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Improved Peripheral Cortical Bone Geometry after Surgical Treatment of Primary Hyperparathyroidism in Postmenopausal Women

Division of Diabetes, Metabolism, and Endocrinology (H.K., R.N.), Department of Internal Medicine, Kobe University Graduate School of Medicine, Kobe 650-0017, Japan; and Internal Medicine 1 (M.Y., T.S.), Shimane University Faculty of Medicine, Shimane 693-8501, Japan

Address all correspondence and requests for reprints to: Hiroshi Kaji, Division of Diabetes, Metabolism, and Endocrinology, Department of Internal Medicine, Kobe University Graduate School of Medicine, 7-5-2 Kusunoki-cho, Chuo-ku, Kobe 650-0017, Japan. E-mail: hiroshik{at}med.kobe-u.ac.jp.

	Abstract

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Context: Cortical bone geometry is one of the most important components of bone strength. Excess endogenous PTH or intermittent PTH administration affects cortical bone geometry; however, the changes in cortical bone geometry in patients with primary hyperparathyroidism (pHPT) after parathyroidectomy (PTX) remain unknown.

Objective: The present study was performed to examine the longitudinal effects of treating endogenous PTH excess on cortical bone geometry in postmenopausal patients with pHPT by using peripheral quantitative computed tomography.

Patients: Twenty postmenopausal pHPT patients and 30 postmenopausal control subjects matched for age participated in this study.

Main Outcome Measures: Volumetric bone mineral density (vBMD), cortical bone geometric parameters, polar strength strain index, and polar cross-sectional moment of inertia were measured using peripheral quantitative computed tomography at the radius during the year after PTX.

Results: After 1 yr, total and cortical vBMD significantly increased after PTX in the pHPT group (2.9 and 1.6%, respectively), whereas they significantly decreased in the control group (–2.1 and –1.3%, respectively). Significant decreases in cortical thickness and area were observed in the control group (–3.0 and –2.5%, respectively). In contrast, the pHPT group showed increases in cortical thickness and area (8.5 and 7.6%, respectively) as well as polar strength strain index 1 year after PTX.

Conclusion: The present longitudinal study showed significant beneficial changes in volumetric BMD, cortical bone geometry, and bone strength index after PTX in postmenopausal women with pHPT.

	Introduction

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Primary hyperparathyroidism (pHPT) is an endocrine disorder that is a secondary cause of osteoporosis. Both bone formation and resorption markers are elevated in pHPT patients, and bone mineral density (BMD) is reduced, especially in cortical bone in pHPT patients (1, 2, 3, 4, 5). pHPT was associated with an increased risk of vertebral and forearm fractures (6, 7, 8). In our and other studies (4, 9, 10, 11, 12, 13, 14, 15, 16), BMD increased in pHPT patients after successful parathyroidectomy (PTX); however, the recovery of radial BMD measured by dual-energy x-ray absorptiometry (DXA) after PTX was slight and slow, compared with that of BMD at the lumbar spine (9, 10, 15, 16). Because radial BMD is predominantly affected in pHPT patients, this seems contradictory.

Peripheral quantitative computed tomography (pQCT) can measure volumetric BMD and quantify the geometric properties of long bones, such as the area and circumference of total bone as well as the cortical area and cortical thickness (17). Cortical bone geometry is thought to be one of the most important factors of bone strength. Bone size increases with age (18), and increased bone loss after the menopause is associated with increased rates of periosteal apposition (19). Our previous study revealed that both excessive and deficient endogenous PTH affected cortical bone geometry determined by pQCT (20), and intermittent administration of PTH for the treatment of osteoporosis induced beneficial changes in cortical bone geometry by pQCT (21, 22). Moreover, we previously reported that age, grip strength, and smoking were related to forearm bone geometry by pQCT (23). These findings suggest that the measurement of bone geometric changes are useful in evaluating the mechanisms responsible for bone strength. Moreover, pQCT is more sensitive than DXA in the detection of increased bone mass after PTH treatment in mice (21). Although continuous PTH excess causes a marked change in bone geometry at cortical sites (20), the change in bone geometry of pHPT patients after PTX remains unknown.

The present study was performed to examine prospectively the effects of PTX on cortical bone geometry in postmenopausal patients with pHPT and compare them with age-matched normal women by using pQCT.

	Subjects and Methods

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Subjects

Twenty postmenopausal female patients with pHPT and 30 postmenopausal control subjects participated in this study. These were consecutive patients with pHPT seen during 2002–2004, and the controls were consecutive postmenopausal women seen during the same time frame. The control group was matched for age and was of similar height, weight, and years since menopause. All subjects took no drugs known to influence bone metabolism during the study. Although none had renal failure, three and four subjects had estimated glomerular filtration rate (eGFR) of 30–59 ml/min in controls and pHPT patients, respectively. Moreover, familial hypocalciuric hypercalcemia was excluded, based on having a calcium to creatinine clearance ratio (<0.01) by 24-h urine collection. PTX was recommended to all patients, regardless of whether they met the National Institutes of Health criteria for surgery (2002). In all 20 subjects who had PTX, one or more abnormal parathyroid glands were removed, and biochemical values such as serum levels of calcium and PTH decreased to normal levels after PTX, indicating that PTX was successful for the treatment of pHPT. Eighteen and two patients had single adenoma and hyperplasia, respectively. Hypocalcemia [serum calcium level <8.5 mg/dl (2.1 mmol/liter] persisting for 2 wk was considered due to the hungry bone syndrome and was observed in two patients. No patients received bisphosphonates.

On the other hand, control subjects were postmenopausal women who were self-referred to our clinic to be screened for osteoporosis. They were free of drugs or diseases known to influence bone metabolism during the study including hormone replacement therapy and calcium and vitamin D supplements. The study was approved by the Ethics Review Board of the Kobe University Hospital. All subjects agreed to participate in the study and gave informed consent. All baseline data were collected within the month before surgery.

Biochemical measurements

Serum and urinary chemistry determinations were performed by standard automated techniques. Serum chemistry was performed in daily routine assays. Urine was collected as second void morning urine except for the measurement of the calcium to creatinine clearance ratio, which was done on 24-h urine specimens. Serum concentrations of intact PTH were measured by immunoradiometric assay (Allegro Intact PTH IRMA kit; Nichols Institute Diagnostics, San Juan Capistrano, CA; normal range, 10–65 pg/ml).

BMD measurements by DXA

BMD values were measured by DXA using QDR-2000 (Hologic Inc., Waltham, MA) at the lumbar spine (L2–4), femoral neck (FN), and distal one third of the radius (1/3R). BMD was automatically calculated from the bone area (square centimeters) and bone mineral content (grams) and expressed absolutely in grams per square centimeter. The T score is the number of SDs by which a given measurement differs from the mean for a normal young adult reference population.

BMD measurements by pQCT

pQCT analysis was performed in the nondominant forearm using an XCT-960 device (Stratec, Pforzheim, Germany) with a single energy x-ray source, as previously described (24). All computed tomography scans were acquired with a slice thickness of 2.5 mm and a pixel size of 0.59 mm. The scanner was positioned at the site of the forearm at a distance from the ulnar styloid process that corresponded to 20% of forearm length for the midradius. This measurement site was selected because it is the most appropriate for the analysis of cortical bone. To separate the cortical bone, all voxels (0.295 x 0.295 x 1 mm) of the scanned image with a BMD lower than a threshold of 267 mg/cm³ were eliminated (25). Total volumetric (v) BMD, cortical vBMD and bone geometry indices were measured at the midradius. The cortical area was the region with linear attenuation. Cortical thickness was defined as the mean distance between the inner and outer edges of the cortical shell. polar strength strain index (SSIp) lies within the theory of stability of mechanical structures against bending or torsion. SSIp was calculated by: (r² x A x CD/1200)/rmax, where A is the area of a voxel (square millimeters), r is its distance from the center of gravity, CD is cortical density (milligrams per cubic millimeter) and is divided by the normal physiological density of cortical bone (1200 mg/mm³), and rmax is the maximum distance of a voxel from the center of gravity (26). The coefficient of variation for each parameter was under 1% in our institution. We calculated polar cross-sectional moment of inertia (pCSMI) as previously described (22, 27). The coefficient of variation of pCSMI was 2–3%. pQCT parameters were measured at 1 yr in control subjects and at 6 months and 1 yr after PTX.

Statistical analysis

All data are expressed as the mean ± SD for each index. Statistical analyses were performed using StatView IV (Abacus Concepts, Inc., Berkley, CA). Comparisons between two groups were made with the nonparametric Mann-Whitney U test. Student’s paired t test was used to compare the basal parameters and later values. Simple regression analyses were performed to assess the linear relationship among several parameters, and Pearson’s correlation coefficients were calculated. Values of P < 0.05 were considered significant.

	Results

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Background data

Baseline data of the control group and postmenopausal patients with pHPT are shown in Table 1. The mean age of each group was similar. Height and weight were not significantly different between the two groups. Serum calcium level of pHPT patients was 12.0 ± 1.0 mg/dl (3.0 ± 0.25 mmol/liter), and this normalized in all patients after PTX. Serum levels of PTH and phosphorus were higher and somewhat lower in the pHPT group, respectively, compared with controls as expected in pHPT. Serum levels of alkaline phosphatase were much higher in pHPT patients than in controls. Areal BMD at L2–4 and FN-BMD were similar between the groups, although areal BMD at the 1/3R was lower in pHPT patients than the control group. Serum levels of calcium and phosphorus corrected into the normal range after short-term treatment (2 wk) with active vitamin D metabolites in two patients who showed a tendency toward hypocalcemia thought to be due to the hungry bone syndrome.

The changes in vBMD and cortical bone geometry obtained by pQCT in control subjects during 1 yr are shown in Table 2. Total and Ct BMD were significantly decreased during 1 yr in the control group. As for bone geometry parameters, cortical area (Ct Ar) and Ct Th were significantly decreased in control subjects. Total area, PERI, ENDO, and SSIp as well as pCSMI did not change during 1 yr, although pCSMI in the pHPT group was slightly higher.

The changes in vBMD and cortical bone geometry obtained by pQCT in pHPT patients 6 and 12 months after PTX are shown in Table 2. Total as well as Ct BMD significantly increased 1 yr after PTX. Total area, PERI, and ENDO were not significantly different 1 yr after PTX. Cortical area, Ct Th, and SSIp were significantly elevated 1 yr after PTX.

Because postmenopausal women usually show decreased bone volume and changes in bone geometry due to aging and estrogen deficiency, we compared the percent change in pQCT indices during 1 yr between control subjects and pHPT patients after PTX. As shown in Table 3, increased changes in total volumetric BMD (Tt BMD) and Ct BMD of pHPT patients were significantly higher than those of the controls. The changes in total area (Tt Ar), PERI, and ENDO were not significantly different between control and pHPT patients. The changes in Ct Ar, Ct Th, SSIp, and pCSMI of the pHPT group were significantly higher than in the control. All individual data in the pHPT group are shown in Fig. 1. The data of pHPT patients (n = 18) who did not show hypocalcemia due to the hungry bone syndrome are shown in Table 3. There were no significant differences between the percent changes in pQCT parameters during 1 yr with or without hypocalcemia due to the hungry bone syndrome. Changes in pQCT parameters during 1 yr were compared between group A (14 subjects) [baseline serum calcium <12 mg/dl (4 mmol/liter)] and group B (6 subjects) [baseline serum calcium 12 mg/dl (4 mmol/liter)] in pHPT patients. The data were as follows: Tt BMD, A, 2.5 ± 5.9%, B, 3.8 ± 4.7%; Ct BMD, A, 1.0 ± 2.3%, B, 1.9 ± 3.7%; Tt Ar, A, 2.29 ± 6.4%, B, –0.4 ± 7.9%; PERI, A, 0.98 ± 3.2%, B, –1.3 ± 4.5%; ENDO, A, –0.3 ± 5.0%, B, –4.8 ± 5.7%; Ct Ar, A, 6.0 ± 16.1%, B, 11.4 ± 10.6%; Ct Th, A, 6.3 ± 16.4%, B, 13.8 ± 8.7%; SSIp, A, 5.3 ± 10.6%, B, 5.8 ± 8.8%; and pCSMI, A, 4.5 ± 12.3%, B, 8.0 ± 13.0%). Changes in Ct Ar and Ct Th after PTX seemed higher in severe cases, although there were no significant differences between the groups because of the small number of subjects.

View larger version (25K): [in this window] [in a new window]   FIG. 1. Individual changes in pQCT parameters during 1 yr in pHPT patients. Data are percent changes, compared with baseline levels. The bar at 1 yr after parathyroidectomy shows each SD value. Percent changes are the mean ± SD of the percent change calculated from baseline data and the data 1 yr later for each subject.

Correlation coefficients and P values of significance for serum calcium/PTH levels and percent changes during 1 yr of Tt BMD, Ct BMD, Ct Ar, Ct Th, SSIp, and pCSMI are shown in Table 4. Although serum PTH levels seemed somewhat related to the changes of Ct BMD and Ct Ar, they were not significant, probably due to the small number of subjects in the correlation analysis. Correlation coefficients and P values of significance for Tt BMD, Ct BMD, Ct Ar, Ct Th, and percent changes of Tt BMD, Ct BMD, Ct Ar, Ct Th, SSIp, and pCSMI are shown in Table 4. Baseline Tt BMD and Ct BMD were significantly related to the changes of pQCT parameters other than Ct BMD, which were compatible with previous findings that areal BMD of the distal radius is more markedly increased after PTX in patients with the lowest BMD preoperatively (4, 9).

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

In the present study, Tt BMD and Ct BMD increased 3.2 and 1.6% 1 yr after PTX, and these increases were significant in pHPT patients. In contrast, these BMD parameters significantly decreased at 1 yr in control subjects. These findings indicate that the increase in cortical BMD was less after PTX, even by the measurement of volumetric BMD by pQCT.

The reason BMD increases markedly after PTX, preferentially at trabecular bone, remains unclear. The BMD changes after PTX are similar to the effects of intermittent PTH treatment for osteoporosis (4, 11, 30) because they are also predominant at trabecular bone. Because the catabolic effects of PTH predominate in cortical bone, withdrawal effects from PTH excess may be important for understanding the anabolic actions of PTX on bone. There is evidence that PTX modulates several osteotropic hormones. An increase in bioavailable testosterone after PTX was related to improved BMD at the hip and lumbar spine in postmenopausal pHPT patients (31). In that study, a postoperative increase in testosterone was positively correlated to BMD change at the hip, although the change in serum PTH was correlated with BMD change at the lumbar spine. Cecconi et al. (32) reported that the impairment in GH secretion in pHPT was reversed in many patients after PTX. Moreover, improvement of BMD at the lumbar spine after PTX was significantly higher in premenopausal women, suggesting that estrogen is important for bone recovery after PTX (12). These findings suggest that sex hormones, the recovery of the GH-IGF-I system, or the withdrawal from PTH itself may play roles in the improvement of BMD after PTX.

Previous evidence indicated that continuous excess endogenous PTH by pHPT increased ENDO, resulting in a reduction of Ct Ar in the long bones, although these effects on PERI are controversial and depend on the measured site (20, 33). On the other hand, intermittent PTH administration increased PERI and decreased ENDO, resulting in increased Ct Th (22). The effects of PTX on bone geometry in pHPT patients are unknown, although markedly increased Ct Th due to increased PERI and decreased ENDO were observed in our case report of one pHPT patient with severe hypercalcemia (34). In the present study, Ct Th significantly increased after PTX in postmenopausal pHPT patients. These changes in bone geometry were also similar to those induced by intermittent PTH treatment. These findings suggest, therefore, that PTH withdrawal by PTX exerts anabolic actions on bone in a similar manner to using intermittent PTH treatment for osteoporosis.

pQCT helps to estimate bone strength by calculating SSIp, which has been suggested to predict bone strength noninvasively (26). A previous study indicated that SSIp at the femur was significantly reduced in postmenopausal pHPT patients (33), although significant changes in SSIp were not observed at the radius in our study of postmenopausal pHPT patients (20). A previous study indicated that fracture risk in pHPT patients was reduced after successful PTX (8), suggesting that PTX improves bone strength in pHPT patients. In the present study, SSIp significantly improved after PTX in pHPT patients. Schneider et al. (35) reported that cortical bone content and area, as well as axial and polar moments of inertia, were significantly higher in women without Colles fracture than in women with Colles fracture by radial pQCT. Because both BMD and bone geometry affect SSIp, bone geometry changes as well as BMD changes after PTX may play a role in increasing bone strength after PTX. The increased forearm fracture risk clearly decreased after PTX in pHPT patients, although no improvement of cortical BMD after PTX was evident (36). Taking into account the present data, the change in bone geometry after PTX may explain some of the reduced fracture risk.

There are limitations to the present study. First, the sample size was likely not large enough to achieve significant changes in some parameters after PTX, such as PERI and ENDO. A larger-scale study will be necessary for more definitive conclusions regarding these parameters. Second, the effects of PTX on bone geometry may differ depending on the site measured because PTH affects cortical and trabecular bone differently as well as weight-bearing and non-weight-bearing bone. Third, 25-hydroxyvitamin D levels were not measured to assess the vitamin D status of the patients in the present study. Thus, differences in vitamin D levels may have affected the changes in peripheral cortical bone geometry after PTX. Fourth, we do not have PTH levels on women in the control group to exclude subtle alterations in PTH secretion. We have excluded only women with hypercalcemia from the control group.

In conclusion, the present longitudinal study demonstrated that the resolution of sustained PTH excess affects cortical bone geometry and that cortical bone geometry and BMD were improved by PTX in pHPT.

	Footnotes

 
Disclosure Statement: All authors have nothing to declare.

First Published Online June 10, 2008

Abbreviations: BMD, Bone mineral density; Ct Ar, cortical area; Ct BMD, cortical volumetric BMD; Ct Th, cortical thickness; DXA, dual-energy x-ray absorptiometry; eGFR, estimated glomerular filtration rate; ENDO, endocortical circumferences; FN, femoral neck; pCSMI, polar cross-sectional moment of inertia; PERI, periosteal circumferences; pHPT, primary hyperparathyroidism; pQCT, peripheral quantitative computed tomography; PTX, parathyroidectomy; 1/3R, distal one third of the radius; SSIp, polar strength strain index; Tt Ar, total area; Tt BMD, total volumetric BMD; v, volumetric.

Received November 7, 2007.

Accepted May 29, 2008.

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