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Original Article

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Vitamin D Deficiency in a Portuguese Cohort of Patients with Inflammatory Bowel Disease: Prevalence and Relation to Disease Activity

Branco J.C. · Cardoso M.F. · Anapaz V. · Lourenço L.C. · Oliveira A.M. · Rodrigues C.G. · Santos L. · Reis J.A.

Author affiliations

Serviço de Gastrenterologia, Hospital Professor Doutor Fernando Fonseca, Amadora, Portugal

Corresponding Author

Dr. Joana C. Branco

Serviço de Gastrenterologia

Hospital Professor Doutor Fernando Fonseca

PT–19 2720-276 Amadora, Lisboa (Portugal)

E-Mail cbranco.joana@gmail.com

Keywords: Crohn diseaseDisease activityEpidemiologyInflammatory bowel diseaseUlcerative colitisVitamin D

Related Articles for ""
GE Port J Gastroenterol 2019;26:155–162
https://doi.org/10.1159/000488744

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Abstract

Background and Aims: Vitamin D deficiency is more common in inflammatory bowel disease (IBD) patients than in the general population. However, there are conflicting data about predictive factors of vitamin D deficiency and its potential association with disease activity. The aims of this study were to determine the prevalence and predictive factors of vitamin D deficiency and to evaluate a possible association with disease activity. Methods: A prospective observational study was conducted, including patients with IBD from January to July 2016. The Endocrine Society guidelines were considered for defining levels of serum 25-hydroxyvitamin D (25-OH-D) as follows: deficient (< 20 ng/mL, < 10 ng/mL being severe deficiency), insufficient (21–29 ng/mL), and adequate (> 30 ng/mL). Results: A total of 152 patients (52% men; 47.2 ± 17.3 years) were included, of whom 70% had Crohn’s disease (CD). Thirty-seven percent of patients were on immunosuppressors and 17% were on biologics. The majority were outpatients (88.2%). Mean 25-OH-D levels were 17.1 ± 8 ng/mL (CD: 16.7 ± 8 ng/mL vs. ulcerative colitis: 17.6 ± 7 ng/mL, p = 0.1). Inadequate levels were present in 90.8% of patients (deficiency: 68.4%; insufficiency: 22.4%). A significant negative correlation between 25-OH-D levels and age (r = –0.2, p = 0.04), C-reactive protein (CRP) levels (r = –0.22, p = 0.004), and Harvey-Bradshaw index (HBi) (r = –0.32, p = 0.001) was found. Patients with severe deficiency showed a higher CRP (0.6 vs. 1.4 mg/dL, p = 0.03), erythrocyte sedimentation rate (ESR) (22 vs. 31 mm/h, p = 0.03), and HBi (2 vs. 5, p < 0.001) and lower hemoglobin (13.6 vs. 12.7 g/dL, p = 0.02). There was no association between vitamin D deficiency and gender, type, extent, and duration of disease, surgery, and other measures of disease activity, such as ESR, hemoglobin (these 2 items except for severe deficiency), fecal calprotectin, or Truelove and Witts classification. Conclusions: There is a high prevalence of inadequate levels of vitamin D in IBD patients, particularly deficiency (68.4%). There seems to exist an association between lower levels of vitamin D and higher disease activity, especially in CD.

© 2018 Sociedade Portuguesa de Gastrenterologia Published by S. Karger AG, Basel

Deficiência de vitamina D numa coorte de doentes Portugueses com doença inflamatória intestinal: prevalência e relação com a atividade da doença

Palavras Chave

Doença de Crohn · Atividade da doença · Epidemiologia · Doença inflamatória do intestino · Vitamina D ·

Resumo

Introdução: A deficiência de vitamina D é mais comum na doença inflamatória intestinal (DII) que na população geral. Contudo, existem dados controversos sobre fatores preditivos da deficiência de vitamina D e a potencial associação com a atividade da doença. Os objetivos deste estudo foram determinar a prevalência e fatores preditivos da deficiência de vitamina D e aferir possível associação à atividade da doença. Métodos: Desenhou-se um estudo observacional prospetivo incluindo doentes com DII entre janeiro e julho/2016. Foram consideradas as orientações da The Endocrine Society para definir níveis de 25-hidroxivitamina D (25-OH-D) sérica como: deficientes (c; 20 ng/mL, sendo c;10 ng/mL deficiência grave [DG]), insuficientes (21–29 ng/mL) e adequados (e; 30 ng/mL). Resultados: Foram incluídos 152 doentes (52% homens; 47.2 ± 17.3 anos), dos quais 70% com Doença de Crohn (DC). Do total, 37% estavam medicados com immunossupressores e 17% com biológicos. A maioria (88.2%) estava em ambulatório. O nível sérico de 25-OH-D foi 17.1 ± 8 ng/mL (DC: 16.7 ± 8 ng/mL vs. Colite ulcerosa: 17.6 ± 7 ng/mL, p = 0.1). Verificaram-se níveis inadequados em 90.8% (deficiência: 68.4%; insuficiência: 22.4%). Registou-se correlação negativa significativa entre níveis de 25-OH-D e idade (r = –0.2, p = 0.04), proteína C-reativa (PCR) (r = –0.22, p = 0.004) e índice Harvey-Bradshaw (iHB) (r = –0.32, p = 0.001). Doentes com DG apresentaram níveis mais elevados de PCR (0.6 vs. 1.4 mg/dL, p = 0.03), velocidade de sedimentação (VS) (22 vs. 31 mm/h, p = 0.03) e iHB (2 vs. 5, p c; 0.001), e mais baixos de hemoglobina (13.6 vs. 12.7 g/dL, p = 0.02). Não se verificou associação entre deficiência de vitamina D e sexo, tipo, extensão e duração da doença, cirurgia, e outras medidas de atividade da doença como VS, hemoglobina (estas duas exceto para DG), calprotectina fecal ou classificação Truelove e Witts. Conclusões: Registou-se prevalência alta de níveis inadequados de vitamina D na DII, particularmente de deficiência (68.4%). Parece existir associação entre níveis mais baixos de vitamina D e maior atividade da doença, nomeadamente na DC.



Related Articles:

References

  1. Holick M, Binkley N, Bischoff-Ferrari HA, Gordon C, Hanley D, Heaney R, et al: Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metab 2011; 96: 1911–1930.
  2. Cashman K, Dowling K, Skrabáková Z, Gonzalez-Gross M, Valtuena J, De Henauw S, et al: Vitamin D deficiency in Europe: pandemic? Am J Clin Nutr 2016; 103: 1033–1044.
  3. Bettencourt A, Boleixa D, Reis J, Oliveira JC, Mendonça D, Costa PP, et al: Serum 25-hydroxyvitamin D levels in a healthy population from the North of Portugal. J Steroid Biochem Mol Biol 2018; 175: 97–101.
  4. Hossein-Nezhad A, Holick MF: Vitamin D for heath: a global perspective. Mayo Clin Proc 2013; 88: 720–755.
  5. Abraham C, Cho JH: Inflammatory bowel disease. N Engl J Med 2009; 361: 2066–2078.
  6. Castro FD, Magalhães J, Carvalho PB, Moreira MJ, Mota P, Cotter J: Lower levels of vitamin D correlate with clinical disease activity and quality of life in inflammatory bowel disease. Arq Gastroenterol 2015; 52: 260–265.
  7. Santos-Antunes J, Nunes AC, Lopes S, Macedo G: The relevance of vitamin D and antinuclear antibodies in patients with inflammatory bowel disease under anti-TNF treatment: a prospective study. Inflamm Bowel Dis 2016; 22: 1101–1106.
  8. Frigstad SO, Hoivik M, Jahnsen J, Dahl SR, Cvancarova M, Grimstad T: Vitamin D deficiency in inflammatory bowel disease: prevalence and predictors in a Norwegian outpatient population. Scand J Gastroenterol 2017; 52: 100–106.
  9. Ulitsky A, Ananthakrishnan AN, Naik A, et al: Vitamin D deficiency in patients with inflammatory bowel disease: association with disease activity and quality of life. JPEN J Parenter Enteral Nutr 2011; 35: 308–316.
  10. Siffledeen JS, Siminoski K, Steinhart H, et al: The frequency of vitamin D deficiency in adults with Crohn’s disease. Can J Gastroenterol 2003; 17: 473–478.
  11. Silvennoinen J: Relationships between vitamin D, parathyroid hormone and bone mineral density in inflammatory bowel disease. J Intern Med 1996; 239: 131–137.
  12. Sadeghian M, Saneei P, Siassi F, et al: Vitamin D status in relation to Crohn’s disease: meta-analysis of observational studies. Nutrition 2016; 32: 505–514.
  13. Suibhne TN, Cox G, Healy M, et al: Vitamin D deficiency in Crohn’s disease: prevalence, risk factors and supplement use in an outpatient setting. J Crohns Colitis 2012; 6: 182–188.
  14. Mouli VP, Ananthakrishnan AN: Review article: vitamin D and inflammatory bowel diseases. Aliment Pharmacol Ther 2014; 39: 125–136.
  15. Del Pinto R, Pietropaoli D, Chandar AK, Ferri C, Cominelli F: Association between inflammatory bowel disease and vitamin D deficiency: a systematic review and meta-analysis. Inflamm Bowel Dis 2015; 21: 2708–2717.
  16. Ulitsky A, Ananthakrishnan AN, Naik A, et al: Vitamin D deficiency in patients with inflammatory bowel disease: association with disease activity and quality of life. JPEN J Parenter Enteral Nutr 2011; 35: 308–316.
  17. Jorgensen SP, Hvas CL, Agnholt J, et al: Active Crohn’s disease is associated with low vitamin D levels. J Crohns Colitis 2013; 7:e407–e413.
  18. Dumitrescu G, Mihai C, Dranga M, Prelipcean CC: Serum 25-hydroxyvitamin D concentration and inflammatory bowel disease characteristics in Romania. World J Gastroenterol 2014; 20: 2392–2396.
  19. Ham M, Longhi MS, Lahiff C, Cheifetz A, Robson S, Moss AC: Vitamin D levels in adults with Crohn’s disease are responsive to disease activity and treatment. Inflamm Bowel Dis 2014; 20: 856–860.
  20. Tan B, Li P, Lv H, Li Y, Wang O, Xing XP, et al: Vitamin D levels and bone metabolism in Chinese adult patients with inflammatory bowel disease. J Dig Dis 2014; 15: 116–123.
  21. Kabbani TA, Koutroubakis IE, Schoen RE, Ramos-Rivers C, Shah N, Swoger J, et al: Association of vitamin D level with clinical status in inflammatory bowel disease: a 5-year longitudinal study. Am J Gastroenterol 2016; 111: 712–719.
  22. Tajika M, Matsuura A, Nakamura T, et al: Risk factors for vitamin D deficiency in patients with Crohn’s disease. J Gastroenterol 2004; 39: 527–533.
  23. Hassan V, Hassan S, Seyed-Javad P, Ahmad K, Asieh H, Maryam S, Farid F, Siavash A: Association between serum 25 (OH) vitamin D concentrations and inflammatory bowel diseases (IBDs) activity. Med J Malaysia 2013; 68: 34–38.
  24. Fu YT, Chatur N, Cheong-Lee C, Salh B: Hypovitaminosis D in adults with inflammatory bowel disease: potential role of ethnicity. Dig Dis Sci 2012; 57: 2144–2148.
  25. Gomollón F, Dignass A, Annese V, Tilg H, Van Assche G, Lindsey J, et al: 3rd European evidence-based consensus on the diagnosis and management of Crohn’s disease 2016: part 1: diagnosis and medical management. J Crohns Colitis 2017; 11: 3–25.
  26. Magro F, Gionchetti P, Eliakim R, Ardizzone S, Armuzzi A, Barreiro-de-Acosta M, et al: Third European evidence-based consensus on diagnosis and management of ulcerative colitis. Part 1: Definitions, diagnosis, extra-intestinal manifestations, pregnancy, cancer surveillance, surgery and ileo-anal pouch disorders. J Crohns Colitis 2017; 11: 649–670.
  27. Limketkai BN, Mullin GE, Limsui D, Parian AM: Role of vitamin D in inflammatory bowel disease. Nutr Clin Pract 2017; 32: 337–345.
  28. Priett B, Treiber G, Pieber TR, Amrein K: Vitamin D and immune function. Nutrients 2013; 5: 2502–2521.
  29. Holick MF: Vitamin D deficiency. N Engl J Med 2007; 357: 266–281.
  30. Battault S, Whiting SJ, Peltier SL, Sadrin S, Gerber G, Maixent JM: Vitamin D metabolism, functions and needs: from science to health claims. Eur J Nutr 2013; 52: 429–441.
  31. Hewison M, Gacad MA, Lemire J, Adams JS: Vitamin D as a cytokine and hematopoetic factor. Rev Endocr Metab Disord 2001; 2: 217–227.
  32. Adams JS, Hewison M: Update in vitamin D. J Clin Endocrinol Metab 2010; 95: 471–478.
  33. Shah D, Gupta P: Vitamin D deficiency: is the pandemic for real? Indian J Community Med 2015; 40: 215–217.
  34. Manson JE, Brannon PM, Rosen CJ, Taylor CL: Vitamin D deficiency – is there really a pandemic? N Engl J Med 2016; 375: 1817–1820.
  35. Jorgensen SP, Agnholt J, Glerup H, Lyhne S, Villadsen GE, Hvas CL, et al: Clinical trial: vitamin D3 treatment in Crohn’s disease – a randomized double-blind placebo-controlled study. Aliment Pharmacol Ther 2010; 32: 377–383.
  36. Miheller P, Muzes G, Hritz I, Lakatos G, Pregun I, Lakatos PL, et al: Comparison of the effects of 1,25 dihydroxyvitamin D and 25 hydroxyvitamin D on bone pathology and disease activity in Crohn’s disease patients. Inflamm Bowel Dis 2009; 15: 1656–1662.
  37. Yang L, Weaver V, Smith JP, Bingaman S, Hartman TJ, Cantorna MT: Therapeutic effect of vitamin D supplementation in a pilot study of Crohn’s patients. Clin Transl Gastroenterol 2013; 4:e33.
  38. Raftery T, Martineau AR, Greiller CL, Ghosh S, McNamara D, Bennett K, et al: Effects of vitamin D supplementation on intestinal permeability, cathelicidin and disease markers in Crohn’s disease: results from a randomised double-blind placebo-controlled study. United European Gastroenterol J 2015; 3: 294–302.
  39. Garg M, Rosella O, Rosella G, Wu Y, Lubel JS, Gibson PR: Evaluation of a 12-week targeted vitamin D supplementation regimen in patients with active inflammatory bowel disease. Clin Nutr 2017, DOI: 10.1016/j.clnu.2017.06.011.
  40. Harbord M, Annese V, Vavricka SR, Allez M, Barreiro-de-Acosta M, Boberg KM, et al: The first European evidence-based consensus on extraintestinal manifestations in inflammatory bowel disease. J Crohns Colitis 2016; 10: 239–254.

Article / Publication Details

First-Page Preview
Abstract of Original Article

Received: January 12, 2018
Accepted: March 18, 2018
Published online: May 14, 2018
Issue release date: May - June

Number of Print Pages: 8
Number of Figures: 0
Number of Tables: 4

ISSN: 2341-4545 (Print)
eISSN: 2387-1954 (Online)

For additional information: https://www.karger.com/PJG

References

  1. Holick M, Binkley N, Bischoff-Ferrari HA, Gordon C, Hanley D, Heaney R, et al: Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metab 2011; 96: 1911–1930.
  2. Cashman K, Dowling K, Skrabáková Z, Gonzalez-Gross M, Valtuena J, De Henauw S, et al: Vitamin D deficiency in Europe: pandemic? Am J Clin Nutr 2016; 103: 1033–1044.
  3. Bettencourt A, Boleixa D, Reis J, Oliveira JC, Mendonça D, Costa PP, et al: Serum 25-hydroxyvitamin D levels in a healthy population from the North of Portugal. J Steroid Biochem Mol Biol 2018; 175: 97–101.
  4. Hossein-Nezhad A, Holick MF: Vitamin D for heath: a global perspective. Mayo Clin Proc 2013; 88: 720–755.
  5. Abraham C, Cho JH: Inflammatory bowel disease. N Engl J Med 2009; 361: 2066–2078.
  6. Castro FD, Magalhães J, Carvalho PB, Moreira MJ, Mota P, Cotter J: Lower levels of vitamin D correlate with clinical disease activity and quality of life in inflammatory bowel disease. Arq Gastroenterol 2015; 52: 260–265.
  7. Santos-Antunes J, Nunes AC, Lopes S, Macedo G: The relevance of vitamin D and antinuclear antibodies in patients with inflammatory bowel disease under anti-TNF treatment: a prospective study. Inflamm Bowel Dis 2016; 22: 1101–1106.
  8. Frigstad SO, Hoivik M, Jahnsen J, Dahl SR, Cvancarova M, Grimstad T: Vitamin D deficiency in inflammatory bowel disease: prevalence and predictors in a Norwegian outpatient population. Scand J Gastroenterol 2017; 52: 100–106.
  9. Ulitsky A, Ananthakrishnan AN, Naik A, et al: Vitamin D deficiency in patients with inflammatory bowel disease: association with disease activity and quality of life. JPEN J Parenter Enteral Nutr 2011; 35: 308–316.
  10. Siffledeen JS, Siminoski K, Steinhart H, et al: The frequency of vitamin D deficiency in adults with Crohn’s disease. Can J Gastroenterol 2003; 17: 473–478.
  11. Silvennoinen J: Relationships between vitamin D, parathyroid hormone and bone mineral density in inflammatory bowel disease. J Intern Med 1996; 239: 131–137.
  12. Sadeghian M, Saneei P, Siassi F, et al: Vitamin D status in relation to Crohn’s disease: meta-analysis of observational studies. Nutrition 2016; 32: 505–514.
  13. Suibhne TN, Cox G, Healy M, et al: Vitamin D deficiency in Crohn’s disease: prevalence, risk factors and supplement use in an outpatient setting. J Crohns Colitis 2012; 6: 182–188.
  14. Mouli VP, Ananthakrishnan AN: Review article: vitamin D and inflammatory bowel diseases. Aliment Pharmacol Ther 2014; 39: 125–136.
  15. Del Pinto R, Pietropaoli D, Chandar AK, Ferri C, Cominelli F: Association between inflammatory bowel disease and vitamin D deficiency: a systematic review and meta-analysis. Inflamm Bowel Dis 2015; 21: 2708–2717.
  16. Ulitsky A, Ananthakrishnan AN, Naik A, et al: Vitamin D deficiency in patients with inflammatory bowel disease: association with disease activity and quality of life. JPEN J Parenter Enteral Nutr 2011; 35: 308–316.
  17. Jorgensen SP, Hvas CL, Agnholt J, et al: Active Crohn’s disease is associated with low vitamin D levels. J Crohns Colitis 2013; 7:e407–e413.
  18. Dumitrescu G, Mihai C, Dranga M, Prelipcean CC: Serum 25-hydroxyvitamin D concentration and inflammatory bowel disease characteristics in Romania. World J Gastroenterol 2014; 20: 2392–2396.
  19. Ham M, Longhi MS, Lahiff C, Cheifetz A, Robson S, Moss AC: Vitamin D levels in adults with Crohn’s disease are responsive to disease activity and treatment. Inflamm Bowel Dis 2014; 20: 856–860.
  20. Tan B, Li P, Lv H, Li Y, Wang O, Xing XP, et al: Vitamin D levels and bone metabolism in Chinese adult patients with inflammatory bowel disease. J Dig Dis 2014; 15: 116–123.
  21. Kabbani TA, Koutroubakis IE, Schoen RE, Ramos-Rivers C, Shah N, Swoger J, et al: Association of vitamin D level with clinical status in inflammatory bowel disease: a 5-year longitudinal study. Am J Gastroenterol 2016; 111: 712–719.
  22. Tajika M, Matsuura A, Nakamura T, et al: Risk factors for vitamin D deficiency in patients with Crohn’s disease. J Gastroenterol 2004; 39: 527–533.
  23. Hassan V, Hassan S, Seyed-Javad P, Ahmad K, Asieh H, Maryam S, Farid F, Siavash A: Association between serum 25 (OH) vitamin D concentrations and inflammatory bowel diseases (IBDs) activity. Med J Malaysia 2013; 68: 34–38.
  24. Fu YT, Chatur N, Cheong-Lee C, Salh B: Hypovitaminosis D in adults with inflammatory bowel disease: potential role of ethnicity. Dig Dis Sci 2012; 57: 2144–2148.
  25. Gomollón F, Dignass A, Annese V, Tilg H, Van Assche G, Lindsey J, et al: 3rd European evidence-based consensus on the diagnosis and management of Crohn’s disease 2016: part 1: diagnosis and medical management. J Crohns Colitis 2017; 11: 3–25.
  26. Magro F, Gionchetti P, Eliakim R, Ardizzone S, Armuzzi A, Barreiro-de-Acosta M, et al: Third European evidence-based consensus on diagnosis and management of ulcerative colitis. Part 1: Definitions, diagnosis, extra-intestinal manifestations, pregnancy, cancer surveillance, surgery and ileo-anal pouch disorders. J Crohns Colitis 2017; 11: 649–670.
  27. Limketkai BN, Mullin GE, Limsui D, Parian AM: Role of vitamin D in inflammatory bowel disease. Nutr Clin Pract 2017; 32: 337–345.
  28. Priett B, Treiber G, Pieber TR, Amrein K: Vitamin D and immune function. Nutrients 2013; 5: 2502–2521.
  29. Holick MF: Vitamin D deficiency. N Engl J Med 2007; 357: 266–281.
  30. Battault S, Whiting SJ, Peltier SL, Sadrin S, Gerber G, Maixent JM: Vitamin D metabolism, functions and needs: from science to health claims. Eur J Nutr 2013; 52: 429–441.
  31. Hewison M, Gacad MA, Lemire J, Adams JS: Vitamin D as a cytokine and hematopoetic factor. Rev Endocr Metab Disord 2001; 2: 217–227.
  32. Adams JS, Hewison M: Update in vitamin D. J Clin Endocrinol Metab 2010; 95: 471–478.
  33. Shah D, Gupta P: Vitamin D deficiency: is the pandemic for real? Indian J Community Med 2015; 40: 215–217.
  34. Manson JE, Brannon PM, Rosen CJ, Taylor CL: Vitamin D deficiency – is there really a pandemic? N Engl J Med 2016; 375: 1817–1820.
  35. Jorgensen SP, Agnholt J, Glerup H, Lyhne S, Villadsen GE, Hvas CL, et al: Clinical trial: vitamin D3 treatment in Crohn’s disease – a randomized double-blind placebo-controlled study. Aliment Pharmacol Ther 2010; 32: 377–383.
  36. Miheller P, Muzes G, Hritz I, Lakatos G, Pregun I, Lakatos PL, et al: Comparison of the effects of 1,25 dihydroxyvitamin D and 25 hydroxyvitamin D on bone pathology and disease activity in Crohn’s disease patients. Inflamm Bowel Dis 2009; 15: 1656–1662.
  37. Yang L, Weaver V, Smith JP, Bingaman S, Hartman TJ, Cantorna MT: Therapeutic effect of vitamin D supplementation in a pilot study of Crohn’s patients. Clin Transl Gastroenterol 2013; 4:e33.
  38. Raftery T, Martineau AR, Greiller CL, Ghosh S, McNamara D, Bennett K, et al: Effects of vitamin D supplementation on intestinal permeability, cathelicidin and disease markers in Crohn’s disease: results from a randomised double-blind placebo-controlled study. United European Gastroenterol J 2015; 3: 294–302.
  39. Garg M, Rosella O, Rosella G, Wu Y, Lubel JS, Gibson PR: Evaluation of a 12-week targeted vitamin D supplementation regimen in patients with active inflammatory bowel disease. Clin Nutr 2017, DOI: 10.1016/j.clnu.2017.06.011.
  40. Harbord M, Annese V, Vavricka SR, Allez M, Barreiro-de-Acosta M, Boberg KM, et al: The first European evidence-based consensus on extraintestinal manifestations in inflammatory bowel disease. J Crohns Colitis 2016; 10: 239–254.
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