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Open access Original research BMJNPH: first published as 10.1136/bmjnph-2018-000022 on 19 March 2019. Downloaded from : no difference in and products consumption in comparison with controls

Fabiana Zingone,1 Paola Iovino,2 Cristina Bucci,2 Carolina Ciacci‍ ‍ 2

1Department of Surgery, Abstract What this paper adds Oncology and , Background Nutritional deficiencies are common University of Padua, Padova, in patients with coeliac disease and they can cause ►► The damaged intestinal mucosa in coeliac disease Italy osteopenia among other associated diseases. Reduced 2Celiac Center, AOU San may cause intolerance. consumption of milk and dairy products may play a major Giovanni di Dio e Ruggi ►► Patients on a gluten-free diet frequently claim lac- role in determining low bone mass in patients with coeliac diAragona, University of Salerno, tose intolerance and therefore avoid milk and dairy disease. Department of , products. Surgery, and Dentistry Scuola Aim We aimed to investigate milk and dairy products ►► We found that 22.2% of the patients with CeD and consumption in patients with coeliac disease compared Medica Salernitana, Salerno, 19.9% controls do not drink fluid milk on a regular Italy with the general population. basis. Methods We examined the average consumption of milk ►► Lactose-free milk is chosen by 20.4% of patients Correspondence to and dairy products and the reasons for not consuming with CeD and 19% of the controls. Dr Carolina Ciacci, Universita them. An online survey was sent by email to patients with degli Studi di Salerno, Fisciano ►► In our study we describe that there is no significant coeliac disease on a gluten-free diet and aged 18–75. 84084, Italy; cciacci@​ ​unisa.it​ difference between patients with coeliacdiseaseand Matched controls were selected among volunteers who controls in regular milk consumption- Follow-up responded to the survey posted on the public access visits for patients with coeliac disease could avoid Received 10 December 2018 sites. Differences in frequencies and means between the unnecessary dietary restrictions. Revised 22 January 2019 two groups were calculated using the χ2 test and t-test, Accepted 26 January 2019 respectively. All tests were two-tailed with a significance level set at p<0.05. abdominal pain and distension, borborygmi, Results 176 patients with coeliac disease and 528 controls participated in the study. We found that 22.2% of flatus and diarrhoea induced by bacterial http://nutrition.bmj.com/ metabolism of undigested lactose in dairy prod- the patients with coeliac disease and 19.9% of controls 1 did not drink fluid milk on a regular basis; lactose-free ucts. In untreated coeliac disease (CeD), the milk was preferred by 20.4% of the patients with coeliac damaged intestinal mucosa may have reduced disease and by 19% of controls (p=0.69). Only a minority the activity, causing lactose intoler- of patients with coeliac disease contacted a doctor before ance in those subjects. However, previous data having lactose-free milk, despite this being led by the suggest that also patients with CeD on a gluten- presence of gastrointestinal symptoms. More patients with free diet frequently claim lactose intolerance 2 coeliac disease than the general population reported a and therefore avoid milk and dairy products. on September 27, 2021 by guest. Protected copyright. breath test before avoiding milk and dairy products. Recently, it has been demonstrated that there is Conclusions There is no significant difference between no association between the type of adult hypo- patients with coeliac disease and controls in regular milk 3 consumption. Follow-up visits for patients with coeliac lactasia gene mutations and CeD. Milk avoid- disease could avoid unnecessary dietary restrictions. ance in patients with CeD may depend on the fact that lactose intolerance is determined not only by the expression of lactase gene but also Introduction by the dose of lactose, intestinal flora, gastro- Milk and dairy products contain lactose, a intestinal motility, small intestinal bacterial © Author(s) (or their made of and . overgrowth and sensitivity of the gastrointes- employer(s)) 2019. Re-use The absorption of lactose by the intestine tinal tract to the generation of gas and other permitted under CC BY-NC. No requires a brush border named lactase products of lactose digestion4 commercial re-use. See rights and permissions. Published by that carries out the hydrolyses of the disaccha- and other unidentified factors. BMJ. ride to its , which easily cross Milk avoidance and consequent reduction of To cite: Zingone F, Iovino P, the small bowel mucosa. Lactase activity decays the intake of calcium is claimed to be one of the Bucci C, et al. bmjnph Epub during childhood in the majority of human possible causes of osteopenia frequently found 5–7 ahead of print: [please include populations leading to adult-type hypolac- in patients with CeD. Recently, we showed Day Month Year]. doi:10.1136/ tasia.1 Lactose intolerance related to primary that 22.2% (260/1173) of the population from bmjnph-2018-000022 or secondary lactase deficiency may cause Southern Italy avoid milk consumption and

Zingone F, et al. bmjnph 2019;0:1–4. doi:10.1136/bmjnph-2018-000022 1 BMJ Nutrition, Prevention & Health BMJNPH: first published as 10.1136/bmjnph-2018-000022 on 19 March 2019. Downloaded from

18.1% (213/1173) drink lactose-free milk, even though Table 2 Consumption of fluid milk in our study population among this only 10.3% had undergone a breath test for lactose tolerance, with positive results in 5.5% of the popu- Patients General with coeliac population, N P lation. The reasons for milk avoidance were mainly gastro- disease, N (%) (%) value intestinal symptoms and the belief in its somewhat toxic effect on health.8 Do not drink milk 39 (22.2) 105 (19.9) 0.69 The present study aimed to investigate, using the same Milk with lactose 101 (57.4) 322 (61.0) survey of the previous study,8 the milk and dairy products Lactose-free milk 36 (20.4) 101 (19.1) consumption in patients with CeD compared with the general population. survey was sent by email to 317 patients with CeD on a gluten-free diet for at least 6 months. Consent was obtained Methods as part of a study dealing with vitamin D levels, bone mass As previously reported,8 we used an online survey investi- and nutrition in CeD funded by a grant from the advocacy gating the average consumption of milk and dairy prod- group Fondazione Celiachia (Italy). Patients specifically ucts and the reasons for not consuming them. The survey accepted to participate in the related online studies. consisted of 16 questions, and we calculated an average We selected controls from the general population who time of 5 min to complete it. The small number of ques- responded to the survey that was posted on the public access tions and short answering time were devised to provide the sites as reported elsewhere8 creating two groups matched best adherence and results. by gender, age and type of job and selecting three controls Subjects aged 18–75 years and living in Campania (South for each patient with CeD. Italy) were invited to answer the questionnaire online. The Categorical variables were expressed as frequency, contin- uous variables as mean±SD. Differences in frequencies and means between the two groups were calculated using the Table 1 Study population characteristics χ2 test and t-test, respectively. Covariates included sex, age Patients with General (18–35, 35–49, 50–75), body mass index (BMI, kg/m2), clas- coeliac disease, population, N (%) P sified as underweight ( 18.5), normal weight (>18.5–25), N (%) 176 528 value ≤ overweight (>25–30) and obese (>30), job type (classified Ethnicity as student, housewife, low-class, middle-class and high-  Caucasian 100 % 100% – class job based on average salary, retired and unemployed)  Female 129 (73.3) 389 (73.7) 0.43 and weekly physical activity. We chose the above covariates Age at test 37.7±10.8 39.1±12.7 0.19 because they may be associated with dietary restrictions and http://nutrition.bmj.com/ (mean±SD) gastrointestinal symptoms like .9–12 Body mass index All tests were two-tailed with a significance level set at p<0.05.  ≤18 5 (2.8) 16 (3.0) 0.1 The data were analysed with STATA V.12. A biomedical stat-  18.1–25 137 (77.8) 382 (72.3) istician performed the statistical review of the study. We have followed the Strengthening the Reporting of Observa-  25.1–30 27 (15.4) 80 (15.2) tional Studies in EpidemiologySTROBE guidelines for this  >30 7 (4.0) 50 (9.5) study. Job on September 27, 2021 by guest. Protected copyright.  Student 25 (14.2) 85 (16.1) 0.9  Housewife 13 (7.4) 28 (5.3) Results  Low-class job 14 (8.0) 45 (8.5) Forty-three of the 317 emails bounced back because of the incorrect email address or server problems; 176 out of 274  Middle-class job 39 (22.1) 120 (22.7) patients with CeD (64.2 %) responded to all questions of  High-class job 70 (39.8) 201 (38.1) the survey and were included in the study; 528 matched  Retired 5 (2.8) 18 (3.4)  Unemployed 10 (5.7) 31 (5.9) Table 3 How much milk do you drink per day? Physical activity Patients W alk 30 mins daily 26 (14.8) 97 (18.4) 0.51 with coeliac General  Practice sport 12 (6.8) 48 (9.1) disease, N population, N once a week (%) total 137 (%) total 423 P value  Practice sport 43 (24.4) 131 (24.8) 1 L 0 5 (1.2) 0.22 more than twice a 0.5 L 5 (3.6) 14 (3.3) week 250 mL (large cup) 68 (49.6) 230 (54.4)  Physical 12 (6.8) 26 (4.9) demanding job 150 mL (medium cup) 49 (35.8) 123 (29.1) No sport activities 83 (47.2) 226 (42.8) 50 mL (small cup) 15 (11.0) 51 (12.0)

2 Zingone F, et al. bmjnph 2019;0:1–4. doi:10.1136/bmjnph-2018-000022 BMJ Nutrition, Prevention & Health BMJNPH: first published as 10.1136/bmjnph-2018-000022 on 19 March 2019. Downloaded from

Table 4 Why do you drink lactose-free milk? undergone a breath test for lactose tolerance with posi- tive results (table 5). However, more patients with CeD Patients than the general population reported a breath test before with coeliac General disease, N population, N avoiding milk and dairy products. (%) total 36 (%) total 101 P value When considering only dairy products consumption, no patient with CeD and only 6 (1.1%) controls state that Doctor’s advice 2 (5.5) 13 (12.9) 0.5 they do not eat dairy products on a regular basis, with Friends 1 (2.8) 6 (5.9) most of them eating these products at least once a week My choice 18 (50) 47 (46.6) (table 6). Subjects who rarely drank dairy products manly GI problems 15 (41.7) 35 (34.6) consumed lactose-free mozzarella, , yoghurt or only parmesan cheese (table 6).

Table 5 Lactose intolerance test Patients with coeliac General Discussion disease, N population, N Our study shows that there is no significant difference (%) (%) P value between the patients with CeD and matched controls in the regular milk consumption. Never 145 (82.4) 474 (89.8) 0.002 This is, to our best knowledge, the first study investi- Negative test 19 (10.8) 20 (3.8) gating the milk and dairy products in CeDs in comparison Positive test 12 (6.8) 34 (6.4) with controls. The results indicate that in our population, the reduced calcium intake is not the dominant player controls were used for the analysis. Details on sex, age, BMI, in determining the low bone mass frequently found in job and physical activity of the two groups were reported in patients with CeD. table 1. Both patients with CeD and controls chose to avoid Our study shows that milk consumption is similar milk consumption because of their choice or because of between patients with CeD and control (p=0.69). We gastrointestinal symptoms, without undergoing a breath found that 22.2% of the patients with CeD and 19.9% test for lactose intolerance or consult a doctor. 8 controls do not drink fluid milk on a regular basis. As previously reported, the use of an online survey has Lactose-free milk is chosen by 20.4% of patients with CeD both strengths and limitations. Our survey, to our best and 19% of the controls (table 2). knowledge, is the first one conducted in a large Italian

Among those who drink milk (regular or lactose free), cohort whose results describe the milk habits of patients http://nutrition.bmj.com/ 49.6% of patients with CeD and 54.4% controls drink with CeD and controls from the general population. a daily average of 250 mL of fluid milk (table 3). Most Online surveys are quite popular because they are conve- of the subjects start to consume lactose-free milk for nient and easy to use. However, possible limitations are personal choice (without any specific reason) or because the recall bias, common in food questionnaires and the of gastrointestinal problems. Only a minority of patients use of a non-standardised questionnaire. We discussed with CeD contacted a doctor before starting the use of these limitations elsewhere.8 Being the questionnaire lactose-free milk (5.5%), despite being driven to this anonymous, we do not have any information regarding, change by gastrointestinal symptoms (41.7%) (table 4). for example, the compliance to the gluten-free diet, the on September 27, 2021 by guest. Protected copyright. Although the high percentage of responders avoid antitransglutaminase antibodies values or the time from regular milk, only a minority of them reported having the CeD diagnosis.

Table 6 Consumption of dairy products in our study population Patients with coeliac General population, N disease, N (%) (%) P value Do not eat dairy products 0 6 (1.1) 0.125 Every day 25 (14.2) 75 (14.2) 3–5 times a week 73 (41.5) 238 (45.1) Once a week 48 (27.3) 140 (26.5) Sometimes lactose-free mozzarella, cheese and yoghurt 8 (4.5) 23 (4.4) Only lactose-free mozzarella and cheese and yoghurt 2 (1.1) 10 (1.9) As ingredients only 11 (6.3) 29 (5.5) Only parmesan cheese 9 (5.1) 7 (1.3) (lactose-free aged cheese)

Zingone F, et al. bmjnph 2019;0:1–4. doi:10.1136/bmjnph-2018-000022 3 BMJ Nutrition, Prevention & Health BMJNPH: first published as 10.1136/bmjnph-2018-000022 on 19 March 2019. Downloaded from The present data confirmed our previous results, Open access This is an open access article distributed in accordance with the adding the information that patients with CeD on a Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, gluten-free diet avoid milk in a percentage similar to that and license their derivative works on different terms, provided the original work is of the general population. The most frequent cause of properly cited, appropriate credit is given, any changes made indicated, and the use avoiding milk in patients with CeD is the persistence of is non-commercial. See: http://​creativecommons.org/​ ​licenses/by-​ ​nc/4.0​ gastrointestinal symptoms despite the starting of a gluten- free diet. There are several reasons for the persistence of symptoms in CeD on a gluten-free diet,2 such as dietary References 1. Lember M. Hypolactasia: a common enzyme deficiency leading lapses and irritable bowel syndrome, and lactose intol- to lactose and intolerance. Pol Arch Med Wewn erance is only one of them. Therefore, daily calcium 2012;122(Suppl 1):60–4. 2. Stasi E, Marafini I, Caruso R, et al. Frequency and cause of persistent absorption may be low in those who avoid dairy products symptoms in celiac disease patients on a long-term gluten-free diet. and contributes, but not fully explains, to the frequent J Clin Gastroenterol 2016;50:239–43. low bone mass observed in patients with CeD from the 3. Kuchay RAH, Thapa BR, Mahmood A, et al. Lactase genetic 13 polymorphisms and coeliac disease in children: a cohort study. Ann same country, both before and after the gluten-free diet. Hum Biol 2015;42:101–4. However, studies reported that dairy food intake is asso- 4. Deng Y, Misselwitz B, Dai N, et al. Lactose intolerance in adults: biological mechanism and dietary management. Nutrients ciated with higher bone mineral density among adults, 2015;7:8020–35. particularly those with sufficient vitamin D status.14 15 5. Zingone F, Ciacci C. The value and significance of 25(OH) and 1,25(OH) vitamin D serum levels in adult coeliac patients: a review of Another aspect to take into consideration when dealing the literature. Dig Liver Dis 2018;50:757–60. with the choice of food is that patients with CeD tend 6. Passananti V, Santonicola A, Bucci C, et al. Bone mass in women already to have psychological problems caused by dietary with celiac disease: role of exercise and gluten-free diet. Dig Liver Dis 16 17 2012;44): :379–83. restriction. Therefore, our data suggest that doctors’ 7. Ciacci C, Cirillo M, Mellone M, et al. Hypocalciuria in overt and and dietitians’ advise during follow-up visits for patients subclinical celiac disease. Am J Gastroenterol 1995;90:1480–4. 8. Zingone Fet al. Consumption of milk and dairy products: facts with CeD on a gluten-free diet should focus on avoiding and figures. . Burbank, Los Angeles County, Calif: Nutrition, unnecessary restriction of milk and of dairy products 2017: 33. 322–5. 9. Meleine M, Matricon J. Gender-related differences in irritable which could further compromise their health and quality bowel syndrome: potential mechanisms of sex hormones. World J of life. Gastroenterol 2014;20:6725–43. 10. Kibune Nagasako C, Garcia Montes C, Silva Lorena SL, et al. Irritable bowel syndrome subtypes: clinical and psychological Contributors FZ and CC designed and performed the research and wrote the features, body mass index and comorbidities. Rev Esp Enferm Dig paper. FZ and PI analysed data. CB performed the research and reviewed the paper. 2016;108): :59–64. All authors accepted the final version of the paper. 11. Johannesson E, Simrén M, Strid H, et al. Physical activity improves Funding The authors declare that they received a grant from Fondazione Celiachia symptoms in irritable bowel syndrome: a randomized controlled trial. Am J Gastroenterol 2011;106): :915–22. (grant no. 008_FC_2015).

12. Fismen A-S, Smith ORF, Torsheim T, et al. Trends in food habits and http://nutrition.bmj.com/ Disclaimer CONSORT 2010: the authors declare that the CONSORT 2010 their relation to socioeconomic status among Nordic adolescents statement guideline has been adopted. 2001/2002-2009/2010. PLoS One 2016;11:e0148541. 13. Ciacci C, Maurelli L, Klain M, et al. Effects of dietary treatment on Competing interests None declared. bone mineral density in adults with celiac disease: factors predicting response. Am J Gastroenterol 1997;92:992–6. Patient consent for publication Not required. 14. Mangano KM, Noel SE, Sahni S, et al. Higher dairy intakes are Ethics approval The study was approved by the by the Ethics Committee of the associated with higher bone mineral density among adults with University of Salerno Campania Sud aut. No 25, 25.4.2015. sufficient vitamin D status: results from the Boston Puerto Rican Study. J Nutr 2019;149:139–48. Provenance and peer review Not commissioned; externally peer reviewed. 15. van Dongen LH, Kiel DP, Soedamah-Muthu SS, et al. Higher dairy

food intake is associated with higher spine quantitative computed on September 27, 2021 by guest. Protected copyright. Data sharing statement Data set is available from the last author at ​cciacci@​ tomography (QCT) bone measures in the Framingham study for men unisa.​it. Consent for data sharing was obtained. All the data were anonymised, and but not women. J Bone Miner Res 2018;33): :1283–90. risk of identification is inconsistent. 16. Zingone F, Swift GL, Card TR, et al. Psychological morbidity of celiac disease: a review of the literature. United European Gastroenterol J Author note Core tip: we examined the average consumption of milk and dairy 2015;3:136–45. products and the reasons for not consuming them in patients with coeliac disease 17. Passananti V, Siniscalchi M, Zingone F, et al. Prevalence of eating compared with controls. We found that there is no significant difference between disorders in adults with celiac disease. Gastroenterol Res Pract patients with coeliac disease and controls in the regular milk consumption. 2013;2013:1–7.

4 Zingone F, et al. bmjnph 2019;0:1–4. doi:10.1136/bmjnph-2018-000022