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. Author manuscript; available in PMC: 2012 Aug 3.
Published in final edited form as: Obesity (Silver Spring). 2011 May 26;19(12):2388–2393. doi: 10.1038/oby.2011.133

Increased PTH and 1.25(OH)2D Levels Associated With Increased Markers of Bone Turnover Following Bariatric Surgery

Naina Sinha 1,2, Albert Shieh 1, Emily M Stein 3, Gladys Strain 1, Aaron Schulman 1,2, Alfons Pomp 4, Michel Gagner 4, Gregory Dakin 4, Paul Christos 5, Richard S Bockman 1,2,6
PMCID: PMC3411200  NIHMSID: NIHMS387898  PMID: 21617641

Abstract

The objective of this study was to characterize changes in metabolic bone parameters following bariatric surgery. Seventy-three obese adult patients who underwent either gastric banding (GB), Roux-en-Y gastric bypass (RYGB), or biliopancreatic diversion with duodenal switch (BPD/DS) were followed prospectively for 18 months postoperatively. Changes in the calcium–vitamin D axis (25-hydroxyvitamin D (25OHD), 1,25-dihydroxyvitamin D (1,25(OH)2D), calcium, parathyroid hormone (PTH)), markers of bone formation (osteocalcin, bone-specific alkaline phosphatase) and resorption (urinary N-telopeptide (NTx)), as well as bone mineral density (BMD) were assessed at 3-month intervals during this time period. Bariatric surgery resulted in significant and progressive weight loss over 18 months. With supplementation, 25OHD levels increased 65.3% (P < 0.0001) by 3 months, but leveled off and decreased <30 ng/ml by 18 months. PTH initially decreased 21.4% (P = 0.01) at 3 months, but later approached presurgery levels. 1,25(OH)2D increased significantly starting at month 12 (50.3% increase from baseline, P = 0.008), and was positively associated with PTH (r = 0.82, P = 0.0001). When stratified by surgery type, median PTH and 1,25(OH)2D levels were higher following combined restrictive and malabsorptive operations (RYGB and BPD/DS) compared to GB. Bone formation/resorption markers were increased by 3 months (P < 0.05) and remained elevated through 18 months. Radial BMD decreased 3.5% by month 18, but this change was not significant (P = 0.23). Our findings show that after transient improvement, preoperative vitamin D insufficiency and secondary hyperparathyroidism persisted following surgery despite supplementation. Postoperative secondary hyperparathyroidism was associated with increased 1,25(OH)2D levels and increased bone turnover markers.

INTRODUCTION

Obesity affects >30% (1) of adults in the United States and is associated with numerous health consequences, including hypertension, hyperlipidemia, diabetes mellitus, heart disease, and osteoarthritis (2,3). The number of bariatric operations is rapidly increasing, with over 340,000 surgeries being performed in 2008 (4). Common bariatric operations include gastric banding (GB), Roux-en-Y gastric bypass (RYGB), and biliopancreatic diversion with duodenal switch (BPD/DS). These procedures produce weight loss through reduction in stomach size (restriction), delayed mixing of food with bile salts and pancreatic juices (malabsorption), or a combination of both.

GB is purely restrictive, and is characterized by the placement of a silicone band around the upper portion of the stomach to create a pouch that holds only a small amount of food. RYGB has both restrictive and malabsorptive features. Restriction occurs through the creation of a small gastric pouch from the proximal stomach. This pouch is then anastamosed to the proximal jejunum to form an alimentary tract that carries ingested food content. A biliopancreatic limb that carries bile and pancreatic secretions is then anastamosed with the alimentary tract at the distal jejunum to form a common channel. Malabsorption occurs because food bypasses the duodenum and does not mix with bile salts and pancreatic secretions until the distal jejunum. BPD/DS has similar restrictive and malabsorptive components. The alimentary tract is constructed by the anastamosis of a gastric sleeve to the distal ileum. The biliopancreatic limb is not anastamosed with the alimentary tract until 50–100 cm proximal to the ileocecal valve. BPD/DS therefore results in greater malabsorption than RYGB as food bypasses more of the small intestine, and does not mix with digestive enzymes until the distal ileum. These operations result in significant long-term weight loss, reduced rates of obesity-related complications, and decreased mortality (5,6).

Despite clear benefits, there is emerging evidence that bariatric surgery is associated with changes in bone metabolism. Vitamin D and calcium malabsorption, secondary hyperparathyroidism, increased bone turnover, and decreased bone mineral density (BMD) have all been reported following bariatric surgery (7–20). Osteomalacia and osteoporosis have been documented 8–12 years following surgery (21). In addition, a fracture incidence as high as 5% within 2–3 years of bariatric surgery has been reported (22). Most of these data, however, have been captured through retrospective reports.

To date, existing prospective longitudinal studies are few, have rarely followed patients past 12 months, and have not universally measured markers of bone turnover and BMD in the postoperative period. Few have studied patients undergoing BPD/DS, the procedure that results in the most weight loss and most malabsorption. This prospective longitudinal study followed patients who underwent GB, RYGB, or BPD/DS for 18 months. We assessed changes in the calcium–vitamin D–PTH axis, markers of bone turnover, and BMD throughout this time period. We report that each type of bariatric surgery studied led to significant weight loss and increased bone turnover; the operations with greater malabsorptive components led to greater disturbances in metabolic bone parameters.

METHODS AND PROCEDURES

Between January 2005 and September 2008, 115 patients were enrolled consecutively from the bariatric practice at New York–Presbyterian Hospital/Weill Cornell Medical College. Forty-two patients declined surgery after providing informed consent. A total of 73 male and female patients were therefore included in this analysis (GB (N = 18), RYGB (N = 50), or BPD/DS (N = 5)) and evaluated prospectively for 18 months following bariatric surgery. The type of surgery for each patient was determined on an individual basis by the operating surgeon. Patients who underwent surgery between January 2005 and December 2006 did not receive routine calcium or vitamin D supplementation. Those who underwent surgery between January 2007 and September 2008 received 1,200 IU vitamin D3 if baseline 25-hydroxyvitamin D (25OHD) was between 25 and 30 ng/ml, 50,000 IU vitamin D2 until surgery if baseline 25OHD was between 20 and 25 ng/ml, 50,000 IU vitamin D2 for 4 weeks if baseline 25OHD was <20 ng/ml, and 1,200 mg calcium carbonate or citrate if serum PTH was elevated. 25OHD, calcium, and PTH were not routinely re-evaluated before surgery. Postoperatively, GB patients were instructed to take 400 IU/day of vitamin D3, and given the option of taking 1,200 mg/day of calcium carbonate as well. RYGB and BPD/DS patients were instructed to take between 1,200 and 1,800 mg/day of calcium citrate and 1,200–1,600 IU/day of vitamin D3. Subjects met regularly with a nutritionist at 3-month intervals for the first year after surgery, and then annually thereafter. At these visits, patient adherence to nutritional supplementation was reviewed and encouraged; however, pills were neither dispensed nor counted by our nutritionists. Patients were excluded if they had known metabolic bone disease (including Paget’s disease and primary hyperparathyroidism), or were taking medications that affect bone metabolism (including bisphosphonates and corticosteroids). The study was approved by the institutional review board at the Weill Cornell Medical College, and conducted at the Weill Medical College Clinical Translational Science Center. All participating patients gave written informed consent.

Patients were evaluated before and at 1, 3, 6, 9, 12, and 18 months after surgery. Changes in anthropomorphic measurements, the calcium–vitamin D–PTH axis, bone turnover, and BMD were measured at each time point based on the following parameters. Anthropomorphic measurements included height (measured to the nearest cm), weight (in kg), and BMI (kg/m2). Markers of the calcium–vitamin D–PTH axis included 25-hydroxy vitamin D (25OHD) (ng/ml; chemiluminescent immunoassay; ARUP Laboratory, Salt Lake City, UT; coefficient of variation (CV) 8.6–10.0%), 1,25-dihydroxyvitamin D (1,25(OH)2D) (pmol/l; radioimmunoassay; ImmunoDiagnostic Systems; Scottsdale, AZ; CV 11.0%), calcium (mg/dl), and total intact parathyroid hormone (PTH, sum of 1–84 PTH and N-truncated peptides) (pg/ml; immunoradiometric assay; Scantibodies Laboratory; Santee, CA; CV 8.8%). Markers of bone turnover included osteocalcin (mg/ml; ELISA; Diagnostic System Laboratory; Webster, TX; CV 10.1%), bone-specific alkaline phosphatase (μg/l; ELISA; ImmunoDiagnostic Systems; CV 10.0%), and urinary N-telopeptide (urinary NTx) (nmol/l BCE/mmol/l creatinine; enzyme immunoassay; Wampole Laboratory; Princeton, NJ; CV 5.0%). BMD (g/cm2) was measured by dual-energy X-ray absorptiometry (DXA) (QDR; Hologic; Waltham, MA). At the time of the study, the DXA machine used could not measure central sites in patients exceeding 300 pounds, and therefore only wrist BMD could be assessed in the majority of subjects.

Statistical methods

For the measured parameters, median percent change from baseline to months 3, 6, 9, 12, and 18 was computed and evaluated by the Wilcoxon signed-rank test (i.e., for comparison to 0% change). The median absolute values for the measured parameters at baseline and at the follow-up time points are also presented for descriptive purposes. Although median percent change for some parameters was further stratified by surgery type (GB vs. RYGB and BPD/DS), no formal statistical comparisons between the surgery groups were made due to the small number of patients in the GB and BPD/DS groups and the limited amount of data at the follow-up time points. All P values are two-sided with statistical significance evaluated at the 0.05 α-level. All analyses were performed in SAS Version 9.2 (SAS Institute, Cary, NC) and SPSS Version 18 (SPSS, Chicago, IL).

RESULTS

Seventy-three patients were enrolled in this study. The mean BMI was 48.2 ± 7.4 kg/m2 with two-thirds being women. Additional baseline features are reported in Table 1. Nineteen patients underwent GB, 49 underwent RYGB, and 5 underwent BPD/DS. Following surgery, significant and progressive weight loss was observed through month 18.

Table 1.

Baseline patient features

Age (mean ± s.d.) 39.2 ± 10.8
Male N (%)0 39 (34.2)
Female N (N%) 75 (65.8)
BMI (kg/m2) (mean ± s.d.) 48.2 ± 7.4
25OHD (ng/ml) (mean ± s.d.) 22.0 ± 14.7
1,25(OH)2D (48–150 pmol/ml) (mean ± s.d.) 117.8 ± 48.4
Serum calcium (8.9–10.3 mg/dl) (mean ± s.d.) 9.8 ± 0.9
Serum PTH (10–57 pg/ml) (mean ± s.d.) 82.9 ± 48.2
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1,25(OH)2D, 1,25-dihydroxyvitamin D; 25OHD, 25-hydroxyvitamin D; PTH, para-thyroid hormone.

Before surgery, 9.6% of patients had 25OHD <10 ng/ml, 73.1% had 25OHD between 10–30 ng/ml, and 17.3% had 25OHD >30 ng/ml. Baseline serum calcium was normal at 9.8 ± 3.5 mg/dl, and serum PTH was elevated at 82.9 ± 48.2 pg/ml. Between the baseline visit and time of surgery, patients received calcium and vitamin D supplementation as outlined in the Methods and Procedures section for between 0 and 4 weeks. 25OHD increased significantly by 65.3% (P < 0.0001) at month 3 to >30 ng/ml. Although 25OHD levels at 18 months remained significantly increased from baseline, they had declined from their peak and were <30 ng/ml (Figure 1a). Serum 1,25(OH)2D levels did not change significantly until month 12 when a 50.3% increase (P = 0.008) from baseline was noted (Figure 1b). At this time point, a Pearson correlation analysis revealed a strong association between 1,25(OH)2D and PTH (r = 0.82, P = 0.0001). Serum calcium remained stable throughout the 18-month study period. Total intact PTH decreased significantly by 21.4% (72.0 to 55.4 pg/ml, P = 0.01) into normal range at month 3, but began to increase at month 6 and continued through month 18 (Figure 1c).

Figure 1.

Figure 1

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Percent change (reported as median values) in serum 25-hydroxyvitamin D (25OHD), 1,25-dihydroxyvitamin D (1,25(OH)2D), and parathyroid hormone (PTH) at postoperative months 3, 6, 9, 12, and 18 compared to baseline. (a) 25OHD: 25OHD levels increased significantly from baseline starting at month 3. As the study progressed, 25OHD remained elevated from preoperative levels, but the magnitude of the increase diminished. (b) 1,25(OH)2D: Serum 1,25(OH)2D levels began to increase at 3–6 months, but this increase did not become significant until 12 months. (c) PTH: PTH initially decreased significantly at 3 months, but began to approach and eclipse preoperative levels thereafter.

Urinary NTx, a marker for bone resorption, increased significantly by 81.4% at month 3 and remained significantly increased from baseline through month 18 (Figure 2a). Osteocalcin, a bone formation marker, also increased signi3-cantly by 31.5% (P = 0.04) at month 3, and remained significantly increased from baseline through month 18 (Figure 2b). Bone-specific alkaline phosphatase (a second marker for bone formation) was increased compared to baseline at all time points through 18 months, but the increases were not statistically significant.

Figure 2.

Figure 2

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Percent change (reported as median values) in bone turnover markers at 3, 6, 9, 12, and 18 months compared to baseline. (a) Urinary N-telopeptide (U-NTx) (a marker for bone resorption), and (b) osteocalcin (a marker for bone formation). Markers for both bone resorption and formation became significantly elevated from baseline at 3 months and remained elevated through 18 months.

BMD was assessed by DXA at baseline and subsequently following surgery through 18 months. A 3.5% decrease in radial BMD from baseline was noted at 18 months, but this change was not statistically significant (P = 0.23). Due to the severe obesity of these patients, hip and spine measurements could not be performed.

To determine whether the mechanism of surgery(purerestriction vs. combined restriction and malabsorption) impacted our observed changes in the calcium–vitamin D–PTH axis, values for 25OHD, 1,25(OH)2D, and PTH from months 9 and 12 were pooled, stratified by surgery type, and compared to baseline. Serum 25OHD increased by 55.8% (P = 0.03) in GB patients from baseline to months 9 and 12, compared to 32.7% (P < 0.0001) in RYGB and BPD/DS patients. Median serum PTH levels at months 9 and 12 were also higher in the RYGB and BPD/DS patients compared to GB patients (71.0 pg/ml vs. = 0.88) 61.0 pg/ml). 1,25(OH)2D levels decreased by 0.16% (P from baseline to months 9 and 12 in GB patients, but increased 56.8% (P = 0.001) during the same period in RYGB and BPD/DS patients. The median 1,25(OH)2D level at months 9 and 12 was 83.7 pmol/ml in GB patients vs. 174.4 pmol/ml in RYGB and BPD/DS patients (Table 2). Data on bone turnover markers could not be stratified by surgery type due to the small number of subjects at each follow-up time point.

Table 2.

Changes in vitamin D/calcium/PTH axis following bariatric surgery

GB RYGB or BPD/DS
N 19 54
Post-op calcium (mg) 1,200 (optional) 1,200–1,800
Post-op vitamin D (IU) 400 1,200–1,600
25OHD (ng/ml)
 Month 0 20.3 (N = 6) 22.1 (N = 36)
 Month 9/12a 33.0 (N = 6) 31.0 (N = 36)
1,25(OH)2D (pmol/ml)
 Month 0 96.2 (N = 4) 114.0 (N = 17)
 Month 9/12a 83.7 (N = 4) 174.4 (N = 17)
Ca (mg/dl)
 Month 0 9.1 (N = 8) 9.3 (N = 37)
 Month 9/12a 9.4 (N = 8) 9.2 (N = 37)
PTH (pg/ml)
 Month 0 92.0 (N = 7) 73.0 (N = 35)
 Month 9/12a 61.0 (N = 7) 71.0 (N = 35)
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1,25(OH)2D, 1,25-dihydroxyvitamin D; 25OHD, 25-hydroxyvitamin D; BPD/DS, biliopancreatic diversion with duodenal switch; GB, gastric banding; post-op, postoperative; PTH, parathyroid hormone; RYGB, Roux-en-Y gastric bypass.

a

Denotes that values from months 9 and 12 were pooled.

DISCUSSION

Following bariatric surgery, aggressive supplementation led to a transient improvement in vitamin D status and secondary hyperparathyroidism. However, patient 25OHD levels decreased by 18 months with evidence of recurrent secondary hyperparathyroidism. PTHlevels were associated with increased serum 1,25(OH)2D. Markers of bone turnover remained elevated throughout the 18-month postoperative study period. No significant change in radial BMD was observed.

Before surgery, the vast majority of the patients had 25OHD levels <30 ng/ml. with evidence of secondary hyperparathyroidism. In the early postoperative period, a significant increase in 25OHD levels >30 ng/ml, accompanied by a significant decrease in PTH, was observed. With time, 25OHD subsequently leveled off and decreased <30 ng/ml, with PTH levels beginning to rise and reaching preoperative levels. The initial increase in 25OHD was likely due either to pre- or postoperative oral vitamin D supplementation and possibly the release of sequestered vitamin D into circulation. The ensuing plateau and fall in serum 25OHD may have occurred because the dose chosen for postoperative supplementation was insuficient. A possible component of malabsorption was suggested by the finding that the percent increase in serum 25OHD was lower in RYGB and BPD/DS patients than in GB patients despite more aggressive vitamin D supplementation in the former group. The early postoperative decrease in PTH was significant, but did not lead to normalization of serum levels, suggesting that even higher concentrations of 25OHD and perhaps more prolonged and aggressive treatment are required to reverse secondary hyperparathyroidism.

Starting at postoperative month 12, PTH began to increase from baseline, and this was possibly related to a combination of suboptimal vitamin D status and calcium malabsorption. Evidence of calcium malabsorption might have been detected had 24-h urinary calcium been measured. Serum 1,25(OH)2D at postoperative month 12 was found to be significantly increased from baseline and was positively associated with PTH. When stratified by surgery type, median 1,25(OH)2D level was 174.4 pmol/ml (a significant increase from baseline) at months 9 and 12 in RYGB or BPD/DS patients, compared to 83.7 pmol/ml (a nonsignificant change from baseline) in GB patients. Median serum PTH at the same time point was also higher in RYGB and BPD/DS patients (71.0 pg/ml vs. 61.0 pg/ml). While other studies (18) have reported 1,25(OH)2D measurements in the context of bariatric surgery, this study is the first to report that increased serum 1,25(OH)2D is associated with increased PTH postoperatively, and that this derangement is more specifically associated with malabsorptive surgical procedures.

Along with the increased levels of PTH and 1,25(OH)2D in RYGB and BPD/DS patients postoperatively, there was increased bone resorption and turnover. The significant and persistent increase in urinary NTx through postoperative month 18, was accompanied by a similar increase in osteocalcin—a bone formation marker—following surgery. These data provide evidence that both bone resorption and formation were increased through 18 months after bariatric surgery. While prior studies have consistently demonstrated increased bone resorption following bariatric surgery, the concurrent increases in bone formation have not been a consistent finding (8,9,11,18,23,24). In the present study, both resorption and formation markers changed in the same direction with no evidence of uncoupling of these processes. The mechanisms that govern bone resorption and bone formation following bariatric surgery are unclear. However, as PTH has been shown to activate both osteoclasts and osteoblasts (25), it seems possible that the postoperative elevation in bone turnover markers seen in this study could in part have been mediated by increased PTH and 1,25(OH)2D levels. In an effort to aggressively supplement postoperative bariatric surgery patients with vitamin D3 and calcium in order to suppress PTH levels and to maintain adequate 25OHD stores the RYGB and BPD/DS patients were instructed to take at least 1,200 mg/day of calcium, and 1,200 IU/day of vitamin D3 postoperatively. While this supplementation regimen was aggressive for the time at which the majority of the study cohort was recruited, it is important to note that the most recent guidelines issued by the American Society for Metabolic and Bariatric Surgery recommend even higher amounts of calcium and vitamin D intake following bariatric surgery (e.g., 1,500–2,000 mg/day of elemental calcium following RYGB, and 1,800–2,400 mg/day of elemental calcium as well as 2,000 IU/day of vitamin D following BPD/DS) (26). Our finding that urinary NTx increased even as 25OHD and PTH moved to normalcy suggests that factors beyond secondary hyperparathyroidism may have contributed to the observed increase in postoperative bone resorption. One potential factor is the rapid weight loss achieved by bariatric surgery, and indeed, prior studies have shown that weight loss alone in obese adults is associated with increased resorption markers, and decreased BMD (27).

BMD was measured at the distal 1/3 radial site by DXA at baseline and at postoperative month 18. Although there was a trend for lower radial BMD, the decrease was not significant. The wrist, with its higher cortical bone content, has a lower rate of turnover and is less likely to show a change in the BMD than other body sites. Our radial density findings, therefore, cannot be generalized to axial skeletal sites. However, prior studies examining sites with greater bone turnover such as hip and spine have reported lower BMD (8,11,12,18).

There were several limitations to this study. The most important was sample size. Second, of the 73 patients that underwent surgery, many did not follow-up at regular intervals. Insuficient follow-up, for example, did not permit stratification of the data on bone turnover markers and BMD by surgery type. This data would be especially valuable given our findings that suggest possible vitamin D malabsorption and secondary hyperparathyroidism following combined restrictive and malabsorptive operations. A third weakness was the lack of explicit data on patient adherence to postoperative nutritional supplementation. However, patients did meet at 3-month intervals with the bariatric surgery nutritionists, at which time the subjects’ dietary and supplement needs use were reinforced, and reviewed in detail. A fourth limitation was that the DXA machines could not measure BMD at the hip, femoral neck, or lumbar spine in patients weighing >300 pounds, thus BMD at these sites with higher trabecular bone content could not be evaluated. Finally, this study did not examine the possible roles of several newly described bone factors such as leptin, serotonin, osteopontin, and FGF23, as these assays were not routinely available at the initiation of this study.

In summary, this prospective longitudinal study followed GB, RYGB, and BPD/DS patients for 18 months. Preoperatively, the vast majority of patients had 25OHD levels <30 ng/ml with secondary hyperparathyroidism. With early postoperative supplementation, 25OHD levels increased, and serum PTH decreased significantly in the early postoperative period. By 18 months after surgery, 25OHD levels fell <30 ng/ml, whereas PTH levels rose and eclipsed preoperative levels. 1,25(OH)2D increased postoperatively, which correlated with serum PTH, possibly reflecting increased conversion of 25OHD to its active metabolite mediated by PTH. Markers of bone resorption and formation increased significantly following surgery, and remained elevated through 18 months. It is reasonable to conclude from this study that it is necessary to maintain adequate vitamin D stores following bariatric surgery in order to suppress PTH and assure better bone health, and that vitamin and mineral malabsorption may occur following operations with malabsorptive components. The postoperative calcium and vitamin D supplementation used in the RYGB and BPD/DS patients (1,200–1,800 mg of calcium and 1,200–1,600 IU vitamin D) was only transiently successful in ameliorating the preoperative secondary hyperparathyroidism. Persistence of adequate supplementation above the levels used in this study are required to maintain the long-term bone health of patients after bariatric surgery.

Acknowledgments

The authors were supported by the grants CTSC NIH 1UL1RR024996 and CTSC UL1-RR024996.

Footnotes

DISCLOSURE

The authors declared no conflict of interest.

References

  • 1.Ogden CL, Carroll MD, Curtin LR, et al. Prevalence of overweight and obesity in the United States, 1999–2004. JAMA. 2006;295:1549–1555. doi: 10.1001/jama.295.13.1549. [DOI] [PubMed] [Google Scholar]
  • 2.Eckel RH, Krauss RM. American Heart Association call to action: obesity as a major risk factor for coronary heart disease. AHA Nutrition Committee Circulation. 1998;97:2099–2100. doi: 10.1161/01.cir.97.21.2099. [DOI] [PubMed] [Google Scholar]
  • 3.Mokdad AH, Ford ES, Bowman BA, et al. Prevalence of obesity, diabetes, and obesity-related health risk factors, 2001. JAMA. 2003;289:76–79. doi: 10.1001/jama.289.1.76. [DOI] [PubMed] [Google Scholar]
  • 4.Buchwald H, Oien DM. Metabolic/bariatric surgery Worldwide 2008. Obes Surg. 2009;19:1605–1611. doi: 10.1007/s11695-009-0014-5. [DOI] [PubMed] [Google Scholar]
  • 5.Christou NV, Sampalis JS, Liberman M, et al. Surgery decreases long-term mortality, morbidity, and health care use in morbidly obese patients. Ann Surg. 2004;240:416–423. doi: 10.1097/01.sla.0000137343.63376.19. discussion 423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Brolin RE. Bariatric surgery and long-term control of morbid obesity. JAMA. 2002;288:2793–2796. doi: 10.1001/jama.288.22.2793. [DOI] [PubMed] [Google Scholar]
  • 7.Pugnale N, Giusti V, Suter M, et al. Bone metabolism and risk of secondary hyperparathyroidism 12 months after gastric banding in obese pre-menopausal women. Int J Obes Relat Metab Disord. 2003;27:110–116. doi: 10.1038/sj.ijo.0802177. [DOI] [PubMed] [Google Scholar]
  • 8.Giusti V, Gasteyger C, Suter M, et al. Gastric banding induces negative bone remodelling in the absence of secondary hyperparathyroidism: potential role of serum C telopeptides for follow-up. Int J Obes (Lond) 2005;29:1429–1435. doi: 10.1038/sj.ijo.0803040. [DOI] [PubMed] [Google Scholar]
  • 9.Olmos JM, Vázquez LA, Amado JA, Hernández JL, González Macías J. Mineral metabolism in obese patients following vertical banded gastroplasty. Obes Surg. 2008;18:197–203. doi: 10.1007/s11695-007-9307-8. [DOI] [PubMed] [Google Scholar]
  • 10.Ybarra J, Sánchez-Hernández J, Gich I, et al. Unchanged hypovitaminosis D and secondary hyperparathyroidism in morbid obesity after bariatric surgery. Obes Surg. 2005;15:330–335. doi: 10.1381/0960892053576758. [DOI] [PubMed] [Google Scholar]
  • 11.Coates PS, Fernstrom JD, Fernstrom MH, Schauer PR, Greenspan SL. Gastric bypass surgery for morbid obesity leads to an increase in bone turnover and a decrease in bone mass. J Clin Endocrinol Metab. 2004;89:1061–1065. doi: 10.1210/jc.2003-031756. [DOI] [PubMed] [Google Scholar]
  • 12.von Mach MA, Stoeckli R, Bilz S, et al. Changes in bone mineral content after surgical treatment of morbid obesity. Metab Clin Exp. 2004;53:918–921. doi: 10.1016/j.metabol.2004.01.015. [DOI] [PubMed] [Google Scholar]
  • 13.El-Kadre LJ, Rocha PR, de Almeida Tinoco AC, Tinoco RC. Calcium metabolism in pre- and postmenopausal morbidly obese women at baseline and after laparoscopic Roux-en-Y gastric bypass. Obes Surg. 2004;14:1062–1066. doi: 10.1381/0960892041975505. [DOI] [PubMed] [Google Scholar]
  • 14.Johnson JM, Maher JW, Samuel I, et al. Effects of gastric bypass procedures on bone mineral density, calcium, parathyroid hormone, and vitamin D. J Gastrointest Surg. 2005;9:1106–1110. doi: 10.1016/j.gassur.2005.07.012. discussion 1110. [DOI] [PubMed] [Google Scholar]
  • 15.Riedt CS, Brolin RE, Sherrell RM, Field MP, Shapses SA. True fractional calcium absorption is decreased after Roux-en-Y gastric bypass surgery. Obesity (Silver Spring) 2006;14:1940–1948. doi: 10.1038/oby.2006.226. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Avgerinos DV, Leitman IM, Martínez RE, Liao EP. Evaluation of markers for calcium homeostasis in a population of obese adults undergoing gastric bypass operations. J Am Coll Surg. 2007;205:294–297. doi: 10.1016/j.jamcollsurg.2007.02.078. [DOI] [PubMed] [Google Scholar]
  • 17.Jin J, Robinson AV, Hallowell PT, et al. Increases in parathyroid hormone (PTH) after gastric bypass surgery appear to be of a secondary nature. Surgery. 2007;142:914–920. doi: 10.1016/j.surg.2007.09.023. [DOI] [PubMed] [Google Scholar]
  • 18.Fleischer J, Stein EM, Bessler M, et al. The decline in hip bone density after gastric bypass surgery is associated with extent of weight loss. J Clin Endocrinol Metab. 2008;93:3735–3740. doi: 10.1210/jc.2008-0481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Youssef Y, Richards WO, Sekhar N, et al. Risk of secondary hyperparathyroidism after laparoscopic gastric bypass surgery in obese women. Surg Endosc. 2007;21:1393–1396. doi: 10.1007/s00464-007-9228-6. [DOI] [PubMed] [Google Scholar]
  • 20.Valderas JP, Velasco S, Solari S, et al. Increase of bone resorption and the parathyroid hormone in postmenopausal women in the long-term after Roux-en-Y gastric bypass. Obes Surg. 2009;19:1132–1138. doi: 10.1007/s11695-009-9890-y. [DOI] [PubMed] [Google Scholar]
  • 21.De Prisco C, Levine SN. Metabolic bone disease after gastric bypass surgery for obesity. Am J Med Sci. 2005;329:57–61. doi: 10.1097/00000441-200502000-00001. [DOI] [PubMed] [Google Scholar]
  • 22.Berarducci A, Haines K, Murr MM. Incidence of bone loss, falls, and fractures after Roux-en-Y gastric bypass for morbid obesity. Appl Nurs Res. 2009;22:35–41. doi: 10.1016/j.apnr.2007.03.004. [DOI] [PubMed] [Google Scholar]
  • 23.Bruno C, Fulford AD, Potts JR, et al. Serum markers of bone turnover are increased at six and 18 months after Roux-en-Y bariatric surgery: correlation with the reduction in leptin. J Clin Endocrinol Metab. 2010;95:159–166. doi: 10.1210/jc.2009-0265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Moreiro J, Ruiz O, Perez G, et al. Parathyroid hormone and bone marker levels in patients with morbid obesity before and after biliopancreatic diversion. Obes Surg. 2007;17:348–354. doi: 10.1007/s11695-007-9063-9. [DOI] [PubMed] [Google Scholar]
  • 25.de Paula FJ, Rosen CJ. Back to the future: revisiting parathyroid hormone and calcitonin control of bone remodeling. Horm Metab Res. 2010;42:299–306. doi: 10.1055/s-0030-1248255. [DOI] [PubMed] [Google Scholar]
  • 26.Aills L, Blankenship J, Buffington C, Furtado M, Parrott J Allied Health Sciences Section Ad Hoc Nutrition Committee. ASMBS Allied Health Nutritional Guidelines for the Surgical Weight Loss Patient. Surg Obes Relat Dis. 2008;4:S73–108. doi: 10.1016/j.soard.2008.03.002. [DOI] [PubMed] [Google Scholar]
  • 27.Villareal DT, Shah K, Banks MR, Sinacore DR, Klein S. Effect of weight loss and exercise therapy on bone metabolism and mass in obese older adults: a one-year randomized controlled trial. J Clin Endocrinol Metab. 2008;93:2181–2187. doi: 10.1210/jc.2007-1473. [DOI] [PMC free article] [PubMed] [Google Scholar]

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