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Parathyroid Hormone Deficiency and Excess: Similar Effects on Trabecular Bone But Differing Effects on Cortical Bone

Department of Endocrinology, Austin and Repatriation Medical Centre, University of Melbourne, Melbourne, Australia 3084

Address all correspondence and requests for reprints: Ego Seeman, M.D., Austin and Repatriation Medical Centre, Heidelberg, Melbourne, 3084, Australia. E-mail: ego{at}austin.unimelb.edu.au

	Abstract

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Parathyroid hormone (PTH) may be anabolic at trabecular bone and catabolic in cortical bone. As many regions of the skeleton contain both types of bone, the effects of PTH deficiency or excess may be difficult to evaluate using bone densitometry, a technique that integrates the cortical and trabecular compartments of bone. We asked the following questions: 1) Is the higher bone mineral density (BMD) in postsurgical hypoparathyroidism due to higher cortical, not trabecular, bone? 2) Is age-related bone loss slowed in patients with postsurgical hypoparathyroidism? 3) Is lower BMD in primary hyperparathyroidism the result of deficits in cortical, not trabecular, bone?

BMD of the lumbar spine, proximal femur, distal radius, and femoral midshaft was measured by postero-anterior (PA) scanning, while bone mineral content (BMC) of the third lumbar vertebra was measured by lateral scanning using dual x-ray absorptiometry in 10 women, ages 64.6 ± 3.2 yr, with postsurgical hypoparathyroidism and in 25 women, ages 68.7 ± 1.6 yr, with primary hyperparathyroidism. Measurements were repeated 4.7 ± 0.6 yr later in 8 patients with hypoparathyroidism and 4.0 ± 0.4 yr later in 20 age-matched controls. Data were expressed as z scores (SD, mean ± sem) derived from 405 postmenopausal women.

In patients with hypoparathyroidism, bone mass z score of the third lumbar vertebra (vertebral body plus posterior processes) was higher than zero by PA scanning (1.26 ± 0.58 SD, P < 0.05) and lateral scanning (1.04 ± 0.60 SD, P = 0.1), and higher at the trabecular-rich vertebral body (1.02 ± 0.47 SD, P = 0.07) and predominantly cortical posterior processes (0.98 ± 0.66 SD, P = 0.1) determined by lateral scanning. The BMD z scores were higher than zero at the femoral neck (0.89 ± 0.48 SD, P = 0.09), but not at the femoral midshaft (0.45 ± 0.60, NS) and distal radius (0.04 ± 0.51, NS). During follow-up, femoral neck BMD decreased in controls but not in patients with hypoparathyroidism (slope, -0.00818 ± 0.00496 g/cm²/year vs. 0.00907 ± 0.00583 g/cm²/year, respectively, P = 0.06). There was no change in lumbar spine BMD in either group. In 25 women with primary hyperparathyroidism, there were no deficits in BMD at the third lumbar vertebra (vertebral body plus posterior processes) by PA or lateral scanning. By lateral scanning, BMC was increased at the vertebral body (0.64 ± 0.31 SD, P < 0.01) and reduced at the posterior processes (- 0.65 ± 0.26 SD, P < 0.05). BMD was lower at the midshaft of the femur (- 0.82 ± 0.37 SD, P < 0.05) and at the distal radius (- 0.68 ± 0.20 SD, P < 0.01), but not at the femoral neck (- 0.08 ± 0.20 SD, NS). Longitudinal data were unavailable in hyperparathyroid patients.

In summary, trabecular bone is increased by both PTH deficiency and excess. Cortical bone loss is slowed by PTH deficiency and accelerated by PTH excess so that suppression of PTH may reduce age-related bone loss and the risk of fracture. Assessment of BMD in PTH deficiency and excess requires the separate study of cortical and trabecular bone.

	Introduction

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PARATHYROID hormone (PTH) is most likely to be involved in the pathogenesis of age-related cortical bone loss and hip fractures because 1) PTH increases with advancing age and is present in higher concentrations in elderly persons and in some patients with hip fractures (1, 2, 3, 4); 2) patients with postsurgical hypoparathyroidism have increased BMD (5, 6, 7, 8); 3) patients with primary hyperparathyroidism have reduced BMD at cortical sites (9, 10); 4) parathyroidectomy for primary hyperparathyroidism has been associated with increased BMD (11, 12); and 5) PTH correlates with activation frequency and cortical porosity (13). However, trabecular bone loss may be independent of PTH, as primary and secondary hyperparathyroidism may be associated with increased trabecular bone mass (14, 15).

As PTH excess may be anabolic at trabecular, and catabolic at cortical, regions, the role of PTH in age-related bone loss may be difficult to evaluate using bone densitometry, a technique that provides a summated or net result of changes that occur in the cortical and trabecular compartments of bone. Thus, patients with PTH deficiency or excess may have reduced, normal, or higher BMD, depending on the region studied. We asked the following questions: 1) Do patients with postsurgical hypoparathyroidism have high BMD at predominantly cortical sites but not at trabecular-rich sites? 2) Is age-related bone loss slowed in patients with postsurgical hypoparathyroidism? 3) Do patients with primary hyperparathyroidism have higher BMD at trabecular-rich sites and reduced BMD at predominantly cortical sites?

	Materials and Methods

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Subjects

We studied 10 postmenopausal women, ages 64.6 ± 3.2 yrs (range 50 - 82 yr), with postsurgical hypoparathyroidism. Surgery was done for thyroid tumor (n = 8), lymphoma (n = 1), and multinodular goitre (n = 1). All patients had hypoparathyroidism confirmed by repeated measurements of immunoreactive PTH that were below the range of normal. All patients required thyroid hormone replacement (Thyroxine, 50–125 µg/day; Glaxo Wellcome, Sydney, Australia), calcium supplements (500–1000 mg/day) with vitamin D (Calcitriol, 0.25–0.5 µg/day; Roche Products, Sydney, Australia) to maintain serum calcium and phosphate within the low limit of normal range. None had been hypothyroid after surgery. Patients were excluded if they had any disease known to affect bone (Paget’s disease, diabetes mellitus, chronic liver, or renal disease). Patients were also excluded if they took medications that could influence BMD (estrogens, progestins, anabolic steroids, bisphosphonates, or fluoride). None of the patients had had fractures.

We also studied 25 postmenopausal women, ages 68.7 ± 1.6 yrs (range 51 - 84 yr), with primary hyperparathyroidism. The diagnosis was based on clinical and laboratory criteria, including persistent hypercalcemia (serum calcium ranged 2.66 to 3.92 mmol/L, normal less than 2.6 mmol/L) and elevated serum immunoreactive PTH ranged from 6.7 to 14.9 pmol/L (normal less than 5.8 pmol/L). Thirteen patients had surgical removal of parathyroid adenomata. Patients were excluded if they had any other illnesses that could affect bone metabolism. None were taking any medications known to influence bone at the initial visit. Two patients had had vertebral fractures.

Four hundred five postmenopausal women, ages 45–87 yr, were recruited to provide a reference group for deviation of z scores. All the controls were healthy volunteers free of any illness and medication that might influence bone metabolism. None had history of osteoporotic fractures. Subjects with apparent osteophytes and facet joint sclerosis were excluded because these factors artefactually increase bone mass. All subjects gave informed consent. The study was approved by the ethics committee of the Austin and Repatriation Medical Centre.

Measurement of bone mineral content and density

BMD of the lumbar vertebra (L2–4) and the proximal femur (femoral neck, Ward’s triangle, and greater trochanter) was measured by PA scanning using dual x-ray absorptiometry (Lunar Corp., DPX-L, Version 1.3z, Madison, WI). The coefficient of variation at these sites ranged from 1.5% to 2.4% (16). Bone mineral content (BMC) of the third lumbar vertebra was measured by lateral scanning in the decubitus position in 8 of 10 hypoparathyroid and 14 of 25 hyperparathyroid patients. A single rectangular region enclosing the vertebral body and posterior processes of the third lumbar vertebra was used to determine BMC. BMC was also determined at each of two regions created by dividing the rectangle by a vertical line separating the vertebral body and the posterior processes as described previously (17). The coefficient of variation was 1.2% by PA scanning and 2.8% by lateral scanning for total BMC of the third lumbar vertebra, 1.2% for vertebral body, and 1.5% for posterior processes (17). BMD of the distal third of the radius was measured in 6 hypoparathyroid and 10 hyperparathyroid patients (18). A manual analysis of BMD at the junction of the distal one third and proximal two thirds of the left femur based on total body scanning was available in 8 hypoparathyroid and 11 hyperparathyroid patients. The coefficients of variation at these two sites were 0.6% and 1.5%, respectively.

The 10 patients with hypoparathyroidism were assessed 18.5 ± 5.2 yr after surgery during the first visit (range 0.5–51 yr), and 8 were followed for 4.7 ± 0.6 yrs (range 2.1–6.7 yr). BMD was measured 4.5 ± 0.7 times (ranging from 2 to 8 times, one patient had two, and the rest had more than two measurements). We randomly selected 20 postmenopausal controls matched by age with serial BMD measurements from the 405 postmenopausal women (mean 4.0 ± 0.3 serial measurements, ranging from 3 to 7 times) and followed for 4.0 ± 0.4 yrs (range 1.3–7.9 yr). The prospective data are not available for the patients with primary hyperparathyroidism as most were treated surgically after the initial measurement.

Statistical analysis

For the cross-sectional analyses, all data were expressed as absolute value (g or g/cm²) and as z scores (standardized deviations, SD units). The z score was calculated by observed value minus age-predicted value (based on the linear regression equation of the 405 postmenopausal women adjusted for age) divided by the standard deviation of the reference population. The regression equations used were: Lumbar spine BMD = 1.4214 - 0.0055 age, SD = 0.1951 (n = 405); Femoral neck BMD = 1.2782 - 0.0067 age, SD = 0.1424 (n = 405); Trochanter BMD = 1.0056 - 0.0042 age, SD = 0.1373 (n = 405); Ward’s triangle BMD = 1.1913 - 0.0076 age, SD = 0.1671 (n = 405); Total BMC of the third lumbar vertebra (PA view) = 20.9244 - 0.0946 age, SD = 3.5638 (n = 405); Total BMC of the third lumbar vertebra (Lateral view) = 18.1367 - 0.0949 age, SD = 3.1265 (n = 136); Vertebral body BMC = 8.5749 - 0.0441 age, SD = 1.6007 (n = 136); Posterior processes BMC = 9.4353 - 0.0507 age, SD = 1.8450 (n = 136); Distal radius BMD = 1.0391 - 0.0071 age, SD = 0.0943 (n = 302); Femoral midshaft BMD = 2.3173 - 0.0092 age, SD = 0.1963, (n = 84).

The z scores were also adjusted for the contribution of height, weight, and yr since menopause based on multiple linear regression analysis of the reference normal postmenopausal populations (19). One-sample t tests were used to determine whether the z scores differ from zero. Paired t tests were used to determine the difference between sites within the same group. Linear regression analysis was used to determine the relationship between the z scores and duration of hypoparathyroidism. For the longitudinal analyses in patients with postsurgical hypoparathyroidism, the slope of BMD on duration of measurement in each patient or control was derived from the linear regression analysis. Differences of the slopes between the two groups were determined by analysis of variance. Results are expressed as the mean ± SEM. P values were two-tailed.

	Results

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In the cross-sectional analyses, BMD in patients with hypoparathyroidism was higher compared with age predicted mean at the lumbar spine, proximal femur, but not at the distal radius or the midshaft of the femur (Table 1, Fig. 1). Relative to age predicted mean, total BMC of the third lumbar vertebra was 1.26 ± 0.58 SD higher by PA scanning (P < 0.05) and 1.04 ± 0.60 SD higher by lateral scanning (P = 0.1). BMC was higher at the vertebral body (1.02 ± 0.47 SD, P = 0.07) and posterior processes (0.98 ± 0.66 SD, P = 0.1). The BMD z scores correlated with duration of hypoparathyroidism (Fig. 2).

View larger version (21K): [in this window] [in a new window]   Figure 1. Z scores for BMC of the total vertebra, vertebral body, and posterior processes of the third lumbar vertebra, and z scores for BMD of the femoral neck, Ward’s triangle, trochanter, midshaft of femur and distal radius in patients with postsurgical hypoparathyroidism (grey circles/bars) and patients with primary hyperparathyroidism (open circles/bars).

View larger version (30K): [in this window] [in a new window]   Figure 2. The relationship between BMD z scores and the duration of hypoparathyroidism in patients with postsurgical hypoparathyroidism.

BMD in the patients with primary hyperparathyroidism was not reduced at the lumbar spine or proximal femur (Table 1 and Fig. 1). Nor was total BMC of the third lumbar vertebra reduced as assessed by PA (-0.02 ± 0.20 SD, NS) or lateral scanning (-0.05 ± 0.27 SD, NS). However, by lateral scanning, BMC was increased by 0.64 ± 0.31 SD at the vertebral body (P < 0.01) and reduced by -0.65 ± 0.26 SD at the posterior processes (P < 0.05). The two regions also differed from each other. Reduced BMD was found at the femoral midshaft (-0.82 ± 0.37 SD, P < 0.05) and distal radius (-0.68 ± 0.20 SD, P < 0.01). These results were unchanged after adjustments for height, weight, and yr since menopause (data not shown). Longitudinal data were not available in patients with primary hyperparathyroidism.

	Discussion

Top Abstract Introduction Materials and Methods Results Discussion References

 
Lumbar spine BMD was increased in patients with hypoparathyroidism and was normal in patients with primary hyperparathyroidism by PA scanning. Lateral scanning allowed separate evaluation of the predominantly cortical posterior processes and the trabecular rich vertebral body. The increased bone mass in hypoparathyroidism was due to increased BMC at the vertebral body and posterior processes. Normal bone mass in primary hyperparathyroidism by PA and lateral scanning was the result of increased vertebral body BMC and reduced BMC of the posterior processes. Thus, PA scanning of the spine by dual energy x-ray absorption (DXA) may provide misleading information when changes in BMC occur in different directions at the vertebral body and the posterior processes. This is the likely explanation for the variable and often contradictory finding of reduced or normal bone mass at the spine in primary hyperparathyroidism (7, 10, 20).

Increased BMD is widely reported in postsurgical hypoparathyroidism (5, 6, 7, 8). However, it is uncertain whether this is the result of higher BMD at cortical and/or trabecular sites. Bone mass was increased at regions containing predominantly cortical bone (proximal femur, posterior processes) as well as the vertebral body, a region with large amounts of trabecular bone (21). The higher BMD is likely to be the result of reduced remodeling rate associated with secondary hypoparathyroidism. The reduced remodeling rate is also likely to explain the lower rate of proximal femoral bone loss during 5-yr follow-up found in this study and the lower rate of bone loss at the spine reported by Fujiyama et al. (6). As bone loss at the proximal femur is likely to be important in the pathogenesis of bone fragility in old age, suppression of PTH by using calcium supplements or correcting vitamin D deficiency in the elderly may reduce the risk of hip fracture (22, 23).

Finding that bone mass was increased at the vertebral body but decreased in the posterior processes in patients with primary hyperparathyroidism is consistent with anabolic effects of PTH on trabecular bone and catabolic effects on cortical bone demonstrated using histomorphometry (15, 24, 25). These opposing effects at cortical and trabecular bone probably account for finding no deficit at the proximal femur in patients with primary hyperparathyroidism as this site contains both types of bone. The opposing effects may also explain the absence of bone loss with aging at the proximal femur in patients with primary hyperparathyroidism (20, 26). Whether vertebral or hip fracture rates are increased in primary hyperparathyroidism is controversial (27, 28, 29). The anabolic effects at trabecular bone may reduce bone fragility while the catabolic effects may increase bone fragility.

This study and the data in the literature argue against a role of PTH in trabecular bone loss during aging. PTH is likely to increase trabecular bone by increasing osteoblast recruitment (30). There is a great deal of evidence to support the notion of a causal relationship between PTH and age-related cortical, but not trabecular, bone loss: 1) there is a positive association between PTH and activation frequency, and PTH and cortical porosity (13); 2) primary hyperparathyroidism may be associated with lower cortical BMD but with preservation of trabecular BMD (10, 24, 25); 3) Parathyroidectomy for primary hyperparathyroidism may be associated with increased BMD at the lumbar spine and femoral neck using PA scanning by DXA, which cannot distinguish trabecular and cortical behaviour (12). However, using quantitative computed tomography in children, Boechat et al. reported that cortical BMD increased consistent with removal of the catabolic effect of PTH, while cancellous BMD decreased consistent with the loss of anabolic action of PTH (31). 4) As shown in this study and by Fujiyama et al. (6), the rate of bone loss is reduced in postsurgical hypoparathyroidism. However, longer follow-up with larger sample sizes will be required before concluding that bone loss is abolished following parathyroidectomy.

In conclusion, assessment of BMD in PTH deficiency and excess requires the separate study of cortical and trabecular bone. Cortical, but not trabecular, bone loss in the elderly is likely to be caused partly by secondary hyperparathyroidism. Drug therapy aimed at suppression of PTH secretion or action may reduce age-related cortical bone loss and risk of fracture.

	Acknowledgments

 
Sincere thanks to Sister Jan Edmonds for her assistance with subject recruitment for this study.

Received May 1, 1998.

Revised August 5, 1998.

Revised November 9, 1998.

Accepted November 10, 1998.

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