The change of bone mineral density and bone metabolism after gastrectomy for gastric cancer: a meta-analysis



Bone mineral density (BMD) is significantly decreased after gastrectomy in patients with gastric cancer. Calcium malabsorption, secondary hyperparathyroidism, and dominant bone resorption appear to contribute to bone loss in these patients. Patients should undergo early surveillance and nutritional or pharmacologic intensive interventions for bone health.


Survivorship care, including bone health, has become an important issue in gastric cancer. We performed a meta-analysis of the available observational studies to determine whether and how osteoporosis risk is increased after gastrectomy in patients with gastric cancer.


A total of 1204 patients (802 men) from 19 cohort studies were included. We evaluated the prevalence of osteoporosis in postgastrectomy patients, comparing the incidence according to the type of gastrectomy and sex. Additionally, we evaluated changes in bone mineral density (BMD) and bone metabolism-related markers pre- to postoperatively and between patients who underwent gastrectomy and matched controls. Proportion meta-analysis was performed and pooled odds ratios (ORs) were calculated.


The pooled incidence estimate was 36% [95% confidence interval (CI), 32–40]. The incidence of osteoporosis was significantly higher in women than in men (OR = 1.90, p < 0.001) but was similar between partial and total gastrectomy groups (OR = 0.983, p = 0.939). BMD was significantly decreased, and calcium, phosphorous, and parathyroid hormone levels were significantly increased in patients after gastrectomy compared to those before gastrectomy. BMD and calcium and 25OH-vitamin D levels were significantly decreased, and parathyroid hormone and 1,25OH-vitamin D levels were significantly increased in the gastrectomy group compared to that in the control group.


We found that BMD is significantly decreased after gastrectomy in patients with gastric cancer. Vitamin D deficiency and secondary hyperparathyroidism are suggested to be common mechanism underlying BMD impairment. After resection, patients should undergo long-term nutritional and bone health surveillance, in addition to their oncological follow-up.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3


  1. 1.

    Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6):394–424

    Article  Google Scholar 

  2. 2.

    Jung K-W, Won Y-J, Kong H-J, Oh C-M, Shin A, Lee J-S (2013) Survival of Korean adult cancer patients by stage at diagnosis, 2006-2010: national cancer registry study. Cancer Res Treat 45(3):162–171

    Article  Google Scholar 

  3. 3.

    Shapiro CL (2018) Cancer Survivorship. N Engl J Med 379(25):2438–2450

    Article  Google Scholar 

  4. 4.

    Miller KD, Siegel RL, Lin CC, Mariotto AB, Kramer JL, Rowland JH, Stein KD, Alteri R, Jemal A (2016) Cancer treatment and survivorship statistics, 2016. CA Cancer J Clin 66(4):271–289

    Article  Google Scholar 

  5. 5.

    Bernstein CN, Leslie WD, Leboff MS (2003) AGA technical review on osteoporosis in gastrointestinal diseases. Gastroenterology 124(3):795–841

    Article  Google Scholar 

  6. 6.

    Shamseer L, Moher D, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA, Group P-P (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ 350:g7647

    Article  Google Scholar 

  7. 7.

    Kanis JA on behalf of the World Health Organization Scientific Group (2007) Assessment of osteoporosis at the primary health-care level. Technical report. Sheffield: World Health Organization Collaborating Centre for Metabolic Bone Diseases, University of Sheffield

  8. 8.

    Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50(4):1088–1101

    CAS  Article  Google Scholar 

  9. 9.

    Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634

    CAS  Article  Google Scholar 

  10. 10.

    Becker BJ (1988) Synthesizing standardized mean-change measures. Br J Math Stat Psychol 41:257–278

    Article  Google Scholar 

  11. 11.

    Climent M, Pera M, Aymar I, Ramón JM, Grande L, Nogués X (2018) Bone health in long-term gastric cancer survivors: a prospective study of high-dose vitamin D supplementation using an easy administration scheme. J Bone Miner Metab 36(4):462–469

    CAS  Article  Google Scholar 

  12. 12.

    Glatzle J, Piert M, Meile T, Besenthal I, Schafer JF, Konigsrainer A, Zittel TT (2005) Prevalence of vertebral alterations and the effects of calcium and vitamin D supplementation on calcium metabolism and bone mineral density after gastrectomy. Br J Surg 92(5):579–585

    CAS  Article  Google Scholar 

  13. 13.

    Krogsgaard MR, Frolich A, Lund B, Lund B (1995) Long-term changes in bone mass after partial gastrectomy in a well-defined population and its relation to tobacco and alcohol consumption. World J Surg 19(6):867–871

    CAS  Article  Google Scholar 

  14. 14.

    Lim JS, Lee JI (2011) Prevalence, pathophysiology, screening and management of osteoporosis in gastric cancer patients. J Gastric Cancer 11(1):7–15

    Article  Google Scholar 

  15. 15.

    Oh HJ, Lim CH, Yoon BH, Yoon SB, Baeg MK, Kim WC, Cho YK, Park JM, Choi MG, Yoo HM, Song KY, Jeon HM, Park CH (2017) Fracture after gastrectomy for gastric cancer: A long-term follow-up observational study. Eur J Cancer 72:28–36

    Article  Google Scholar 

  16. 16.

    Seo GH, Kang HY, Choe EK (2018) Osteoporosis and fracture after gastrectomy for stomach cancer: A nationwide claims study. Medicine (Baltimore) 97(17):e0532

    Article  Google Scholar 

  17. 17.

    Yoo SH, Lee JA, Kang SY, Kim YS, Sunwoo S, Kim BS, Yook JH (2018) Risk of osteoporosis after gastrectomy in long-term gastric cancer survivors. Gastric Cancer 21(4):720–727

    CAS  Article  Google Scholar 

  18. 18.

    Baek KH, Jeon HM, Lee SS, Lim DJ, Oh KW, Lee WY, Rhee EJ, Han JH, Cha BY, Lee KW, Son HY, Kang SK, Kang MI (2008) Short-term changes in bone and mineral metabolism following gastrectomy in gastric cancer patients. Bone 42(1):61–67

    CAS  Article  Google Scholar 

  19. 19.

    Koufuji K, Takeda J, Aoyagi K, Yano S, Murakami N, Hori H, Terasaki Y, Shirouz K (1999) A study on metabolic bone disease before and after distal gastrectomy in gastric cancer patients by dual X-ray mineral absorptiometry measurements and markers of bone metabolism. Jpn J Gastroenterol Surg 32(12):2631–2636

    Article  Google Scholar 

  20. 20.

    Liedman B, Bosaeus I, Mellström D, Lundell L (1997) Osteoporosis after total gastrectomy: results of a prospective, clinical study. Scand J Gastroenterol 32(11):1090–1095

    CAS  Article  Google Scholar 

  21. 21.

    Wetscher G, Redmond E, Watfah C, Perdikis G, Gadenstatter M, Pointner R (1994) Bone disorders following total gastrectomy. Dig Dis Sci 39(12):2511–2515

    CAS  Article  Google Scholar 

  22. 22.

    Noh HM, Yoo JH, Jeong JY, Park YS (2018) Bone mineral density after treatment for gastric cancer: endoscopic treatment versus gastrectomy. Medicine (Baltimore) 97(1):e9582

    Article  Google Scholar 

  23. 23.

    Heiskanen JT, Kroger H, Paakkonen M, Parviainen MT, Lamberg-Allardt C, Alhava E (2001) Bone mineral metabolism after total gastrectomy. Bone 28(1):123–127

    CAS  Article  Google Scholar 

  24. 24.

    Klein KB, Orwoll ES, Lieberman DA, Meier DE, McClung MR, Parfitt AM (1987) Metabolic bone disease in asymptomatic men after partial gastrectomy with Billroth II anastomosis. Gastroenterology 92(3):608–616

    CAS  Article  Google Scholar 

  25. 25.

    Kwon SJ, Hahm JS, Cho YJ, Ahn Y, Shin DI (2000) The influence of gastrectomy on the change of bone metabolism and bone density. Korean J Intern Med 15(1):25–31

    CAS  Article  Google Scholar 

  26. 26.

    Resch H, Pietschmann P, Pernecker B, Krexner E, Willvonseder R (1992) The influence of partial gastrectomy on biochemical parameters of bone metabolism and bone density. Clin Investig 70(5):426–429

    CAS  Article  Google Scholar 

  27. 27.

    Bisballe S, Eriksen EF, Melsen F, Mosekilde L, Sorensen OH, Hessov I (1991) Osteopenia and osteomalacia after gastrectomy: interrelations between biochemical markers of bone remodelling, vitamin D metabolites, and bone histomorphometry. Gut 32(11):1303–1307

    CAS  Article  Google Scholar 

  28. 28.

    Imawari M, Kozawa K, Akanuma Y, Koizumi S, Itakura H, Kosaka K (1980) Serum 25-hydroxyvitamin D and vitamin D-binding protein levels and mineral metabolism after partial and total gastrectomy. Gastroenterology 79(2):255–258

    CAS  Article  Google Scholar 

  29. 29.

    Inoue K, Shiomi K, Higashide S, Kan N, Nio Y, Tobe T, Shigeno C, Konishi J, Okumura H, Yamamuro T et al (1992) Metabolic bone disease following gastrectomy: assessment by dual energy X-ray absorptiometry. Br J Surg 79(4):321–324

    CAS  Article  Google Scholar 

  30. 30.

    Park EJ, Joo IW, Jang M-J, Kim YT, Oh K, Oh HJ (2014) Prevalence of osteoporosis in the Korean population based on Korea National Health and Nutrition Examination Survey (KNHANES), 2008-2011. Yonsei Med J 55(4):1049–1057

    Article  Google Scholar 

  31. 31.

    Looker AC, Melton LJ, Harris TB, Borrud LG, Shepherd JA (2010) Prevalence and trends in low femur bone density among older US adults: NHANES 2005–2006 compared with NHANES III. J Bone Miner Res 25(1):64–71

    Article  Google Scholar 

  32. 32.

    Melton LJ 3rd, Chrischilles EA, Cooper C, Lane AW, Riggs BL (1992) Perspective. How many women have osteoporosis? J Bone Miner Res 7(9):1005–1010

    Article  Google Scholar 

  33. 33.

    Roder DM (2002) The epidemiology of gastric cancer. Gastric Cancer 5(1):5–11

    Article  Google Scholar 

  34. 34.

    Compston J, Cooper A, Cooper C, Gittoes N, Gregson C, Harvey N, Hope S, Kanis J, McCloskey E, Poole KE (2017) UK clinical guideline for the prevention and treatment of osteoporosis. Arch Osteoporos 12(1):43

    CAS  Article  Google Scholar 

  35. 35.

    Blom-Hogestol IK, Hewitt S, Chahal-Kummen M, Brunborg C, Gulseth HL, Kristinsson JA, Eriksen EF, Mala T (2019) Bone metabolism, bone mineral density and low-energy fractures 10 years after Roux-en-Y gastric bypass. Bone 127:436–445

    Article  Google Scholar 

  36. 36.

    Bredella MA, Greenblatt LB, Eajazi A, Torriani M, Yu EW (2017) Effects of Roux-en-Y gastric bypass and sleeve gastrectomy on bone mineral density and marrow adipose tissue. Bone 95:85–90

    Article  Google Scholar 

  37. 37.

    Geoffroy M, Charlot-Lambrecht I, Chrusciel J, Gaubil-Kaladjian I, Diaz-Cives A, Eschard JP, Salmon JH (2019) Impact of bariatric surgery on bone mineral density: observational study of 110 patients followed up in a specialized center for the treatment of obesity in France. Obes Surg 29(6):1765–1772

    Article  Google Scholar 

  38. 38.

    Luhrs AR, Davalos G, Lerebours R, Yoo J, Park C, Tabone L, Omotosho P, Torquati A, Portenier D, Guerron AD (2019) Determining changes in bone metabolism after bariatric surgery in postmenopausal women. Surg Endosc

  39. 39.

    Deller DJ (1966) Radiocalcium absorption after partial gastrectomy. Am J Dig Dis 11(1):10–19

    CAS  Article  Google Scholar 

  40. 40.

    Fischermann K, Harly S, Worning H, Zacho A (1967) Pancreatic function and the absorption of fat, iron, vitamin B12, and calcium after total gastrectomy for gastric cancer. Gut 8(3):260–266

    CAS  Article  Google Scholar 

  41. 41.

    Lips P (2006) Vitamin D physiology. Prog Biophys Mol Biol 92(1):4–8

    CAS  Article  Google Scholar 

  42. 42.

    Cuerda C, Camblor M, Bretón I, Velasco C, Parón L, Hervás E, Muñoz-Calero A, García-Peris P (2007) Cirugía gástrica como factor de riesgo nutricional. Nutr Hosp 22(3):330–336

    CAS  PubMed  Google Scholar 

Download references


This study was funded by a grant of the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea [grant number: HI18C0284].

Author information



Corresponding authors

Correspondence to S.-M. Lee or Y.-K. Lee.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval and consent to participate

This meta-analysis summarizes previously published data and does not include new human data or tissue that requires ethical approval and consent. The authors assume that the studies reviewed were conducted after ethical approval and consent and in accordance with the Declaration of Helsinki.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Oh, H., Yoon, BH., Ha, YC. et al. The change of bone mineral density and bone metabolism after gastrectomy for gastric cancer: a meta-analysis. Osteoporos Int 31, 267–275 (2020).

Download citation


  • Bone mineral density
  • Gastrectomy
  • Gastric cancer
  • Osteoporosis
  • Parathyroid hormone
  • Vitamin D