is important to understand the relationship between the extent of the resection and the anticipated function of the spared limb. In the present study, we explored this relationship and found that changes in energy cost, gait, and muscle torque were related to the extent of the resection. We also established the objective validity of the functional evaluation of the International Society of Limb Salvage for patients who have had a knee replacement.

The net energy cost during walking increased according to the percentage of the distal aspect of the femur that had been resected. Evaluation of energy cost on the basis of the measured oxygen consumption is the best method with which to compare the over-all gait performances of patients who have major alterations in the function of the lower extremities^5,8. Waters et al. demonstrated that oxygen cost increases with more proximal levels of amputation. One of us (J. C. O.) and colleagues found that oxygen consumption by patients who had had a segmental knee replacement after resection of a tumor at the knee joint was less than that by patients who had had an above-the-knee amputation after such a resection¹¹. The present study showed that the efficiency of gait after prosthetic knee replacement following resection of a malignant tumor is inversely related to the extent of the femoral and soft-tissue resections. The increased energy cost is likely due to inefficient additional muscle activity that is required to compensate for the lost function of the resected tissues.

To reduce the load on the affected lower limb, patients who have unilateral disease tend to have a shorter single-limb support time on the affected side^1,13. All patients in the present series had a shorter single-limb support time on the affected side, and the asymmetry correlated with the percentage of the femur that had been resected and the extent of the excision of the quadriceps muscle. During single-limb support, knee extensor activity is required to control the position of the knee in response to the knee flexion moment that is usually present at this time. The decrease in the single-limb support time with increasing excision of the quadriceps is consistent with the requirement of knee extensor activity during this phase of gait.

The asymmetry of the single-limb support time had a significant positive correlation with the net energy cost and a negative correlation with the free-walking velocity. We believe that the asymmetry of the single-limb support time is as important an indicator of the functional result for patients who have had prosthetic knee replacement after resection of a malignant tumor as it is for patients who have had pelvic reconstruction after internal hemipelvectomy⁶.

We found a negative relationship between the number of heads of the quadriceps muscle that were resected and residual extensor torque. With the use of ultrasound to quantitate muscle volume, Tsuboyama et al. showed a correlation between residual quadriceps muscle mass and extension strength of the knee. Although anterior transfer of the sartorius muscle in the present study improved soft-tissue coverage around the knee joint, it did not improve torque production in patients who had had extensive resection of the quadriceps muscle. This is not surprising, since the activity of the sartorius and quadriceps muscles are out of phase despite innervation by the femoral nerve. The muscle torques at the knee joint also had a significant negative correlation with the percentage of the femur that had been resected. It is possible that large tumors that required resection of a large segment of the distal aspect of the femur also necessitated an extensive resection of the surrounding muscles. There was a slight trend for longer osseous resections to have been performed in patients in whom more muscle had been excised, but this relationship failed to reach significance with the numbers available.

Although extra-articular resection is necessary to avoid contamination by the tumor in some patients, it requires extensive soft-tissue dissection, including removal of the extensor mechanisms. The present study showed that an extra-articular resection had a negative effect not only on the strength of the knee extensors but also on the strength of the knee flexors. Removal of more of the short head of the biceps with a more extensive femoral resection as well as release and resection of the semimembranosus and pes anserinus (medial knee flexors) may have contributed to this finding. With refinement of the ability to determine the extension of a tumor, the need for unnecessarily wide resections will be obviated and function after segmental knee replacement will be improved.

The functional evaluation system of the International Society of Limb Salvage is a subjective non-parametric system that encompasses several functional and emotional domains. We found that net energy cost and asymmetry of the single-limb support time had significant negative correlations with the overall functional score. As far as we know, this is the first objective evidence to validate this widely used functional evaluation system. The gait subscale of the evaluation system was significantly related to objective gait parameters.

Measurements of energy cost have not been readily available to most surgeons who evaluate the functional results for patients who have had resection of a tumor. However, this important functional parameter can be predicted with universally available, inexpensive measures and will enable investigators to calculate the energy cost of walking after limb-sparing reconstructions of the knee. Measurement of net energy cost will be an accessible clinical and research tool that will facilitate comparative studies of reconstructive procedures after excision of a tumor.

NOTE: The authors gratefully acknowledge Dr. Albert Burstein, who provided encouragement and guidance throughout every aspect of this project.

References

Introduction | Materials and Methods | Results | Discussion | References

Cammisa, F. P., Jr.; Glasser, D. B.; Otis, J. C.; Kroll, M. A.; Lane, J. M.; and Healey, J. H.: The Van Nes tibial rotationplasty. A functionally viable reconstructive procedure in children who have a tumor of the distal end of the femur. J. Bone and Joint Surg.,72-A: 1541-1547, Dec. 1990.72-A1541 1990

Capanna, R.; Morris, H. G.; Campanacci, D.; Del Ben, M.; and Campanacci, M.: Modular uncemented prosthetic reconstruction after resection of tumours of the distal femur. J. Bone and Joint Surg.,76-B(2): 178-186, 1994.76-B(2)178 1994

Enneking, W. F.; Dunham, W.; Gebhardt, M. C.; Malawar, M.; and Pritchard, D. J.: A system for the functional evaluation of reconstructive procedures after surgical treatment of tumors of the musculoskeletal system. Clin. Orthop.,286: 241-246, 1993.286241 1993 [PubMed]

Finn, H. A.; Golden, D.; Kneisl, J. A.; and Simon, M. A.: The Finn knee. In Complications of Limb Salvage, Prevention, Management and Outcome, pp. 413-416. Edited by K. L. B. Brown. Rennes, France, International Society of Limb Salvage, 1991.

Harris, I. E.; Leff, A. R.; Gitelis, S.; and Simon, M. A.: Function after amputation, arthrodesis, or arthroplasty for tumors about the knee. J. Bone and Joint Surg.,72-A: 1477-1485, Dec. 1990.72-A1477 1990

Healey, J. H.; Lane, J. M.; Marcove, R. C.; Duane, K.; and Otis, J. C.: Resection and reconstruction of periacetabular malignant and aggressive tumors. In New Developments for Limb Salvage in Musculoskeletal Tumors, pp. 443-450. Edited by T. Yamamuro. New York, Springer, 1989.

Londeree, B. R., and Moeschberger, M. L.: Effect of age and other factors on maximal heart rate. Res. Quart. Exerc. and Sport,53: 297-304, 1982.53297 1982

McClenaghan, B. A.; Krajbich, J. I.; Pirone, A. M.; Koheil, R.; and Longmuir, P.: Comparative assessment of gait after limb-salvage procedures. J. Bone and Joint Surg.,71-A: 1178-1182, Sept. 1989.71-A1178 1989

Muschler, G. F.; Ihara, K.; Lane, J. M.; Healey, J. H.; Levine, M. J.; Otis, J. C.; and Burstein, A. H.: A custom distal femoral prosthesis for reconstruction of large defects following wide excision for sarcoma: results and prognostic factors. Orthopedics,18: 527-538, 1995.18527 1995 [PubMed]

Otis, J. C., and Burstein, A. H.: Evaluation of the VA-Rancho gait analyzer, Mark I. Bull. Prosthet. Res.,10-35: 21-25, 1981.10-3521 1981 [PubMed]

Otis, J. C.; Lane, J. M.; and Kroll, M. A.: Energy cost during gait in osteosarcoma patients after resection and knee replacement and after above-the-knee amputation. J. Bone and Joint Surg.,67-A: 606-611, April 1985.67-A606 1985

Otis, J. C.; Burstein, A. H.; Lane, J. M.; Wright, T. M.; and Klein, R. W.: The HSS modular linked system for segmental replacement. In New Developments for Limb Salvage in Musculoskeletal Tumors, pp. 233-236. Edited by T. Yamamuro. New York, Springer, 1989.

Perry, J.: Gait Analysis: Normal and Pathological Function, pp. 3-16. Thorofare, New Jersey, Slack, 1992.

Tsuboyama, T.; Windhager, R.; and Kotz, R.: Quadriceps muscle mass and knee extension strength after limb-salvaging operation. In Limb Salvage Current Trends, p. 579. Rennes, France, International Society of Limb Salvage, 1993.

Unwin, P. S.; Cannon, S. R.; Grimer, R. J.; Kemp, H. B. S.; Sneath, R. S.; and Walker, P. S.: Aseptic loosening in cemented custom-made prosthetic replacements for bone tumours of the lower limb. J. Bone and Joint Surg.,78-B(1): 5-13, 1996.78-B(1)5 1996

Waters, R. L.; Perry, J.; Antonelli, D.; and Hislop, H.: Energy cost of walking of amputees: the influence of level of amputation. J. Bone and Joint Surg.,58-A: 42-46, Jan. 1976.58-A42 1976

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TABLE I SYSTEM OF THE INTERNATIONAL SOCIETY OF LIMB SALVAGE³

Score (points)	Pain	Function	Emotional Acceptance	Supports	Walking Ability	Gait
5	None	No restrictions	Enthused	None	Unlimited	Normal
4	Intermediate	Intermediate	Intermediate	Intermediate	Intermediate	Intermediate
3	Modest	Restriction in recreational activities	Satisfied	Brace	Limited	Minor cosmetic
2	Intermediate	Intermediate	Intermediate	Intermediate	Intermediate	Intermediate
1	Moderate	Partial disability	Accepts	One cane or crutch	Household	Major cosmetic, minor handicap
0	Severe	Total disability	Dislikes	Two canes or crutches	Unable to walk unaided	Major cosmetic, major handicap

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TABLE I SYSTEM OF THE INTERNATIONAL SOCIETY OF LIMB SALVAGE³

Score (points)	Pain	Function	Emotional Acceptance	Supports	Walking Ability	Gait
5	None	No restrictions	Enthused	None	Unlimited	Normal
4	Intermediate	Intermediate	Intermediate	Intermediate	Intermediate	Intermediate
3	Modest	Restriction in recreational activities	Satisfied	Brace	Limited	Minor cosmetic
2	Intermediate	Intermediate	Intermediate	Intermediate	Intermediate	Intermediate
1	Moderate	Partial disability	Accepts	One cane or crutch	Household	Major cosmetic, minor handicap
0	Severe	Total disability	Dislikes	Two canes or crutches	Unable to walk unaided	Major cosmetic, major handicap

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TABLE II DATA ON THE PATIENTS

*The patient used a cane at the time of the examination.

Case	Gender, Age at Op. (yrs.)	Diagnosis	Side	Type of Excision	Percentage of Femur Resected	No. of Heads of Quadriceps Excised	Transfer of Sartorius	Type of Prosthesis
1	F, 16	Osteosarcoma	L	Intra-articular	58	3	No	Lane-Burstein
2	M, 17	Osteosarcoma	R	Extra-articular	55	3	Yes	Lane-Burstein
3	F, 21	Malignant fibrous histiocytoma	L	Extra-articular	39	3	No	Lane-Burstein
4	M, 17	Osteosarcoma	L	Intra-articular	42	3	Yes	Lane-Burstein
5	F, 37	Osteosarcoma	L	Extra-articular	40	1	No	Lane-Burstein
6	M, 19	Osteosarcoma	R	Extra-articular	50	2	No	Lane-Burstein
7	F, 16	Osteosarcoma	L	Intra-articular	32	1	No	Lane-Burstein
8	M, 24	Osteosarcoma	R	Extra-articular	43	3	No	Lane-Burstein
9	M, 16	Osteosarcoma	L	Extra-articular	44	1	No	Lane-Burstein
10	M, 20	Osteosarcoma	R	Extra-articular	63	3	No	Lane-Burstein
11	M, 15	Osteosarcoma	R	Extra-articular	44	3	No	Lane-Burstein
12	M, 55	Chondrosarcoma	L	Intra-articular	45	1	No	Finn
13*	F, 37	Malignant fibrous histiocytoma	L	Extra-articular	31	2	No	Lane-Burstein
14	M, 22	Osteosarcoma	L	Extra-articular	33	1	No	Lane-Burstein
15	F, 17	Osteosarcoma	L	Intra-articular	45	1	No	Lane-Burstein
16	F, 14	Osteosarcoma	R	Intra-articular	30	2	No	Lane-Burstein
17	F, 22	Osteosarcoma	L	Intra-articular	42	1	No	Lane-Burstein
18	F, 19	Osteosarcoma	R	Extra-articular	40	3	No	Lane-Burstein
19	F, 20	Osteosarcoma	L	Extra-articular	38	4	No	Lane-Burstein
20	M, 36	Ewing sarcoma	L	Intra-articular	35	1	No	Lane-Burstein
21	F, 22	Ewing sarcoma	R	Extra-articular	30	2	Yes	Lane-Burstein
22	F, 21	Osteosarcoma	L	lntra-articular	37	1	No	Lane-Burstein
23	F, 20	Osteosarcoma	L	Extra-articular	49	3	Yes	Lane-Burstein
24	M, 27	Osteosarcoma	R	Intra-articular	50	2	No	Lane-Burstein
25	M, 18	Osteosarcoma	L	Intra-articular	40	3	No	Lane-Burstein
26	F, 24	Osteosarcoma	L	Extra-articular	35	4	No	Lane-Burstein
27*	F, 17	Osteosarcoma	R	Extra-articular	45	1	No	Lane-Burstein
28	F, 18	Osteosarcoma	R	Extra-articular	52	4	Yes	Lane-Burstein
29	F, 66	Lymphoma	L	Intra-articular	30	1	No	Finn
30	F, 16	Osteosarcoma	L	Extra-articular	35	3	No	Lane-Burstein
31	M, 17	Osteosarcoma	L	Intra-articular	30	2	No	Finn
32	F, 49	Osteosarcoma	R	Intra-articular	55	2	No	Lane-Burstein
33	M, 14	Osteosarcoma	L	Intra-articular	40	2	No	Lane-Burstein
34	M, 19	Osteosarcoma	L	Extra-articular	48	3	No	Lane-Burstein
35	F, 18	Osteosarcoma	L	Intra-articular	55	1	No	Lane-Burstein
36*	M, 22	Osteosarcoma	L	Extra-articular	43	3	No	Lane-Burstein

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TABLE II DATA ON THE PATIENTS

*The patient used a cane at the time of the examination.

Case	Gender, Age at Op. (yrs.)	Diagnosis	Side	Type of Excision	Percentage of Femur Resected	No. of Heads of Quadriceps Excised	Transfer of Sartorius	Type of Prosthesis
1	F, 16	Osteosarcoma	L	Intra-articular	58	3	No	Lane-Burstein
2	M, 17	Osteosarcoma	R	Extra-articular	55	3	Yes	Lane-Burstein
3	F, 21	Malignant fibrous histiocytoma	L	Extra-articular	39	3	No	Lane-Burstein
4	M, 17	Osteosarcoma	L	Intra-articular	42	3	Yes	Lane-Burstein
5	F, 37	Osteosarcoma	L	Extra-articular	40	1	No	Lane-Burstein
6	M, 19	Osteosarcoma	R	Extra-articular	50	2	No	Lane-Burstein
7	F, 16	Osteosarcoma	L	Intra-articular	32	1	No	Lane-Burstein
8	M, 24	Osteosarcoma	R	Extra-articular	43	3	No	Lane-Burstein
9	M, 16	Osteosarcoma	L	Extra-articular	44	1	No	Lane-Burstein
10	M, 20	Osteosarcoma	R	Extra-articular	63	3	No	Lane-Burstein
11	M, 15	Osteosarcoma	R	Extra-articular	44	3	No	Lane-Burstein
12	M, 55	Chondrosarcoma	L	Intra-articular	45	1	No	Finn
13*	F, 37	Malignant fibrous histiocytoma	L	Extra-articular	31	2	No	Lane-Burstein
14	M, 22	Osteosarcoma	L	Extra-articular	33	1	No	Lane-Burstein
15	F, 17	Osteosarcoma	L	Intra-articular	45	1	No	Lane-Burstein
16	F, 14	Osteosarcoma	R	Intra-articular	30	2	No	Lane-Burstein
17	F, 22	Osteosarcoma	L	Intra-articular	42	1	No	Lane-Burstein
18	F, 19	Osteosarcoma	R	Extra-articular	40	3	No	Lane-Burstein
19	F, 20	Osteosarcoma	L	Extra-articular	38	4	No	Lane-Burstein
20	M, 36	Ewing sarcoma	L	Intra-articular	35	1	No	Lane-Burstein
21	F, 22	Ewing sarcoma	R	Extra-articular	30	2	Yes	Lane-Burstein
22	F, 21	Osteosarcoma	L	lntra-articular	37	1	No	Lane-Burstein
23	F, 20	Osteosarcoma	L	Extra-articular	49	3	Yes	Lane-Burstein
24	M, 27	Osteosarcoma	R	Intra-articular	50	2	No	Lane-Burstein
25	M, 18	Osteosarcoma	L	Intra-articular	40	3	No	Lane-Burstein
26	F, 24	Osteosarcoma	L	Extra-articular	35	4	No	Lane-Burstein
27*	F, 17	Osteosarcoma	R	Extra-articular	45	1	No	Lane-Burstein
28	F, 18	Osteosarcoma	R	Extra-articular	52	4	Yes	Lane-Burstein
29	F, 66	Lymphoma	L	Intra-articular	30	1	No	Finn
30	F, 16	Osteosarcoma	L	Extra-articular	35	3	No	Lane-Burstein
31	M, 17	Osteosarcoma	L	Intra-articular	30	2	No	Finn
32	F, 49	Osteosarcoma	R	Intra-articular	55	2	No	Lane-Burstein
33	M, 14	Osteosarcoma	L	Intra-articular	40	2	No	Lane-Burstein
34	M, 19	Osteosarcoma	L	Extra-articular	48	3	No	Lane-Burstein
35	F, 18	Osteosarcoma	L	Intra-articular	55	1	No	Lane-Burstein
36*	M, 22	Osteosarcoma	L	Extra-articular	43	3	No	Lane-Burstein

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TABLE III ENERGY COST AND STRIDE CHARACTERISTICS

*The values are given as the mean and the standard deviation.

	Patients*	Controls*	P Value
Net energy cost (ml O2/m/kg)	0.23 ± 0.04	0.17 ± 0.02	<0.0001
Percentage of maximum aerobic capacity	38.5 ± 14.7	22.9 ± 5.8	<0.0001
Free velocity (m/min.)	62.3 ± 10.8	78.8 ± 9.7	<0.0001
Cadence (steps/min.)	97.4 ± 12.6	110.8 ± 7.2	<0.0001
Stride length (m)	1.27 ± 0.17	1.42 ± 0.14	<0.0001

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TABLE III ENERGY COST AND STRIDE CHARACTERISTICS

*The values are given as the mean and the standard deviation.

	Patients*	Controls*	P Value
Net energy cost (ml O2/m/kg)	0.23 ± 0.04	0.17 ± 0.02	<0.0001
Percentage of maximum aerobic capacity	38.5 ± 14.7	22.9 ± 5.8	<0.0001
Free velocity (m/min.)	62.3 ± 10.8	78.8 ± 9.7	<0.0001
Cadence (steps/min.)	97.4 ± 12.6	110.8 ± 7.2	<0.0001
Stride length (m)	1.27 ± 0.17	1.42 ± 0.14	<0.0001

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TABLE IV CORRELATION BETWEEN EACH PARAMETER OF THE SYSTEM OF THE INTERNATIONAL SOCIETY OF LIMB SALVAGE³ AND THE OVERALL FUNCTIONAL SCORE, EXTENT OF RESECTION, AND GAIT CHARATERISTICS*

*The values are given as the p values.

Parameter	Overall Functional Score³	Percentage of Femur Resected	No. of Heads of Quadriceps Excised	Net Energy Cost	Velocity	Asymmetry of Single-Limb Support Time
Pain	0.051	0.321	0.863	0.725	0.512	0.879
Function	0.001	0.681	0.466	0.182	0.585	0.081
Acceptance	0.008	0.555	0.501	0.397	0.389	0.307
Supports	0.004	0.621	0.290	0.223	0.528	0.611
Walking ability	<0.001	0.938	0.219	0.413	0.330	0.150
Gait	0.002	0.123	0.049	<0.001	0.019	<0.001

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TABLE IV CORRELATION BETWEEN EACH PARAMETER OF THE SYSTEM OF THE INTERNATIONAL SOCIETY OF LIMB SALVAGE³ AND THE OVERALL FUNCTIONAL SCORE, EXTENT OF RESECTION, AND GAIT CHARATERISTICS*

*The values are given as the p values.

Parameter	Overall Functional Score³	Percentage of Femur Resected	No. of Heads of Quadriceps Excised	Net Energy Cost	Velocity	Asymmetry of Single-Limb Support Time
Pain	0.051	0.321	0.863	0.725	0.512	0.879
Function	0.001	0.681	0.466	0.182	0.585	0.081
Acceptance	0.008	0.555	0.501	0.397	0.389	0.307
Supports	0.004	0.621	0.290	0.223	0.528	0.611
Walking ability	<0.001	0.938	0.219	0.413	0.330	0.150
Gait	0.002	0.123	0.049	<0.001	0.019	<0.001

Londeree, B. R., and Moeschberger, M. L.: Effect of age and other factors on maximal heart rate. Res. Quart. Exerc. and Sport,53: 297-304, 1982.53297 1982

Otis, J. C., and Burstein, A. H.: Evaluation of the VA-Rancho gait analyzer, Mark I. Bull. Prosthet. Res.,10-35: 21-25, 1981.10-3521 1981 [PubMed]

Perry, J.: Gait Analysis: Normal and Pathological Function, pp. 3-16. Thorofare, New Jersey, Slack, 1992.

Waters, R. L.; Perry, J.; Antonelli, D.; and Hislop, H.: Energy cost of walking of amputees: the influence of level of amputation. J. Bone and Joint Surg.,58-A: 42-46, Jan. 1976.58-A42 1976

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AKIRA KAWAI, SHERRY I. BACKUS, JAMES C. OTIS, JOHN H. HEALEY; Interrelationships of Clinical Outcome, Length of Resection, and Energy Cost of Walking after Prosthetic Knee Replacement following Resection of a Malignant Tumor of the Distal Aspect of the Femur*. The Journal of Bone & Joint Surgery. 1998 Jun;80(6):822-31.

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