Changes in Bone Mineral Density in Patients with Type 2 Diabetes After Different Bariatric Surgery Procedures and the Role of Gastrointestinal Hormones

  • Fernando Guerrero-Pérez
  • Anna Casajoana
  • Carmen Gómez-Vaquero
  • Nuria Virgili
  • Rafael López-Urdiales
  • Laura Hernández-Montoliu
  • Jordi Pujol-Gebelli
  • Javier Osorio
  • Carolina Alves
  • Manuel Perez-Maraver
  • Silvia Pellitero
  • Anna Vidal-Alabró
  • Sonia Fernández-Veledo
  • Joan VendrellEmail author
  • Nuria VilarrasaEmail author
Original Contributions



To compare changes in bone mineral density (BMD) in patients with morbid obesity and type 2 diabetes (T2D) a year after being randomized to metabolic gastric bypass (mRYGB), sleeve gastrectomy (SG), and greater curvature plication (GCP). We also analyzed the association of gastrointestinal hormones with skeletal metabolism.


Forty-five patients with T2D (mean BMI 39.4 ± 1.9 kg/m2) were randomly assigned to mRYGB, SG, or GCP. Before and 12 months after surgery, anthropometric, body composition, biochemical parameters, fasting plasma glucagon, ghrelin, and PYY as well as GLP-1, GLP-2, and insulin after a standard meal were determined.


After surgery, the decrease at femoral neck (FN) was similar but at lumbar spine (LS), it was greater in the mRYGB group compared with SG and GCP − 7.29 (4.6) vs. − 0.48 (3.9) vs. − 1.2 (2.7)%, p < 0.001. Osteocalcin and alkaline phosphatase increased more after mRYGB. Bone mineral content (BMC) at the LS after surgery correlated with fasting ghrelin (r = − 0.412, p = 0.01) and AUC for GLP-1 (r = − 0.402, p = 0.017). FN BMD at 12 months correlated with post-surgical fasting glucagon (r = 0.498, p = 0.04) and insulin AUC (r = 0.384, p = 0.030) and at LS with the AUC for GLP-1 in the same time period (r = − 0.335, p = 0.049). However, in the multiple regression analysis after adjusting for age, sex, and BMI, the type of surgery (mRYGB) remained the only factor associated with BMD reduction at LS and FN.


mRYGB induces greater deleterious effects on the bone at LS compared with SG and GCP, and gastrointestinal hormones do not play a major role in bone changes.


Gastrointestinal hormones Bone mineral density Bariatric surgery 



The authors thank Dr. Jonathan Rogerson for helpful discussions on the manuscript and Bernat Miguel Huguet for statistical analysis. We thank CERCA Programme Generalitat de Catalunya for institutional support.

Compliance with Ethical Standards

Conflict of Interest

All authors declare that they have no conflict of interest. NV is the recipient of grants “Ajuts per a projectes de recerca clínica de l’Hospital Universitari de Bellvitge (2011-PR143/11)” and of the project “PI11/01960; PI14/01997 and PI17/01556” funded by the Instituto de Salud Carlos III and co-funded by the European Union (ERDF, “A way to build Europe”). JV has funding from the Instituto de Salud Carlos III through the project PI14/00228 and PI17/01503 co-funded by the European Union (ERDF, “A way to build Europe”). SFV has funding from the Spanish Ministry of Economy and Competitiveness and the European Regional Development Fund (ERDF) (SAF2015–65019-R). The Spanish Biomedical Research Center in Diabetes and Associated Metabolic Disorders (CIBERDEM) (CB07708/0012) is an initiative of the Instituto de Salud Carlos III. SFV acknowledges support from the Miguel Servet tenure-track program (CP10/00438 and CPII16/0008) from the Fondo de Investigación Sanitaria (FIS) co-financed by the ERDF.

Ethical Approval

The study was conducted according to the principles of the Declaration of Helsinki.

Informed Consent

All patients included in the study signed an informed consent form approved by the institutional ethics committee.


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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Fernando Guerrero-Pérez
    • 1
  • Anna Casajoana
    • 2
  • Carmen Gómez-Vaquero
    • 3
  • Nuria Virgili
    • 1
  • Rafael López-Urdiales
    • 1
  • Laura Hernández-Montoliu
    • 1
  • Jordi Pujol-Gebelli
    • 2
  • Javier Osorio
    • 2
  • Carolina Alves
    • 4
  • Manuel Perez-Maraver
    • 1
  • Silvia Pellitero
    • 5
    • 6
  • Anna Vidal-Alabró
    • 7
  • Sonia Fernández-Veledo
    • 6
    • 8
  • Joan Vendrell
    • 6
    • 8
    Email author
  • Nuria Vilarrasa
    • 1
    • 6
    Email author
  1. 1.Department of Endocrinology and NutritionBellvitge University Hospital-IDIBELLL’Hospitalet de LlobregatSpain
  2. 2.Department of General and Gastrointestinal Surgery. Bariatric Surgery UnitBellvitge University Hospital-IDIBELLL’Hospitalet de LlobregatSpain
  3. 3.Department of RheumatologyBellvitge University Hospital-IDIBELLL’Hospitalet de LlobregatSpain
  4. 4.Clinical Nutrition UnitBellvitge University Hospital-IDIBELLL’Hospitalet de LlobregatSpain
  5. 5.Department of Endocrinology and Nutrition and Health Sciences Research InstituteUniversity Hospital Germans Trias i PujolBadalonaSpain
  6. 6.CIBERDEM-CIBER de Diabetes y Enfermedades Metabólicas AsociadasInstituto de Salud Carlos IIIBarcelonaSpain
  7. 7.Instituto de Investigación Biomédica-IDIBELL,L’Hospitalet de LlobregatSpain
  8. 8.Diabetes and Metabolic Associated Diseases Research Group, Hospital Joan XXIII, School of MedicineRovira i Virgili UniversityTarragonaSpain

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