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Inicio Endocrinología, Diabetes y Nutrición Bone metabolism and fracture risk after Biliopancreatic Diversion
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Original article
Bone metabolism and fracture risk after Biliopancreatic Diversion
Metabolismo óseo y riesgo de fracturas tras la derivación biliopancreática
Mirian Alejo Ramosa,
Corresponding author
mirian_alejo@hotmail.com

Corresponding author.
, María D. Ballesteros Pomara, Ana M. Urioste Fondoa, Luis González Herráezb, Tomás González de Franciscob, Matilde Sierra Vegac, Isidoro M. Cano Rodrígueza
a Department of Endocrinology and Nutrition, Complejo Asistencial Universitario de León, Spain
b Department of General Surgery, Complejo Asistencial Universitario de León, Spain
c Department of Biomedical Sciences, IBIOMED, University of León, Spain
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accompanied by a reduction in mortality and associated comorbidities&#46; The recommendations for its use are the following&#58; body mass index &#40;BMI&#41;<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>40<span class="elsevierStyleHsp" style=""></span>kg&#47;m<span class="elsevierStyleSup">2</span> or between 35 and 40<span class="elsevierStyleHsp" style=""></span>kg&#47;m<span class="elsevierStyleSup">2</span> with associated comorbidities&#46;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">3</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Bariatric surgery &#40;BS&#41; procedures can be restrictive&#44; mixed&#44; and malabsorptive&#44; and it is usually effective but not risk free&#46;<a class="elsevierStyleCrossRefs" href="#bib0165"><span class="elsevierStyleSup">4&#44;5</span></a> One of the least known complications is the alteration of the phospho-calcium metabolism&#44; especially in predominantly malabsorptive techniques&#46; The most recent studies have suggested a negative effect on bone health at the expense of increased bone resorption and consequently&#44; a decrease in bone mineral density&#46;<a class="elsevierStyleCrossRefs" href="#bib0175"><span class="elsevierStyleSup">6&#8211;11</span></a> The mechanisms by which bone health is affected after weight loss in patients undergoing BS are not entirely clear&#59; multiple theories have been put forward in an attempt to explain this alteration&#44; with malabsorption caused by these procedures being the most studied&#46;<a class="elsevierStyleCrossRefs" href="#bib0195"><span class="elsevierStyleSup">10&#44;12&#8211;16</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">Biliopancreatic diversion &#40;BPD&#41;&#44; being a technique with a greater malabsorptive component and in spite of the exogenous contribution of calcium and vitamin D&#44; seems to have more influence on the elevation of the markers of bone turnover and a greater reduction of bone mineral density&#46;<a class="elsevierStyleCrossRefs" href="#bib0180"><span class="elsevierStyleSup">7&#44;10&#44;17</span></a> Consequently&#44; these patients may have greater bone fragility&#44; which in the long term may lead to a greater number of bone fractures in areas typical or atypical of osteoporosis or secondary to osteomalacia&#46; In recent years&#44; several retrospective studies have been published on the incidence of bone fragility fractures in patients undergoing bariatric surgery&#44; mostly with less than 5 years of follow-up and with controversial results&#46;<a class="elsevierStyleCrossRefs" href="#bib0185"><span class="elsevierStyleSup">8&#44;18</span></a> Subsequently&#44; in other reviews published with longer-term follow-up &#40;between 5 and 15 years after BS&#41;&#44; the results coincide because there is an increased risk of osteoporotic fractures&#46;<a class="elsevierStyleCrossRefs" href="#bib0190"><span class="elsevierStyleSup">9&#44;10&#44;19</span></a> In addition&#44; in their meta-analysis published in 2018&#44; Zhang et al&#46;<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">6</span></a> also concluded that BS increases the risk of bone fractures&#44; especially in atypical areas of osteoporosis&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">Given the disparity of results on this subject and the concern that this problem represents in the long term&#44; we plan to carry out this research&#44; with the aim of determining the incidence of bone fractures and the evolution of bone metabolism in patients who underwent BPD in the long term&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Material and methods</span><p id="par0025" class="elsevierStylePara elsevierViewall">A retrospective observational study of morbidly obese patients undergoing BPD at Complejo Asistencial Universitario de Le&#243;n &#40;CAULE&#41; was performed to determine the incidence of postoperative fractures&#46; The study period was from January 1998 to December 2017&#46; The BS performance criteria included age between 18 and 60 years&#44; BMI<span class="elsevierStyleHsp" style=""></span>&#62;<span class="elsevierStyleHsp" style=""></span>40<span class="elsevierStyleHsp" style=""></span>kg&#47;m<span class="elsevierStyleSup">2</span>&#44; or 35&#8211;40<span class="elsevierStyleHsp" style=""></span>kg&#47;m<span class="elsevierStyleSup">2</span> with comorbidities&#46; Included in the study were patients with a minimum follow-up of 1 year in the Clinical Nutrition and Dietetics Unit&#44; who agreed to respond to the telephone survey&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">The BS technique performed was BPD&#46;<a class="elsevierStyleCrossRefs" href="#bib0245"><span class="elsevierStyleSup">20&#44;21</span></a> Follow-up was performed&#58; presurgery&#44; postsurgery&#44; every 3 months in the first year&#44; every 6 months in the second year&#44; and annually thereafter&#46; Data were collected on associated comorbidities&#44; anthropometric parameters of weight&#44; height&#44; BMI&#44; percentage weight lost &#40;&#37;WL<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#40;weight initial<span class="elsevierStyleHsp" style=""></span>&#8722;<span class="elsevierStyleHsp" style=""></span>current weight&#41;&#47;&#40;weight initial&#41;<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>100&#41;&#44; and percentage of excess weight lost &#91;&#40;&#37;WL<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#37;EWL<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>weight initial<span class="elsevierStyleHsp" style=""></span>&#8722;<span class="elsevierStyleHsp" style=""></span>current weight&#47;initial weight<span class="elsevierStyleHsp" style=""></span>&#8722;<span class="elsevierStyleHsp" style=""></span>ideal weight&#41;<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>100&#93;&#44; bone metabolism analysis&#44; and data from before and after BS fractures&#46; To measure body weight&#44; an electric bioimpedance scale Tanita TBF-300A &#40;TANITA Corporation&#44; Japan&#41; was used&#44; and length was measured with an analog measuring rod&#46; Since the ideal weight does not coincide with the &#8220;normal&#8221; average weight of the population&#44; the Metropolitan Life Insurance<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">22</span></a> ideal weight charts were used&#46; All data were collected using structured questionnaires and subsequently registered in a database&#46; Being a retrospective study and given the difficulty of obtaining each patient&#39;s informed consent&#44; this was not performed&#46; However&#44; verbal consent was obtained during the telephone survey&#46;</p><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Blood test</span><p id="par0035" class="elsevierStylePara elsevierViewall">All analytical determinations were performed in the central laboratory of CAULE&#44; using fresh serum collected while fasting&#46; Having attained the results&#44; the clinical analysis specialist was responsible for validating them and comparing them with reference values by age and sex &#40;the equipment used was Cobas 800 Roche&#174; Omega 3000 program&#41;&#46; Calcium &#40;mg&#47;dl&#41; was determined using direct colorimetry &#40;Cresolphthalein complexone&#41;&#46; The total serum calcium was corrected for serum albumin &#40;corrected calcium&#41;&#46; Intact PTH &#40;1&#8211;84&#41;&#44; 25-hidroxy-vitamina D &#91;25&#40;OH&#41;D&#93;&#44; Osteocalcin&#44; and &#946;-CrossLaps &#40;ng&#47;ml&#41;&#58; PTH &#40;pg&#47;ml&#41;&#44; osteocalcin&#44; and &#946;-Crosslaps were analyzed from a plasma sample with EDTA by immunochemiluminescence&#46; Also&#44; 25&#40;OH&#41;D was determined using fresh serum and subsequently kept in a tube without anticoagulant&#46; The normal ranges of each parameter are&#58; corrected calcium &#40;8&#46;5&#8211;10&#46;5<span class="elsevierStyleHsp" style=""></span>mg&#47;dL&#41;&#44; PTH &#40;15&#8211;65<span class="elsevierStyleHsp" style=""></span>pg&#47;mL&#41;&#44; 25&#40;OH&#41;D &#40;30&#8211;100<span class="elsevierStyleHsp" style=""></span>ng&#47;mL&#41;&#44; &#946;-Crosslaps &#40;0&#46;1&#8211;0&#46;4<span class="elsevierStyleHsp" style=""></span>ng&#47;mL&#41;&#44; and osteocalcin &#40;&#60;26<span class="elsevierStyleHsp" style=""></span>ng&#47;mL&#41;&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Bone fracture data</span><p id="par0040" class="elsevierStylePara elsevierViewall">To collect the fracture data&#44; a structured questionnaire was carried out with the variables necessary to compile the history of fracture risk&#46; Parameters were collected from various tools&#58; Frax&#174;&#44; complementing the data with the QFracture&#174; tool and the European guide on the diagnosis and treatment of osteoporosis&#46; Patients who met the initial inclusion criteria were contacted by telephone&#44; verbal consent was first requested before asking the questionnaire questions&#44; and the data obtained from the hospital medical history record were subsequently confirmed&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Statistical analysis</span><p id="par0045" class="elsevierStylePara elsevierViewall">Statistical analysis was performed with SPSS v&#46;20 for Windows 10 Pro&#46; Kolmogorov&#8211;Smirnov tests were used to assess the adjustment to a normal distribution&#44; and data are shown as the mean &#40;standard deviation&#41; in this case or median &#40;interquartile range &#91;IQR&#93;&#41;&#46; The significance value used was <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#46; Student&#39;s <span class="elsevierStyleItalic">t</span> test was used to compare the independent mean variables&#44; ANOVA was used to compare the means&#44; and chi-square was used for proportions&#46; For correlations&#44; Pearson correlation and Spearman&#39;s Rho were used&#46; Cox proportional hazards regression was used to estimate the hazard ratios &#40;HRs&#41; and 95&#37; confidence intervals &#40;CIs&#41; of fractures after bariatric surgery&#46; Further assessed interactions by age&#44; sex&#44; comorbidities&#44; anthropometric parameters and bone metabolism&#46; To observe changes in fracture risk across the follow-up period&#44; we also assessed the HRs of fracture in the following times&#58; 1&#44; 2&#44; 3&#8211;5&#44; 6&#8211;9&#44; &#8805;10 years after the index date&#46;</p></span></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Results</span><p id="par0050" class="elsevierStylePara elsevierViewall">During the study period&#44; 352 patients were intervened for BPD&#44; and after applying the exclusion criteria&#44; only 216 subjects were included &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; Of this sample&#44; 78&#46;2&#37; were female and the mean age was 42&#46;5 &#40;10&#46;6&#41; years&#44; with a median follow-up of 6&#46;8 &#40;IQR 10&#46;0&#8211;3&#46;2&#41; years&#46; From all patients&#44; 25&#46;5&#37; were smokers&#44; and 71&#46;3&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>154&#41; of individuals suffered from more than one associated comorbidity&#58; 61&#37; suffered from hypertension&#44; 32&#46;4&#37; from type 2 diabetes &#40;T2D&#41;&#44; 30&#46;1&#37; from hypercholesterolemia&#44; and 10&#46;6&#37; from chronic pulmonary disease&#46; The mean initial BMI was 49&#46;7 &#40;6&#46;3&#41; kg&#47;m<span class="elsevierStyleSup">2</span>&#46; Before surgery&#44; 19&#46;9&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>43&#41; had suffered some type of bone fracture during their lifetime&#44; most of which occurred during childhood due to various traumatisms&#46; Parameters of bone metabolism previous BS&#58; calcium 9&#46;1 &#40;0&#46;5&#41; mg&#47;dl&#44; PTH 66&#46;6 &#40;29&#46;5&#41; pg&#47;ml&#44; osteocalcina 18&#46;5 &#40;8&#46;7&#41; ng&#47;ml&#44; &#946;-Crosslaps 0&#46;27 &#40;0&#46;14&#41; ng&#47;ml&#44; 25&#40;OH&#41;D 20&#46;6 &#40;36&#46;9&#8211;13&#46;3&#41; ng&#47;ml&#46; After BS&#44; bone fractures occurred in 13&#46;2&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>29&#41; of the patients&#58; 82&#46;8&#37; were female&#44; the mean age was 50&#46;4 &#40;12&#46;5&#41; years&#44; and the mean time until the first fracture was 7&#46;9 &#40;3&#46;8&#41; years&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0055" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a> describes the evolution of anthropometric data and analytical parameters of bone metabolism&#46; The &#37;WL ranged between 30 and 37&#37; remained stable during the follow-up&#46; A &#37;EWL of more than 60&#37; is objective&#44; which remains stable throughout monitoring&#46; PTH&#44; osteocalcin&#44; and &#946;-Crosslaps show a tendency to increase from the first year after surgery&#44; the latter two reaching their peak in the first year&#58; osteocalcin&#58; 47&#46;3 vs&#46; 18&#46;5 &#40;ng&#47;ml&#41; basal&#44; &#946;-Crosslaps 0&#46;91 vs&#46; 0&#46;27 &#40;ng&#47;ml&#41; basal&#46; PTH reaches maximum levels at 8 years postsurgery&#58; 129&#46;1 &#40;113&#46;3&#41; pg&#47;ml&#44; maintaining an inverse relationship to serum calcium corrected and 25&#40;OH&#41;D&#46; Calcium&#58; maximum association at the sixth year after surgery &#40;Pearson correlation <span class="elsevierStyleItalic">r</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;0&#46;49&#59; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;000&#41;&#59; 25&#40;OH&#41;D&#58; maximum association at the fourth year after surgery &#40;Rho Spearman &#8722;0&#46;60&#59; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;000&#41;&#46; Levels of 25&#40;OH&#41;D were maintained in the deficit range &#40;&#60;30<span class="elsevierStyleHsp" style=""></span>ng&#47;ml&#41; in all visits&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0060" class="elsevierStylePara elsevierViewall">The incidence rate of postoperative bone fractures was 19&#46;6 per 1000 person-years follow-up &#40;95&#37;CI&#58; 1&#46;3&#8211;2&#46;7&#41;&#44; with a prevalence of 13&#46;4&#37; &#40;95&#37;CI&#58; 8&#46;9&#8211;18&#46;0&#41;&#46; Of the sample&#44; 10&#46;4&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>3&#41; had more than one fracture episode during follow-up&#46; The mean follow-up to the first fracture was at 7&#46;9 years postsurgery&#46; Most fractures occurred in the upper limbs 44&#46;8&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>13&#41; and lower limbs 20&#46;7&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>6&#41;&#44; in the spine 20&#46;7&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>6&#41;&#44; and in the hip 13&#46;8&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>4&#41;&#46; Amongst the causes of fractures&#44; the most common was secondary to casual fall in 55&#46;2&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>16&#41;&#44; followed by spontaneous in 17&#46;2&#37;&#44; traffic accident in 13&#46;8&#37;&#44; traumatic in 10&#46;3&#37;&#44; and&#44; finally&#44; pathological or tumoral in 3&#46;4&#37;&#46; See <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0065" class="elsevierStylePara elsevierViewall">An increased risk of bone fractures to longer evolution time was observed&#44; suffering from 0 to 3 fractures during the first 5 postoperative years &#40;cumulative incidence 0&#8211;1&#46;7&#37;&#41;&#44; between the fifth and tenth postoperative years&#44; 2&#8211;4 new fractures episodes occurred each year&#46; Also&#44; for individuals with more than 10 postoperative years&#44; 7 bone fracture events were reported &#40;cumulative incidence 14&#46;5&#37;&#41;&#46; See <a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#46; The bivariate analysis did not show significant differences between age&#44; sex and associated comorbidities in fractured versus unfractured patients&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><p id="par0070" class="elsevierStylePara elsevierViewall">Subjects who presented postsurgery bone fractures had a higher mean BMI &#40;kg&#47;m<span class="elsevierStyleSup">2</span>&#41;&#58; 35&#46;2&#40;5&#46;2&#41; vs&#46; 32&#46;2&#40;5&#46;1&#41; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;03&#59; 34&#46;4&#40;4&#46;8&#41; vs&#46; 31&#46;4&#40;5&#46;3&#41; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;03&#41; and lower &#37;EWL &#40;57&#46;3&#37; vs&#46; 65&#46;6&#37; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;02&#59; 59&#46;5&#37; vs&#46; 67&#46;6&#37; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;04&#41; than those unfractured patients in the first and second year after bariatric surgery&#46; In terms of bone metabolism parameters&#44; subjects with some type of postsurgery fracture had higher PTH &#40;pg&#47;ml&#41; levels in the first years of follow-up&#46; At 1 year&#58; 98&#46;1&#40;50&#46;1&#41; vs&#46; 77&#46;8&#40;32&#46;8&#41;&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;04&#59; 2 years&#58; 130&#46;2&#40;115&#46;6&#41; vs&#46; 92&#46;8&#40;51&#46;5&#41;&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;03&#59; 3 years&#58; 142&#46;8&#40;128&#46;7&#41; vs&#46; 98&#46;9&#40;57&#46;8&#41;&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;07&#59; 5 years&#58; 162&#46;5&#40;106&#46;4&#41; vs&#46; 110&#46;3&#40;76&#46;0&#41;&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;03&#46; 25&#40;OH&#41;D was lower in fractured patients&#44; and the levels of &#946;-Crosslaps and osteocalcin levels were slightly higher in comparison to the unfractured patients &#40;without reaching statistical significance&#41;&#46; &#37;WL and corrected calcium levels do not differ in the groups&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">There was no association of fracture risk with sex&#44; age&#44; tobacco use&#44; type 2 diabetes&#44; hypertension&#44; hyperlipidemia&#44; chronic pulmonary disease&#44; weight or BMI prior to surgery &#40;unadjusted&#44; sex&#44; age adjusted&#44; and fully adjusted&#41;&#46; Likewise&#44; the subjects with a history of fracture before undergoing bariatric surgery were not at significant risk of fracture after surgery &#40;HR&#58; 0&#46;85&#44; 95&#37; CI&#58; 0&#46;25&#8211;2&#46;87&#41;&#46; See <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>&#46; In a univariate analysis&#44; 25&#40;OH&#41;D was a risk factor for any fracture from the tenth year after surgery &#40;Cox model&#44; HR&#58; 1&#46;02&#59; 95&#37; CI&#58; 1&#46;01&#8211;1&#46;04&#59; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;01&#41;&#44; and no significant interactions of adjusted HR were found&#46; In a multivariate analysis&#44; the risk of fractures was associated with increased levels of PTH at the fourth year after BS &#40;adjusted HR&#58; 1&#46;10&#59; 95&#37; CI&#58; 1&#46;01&#8211;1&#46;11&#59; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;03&#41;&#46; Subjects with a higher &#37;EWL had less risk of fractures from the fifth year after surgery &#40;adjusted Cox model HR 0&#46;97&#59; 95&#37; CI 0&#46;94&#8211;0&#46;99&#59; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;02&#41;&#46; See <a class="elsevierStyleCrossRef" href="#tbl0015">Table 3</a>&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><elsevierMultimedia ident="tbl0015"></elsevierMultimedia></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Discussion</span><p id="par0080" class="elsevierStylePara elsevierViewall">Currently&#44; few studies have described the risk of fracture after BS and the results obtained to date are controversial&#46; In this study we observed an incidence of 19&#46;6 per 1000 person-years of follow-up &#40;95&#37;CI&#58; 1&#46;3&#8211;2&#46;7&#41; and a prevalence of 13&#46;4&#37; &#40;95&#37;CI 8&#46;9&#8211;18&#46;0&#41;&#46; The risk of bone fractures increased to longer surgery evolution time&#46; It should be noted that this study highlights a pattern of bone fractures in typical osteoporotic areas<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">23</span></a> &#40;greater frequency in the upper limbs&#44; spine and hip&#44; pelvis&#44; and femur&#41;&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">The Spanish population presents a medium risk of bone fractures due to fragility&#46; The probability of presenting a hip fracture is lower than in the United States and Northern European countries&#46;<a class="elsevierStyleCrossRef" href="#bib0265"><span class="elsevierStyleSup">24</span></a> The study published by Alvarez-Nebreda et al&#46;<a class="elsevierStyleCrossRef" href="#bib0270"><span class="elsevierStyleSup">25</span></a> in 2008 estimated the incidence of hip fracture between 125&#46;9&#8211;353&#46;0 per 100&#44;000 person-years over 65&#44; and the incidence of hip fracture found in our series was similar with 2&#46;7 per 1000 person-years &#40;270&#46;0 per 100&#44;000 person-years&#41;&#46; However&#44; it should be noted that the mean age of the patients in this study was under 50 vs 65 years of age&#46; As for vertebral fracture&#44; it is usually infrequent in patients under 50 years of age&#44; according to the <span class="elsevierStyleItalic">European Prospective Osteoporosis Study</span> &#40;EPOS&#41;<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">26</span></a> and it presents an annual incidence of 1&#8211;3 in women and 5&#46;7&#8211;6&#46;8 in men per 1000 person-years over 65 years of age&#46; If we compare our data with those of EPOS&#44; it could be said that they are similar &#40;incidence of 4&#46;1 per 1000 person-years&#41;&#46; However&#44; the shorter longevity of this month should be highlighted again&#46;</p><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Comparison with other studies</span><p id="par0090" class="elsevierStylePara elsevierViewall">Nakamura et al&#46;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">10</span></a> conducted a retrospective study &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>258&#41; undergoing Roux-en-Y gastric bypass with a mean follow-up of 7&#46;7 years&#44; in which they studied the risk of fractures compared with the general U&#46;S&#46; population&#44; described a history of fracture in 36&#37; of presurgery&#44; and 51&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>132&#41; of postsurgery patients&#44; and the median time to first fracture was at 13 years of follow-up&#46; They concluded that there is an early and sustained increase in the cumulative incidence of fractures in the BS group compared to what was expected &#40;58 vs&#46; 24&#37;&#41; respectively&#44; with an increase in the overall fracture rate by more than double &#40;RR 2&#46;3&#59; 95&#37;CI 1&#46;8&#8211;2&#46;8&#41;&#46; In our study&#44; the mean time to the first fracture occurred much earlier &#40;7&#46;9 years postsurgery&#41;&#46; This could be explained by the type of technique used &#40;BPD&#41;&#44; which involves a greater malabsorptive component and may cause more significant changes in bone metabolism&#46; The percentage of patients with bone fractures was high but lower than that observed by Nakamura&#58; 19&#46;9&#37; vs&#46; 36&#37; before surgery and 13&#46;4&#37; vs&#46; 58&#37; postsurgery&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">In the United Kingdom&#44; Lalmohamed et al&#46;<a class="elsevierStyleCrossRef" href="#bib0185"><span class="elsevierStyleSup">8</span></a> studied a total of 2079 obese patients undergoing BS &#40;60&#37; with adjustable gastric banding&#41; to assess the risk of fracture compared with a control group during a mean of 2&#46;2 years of follow-up&#44; they concluded that there is no increased risk in the general population ratio of any type of fracture &#40;8&#46;8 vs 8&#46;2 per 1000 person-years&#59; RR 0&#46;89 95&#37;CI 0&#46;6 to 1&#46;3&#41; compared to the control group&#46; These results differ from those observed in this series&#44; where we do find an increased risk of bone fractures&#46; These differences may be caused by the type of technique used and the short follow-up time&#46; Vertical gastrectomy carries less risk of malabsorption Regarding the short follow-up period&#44; in this type of patient&#44; 2&#46;2 years is not enough time to assess the risk of fractures after BS&#46; In our study&#44; the increase in bone fractures was more evident after 10 years postsurgery&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">Rousseau et al&#46;<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">9</span></a> developed a retrospective study of cases and controls to study the risk of bone fractures in patients undergoing BS compared with two groups of subjects &#40;obese and non-obese&#41;&#46; They studied a sample of <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>12&#44;676 &#40;72&#44;3 were women&#44; and the mean age was 42&#46;6 years&#41;&#44; demonstrating that patients undergoing BS had a higher risk of fractures compared to the controls &#40;RR 1&#46;4 95&#37;CI&#58; 1&#46;2&#8211;1&#46;5&#41;&#44; with a frequency of 4&#46;1&#37; of fractures and a mean time until the first fracture of 3&#46;9 years&#44; being higher in typical areas of osteoporosis &#40;upper limbs&#44; spine&#44; and hip&#41;&#46; In addition&#44; this relationship was only observed in patients undergoing BPD&#59; however&#44; this was not conclusive in the remaining patients undergoing gastrectomy or gastric bypass due to the small number of cases and the short follow-up time&#46; The fracture percentage was higher in our series 19&#46;9&#37; vs&#46; 4&#46;1&#37; with a mean time until the first fracture of 7&#46;9 years&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">Regarding the anthropometric data from BMI and &#37;EWL and their relationship to bone fractures&#44; the data are more controversial&#46; Subjects with some event of fractures during follow-up presented higher BMI and lower decrease in &#37;EWL than patients who did not present any fracture&#58; at one year&#58; BMI 35&#46;2 vs&#46; 32&#46;2<span class="elsevierStyleHsp" style=""></span>kg&#47;m<span class="elsevierStyleSup">2</span>&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;03&#59; &#37;EWL 57&#46;3&#37; vs&#46; 65&#46;5&#37;&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;03&#59; 2 years postsurgery&#58; BMI 34&#46;4 vs&#46; 31&#46;5<span class="elsevierStyleHsp" style=""></span>kg&#47;m<span class="elsevierStyleSup">2</span>&#44; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;03&#59; &#37;EWL 59&#46;5&#37; vs&#46; 67&#46;6&#37;&#46; In addition&#44; subjects with a higher &#37;EWL had less risk of fractures from the fifth year after surgery &#40;adjusted Cox model HR 0&#46;97&#59; 95&#37; CI&#58; 0&#46;94&#8211;0&#46;99&#59; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;02&#41;&#46; Some studies on the risk of fractures and BS have proposed a ratio of fracture protection to greater &#37;EWL&#46;<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">27</span></a> The association of this study between lower loss of BMI and &#37;EWL with increased risk of fractures may be related to poor adherence to lifestyle changes&#44; calcium and vitamin D supplementation&#44; which in a malabsorptive technique would be crucial to produce increased risk in the rate of bone fractures&#46; Rousseau et al&#46;<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">9</span></a> also suggested that patients with higher BMI had more fracture episodes&#44; hypothesizing that obesity may not be as protective for fractures as originally thought&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">So far&#44; most studies on bariatric surgery and its bone effects have been based on the evolution of resorption markers and bone mineral density&#44; agreeing that BS caused negative changes in bone metabolism&#46;<a class="elsevierStyleCrossRefs" href="#bib0220"><span class="elsevierStyleSup">15&#44;17&#44;28</span></a> In our series the levels of PTH&#44; osteocalcin and &#946;-Crosslaps increased gradually from the first year after surgery&#44; maintaining an inverse relationship with 25&#40;OH&#41;D levels&#46; However&#44; only high levels of PTH &#40;pg&#47;ml&#41; were significantly associated with patients with bone fractures&#44; with higher levels than those not fractured during the first 5 years of follow-up&#58; at 77&#46;8 vs&#46; 98&#46;1and at 5 years&#58; 110&#46;3 vs&#46; 162&#46;5&#59; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#44; adjusted Cox HR 1&#46;10&#59; 95&#37;CI&#58; 1&#46;01&#8211;1&#46;11&#59; <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;03&#41;&#46; Other authors have agree with these results&#44;<a class="elsevierStyleCrossRefs" href="#bib0180"><span class="elsevierStyleSup">7&#44;11&#44;15&#44;17</span></a> highlighting the negative effect of bariatric surgery on bone metabolism using the BPD technique and the relationship of increased PTH&#44; osteocalcin and &#946;-Crosslaps with decreased bone mineral density&#46; Therefore&#44; it is essential to implement supplementation with calcium and vitamin D&#44; and thus avoid or reduce the persistent secondary hyperparathyroidism that may occur in these patients&#44; which causes an increase in the fracture risk&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Strengths and limitations</span><p id="par0115" class="elsevierStylePara elsevierViewall">The main strength of our study is the long follow-up time &#40;&#62;10 years&#41;&#44; as when the postsurgery evolution time&#44; is longer&#44; the probability of bone fracture risk is greater&#46; Another strength is our description of a cohort with a good number of patients from a single center undergoing malabsorptive surgery&#44; which can cause greater problems in bone metabolism&#46; We applied an equal follow-up protocol for all patients and performed blood tests in the same hospital&#46;</p><p id="par0120" class="elsevierStylePara elsevierViewall">With respect to limitations&#44; the study&#39;s retrospective design leads to the incomplete follow-up of some subjects and the lack of a control group&#58; in addition&#44; collecting data on calcium and vitamin D supplementation plays an important role in bone metabolism&#46; Also&#44; we did not evaluate several determinants of bone health&#44; such as exposure to estrogens in women&#44; taking drugs that may cause bone damage or other causes of primary and secondary bone diseases&#46; Another limitation was that we had no information on bone mineral density&#44; which would have helped us in determining the underlying biological mechanism in the association between BS and fractures&#46;</p></span></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Conclusion</span><p id="par0125" class="elsevierStylePara elsevierViewall">Despite the limitations&#44; we estimated the incidence of fractures over a long follow-up period in women and men undergoing biliopancreatic diversion&#46; A specific analysis of the fracture site&#44; objectified a greater frequency in the typical sites of osteoporotic fractures&#44; mainly in the spine and upper limbs&#44; and observed a positive relationship between the increase in PTH&#44; &#946;-Crosslaps&#44; and the risk of fracture&#46; To minimize the effect of BS especially in malabsorptive techniques such as BPD on bone health&#44; the importance of adherence to calcium and vitamin D supplements should be reinforced&#46; Finally&#44; more studies should be conducted on the mechanisms involved in increasing the risk of fractures after bariatric surgery&#44; given the paucity of evidence in this area&#46;</p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0115">Authors&#8217; contribution</span><p id="par0130" class="elsevierStylePara elsevierViewall">Mirian Alejo Ramos&#46; Conception and design of the study&#44; data acquisition&#44; analysis and interpretation of the data&#44; preparation of the article&#44; final approval of the version presented&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">Mar&#237;a D&#46; Ballesteros Pomar&#46; Conception and design of the study&#44; data acquisition&#44; analysis and interpretation of the data&#44; final approval of the version presented</p><p id="par0140" class="elsevierStylePara elsevierViewall">Ana Urioste Fondo&#46; Data acquisition&#44; critical review of the article&#46;</p><p id="par0145" class="elsevierStylePara elsevierViewall">Luis Gonzalez Herr&#225;ez&#46; Critical review of the article&#46;</p><p id="par0150" class="elsevierStylePara elsevierViewall">Tomas Gonz&#225;lez de Francisco&#46; Critical review of the article&#46;</p><p id="par0155" class="elsevierStylePara elsevierViewall">Matilde Sierra Vega&#46; Critical review of the article&#46;</p><p id="par0160" class="elsevierStylePara elsevierViewall">Isidoro M&#46; Cano Rodr&#237;guez&#46; Critical review of the article and final approval of the version presented&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0120">Informed consent</span><p id="par0165" class="elsevierStylePara elsevierViewall">Informed consent was not needed in this study&#46; However&#44; an informed verbal consent was requested to complete the telephone survey&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0125">Funding sources</span><p id="par0170" class="elsevierStylePara elsevierViewall">No funding sources were required in the study&#46;</p></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0130">Conflict of interest</span><p id="par0175" class="elsevierStylePara elsevierViewall">The authors declare no conflicts of interest&#46;</p></span></span>"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Background</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Bariatric surgery &#40;BS&#41; is an effective treatment&#46; However&#44; there have been concerns regarding the negative effect on the bone&#46; The aim of this study was to assess changes in bone metabolism and the risk of fracture after biliopancreatic diversion &#40;BPD&#41;&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Material and methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">A retrospective analysis of obese patients undergoing BPD between 1998 and 2017 was conducted&#44; and patients with at least 1 year of follow-up were included&#46; The incidence of fracture and of changes in bone metabolism was studied&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">In total&#44; 216 patients were included &#40;78&#46;2&#37; female&#41;&#44; with a mean age of 42&#46;5&#40;10&#46;6&#41; years&#46; The median follow-up was 6&#46;8&#40;IQR 10&#46;2&#8211;3&#46;2&#41; years&#46; The mean body mass index &#40;BMI&#41; was 49&#46;7&#40;6&#46;3&#41; kg&#47;m<span class="elsevierStyleSup">2</span>&#46; 13&#46;2&#37; &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>29&#41; suffered a bone fracture after surgery&#59; the time until the first fracture was 7&#46;9&#40;3&#46;8&#41; years &#40;55&#46;2&#37; secondary to a casual fall&#41;&#46; The rate of fracture incidence was 19&#46;6 per 1000 person-years &#40;95&#37;CI&#58; 1&#46;3&#8211;2&#46;7&#41;&#44; prevalence was 13&#46;4&#37; &#40;95&#37;CI&#58; 8&#46;9&#8211;18&#46;0&#41;&#46; The risk of bone fractures seems to increase with longer postoperative evolution time&#46; PTH &#40;pg&#47;ml&#41; levels were significantly higher in patients with fractures &#40;1 year&#44; 98&#46;1 vs&#46; 77&#46;8&#59; 5 years&#44; 162&#46;5 vs&#46; 110&#46;3 <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#44; adjusted HR 1&#46;10&#59; 95&#37;CI 1&#46;01&#8211;1&#46;11&#41;&#46; Subjects with a higher &#37;EWL had less risk of fractures after surgery &#40;adjusted HR 0&#46;97&#59; 95&#37;CI 0&#46;94&#8211;0&#46;99&#41;&#46; Moreover&#44; 25&#40;OH&#41;D levels were lower&#44; and osteocalcin and &#946;-Crosslaps levels were slightly higher &#40;not significant&#41; in patients with fractures&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusion</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">BPD is related to important changes in bone metabolism&#44; which can lead to an increased risk of bone fractures&#46; Assessing the risk of fractures should be part of BS patient care&#46;</p></span>"
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            "titulo" => "Background"
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        "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Objetivo</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">La cirug&#237;a bari&#225;trica &#40;CB&#41; es un tratamiento eficaz&#46; Sin embargo&#44; sus efectos negativos sobre el metabolismo &#243;seo son pocos conocidos&#46; El objetivo del estudio fue evaluar los cambios del metabolismo &#243;seo y el riesgo de fracturas tras derivaci&#243;n biliopancre&#225;tica &#40;DBP&#41;&#46;</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Material y m&#233;todos</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Estudio retrospectivo en obesos sometidos a DBP entre 1998-2017&#46; Se incluy&#243; apacientes con seguimiento m&#237;nimo de un a&#241;o y se estudi&#243; el riesgo de fracturas y los cambios en el metabolismo &#243;seo&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Se estudi&#243; an 216 sujetos &#40;78&#44;2&#37; femenino&#41;&#44; edad media 42&#44;5&#40;10&#44;6&#41; a&#241;os&#44; mediana de seguimiento fue 6&#44;8 &#40;rango intercuart&#237;lico 10&#44;2-3&#44;2&#41; a&#241;os&#46; Media inicial de &#237;ndice de masa corporal fue 49&#44;7 &#40;6&#44;3&#41; kg&#47;m<span class="elsevierStyleSup">2</span>&#59; el 13&#44;2&#37; &#40;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>29&#41; present&#243; alguna fractura &#243;sea poscirug&#237;a&#44; la media de tiempo hasta la primera fractura fue 7&#44;9 &#40;3&#44;8&#41; a&#241;os &#40;55&#44;2&#37; secundarias a ca&#237;da casual&#41;&#46; La tasa de incidencia de fracturas fue 19&#44;6 por 1&#46;000 personas-a&#241;o &#40;IC del 95&#37;&#44; 1&#44;3-2&#44;7&#41;&#44; prevalencia 13&#44;4&#37; &#40;IC del 95&#37;&#44; 8&#44;9-18&#44;0&#41;&#46; El riesgo de fracturas &#243;seas parece aumentar a mayor tiempo de evoluci&#243;n tras CB&#46; Los niveles de parathormona &#40;pg&#47;ml&#41; fueron mayores en los pacientes con fracturas &#40;al a&#241;o 98&#44;1 vs&#46; 77&#44;8&#59; 5 a&#241;os 162&#44;5 vs&#46; 110&#44;3&#44; p<span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#44;05&#41; HR ajustada 1&#44;10&#44; IC del 95&#37;&#44; 1&#44;01-1&#44;11&#46; Un mayor porcentaje de sobrepeso perdido implic&#243; menos riesgo de fracturas &#40;HR ajustada 0&#44;97&#59; IC del 95&#37;&#44; 0&#44;94-0&#44;99&#41;&#46; Los sujetos con fractura poscirug&#237;a presentaron niveles de 25&#40;OH&#41;D m&#225;s bajos y cifras de &#946;-Crosslaps y osteocalcina m&#225;s elevadas&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusi&#243;n</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">La DBP asocia importantes cambios en el metabolismo &#243;seo&#44; con probable aumento del riesgo de fracturas&#46; La evaluaci&#243;n del riesgo de fracturas debe formar parte de la atenci&#243;n al paciente con CB&#46;</p></span>"
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                  \t\t\t\t\tvoid\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t" scope="col">Type of fractures&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col">Incidence&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">N</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&#37;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">N</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&#37;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">N</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&#37;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">N</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">N</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">N</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&#37;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">10<span class="elsevierStyleSup">3</span>&#47;p&#47;a&#241;o<a class="elsevierStyleCrossRef" href="#tblfn0015"><span class="elsevierStyleSup">c</span></a>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Clinical spine&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">3&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">50&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">16&#46;7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">0&#46;0&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">2&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">33&#46;3&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">0&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">20&#46;7&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t">4&#46;1&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Pelvis&#44; hip and femur&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">1&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">25&#46;0&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">50&#46;0&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">13&#46;8&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Distal lower limbs<a class="elsevierStyleCrossRef" href="#tblfn0005"><span class="elsevierStyleSup">a</span></a>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">33&#46;3&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">20&#46;7&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Total&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">16&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">4&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">19&#46;6&nbsp;\t\t\t\t\t\t\n
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                  """
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          "leyenda" => "<p id="spar0070" class="elsevierStyleSimplePara elsevierViewall">Events&#44; <span class="elsevierStyleItalic">n</span> &#40;&#37;&#41;&#58; 29 &#40;13&#46;2&#37;&#41;&#44; 19&#46;6 per 1000 person years &#40;95&#37; CI 1&#46;3&#8211;2&#46;7&#41; TD2&#58; Type 2 Diabetes&#44; CPD&#58; Chronic Pulmonary disease&#44; HR&#58; hazard ratio&#44; 1&#58; adjusted for age&#44; sex&#44; smoking&#44; hypertension&#44; hyperlipidemia&#44; type 2 diabetes&#44; Chronic Pulmonary disease&#44; previous weight&#44; BMI and previous fracture&#46;</p>"
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                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td-with-role" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t" scope="col">Risk factor&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">1&#46;14 &#40;0&#46;33&#8211;3&#46;87&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">0&#46;38 &#40;0&#46;11&#8211;2&#46;22&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">1&#46;07 &#40;0&#46;51&#8211;2&#46;26&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">TD2 &#40;yes&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">0&#46;81 &#40;0&#46;37&#8211;1&#46;76&#41;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&#46;02 &#40;0&#46;37&#8211;2&#46;82&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
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                  \t\t\t\t">1&#46;29 &#40;0&#46;39&#8211;4&#46;22&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">Hyperlipidemia&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&#46;29 &#40;0&#46;54&#8211;3-10&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&#46;36 &#40;0&#46;57&#8211;3&#46;24&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&#46;72 &#40;0&#46;59&#8211;4&#46;96&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Previous weight &#40;kg&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&#46;01 &#40;0&#46;99&#8211;1&#46;03&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&#46;00 &#40;0&#46;98&#8211;1&#46;03&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&#46;02 &#40;0&#46;99&#8211;1&#46;05&#41;&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Previous BMI&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="char" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">1&#46;00 &#40;0&#46;94&#8211;1&#46;10&#41;&nbsp;\t\t\t\t\t\t\n
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Article information
ISSN: 25300164
Original language: English
DOI:10.1016/j.endinu.2020.08.005
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