Skip to main content
Gut logoLink to Gut
. 1998 Feb;42(2):188–194. doi: 10.1136/gut.42.2.188

Bone mineral density and nutritional status in children with chronic inflammatory bowel disease

A Boot 1, J Bouquet 1, E Krenning 1, Keizer- S M P F de Muinck 1
PMCID: PMC1726993  PMID: 9536942

Abstract

Background—Osteoporosis has been reported in adult patients with inflammatory bowel disease. 
Aims—To evaluate bone mineral density (BMD), nutritional status, and determinants of BMD in children with inflammatory bowel disease. 
Patients—Fifty five patients (34 boys and 21 girls, age range 4-18) were studied; 22 had Crohn's disease and 33 ulcerative colitis. 
Methods—Lumbar spine and total body BMD, and body composition were assessed by dual energy x ray absorptiometry (DXA). Results were expressed as standard deviation scores (SDS). Lean body mass was also assessed by bioelectrical impedance analysis (BIA). Yearly measurements during two years were performed in 21patients. 
Results—The mean SDS of lumbar spine BMD and total body BMD were significantly lower than normal (−0.75 and −0.95, both p<0.001). Height SDS and body mass index SDS were also decreased. The decrease in BMD SDS could not be explained by delay in bone maturation. The cumulative dose of prednisolone correlated negatively with lumbar spine BMD SDS (r=−0.32, p<0.02). Body mass index SDS correlated positively with total body BMD SDS (r=0.36, p<0.02). Patients with Crohn's disease had significantly lower lumbar spine and total body BMD SDS than patients with ulcerative colitis, even after adjustment for cumulative dose of prednisolone. In the longitudinal data cumulative dose of prednisolone between the measurements correlated negatively with the change in lumbar spine and total body BMD SDS. Lean tissue mass measured by DXA had a strong correlation with lean body mass measured by BIA (r=0.98). 
Conclusions—Children with inflammatory bowel disease have a decreased BMD. Children with Crohn's disease have a higher risk of developing osteopaenia than children with ulcerative colitis. Corticosteroid therapy and nutritional status are important determinants of BMD in these patients. 



Keywords: bone mineral density; inflammatory bowel disease; children; nutritional status; corticosteroid treatment; body composition

Full Text

The Full Text of this article is available as a PDF (135.8 KB).

Figure 1 .

Figure 1

Lumbar spine and total body BMD results of the first measurement in 55 patients with IBD. The continuous line represents the mean of reference values, the dotted lines +2 and 2 SD.

Figure 2 .

Figure 2

(A) Relation between lean tissue mass measured by DXA and lean body mass measured by BIA. The continuous line represents the regression line. (B) Difference between lean tissue mass by DXA and lean body mass by BIA against the mean for the two methods. LBM, lean body mass; LTM, lean tissue mass.

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Allgrove J. Biphosphonates. Arch Dis Child. 1997 Jan;76(1):73–75. doi: 10.1136/adc.76.1.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blumsohn A., Hannon R. A., Wrate R., Barton J., al-Dehaimi A. W., Colwell A., Eastell R. Biochemical markers of bone turnover in girls during puberty. Clin Endocrinol (Oxf) 1994 May;40(5):663–670. doi: 10.1111/j.1365-2265.1994.tb03019.x. [DOI] [PubMed] [Google Scholar]
  3. Boot A. M., Bouquet J., de Ridder M. A., Krenning E. P., de Muinck Keizer-Schrama S. M. Determinants of body composition measured by dual-energy X-ray absorptiometry in Dutch children and adolescents. Am J Clin Nutr. 1997 Aug;66(2):232–238. doi: 10.1093/ajcn/66.2.232. [DOI] [PubMed] [Google Scholar]
  4. Boot A. M., de Ridder M. A., Pols H. A., Krenning E. P., de Muinck Keizer-Schrama S. M. Bone mineral density in children and adolescents: relation to puberty, calcium intake, and physical activity. J Clin Endocrinol Metab. 1997 Jan;82(1):57–62. doi: 10.1210/jcem.82.1.3665. [DOI] [PubMed] [Google Scholar]
  5. Büller H. A., Maas S. M. Consensus inflammatoire darmziekte bij kinderen: colitis ulcerosa en ziekte van Crohn. Werkgroep Academisch Medisch Centrum, Amsterdam. Ned Tijdschr Geneeskd. 1996 Mar 9;140(10):544–550. [PubMed] [Google Scholar]
  6. Cohen-Solal M. E., Graulet A. M., Denne M. A., Gueris J., Baylink D., de Vernejoul M. C. Peripheral monocyte culture supernatants of menopausal women can induce bone resorption: involvement of cytokines. J Clin Endocrinol Metab. 1993 Dec;77(6):1648–1653. doi: 10.1210/jcem.77.6.8263153. [DOI] [PubMed] [Google Scholar]
  7. Compston J. E., Judd D., Crawley E. O., Evans W. D., Evans C., Church H. A., Reid E. M., Rhodes J. Osteoporosis in patients with inflammatory bowel disease. Gut. 1987 Apr;28(4):410–415. doi: 10.1136/gut.28.4.410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cowan F. J., Warner J. T., Dunstan F. D., Evans W. D., Gregory J. W., Jenkins H. R. Inflammatory bowel disease and predisposition to osteopenia. Arch Dis Child. 1997 Apr;76(4):325–329. doi: 10.1136/adc.76.4.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Finkelstein J. S., Neer R. M., Biller B. M., Crawford J. D., Klibanski A. Osteopenia in men with a history of delayed puberty. N Engl J Med. 1992 Feb 27;326(9):600–604. doi: 10.1056/NEJM199202273260904. [DOI] [PubMed] [Google Scholar]
  10. Genant H. K., Mall J. C., Wagonfeld J. B., Horst J. V., Lanzi L. H. Skeletal demineralization and growth retardation in inflammatory bowel disease. Invest Radiol. 1976 Nov-Dec;11(6):541–549. doi: 10.1097/00004424-197611000-00007. [DOI] [PubMed] [Google Scholar]
  11. Ghosh S., Cowen S., Hannan W. J., Ferguson A. Low bone mineral density in Crohn's disease, but not in ulcerative colitis, at diagnosis. Gastroenterology. 1994 Oct;107(4):1031–1039. doi: 10.1016/0016-5085(94)90227-5. [DOI] [PubMed] [Google Scholar]
  12. Griffiths A. M., Nguyen P., Smith C., MacMillan J. H., Sherman P. M. Growth and clinical course of children with Crohn's disease. Gut. 1993 Jul;34(7):939–943. doi: 10.1136/gut.34.7.939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Harries A. D., Brown R., Heatley R. V., Williams L. A., Woodhead S., Rhodes J. Vitamin D status in Crohn's disease: association with nutrition and disease activity. Gut. 1985 Nov;26(11):1197–1203. doi: 10.1136/gut.26.11.1197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hertel N. T., Stoltenberg M., Juul A., Main K. M., Müller J., Nielsen C. T., Lorenzen I., Skakkebaek N. E. Serum concentrations of type I and III procollagen propeptides in healthy children and girls with central precocious puberty during treatment with gonadotropin-releasing hormone analog and cyproterone acetate. J Clin Endocrinol Metab. 1993 Apr;76(4):924–927. doi: 10.1210/jcem.76.4.8473407. [DOI] [PubMed] [Google Scholar]
  15. Hokken-Koelega A. C., Hackeng W. H., Stijnen T., Wit J. M., de Muinck Keizer-Schrama S. M., Drop S. L. Twenty-four-hour plasma growth hormone (GH) profiles, urinary GH excretion, and plasma insulin-like growth factor-I and -II levels in prepubertal children with chronic renal insufficiency and severe growth retardation. J Clin Endocrinol Metab. 1990 Sep;71(3):688–695. doi: 10.1210/jcem-71-3-688. [DOI] [PubMed] [Google Scholar]
  16. Issenman R. M., Atkinson S. A., Radoja C., Fraher L. Longitudinal assessment of growth, mineral metabolism, and bone mass in pediatric Crohn's disease. J Pediatr Gastroenterol Nutr. 1993 Nov;17(4):401–406. doi: 10.1097/00005176-199311000-00012. [DOI] [PubMed] [Google Scholar]
  17. Jahnsen J., Falch J. A., Aadland E., Mowinckel P. Bone mineral density is reduced in patients with Crohn's disease but not in patients with ulcerative colitis: a population based study. Gut. 1997 Mar;40(3):313–319. doi: 10.1136/gut.40.3.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Johnson J., Dawson-Hughes B. Precision and stability of dual-energy X-ray absorptiometry measurements. Calcif Tissue Int. 1991 Sep;49(3):174–178. doi: 10.1007/BF02556113. [DOI] [PubMed] [Google Scholar]
  19. Kirschner B. S. Growth and development in chronic inflammatory bowel disease. Acta Paediatr Scand Suppl. 1990;366:98–105. doi: 10.1111/j.1651-2227.1990.tb11608.x. [DOI] [PubMed] [Google Scholar]
  20. Kirschner B. S., Sutton M. M. Somatomedin-C levels in growth-impaired children and adolescents with chronic inflammatory bowel disease. Gastroenterology. 1986 Oct;91(4):830–836. doi: 10.1016/0016-5085(86)90683-9. [DOI] [PubMed] [Google Scholar]
  21. Kirschner B. S., Voinchet O., Rosenberg I. H. Growth retardation in inflammatory bowel disease. Gastroenterology. 1978 Sep;75(3):504–511. [PubMed] [Google Scholar]
  22. Kruse K., Kracht U. Evaluation of serum osteocalcin as an index of altered bone metabolism. Eur J Pediatr. 1986 Apr;145(1-2):27–33. doi: 10.1007/BF00441848. [DOI] [PubMed] [Google Scholar]
  23. König A., Mühlbauer R. C., Fleisch H. Tumor necrosis factor alpha and interleukin-1 stimulate bone resorption in vivo as measured by urinary [3H]tetracycline excretion from prelabeled mice. J Bone Miner Res. 1988 Dec;3(6):621–627. doi: 10.1002/jbmr.5650030607. [DOI] [PubMed] [Google Scholar]
  24. Lukaski H. C., Johnson P. E., Bolonchuk W. W., Lykken G. I. Assessment of fat-free mass using bioelectrical impedance measurements of the human body. Am J Clin Nutr. 1985 Apr;41(4):810–817. doi: 10.1093/ajcn/41.4.810. [DOI] [PubMed] [Google Scholar]
  25. Lukert B. P., Raisz L. G. Glucocorticoid-induced osteoporosis: pathogenesis and management. Ann Intern Med. 1990 Mar 1;112(5):352–364. doi: 10.7326/0003-4819-112-5-352. [DOI] [PubMed] [Google Scholar]
  26. Martin T. J., Ng K. W., Nicholson G. C. Cell biology of bone. Baillieres Clin Endocrinol Metab. 1988 Feb;2(1):1–29. [PubMed] [Google Scholar]
  27. Mazess R. B., Barden H. S., Bisek J. P., Hanson J. Dual-energy x-ray absorptiometry for total-body and regional bone-mineral and soft-tissue composition. Am J Clin Nutr. 1990 Jun;51(6):1106–1112. doi: 10.1093/ajcn/51.6.1106. [DOI] [PubMed] [Google Scholar]
  28. Mazlam M. Z., Hodgson H. J. Peripheral blood monocyte cytokine production and acute phase response in inflammatory bowel disease. Gut. 1992 Jun;33(6):773–778. doi: 10.1136/gut.33.6.773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Motil K. J., Grand R. J., Davis-Kraft L., Ferlic L. L., Smith E. O. Growth failure in children with inflammatory bowel disease: a prospective study. Gastroenterology. 1993 Sep;105(3):681–691. doi: 10.1016/0016-5085(93)90883-e. [DOI] [PubMed] [Google Scholar]
  30. Motley R. J., Clements D., Evans W. D., Crawley E. O., Evans C., Rhodes J., Compston J. E. A four-year longitudinal study of bone loss in patients with inflammatory bowel disease. Bone Miner. 1993 Nov;23(2):95–104. doi: 10.1016/s0169-6009(08)80046-3. [DOI] [PubMed] [Google Scholar]
  31. Motley R. J., Crawley E. O., Evans C., Rhodes J., Compston J. E. Increased rate of spinal trabecular bone loss in patients with inflammatory bowel disease. Gut. 1988 Oct;29(10):1332–1336. doi: 10.1136/gut.29.10.1332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Patel S. Current and potential future drug treatments for osteoporosis. Ann Rheum Dis. 1996 Oct;55(10):700–714. doi: 10.1136/ard.55.10.700. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pigot F., Roux C., Chaussade S., Hardelin D., Pelleter O., Du Puy Montbrun T., Listrat V., Dougados M., Couturier D., Amor B. Low bone mineral density in patients with inflammatory bowel disease. Dig Dis Sci. 1992 Sep;37(9):1396–1403. doi: 10.1007/BF01296010. [DOI] [PubMed] [Google Scholar]
  34. Pintauro S. J., Nagy T. R., Duthie C. M., Goran M. I. Cross-calibration of fat and lean measurements by dual-energy X-ray absorptiometry to pig carcass analysis in the pediatric body weight range. Am J Clin Nutr. 1996 Mar;63(3):293–298. doi: 10.1093/ajcn/63.3.293. [DOI] [PubMed] [Google Scholar]
  35. Sambrook P., Birmingham J., Kelly P., Kempler S., Nguyen T., Pocock N., Eisman J. Prevention of corticosteroid osteoporosis. A comparison of calcium, calcitriol, and calcitonin. N Engl J Med. 1993 Jun 17;328(24):1747–1752. doi: 10.1056/NEJM199306173282404. [DOI] [PubMed] [Google Scholar]
  36. Scharla S. H., Minne H. W., Lempert U. G., Leidig G., Hauber M., Raedsch R., Ziegler R. Bone mineral density and calcium regulating hormones in patients with inflammatory bowel disease (Crohn's disease and ulcerative colitis). Exp Clin Endocrinol. 1994;102(1):44–49. doi: 10.1055/s-0029-1211264. [DOI] [PubMed] [Google Scholar]
  37. Silvennoinen J. A., Karttunen T. J., Niemelä S. E., Manelius J. J., Lehtola J. K. A controlled study of bone mineral density in patients with inflammatory bowel disease. Gut. 1995 Jul;37(1):71–76. doi: 10.1136/gut.37.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Silvennoinen J. Relationships between vitamin D, parathyroid hormone and bone mineral density in inflammatory bowel disease. J Intern Med. 1996 Feb;239(2):131–137. doi: 10.1046/j.1365-2796.1996.420765000.x. [DOI] [PubMed] [Google Scholar]
  39. Soliman A. T., Hassan A. E., Aref M. K., Hintz R. L., Rosenfeld R. G., Rogol A. D. Serum insulin-like growth factors I and II concentrations and growth hormone and insulin responses to arginine infusion in children with protein-energy malnutrition before and after nutritional rehabilitation. Pediatr Res. 1986 Nov;20(11):1122–1130. doi: 10.1203/00006450-198611000-00012. [DOI] [PubMed] [Google Scholar]
  40. Svendsen O. L., Haarbo J., Hassager C., Christiansen C. Accuracy of measurements of body composition by dual-energy x-ray absorptiometry in vivo. Am J Clin Nutr. 1993 May;57(5):605–608. doi: 10.1093/ajcn/57.5.605. [DOI] [PubMed] [Google Scholar]
  41. Tanner J. M., Whitehouse R. H. Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Arch Dis Child. 1976 Mar;51(3):170–179. doi: 10.1136/adc.51.3.170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Thomas A. G., Holly J. M., Taylor F., Miller V. Insulin like growth factor-I, insulin like growth factor binding protein-1, and insulin in childhood Crohn's disease. Gut. 1993 Jul;34(7):944–947. doi: 10.1136/gut.34.7.944. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Weststrate J. A., Deurenberg P., van Tinteren H. Indices of body fat distribution and adiposity in Dutch children from birth to 18 years of age. Int J Obes. 1989;13(4):465–477. [PubMed] [Google Scholar]
  44. van Persijn van Meerten E. L., Kroon H. M., Papapoulos S. E. Epi- and metaphyseal changes in children caused by administration of bisphosphonates. Radiology. 1992 Jul;184(1):249–254. doi: 10.1148/radiology.184.1.1609087. [DOI] [PubMed] [Google Scholar]

Articles from Gut are provided here courtesy of BMJ Publishing Group

RESOURCES