The Journal of Bone & Joint Surgery

The Journal of Bone & Joint Surgery, Volume 83, Issue 8

Articles | August 01, 2001

Regional Osteoporosis in Women Who Have a Complete Spinal Cord Injury

Douglas E. Garland, MD; Rodney H. Adkins, PhD; Charles A. Stewart, MD; Roy Ashford, MD; Daniel Vigil, MD

Investigation performed at Rancho Los Amigos National Rehabilitation Center, Downey, California
Douglas E. Garland, MD
Rodney H. Adkins, PhD
Charles A. Stewart, MD
Roy Ashford, MD
Daniel Vigil, MD
Neurotrauma Division (D.E.G., R.A., and D.V.), Rehabilitation Research and Training Center on Aging with Spinal Cord Injury (D.E.G. and R.H.A.), Regional Spinal Cord Injury Care System of Southern California (D.E.G. and R.H.A.), and Department of Medical Imaging (C.A.S.), Rancho Los Amigos National Rehabilitation Center, 7601 East Imperial Highway, Downey, CA 90242
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 sources were Grants H133N00026, H133830029, and H133B70011 from the National Institute on Disability and Rehabilitation Research, Office of Special Education and Rehabilitative Services, United States Department of Education, Washington, DC.

J Bone Joint Surg Am, 2001 Aug 01;83(8):1195-1200

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Abstract

Background: Regional bone loss in patients who have a spinal cord injury has been evaluated in males. In addition, there have been reports on groups of patients of both genders who had an acute or chronic complete or incomplete spinal cord injury. Regional bone loss in females who have a complete spinal cord injury has not been reported, to our knowledge.

Methods: In a study of thirty-one women who had a chronic, complete spinal cord injury, we assessed bone mineral density in relation to age, weight, and time since the injury. The results were compared with the bone mineral density in seventeen healthy, able-bodied women who had been age-matched by group (thirty years old and less, thirty-one to fifty years old, and more than fifty years old). Dual-energy x-ray absorptiometry was used to measure the bone mineral density of the lumbar spine, hip, and knee; Z-scores for the hip and spine were calculated.

Results: The mean bone mineral density in the spine in the youngest, middle, and oldest spinal-cord-injury groups was 98%, 108%, and 115% of the densities in the respective age-matched control groups (p < 0.0001), and the mean bone mineral density in the oldest spinal-cord-injury group was equal to that in the youngest control group. This gain in bone mineral density in the spine was reflected by the spine Z-scores, as the mean score in the oldest injured group averaged more than one standard deviation above both the norm and the mean score in the control group. The mean loss of bone mineral density in the knee in the youngest, middle, and oldest spinal-cord-injury groups was 38%, 41%, and 47% compared with the densities in the corresponding control age-groups (p < 0.0001). Furthermore, the oldest injured group had a mean reduction of knee bone mineral density of 54% compared with the youngest control group. The mean loss of bone mineral density in the hips of the injured patients was 18%, 25%, and 25% compared with the densities in the control subjects in the respective age-groups (p < 0.0001).

Conclusions: The bone mineral density in the spine either was maintained or was increased in relation to the time since the injury. This finding is unlike that seen in healthy women, in whom bone mineral density decreases with age. The bone mineral density in the hips of the injured patients initially decreased approximately 25%; thereafter, the rate of loss was similar to that in the control group. The bone mineral density in the knees of the injured patients rapidly decreased 40% to 45% and then further decreased only minimally.

Clinical Relevance: The results provide a partial explanation of the fracture patterns seen after spinal cord injuries. Vertebral fractures rarely occur, whereas the knee is at risk for fracture soon after the spinal cord injury. The potential for fracture of the hip also occurs soon after the spinal cord injury. This risk increases with age and the amount of time since the spinal cord injury.

Figures in this Article

Introduction

It is believed that, in patients who have a complete spinal cord injury, disuse osteoporosis develops distal to the level of the injury, leading to an increased prevalence of pathological fractures. In the past, bone loss could be detected only biochemically, and the sites of the loss were left to conjecture^1-3. Clinical reports of a higher prevalence of pathological fractures of the knee suggested that there was more bone loss in the knee than in the hip^4-7.

The sites of skeletal bone loss can now be more accurately determined with use of densitometry, and most of the bone loss has been reported to occur in the lower extremities. It has also been reported that bone mineral density may remain relatively unchanged or may actually increase in the lumbar spine following spinal cord injury^8-12.

Spinal cord injury is uncommon in women, with a male-to-female ratio of approximately four to one¹³. In a series of women who had a chronic, complete spinal cord injury, we studied the regional changes in bone mineral density to assess any association with age, body weight, and time since the injury.

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Fig. 1-A:: The relationships between age and the spine Z-scores for the women with spinal cord injury (SCI) and the able-bodied women (non-SCI) demonstrate that spine Z-scores in spinal-cord-injured women increase with age (thin solid line) when compared with expected values for the general population. This effect most likely reflects increased or maintained bone density in spinal-cord-injured women as their age increases.

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Fig. 1-B:: The relationship between the duration of injury (in years) and the spine Z-scores. The stepwise multiple regression analysis used to assess multiple associations demonstrated that the time since the injury, not the age of the injured woman, accounted for the increasing bone density relative to age.

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TABLE I: Bone Mineral Density (g/cm²)*

*Adjusted for participant’s weight in pounds.

	Knee	Hip	Spine
Age £30 yr
Control
Mean and standard deviation	0.95 0.18	0.80 0.09	1.02 0.11
Adjusted mean*	0.95	0.80	1.01
Spinal cord injury
Mean and standard deviation	0.58 ± 0.11	0.65 ± 0.15	0.97 ± 0.22
Adjusted mean*	0.59	0.66	0.99
Age 31-50 yr
Control
Mean and standard deviation	0.93 ± 0.18	0.74 ± 0.25	1.02 ± 0.17
Adjusted mean*	0.92	0.72	0.99
Spinal cord injury
Mean and standard deviation	0.52 ± 0.13	0.52 ± 0.11	0.05 ± 0.15
Adjusted mean*	0.54	0.54	1.07
Age >50 yr
Control
Mean and standard deviation	0.83 ± 0.09	0.51 ± 0.14	0.88 ± 0.14
Adjusted mean*	0.83	0.51	0.88
Spinal cord injury
Mean and standard deviation	0.45 ± 0.12	0.39 ± 0.18	1.02 ± 0.14
Adjusted mean*	0.44	0.38	1.01

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TABLE I: Bone Mineral Density (g/cm²)*

*Adjusted for participant’s weight in pounds.

	Knee	Hip	Spine
Age £30 yr
Control
Mean and standard deviation	0.95 0.18	0.80 0.09	1.02 0.11
Adjusted mean*	0.95	0.80	1.01
Spinal cord injury
Mean and standard deviation	0.58 ± 0.11	0.65 ± 0.15	0.97 ± 0.22
Adjusted mean*	0.59	0.66	0.99
Age 31-50 yr
Control
Mean and standard deviation	0.93 ± 0.18	0.74 ± 0.25	1.02 ± 0.17
Adjusted mean*	0.92	0.72	0.99
Spinal cord injury
Mean and standard deviation	0.52 ± 0.13	0.52 ± 0.11	0.05 ± 0.15
Adjusted mean*	0.54	0.54	1.07
Age >50 yr
Control
Mean and standard deviation	0.83 ± 0.09	0.51 ± 0.14	0.88 ± 0.14
Adjusted mean*	0.83	0.51	0.88
Spinal cord injury
Mean and standard deviation	0.45 ± 0.12	0.39 ± 0.18	1.02 ± 0.14
Adjusted mean*	0.44	0.38	1.01

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TABLE II: Age-Normalized Z-Scores

*Adjusted for participant’s weight in pounds.

	Hip	Spine
Age £30 yr
Control
Mean	0.33	0.47
Adjusted mean*	0.27	0.37
Spinal cord injury
Mean	-1.13	-0.53
Adjusted mean*	-1.01	-0.31
Age 31-50 yr
Control
Mean	1.01	0.34
Adjusted mean*	0.86	0.08
Spinal cord injury
Mean	-1.33	0.52
Adjusted mean*	-1.17	0.77
Age >50 yr
Control
Mean	-0.42	-0.34
Adjusted mean*	-0.39	-0.28
Spinal cord injury
Mean	-1.14	1.31
Adjusted mean*	-1.24	1.14

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TABLE II: Age-Normalized Z-Scores

*Adjusted for participant’s weight in pounds.

	Hip	Spine
Age £30 yr
Control
Mean	0.33	0.47
Adjusted mean*	0.27	0.37
Spinal cord injury
Mean	-1.13	-0.53
Adjusted mean*	-1.01	-0.31
Age 31-50 yr
Control
Mean	1.01	0.34
Adjusted mean*	0.86	0.08
Spinal cord injury
Mean	-1.33	0.52
Adjusted mean*	-1.17	0.77
Age >50 yr
Control
Mean	-0.42	-0.34
Adjusted mean*	-0.39	-0.28
Spinal cord injury
Mean	-1.14	1.31
Adjusted mean*	-1.24	1.14

Materials and Methods

This prospective study was performed, after approval by our institutional review board, to evaluate bone mineral density in thirty-one women (see Appendix) who had a chronic, complete spinal cord injury at the cervical or thoracic level and were unable to walk, though they were able to participate in wheelchair activities. Seventeen able-bodied women, recruited from the staff of the medical center, served as controls. The control subjects were questioned to identify risk factors for osteoporosis. Individuals who smoked one or more packs of cigarettes per day, consumed more than two alcoholic drinks per day, had a systemic disease, or were taking medication for possible osteoporosis were excluded from the study. Injured women who had used birth control medication for more than five years or who had heterotopic ossification or osteoarthrosis were also excluded from the study.

All individuals were grouped according to age. Group-I individuals (thirty years of age and less) were said to be in their active-bone-building years. This group included six injured patients who had a mean age and standard deviation of 25.7 ± 4.2 years (median, twenty-seven years; range, twenty to thirty years) and five controls who had a mean age of 27.4 ± 1.7 years (median, twenty-seven years; range, twenty-six to thirty years). The mean time from the injury was 5.7 ± 2.3 years (median, six years; range, two to eight years). Three control subjects used oral contraceptives, but it was unlikely that they had had appreciable bone loss that would have been offset by the contraceptives.

Group-II individuals (thirty-one to fifty years of age) were at the beginning of the period of age-related bone loss. In this group, there were sixteen injured women who had a mean age of 41.1 ± 6.2 years (median, 41.5 years; range, thirty-one to fifty years) and seven able-bodied women who had a mean age of 47.4 ± 2.4 years (median, forty-eight years; range, forty-four to fifty years). The mean time from the injury was 16.1 ± 9.4 years (median, 15.5 years; range, three to thirty years). None of the patients had a history of chronic medical problems or used medications known to affect bone metabolism. One member of the control group was taking oral contraceptives.

Group-III individuals (more than fifty years of age) were in the postmenopausal years, which typically are characterized by accelerated bone loss. There were nine injured women who had a mean age of 64.9 ± 7.9 years (median, sixty-seven years; range, fifty-three to seventy-seven years) and five able-bodied women who had a mean age of 59.4 ± 2.7 years (median, fifty-nine years; range, fifty-six to sixty-three years). The mean time from the injury was 28.9 ± 11.4 years (median, thirty years; range, nine to forty-four years). One of the women in the control group smoked occasionally. All of the women in this group had reached menopause, although they could not precisely define the time at which menopause had begun.

Dual-energy x-ray absorptiometry (DEXA) was used to estimate bone mineral density of the lumbar spine, hip, and knee (QDR-2000; Hologic, Waltham, Massachusetts). Race, gender, and age-matched reference norms were available for the hip and spine but not for the knee; thus, the Z-scores (the number of standard deviations that the bone mineral density measurement of the subject was above or below the bone mineral density norm) could be calculated for the hip and spine but not for the knee. Bone mineral density in the lumbar spine was measured on position-synchronized anteroposterior images made with the subject supine; that in the hip was measured on an anteroposterior image of Ward’s triangle; and that in the knee was the net mean of the density of the distal part of the femur and the proximal part of the tibia as measured on scans with a modification of the FM-1 Forearm Application Protocol software (Hologic). All scans were reviewed by one of us, an experienced radiologist. Plain radiographs were evaluated when questionable abnormalities were noted on dual-energy x-ray absorptiometry scans¹⁴.

We performed a multivariate analysis of covariance with two between factors (three age-groups and two deficit-groups [injured and controls]) controlling for participant weight, as body weight has been reported to alter bone mineral density¹⁵. This was followed by the appropriate univariate analyses of variance. The effects of age, weight, and time since the injury in the patients and the effects of age and weight in the controls were determined with correlation and stepwise multiple regression analyses.

Results

Knee

The mean weight-adjusted bone mineral density in the knees of the injured patients was reduced by 38% in Group I (1 — [0.59/0.95]), 41% in Group II (1 — [0.54/0.92]), and 47% in Group III (1 — [0.44/0.83]) compared with the density values in the corresponding control groups (Table I). The comparisons between the injured and control subjects in the three groups showed that the major factor influencing the loss of bone mineral density in the knee was the injury. The difference between the injured patients and the control subjects (in all three age-groups) was highly significant regardless of age (p < 0.0001). There was a modest correlation of bone mineral density with age and with the time since the injury (r = — 0.34, p = 0.032, and r = — 0.32, p = 0.037, respectively); however, stepwise multiple regression analyses showed no significance.

Hip

The mean weight-adjusted bone mineral density in the hips of the injured patients was reduced by 18% in Group I (1 — [0.66/0.80]), 25% in Group II (1 — [0.54/0.72]), and 25% in Group III (1 — [0.38/0.51]) compared with the bone mineral densities in the corresponding control groups. The mean bone mineral density in the hips of the injured group was significantly decreased regardless of age (p < 0.0001). Multivariate analysis of covariance revealed the differences between the weight-adjusted means of the injured patients and the control subjects to be similar in all three age-groups. The differences between the mean hip Z-scores in the control and injured groups were also significant (p = 0.009) (Table II).

In the injured patients, the correlation between bone mineral density in the hip and age (r = —0.58, p = 0.001) and time since injury (r = -0.36, p = 0.025) seemed to be significant. Stepwise multiple regression analysis showed a significant negative relationship between age and bone mineral density (p = 0.0006).

Spine

In comparison with the values in the corresponding control groups, the weight-adjusted mean bone mineral density in the spine was decreased by 2% in the injured Group-I patients but was increased by 8% in the injured Group-II patients and by 15% in the injured Group-III patients. We found the bone mineral density in the spine in the oldest injured patients to be equal to that in the youngest control individuals. Furthermore, Z-scores decreased with age in the control population whereas they increased with age in the injured groups (p = 0.049) (Table II, Fig. 1-A).

In the injured patients, the correlation of bone mineral density in the spine with body weight was significant (r = 0.42, p = 0.01). Stepwise multiple regression analyses of the multiple associations of bone mineral density with age, body weight, and time since the injury reflected a similar correlation (p = 0.02). The correlations between spine Z-scores and age (r = 0.46, p = 0.004), body weight (r = 0.55, p = 0.001), and time since the injury (r = 0.51, p = 0.002) were significant.

There was a significant positive association between increased bone mineral density in the spine and the time since the injury (p = 0.005) (Fig. 1-B). Approximately 50% of individuals who sustain a spinal cord injury are between eighteen and twenty-five years old and 75% are less than thirty-five years old, suggesting that there should be a high correlation between age and duration of injury (r = 0.72, p < 0.001). However, stepwise multiple regression analysis demonstrated that the time since the injury, not the age of the injured patient, was related to the increase in bone mineral density relative to age.

Stepwise multiple regression analyses indicated that weight accounted for 30% of the variance in the spine Z-scores of the injured patients and the time since the injury accounted for an additional 18%. The remaining 52% of the differences in the Z-scores could be related to the mechanism of the injury, genetic factors, and diet; however, there were insufficient data on such other factors to further analyze their role. The relationships between spine Z-scores and weight (p = 0.002) and time since the injury (p = 0.005) were significant.

Discussion

In healthy women, bone mass generally increases substantially until the age of twenty years, with minimal increases continuing until the age of thirty-five to forty years, when age-related bone loss usually begins^15-17. Bone loss is accelerated with the onset of menopause, after which a loss of 2% to 3% per year has been reported¹⁸. Trabecular bone loss is more rapid and greater than is cortical bone loss; therefore, there is an increase in the risk of fracture of the spine, hip, metaphyseal regions of the knee, distal part of the radius, and proximal part of the humerus¹⁸.

A cross-sectional study of the lumbar spine in 105 women, twenty to eighty-nine years old, demonstrated a peak bone mineral density measuring 1.4 g/cm² before the age of thirty years¹⁷. Bone loss did not occur until the age of fifty years, and it continued in a linear pattern at a rate of 0.0082 g/cm² per year until the age of sixty-five years. The predicted mean bone mineral density in a ninety-year-old woman is 42% of the mean when she was twenty years old¹⁸. A cross-sectional study of 123 women19, twenty to ninety-two years old, revealed a similar peak bone mineral density in the neck of the femur (1.4 g/cm²), and the bone loss was linear at 0.0129 g/cm² per year. The majority of fractures occur when bone mineral density is <1.0 g/cm² in the spine and <0.75 g/cm² in the proximal part of the femur¹⁹. In many postmenopausal women, the bone mineral density in the spine and hip is below these thresholds in the sixth decade²⁰. We have reported that most pathological fractures of the lower extremities of patients with a spinal cord injury occur when 50% of bone mineral density has been lost²¹.

In several studies, the bone mineral content in the spine in individuals who had a spinal cord injury was reported to be similar to that in a control population^8-12. However, those studies included both male and female patients who had an arthrodesis of the lumbar spine, incomplete spinal cord injury, or acute or chronic injuries, thereby making it difficult to assess the relevance of the data. Also, the effects of age, body weight, and time since the injury were not evaluated.

In our series, bone mineral density in the spine was 8% higher in Group II and 15% higher in Group III than it was in the controls, and the bone mineral density was the same in the oldest injured patients and the youngest control subjects. The Z-scores decreased with age in the control subjects but increased with age in the injured women, suggesting that bone mineral density of the lumbar vertebrae is maintained, if not indeed enhanced, in older women with spinal cord injury.

Body weight was a significant positive predictor of spine Z-scores for both the injured patients and the controls; however, there was a greater positive influence in the control group. The mean Z-score for the spine in the injured women was higher than that in the control group, even when we controlled for differences in body weight. Therefore, weight-bearing activities of the injured women cannot be the sole explanation for the increased bone mineral density in the spine in those women. Furthermore, the spine Z-scores in the injured women increased in relation to the time since the injury and the age of the patient, suggesting that factors related to the injury may have been responsible for the changes in bone mineral density.

Several authors have reported a mean loss of bone mineral content of 25% in the femoral necks of patients with spinal cord injury as compared with those of controls^8,9,11,12,22. We found bone density in the hip to be 18% less in Group I and 25% less in Groups II and III when compared with the values in the control groups. Regression analysis showed that, following a phase of initial rapid bone loss, further loss occurred in a linear pattern, regardless of the age at the time of injury. The hip is increasingly at risk for fracture since the oldest injured women had a 53% loss compared with the youngest controls. This difference is clinically and statistically significant (p < 0.0001), and it is a valid comparison in relation to fracture thresholds and bone loss noted in relation to fractures of the hip in the general population^19-21.

Clinically, the majority of pathological fractures in patients with spinal cord injury occur about the knee^4-7. Supracondylar fracture of the femur was so prevalent in the series reported by Comarr et al. that they termed it "the paraplegic fracture."⁴ Young males who have a complete spinal cord injury lose approximately one-third of the bone mineral density in the knee within eighteen months after the injury. Additional annual bone loss is then minimal^22,23. In our study, the bone mineral density in the knees of the injured women was 38%, 41%, and 47% less than the bone mineral density in the knees of the uninjured individuals of the same age. Thus, initial bone loss in the knee of an injured woman is approximately 5% to 10% greater than that in injured men, and injured women, regardless of their age, initially have a rapid decrease in bone density of 40% to 45% in the knee. Subsequently, the rate of bone loss is similar to that seen in comparable able-bodied women.

Several conclusions can be drawn regarding women with a complete spinal cord injury:

1. Initial bone loss in the lumbar spine is minimal. With increased time since the injury, bone mass increases and surpasses that of uninjured women of similar age, with the potential to equal peak bone mass in young women. Greater body weight is associated with increased bone mineral density, but to a lesser extent than it is in able-bodied women. The risk of fracture in the lumbar spine of a woman with a spinal cord injury who does not have preexisting osteoporosis is low.

2. The rate of initial bone loss in the hip after spinal cord injury lies between that in the spine and that in the knee. Bone mineral density in the hip reaches a steady state of approximately 25% less than that of age-matched able-bodied women. Thereafter, it declines in a straight-line fashion at a rate essentially equivalent to that seen in the general population. Unlike the case with able-bodied women, body weight does not influence bone mineral density in the proximal part of the femur in a patient with a spinal cord injury. However, as with able-bodied women, advancing age contributes to bone loss. The initial risk of fracture depends on the proximity of the age at the time of injury to the age associated with peak bone mass; the risk increases with age, and women with a spinal cord injury reach fracture-potential levels earlier in life than do able-bodied women.

3. In women, bone loss in the knee occurs rapidly after a complete spinal cord injury, resulting in a bone mineral density of only about 40% to 45% of that in able-bodied women. Furthermore, it is greater than the loss seen in males with similar injury.

Appendix

A table providing the raw data for all measurements in the study participants with spinal cord injury is available with the electronic versions of this article, on our web site (www.jbjs.org) and on our CD-ROM (call 781-449-9780, ext. 140, to order).

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Topics

osteoporosis ; bone mineral density ; hip joint ; knee joint ; spinal cord injuries ; spine ; women ; osteopenia

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Douglas E. Garland, Rodney H. Adkins, Charles A. Stewart, Roy Ashford, Daniel Vigil; Regional Osteoporosis in Women Who Have a Complete Spinal Cord Injury. The Journal of Bone & Joint Surgery. 2001 Aug;83(8):1195-1200.

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