Cancer Res Treat.  2019 Apr;51(2):530-537. 10.4143/crt.2018.164.

Increased Risk of Osteoporosis in Gastric Cancer Survivors Compared to General Population Control: A Study with Representative Korean Population

• Jeong SM
• Shin DW
• Lee JE
• Jin SM
• Kim S

• KMID: 2464400
• DOI: http://doi.org/10.4143/crt.2018.164

Abstract

PURPOSE
Although several studies have suggested that osteoporosis is common in survivors of gastric cancer (GC), no study to date has directly assessed the risk for osteoporosis in GC survivors compared to matched controls. Thus, we aimed to investigate the relative risk for osteoporosis in survivors of GC compared to general population.
MATERIALS AND METHODS
We used the Korea National Health and Nutrition Examination Survey data (2008-2011). Patients with a history of GC (n=94) were defined as case among 8,142 individuals over 50 years old who were evaluated by dual-energy X-ray absorptiometry. Controls (n=470) were matched to cases by age and sex in a 1:5 ratio. Osteopenia (-2.5 < T-score <-1.0) and osteoporosis (T-score ≤-2.5) were defined.
RESULTS
The prevalence of osteoporosis in GC survivors was 30.2%, which was significantly greater than that of controls (19.7%). In total, GC survivors had a 3.7-fold increased risk for osteoporosis compared to controls (p=0.021). In addition, the risk for osteoporosis of the total proximal femur total (TF) and femur neck (FN) was significantly increased among GC survivors compared to controls (adjusted relative risk, 4.64; 95% confidence interval, 1.16 to 18.6 in TF and adjusted relative risk, 3.58; 95% confidence interval, 1.19 to 10.8 in FN). Furthermore, we found sub-optimal daily calcium intake and mean serum levels of 25-hydroxy-vitamin D in both groups.
CONCLUSION
GC survivors are at significantly increased risk for osteoporosis, especially in the femur. Clinically, our finding supports the importance of screening bone health and adequate nutrient supplementation in survivors of GC.

Keyword

Osteoporosis; Gastric neoplasms; Calcium; Vitamin D

MeSH Terms

Absorptiometry, Photon
Bone Diseases, Metabolic
Calcium
Femur
Femur Neck
Humans
Korea
Mass Screening
Nutrition Surveys
Osteoporosis*
Population Control*
Prevalence
Stomach Neoplasms*
Survivors*
Vitamin D
Calcium
Vitamin D

Reference

References

1. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015; 136:E359–86.

2. Howlader N, Noone AM, Krapcho M, Miller D, Bishop K, Altekruse SF, et al. SEER cancer statistics review, 1975-2014. Bethesda, MD: National Cancer Institute;2016.

3. Jung KW, Won YJ, Oh CM, Kong HJ, Lee DH, Lee KH, et al. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2014. Cancer Res Treat. 2017; 49:292–305.

4. Suh M, Choi KS, Park B, Lee YY, Jun JK, Lee DH, et al. Trends in cancer screening rates among Korean men and women: results of the Korean national cancer screening survey, 2004-2013. Cancer Res Treat. 2016; 48:1–10.

5. Jeong O, Park YK. Clinicopathological features and surgical treatment of gastric cancer in South Korea: the results of 2009 nationwide survey on surgically treated gastric cancer patients. J Gastric Cancer. 2011; 11:69–77.

6. Bang YJ, Van Cutsem E, Feyereislova A, Chung HC, Shen L, Sawaki A, et al. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet. 2010; 376:687–97.

7. Jung KW, Won YJ, Kong HJ, Oh CM, Shin A, Lee JS. Survival of Korean adult cancer patients by stage at diagnosis, 2006-2010: national cancer registry study. Cancer Res Treat. 2013; 45:162–71.

8. Seo SH, Kim SE, Kang YK, Ryoo BY, Ryu MH, Jeong JH, et al. Association of nutritional status-related indices and chemotherapy-induced adverse events in gastric cancer patients. BMC Cancer. 2016; 16:900.

9. Lim JS, Kim SB, Bang HY, Cheon GJ, Lee JI. High prevalence of osteoporosis in patients with gastric adenocarcinoma following gastrectomy. World J Gastroenterol. 2007; 13:6492–7.

10. Yu W, Park KB, Chung HY, Kwon OK, Lee SS. Chronological changes of quality of life in long-term survivors after gastrectomy for gastric cancer. Cancer Res Treat. 2016; 48:1030–6.

11. Teng GG, Curtis JR, Saag KG. Mortality and osteoporotic fractures: is the link causal, and is it modifiable? Clin Exp Rheumatol. 2008; 26(5 Suppl 51):S125–37.

12. Yoo SH, Lee JA, Kang SY, Kim YS, Sunwoo S, Kim BS, et al. Risk of osteoporosis after gastrectomy in long-term gastric cancer survivors. Gastric Cancer. 2018; 21:720–7.

13. Oh HJ, Lim CH, Yoon BH, Yoon SB, Baeg MK, Kim WC, et al. Fracture after gastrectomy for gastric cancer: a long-term follow-up observational study. Eur J Cancer. 2017; 72:28–36.

14. Kanis J, Johnell O, Gullberg B, Allander E, Elffors L, Ranstam J, et al. Risk factors for hip fracture in men from southern Europe: the MEDOS study. Mediterranean Osteoporosis Study. Osteoporos Int. 1999; 9:45–54.

15. Kweon S, Kim Y, Jang MJ, Kim Y, Kim K, Choi S, et al. Data resource profile: the Korea National Health and Nutrition Examination Survey (KNHANES). Int J Epidemiol. 2014; 43:69–77.

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

17. Kim KM, Choi HS, Choi MJ, Chung HY. Calcium and vitamin D supplementations: 2015 position statement of the Korean Society for Bone and Mineral Research. J Bone Metab. 2015; 22:143–9.

18. Heiskanen JT, Kroger H, Paakkonen M, Parviainen MT, Lamberg-Allardt C, Alhava E. Bone mineral metabolism after total gastrectomy. Bone. 2001; 28:123–7.

19. Adachi Y, Shiota E, Matsumata T, Iso Y, Yoh R, Kitano S. Osteoporosis after gastrectomy: bone mineral density of lumbar spine assessed by dual-energy X-ray absorptiometry. Calcif Tissue Int. 2000; 66:119–22.

20. Eom BW, Kim J, Kim DH, Kim YI, Yoon HM, Cho SJ, et al. Recovery of food intake after gastrectomy for gastric cancer: based on a large-scale gastric cancer cohort. Dig Surg. 2018; 35:220–9.

21. Baek KH, Jeon HM, Lee SS, Lim DJ, Oh KW, Lee WY, et al. Short-term changes in bone and mineral metabolism following gastrectomy in gastric cancer patients. Bone. 2008; 42:61–7.

22. Recker RR. Calcium absorption and achlorhydria. N Engl J Med. 1985; 313:70–3.

23. Oh MG, Han MA, Park J, Ryu SY, Choi SW. The prevalence of vitamin D deficiency among cancer survivors in a nationwide survey of the Korean population. PLoS One. 2015; 10:e0129901.

24. Straatman J, Wiegel J, van der Wielen N, Jansma EP, Cuesta MA, van der Peet DL. Systematic review of exocrine pancreatic insufficiency after gastrectomy for cancer. Dig Surg. 2017; 34:364–70.

25. Jin J, Robinson AV, Hallowell PT, Jasper JJ, Stellato TA, Wilhem SM. Increases in parathyroid hormone (PTH) after gastric bypass surgery appear to be of a secondary nature. Surgery. 2007; 142:914–20.

26. Costa AG, Bilezikian JP. Bone turnover markers in primary hyperparathyroidism. J Clin Densitom. 2013; 16:22–7.

27. Stein EM, Carrelli A, Young P, Bucovsky M, Zhang C, Schrope B, et al. Bariatric surgery results in cortical bone loss. J Clin Endocrinol Metab. 2013; 98:541–9.

28. Duan Y, De Luca V, Seeman E. Parathyroid hormone deficiency and excess: similar effects on trabecular bone but differing effects on cortical bone. J Clin Endocrinol Metab. 1999; 84:718–22.

29. Cheng N, Green ME. Osteoporosis screening for men: are family physicians following the guidelines? Can Fam Physician. 2008; 54:1140–1.

30. Lee JE, Shin DW, Lee H, Son KY, Kim WJ, Suh YS, et al. Oneyear experience managing a cancer survivorship clinic using a shared-care model for gastric cancer survivors in Korea. J Korean Med Sci. 2016; 31:859–65.

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

32. Kochersberger G, Bales C, Lobaugh B, Lyles KW. Calcium supplementation lowers serum parathyroid hormone levels in elderly subjects. J Gerontol. 1990; 45:M159–62.

33. Cho S, Shin A, Song D, Park JK, Kim Y, Choi JY, et al. Validity of self-reported cancer history in the health examinees (HEXA) study: a comparison of self-report and cancer registry records. Cancer Epidemiol. 2017; 50:16–21.

34. Cho LY, Kim CS, Li L, Yang JJ, Park B, Shin A, et al. Validation of self-reported cancer incidence at follow-up in a prospective cohort study. Ann Epidemiol. 2009; 19:644–6.