SciELO - Scientific Electronic Library Online

 
vol.29 número3Características físico-químicas y nutricionales de las dietas enterales caserasEfecto de lactobacillus casei shirota sobre concentraciones de urea en la enfermedad renal crónica índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados

Revista

Articulo

Indicadores

Links relacionados

  • En proceso de indezaciónCitado por Google
  • No hay articulos similaresSimilares en SciELO
  • En proceso de indezaciónSimilares en Google

Compartir


Nutrición Hospitalaria

versión On-line ISSN 1699-5198versión impresa ISSN 0212-1611

Nutr. Hosp. vol.29 no.3 Madrid mar. 2014

http://dx.doi.org/10.3305/NH.2014.29.3.7124 

ORIGINAL / Alimentos funcionales

 

Restriction of dairy products; a reality in inflammatory bowel disease patients

Restricción de productos lácteos; una realidad en pacientes con enfermedad inflamatoria intestinal

 

 

Mirella Brasil Lopes1, Raquel Rocha1, André Castro Lyra2, Vanessa Rosa Oliveira1, Fernanda Gomes Coqueiro1, Naiade Silveira Almeida1, Sandra Santos Valois1 and Genoile Oliveira Santana2

1Department of Sciences of Nutrition. School of Nutrition. Federal University of Bahia. Salvador. Bahia. Brazil.
2Gastroenterology Unit. University Hospital Professor Edgard Santos. Federal University of Bahia. Salvador. Bahia. Brazil.

Source of funding: Fundação de Amparo a Pesquisa do Estado da Bahia (FAPESB) and the National Counsel of Technological and Scientific Development (CNPq).

Correspondence

 

 


ABSTRACT

Introduction: Calcium deficiency is considered a risk factor for the development of osteoporosis in inflammatory bowel disease (IBD) patients. Various dietary restrictions, including milk products are reported by these patients.
Objective: To evaluate dairy product and dietary calcium intake by IBD patients.
Methods: This cross-sectional study enrolled 65 outpatients with IBD recruited from one reference center for IBD. A semi-structured questionnaire (to collect demographic, socioeconomic and clinical data) and a quantitative food frequency questionnaire were administered. With regard to clinical data, we evaluated the anthropometric nutritional status, the disease classification, the disease activity index and the presence of gastrointestinal symptoms. Selfreported modifications in the use of dairy products were evaluated.
Results: The IBD patients´ ages ranged from 20-75 years and 67.0% were diagnosed with ulcerative colitis. The majority (64.7%) reported restricting dairy products. The frequency of gastrointestinal symptoms was higher among the Crohn´s disease patients who restricted dairy products than among those with no restrictions (100% vs 42.9%; p = 0.013); this result was not observed among the UC (ulcerative colitis) patients. Disease activity was also more frequent in the IBD patients who restricted dairy products than in those with no restrictions (23.8% vs 4.5%; p = 0.031), and among the UC patients, extensive disease was more common in the patients who restricted dairy products than in those with no restrictions (42.9% vs 20.0%; p = 0.03).
Conclusion: Restricting dairy products is common among IBD patients, possibly due to disease activity, the presence of gastrointestinal symptoms and the extension of the disease.

Key words: Inflammatory bowel disease. Ulcerative colitis. Crohn's disease. Dairy products. Dietary calcium.


RESUMEN

Introducción: Se considera que la deficiencia de calcio es un factor de riesgo para el desarrollo de osteoporosis en pacientes con enfermedad inflamatoria intestinal (EII). En estos pacientes se han notificado diversas restricciones dietéticas.
Objetivo: Evaluar la ingesta de productos lácteos y calcio de la dieta en pacientes con EII.
Métodos: En este estudio cruzado se reclutaron 65 pacientes ambulatorios con EII procedentes de un centro de referencia para EII. Se administraron un cuestionario semi-estructurado (que recogía datos demográficos, socio-económicos y clínicos) y un cuestionario de frecuencia de consumo de alimento. Con respecto a los datos clínicos, evaluamos el estado nutricional antropométrico, la clasificación de la enfermedad, el índice de actividad de la enfermedad y la presencia de síntomas gastrointestinales. Se evaluaron las modificaciones auto-notificadas en el uso de los productos lácteos.
Resultados: Las edades de los pacientes con EII variaban entre los 20 y 75 años y el 67,0% fueron diagnosticados de colitis ulcerosa. La mayoría (64,7 %) notificaban una restricción de los productos lácteos. La frecuencia de síntomas gastrointestinales fue mayor en los pacientes con enfermedad de Crohn que restringían los productos lácteos que en aquellos que no lo hacían (100% frente a 42,9%; p = 0,013); este resultado no se observó en los pacientes con colitis ulcerosa CU. La actividad de la enfermedad también fue más frecuente en los pacientes con EII que restringían los productos lácteos que en aquellos sin restricción (23,8% frente a 4,5%; p = 0,031) y, en los pacientes con CU, la enfermedad extensa fue más habitual en pacientes que restringían los productos lácteos que en aquellos que no lo hacían (42,9 % frente a 20,0%; p = 0,03).
Conclusión: La restricción de productos lácteos es habitual en pacientes con EII, posiblemente debido a la actividad de la enfermedad, la presencia de síntomas gastrointestinales y la extensión de la enfermedad.

Palabras clave: Enfermedad inflamatoria intestinal. Colitis ulcerosa. Enfermedad de Crohn. Productos lácteos. Calcio de la dieta.


Abbreviations
IBD: Inflammatory bowel disease.
CD: Crohn´s disease.
UC: Ulcerative colitis.
BMI: Body Mass Index.
FFQ: food frequency questionnaire.

 

Introduction

Inflammatory bowel disease (IBD), mainly represented by Crohn´s disease (CD) and ulcerative colitis (UC), is a chronic inflammatory disorder associated with gastrointestinal and systemic complications.1 IBD has been a major gastroenterological problem in the Westernized world.2

Calcium deficiency, mainly as a result of steroid use, has been reported in both CD and UC patients.3 The development of osteoporosis and an increased risk of fractures are increasingly common in these patients.4 These problems become more severe when patients reduce the amount of calcium-rich foods they consume. This behavior is perpetuated by food beliefs in an attempt to control symptoms or to prevent the recurrence of the disease. Health professionals who advise restrictive diets also contribute to this deficiency.5

Between 1960 and 1970, some studies reported an improvement in symptoms and a lower likelihood of the recurrence of disease activity in UC patients who excluded dairy products from their diet. These results suggested that milk could be an important factor in the onset or exacerbation of UC,6,7 although the studies had methodological limitations.8

Considering the significant impact of calcium deficiency on bone health and patients´ quality of life, the objective of this study was to evaluate the intake of dairy products and dietary calcium by inflammatory bowel disease patients.

 

Materials and methods

Patients

This is a cross-sectional study conducted between September 2011 and March 2012 in the outpatient Gastroenterology and Nutrition Unit at Professor Edgar Santos University Hospital, Salvador, Bahia, Brazil. Sixty-five consecutive patients were included in this study. Informed consent was obtained from all the patients, and the Ethics Committee and the Institutional Review Board of the Professor Edgar Santos University Hospital approved the protocol of this study.

Inclusion and exclusion criteria

Patients were invited to participate in the study according to the following inclusion criteria: age over 18 years and a UC or CD diagnosis according to clinical, endoscopic, radiological and/or pathological study findings.9 The exclusion criteria were pregnancy, intestinal resection, malignant diseases, celiac disease, lactose intolerance, chronic renal failure and severe liver disease.

Demographic, socioeconomic, clinical and dietary data

The demographic and socioeconomic data included gender, age and education level. With regard to clinical data, we evaluated anthropometric nutritional status, the disease classification, the disease activity index and the presence of gastrointestinal symptoms (abdominal pain, bloating, nausea, vomiting, diarrhea, bloating and bloody stools). The dietary data comprised self-reported information about changes in the current consumption of dairy products (cow´s milk and derivatives) as well as the reasons for such changes.

For the CD patients, we applied the Harvey and Bradshaw index (1980),10 considering disease activity as a score ≥ 5 points. The Lichtiger index (1994)11 was used for UC patients, and active disease was defined as an index value ≥ 10 points. We applied the Montreal Classification for both CD and UC patients.12

The Body Mass Index (BMI) was used to describe the patients´ anthropometric nutritional status.13,14 The anthropometric measurements were taken by professionals who were experienced in taking these measurements. Body weight (kg) was measured twice with the patients wearing light clothes and no shoes. Weight was evaluated using a digital scale accurate to 100 g, and height (in centimeters) was measured with a stadiometer accurate to 0.5 cm.13

Evaluation of dietary data

The food frequency questionnaire (FFQ) was used in combination with a photo album for the assessment of the portions and average daily intake of dairy products and calcium (dietary calcium). This FFQ was validated for use in studies of interventions and/or prevention programs for chronic diseases.15

The consumption of dairy products was transformed into daily portions for the statistical analysis, and one serving or more per day was considered adequate intake.16 We analyzed information concerning the self-reported changes in the most recent consumption of dairy products (cow´s milk and derivatives) as well as the justifications for these changes. The reduction or exclusion of cow´s milk and derivatives or substitution with soy milk was considered dairy product restriction.

The average daily dietary calcium intake was calculated using the Personal Nutrition software (DietWin-Porto Alegre, Rio Grande do Sul, Brazil). Adequate calcium intake was defined as the equivalent of 800 mg per day for individuals from 19 to 50 years old of both genders, 800 mg per day for males 51 to 70 years old and 1000 mg per day for female subjects 51 to 70 years old.17 The calcium present in beverages, nutritional supplements and medications was not recorded in this study.

Statistical analysis

For the descriptive analysis, we calculated the means with standard deviations (mean ± SD) and medians with ranges for the continuous variables; we calculated the absolute and relative frequencies for the categorical variables. The differences between CD and UC patients with regard to calcium and dairy product intake, the restriction of dairy products and disease duration were analyzed with the Mann-Whitney test. The chi-square test or Fisher´s exact test was calculated to determine the strength of the association between two categorical variables. SPSS 15.0 software (SPSS, Chicago, IL, United States) was used for the statistical analyses. P < 0.05 was considered statistically significant.

 

Results

The patients´ mean age was 44.8 ± 13.5 years, and the mean disease duration was 7.2 ± 4.4 years. The age ranges of the men and the women were 20-61 years and 23-75 years, respectively. The majority were female (61.5%), and 72.0% had at least a high school education. Among the women, 45.0% were older than 50 years.

Of the IBD patients, 56.9% had adequate anthropometric nutritional status, and 30.8% were overweight. Of the patients evaluated, 89.2% were clinically in remission. Gastrointestinal symptoms were reported by 44.6% of the IBD patients. Bloating and bleeding were the main symptoms, reported by 20.5% (9/44) and 18.2% (8/44) of the UC patients, respectively. However, abdominal distension and abdominal pain were reported by 57.1% (12/21) and 33.3% (7/21) of the CD patients, respectively (data not shown). The demographic and medical characteristics of the Crohn´s disease and ulcerative colitis patients are shown in table I.

 

 

Modifications to the consumption of dairy products

Regarding the patients´ dietary characteristics, 52.3% of the patients reported some change in their consumption of dairy products after being diagnosed with IBD. The majority of the patients (64.7%) reported restricting cow´s milk and its derivatives (reducing or excluding these foods and substituting soy milk). The most common reason for this behavior was the exacerbation or onset of symptoms (45.5%), followed by guidance by health professionals (36.4%). Approximately 80.0% of the CD patients had seen a nutritionist (table II).

Consumption of dairy products and dietary calcium

The majority of IBD patients had low dairy product intake (52.0%) and inadequate dietary calcium intake (90.8%) (table II). Only three patients reported taking calcium supplements (data not shown).

There was no statistically significant difference in the intake of dairy products or dietary calcium between the CD and uC patients (P = 0.37 and P = 0.28, respectively) (table II).

Consumption of dairy products and demographic, anthropometric and clinical characteristics

No association was observed between the reported restriction of dairy products and age, gender, anthropometric status, disease duration or counseling from a nutritionist (P > 0.05). Among the CD patients, no association was found between the restriction of dairy products and the location and behavior of Crohn´s disease (P > 0.05). However, the frequency of gastrointestinal symptoms was higher among the CD patients who restricted dairy products compared with those with no restrictions (100% vs 42.9%; P = 0.013); the same result was not observed in UC patients (table III).

Disease activity was more frequent in the IBD patients who restricted dairy products than in those with no restrictions (23.8% vs 4.5%; P = 0.031). Among the UC patients, extensive disease was more frequent among the patients who restricted dairy products than among those with no restrictions (42.9% vs 20.0%; P = 0.03) (table III).

 

Discussion

In our study, the majority of IBD patients reported having changed their dairy product intake after being diagnosed with IBD, and the majority had low dairy product intake and inadequate dietary calcium intake. The restriction of dairy products seems to be associated with gastrointestinal symptoms and the activity and extension of the disease in these patients.

During active disease, the restriction of dairy products is common among IBD patients.18 Among the factors associated with the restriction of dairy products, the presence of gastrointestinal symptoms, the desire to relieve symptoms, food beliefs and dietary advice are most strongly related.5,18,19 However, in prospective studies, no association was found between dairy product intake and an increased frequency of disease relapse.5,20

In this study, the extensive form of the disease in UC patients seems to be associated with the restriction of dairy products. However, Jowett and colleagues (2004) found the same association in a group of UC patients.5 One possible explanation for our findings is that gastrointestinal symptoms are related to active disease and the extensive form of the disease in UC patients. Thus, the restriction of dairy products could be attributable to the spread of information among patients and health professionals about the occurrence of lactose intolerance in IBD patients.

Although no association was found between dairy product restriction and counseling from a nutritionist, the recommendation of a health professional is another factor that has encouraged these individuals to restrict their dairy product intake.5 The fact that some IBD patients, most commonly CD patients, may develop lactose intolerance contributes to the prescription of this nutritional restriction. Some factors must be evaluated before the patient restricts dairy products, such as the fat present in these foods,21,22 the amount of lactose consumed, the residual activity of intestinal lactase, the ability of the colonic flora to ferment lactose and individual sensitivity to the products of lactose fermentation.23

Some patients have replaced dairy products with soy milk. However, it is known that soy milk products are usually enriched with tricalcium phosphate. This fortificant has the best sensory characteristics, however, the calcium bioavailability is lower compared with cow´s milk and other fortificants such as calcium carbonate.24-27 Therefore, soy milk does not seem to be a good option as a rich source of bioavailable calcium, and recommendations for the intake of foods rich in calcium need to be part of the treatment for IBD patients if dairy product restriction is recommended for some reason. In addition, dairy products are poor sources of lactose and can be consumed by patients with lactose intolerance. They are not only rich sources of calcium but also sources of other micronutrients such as B complex vitamins.

Low dietary calcium intake is already common among the Brazilian population.25 The mean daily dietary calcium intake among adults is 476.4 mg for females and 546.4 mg for males, and the prevalence of inadequacy among females and males is 90.7% and 83.8%, respectively.28 The decrease in dietary calcium intake is clinically important in IBD patients, particularly those treated with steroids, postmenopausal women and the elderly because they have a higher risk of developing osteoporosis29 and fractures.30,31 Adequate dietary calcium intake is one of the preventive measures to reduce osteoporosis in IBD patients.32 The minimum recommended daily intake of calcium for the prevention of fractures in IBD patients is 1,000 mg and for postmenopausal women and men over the age of 55 years, the recommendation is 1,200 mg.33

This study has some limitations, such as the sample size, the absence of a control group and the fact that patients who agree to participate in this type of study may have different eating habits. In addition, dietary restrictions could be associated with other medical conditions not evaluated in this study. Nevertheless, some of the results were similar to other studies, but prospective studies are still necessary to confirm the findings.

In summary, the restriction of dairy products and reduced dietary calcium intake are evident in IBD patients. These restrictions are mainly influenced by gastrointestinal symptoms and the activity and extension of the disease. Even in the absence of conclusive data on the frequency of lactose intolerance in these patients and the advancements in the knowledge about the absence of an association between diet and the exacerbation of symptoms or disease activity, restrictive diets are still a reality and may contribute to the compromised nutritional status of IBD patients. However, we must investigate other possible diagnoses that can cause gastrointestinal symptoms and address the complaints of the patients more thoroughly.

 

Acknowledgements

The FAPESB/CNPq had no involvement in the study design; the collection, analysis and interpretation of the data; the writing of the manuscript; or the decision to submit the manuscript for publication.

 

References

1. Kirsner JB. Historical origins of current IBD concepts. Historical origins of current IBD concepts. World J Gastroenterol 2001; 7 (2): 175-84.         [ Links ]

2. Ekbom A. The Epidemiology of IBD. Inflamm Bowel Dis 2004; (10 Suppl. 1): S32-4.         [ Links ]

3. Van Hogezand RA, Hamdy NA. Skeletal morbidity in inflammatory bowel disease. Scand J Gastroenterol Suppl 2006; 41 (243): 59-64.         [ Links ]

4. Bernstein CN, Blanchard JF, Leslie W, Wajda A, Yu BN. The incidence of fracture among patients with inflammatory bowel disease. Ann Intern Med 2000; 133 (10): 795-9.         [ Links ]

5. Jowett SL, Seal CJ, Phillips E, Gregory W, Barton JR, Welfare MR. Dietary beliefs of people with ulcerative colitis and their effect on relapse and nutrient intake. Clin Nutr 2004; 23 (2): 161-70.         [ Links ]

6. Truelove SC. Ulcerative colitis provoked by milk. Br Med J 1961; 1 (5220): 154-60.         [ Links ]

7. Wright R, Truelove SC. A controlled therapeutic trial of various diets in ulcerative colitis. Br Med J 1965; 2 (5454): 138-41.         [ Links ]

8. Taxonera C, Mendoza JL. Consumo de lácteos y enfermedad inflamatoria intestinal: ¿invertir la tendencia? An Med Interna 2004; 21 (5): 209-11.         [ Links ]

9. Bernstein CN, Fried M, Krabshuis JH, Cohen H, Eliakim R, Fedail S, Gearry R, Goh KL, Hamid S, Khan AG, LeMair AW, Malfertheiner, Ouyang Q, Rey JF, Sood A, Steinwurz F, Thomsen OO, Thomson A, Watermeyer G. World Gastroenterology Organization Practice Guidelines for the Diagnosis and Management of IBD in 2010. Inflamm Bowel Dis 2010; 16 (1): 112-24.         [ Links ]

10. Harvey RF, Bradshaw JM. A simple index of Crohn´s-disease activity. Lancet 1980; 1 (8167): 514.         [ Links ]

11. Lichtiger S, Present DH, Kornbluth A, Gelernt I, Bauer J, Galler G, Michelassi F, Hanauer S. Cyclosporine in severe ulcerative colitis refractory to steroid therapy. N Engl J Med 1994; 330 (26): 1841-5.         [ Links ]

12. Silverberg MS, Satsangi J, Ahmad T, Arnott ID, Bernstein CN, Brant SR, Caprilli R, Colombel JF, Gasche C, Geboes K, Jewell DP, Karban A, Loftus EV Jr, Peña AS, Riddell RH, Sachar DB, Schreiber S, Steinhart AH, Targan SR, Vermeire S, Warren BF. Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: report of a Working Party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol 2005; 19 (Suppl. A): 5A-36A.         [ Links ]

13. World Health Organization. Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. World Health Organ Tech Rep Ser 1995; 854: 1-452.         [ Links ]

14. Nutrition Screening Initiative. Incorporating Nutrition Screening and Interventions into Medical Practice. A monograph for phycicians. The Nutrition Screening Initiative. Washington (DC): The American Dietetic Association; 1994.         [ Links ]

15. Ribeiro AB, Cardoso MA. Development of a food frequency questionnaire as a tool for programs of chronic diseases prevention. Rev Nutr 2002; 15: 239-45.         [ Links ]

16. Harvard School of Public Health. The Nutrition Source. Healthy Eating Plate. Available from: URL: http://www.hsph.harvard.edu/nutritionsource/healthy-eating-plate.         [ Links ]

17. Ross AC, Manson JE, Abrams SA, Aloia JF, Brannon PM, Clinton SK, Durazo-Arvizu RA, Gallagher JC, Gallo RL, Jones G, Kovacs CS, Mayne ST, Rosen CJ, Shapses SA. The 2011 Report on Dietary Reference Intakes for Calcium and Vitamin D from the Institute of Medicine: What Clinicians Need to Know. J Clin Endocrinol Metab 2011; 96 (1): 53-8.         [ Links ]

18. Ripoli J, Miszputen SJ, Ambrogini Jr O, Carvalho Ld. Nutritional follow-up of patients with ulcerative colitis during periods of intestinal inflammatory activity and remission. Arq Gastroenterol 2010; 47 (1): 49-55.         [ Links ]

19. Zallot C, Quilliot D, Chevaux JB, Peyrin-Biroulet C, Guéant-Rodriguez RM, Freling E, Collet-Fenetrier B, Williet N, Ziegler O, Bigard MA, Guéant JL, Peyrin-Biroulet L. Dietary Beliefs and Behavior Among Inflammatory Bowel Disease Patients. Inflamm Bowel Dis 2012; 19 (1): 66-72.         [ Links ]

20. Jowett SL, Seal CJ, Pearce MS, Phillips E, Gregory W, Barton JR, Welfare MR. Influence of dietary factors on the clinical course of ulcerative colitis: a prospective cohort study. Gut 2004; 53 (10): 1479-84.         [ Links ]

21. Triggs CM, Munday K, Hu R, Fraser AG, Gearry RB, Barclay ML, Ferguson LR. Dietary factors in chronic inflammation: Food tolerances and intolerances of a New Zealand Caucasian Crohn´s disease population. Mutat Res 2010; 690 (1-2): 123-38.         [ Links ]

22. Nolan-Clark D, Tapsell LC, Hu R, Han DY, Ferguson LR. Effects of Dairy Products on Crohn´s Disease Symptoms Are Influenced by Fat Content and Disease Location but not Lactose Content or Disease Activity Status in a New Zealand Population. J Am Diet Assoc 2011; 111 (8): 1165-72.         [ Links ]

23. Vonk RJ, Priebe MG, Koetse HA, Stellaard F, Lenoir-Wijnkoop I, Antoine JM, Zhong Y, Huang CY. Lactose intolerance: analysis of underlying factors. Eur J Clin Invest 2003; 33 (1): 70-5.         [ Links ]

24. Heaney RP, Dowell MS, Raferty K, Bierman J. Bioavailability of the calcium in fortified soy imitation milk, with some observations on method. Am J Clin Nutr 2000; 71 (5): 1166-9.         [ Links ]

25. Cheung AL, Wilcox G, Walker KZ, Shah NP, Strauss B, Ashton JF, Stojanovska L. Fermentation of calcium-fortified soya milk does not appear to enhance acute calcium absorption in osteopenic post-menopausal women. Br J Nutr 2011; 105 (2): 282-6.         [ Links ]

26. Zhao Y, Martin BR, Weaver CM. Calcium bioavailability of calcium carbonate fortified soymilk is equivalent to cow´s milk in young women. J Nutr 2005; 135 (10): 2379-8232.         [ Links ]

27. Tang AL, Walker KZ, Wilcox G, Strauss BJ, Ashton JF, Stojanovska L. Calcium absorption in Australian osteopenic post-menopausal women: an acute comparative study of fortified soymilk to cows´ milk. Asia Pac J Clin Nutr 2010; 19 (2): 243-9.         [ Links ]

28. Pesquisa de Orçamentos Familiares 2008-2009: analise do consumo alimentar pessoal no Brasil / IBGE, Coordenação de Trabalho e Rendimento. - Rio de Janeiro: IBGE. 150p (Internet). 2011 (acess 2012 maio 31). Disponivel em: eli://www.ibge.gov.br/home/eliacaoa/eliacao/condicaodevida/pof/2008_2009_analise_consumo/pofanalise_2008_2009.pdf.         [ Links ]

29. Targownik LE, Leslie WD, Carr R, Clara I, Miller N, Rogala L, Graff LA, Walker JR, Bernstein CN. Longitudinal Change in Bone Mineral Density in a Population-Based Cohort of Patients with Inflammatory Bowel Disease. Calcif Tissue Int 2012; 91 (5): 356-63.         [ Links ]

30. Bernstein CN, Blanchard JF, Leslie W, Wajda A, Yu BN. The incidence of fracture among patients with inflammatory bowel disease. Ann Intern Med 2000; 133 (10): 795-9.         [ Links ]

31. Ananthakrishnan AN, McGinley EL, Binion DG, Saeian K. Fracture-associated hospitalizations in patients with inflammatory bowel disease. Dig Dis Sci 2011; 56 (1): 176-82.         [ Links ]

32. Weaver CM, Proulx WR, Heaney R. Choices for achieving adequate dietary calcium with a vegetarian diet. Am J Clin Nutr 1999; 70 (Suppl. 3): 543S-548S.         [ Links ]

33. Lewis NR, Scott BB. Guidelines for osteoporosis in inflammatory bowel disease and coeliac disease. London (UK): British Society of Gastroenterology, 2007.         [ Links ]

 

 

Correspondence:
Raquel Rocha.
Avenida Araújo Pinho, 32. Canela.
CEP: 40.110-150. Salvador - Bahia - Brazil.
E-mail: raquelrocha2@yahoo.com.br

Recibido: 8-XI-2013.
Aceptado: 8-XII-2013.

Creative Commons License Todo el contenido de esta revista, excepto dónde está identificado, está bajo una Licencia Creative Commons