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Biochemical Markers of Bone Metabolism in Children with Helicobacter pylori Infection

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Abstract

We investigated the biochemical markers of bone metabolism in children with Helicobacter pylori infection. Biochemical markers of bone metabolism and serum levels of vitamin B12, ferritin and estradiol were measured in 41 H. pylori-positive (+) children (23 girls, 18 boys; aged 11.8±3 years). Serum levels of intact parathyroid hormone, ß-collagen I carboxy terminal telopeptide, total alkaline phosphatase (ALP), bone-specific ALP, N-terminal cross-links of human procollagen type I, N-mid-osteocalcin, calcium, phosphate, ferritin, and estradiol did not differ significantly between H. pylori(+) and H. pylori negative (−) children. Vitamin B12 levels were significantly decreased in H. pylori(+) compared to H. pylori(−) children. H. pylori infection was not accompanied by significant changes in markers of bone metabolism in children, although vitamin B12 levels were decreased. Further studies are required to clarify whether H. pylori infection causes time-dependent changes in bone turnover markers during the long course of this inflammatory disease.

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References

  1. Consensus Development Conference (Peck WA, Chairman) (1993) Diagnosis, prophylaxis and treatment of osteoporosis. Am J Med 94:646–650

    Article  Google Scholar 

  2. NIH (2001) NIH Consensus Development Panel on Osteoporosis, Prevention, Diagnosis, and Therapy. JAMA 285:785–795

    Article  Google Scholar 

  3. Boonen S, Autier P, Barette M, Vanderschueren D, Lips P, Haentjens P (2004) Functional outcome and quality of life following hip fracture in elderly women: A prospective controlled study. Osteoporos Int 15:87–94

    Article  PubMed  CAS  Google Scholar 

  4. Rusinska A, Chlebna-Sokoł D (2005) Evaluation of interleukin-1 and -6 in the etiopathogenesis of idiopathic osteoporosis and osteopenia in children. Arch Immunol Ther Exp 53:257–265

    CAS  Google Scholar 

  5. Campos LMA, Liphaus BL, Silva CAA, Pereira RMR (2003) Osteoporosis in childhood and adolescence. J Pediatr 79:481–482

    Google Scholar 

  6. Bonjour JP, Rizzoli R (1996) Bone acquisition in adolescence. In: Marcus R, Feldman D, Kelsey J (eds) Osteoporosis. Academic Press, San Diego, pp 465–476

    Google Scholar 

  7. Marshall BJ, Warren JR (1984) Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1:1311–1315

    Article  PubMed  CAS  Google Scholar 

  8. Olbe L, Fandriks L, Hamlet A, Svennerholm AM, Thoreson AC (2000) Mechanisms involved in Helicobacter pylori induced duodenal ulcer disease:an overview. World J Gastroenterol 6:619–623

    PubMed  CAS  Google Scholar 

  9. Forman D, Newell DG, Fullerton F, Yarnell JW, Stacey AR, Wald N, Sitas F (1991) Association between infection with Helicobacter pylori and risk of gastric cancer: evidence from a prospective investigation. BMJ 302:1302–1305

    Article  PubMed  CAS  Google Scholar 

  10. Nomura A, Stemmermann GN, Chyou PH, Kato I, Perez-Perez GI, Blaser MJ (1991) Helicobacter pylori infection and gastric carcinoma among Japanese Americans in Hawaii. N Engl J Med 325:1132–1136

    Article  PubMed  CAS  Google Scholar 

  11. Parsonnet J, Friedman GD, Vandersteen DP, Chang Y, Vogelman JH, Orentreich N, Sibley RK (1991) Helicobacter pylori infection and the risk of gastric carcinoma. N Engl J Med 325:1127–1131

    Article  PubMed  CAS  Google Scholar 

  12. Taylor DN, Parsonnet J (1995) Epidemiology and natural history of Helicobacter pylori infection. In: Blaser MJ, Smith PD, Ravdin JI (eds) Infections of the gastrointestinal tract. Raven Press, New York, pp 551–563

    Google Scholar 

  13. Graham DY, Malaty HM, Evans DG, Evans DJJr, Klein PD, Adam E (1991) Epidemiology of Helicobacter pylori in an asymptomatic population in the United States. Effect of age, race and socioeconomic status. Gastroenterology 100:1495–1501

    PubMed  CAS  Google Scholar 

  14. Blaser MJ, Atherton JC (2004) Helicobacter pylori persistence: biology and disease. J Clin Invest 113:321–333

    Article  PubMed  CAS  Google Scholar 

  15. Shuval-Sudai O, Granot E (2003) An association between Helicobacter pylori infection and serum vitamin B12 levels in healthy adults. J Clin Gastroenterol 36:130–133

    Article  PubMed  CAS  Google Scholar 

  16. Serin E, Gumurdulu Y, Ozer B, Kayaselcuk F, Yilmaz U, Kocak R (2002) Impact of Helicobacter pylori on the development of vitamin B12 deficiency in the absence of gastric atrophy. Helicobacter 7:337–341

    Article  PubMed  Google Scholar 

  17. Annibale B, Capurso G, Delle Fave G (2002) Consequences of Helicobacter pylori infection on the absorption of micronutrients. Dig Liver Dis 34(Suppl 2):S72–S77

    Article  PubMed  CAS  Google Scholar 

  18. Richter T, Richter T, List S, Müller DM, Deutscher J, Uhlig HH, Krumbiegel P, Herbarth O, Gutsmuths FJ, Kiess W (2001) Five- to 7-year-old children with Helicobacter pylori infection are smaller than Helicobacter-negative children: a cross-sectional population-based study of 3,315 children. J Pediatr Gastroenterol Nutr 33:472–475

    Article  PubMed  CAS  Google Scholar 

  19. Demir H, Saltik IN, Kocak N, Yuce A, Ozen H, Gurakan F (2001) Subnormal growth in children with Helicobacter pylori infection. Arch Dis Child 84:89–90

    Article  PubMed  CAS  Google Scholar 

  20. Bravo LE, Mera R, Reina JC, Pradilla A, Alzate A, Fontham E (2003) Impact of Helicobacter pylori infection on growth of children: a prospective cohort study. J Pediatr Gastroenterol Nutr 37:614–619

    Article  PubMed  Google Scholar 

  21. Guiraldes E, Duarte I, Pea A, Godoy A, Espinosa MN, Bravo R, Larrain F, Schultz M, Harris P (2001) Proinflammatory cytokine expression in gastric tissue from children with Helicobacter pylori-associated gastritis. J Pediatr Gastroenterol Nutr 33:127–132

    Article  PubMed  CAS  Google Scholar 

  22. Fan XG, Chua A, Fan XJ, Keeling PW (1995) Increased gastric production of interleukin-8 and tumour necrosis factor in patients with Helicobacter pylori infection. J Clin Pathol 48:133–136

    PubMed  CAS  Google Scholar 

  23. Figura N, Gennari L, Merlotti D, Lenzi C, Campagna S, Franci B, Lucani B, Trabalzini L, Bianciardi L, Gonnelli C, Santucci A, Nut A (2005) Prevalence of Helicobacter pylori infection in male patients with osteoporosis and controls. Dig Dis Sci 50:847–852

    Article  PubMed  CAS  Google Scholar 

  24. Dixon MF, Genta RM, Yardley JH, Correa P (1996) Classification and grading of gastritis: the Updated Sydney System. Am J Surg Pathol 20:1161–1181

    Article  PubMed  CAS  Google Scholar 

  25. Natale VM, Filho WJ, Duarte AJS (1997) Does the secretion of cytokines in the periphery reflect their role in bone metabolic diseases? Mech Age Dev 94:14–23

    Article  Google Scholar 

  26. Ershler WB, Harman SM, Keller ET (1997) Immunologic aspects of osteoporosis. Dev Comp Immunol 21:487–499

    Article  PubMed  CAS  Google Scholar 

  27. Holloway WR, Collier FM, Aitken CJ, Myers DE, Hodge JM, Malakellis M, Gough TJ, Collier GR, Nicholson GC (2002) Leptin inhibits osteoclast generation. J Bone Miner Res 17:200–209

    Article  PubMed  CAS  Google Scholar 

  28. Angeletti RH, D’Amico T, Ashok S, Russell J (1998) The chemokine interleukin- 8 regulates parathyroid secretion. J Bone Miner Res 13:1232–1237

    Article  PubMed  CAS  Google Scholar 

  29. Gur A, Denli A, Nas K, Cevik R, Karakoc M, Sarac AJ, Erdogan F (2002) Possible pathogenetic role of new cytokines in postmenopausal osteoporosis and changes during calcitonin plus calcium therapy. Rheumatol Int 22:194–198

    Article  PubMed  CAS  Google Scholar 

  30. Crabtree JE, Shallcross TM, Heatley RV, Wyatt JI (1991) Mucosal tumor necrosis factor alpha and interleukin-6 in patients with Helicobacter pylori associated gastritis. Gut 32:1473–1477

    PubMed  CAS  Google Scholar 

  31. Harris PR, Mobley HL, Perez-Perez GI, Blaser MJ, Smith PD (1996) Helicobacter pylori urease is a potent stimulus of mononuclear phagocyte activation and inflammatory cytokine production. Gastroenterology 111:419–425

    Article  PubMed  CAS  Google Scholar 

  32. Ashorn M, Ruuska T, Karikoski R, Valipakka J, Maki M (1994) Gastric mucosal densities in Helicobacter pylori-positive and -negative dyspeptic children and healthy controls. J Pediatr Gastroenterol Nutr 18:146–151

    Article  PubMed  CAS  Google Scholar 

  33. Ashorn M (1995) What are the specific features of Helicobacter pylori gastritis in children? Ann Med 27:617–620

    PubMed  CAS  Google Scholar 

  34. Lopes AI, Quiding-Jarbrink M, Palha A, Ruivo J, Monteiro L, Oleastro M, Santos A, Fernandes A (2005) Cytokine expression in pediatric Helicobacter pylori infection. Clin Diag Lab Immun 12:994–1002

    Article  CAS  Google Scholar 

  35. Bontems P, Robert F, Van Gossum A, Cadranel S, Mascart F (2003) Helicobacter pylori modulation of gastric and duodenal mucosal T cell cytokine secretions in children compared with adults. Helicobacter 8:216–226

    Article  PubMed  CAS  Google Scholar 

  36. Kutukculer N, Aydogdu S, Goksen D, Caglayan S, Yagci RV (1997) Increased mucosal inflammatory cytokines in children with Helicobacter pylori-associated gastritis. Acta Paediatr 86:928–931

    PubMed  CAS  Google Scholar 

  37. Luzza F, Parrello T, Sebkova L, Pensabene L, Imeneo M, Mancuso M, La Vecchia AM, Monteleone G, Strisciuglio P, Pallone F (2001) Expression of proinflammatory and Th1 but not Th2 cytokines is enhanced in gastric mucosa of Helicobacter pylori infected children. Dig Liver Dis 33:14–20

    Article  PubMed  CAS  Google Scholar 

  38. Shimizu T, Haruna H, Ohtsuka Y, Kaneko K, Gupta R, Yamashiro Y (2004) Cytokines in the gastric mucosa of children with Helicobacter pylori infection. Acta Paediatr 93:322–326

    Article  PubMed  CAS  Google Scholar 

  39. Daughaday WH (2000) Growth hormone axis overview-somatomedin hypothesis. Pediatr Nephrol 14:537–540

    Article  PubMed  CAS  Google Scholar 

  40. Baricevic I, Nedic O, Nikolic JA, Bojic B, Jojic N (2004) Circulating insulin-like growth factors in patients infected with Helicobacter pylori. Clin Biochem 37:997–1001

    Article  PubMed  CAS  Google Scholar 

  41. Canalis E, Lian JB (1988) Effects of bone associated growth factors on DNA, collagen and osteocalcin synthesis in cultured fetal rat calvariae. Bone 9:243–246

    Article  PubMed  CAS  Google Scholar 

  42. Choe YH, Kim SK, Hong YC (2000) Helicobacter pylori infection with iron deficiency anaemia and subnormal growth at puberty. Arch Dis Child 82:136–140

    Article  PubMed  CAS  Google Scholar 

  43. Yang YJ, Sheu BS, Lee SC, Yang HB, Wu JJ (2005) Children of Helicobacter pylori-infected dyspeptic mothers are predisposed to H. pylori acquisition with subsequent iron deficiency and growth retardation. Helicobacter 10:249–255

    Article  PubMed  Google Scholar 

  44. Sipponen P, Laxen F, Huotari K, Harkonen M (2003) Prevalence of low vitamin B12 and high homocysteine in serum in an elderly male population: association with atrophic gastritis and Helicobacter pylori infection. Scand J Gastroenterol 38:1209–1216

    Article  PubMed  CAS  Google Scholar 

  45. Annibale B, Lahner E, Bordi C, Martino G, Caruana P, Grossi C, Negrini R, Delle Fave G (2000) Role of Helicobacter pylori infection in pernicious anemia. Digest Liver Dis 32:756– 762

    Article  CAS  Google Scholar 

  46. Kim GS, Kim CH, Park JY, Lee KU, Park CS (1996) Effects of vitamin B-12 on cell proliferation and cellular alkaline phosphatase activity in human bone marrow stromal osteoprogenitor cells and UMR106 osteoblastic cells. Metabolism 45:1443–1446

    Article  PubMed  CAS  Google Scholar 

  47. Carmel R, Lau KH, Baylink DJ, Saxena S, Singer FR (1988) Cobalamin and osteoblast-specific proteins. N Engl J Med 319:70–75

    Article  PubMed  CAS  Google Scholar 

  48. Del Corral A, Carmel R (1990) Transfer of cobalamin from the cobalamin-binding protein of egg-yolk to R binder of human saliva and gastric juice. Gastroenterology 98:1460–1466

    PubMed  CAS  Google Scholar 

  49. Appelmelk BJ, Simoons-Smit I, Negrrini R, Moran AP, Aspinall GO, Forte JG, De Vries T, Quan H, Verboom T, Maaskant JJ, Ghiara P, Kuipers EJ, Bloemena E, Tadema TM, Townsend RR, Tyagarajan K, Crothers JMJr, Monteiro MA, Savio A, De Graaff J (1996) Potential role of molecular mimicry between Helicobacter pylori lipopolysaccharide and host Lewis blood group antigens in autoimmunity. Infect Immun 64:2031–2040

    PubMed  CAS  Google Scholar 

  50. Janulaityte-Gunther D, Kucinskiene R, Kupcinskas L, Pavilonis A, Labanauskas L, Cizauskas A, Schmidt U, Wadstrom T, Andersen LP (2005) The humoral immune response to Helicobacter pylori infection in children with gastrointestinal symptoms. FEMS Immun Med Microbiol 44:205–212

    Article  CAS  Google Scholar 

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Acknowledgments

This study was supported by the Akdeniz University Research Projects Unit. The authors thank Dr. Levent Donmez for his contribution in data analysis.

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Correspondence to Sebahat Ozdem.

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Ozdem, S., Akcam, M., Yilmaz, A. et al. Biochemical Markers of Bone Metabolism in Children with Helicobacter pylori Infection. Dig Dis Sci 52, 967–972 (2007). https://doi.org/10.1007/s10620-006-9292-0

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  • DOI: https://doi.org/10.1007/s10620-006-9292-0

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