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Obesity Surgery

, Volume 29, Issue 4, pp 1327–1342 | Cite as

Fractures in Adults After Weight Loss from Bariatric Surgery and Weight Management Programs for Obesity: Systematic Review and Meta-analysis

  • Andrew D. Ablett
  • Bonnie R. Boyle
  • Alison AvenellEmail author
Open Access
Original Contributions

Abstract

Background

Weight loss interventions for obesity, such as bariatric surgery, are associated with reductions in bone mineral density and may increase the risk of fractures. We undertook a systematic review and meta-analysis of bariatric surgery and lifestyle weight management programs (WMPs) with fracture outcomes.

Methods

We searched MEDLINE, Embase, the Cochrane Central Register of Controlled Trials from 1966 to 2018, and our trial registry of WMP randomized controlled trials (RCTs). We included RCTs, non-randomized trials, and observational studies of bariatric surgery, and RCTs of WMPs. Studies had follow-up ≥ 12 months, mean group body mass index ≥ 30 kg/m2. The primary outcome measure was incidence of any type of fracture in participants, and the secondary outcome was weight change. We used random effects meta-analysis for trial data.

Results

Fifteen studies were included. Three small trials provided short-term evidence of the association between bariatric surgery and participants with any fracture (365 participants; RR 0.82; 95% CI 0.29 to 2.35). Four out of six observational studies of bariatric surgery demonstrated significantly increased fracture risk. Six RCTs of WMPs with 6214 participants, the longest follow-up 11.3 years, showed no clear effect on any type of fracture (RR 1.04; 95% CI 0.91 to 1.18), although authors of the largest RCT reported an increased risk of frailty fracture by their definition (RR 1.40; 95% CI 1.04 to 1.90).

Conclusion

Bariatric surgery appears to increase the risk of any fracture; however, longer-term trial data are needed. The effect of lifestyle WMPs on the risk of any fracture is currently unclear.

Keywords

Fractures Bariatric surgery Obesity Weight loss 

Introduction

While bariatric surgery for adults with obesity is effective for weight loss and reduces many obesity-related diseases, reports on long-term complications beyond mortality are currently limited [1]. Risk of malnutrition and malabsorption of fat-soluble vitamins including vitamin D, as well as increased bone turnover and reduced bone mineral density (BMD) after surgery [2, 3], could increase the risk of fracture. Lifestyle weight management programs (WMPs), consisting of a variety of diets with or without exercise advice, are reported to be associated with a small reduction in total hip but not lumbar spine BMD measurements in observational data [4].

We undertook a systematic review of fracture outcome data from studies of bariatric surgery and lifestyle WMPs. Our aim was to examine whether weight loss increased the risk of participants sustaining any fracture, compared to adults with obesity who did not undergo bariatric surgery or undertake WMPs.

Materials and Methods

We used a pre-specified protocol and followed PRISMA (Preferred Reporting Items for Systematic reviews and Meta-analyses) guidelines.

Selection Criteria

Bariatric Surgery Studies

There are presently few randomized controlled trials (RCTs) reporting fracture data post-bariatric surgery compared to no surgery; therefore, we included non-randomized controlled trials and observational studies in adults (≥ 18 years), with mean pre-surgery group body mass index (BMI) ≥ 30 kg/m2. Studies had a minimum follow-up ≥ 1 year.

Lifestyle Weight Management Programs

We included RCTs of WMPs of reducing diets with or without physical activity advice and/or programs to attend, versus usual care/no intervention. Studies had minimum follow-up ≥ 1 year, mean baseline group BMI ≥ 30 kg/m2, and mean group age ≥ 18 years.

Outcomes

Our primary outcome was participants with any fracture and our secondary outcome was weight change.

Search Strategy

We searched full texts of trial reports in our database of long-term RCTs of lifestyle WMPs for adults, compiled from MEDLINE, Embase, and the Cochrane Central Register of Controlled Trials, from 1966 to 2016 [5, 6]. We performed an updated search from 2016 to July 2018 for WMP RCTs. Details of the search strategy (including for bariatric surgery) in MEDLINE can be found in Appendix A, which was adapted for other databases. We contacted the authors of eight WMP and bariatric surgery RCTs with bone mineral density data to request any additional unpublished fracture data.

Data Analysis

AA and ADA/BRB independently confirmed study eligibility. ADA extracted data, which were checked by AA. AA and ADA independently assessed quality of RCTs and non-randomized trials using the Cochrane risk of bias tool [7] and for observational studies using the Newcastle-Ottawa Quality Assessment Scale [8]. All differences were resolved by discussion.

Owing to limited data, we combined data from RCTs and non-randomized controlled trials of bariatric surgery in meta-analyses, using Review Manager Software version 5.3. Risk ratios (RR) and 95% confidence intervals (95% CI) were calculated for dichotomous outcomes. Heterogeneity was assessed using the I2 test (I2 > 50% was considered significant heterogeneity) in conjunction with the chi-squared test. Random effects meta-analysis was used to pool outcome data, due to known heterogeneity in weight loss interventions. We estimated mean differences (MD) and 95% CI for weight data, giving preference to follow-up data for all participants or data taking account of drop-outs (preferentially baseline observation carried forward) if these were provided. Missing standard deviations (SD) were derived using previously described methods [5].

Data from observational studies of bariatric surgery were not combined, but are discussed in a narrative review.

No external funding was provided. No ethical approval was required.

Results

We screened 1174 full-text trial reports and 4153 titles and abstracts, as outlined in Fig. 1.
Fig. 1

Study selection

Quality Assessment

Bariatric Surgery Trials

Appendix Table 3 provides our full risk of bias assessments for the three trials, two of which were RCTs. None were judged to be at low risk of bias for outcome assessment. We judged that there was a high risk of bias for incomplete outcome data due to high drop-out rates [9, 10], and the non-randomized controlled trial was potentially at a high risk of other bias due to the study being funded by industry [11].

All six observational studies of surgery (Appendix Table 4) were judged to be moderately representative of the average obese person in their communities. We judged the comparability of all of the studies in terms of controlling for factors associated with fractures to be acceptable; however, two of the studies failed to report numerical BMI data [12, 13].

Lifestyle Intervention Studies

Three of the RCTs (see Appendix Table 3) were judged to be at low risk of bias for outcome assessment [14, 15, 16]. Three trials were also at low risk for both incomplete outcome data and selective reporting [15, 16, 17]. Two trials were judged to be potentially at high risk of bias due to premature termination [15] and industry sponsorship [18].

Study Characteristics

Bariatric Surgery Trials

Two RCTs (Table 1) were from the USA [9, 10] and one non-randomized controlled trial was from Norway [11], involving a total of 365 adults, mostly women (see Table 1). Roux-en-Y gastric bypass (RYGB) was used in all three trials, laparoscopic adjustable gastric banding (LAGB) in one [9] and laparoscopic sleeve gastrectomy (LSG) in one [10]. Both of the RCTs included participants with type 2 diabetes and associated comorbidities, and 27% of participants in the non-randomized trial had type 2 diabetes. At baseline, prior to bariatric surgical intervention, mean group ages ranged from 42.8–50.0 years and mean group BMI ranged from 35.3–46.7 kg/m2. The maximum follow-up was only 2 years.
Table 1

Summary of bariatric surgery and weight loss trials

Author year location

 

Number

Intervention

Diet; calories kcal/day

Exercise minutes per/week + intensity

% drop-out at the end of study

Follow-up months

Comorbidities/medications

Age (years)

mean (SD)

% female

% ethnicity

BMI kg/m2 mean (SD)

Weight change (kg) (SD)

Fractures

Courcoulas et al. 2014

Pittsburgh, USA [9]

Control

23

Lifestyle weight loss intervention

1200–1800

Based on meal plans

300 min of moderate physical activity

26.1

12

Type 2 diabetes

Hypertension

48.3 (4.7)

82.6

Black = 17.4

35.7 (3.3)

− 10.3 (11.8)

0

Intervention

46

Roux-en-Y gastric bypass surgery

Laparoscopic adjustable gastric banding

NR

Exercise a min of 3–4 times per week and to focus on weight-bearing, aerobic activity

17.4

12

46.8 (7.0)

80.5

Black = 23.5

35.5 (3.0)

− 22.2 (10.3)

1

Daumit et al. 2013

Baltimore, USA [16]

Control

147

Group health classes quarterly with topics not related to weight

NR

3.4

18

Schizophrenia

Schizo-affective disorder

Bipolar disorder

Major depression

44.1 (11.0)

49.0

White = 81.0

Black = 59.0

Other = 7.0

36.5 (7.3)

− 0.2 (9.1)

4

Intervention

144

Group and individual weight loss counseling and group physical activity classes

Moderate caloric restriction based on DASH diet

≥ 150 min/week of moderate physical activity

4.9

18

46.6 (11.5)

51.4

White = 82.0

Black = 52.0

Other = 10.0

36.0 (7.2)

− 3.4 (7.8)

2

Ditschuneit et al. 1999

Ulm, Germany [18]

Control

50

Conventional foods

1200–1500

Balanced diet

38.0

27

Absence of endocrine or psychiatric disease

46.6 (11.2)

82.0

33.8 (3.2)

− 5.9 (5)

1

Intervention

50

2 meal replacements

1200–1500

36.0

27

44.8 (9.7)

76.0

32.4 (4.2)

− 11.3 (6.8)

1

Hofso et al. 2010

Tonsberg, Norway [11]

Control

66

Lifestyle modification

NR

4.5

12

Type 2 diabetes

Hypertension

Metabolic syndrome

Albuminuria

Left ventricular hypertrophy

Coronary heart disease

47.0 (11.0)

66.7

White = 92.4

43.3 (5.0)

− 10.7 (12.0)

1

Intervention

80

Roux-en-Y gastric bypass surgery

788–908

3–6 weeks preceding surgery

5.0

12

42.8 (10.5)

66.3

White = 92.5

46.7 (5.7)

− 41.3 (13.1)

1

Look AHEAD

(Johnson et al. 2017)

16 clinical sites across the USA [15]

Control

2575

Diabetes support and education

NR

11.7

115

Diabetes

58.9 (6.9)

59.7

Black = 15.7

White = 63.3

Hispanic = 13.2

Other = 7.8

36.0 (5.8)

− 4.8 (7.3)

358

Intervention

2570

Calorie restriction and exercise

1200–1800

Based on guidelines of the ADA and National Cholesterol Education program

≥ 175 min of moderate

physical activity

10.1

115

58.6 (6.8)

59.4

Black = 15.6

White = 63.1

Hispanic = 13.2

Other = 8.1

35.9 (6.0)

− 7.4 (8)

373

Ma et al. 2013

California, USA [14]

Control

81

Usual care

NR

18.5

15

Pre-diabetes mellitus or metabolic syndrome

52.5 (10.9)

45.7

White = 77.8

Asian/Pacific Islander = 17.3

Latino/Hispanic = 4.9

32.4 (6.3)

− 2.4 (8.1)

0

Intervention

160

Coach lead exercise and self-directed exercise

Group Lifestyle Balance Program™

Lose 7% of weight through healthy eating

≥ 150 min of moderate physical activities

19.5

15

53.2 (10.5)

46.9

White = 78.1

Asian/Pacific Islander = 16.9

Latino/Hispanic = 3.8

31.7 (4.9)

− 5.4 (8.1)

3

Ma et al. 2015

California, USA [19]

Control

165

Usual care

NR

10.9

12

Asthma

47.7 (12.1)

70.9

White = 49.7

Black = 19.4

Asian/Pacific Islander = 8.5

Hispanic/Latino = 20.6

37.6 (5.7)

− 2.1 (10.3)

0

Intervention

165

Weight loss intervention

500–1000 kcal/d reductions, but daily total calories no less than 1200 kcal

≥ 150 min moderate physical activity

13.9

12

47.5 (12.6)

70.3

White = 49.7

Black = 20.6

Asian/Pacific Islander = 7.9

Hispanic/Latino = 20.0

37.4 (6.0)

− 4.0 (10.3)

1

Maghrabi et al. 2015

Ohio, USA [10]

Control

50

Intensive medical therapy for diabetes

NR

15.0

24

Diabetes

Dyslipidemia Hypertension

50.0 (8.4)

47.1

Caucasian = 82.4

35.8 (3.0)

− 0.5 (4.1)

4

Intervention

100

RYGB plus intensive medical therapy and laparoscopic sleeve gastrectomy plus intensive medical therapy

NR

7.5

24

47.7 (9.7)

64.3

Caucasian = 67.4

36.3 (2.9)

− 23.9 (9.54)

6

Villareal et al. 2011

St Louis, USA [17]

Control

53

Usual care and exercise

1500 mg/day calcium and 1000 ID/day of vitamin D

270 min

65% of their peak heart rate

15.1

12

Chronic disease

69.5 (4.0)

64.5

White = 81

Black = 15

Other = 4

37.1 (5.0)

− 0.3 (3.52)

3

Intervention

54

Weight loss and weight loss with exercise

Supplements as per controls. Energy deficit of 500 to 750 kcal/day. 1 g of high-quality protein/kg weight

270 min

65% of their peak heart rate

11.1

12

70.0 (4.0)

61.0

White = 88.5

Black = 11.5

Other = 0

37.0 (4.9)

− 9.1 (4.6)

0

Bariatric Surgery Observational Studies

Table 2 provides details of the observational studies of bariatric surgery. There were 1872 fractures in 59,930 patients who underwent bariatric surgery versus 5408 fractures in 223,110 control patients, from the UK, Taiwan, and North America in one case-control study [13] and five cohort studies [7, 12, 20, 21, 22, 23]. Each of the studies included patients undergoing a variety of restrictive and malabsorptive procedures, with the exception of one study of gastric bypass surgery only [20]. Trial participants had a wide range of comorbidities and were predominantly female. Where reported, group mean BMI was ≥ 40 kg/m2 and group mean age < 50 years before surgery.
Table 2

Summary of bariatric surgery cohort and case-control studies by characteristics and fracture results

Author, year

Location

 

Number

Intervention

Follow-up months

Comorbidities/medications

Age (years)

mean (SD)

% female

BMI (kg/m2)

mean (SD)

Fractures

Results (95% confidence interval)

Axelsson et al. 2018

Sweden [20]

Control

38,971

Usual Care

37.2 (median)

Comprehensive list of comorbidities, including the following:

Diabetes

Thyroid diseases

Malnutrition

Bone diseases

Liver disease

Renal diseases

Bisphosphonates

Hormone replacement

41.0 (11.2)

75.0

NA

774

Hazard ratio-

Reference category

Bariatric surgery

38,971

A variety of bariatric surgical interventions

37.2 (median)

40.9 (11.2)

76.4

42.4 (5.5)

1019

Adjusted hazard ratio for any fracture

Patients with diabetes 1.26 (1.05–1.53)

Patients without diabetes 1.32 (1.18–1.47)

Adjusted for propensity score, age, sex, weight (only for patients with diabetes), height (only for patients with diabetes), rheumatoid arthritis, alcohol-related diseases, fracture-free time, any previous fracture, previous hip fracture, previous vertebral fracture, previous number of fractures, previous fall injury without fracture, previous osteoporosis, previous secondary osteoporosis, previous glucocorticoids (≥ 5 mg of prednisolone equivalents per day more than 3 months), previous calcium and vitamin D, Charlson comorbidity index

Douglas et al. 2015

UK [21]

Control

3882

Usual care

36 (median)

T2DM, hypertension, coronary heart disease, cerebrovascular disease, peripheral vascular disease, other atheroma, smoking status, alcohol consumption, and use of insulin, OADs, and statins

45 (11)

81.6

42.1 (6.5)

32

Hazard ratio-

Reference category

Bariatric surgery

3882

Gastric band, gastric bypass or sleeve gastrectomy

36 (median)

45 (11)

80.5

44.7 (8.8)

39

Hazard ratio

Any fracture 1.26 (0.79–2.01)

All patients in the bariatric surgery group were propensity matched with the non-surgery patients with the closest propensity score when considering the following factors: age (within 2.5 years), sex, general practice, and presence in the CPRD on the date bariatric surgery was recorded

Lalmohamed et al. 2012

UK [22]

Control

10,442

Usual care

28 (mean)

Rheumatoid arthritis

Cerebrovascular disease

Smoking

44.9 (11.2)

85.3

40.8 (6.4)

207

Relative risk-

Reference category

Bariatric surgery

2079

A variety of bariatric surgical interventions

26 (mean)

44.6 (11.1)

83.9

43.2 (7.2)

38

Adjusted relative risk for any fracture

0.89 (0.60–1.33)

Adjusted for age, sex, and most recent record of body mass index before the index date; a history of fracture, inflammatory bowel disease, and cerebrovascular disease ever before; a history of falls in the previous 6–12 months; and use of glucocorticoids, calcium or vitamin D supplements, anti-obesity drugs, antihypertensive drugs, loop diuretics, organic nitrates, antidepressants, anxiolytics or hypnotics, bisphosphonates, opioids (tramadol or stronger), and proton pump inhibitors in the previous 6 months

Lu et al. 2015

Taiwan [12]

Control

5027

Usual care

59 (mean)

Diabetes

Hypertension

Hyperlipidemia

31.9 (9.9)

63.7

374

Adjusted hazard ratio-

Reference category

Bariatric surgery

2064

A variety of bariatric surgical interventions

57 (mean)

31.8 (9.2)

64.4

183

Adjusted hazard ratio for any fracture

1.21 (1.01–1.44)

Adjusted for duration of follow-up, material and social deprivation, area of residence, history of fractures (analysis for period after index date only), and number of comorbidities in the previous 5 years

Nakamura et al. 2014

Minnesota, USA [23]

Control

Standardized Incidence Ratio-

Reference category

Bariatric surgery

258

A variety of bariatric surgical interventions

107 (mean)

43.6 (9.9)

82.2

49.0 (8.4)

79

Standardized incidence ratio for any fracture

2.3 (1.8–2.8)

Expected numbers were derived by applying age and sex-specific fracture incidence rates in the general population of this community to the age specific person-years of follow-up

Rousseau et al. 2016

Quebec, Canada [13]

Control

126,760

Non-obese

53 (mean)

Cardiovascular disease

Hypertension

Chronic pulmonary disease

Diabetes

Hypothyroidism

Renal failure

Depression

Osteoporosis

42.6 (11)

72.3

3008

Adjusted relative risk-

Reference category

Control

38,028

Obese without bariatric surgical intervention

42.7 (11)

1013

Adjusted relative risk-

1.04 (0.96 to 1.12)

Adjusting for duration of follow-up, social deprivation, area of residence, history of fractures (analysis for period after index date only), and number of comorbidities in the previous 5 years, using multivariate conditional Poisson regression model

Bariatric surgery group

12,676

A variety of bariatric surgical interventions

42.6 (11)

514

Adjusted relative risk-

1.44 (1.29 to 1.59)

NA not available

Lifestyle WMP RCTs

Table 1 provides details of the six WMP RCTs involving 6214 adult participants [14, 15, 16, 17, 18, 19]. The Look AHEAD trial [15] was the largest study by far, with 5145 participants with type 2 diabetes followed for 11.3 years.

Five RCTs provided both diet and exercise advice (≥ 150 min of moderate physical activity per week) [14, 15, 16, 17, 19] and one diet advice only [18]. Three trials [15, 16, 17] provided exercise programs for participants to attend. Two RCTs prescribed a calorie restriction of 1200–1800 kcal/day, which lasted between 27 and 115 months [15, 18]; two RCTs a calorie deficit of 500–1000 kcal/day [17, 19]; and two RCTs were unclear as to the calorie content prescribed [14, 16].

All six trials recruited participants with pre-existing comorbidities, with one trial enrolling participants with uncontrolled asthma where 32.1% of patients reported systemic corticosteroid use [19]. Five RCTs were conducted in the USA [14, 15, 16, 17, 19] and one in Germany [18]. Two trials at baseline had group mean BMI ≤ 35 kg/m2 [14, 18]. The studies recruited predominantly middle-aged adults, with the exception of Villareal and colleagues who recruited older adults (mean group age 69–70 years) [17]. Follow-up was usually ≤ 2 years, with the exception of the Look AHEAD trial with follow-up of 11.3 years [15]. The mean drop-out rate ranged from 3.4 to 38.0%, with the highest drop-out rate reported in the trial from Ditschuneit and colleagues [18].

Data Analyses

Appendix Table 5 provides details of the fractures reported and definitions of osteoporotic or frailty fractures, as defined by the investigators.

Bariatric Surgery RCTs

For our primary outcome, the results of our meta-analysis of trials revealed no significant association between bariatric surgery and participants developing any fracture (n = 3 trials; 13 events; RR 0.82; 95% CI 0.29 to 2.35; I2 = 0%) (Fig. 2). For our secondary outcome, bariatric surgery led to marked weight loss, with high heterogeneity between studies (n = 3 trials; MD − 22.2 kg; 95% CI − 31.6 to − 12.8; I2 = 93%) (Fig. 3).
Fig. 2

Meta-analysis of weight loss intervention and incidence of fractures

Fig. 3

Meta-analysis of weight loss intervention and sustained weight loss

Bariatric Surgery Observational Studies

Four out of the six observational studies reported a statistically significant association between bariatric surgery and an increased likelihood of fracture (Table 2). The studies which reported an association between bariatric surgery and fracture incidence had longer periods of observation than the 3 years follow-up of the studies which reported no association. All studies adjusted for risk factors associated with fractures, such as fracture history, comorbidities, and age. However, Lalmohamed and colleagues, who observed no association between bariatric surgery and fracture, adjusted for a broader range of confounders, such as inflammatory bowel disease, glucocorticoids, proton pump inhibitors, and calcium and vitamin D supplementation [22].

Axelsson and colleagues [20] reported an increased risk of osteoporotic and hip fractures post-bariatric surgery. Lu and colleagues [12] had fewer events and did not find a statistically significant increase in osteoporotic or hip fractures. The increased risk post-surgery in the study by Rousseau and colleagues appeared to mainly relate to biliopancreatic diversion [13], which is rarely used today. Nakamura and colleagues reported an increased risk of fractures at traditional osteoporotic sites compared to community controls, matched for age and sex but not BMI [23].

Lifestyle WMP RCTs

In the lifestyle WMP RCTs, our meta-analysis showed no significant association between WMPs and participants developing any fracture (n = 6 trials; 746 events; RR 1.04; 95% CI 0.91 to 1.19; I2 = 0%) (Fig. 2). However, the largest trial, with follow-up of 5145 participants with diabetes, reported an increased risk of frailty fractures, a composite of hip, pelvis, upper arm, and shoulder fractures (hazard ratio 1.39; 95% CI 1.02 to 1.89). Weight loss at final follow-up showed high heterogeneity (n = 6 trials; MD − 4.15; 95% CI − 6.41 to −1.89; I2 = 92%).

Discussion

We found that bariatric surgery, predominantly malabsorptive in nature [12, 20], was associated with an increased risk of fracture compared to people of similar starting weight who did not undergo surgery. However, it is unclear whether the risk of fracture for adults post-bariatric surgery at their lower weight exceeds people of similar weight in the general population. Lifestyle WMPs were not associated with an increased risk of any fracture. However, there was some evidence from the Look AHEAD trial [15] to suggest that the risk of frailty fractures might be increased, but this trial did not report vertebral fractures and only around half of frailty fractures appeared to be related to low trauma. In the Look AHEAD trial, frailty fractures related to a composite of the first occurrence of a hip, upper arm, or shoulder fracture [15].

Weight loss programs, with or without bariatric surgery, are generally associated with advice to increase physical activity with or without exercise programs to attend. Thus, the effects of weight reduction on fracture risk cannot be separated in our studies from the possibility that a sudden increase in physical activity alone may have resulted in an increased propensity for injury.

There have been a number of systematic reviews and meta-analyses reporting on the association between bariatric surgery, particularly malabsorptive surgery, and significant BMD loss at the hip with less consistent results for the lumbar spine [2, 24, 25, 26]. However, the studies were sometimes without comparator groups and are difficult to interpret due to imaging limitations in severe obesity [27]. In a meta-analysis of five cohort studies and one RCT, Zhang and colleagues reported that bariatric surgery was associated with fractures at non-vertebral sites, especially upper limb fractures [28]. In contrast, in our meta-analysis of trials alone, the fractures reported were predominantly lower limb fractures such as tarsal and metatarsal fractures, but also included phalangeal fractures, suggesting short-term fractures secondary to physical activity [9, 10, 11]. Lu and colleagues in particular reported an increased risk of foot fractures, along with other sites not normally associated with osteoporosis [12].

The potential mechanisms underlying reductions in bone density and strength from weight loss which may precipitate bone fracture include mechanical, hormonal changes, and malabsorptive factors [27]. The reduction in force placed upon bones due to weight loss leads to higher levels of sclerostin, which inhibits osteoblastic activity and bone formation [27], while markers of bone turnover are considerably increased [4, 27]. Furthermore, estrogen and androgen status may decline particularly in postmenopausal women after bariatric surgery [29]. Bariatric procedures such as Roux-en-Y may lead to malabsorption of micronutrients required to maintain BMD [30]. Malabsorption of micronutrients including vitamin D, protein, and calcium, particularly after certain bypass procedures, may therefore require supplementation, e.g., vitamin D supplementation, to prevent secondary hyperparathyroidism [31]. Despite recommendations for patients post-bariatric surgery to take additional nutrient supplementation [31, 32], adherence is poor, e.g., vitamin D supplementation has been reported to be as low as 33% at 1 year [33], with factors such as male sex and working full-time associated with poor concordance [34]. BMD loss due to these factors, when additionally compounded by a sudden rise in physical activity in a previously sedentary adult, may place the bone under increased stress while also increasing the opportunities for the bone to fracture.

We attempted to identify all studies of WMPs and surgical RCTs which reported fractures, including contacting authors who had published BMD data to seek additional fracture data. However, the fracture data in the trials were often only reported as adverse events, and it is likely that fracture outcome data in other trials are unreported in the literature. Trials were often underpowered with short follow-up periods, such that it would be unlikely for changes in BMD to manifest as fractures.

In order for trials to meaningfully assess the long-term risk of fractures in bariatric patients, results from observational studies suggest that it is imperative that follow-up periods are sufficiently long [12, 13, 23], for example, Nakamura and colleagues reported that the median time to first fracture was 13 years [23]. It is important to acknowledge the difficulty maintaining prolonged follow-up in this patient group, but routine data collection through health records would allow evaluation. In a nationwide cohort study of 16,620 patients, Thereaux and colleagues observed that follow-up rates at 1 year and 5 years decreased from 87.1 to 29.6% [33]. Factors such as male sex and younger age were predictors of poor 5-year follow-up [33].

There is growing evidence to suggest that very large weight losses produced by bariatric surgery are associated with an increased risk of fracture. High rates of loss to follow-up in this patient group may hinder accurate evaluation; nevertheless, there remains a concerning lack of reporting on this adverse outcome. We suggest that bariatric surgery studies habitually report the presence (or absence) of fractures during long-term follow-up, including information on patient characteristics and types of fractures.

Notes

Acknowledgements

We thank Cynthia Fraser, Health Services Research Unit, University of Aberdeen, Scotland, for her help with literature searching. We thank Mark Bolland and Andrew Grey, University of Auckland, New Zealand, for their advice.

Funding

The Health Services Research Unit is funded by the Chief Scientist Office of the Scottish Government Health and Social Care Directorates.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interests.

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© The Author(s) 2019

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.Health Services Research Unit, Health Sciences BuildingUniversity of AberdeenAberdeenUK

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