By Susan E. Williams, RD, MD, MS, and Bradford Richmond, MD
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A 56-year-old woman with a history of severe obesity and Roux-en-y bariatric surgery six years ago presents to her primary care provider with vague complaints of fatigue, myalgias, arthralgias and weakness that have slowly been getting worse. Her medical history includes a pre-surgical weight of 340 pounds (154 kg) with a noted 160-pound (72.5 kg) weight loss in the first two years following the surgery. She is postmenopausal, has no history of fractures, nephrolithiasis or thyroid disease; does not smoke or consume alcohol; self-administers monthly intramuscular B12 injections, and takes a multivitamin tablet, 500 mg of calcium carbonate and 400 IU of vitamin D daily.
Following the patient’s bariatric surgery, she returned for her first two post-operative appointments but because she was feeling well, losing weight and had returned to work full-time, she cancelled all subsequent appointments with the surgeon, bariatrician and dietitian.
On physical examination, the patient’s weight is stable at 84.5 kg, height 165.1 cm, and BMI of 31. Her head, eyes, ears, nose, throat, heart lungs and abdomen are normal. She has weakness of the proximal leg musculature requiring her to use her arms to assist in arising from a chair, and reported discomfort when the proximal muscles of her arms and legs were palpated. The joint exam was significant for mild osteoarthritis of the hands and knees. Her neurological exam was normal.
Pertinent laboratory data
- Calcium: 7.9 mg/dL (reference range: 8.5–10.5 mg/dL)
- Albumin: 3.7 g/dL (3.4–4.7 g/dL)
- Magnesium 1.9 mg/dL (1.7–2.6 mg/dL)
- Phosphorus 2.7 mg/dL (2.4–4.5 mg/dL)
- Alkaline phosphatase 420 U/L (40–150 U/L)
- Intact parathyroid hormone 215 pg/mL (10–60 pg/mL)
- 25-hydroxyvitamin D < 7.0 ng/mL (31–80 ng/mL)
- 24-hour urine volume 2310 mL
- Urine creatinine normal
- Urine calcium 25.4 mg (100–300)
Dual-energy x-ray absorptiometry (DXA) data, lumbar spine
- Bone mineral density 0.933 g/cm2
- T-score -2.0
- Z-score -0.8
Left total hip
- Bone mineral density 0.628 g/cm2
- T-score -2.6
- Z-score -2.4
This classic presentation of a patient post-bariatric surgery who was lost to follow-up highlights the nonspecific and vague complaints that are frequently present for many months or years, and are often incorrectly diagnosed as fibromyalgia, rheumatoid arthritis, polymyalgia rheumatica, Paget’s’ disease or depression.1 It captures the following features that many of these patients have in common: low serum and urine calcium levels, very low or undetectable 25-hydroxyvitamin D levels, high alkaline phosphatase and secondary hyperparathyroidism; and a clinical picture consistent with both osteomalacia and osteoporosis.1 It also underscores the importance of baseline and continued monitoring of nutrients and biochemical markers in an effort to detect early indicators of malabsorption and ultimately prevent the development of metabolic bone disease (MBD), and the morbidity and mortality of a fragility fracture.
Initial treatment for this individual should include vitamin D repletion with 50,000 IU cholecalciferol, calcium supplements of at least 1,200 mg daily and address modifiable risk factors for fracture to include fall risk due to her proximal weakness. Repeat laboratory studies should be performed in 6–12 weeks, with calcium and vitamin D supplement dosages adjusted based on individual patient response. Once the serum calcium and PTH have normalized, consideration of the use of a bisphosphonate is appropriate, and repeat DXA in one to two years to monitor the effectiveness of the prescribed interventions is recommended.
The Obesity–Bone Connection
Severe obesity has historically been viewed as having a protective effect against the development of MBD. In fact, vitamin D and calcium deficiencies and elevated parathyroid hormone (PTH) levels are common in extremely obese individuals, placing them at risk for low bone mass.2-6 Studies attempting to define the prevalence of vitamin D deficiency have identified rates in excess of 60% among patients selected to undergo weight loss surgery.5,7 Similarly, the prevalence of elevated PTH in this population ranged from 25% to 48%.5,6
Postsurgically, severely restricted oral intake and significant weight loss, coupled with a procedure that bypasses the major site of calcium absorption, places many patients who have had bariatric surgery at extremely high risk for the development of MBD.5,8 With excess weight loss after combination restrictive/malabsorptive procedures, PTH levels increase, 25-hydroxyvitamin D levels decrease and corrected calcium levels usually remain within normal limits.3,9 Exclusively restrictive procedures such as gastric banding, first presumed not to alter bone metabolism, now also appear to place patients at risk for MBD due to inadequate intake of calcium and vitamin D in the immediate postoperative period.10
Numerous case reports in the literature further emphasize the ever-present risk of MBD in this population in the absence of adequate supplementation, citing occurrences of significant bone disease from eight weeks to 32 years after bariatric surgery.8,11-13
Although there are a wide variety of recommendations in the current literature, there are no uniformly accepted guidelines for perioperative screening, risk stratification and management of MBD in bariatric patients.6,14-17 Additionally, the literature remains inconclusive on key issues, such as when to start supplements, biochemical indices that should be checked prior to surgery, whether baseline and annual dual energy x-ray absorptiometry (DXA) should be done and if antiresorptive agents such as bisphosphonates should be used prophylactically during periods of rapid weight loss. With the prevalence of obesity increasing at an alarming rate, specialized medical management for this patient population is also essential.
The Role of DXA in the Care of the Patients Following Bariatric Surgery
We recommend that all patients seeking bariatric surgery have a baseline DXA as part of the preoperative evaluation. Until just a few years ago, central DXA was only available to patients weighing less than 275 pounds. In the absence of scanning tables that would accommodate patients with severe obesity, forearm DXA had been used to assess bone health and fracture risk; however, the forearm does not respond well to pharmacological therapy and therefore the ability to assess intervention efficacy will be severely limited. Larger scanning tables that accommodate patients up to 450 pounds are now available and allow the practitioner to use central measurements for baseline and follow-up with the precision equal to that of the traditional DXA scanners. For those patients who exceed the width of the table and in whom total body composition measurements are desired, a technique validated by one manufacturer (GE Lunar, Madison, Wisconsin) measures one side of the body then creates a computer-generated mirror image to accurately estimate total body composition.
The assessment of body composition has evolved from the use of anthropometrics to total body DXA. Initially, only total body measurements were reproducible. Today, the body can be divided into regions of interest such as the trunk, abdomen and extremities. Adipose distribution can be further delineated as either gynecoid or android thereby identifying patients at increased risk for cardiovascular disease.23-27
As with any disease process, patient-specific interventions for the prevention and treatment of MBD should be implemented. When considering treatment options, modifiable risk factors, severity of disease, and the patient’s ability and willingness to participate in their care must all be carefully considered. Modifiable risk factors for progression of bone disease must be addressed with all patients at risk. It is also important to identify those patients at high risk for falls due to poor visual acuity, frailty, neuropathy or dementia, and risk management strategies implemented to the degree possible.18
Follow-up BMD should be done according to the estimated monitoring time interval (MTI), which is derived from the statistically-defined least significant change divided by the anticipated change in bone density over time.28 When estimating the MTI for changes in body composition, the rate of weight loss and the psychological impact on the patient must be taken into consideration. In general, the use of DXA testing more frequently than every two years remains controversial unless initiating, monitoring or changing therapy, or monitoring conditions associated with rapid bone loss such as glucocorticoid therapy. In patients who have had bariatric surgery, however, there is convincing evidence that significant changes may be detected after 12 months that would influence clinical decision-making, particularly in the year immediately following surgery.8,10,13,15,20,21 Prescribed medications for the prevention and treatment of osteoporosis should also be an integral part of the treatment plan for at-risk patients with severe obesity. As with any medication, the decision to prescribe an antiresorptive or bone forming medication must take into consideration the patient’s risk-benefit profile, including the likelihood of gastrointestinal side effects and the ability and willingness to follow specific dosing instructions. Finally, for patients who are unable to absorb or tolerate oral antiresorptive medications, intravenous preparations are now available; however, specific recommendations concerning the use of anabolic or antiresorptive bone medications in perioperative bariatric patients have yet to be elucidated.
Preoperative assessment: We recommend obtaining baseline biochemical indices to include albumin, 25-hydroxyvitamin D, calcium, magnesium, phosphorus, alkaline phosphatase, folate, B12, TSH, parathyroid hormone and DXA on all candidates for bariatric surgery. These indices should be used to assess for MBD — and fracture risk, prompt pre-surgical interventions and guide the clinician in selecting appropriate postoperative interventions and surveillance. Starting a multivitamin with minerals and calcium with vitamin D is also recommended; however, prior to prescribing supplementation, a thorough nutrition history including the use of homeopathic medications, herbal preparations and supplements must be carefully reviewed. Many over-the-counter and over-the-internet supplements target bone health. While some may indeed be beneficial, others can be detrimental and need to be discontinued.21,22 Furthermore, in the patient with a severely restricted stomach capacity, it is important to ensure that less efficacious supplements do not compromise the intake of essential fluids, protein and prescribed medications.
Immediate postoperative period: It has been well demonstrated that hospitalization and surgical interventions result in nutrient deficiencies. In the patient who has had bariatric surgery, particularly those patients who had preoperative nutritional deficiencies, repletion in the immediate post-operative period is believed to be of benefit. Therefore, in the immediate post-operative period we recommend infusing a standard dose multivitamin (MVI) with minerals daily along with adequate intravenous hydration until the patient can resume oral feeding. Once the patient is able to tolerate liquids, pre-surgical supplementation needs to be resumed, preferably in a liquid or chewable form to facilitate tolerance and absorption.
Short and long-term follow-up: Postoperative follow-up visits with the bariatric specialist should start four weeks after surgery and should be conducted every three to four months for the first year. Provided the patient continues to do well, annual visits may be sufficient thereafter. During each visit, compliance with supplements and nutritional indices should be checked as indicated. A DXA should be repeated every one to two years depending upon the risk profile of the individual. A summary of risk factors, recommendations and interventions is provided in Table 2.5,18,19,29-31
Patients with severe obesity and patients who have had bariatric surgery are at increased risk of nutritional deficiencies that can result in the devastating effects of MBD. Meticulous preoperative screening, and aggressive interventions to normalize nutritional and bone indices prior to surgery are recommended. Providing a daily MVI with minerals in the immediate post-operative period is seen as potentially beneficial with little risk or cost associated with the intervention. Long-term follow-up should include monitoring of nutritional indices, judicious use of DXA, continued risk factor modification, and instituting timely medical management in an effort to prevent metabolic bone disease and the in patients who have had bariatric surgery.
- De Prisco C, Levine SN. Metabolic bone disease after gastric bypass surgery for obesity. Am J Med Sci. 2005;329:57-61.
- Ybarra J, Sanchez-Harnandez J, Gich I, et al. Unchanged hypovitaminosis D and secondary hyperparathyroidism in morbid obesity after bariatric surgery. Obes Surg. 2005;15:330-5.
- Hamoui N, Anthone G, Crookes F. Calcium metabolism in the morbidly obese. Obes Surg. 2004;14(1):9-12.
- Parikh SJ, Edelman M, Uwaifo GI, et al. Gastric bypass surgery for morbid obesity leads to an increase in bone turnover and a decrease in bone mass. J Clin Endocrinol Metab. 2004;89:1-9.
- Carlin AM, Rao DS, Meslemani AM, et al. Prevalence of vitamin D depletion among morbidly obese patients seeking gastric bypass surgery. Surg Obes Rel Dis. 2006;2(2):98-103.
- Puzziferri N, Blankenship J, Wolfe BM. Surgical treatment for obesity. Endocrine. 2006;29(1):11-19.
- Mason EM, Jalagani H, Vinik AI. Metabolic complications of bariatric surgery: diagnosis and management issues. Gastroenterol Clin N Am. 2006 34:25-33.
- Haria DM, Sibonga JD, Taylor HC. Hypocalcemia, hypovitaminosis D osteopathy, osteopenia and secondary hyperparathyroidism 32 years after jejunoileal bypass. Endocrine Prac. 2005;11(5):335-40.
- Newbery L, Dolan K, Hatzifotis M, et al. Calcium and vitamin D depletion and elevated parathyroid hormone following biliopancreatic diversion. Obes Surg. 2003;13(6):893-895.
- Pugnale N, Guisti V, Suter M, et al. Bone metabolism and risk of secondary hyperparathyroidism 12 months after gastric banding in obese pre-menopausal women. Int J Obesity. 2003;27:110-116.
- Goldner WS, O’Dorisio TM, Dillon JS, Mason EE. Severe metabolic bone disease as a long-term complication of obesity surgery. Obes Surg. 2002;12:685-92.
- Atreja A, Abacan C, Licata A. A 51-year-old woman with debilitating cramps 12 years after bariatric surgery. Cleveland Clin J Med. 2003;70:417-426.
- Collazo-Clavell ML, Jimenez A, Hodgson SF, et al. Osteomalacia after Roux-en-Y gastric bypass. Endocrine Pract. 2004;10:287-288.
- Hensrud DD, McMahon MM. Bariatric surgery in adults with extreme (not morbid) obesity. Mayo Clin Proc. 2006;81(10, suppl):S3-S4.
- Mason EM, Jalagani H, Vinik AI. Metabolic complications of bariatric surgery: diagnosis and management issues. Gastroenterol Clin N Am. 2006 34:25-33.
- McGlinch BP, Que FG, Nelson JL et al. Perioperative care of patients undergoing bariatric surgery. Mayo Clin Proc. 2006;81(10, suppl):S25-S33.
- Brethauer SA, Chand C, Schauer PR. Risks and benefits of bariatric surgery: Current evidence. Cleveland Clin J Med. 2006;73(11):993-1007.
- National Osteoporosis Foundation. Physician’s Guide to Prevention and Treatment of Osteoporosis. http://www.nof.org/physguide. Washington D.C. 1998.
- Bernstein CN, Leslie WD, Leboff M. AGA Technical Review: Osteoporosis in gastrointestinal diseases. Gastroenterology. 2003;124(3):795-841.
- Bloomberg RD, Fleishman A, Nalle JE, et al. Nutritional deficiencies following bariatric surgery: What have we learned? Obes Surg. 2005;15:145-154.
- Williams S, Seidner D. Metabolic Bone Disease in Gastrointestinal Illness. Gastroenterol Clin N Am. 2007;36(1):161–190.
- National Osteoporosis Foundation. Osteoporosis Clinical Updates: Over-the-counter products & osteoporosis: Case discussions. 2002; Vol III Issue 2. Washington D.C.
- Park YW, Heymsfield SB, Gallagher D. Are dual-energy X-ray absorptiometry regional estimates associated with visceral adipose tissue mass? Int J Obes Relat Metab Disord. 2002;26(7):978-983.
- Glickman SG, Marn CS, Supiano MA, et al. Validity and reliability of dual-energy X-ray absorptiometry for the assessment of abdominal adiposity. J Appl Physiol. 2004;97:509-514.
- Hull HR, Hester CN, Fields DA. The effect of the holiday season on body weight and composition in college students. Nutr & Metab. 2006;3:44-51.
- Aubertin-Leheudre M, Goulet EDB, Khalil A, et al. Effect of Sarcopenia on Cardiovascular Disease Risk Factors in Obese Postmenopausal Women. Obesity. 2006;14:2277-2283.
- Lubrano C, Cornoldi A, Pili M, et al. Reduction of risk factors for cardiovascular diseases in morbid-obese patients following biliary-intestinal bypass: 3 years’ follow-up. Int J Obes Relat Metab Disord. 2004;28(12):1600-1606.
- Bonnick SL, Johnston Jr CC, Kleerekoper M, et al. Importance of Precision in Bone Density Measurements. J Clin Densitom. 2001;4(2):105-110.
- Neumann L, Jensen BG. Osteomalacia from Al and Mg antacids. Report of a case of bilateral hip fracture. Acta Orthop Scand. 1989;60(3):361-362.
- Xanthakos SA, Daniels SR, Inge TH. Bariatric surgery in adolescents: an update. Adolesc Med. 2006;17:589-612.
- National Institutes of Health Osteoporosis and Related Bone Diseases: National Resource Center Web Site. National Institute of Arthritis and Musculoskeletal and Skin Diseases. Washington D.C. www.niams.nih.gov