Osteoporosis Clinical Updates

www.nof.org Clinical Information for Healthcare Professionals Fall 2013

Bariatric Surgery and Skeletal HealtH

Obesity is a public health issue of epidemic proportions, ranked the number-one threat to American health by the CDC since 2004. One third of American adults are obese (BMI ≥ 30 kg/m2) and 68% are either overweight or obese (BMI ≥ 25 kg/m2).1 Although overall obesity rates have leveled off in the U.S., the rate of severe obesity (BMI ≥40 kg/m2) continues to climb. Obesity in children and adolescents is also increasing at alarming rates, with an estimated 30% of the population age 2 to 19 at or above the 85th percentile of BMI for their age in 2008.2,3

There has been a marked increase in weight loss (bariatric) surgical procedures in the U.S. in recent decades, from 13,365 in 1998 to an estimated 220,000 in 2008 (most current year’s data).1,3,7,8 Primary care practitioners are expected to see increasing numbers of patients who have had weight-loss surgery. Managing their care requires recognizing the special nutritional needs of these patients and the hazards presented by long-term nutrient insufficiencies, such as osteomala-cia, osteoporosis, and bone fractures. If carefully followed and appropriately supplemented, post-bariatric patients can avoid these risks and reap the numerous benefits of weight loss.

In this issue of “Osteoporosis: Clinical Updates,” we will take a look at surgical weight management techniques and their effects on skeletal health, highlighting the need for lifelong surveillance in this patient population. Editor-in-Chief, Angelo Licata, MD, PhD, FACP, FACE

National Osteoporosis Foundation

1150 17th Street, NW • Washington, DC 20036 • 202/223-2226 • www.nof.org

© National Osteoporosis Foundation. All rights reserved

EDITORIAL BOARDEditor-in-Chief, Angelo Licata, MD, PhDDepartment of EndocrinologyCleveland Clinic

Adrienne Berarducci, PhD, ARNP, BCUniversity of South Florida

Carolyn J. Bolognese, RN, CDEBethesda Health Research Center

JoAnn Caudill, RT, BD, CDTCarroll Arthritis, P.A.

Peggy Doheny, PhD, RN, CNS, ONCKent State University College of Nursing

Patricia Graham, MD, PCPhysical Medicine and Rehabilitation /Integrative Medicine

Craig Langman, MDNorthwestern University

Barbara Messinger-Rapport, MD, PhDCleveland Clinic

Paul D. Miller, MDColorado Center for Bone Research

Jeri Nieves, PhD Columbia University, Helen Hayes Hospital

Mary Beth O’Connell, PharmD, BCPSEugene Applebaum College of Pharmacy and Health Sciences

Rick Pope, MPAS, PA-C, DFAAPAQuinnipiac University

Carol Sedlak, PhD, RN, CNS, ONC, CNEKent State University College of Nursing

Andrea Sikon, MD, FACP, CCD, NCMPCleveland Clinic

NOF Clincal Director, Andrea Singer, MDGeorgetown University Medical School

Managing Editor, Kelly Trippe, MANational Osteoporosis Foundation

Nurse CE Planner, Susan Randall, RN National Osteoporosis FoundationDisclaimer: Osteoporosis: Clinical Updates is published by the National Osteoporosis Foundation (NOF).The views and observations presented in Osteoporosis: Clinical Updates are not those of the authors/editors and do not reflect those of the funders or producers of this publication. Readers are urged to consult current prescribing and clinical practice information on any drug, device, or procedure discussed in this publication.

ContentsBariatric Surgery: Implications for Bone Health . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

Indications for Bariatric Surgery . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2Bariatric Surgery for Older Adults and Adolescents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4Impact of Obesity on Bone . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5Impact of Weight Loss on Bone . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

Bariatric Surgical Procedures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6Roux-en-Y Gastric Bypass (RYGB) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7Biliopancreatic Diversion with Duodenal Switch (BPD/DS) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7Bone Loss Following RYGB and BPD/DS Procedures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9Laparoscopic Sleeve Gastrectomy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9Laparoscopic Adjustable Gastric Band . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10Bone Loss Following LSG and LAGB Procedures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

Protecting Bone Health in Bariatric Patients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11Diagnosing and Treating Osteoporosis in Bariatric Patients . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13Drug Treatment for Osteoporosis in Bariatric Patients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

Patient Cases: Preserving Bone Health Following Bariatric Surgery . . . . . . . . . . . 14Case 1: 45-Year-Old Woman who Had Roux-en-Y Gastric Bypass Surgery . . . . . . . . . . . . . . . . 14 Case 2 . 60-Year Woman 20 Years after Jejunoileal Bypass Surgery . . . . . . . . . . . . . . . . . . . . . . . . 16Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18

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Bariatric Surgery: implicationS for Bone HealtH

Obesity is responsible for more than 40 serious medical conditions including hypertension, multiple cancers, metabolic syndrome, nonfatty liver disease, degenera-tive joint disease, and reproductive complications. It is estimated to increase risk for premature death 50% to 100% from all causes.4,5,6 According to a report from the U.S. Office of the Surgeon General, roughly 300,000 deaths per year are linked to obesity.6

Although recognized as a cause of disease and increased mortality, obesity has long been viewed as beneficial to bone. Increasing evidence has challenged this belief and implicated overweight and obesity in disordered bone metabolism.

Severely obese people are frequently unable to achieve and maintain a healthy weight through diet and exer-cise. Many spend adolescence and adulthood in a con-stant struggle, losing weight only to regain that weight and more. Bariatric surgery is the most effective treat-ment for people who have failed at supervised medical weight loss. It can provide durable weight reduction and improve or reverse obesity-related illnesses.

Common bariatric procedures alter hormonal mecha-nisms that control the body’s hunger and satiety re-sponses, increasing glucose metabolism, accelerating burning of fat, and improving glucose homeostasis, type 2 diabetes, and cardiometabolic disease. This has led to the view that these procedures should be consid-ered “metabolic,” rather than simply weight-reduction,

surgeries.9

Large prospective studies of patients who have under-gone bariatric surgery, show high rates of remission or significant improvement in many obesity-related ill-nesses, such as diabetes (77% to 86%), hyperlipidemia (70%), hypertension (62% to 79%), obstructive sleep apnea (84% to 86%), and overall mortality (30% in the15 years post surgery). Risk for developing certain types of cancer has also been observed to decline by 60% following bariatric surgery.6, 10-16

These enormous health benefits do not come without costs. Bariatric surgery induces weight loss by limiting intake and/or absorption of nutrients, including those necessary for healthy bone. If these nutrients are not replaced, serious complications can develop, both in the immediate postsurgical period and decades down the road.

The take-away message for primary care providers is that all bariatric patients will have some sort of nutri-tional deficit. Lifelong medical surveillance and supple-mental nutrient support are key components of patient care in this setting. Without this support, patients will be at increased risk for many disorders, including bone loss, metabolic bone disease, and fragility fracture.

Because long-term data on post-bariatric rates of osteo-porosis and fracture are unavailable, we rely on surro-gate indicators of bone strength, primarily bone miner-al density (BMD) by dual x-ray absorptiometry (DXA). In addition, fracture risk is inferred by applying what is known about conditions that precipitate osteoporosis in non-obese individuals, such as calcium and vitamin D deficiency and secondary hyperparathyroidism.

Indications for Bariatric Surgery

An expert panel convened by the National Institutes of Health in 1991 developed guidelines that included rec-ommendations for adults who should be considered for weight-loss surgery:

“Weight loss surgery is an option for carefully selected patients with clinically severe obesity BMI ≥40 or ≥35 with comorbid conditions when less invasive methods of weight loss have failed and the patient is at high risk for obesity-associated morbidity or mortality.” 17

On the strength of evidence that bariatric surgery is effective in resolving type 2 diabetes in 48% to

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98% of patients, the American Association of Clinical Endocrinologists as well as the International Diabetes Federation now recommend bariatric surgery for adult patients with BMI 30 to 35 with type 2 diabetes who have been unable to achieve adequate glycemic control through diet, exercise, and standard medi-cal therapies.9,18 This recommendation is included in guidelines developed by a joint committee of the American Association of Clinical Endocrinologists, The Obesity Society, and American Society for Metabolic & Bariatric Surgery (AACE/TOS/ASMBMS).9

The long-term impact on type 2 diabetes and metabolic syndrome has yet to be validated. One large retrospec-tive cohort study looking at over 4,000 patients with type 2 diabetes who underwent gastric bypass surgery found 68.2% achieved remission after surgery. A little over 1/3 of these (35.1%) redeveloped diabetes within 5 years.19 Durability of remission has been associated with many factors including bariatric technique, patient age, duration of diabetes, preoperative insulin therapy, preoperative glycemic control, as well as postoperative percentage of excess weight lost and/or regained.19,20,21

NIH Classifications for BMI2

Underweight <18.5 kg/m2

Normal weight 18.5 to 24.9 kg/m2

Overweight 25 to 29.9 kg/m2

Obesity (class 1) 30 to 34.9 kg/m2

Obesity (class 2) 35 to 39.9 kg/m2

Extreme obesity (class 3) ≥40 kg/m2

A new category, super obesity, is used in the field to describe people with BMI ≥50 kg/m2. There is no ev-idence-based consensus regarding contraindications to bariatric surgery; however, the AACE/TOS/ASMBMS guidelines recommend exclusion of patients with cur-rent substance abuse, poorly controlled mental illness, or underlying conditions that put them at unacceptably high surgical risk.

These guidelines also recommend exclusion of indi-viduals who are judged to be unable or unwilling to comply with lifelong clinical monitoring, nutrient supplementation, and dietary requirements.9

Calculating Body Mass Index (BMI)

Measurement Units Formula and Calculation

Kilograms and meters (or centimeters)

Formula: weight (kg) / [height (m)]2

With the metric system, the

formula for BMI is weight

in kilograms divided by

height in meters squared.

Since height is commonly

measured in centimeters,

divide height in centimeters

by 100 to obtain height in

meters.

Example: Weight = 68 kg,

Height = 165 cm (1.65 m)

Calculation: 68 ÷ (1.65)2 =

24.98

Pounds and inches

Formula: weight (lb) / [height (in)]2 x 703

Calculate BMI by dividing

weight in pounds (lbs)

by height in inches (in)

squared and multiplying by

a conversion factor of 703.

Example: Weight = 150 lbs,

Height = 5'5" (65")

Calculation: [150 ÷ (65)2] x

703 = 24.96

This last issue is of particular relevance in primary care. It is difficult for many post-surgical bariatric patients to keep up with frequent clinical follow up and the demands of daily supplementation/dietary require-ments. Clinicians can improve compliance through a coordinated multi-pronged approach that includes ap-pointment reminders, nutritional counseling, exercise

Table 1. Conversion formulas for calculating body mass index (BMI) values. (Graphic Source: U.S. Centers for Disease Control and Prevention. Division of Nutrition, Physical Activity, and Obesity, National Center for Chronic Disease Prevention and Health Promotion. http://www.cdc.gov/healthyweight/assessing/bmi/adult_bmi/. Accessed September 27, 2013.)

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programs, and patient support groups. A team of nurs-es, dieticians, physical therapists, and patient educators working in coordination has repeatedly been shown to increase the odds that patients will be able to maintain a healthy weight and avoid complications.23-26

Bariatric Surgery for Older Adults and Adolescents

Advanced age was once considered a contraindication for bariatric surgery. However, today the prevalence of adults over age 65 receiving bariatric surgery is in-creasing (around 5%). Although data are lacking, it is reasonable to assume that bariatric patients over age 65 have higher rates of osteoporosis and fracture than those under 65. In this population, many factors con-tribute to increased fracture risk beyond age-related BMD decline. Older patients are more likely to be diabetic, which may put them at increased risk for certain fractures following weight loss surgery (e.g. humerus). They are also more likely to have peripheral neuropathy, either diabetes related or due to nutrient deficiency (B6, B12).

Neuropathy significantly increases risk of falls, which are the leading cause of traumatic death in older adults. We don’t currently have data on long-term fracture rates of bariatric patients at various ages. More research is needed to assess the skeletal consequences of bariat-ric surgery in older adults.

As obesity has risen in the pediatric population, so has the frequency of weight-loss surgery among individu-als under age 18, although it is still relatively rare. Prevalence rates for weight loss surgery in adolescents have not changed substantially in the past decade, cur-rently representing about 2.5 out of 100,000 proce-dures. However, absolute numbers have risen.27,28 A retrospective cross-sectional study of discharge data obtained from Healthcare Cost and Utilization Project Kid’s Inpatient Database, published in the February, 2013, issue of JAMA Pediatrics, reported that bariatric procedures on adolescents increased from ~300 in 2000 to ~1000 in 2009.26

From the perspective of bone health, bariatric surgery presents a potentially serious threat for children and teens. Vitamin D deficiency in adolescence can lead to increased risk for metabolic bone disease if uncorrect-ed.29 The long-term health effects of pediatric bariatric surgery are beyond the scope of this article. However,

Osteoporosis: Clinical Updates

Osteoporosis Clinical Updates is a publication of the National Osteoporosis Foundation (NOF). Use and reproduction of this publication for educational purposes is permitted and encouraged without permission, with proper citation. This publication may not be used for commercial gain. NOF is a non-profit, 501(c)(3) educational organization. Suggested citation: National Osteoporosis Foundation. Osteoporosis Clinical Updates. Issue Title. Washington, DC; Year.

Please direct all inquiries to: National Osteoporosis Foundation 1150 17th Street NW Washington, DC 20037, USA Phone: 1 (202) 223-2226Fax: 1 (202) 223-1726 www.nof.org

Statement of Educational PurposeOsteoporosis Clinical Updates is published to improve osteoporosis patient care by providing clinicians with state-of-the-art information and pragmatic strategies on prevention, diagnosis, and treatment that they may apply in clinical practice.

Overall Objectives Despite the availability of effective prevention, diagnostic, and treatment protocols for osteoporosis, research indicates that it is significantly underdiagnosed and undertreated in the general population. Through this publication, NOF encourages participants to incorporate current evidence and expert recommendations into clinical practice to improve the bone health of their patients. Upon completion of each issue of Osteoporosis Clinical Updates, participants should be able to:• Recognize current concepts in osteoporosis research

and clinical practice • Identify implications of these concepts for osteoporosis

patient care• Adopt evidence-based strategies to study, prevent, and/

or treat osteoporosis• Improve patient care practices by integrating new data

and/or techniques

Intended AudienceThis continuing education activity is intended for health professionals who care for patients at risk for or suffering from osteoporosis practicing in primary care, endocrinology, geriatrics, gynecology, internal medicine, obstetrics, orthopedics, osteopathy, pediatrics, physiatry, radiology, rheumatology, and/or physical therapy.

This includes physicians, nurse practitioners, registered nurses, pharmacists, physician assistants, technologists, researchers, public health professionals and health educators with an interest in osteoporosis and bone health.

5

it is a subject of growing concern and focused research.

Impact of Obesity on Bone

Bone health is mediated by a complex metabolic system of checks and balances involving, among other things, calcium, vitamin D, and parathyroid hormone (PTH). The link between vitamin D deficiency, elevated PTH, and bone disease has long been recognized.30 When serum calcium drops below a healthy level, PTH secre-tion rises, mobilizing release of calcium from bone. By this mechanism, a sustained state of calcium deficiency leads to secondary hyperparathyroidism, which is known to cause skeletal deterioration.31

Vitamin D deficiency is extremely common in obese individuals. The reasons suggested for this are complex. Poor diet plays a part, as does sequestration of vitamin D in adipose tissue, which reduces serum bioavailabil-ity.32 Studies have shown 60 to 86% of candidates for bariatric procedures are deficient in vitamin D before surgery.33-35

Vitamin D deficiency is seen following bariatric surgery as well. An initial upward trend in serum vitamin D has been observed in the first month following bariatric surgery, but levels decline thereafter.36 It has been spec-ulated that the initial rise is from release of fat-stored vitamin D during the immediate postsurgical period of rapid and intense weight loss.37 Studies at one to three years following surgery have found no change or mod-est reductions in the rates of vitamin D deficiency. One retrospective study found that, whereas 86% of the study cohort was vitamin D deficient before bariatric surgery, 70% were one year after.38 Several other stud-ies have seen no improvement in vitamin D status three years following malabsorptive bariatric surgery.39,40 Causes for postsurgical vitamin D deficiency are under study; however, known contributing factors include continued obesity, reduced food intake, and impaired absorption.14,41

In both obese and healthy-weight people, vitamin D deficiency varies by population. Prevalence of vita-min D deficiency before and after bariatric surgery is significantly higher in African Americans than in Caucasians.42,43

Impact of Weight Loss on Bone

Obesity has long been viewed as protective against

CME Program Eligibility Method of Participation in the Learning Process: Clinician learners will read and analyze the subject matter, conduct additional informal research through related internet searches on the subject matter, and complete a post-test assessment of knowledge and skills gained as a result of the activity.

After participating in this activity, the reader has the option of taking a post-test with a passing grade of 70% or better to qualify for continuing education credit for this activity. It is estimated it will take 1.0 hour(s) to complete the reading and take the post-test. Continuing education credit will be available for two years from the date of publication.

Accreditation The National Osteoporosis Foundation is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. The National Osteoporosis Foundation designates this educational activity for a maximum of 1.0 AMA PRA Category 1 Credit(s)TM. Physicians should only claim credit commensurate with the extent of their participation in the activity.

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The National Osteoporosis Foundation designates this educational activity for a maximum of 1.0 continuing nursing education credit(s).

Other healthcare providers will also be able to receive a certificate of completion; nurse practitioners and physician assistants may request an AMA PRA Category 1 Credit(s)™ certificate of participation.

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in the body and its response to mechanical loading and hormonal changes that result from weight loss.

Weight loss, whether by surgical or nonsurgical means, causes bone loss and fragility fractures in older individ-uals, regardless of BMI. One large prospective study of 6000+ older women (>68 years) observed a two-fold increase in hip fracture among women who lost 5% of their body weight, regardless of their baseline or final weight.49 Several studies of older men showed declines in BMD associated with weight loss 3 to 4 times higher than control cohorts.50,51,52

The degree of bone loss attributable to surgical weight reduction is proportional to the magnitude and speed of weight loss, which varies by bariatric procedure.53,54 More weight is lost in the year following procedures that induce malabsorption than following procedures that solely restrict caloric intake (30% to 40% vs. 25%). So too, greater bone loss is seen following malabsorptive type procedures than restrictive. As ob-served in nonsurgical weight loss, this bone loss varies by site, with more bone lost at the weight-bearing hip region than at spine and radius.54 We will discuss data for bone effects of specific bariatric procedures below.

Bariatric Surgical procedureS

The most commonly performed bariatric procedures in the U.S. are the Roux-en-Y gastric bypass (RYGB), the laparoscopic sleeve gastrectomy (LSG), the laparo-scopic adjustable gastric band (LAGB), and the bilio-pancreatic diversion with duodenal switch (BPD/DS).9 All rely on structural and hormonal mechanisms to in-duce weight loss, either by restricting intake or limiting absorption, or both.

With the exception of the LAGB, bariatric procedures performed today alter neuro-hormonal mechanisms that control hunger and satiety. All are usually per-formed laparoscopically. As compared with open pro-cedures, laparoscopic procedures are associated with less postoperative pain, lower morbidity and mortality, lower risk of hernia, and shorter hospital stays and re-covery periods.55

A variety of older gastric bypass bariatric procedures have been abandoned for reasons of complications; severe nutrient deficiencies; inadequate, excessive, or unsustained weight loss; and/or high rates of surgi-cal revision. These include biliopancreatic diversion

bone loss and fracture due to the positive effects of mechanical loading on bone formation. Research sug-gests that any such protection is site specific. Whereas obesity is associated with lower fracture risk and higher BMD at weight-bearing sites (e.g. hip and pelvis), it is associated with higher fracture risk at non-weight-bear-ing sites (e.g. humerus and ankle).44-48 Data on obesity-related vertebral fracture rates are inconsistent, with some studies reporting no difference and others seeing increased risk over normal weight cohorts.10,48 These variations reflect the effects of vitamin, mineral, and metabolic conditions prevalent in obese individuals as well as the distribution of trabecular and cortical bone

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(BPD), jejunocolic bypass, jejunoileal bypass, and verti-cal banded gastroplasty. Although these procedures are no longer performed, thousands who underwent them still need to be followed for nutritional deficiencies and their metabolic sequellae.

Roux-en-Y Gastric Bypass (RYGB)

The Roux-en-Y gastric bypass (RYGB), frequently re-ferred to simply as gastric bypass, is the technique used in 80% of the weight-loss surgery performed in the U.S.3

The RYGB has been called a “combined” bariatric pro-cedure because it induces weight loss through both intake restriction and malabsorption. RYGB patients experience dramatic weight loss of up to 70% of ex-cess body weight that is sustained for more than 10 years.56,57 RYGB surgery is performed by creating a small pouch at the opening to the stomach, restricting gastric capacity. Next, a Y-shaped section of the small intestine is attached to the pouch, allowing food to bypass the lower stomach, the duodenum, and the first portion of the jejunum, reducing absorption of calories and nutrients.

The RYGB procedure alters secretion of hormones that signal satiety, contributing to weight loss. In addi-tion, many patients who have undergone RYGB surgery

develop “dumping syndrome” in response to ingestion of high-density carbohydrates. Eating carbohydrate-dense foods becomes very unpleasant, motivating pa-tients to adopt healthier eating habits and improving the likelihood of long-term maintenance of weight loss.

Biliopancreatic Diversion with Duodenal Switch (BPD/DS)

Biliopancreatic diversion with duodenal switch (BPD/DS) is a combination restrictive-gastric bypass proce-dure that induces weight loss predominantly through caloric and fat malabsorption. The BPD/DS is distinct from the no-longer-performed biliopancreatic diver-sion (BPD) surgical technique; however, they share the common feature of diverting bile and pancreatic fluids that are normally released into the duodenum to digest food and break down fats, carbohydrates, and proteins.

BPD/DS is typically the surgery of choice for super-obese patients (BMI ≥50). It has been shown to pro-duce the greatest sustained excess weight reduction (~70%), as well as superior long-term resolution of diabetes, hypertension, and dyslipidemia in the super-obese population.58-61

In a BDP/DS procedure, the stomach is sectioned vertically, creating a small tube that terminates past

Figure 1. The Roux-en-Y gastric bypass procedure creates a small gastric pouch that is anastamosed to the proximal jejunum. The remainder of the stomach, duodenum, and proximal jejunum are bypassed and rejoin the distal roux limb in a Y configuration. (Graphic Source: NIH Publication Number 00-4084. Copyright 1997-2013, A.D.A.M., Inc.)

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Every 3 to 6 months• CBC, platelets • Electrolytes • Glucose • Iron studies, ferritin • Phosphorus• Vitamin B12 • Liver function • Lipid profile • Albumin and prealbumin • RBC folate Every 6 to 12 months• Vitamin A • 25-Hydroxyvitamin D • Vitamin E • Vitamin K1 and INR• Intact PTH Annually• 24-Hour urine calcium, citrate, uric acid, and

oxalate• Selenium • Urine N-telopeptide • ZincAs indicated• Osteocalcin • Carnitine • Essential fatty acid chromatography

the pylorus and empties through a shortened segment of duodenum. The small intestine is divided close to the large intestine and then attached to this shortened duodenal segment, creating a bypass limb. The remain-ing duodenal segment, still connected to the pancreas and gallbladder, is attached to this bypass limb, allowing ingested food to mix with digestive secretions before passing into the large intestine. Reducing exposure to digestive breakdown and intestinal absorption struc-tures in this way dramatically limits caloric and nutri-ent uptake.

BDP/DS procedures have not been widely performed in the U.S. (~3% of bariatric procedures). However, as the prevalence of super-obesity increases, this may change. BPD/DS is a more complex and lengthy surgi-cal procedure than RYGB, LSG, and AGB and is associ-ated with greater blood loss and longer recovery time. BDP/DS is also associated with a variety of postsurgi-cal nutritional and metabolic complications, including protein-calorie malnutrition, anemia, vitamin D defi-ciency, and metabolic bone disease.

To ensure nutrient sufficiency in BPD/DS (and BDP) patients, AACE/TOS/ASMBS guidelines recommend the following laboratory tests, every three months in the first year after surgery, and every 3 to 12 months thereafter, depending on symptoms.62

Figure 2. The biliopancreatic diversion with duodenal switch procedure creates a vertical (sleeve) gastrectomy that preserves the pylorus. The biliopancreatic limb is attached just distal to the pylorus and 50 cm from the ileo-cecal valve. Weight loss occurs predominantly because of calorie and fat malabsorption. (Graphic Source: NIH Publication Number 00-4084. Copyright 1997-2013, A.D.A.M., Inc.)

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following RYGB. In this study, an inverse relationship was seen between rising serum PTH and declining cor-tical density, thickness, and area.54

Evidence for bone loss in older, more severely malab-sorptive techniques has been documented.57,70 Looking at jeujunoileostomy and BPD patients 15 years after surgery, a study conducted by Bano, et. al., found sig-nificantly lower spine BMD (15%) in men over 50 and postmenopausal women not on hormone therapy.70

Laparoscopic Sleeve Gastrectomy

Until recently, the laparoscopic sleeve gastrectomy (LSG) was considered an investigational bariatric tech-nique. It is now considered a primary procedure. Data from large placebo-controlled studies have shown LSG to be comparable or superior to RYGB and LAGB in magnitude and durability of weight reduction, rate of complications, and improvement in obesity-related conditions, such as diabetes and cardiovascular disease.71,72

Data reported from the American College of Surgeons Bariatric Surgery Center Network’s longitudinal da-tabase (n=28,616) positioned LSG above LAGB and below RYGB with regard to rates of morbidity, read-mission, and reoperation/interventions.73

Bone Loss Following RYGB and BPD/DW Procedures

Bariatric techniques that induce malabsorption, such as RYGB and BDP/DS, bypass the duodenum and proximal jejunum, the primary absorption sites for vitamins and minerals such as iron and calcium. As a result, deficiencies in calcium (25% to 50%) and vita-min D (>50%) have been observed in patients follow-ing RYGB and BPD/DS.63,64 Depending on the length of intestine bypassed, patients also experience greater or lesser deficits of other nutrients necessary for bone health including protein, folate, iron, magnesium, thia-mine, B12, and fat-soluble vitamin A.

Even with increased intake of calcium and vitamin D, malabsorptive procedures are linked to bone loss. One year following RYGB, BMD declined 9.2% to 10.9% at femoral neck and 8% to 10% at total hip in women on supplemental vitamin D and calcium in two studies.65,66,67 Declines have also been observed at the lumbar spine one year after RYGB surgery (3.6% to 7.4%).65,66

Data for bone loss at the forearm are inconclusive. Studies have shown between 0% and 5% at one year postoperative (n=12; n=23).68,69 A study that distin-guished total forearm from radius measured BMD declines at the total forearm that continued for three years but no change at the radius (total forearm T-score 0.55 year 1, -3.6 year 2, -1.8 year 3).67 Losses at the hip and spine stabilized after the first year as weight re-duction plateaus.

In addition to nutrient-related causes of bone loss, re-duced mechanical loading increases bone turnover at weight-bearing sites, such as the hip, in direct propor-tion to the magnitude of weight lost, which is substan-tial following malabsorptive procedures.

Bone at weight-bearing sites, predominantly trabecular bone, has been observed to increase or decrease in den-sity as mechanical loading increases or decreases. Non-weight-bearing bone, predominantly cortical, does not respond in the same way to mechanical loading. It is, however, sensitive to the effects of PTH, which in-creases dramatically with the substantial weight loss in-duced by malabsorptive bariatric procedures. A recent study that used high-resolution peripheral quantitative computed tomography (HR-PQCT) identified deterio-ration in cortical bone at the tibia but not other sites

Figure 3. The laparoscopic sleeve gastrectomy creates a narrow gastric tube by removing 2/3 of the stomach, preserving the duodenum and jejunum. (Graphic Source: NIH Publication Number 00-4084)

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stomach to create a small pouch that reduces stomach capacity to approximately 30 to 50 ml. The new stom-ach fills quickly and gives the patient a feeling of sati-ety. The band slows the flow of food into the digestive tract. The band’s tightness, and thus the pouch outlet, is adjustable through saline injection via subcutaneous injection port.

Recovery following LAGB surgery is quicker than laproscopic RYGB. It is fully reversible and does not result in the malabsorption syndromes attendant to RYGB and other surgeries that bypass all or portions of the small intestine. However, LAGB has been shown to result in significantly less initial weight loss than RYGB, although this difference may diminish over time.76 Studies of patients 4 to 10+ years after LAGB show sustained weight loss of >40% excess body weight, which is comparable to RYGB.58

LAGB is, however, associated with a high rate of major complications. Postoperative complications requiring revision, mainly band slippage and/or erosion, have been seen in 30% to 60% of patients depending on study cohort.77,78,79,80 The incidence of failure rises with time. One study showed the failure rate due to excessive weight loss or device/surgical failure increas-ing from ~40% at year 5 to ~60% at year 7 following LAGB.81 As a result of these complications, perfor-mance of LAGB is on the decline.

The LSG is so called because it creates a sleeve-like structure by removing 1/3 of the stomach vertically. Originally conceived as purely restrictive in mecha-nism, recent findings suggest that LSG also induces weight reduction through regulation of intestinal hormones that control hunger and satiety as is seen in RYGB.71

As a surgical technique, LSG is less complicated than RYGB and BPD/DS. It takes less time to perform and results in less blood loss. Another key advantage is a lower risk of postoperative nutritional deficiency. This is because LSG does not bypass sites of nutrient absorp-tion. The duodenum and jejunum are left intact. As with other bariatric procedures, LSG must be followed by lifelong surveillance and nutrient support.

In the small number of studies that have reported longer-term outcomes, the percentage of excess weight lost 5 to 9 years following LSG is between 53% and 69%, depending on the study.74,75

Laparoscopic Adjustable Gastric Band

The laparoscopic adjustable gastric band (LAGB), also known as the “lap band,” surgery has been performed in the U.S. since the mid 1980s. The LAGB procedure uses an inflatable band cinched around the top of the

Figure 4. Laparoscopic adjustable gastric band restricts food intake by radically reducing “stomach” size and limiting outflow, thereby promoting early satiety. The band can be adjusted by infusing or withdrawing saline via a subcutaneous port. (Graphic Source: NIH Publication Number 00-4084. Copyright 1997-2013, A.D.A.M., Inc.)

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reduce risk of hip and nonvertebral fractures by 20% among individuals aged 65 and older.91,92

Supplementation is recommended following all types of bariatric surgery. Recommendations for prophylactic nutritional supplementation of post-bariatric patients were published in AACE/TOS/ASMBS Guidelines in 2008 and updated in 2013, as follows:9,62 • OTC multivitamin+ mineral preparation containing

thiamine, copper, and zinc • 1 tablet/day (LAGB) • 2 tablet/day (RYGB, LSG, BDP, BDP/DS)• Calcium citrate + vitamin D:1200 to 2000 mg/day

+ 400 to 800 IU/day • Folic acid: 400 mg/day in multivitamin (menstruat-

ing women)• Elemental iron: 40 to 65 mg/day • Vitamin K: 300 mg/day • Vitamin B12: ≥350 mg/day orally (or 1000 mg/

month intramuscularly, or 3000 mg every 6 month intramuscularly or 500 mg every week intranasally)

It is always preferable for nutritional needs to be met through food intake rather than dietary supplementa-tion. To this end, bariatric patients should be counseled on healthy eating practices by trained dieticians or oth-er qualified clinicians. However, even with nutritious and balanced diet, bariatric patients are unlikely to be able to maintain adequate levels of critical vitamins, minerals, and micronutrients.

In patients who have undergone malabsorptive RYGB or BDP/DS and BDP procedures, additional supple-mentation with Vitamin A and zinc may be needed to maintain normal levels. Additional supplementation of other nutrients may also be needed in patients with pre- or post-bariatric deficiencies.

Lifelong routine metabolic and nutritional monitoring is necessary to maintain the health of people following bariatric surgery. AACE/TOS/ASMBS guidelines for screening and supplementation of patients after the im-mediate postoperative period are summarized on the next page.

Bone Loss Following LSG and LAGB Procedures

Bariatric procedures that restrict intake as the primary mechanism to promote weight reduction avoid the se-vere nutrient deficiencies seen following malabsorptive procedures. In general, restrictive bariatric procedures result in less bone loss at all sites. Several small studies showed no change in BMC or BMD following gastric banding.82,83 Nonetheless, bone loss at the hip has been seen, although at a lesser degree than in malabsorptive procedures. One year following LAGB surgery, in a study of 37 premenopausal women, reported by Giusti, et. al., subjects lost 2.3% at the femoral neck and 2.1% at the trochanter.84 At two years postsurgery, the same group had lost 5.8% at the femoral neck and 6.5% at the trochanter.84

Several studies have shown evidence of negative bone remodeling as indicated by markers of bone resorp-tion for the first year following LAGB.84,85 A study by Giorno, et. al., observed the increase in bone turnover to resolve by 24 months.86

Compared to RYGB, LAGB surgery has less of an im-pact on vertebral bone. Multiple studies have reported either a slight increase or no change in BMD at the lumbar spine in the first two years following LAGB surgery, when the majority of the weight is lost.84,87,88

We currently have no data on long-term skeletal conse-quences of LAGB surgery. No fracture outcomes have been reported to date.

protecting Bone HealtH in Bariatric patientS

The caloric restriction and nutrient malabsorption that are central features of bariatric procedures induce suboptimal levels of calcium, vitamin D, minerals, fats, protein, and other nutrients normally absorbed in the small bowel.9,89,90

Protecting bone health of patients after bariatric sur-gery starts with correction of nutrient deficiencies. Without any other intervention, repletion of vitamins and minerals to normal levels can significantly improve skeletal status. Randomized placebo-controlled clinical trials have shown correction of vitamin D deficiency to

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Summary of Screening and Supplementation Recommendations for Patients following Bariatric Surgery (AACE/TOS/ASMBS)

Unless otherwise indicated, routine screening intervals listed below are annual in RYGB, LSG, and LAGB patients and biannual in BDP/DS and BDP patients.

25-hydroxyvitamin D Screening recommended every 6 to 12 months. If below 30 ng/ml, supplement with vitamin D3 or D2 as indicated by serum levels. May require oral doses of 50,000 IUs 1 to 3 times/day or week to reach sufficiency. Supplement thereafter 2,000 to 10,000 IU/day as needed to attain and maintain replete serum levels.

Calcium Routine screening recommended for all bariatric patients. Calcium from diet plus supplementation with oral calcium citrate 1,500 to 2,000 mg/day. Calcium citrate has been demonstrated to have better bioavailability, superior fractional uptake in bone, and efficacy in normalizing markers of bone turnover when compared to other commercial calcium supplements.93

Copper Screen with specific findings: in patients with anemia, neutropenia, myeloneuropathy, and/or impaired wound healing. Maintenance supplementation 2 mg/d as part of multivitamin/mineral preparation. (Zinc replacement can cause copper deficiency. Supplement 1 mg copper for every 8 to 15 mg zinc.)

Folate Supplement with folic acid (400 mg/day) as part of multivitamin-mineral supplement. Additional supplementation in women of childbearing years.

iPTH (intact parathyroid hormone)

Screening recommended every 6 to 12 months. Monitor along with Vitamin D.

Iron Routine screening recommended. Deficiency common in menstruating women and super-obese. Supplement as indicated, adding vitamin C or taking with orange juice to aid absorption.

Phosphorus Routine screening recommended. Oral supplementation of phosphate if level is low (1.5 to 2.5 mg/dl) usually due to vitamin D deficiency. RDA 1000 mg/day.

Prealbumin Routine screening recommended as indicator of overall nutritional status. Protein from diet with supplementation as needed.

Thiamine Screen with specific findings. Supplement as routine part of multivitamin-mineral preparation. Rare incidence of severe thiamine deficiency following RYGB.

Vitamin A Screening every 6 to 12 months recommended for patients who have had purely malabsorptive techniques: BDP, BDP/DS. Supplement as needed to reach adequate serum levels.

Vitamin B12 Baseline screening recommended for all bariatric patients. Yearly screening following RYGB and LSG. Maintenance supplementation 1000 mg/day.

Vitamin K Deficiency is common starting one year after surgery. Supplement with 300 μg/d.

Zinc Screening recommended following RYGB, BPD and BPD/DS. Deficiency common in BPD/DS patients starting one year after surgery. Supplement following BPD and BPD/DS.

Table 2. Summary of screening and supplementation recommendations for bariatric patients. (AACE/TOS/ASMBS Guidelines, 2008, 2013)9,62

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Diagnosing and Treating Osteoporosis in Bariatric Patients

Primary osteoporosis is a progressive degenerative bone disease found most frequently in women after menopause and men over 50. The majority of pa-tients (80%) who undergo bariatric surgery are young women with an average age of forty-two.94 Women this age are unlikely to have primary osteoporosis. When osteoporosis is suspected in a bariatric surgery patient, secondary disease – most likely related to nutritional insufficiencies – should be suspected first. Correction of nutrient-related deficits can lead to substantial improvements.

Women and men who have had bariatric surgery should have BMD measured by DXA. In younger patients, this provides a baseline measurement for future compari-son. In men over age 50 and postmenopausal women, it can be used to diagnose osteoporosis.

Accurate BMD measurement in very obese individu-als can be difficult. Patients over 450 pounds exceed the weight limit of contemporary DXA tables. Central DXA may not accurately reflect bone density in over-weight subjects. When tissue depth is over 25 cm and there is fat surrounding bone, DXA tends to overesti-mate BMD.95,96

Alternatives to spine and hip BMD measurements include peripheral DXA (pDXA) measurements of the forearm, heel, or finger; peripheral quantitative ultrasound (pQUS) of the heel, shin, and kneecap; and peripheral quantitative computed tomography (pQCT) of the forearm. The International Society for Clinical Densitometry (ISCD) recommends pDXA of the fore-arm for very obese individuals who cannot be mea-sured at the hip and spine.97

Although both T and Z scores are given on bone den-sity measurements, they are not always equally helpful in assessing a patient’s bone health. Z-scores are a bet-ter gauge of bone status in premenopausal women and men under age 50. The Z-score compares bone mineral density to the mean for individuals of the same age, race, and gender. A Z-score near 0 represents expected age-related bone loss. The ISCD position statement defines a Z-score of -2.0 or lower to be “below the ex-pected for age,” and a Z-score above -2.0 to be “within the expected range for age.” This cut-off point recom-mendation as well as the use of the Z-score clinically

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lateral spine radiograph.

Drug Treatment for Osteoporosis in Bariatric Patients

In a bariatric patient with DXA T-scores diagnostic of osteoporosis, all vitamin and mineral deficiencies must be aggressively treated before pharmacologic therapy can be started. Once normal serum values have been achieved, an antiresorptive or anabolic treatment agent can be considered.

Bisphosphonates are the most widely prescribed class of antiresorptives. AACE/TOS/ASMBS 2013 guide-lines recommend intravenous bisphosphonates rather than orally administered agents. This avoids inadequate absorption in the altered digestive tract and potential ulceration at sites of surgical anastomosis. Daily supple-mentation of vitamin D and calcium must be main-tained in any treatment plan.

Recommended intravenous dosages of antiresorptives include the bisphosphonates zoledronic acid, (5 mg once a year) and ibandronate (3 mg every 3 months) as well the RANK ligand inhibitor denosumab (60 mg ev-ery 6 months). The anabolic agent, teriparatide, is avail-able in subcutaneous dose of 20 mcg once a day.

Patients will need to be reassessed regularly to ensure calcium and vitamin D sufficiency. Repeat DXA mea-surement should be done every two years or starting at menopause in younger women. In between scans, measurement of biochemical markers of bone turn-over may be used to identify any escalation in bone resorption.

patient caSeS: preServing Bone HealtH following Bariatric Surgery In the following case studies, we will explore issues that arise in the clinical management of patients who have undergone bariatric surgery and subsequent weight loss.

Case 1: 45-Year-Old Woman who Had Roux-en-Y Gastric Bypass Surgery.

The first patient we will discuss is a 45-year-old African-American woman who underwent RYGB surgery one year ago. The patient reports having had

may change, as additional data become available.97 (Z-score assessment is also appropriate for growing children and adolescents, but is beyond the scope of this article.)

In older men and postmenopausal women, the T-score, which compares a patient’s BMD to healthy 30-year-old normative values, has been validated as a predictor of fracture risk.

In patients suspected of having a vertebral fracture, ei-ther because of acute back pain or height loss of 2" or greater, assessment is recommended by DXA and/or

Conflicting Research on Bariatric-Related Bone Loss Data on bone loss following bariatric surgery differs between prospective studies and retrospective/cross-sectional studies. Multiple prospective studies conducted over the past 20 years have documented significant bone loss following all types of bariatric surgery. In contrast, as reported in a recent literature review and analysis conducted by Scibora, et. al, the majority of cross-sectional and retrospective studies have observed either better or equal BMD following bariatric surgery. 98

The disparity between these findings illustrates the difficulty of teasing out variables that contribute to bone loss in individual weight-loss patients. All but one of the cross-sectional studies in Scibora’s analysis compare BMD in people after bariatric surgery with BMD in others of healthy or obese weight, matching them by age, gender, and menopausal status. In this paradigm, accelerated bone loss has not been documented.

A possible explanation, suggested by Scibora, et. al., may be the matching of people by post-surgical BMI, rather than pre-surgical BMI in the cross-sectional studies.98 Higher BMI is associated with higher BMD. Obese people have above-average BMD before surgery. It follows that in this cohort, average BMD following surgery signifies bone loss, even if still within normal parameters. Whether this bone loss increases fracture risk in the long term is as yet unknown and under study.

The predictive power of cross-sectional and retrospective studies is also limited by the study, including size, heterogeneity of subject groups, inconsistent lengths of follow-up, differing calcium and vitamin D intakes, and differences in methodology of biochemical and bone density measurements.

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• Intact PTH 128 pg/ml (10 to 72 pg/ml) • C reactive protein 2.5 mg/l (<3.0 mg/l)• Magnesium 1.9 mg/dl (1.5 to 2.3 mg/dl)• B12/cobalamin 150 ng/l (130 to 950 ng/l)• Thiamine 200 ng/l (150 to 255 ng/l)

What do these lab results suggest may be done to protect the patient’s bone health?The patient’s protein, vitamin D, and calcium levels are low. Her elevated PTH indicates secondary hyper-parathyroidism. Her nutrient insufficiencies can be ad-dressed through diet and supplementation.

What dietary interventions should be put in place to guard against bone loss?The clinician prescribes 50,000 IU vitamin D3 daily for seven consecutive days, then three times weekly. She is switched from calcium carbonate to chewable calcium citrate and instructed to take 600 mg twice daily and to increase her intake of calcium-rich foods. Her mul-tivitamin-mineral supplement is changed to a chewable form and doubled. Her B12 is on the low side, as is her albumin. Her prealbumin is frankly deficient, indicating inadequate protein intake. She is encouraged to con-sume an ounce or two of lean protein with each meal and snack. She is prescribed oral vitamin B12 at a dos-age of 1000 mg daily for six months. She will be reas-sessed at that time.

Should the patient have a bone density test?It would probably be a good idea. A DXA will pro-vide a baseline for future bone density measurements. Because this is her first DXA, we cannot use it to ascer-tain how much, if any, bone she has lost since weight-loss surgery. Because she is premenopausal, she is at low risk of primary osteoporosis. However, secondary causes of bone loss may have increased her risk for fracture.

She has a BMD scan by DXA.

DXA results:• Hip: 0.781 g/cm2; Z-score -1.9; T-score -2.2• Lumbar spine: 0.800 g/cm2; Z-score -1.71; T-score

-2.0

How should these DXA results be interpreted?In the patient’s age group, the race- and aged-matched Z-score is a better indicator of bone health and fracture risk than T-score (which is validated for postmenopaus-al women). A Z-score above -2.0 is considered within

weight problems since her teen years, she has lost and regained weight numerous times, each time ending up weighing more.

Prior to bariatric surgery, the patient met with a reg-istered dietician and was prescribed multivitamins as well as calcium and vitamin D supplements (1000 mg/500 IU).

At age 44, with hypertension, type 2 diabetes, and painful knees due to arthritis, she underwent RYGB surgery. Her starting weight was 240 pounds, with a BMI of 42. Now, one year later and 102 pounds lighter, her BMI is 24 and she no longer requires routine medications.

Medical history:• Height by stadiometer 5'6" (at baseline 5'4")• Weight 138 lbs (baseline 240 lbs)• RYGB bariatric surgery 1 year prior• Positive family history for osteoporosis• Personal history of nontraumatic wrist fracture as an

adult• Drinks fewer than 5 alcoholic beverages per week• Does not smoke• Takes 1000 mg calcium/day as calcium carbonate• Takes 600 IU vitamin D daily • Swims weekly for 1 hour • History of hypertension, now resolved, with no

drug treatment• Type 2 diabetes diagnosed prior to weight loss, now

under control with no medication

The patient presents for routine primary care follow-up.

What tests should the clinician use to assess the patient’s bone health?The patient should have blood work to identify any postoperative chemical or metabolic abnormalities. Her serum chemistry study results are as follows (nor-mal range shown in parentheses): • Complete blood count • Albumin 3.1 g/ml (4 to 6 g/dl)• Prealbumin 4 mg/dl (18 to 45 mg/dl)• Total calcium 8.2 mg/dl (8.6 to 10.5 mg/dl) • Ionized calcium 0.87 mmol/l (1.15 to 1.35

mmol/l)• Phosphorus 1.75 mg/dl (1.5 to 2.5 mg/dl)• 25-hydroxyvitamin D 12 ng/ml (30 to 80 ng/ml)

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• Height by stadiometer 5'3" (reported height at age 30: 5'6")

• Weight 275 lbs (weight at age 40: 420)• Natural menopause age 51• No DXA results on record• Malabsorptive bariatric surgery 20 year prior• Negative family history for osteoporosis• Positive history for nontraumatic ankle fracture as an

adult• Drinks 5-10 alcoholic beverages per week• Does not smoke• Takes daily multivitamin• Active lifestyle, but no other exercise• Hypertension, managed with drug treatment• Negative for type 2 diabetes

The patient presents with back pain. She has not con-tinued follow-up with her bariatric surgeon’s practice.

What tests should the clinician do to assess the patient’s bone health?There are many metabolic unknowns with this patient. Because she has had only minimal nutritional supple-mentation, she may have serious insufficiencies. Her height loss is suggestive of vertebral fracture, which could point to osteoporosis, but we do not know if her baseline height is accurate. Before going forward, a basic work up for malabsorption-related deficiencies should be done:• CBC, platelets • Electrolytes • Glucose • Iron studies, ferritin • Vitamin B12 (MMA, HCy optional) • Liver function (GGT optional) • Lipid profile • Albumin and prealbumin • RBC folate • Phosphorus• Vitamin A, E, and K• 25-hydroxyvitamin D • INR• Intact PTH • 24-hour urine calcium • Zinc• Selenium• Osteocalcin• Urine N-telopeptide

The patient’s lab results indicate elevated serum PTH

the range of normal.

Is the patient’s BMD measurement a cause for concern?It may be. Her hip Z-score is within the suggested range for normal. However, added to her history of low-impact fracture and positive family history for osteoporosis, she may be at increased risk for primary osteoporosis after menopause.

Should pharmacologic therapy to prevent bone loss be initiated at this time? Not at this time. Correction of the patient’s vitamin D deficiency, secondary hyperparathyroidism, low pro-tein, and low serum calcium should substantially im-prove her bone status.

What should be done to assess the efficacy of nutritional interventions?Follow-up labs eight weeks later are done. The results are normal albumin and B12, improved prealbumin, normal calcium, 25-hydroxyvitamin D (42 ng/ml), and PTH (71 pg/ml).

How should the patient be followed?This patient should have biochemical indices including prealbumin, CRP, calcium, 25-hydroxyvitamin D, and PTH checked every 3 to 4 months until her labs nor-malize, optimal vitamin D ≥40 ng/ml is achieved, and PTH is consistently suppressed. Once these goals have been met, the patient can safely be monitored every 6 to 12 months.

In addition, she will be assessed annually for signs and symptoms of osteoporosis such as height loss, postural changes, and back pain. She will have repeat DXA at menopause or sooner if symptoms warrant.

Case 2. 60-Year Woman 20 Years after Jejunoileal Bypass Surgery.

The second patient we will discuss is a Caucasian wom-an, age 60, who had jejunoileal bypass 20 years ago. Her starting weight was 420 pounds, with a BMI of 69, based on a reported 5'6" baseline height. She reports having lost 150 pounds in the two years following sur-gery. Since that time, she has regained 75. Her weight is now 275 pounds, with a BMI of 47, based on her current height measurement.

Medical history:

17

calcium citrate (chewable to improve absorption). Her target daily calcium intake is 1500 to 2000 mg.

She is not prescribed a phosphate supplement. Once she is vitamin D replete, her hypophosphatemia will likely not recur.

The patient is encouraged to increase her intake of dairy products for their protein and calcium benefits. If she cannot tolerate lactose, she is advised to try lactose-free milk and/or milk-only yogurt that contains no added milk sugars or solids. She is advised to increase her protein intake through many small high-protein snacks per day.

and significant deficiencies of calcium, phosphorus, protein, zinc, copper, and vitamins D, B12, A, and E:• Albumin 3.1 g/ml (4 to 6 g/dl)• Prealbumin 4 mg/dl (18 to 45 mg/dl)• Total calcium 7.8 mg/dl (8.6 to 10.5 mg/dl) • Ionized calcium 1.00 mmol/l (1.15 to 1.35)• 25-hydroxyvitamin D 10 ng/ml (30 to 80 ng/ml)• Intact PTH 130 pg/ml (10 to 72 pg/ml) • C reactive protein 0.3 mg/l (<1.0 mg/l)• Magnesium 1.9 mg/dl (1.5 to 2.3 mg/dl)• Zinc 0.30 mcg/ml (0.66 to 1.10 mcg/ml)• Vitamin E 4 µg/ml (5 to 20 µg/ml)• Vitamin A 28 µg/dl (30 to 95 µg/dl)• B12/cobalamin 100 ng/l (130 to 950 ng/l)• Thiamine 200 ng/l (150 to 255 ng/l) • Phosphorus 1.25 mg/dl (1.5 to 2.5 mg/dl)

Should this patient be evaluated for metabolic bone disease?Yes. Her lab work points to a high risk for osteoporosis, from both primary and secondary causes.

A bone density scan by DXA is ordered. In addition, she has a lateral spine radiograph to detect any verte-bral fractures.

DXA results:• Hip: 0.66 g/cm2; T-score -3.4• Lumbar spine: 0.69 g/cm2; T-score -3.1

Her lateral radiograph identifies vertebral compres-sion fractures at L2 and L4. Because the patient is past menopause, it is appropriate to use T-scores to evaluate her BMD. The patient is diagnosed with osteoporosis.

Should she be treated to prevent further bone loss? Yes. She will first need to have her nutrient-related ab-normalities corrected. In addition to supporting bone density, vitamin D and calcium repletion are necessary for optimized therapeutic effect.

The patient is prescribed 50,000 IUs oral vitamin D3 to be taken daily for two weeks, at which time she will be rechecked. Once her serum level reaches ≥30 ng/ml she will be switched to a maintenance dose of 50,000 three times weekly.

Her calcium deficiency is addressed through both diet and supplement. Working with a nutritionist, she is started on a high-calcium diet and supplemented with

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strength and balance. In individuals with osteoporosis or low bone density, falls are the leading cause of fragil-ity fracture.

Summary

There is no doubt that bariatric surgery saves lives that would be lost due to obesity-related diseases. However, it is not without its potential costs, which include severe nutrient depletion and the wide-ranging conse-quences of prolonged suboptimal nutrition. Bariatric surgery patients require meticulous life-long surveil-lance. Targeted nutritional support and vitamin-mineral supplementation dosed to achieve and maintain healthy serum levels can significantly improve bone health in bariatric patients. With awareness of potential risks, consistent monitoring, prophylactic nutrient supple-mentation, and appropriate pharmacologic interven-tion, clinicians can help patients protect their bone health after bariatric surgery and throughout their lives.

References1 Ogden CL, Carroll MD, Kit BK, et al. Prevalence of obesity in the United

States, 2009-2020. NCHS Data Brief. 2012;82:1-8. 2 Ogden CL, Carrol MD, Curtin LR, Flegal KM. Epidemiologic trends in

overweight and obesity. Endocrinology & Metabolism Clinics of North America. 2003;32:741-60.

3 Ogden CL, Carrol MD, Curtin LR, Lamb MM. Prevalence of High Body Mass Index in US Children and Adolescents, 2007-2008. JAMA. 2010;303:242-7.

4 Renehan AG, Tyson M, Egger M, Heller RF, Zwahlen M. Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospec-tive observational studies. Lancet. 2008; 371 (9612):569–78.

5 Romero-Corral A, Montori VM, Somers VK, et al. Association of body-weight with total mortality and with cardiovascular events in coronary artery disease: a systematic review of cohort studies. Lancet. 2006;368 (9536):666–78.

6 U.S. Department of Health and Human Services Office of the Surgeon General. Overweight and obesity: health consequences. Available at: http://www.surgeongeneral.gov/library/calls/obesity/fact_conse-quences.html. Accessed July 8, 2013.

7 American Society for Metabolic & Bariatric Surgery. (2009) ASMBS estimates are based on the Bariatric Outcomes Longitudinal Database (BOLD), American College of Surgeons Bariatric Surgery Center Net-work (ACS BSCN), the National Inpatient Sample data and the best esti-mation on the number of outpatient cases.

8 Maggard MA, Shugarman LR, Suttorp M., et al. Meta-analysis: surgical treatment of obesity. Ann Intern Med. 2005;142(7):547-559.

9 Mechanick JI, Youdim A, Jones DB, et. al. Clinical practice guidelines for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient--2013 update: cosponsored by American Associa-tion of Clinical Endocrinologists, The Obesity Society, and American So-ciety for Metabolic & Bariatric Surgery. Obesity (Silver Spring). 2013;21 Suppl 1:S1-27.

10 Maggard MA, Shugarman LR, Suttorp M, et. al. Meta-analysis: surgical treatment of overweight and obesity in adults: the evidence report. Obes Res. 1998;6(suppl 2):51S-209S.

11 Sjöström L, Narbro K, Sjöström D, et al. Effects of bariatric surgery on mortality in Swedish obese subjects. NEJM. 2007;357:741-52.

12 Buchwald H, Avidor Y, Braunwald E, et. al. Bariatric surgery: a systematic

She is also prescribed an OTC chewable multivitamin-mineral twice daily, 1000 µg oral vitamin B12, and supplemental vitamin A, E, and K.

What osteoporosis medication would be appropriate for this patient?Absorption of oral bisphosphonates may be compro-mised in patients who have undergone gastric bypass. Studies of other poorly absorbed drugs have shown diminished bioavailability following bariatric surgery; however, no data have been published specifically ad-dressing absorption of bisphsophonates.99 Intravenous agents such as yearly zoledronic acid, twice yearly de-nosumab, quarterly ibandronate, or daily teriparatide are potential non-oral options. Due to the higher cost of these options, it may be difficult to get insurer ap-proval without evidence that the less-expensive oral bisphosphonates do not work.

After considering her options, the patient agrees to try 35 mg once-weekly oral alendronate.

What is her follow-up plan?The clinician will repeat the patient’s biochemical panels every 6 to 12 months. Once she is on oral alen-dronate, she will be reassessed by DXA at one year. If her BMD is stable, she will be continued on the alen-dronate. If her BMD continues to decline, the patient’s medication options will be reconsidered.

She will then be followed with DXA every two years. In intervals between DXA scans, to confirm that the patient is not continuing to lose bone, the patient’s rate of bone turnover will be assessed using biochemical markers, such as urine N-telopeptide (NTX) or serum bone specific alkaline phosphatase. If evidence is found of elevated bone turnover, appropriate action can be taken.

What other strategies can help support this patient’s health and quality of life?The patient can be encouraged to engage in an exercise program of moderate intensity and to join a support group for patients who have undergone weight-loss surgery. Both measures have been shown to improve quality of life and increase the odds of maintaining weight reduction. An added benefit of exercise is that, in addition to supporting cardiovascular health and gly-cemic control, it reduces fall risk by improving muscle

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35 Compher CW, Badellino KO, Boullata JI. Vitamin D and the bariatric sur-gical patient: a review. Obes Surg. 2008;18(2):220–4.

36 Lin E, Armstrong-Moore D, Liang Z, Sweeney JF, Torres WE, Ziegler TR. Contribution of adipose tissue to plasma 25-hydroxyvitamin D concentra-tions during weight loss following gastric bypass surgery. Obesity (Silver Spring) 2011 Mar;19(3):588–94.

37 Sawaya RA, Jaffe J, Friedenberg L, Friedenberg FK. Vitamin, min-eral, and drug absorption following bariatric surgery. Curr Drug Meta. 2012;13(9):1345-55.

38 Signori C, Zalesin KC, Franklin B, Miller WL, McCullough PA. Effect of gastric bypass on vitamin D and secondary hyperparathyroidism. Obes Surg. 2010;20(7):949-52.

39 Carlin AM, Rao DS, Yager KM, Genaw JA, Parikh NJ, Szymanski W. Effect of gastric bypass surgery on vitamin D nutritional status. Surg Obes Relat Dis. 2006;2(6):638-42.

40 Sánchez-Hernández J, Ybarra J, Gich I, et. al. Effects of bariatric surgery on vitamin D status and secondary hyperparathyroidism: a prospective study. Obes Surg. 2005;15(10):1389-95.

41 Youssef Y, Richards WO, Sekher J, et. al. Risk of secondary hyperparathy-roidism after laparoscopic gastric bypass surgery in obese women, Surg Endosc. 2007;21(8):1393-6.

42 Ybarra J, Sánchez-Hernández J, Gich I, et. al. Unchanged hypovitaminosis D and secondary hyperparathyroidism in morbid obesity after bariat-ric surgery. Obes Surg. 2005 Mar;15(3):330-5.

43 Carlin AM, Rao DS, Meslemani AM, et al. Prevalence of vitamin D deple-tion among morbidly obese patients seeking gastric bypass surgery. Surg Obes Rel Dis. 2006; 2:98–103.

44 Tanaka S, Kuroda T, Saito M, Shiraki M. Overweight/obesity and under-weight are both risk factors for osteoporotic fractures at different sites in Japanese postmenopausal women. Osteoporos Int. 2013;24(1):69-76.

45 Compston JE, Watts NB, Chapurlat R, et. al.; GLOW Investigators. Obe-sity is not protective against fracture in postmenopausal women: GLOW. Am J Med. 2011;124(11):1043-50.

46 Ensrud KE, Fullman RL, Barrett-Connor E, et. al.; Osteoporotic Frac-tures in Men Study Research Group.Voluntary weight reduction in older men increases hip bone loss: the osteoporotic fractures in men study. J Clin Endocrinol Metab. 2005;90(4):1998-2004.

47 Prieto-Alhambra D, Premaor MO, Fina Avilés F, et. al. The association between fracture and obesity is site-dependent: a population-based study in postmenopausal women. J Bone Miner Res. 2012;27(2):294-300.

48 Tang X, Liu G, Kang J, et. al. Obesity and risk of hip fracture in adults: a meta-analysis of prospective cohort studies. PLoS One. 2013;8(4):e55077.

49 Ensrud KE, Ewing SK, Stone KL, et. al. Intentional and unintentional weight loss increases bone loss and hip fracture risk in older women. J Am Geriatr Soc. 2003;51(12):1740-7.

50 Ensrud KE, Fullman RL, Barrett-Connor E, et al. Voluntary weight reduc-tion in older men increases hip bone loss: the osteoporotic fractures in men study. J Clin Endocrinol Metab. 2005;90 (4):1998–2004.

51 Hannan MT, Felson DT, Dawson-Hughes B, et. al. 2000 Risk factors for longitudinal bone loss in elderly men and women: the Framingham Os-teoporosis Study. J Bone Miner Res. 15:710-20.

52 Knoke JD, Barrett-Connor E. Weight loss: a determinant of hip bone loss in older men and women: The Rancho Bernardo Study. Am J Epidemiol. 2003;158 (12):1132-8.

53 Shapses SA, Cifuentes M, Sherrell R, et al. Rate of weight loss influences calcium absorption. J Bone Miner Res. 2002; 17:S471.

54 Stein EM, Carrelli A, Young P, Bucovsky M, et. al. Bariatric surgery results in cortical bone loss. J Clin Endocrinol Metab. 2013 Feb;98(2):541-9.

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56 Brolin RE. Bariatric surgery and long-term control of morbid obesity. JAMA. 2002;288(22):2793-6.

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17 Consensus Development Conference Panel. NIH conference: Gastrointes-tinal surgery for severe obesity. Ann Intern Med. 1991;115:956-961.

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21 Arterburn DE, Bogart A, Sherwood NE, et. al. A multisite study of long-term remission and relapse of type 2 diabetes mellitus following gastric bypass. Obes Surg. 2013 Jan;23(1):93-102.

22 NHLBI Obesity Education Initiative Expert Panel on the Identification, Evaluation, and Treatment of Overweight and Obesity in Adults. Practi-cal Guide to the Identification, Evaluation, and Treatment of Overweight and Obesity in Adults. NIH Publication Number 00-4084 October 2000. Available at: http://www.nhlbi.nih.gov/guidelines/obesity/prctgd_c.pdf. Accessed July 13, 2013.

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24 Egberts K, Brown WA, Brennan L, et al. Does exercise improve weight loss after bariatric surgery? A systematic review. Obes Surg. 2012;22:335-41.

25 Song Z, Reinhardt K, Busdon M, et al. Association between support group attendance and weight loss after Roux-en-Y gastric bypass. Surg Obes Relat Dis. 2008;4:100-3.

26 Kaiser KA, Franks SF, Smith AB. Positive relationship between support group attendance and one-year postoperative weight loss in gastric band-ing patients. Surg Obes Relat Dis. 2011;7:89-93.

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28 Kelleher DC, Merrill CT, Cottrell LT, Nadler EP, Burd RS. Recent nation-al trends in the use of adolescent inpatient bariatric surgery: 2000 through 2009.JAMA Pediatr. 2013 Feb;167(2):126-32.

29 Censani M, Stein EM, Shane E, et. al. Vitamin D Deficiency Is Preva-lent in Morbidly Obese Adolescents Prior to Bariatric Surgery. ISRN Obes. 2013;May 28;2013. pii: 284516. 7 Pages.

30 Heaney RP, Dowell MS, Hale CA, Bendich A. Calcium absorption varies within the reference range for serum 25-hydroxyvitamin D. J Am Coll Nutr. 2003 Apr;22(2):142-6.

31 Lips P. Vitamin D deficiency and secondary hyperparathyroidism in the elderly: consequences for bone loss and fractures and therapeutic implica-tions. Endocr Rev. 2001 Aug;22(4):477-501.

32 Brouwer DA, van Beek J, Ferwerda H, et al. Rat adipose tissue rapidly ac-cumulates and slowly releases an orally-administered high vitamin D dose. Br J Nutr. 1998;79:527–32.

33 Gemmel K, Santry HP, Prachand VN, Alverdy JC. Vitamin D deficiency in preoperative bariatric surgery patients. Surg Obes Relat Dis. 2009;5:54–9.

34 Goldner WS, Stoner JA, Thompson J, et al. Prevalence of vitamin D insuf-ficiency and deficiency in morbidly obese patients: a comparison with non-obese controls. Obes Surg. 2008;18:145–50.

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2011;21:1458-68.59 Nelson DW, Blair KS, Martin MJ. Analysis of obesity-related outcomes

and bariatric failure rates with the duodenal switch vs gastric bypass for morbid obesity. Archives of Surgery. 2012; 147 (9): 847-54.

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79 Cobourn C, Chapman MA, Ali A, Amrhein J. Five-year weight loss experi-

NOF’s Support Group ProgramNOF sponsors osteoporosis support groups throughout the country. Patients can benefit in many ways from joining a support group:

• Learning more about the disease and treatment choices

• Receiving the most up-to-date information about osteoporosis

• Improving coping skills by learning how others handle the disease

• Exchanging information about community resources

• Helping identify healthcare providers who treat osteoporosis

• Improving mental and physical well-being• Finding hope and encouragement

Starting a Support GroupIf you are interested in starting your own support group, review and complete the NOF Support Group Application, available online at www.nof.org under Connect to Our Community

Support Group ResourcesNOF provides all support groups leaders with excellent resources including:

• Support group manual — A comprehensive guide to help you start, promote and conduct successful support group meetings.

• Free educational materials — NOF will provide brochures, information sheets, quarterly newsletters, PowerPoint presentations, posters and more.

• Networking opportunities — NOF will connect you with other support group leaders to help you network and exchange ideas.

• Topics and program ideas — NOF maintains a list of topics and program ideas.

• Referrals — NOF will direct all inquiries to join a support group in your area to you, helping you grow your membership.

For more information on joining a support group or to find a support group In your community, contact the National Osteoporosis Foundation at (202) 223-2226 or toll free at (800) 231-4222.

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EMBO Journal. 2006;25:1419-25.90 Keitel V, Kubitz R, Haussinger D. Endocrine and paracrine role of bile

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T, Dawson-Hughes B. Fracture prevention with vitamin D supple-mentation: a meta-analysis of randomized controlled trials. JAMA. 2005;293(18):2257-64.

92 Bischoff-Ferrari HA, Willett WC, Wong JB, et. al. Prevention of nonver-tebral fractures with oral vitamin D and dose dependency: a meta-analysis of randomized controlled trials. Arch Intern Med. 2009 Mar 23;169(6):551-61.

93 Sakhaee K, Bhuket T, Adams-Huet B, Rao DS. Meta-analysis of calcium bioavailability: a comparison of calcium citrate with calcium carbonate. Am J Ther. 1999;6:313–21.

94 Maggard M, Li Z, Yermilov I, et al. Bariatric Surgery in Women of Repro-ductive Age: Special Concerns for Pregnancy. Rockville (MD): Agency for Healthcare Research and Quality (US); 2008 Nov. (Evidence Reports/Technology Assessments, No. 169.) 1, Introduction. Available from: http://www.ncbi.nlm.nih.gov/books/NBK38563/. Accessed July 23, 2013.

95 Bolotin HH, Sievänen H, Grashuis JL. Patient-specific DXA bone mineral density inaccuracies: quantitative effects of nonuniform extraosseous fat distributions. J Bone Miner Res. 2003 Jun;18(6):1020-7.

96 Binkley N, Krueger D, Vallarta-Ast N. An overlying fat panniculus affects femur bone mass measurement. J Clin Densitom. 2003;6:199 –204.

97 The International Society for Clinical Densitometry (ISCD) - 2007 ISCD Official Positions. http://www.iscd.org/official-positions/official-posi-tions/ Accessed June 12, 2013.

98 Scibora LM, Ikramuddin S, Buchwald H, Petit MA. Examining the link between bariatric surgery, bone loss, and osteoporosis: a review of bone density studies. Obes Surg. 2012;22(4):654-67.

99 Padwal R, Brocks D, Sharma AM. A systematic review of drug absorp-tion following bariatric surgery and its theoretical implications. Obes Rev. 2010;11(1):41-50.

ence of outpatients receiving laparoscopic adjustable gastric band surgery. Obes Surg. 2013;23(7):903-10.

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81 Suter M, Calmes JM, Paroz A, Giusti V. A 10-year experience with lapa-roscopic gastric banding for morbid obesity: high long-term complication and failure rates. Obes Surg. 2006;16(7):829-35.

82 von Mach MA, Stoeckli R, Bilz S, Kraenzlin M, Langer I, Keller U. Changes in bone mineral content after surgical treatment of morbid obe-sity. Metabolism. 2004;53(7):918-21.

83 Strauss BJ, Marks SJ, Growcott JP, et. al. Body composition changes fol-lowing laparoscopic gastric banding for morbid obesity. Acta Diabetol. 2003;40 Suppl 1:S266-9.

84 Giusti V, Gasteyger C, Suter M, et. al. Gastric banding induces nega-tive bone remodeling in the absence of secondary hyperparathyroidism: potential role of serum C telopeptides for follow-up. Int J Obes (Lond). 2005;29(12):1429-35.

85 Pugnale N, Giusti V, Suter M, et.al.Bone metabolism and risk of second-ary hyperparathyroidism 12 months after gastric banding in obese pre-menopausal women. Int J Obes Relat Metab Disord. 2003;27(1):110-6.

86 DiGiorgi M, Daud A, Inabnet WB, et. al. Markers of bone and calcium metabolism following gastric bypass and laparoscopic adjustable gastric banding. Obes Surg. 2008;18(9):1144-8.

87 Cundy T, Evans MC, Kay RG, et al. Effects of vertical-banded gastro-plasty on bone and mineral metabolism in obese patients. Br J Surg. 1996;83(10):1468–72.

88 Guney E, Kisakol G, Ozgen G, et al. Effect of weight loss on bone metab-olism: comparison of vertical banded gastroplasty and medical interven-tion. Obes Surg. 2003;13(3):383–8.

89 Houten SM, Watanabe M, Auwerx J. Endocrine functions of bile acids. The

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Osteoporosis InternationalOsteoporosis International is the leading scientific journal for clinical research in osteoporosis and related bone diseases. Published monthly, the journal is an international, multi-disciplinary joint initiative of NOF and the International Osteoporosis Foundation.

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