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  • 1. RESEARCHQualitative ResearchEffects of Dairy Products on Crohn’s DiseaseSymptoms Are Influenced by Fat Content andDisease Location but not Lactose Content orDisease Activity Status in a New ZealandPopulationDEBORAH NOLAN-CLARK; LINDA C. TAPSELL, PhD, MHPEd; RONG HU, MSc; DUG YEO HAN, PhD;LYNNETTE R. FERGUSON, MSc, DPhil (Oxon), DScABSTRACTBackground Dairy products have been perceived as havingthe potential to cause adverse effects in individuals withCrohn’s disease (CD) and are often avoided, potentiallyincreasing the risk of osteoporosis and related morbidityassociated with inadequate dietary calcium intake.Objective To evaluate the self-reported effects of dairyproducts on CD symptoms and to determine whetherthese effects differed between types of dairy productsconsumed and disease state or location.Design Secondary analysis of dietary survey and clinicaldata from participants in the Genes and Diet in Inflam-matory Bowel Disease study based in Auckland, NewZealand.Subjects/setting One hundred and sixty-five men andwomen diagnosed with CD for which both dietary surveydata and clinical information were available.Statistical analyses performed ␹2analysis was conducted toassess whether significant differences in the proportionsof responses relating to a worsening of CD symptomsfrom individual dairy products were evident between in-dividuals with active or quiescent CD, or ileal or colonicdisease locations. Odds ratios with confidence intervalwere calculated to determine whether CD location wasassociated with risk of any type of adverse reaction tomilk products. Logit scales were utilized to depict self-reported CD symptoms associated with individual dairyproduct consumption for ileal and colonic CD patients.Results Dairy products had no effect on self-reported CDsymptoms for most people. Dairy products with a high fatcontent were most frequently reported to worsen per-ceived CD symptoms. Clinically, self-reported CD activitystatus did not influence responses to dairy products; how-ever, colonic inflammation was more frequently associ-ated with adverse CD effects in comparison to ileal CDinvolvement.Conclusions Research outcomes question the necessity ofdairy product avoidance in CD patients and illustrate thehighly individual nature of dairy product tolerance in thisclinical population.J Am Diet Assoc. 2011;111:1165-1172.Crohn’s disease (CD) is a debilitating form of inflam-matory bowel disease that can affect any location ofthe gastrointestinal tract, resulting in considerablemorbidity (1). The incidence of CD in a New ZealandϪbased epidemiological study was 16.5/100,000 per year,(2), higher than in many Western countries and, thus,affecting a substantial proportion of the New Zealandpopulation.Dairy products have often been perceived as having thepotential to cause adverse effects in individuals with CDand so are often avoided, potentially increasing the risk ofosteoporosis and related morbidity associated with inad-equate dietary calcium intake.There are several hypotheses proposed to explain thisperceived adverse effect. Perhaps the most frequentlyreported theory relates to the prevalence of lactose intol-erance in CD patients. A higher prevalence of lactosemalabsorption, as diagnosed by hydrogen breath testing,in individuals with CD has been reported in comparisonto controls (3). Allergy to major milk proteins may beanother reason that a small number of CD patients reportadverse effects from dairy products (4). In addition, indi-viduals with CD might be susceptible to secondary lactoseD. Nolan-Clark is a PhD candidate, Smart Foods Cen-tre, University of Wollongong, Wollongong, NSW, Aus-tralia. L. C. Tapsell is Director, Nutrition Research,Illawarra Health and Medical Research Institute andDirector, Smart Foods Centre, University of Wollongong,Wollongong, NSW, Australia. R. Hu and D. Y. Han arestatisticians, Discipline of Nutrition, University of Auck-land, Auckland, New Zealand. L. R. Ferguson is pro-gram leader, Nutrigenomics New Zealand and Head ofthe Discipline of Nutrition, University of Auckland,Auckland, New Zealand.Address correspondence to: Deborah Nolan-Clark,Smart Foods Centre, University of Wollongong, Wollon-gong, NSW 2522, Australia. E-mail: djn297@uow.edu.auManuscript accepted: January 5, 2011.Copyright © 2011 by the American DieteticAssociation.0002-8223/$36.00doi: 10.1016/j.jada.2011.05.004© 2011 by the American Dietetic Association Journal of the AMERICAN DIETETIC ASSOCIATION 1165
  • 2. intolerance. During the periods of the acute gastrointes-tinal inflammation characteristic of CD, quantities of lac-tase, the lactose digesting enzyme, may decline in theduodenal mucosa, resulting in the gastrointestinal dis-comfort associated with lactose maldigestion (5). Thus,disease state (active or quiescent) can affect response todairy products in this clinical population.Disease location may further influence tolerance todairy products in individuals with CD. Barrett and col-leagues reported a higher proportion of lactose malab-sorption in patients with ileal CD in comparison to colonicCD (3). As lactase is located within small intestinal villi,this is the primary site of lactose digestion (6). Thus,individuals with inflammation located within this regionof the gastrointestinal tract may have difficulties withlactose intolerance and, thus, perceive that adverse CDsymptoms are associated with consumption of dairy prod-ucts.The aim of this study was to evaluate the self-reportedeffects of dairy products on CD symptoms and to deter-mine whether these perceived effects differed betweentypes of dairy products consumed, disease state, or loca-tion. The identification of dairy-mediated effects on CDsymptoms may facilitate the provision of more targeteddietary advice on dairy products for this clinical popula-tion.METHODSThis study was based on a secondary analysis of dietarysurvey and clinical data from 165 adults with CD. Allsubjects were white participants in the Genes and Diet inInflammatory Bowel Disease study, which was an obser-vational study based in Auckland, New Zealand (7). Sub-jects were selected on the basis that a complete set ofdietary and clinical data was available.The original study was approved by the New ZealandMulti-Region Human Ethics Committee (MEC/04/12/011). Access to the data for this secondary analysis metethical approval and all information utilized was coded toprotect the anonymity of participants.Clinical DataClinical information including age, inflammatory boweldisease diagnosis, and latest Montreal classification illus-trating latest CD location (8) was provided after evalua-tion of patient medical notes and secondary patient in-vestigation by an experienced gastroenterologist as a partof the Genes and Diet in Inflammatory Bowel Diseasestudy. Individuals with a latest Montreal classification ofL1, indicating ileal involvement, were grouped into theIleal Involvement group. Although individuals with aclassification of L2, indicating isolated colonic involve-ment, were classified as the Colonic Involvement group.To ensure that effects observed could be attributable toeither colonic or ileal disease locations, individuals with aclassification of L3 and L4 (indicating ileocolonic andupper gastrointestinal disease in the presence of classifi-cations of L1 to L3, respectively (9), were excluded fromthis part of the analysis.Additional clinical information was sought from thedietary questionnaire whereby subjects self-reported cur-rent disease activity status (active or quiescent).Dietary DataFor the purpose of this study, dairy products were cate-gorized to include ruminant milk (inclusive of sheep, cow,and goat varieties), yogurt, butter, custard, ice cream,cream, and cheese.The original dietary questionnaire utilized for thisstudy was developed in conjunction with CD patients andaimed to identify foods that were considered either ben-eficial or detrimental to self-reported CD symptoms. Di-etary data were reassessed 6 months after completion ina subset of CD patients with consistent results indicatinggood survey reliability. All data were cross-checked inde-pendently by two researchers to ensure accuracy. Thecomplete dietary questionnaire is described in more de-tail elsewhere (7).Self-reported data on effects of dairy products wereextracted from this dietary questionnaire, which requiredparticipants to indicate whether particular foods itemsmade their inflammatory bowel disease condition “defi-nitely worse,” “probably worse,” “had no effect,” “probablybetter,” or “definitely better.” Subjects reporting that par-ticular dairy products made their condition either “defi-nitely” or “probably worse” were categorized as havingCD symptom worsening associated with consumption ofthat food. Similarly, those reporting a “definitely” or“probably better” effect of a particular dairy product ontheir CD condition were categorized as having a benefi-cial effect on CD symptoms from consuming that food.Several open-ended questions within the questionnairewere also analyzed to determine qualitative informationabout perceived effects on CD condition associated withparticular dairy products. These questions included:● Is there a difference with the type of cheese eaten? If so,please outline.● Is there a difference with the type of yogurt eaten? If so,please outline.Both quantitative and qualitative information aboutthe frequency and nature of having any form of adversereaction (such as nausea or bloating) to milk productswas extracted from this supplementary questionnaire af-ter an analysis of open-ended questions including:● Have you ever had an adverse reaction to a milk prod-uct?● What were your adverse symptoms after consumingmilk products?● Have you seen a health professional about your reac-tions to milk products (if applicable)?● Have you been formally diagnosed with an intoleranceor allergy?Data AnalysisQualitative data (including reports on symptoms of ad-verse reactions to dairy products and of symptomaticdifferences from different types of dairy products con-sumed) were categorized accordingly and the proportionof individuals responding to each category was calcu-lated.␹2analysis was conducted to assess whether substan-tial differences in the proportions of responses relating toa worsening of CD symptoms from individual dairy prod-1166 August 2011 Volume 111 Number 8
  • 3. ucts were evident between individuals with active or qui-escent CD, or ileal or colonic disease locations. Oddsratios with confidence interval were calculated to deter-mine whether CD location was associated with a risk ofhaving any type of adverse reaction to milk products.Results were considered statistically significant atPϽ0.05.For interpretation of data grouped by disease location(ileal vs colonic), logit scales were utilized to create a clearvisual representation of self-reported CD symptoms asso-ciated with consumption of individual dairy productswhile addressing the issue of the variance of proportionsbetween the groups.All analyses were conducted using SPSS (V15.0 1989-2006, SPSS Inc, Chicago IL), R (2009, R DevelopmentCore Team, Vienna, Austria, http://www.R-project.org.ref),and SAS (V9.1, 2003, SAS Institute, Cary, NC) statisticalsoftware packages.RESULTSDietary and clinical data were available for 165 patientswith CD (mean ageϭ48.8Ϯ16.3 years). The study samplewas predominantly female (males, nϭ49; mean ageϭ50.6Ϯ17.8 years; females, nϭ116; mean ageϭ48.0Ϯ15.6years).Clinical ProfilesOf the study sample, 80 patients (48.5%) reported thattheir CD was currently active and 82 (49.7%) identifiedtheir CD as being in the quiescent phase. Three patientsdid not answer this survey question. There was no differ-ence between the sexes in the proportion reporting anactive CD period at the time of survey completion(␹2ϭ0.38, Pϭ0.54).Data were available for 160 patients on the latest Mon-treal classification indicating the location of CD. Isolatedileal disease involvement was present for 32.7% of thestudy sample, while 27.9% displayed evidence of isolatedcolonic involvement (Table 1).There was no significant difference between males andfemales in terms of CD location (␹2ϭ0.98; Pϭ0.81).Effects of All Dairy Products on Self-Reported CD SymptomsForty-two participants (25.5%) reported having an ad-verse reaction to a product containing milk, while 111(67.3%) felt that they had no experience of an adverseevent with milk product consumption. Of patients report-ing an adverse reaction associated with a milk product,24 (61.5%) reported that the reaction was persistent,while seven individuals (4.2%) felt that it was an isolatedevent.A formal diagnosis of lactose intolerance was reportedfor 11 patients (6.7% of the study population). A total of41 CD patients described adverse symptoms experiencedafter consumption of milk products (Figure 1).As an aside to these data, naturopaths were listed asthe health practitioner most frequently sought for adviceregarding adverse effects to dairy products (nϭ9), spe-cialist consultants, including gastroenterologists and al-lergy specialists, were the next most frequently sought(nϭ8), followed by general practitioners (nϭ7). Only oneindividual reported seeking advice in relation to dairyproduct intolerance from a registered dietitian.Associations Between Individual Dairy Products and Self-Reported CD SymptomsNo effect on CD symptoms was reported to be associatedwith the consumption of butter, standard cow’s milk, andreduced-fat cow’s milk in 71.5%, 55.2%, and 58.2% of allpatients, respectively. Dairy products most frequentlyreported to worsen CD symptoms were cream (43.6%), icecream (37.6%), and cheese (34.5%). Conversely, yogurt,the dairy product most frequently perceived as beneficial,was reported by 14.5% of individuals as having favorableeffects on CD symptoms. The response to this questionwas quite varied (Table 2).CheeseWhen asked whether the type of cheese may influence CDsymptoms, 26.1% of participants responded positively.The flavor strength of the cheese was most frequentlyTable 1. Latest subject Montreal classifications for location ofCrohn’s disease (CD) (nϭ160)Montreal classificationfor CD location Group Males Females4™™™™™™™™™™ n (%) ™™™™™™™™™™3L1 Ileal 54 (32.7) 14 (28.6) 40 (34.5)L2 Colonic 46 (27.9) 16 (32.7) 30 (25.9)L3 Ileocolonic 51 (30.9) 15 (30.6) 36 (31.0)L4 Isolated upperdisease9 (5.5) 3 (6.1) 6 (5.2)Figure 1. Adverse symptoms reported by Crohn’s disease patientsafter consumption of dairy products (nϭ41). Some patients reportedmore than one symptom. Other adverse symptoms reported include:asthma (nϭ1), reflux (nϭ1), bowel irritation (nϭ1), and inflammation(nϭ1).August 2011 ● Journal of the AMERICAN DIETETIC ASSOCIATION 1167
  • 4. reported as influencing tolerance, with 15 patients re-porting that increased strength cheese decreased toler-ance. Richer/soft cheeses were reported to worsen CDsymptoms for nine patients, with a preference for fetaand edam cheese varieties reported by eight and sevenpatients, respectively. Cheeses with a lower fat contentwere reported to increase tolerance (nϭ6), as did hardcheeses (nϭ5) and plain cheeses without added herbs(nϭ3). Melted cheese was associated with worsening CDsymptoms for four patients.YogurtIn total, 23.0% of respondents reported that the type ofyogurt consumed may also be a key factor relating towhether it would be tolerated. Patients reported thatyogurts containing live cultures such as acidophilus weremost beneficial to CD symptoms (nϭ19), while naturalyogurt was preferable to sweetened alternatives for 11patients. A preference for reduced-fat yogurt was re-ported (nϭ9), with yogurt lacking seeds or fruit preferredby an additional 4.8% (nϭ8) of individuals.Disease Activity and Self-Reported Effect of Dairy Products onCD SymptomsThere were no significant differences in the proportion ofindividuals reporting a worsening of CD symptoms asso-ciated with the consumption of individual dairy productsbetween patients in the active or quiescent CD state(Table 3).Site of Disease and Self-Reported Effect of Dairy Products onCD SymptomsLikewise, no significant differences were detected be-tween self-reported CD symptoms associated with con-sumption of individual dairy products and ileal or colonicdisease location (data not shown). However, considerablyfewer patients with ileal disease activity reported everhaving any type of adverse reaction to dairy productscompared to those with colonic disease involvement(␹2ϭ5.90; Pϭ0.015; odds ratioϭ0.32; 95% confidence in-terval: 0.13 to 0.82; Pϭ0.017).Logit scales of self-reported improvement or worseningof CD symptoms associated with consumption of individ-ual dairy products in individuals with either small intes-Table 2. Self-reported effect of individual dairy products on Crohn’s disease (CD) symptoms (nϭ165)Food itemCD symptomsworseNo difference toCD symptomsCD symptomsbetterQuestion notanswered4™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™ n (%) ™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™3Standard cow’s milk 51 (30.9) 91 (55.2) 2 (1.2) 21 (12.7)Reduced-fat cow’s milk 30 (18.2) 96 (58.2) 10 (6.0) 29 (17.6)Butter 29 (17.6) 118 (71.5) 2 (1.2) 16 (9.7)Custard 32 (19.4) 106 (64.2) 8 (4.8) 19 (11.5)Goat’s milk 11 (6.7) 27 (16.4) 4 (2.4) 123 (74.5)Sheep’s milk 11 (6.7) 27 (16.4) 5(3.0) 122 (73.9)Ice cream 62 (37.6) 94 (57.0) 3 (1.8) 6 (3.6)Yogurt 31 (18.8) 94 (57.0) 24 (14.5) 16 (9.7)Cheese 57 (34.5) 95 (57.6) 5 (3.0) 8 (4.8)Cream 72 (43.6) 72 (43.6) 1 (0.6) 20 (12.1)Table 3. Self-reported effect of individual dairy products on worsening Crohn’s disease (CD) symptoms analyzed by disease activity status(nϭ162)Food itemCD Symptoms Worse No Difference in CD SymptomsActive CD(n‫)08؍‬Quiescent CD(n‫؍‬ 82)Active CD(n‫)08؍‬Quiescent CD(n‫؍‬ 82) ␹2analysis4™™™™™™™™™™™™™™™™™™™™™™™™™™™™ n ™™™™™™™™™™™™™™™™™™™™™™™™™™3Standard cow’s milk 21 30 45 43 (␹2ϭ1.28; Pϭ0.26)Reduced-fat cow’s milk 14 15 46 48 (␹2ϭ0.004; Pϭ0.95)Butter 15 9 57 61 (␹2ϭ1.61; Pϭ0.20)Custard 17 14 50 54 (␹2ϭ0.48; Pϭ0.51)Goat’s milk 7 4 13 13 (␹2ϭ0.58; Pϭ0.45)Sheep’s milk 5 6 13 13 (␹2ϭ0.64; Pϭ0.80)Ice cream 31 30 45 47 (␹2ϭ0.053; Pϭ0.82)Yogurt 16 14 46 47 (␹2ϭ0.14; Pϭ0.71)Cheese 27 29 46 47 (␹2ϭ0.02; Pϭ0.883)Cream 36 36 35 35 (␹2ϭ0.00; Pϭ1.00)1168 August 2011 Volume 111 Number 8
  • 5. tinal (ileal) or colonic CD involvement are displayed inFigure 2A and B. Only dairy products with at least onereported beneficial/adverse effect on CD symptoms can beplotted with the Logit scale. For patients with ileal in-volvement, butter, goat, and sheep milk were not in-cluded in the Logit graph. Similarly, cream, ice cream,sheep, and goat milk were not graphed for individualswith colonic involvement.AStandard MilkReduced-Fat MilkCustardIce CreamYogurtCheeseCream1% %01%5%2 12% 15% 20% 25% 30% 35% 40% 45% 50% 55%1%2%3%4.5%7%10%15%25%35%45%55%Increasing perceived worsening of CD symptomsIncreasingperceivedimprovementofCDsymptomsBStandard MilkReduced-Fat MilkButter CustardYogurtCheese1% %01%5%2 12% 15% 20% 25% 30% 35% 40% 45% 50% 55%1%2%3%4.5%7%10%15%25%35%45%55%Increasing perceived worsening of CD symptomsIncreasingperceivedimprovementofCDsymptomsFigure 2. (A) Self-reported effects of individual dairy products on Crohn’s disease (CD) symptoms for individuals with ileal disease involvement.(B) Self-reported effects of individual dairy products on CD symptoms for individuals with colonic disease involvement.August 2011 ● Journal of the AMERICAN DIETETIC ASSOCIATION 1169
  • 6. DISCUSSIONThis analysis of self-reported effects of dairy products onCD symptoms has clearly illustrated the extent of varia-tion in perceived tolerance to these items within thisclinical population.Most importantly, the majority of the study samplereported that consumption of dairy products made nodifference to CD symptoms. This finding reinforces theneed to determine tolerance to dairy products in CD pa-tients before encouraging widespread avoidance of thisfood group, an idea that may still be encouraged by somephysicians and many alternative health consultants. Al-though it may be pertinent to avoid some dairy productsfor CD patients with congenital hypolactasia or duringperiods of active disease, unnecessary avoidance of alldairy products by this clinical group without appropriatenutrition support may have deleterious consequences.Individuals with CD are more susceptible to osteoporosis(10). Prolonged corticosteroid use to induce remission ofinflammation has been demonstrated to reduce bone min-eral density in CD patients (11). CD itself may be anindependent risk factor for osteoporosis (12), with anincrease in proinflammatory cytokines associated withdisease pathogenesis mediating excessive bone resorption(13). According to the National New Zealand NutritionSurvey (14), milk, cheese, and other dairy products werethe highest food contributors of dietary calcium in theNew Zealand population, contributing 37%, 11%, and 5%of total calcium consumed, respectively. Although evi-dence is conflicting, Abitbol and colleagues (15) demon-strated a protective effect of calcium intake on bone min-eral density in individuals with inflammatory boweldisease, and increased dairy product consumption hasbeen reported to retard bone loss (16). Eliminating dairyproducts as the highest contributor of dietary calciumfrom the diet may further exacerbate risk of osteoporosisand related morbidity in individuals with CD in NewZealand.Intermittent secondary lactose intolerance may be ex-perienced by some individuals with CD during periods ofactive gastrointestinal inflammation (5). Formally diag-nosed lactose intolerance was reported for only a smallproportion of the study sample. However, symptoms con-sistent with lactose maldigestion, including bloating, di-arrhea, and gas (17), were the most frequently reportedadverse effects associated with milk product consump-tion. This finding indicates that secondary lactose intol-erance may have influenced the response to dairy prod-ucts for a greater number of this CD study sample.Seeking assistance from alternative health practitio-ners is a practice frequently observed in individuals suf-fering from inflammatory bowel conditions (18). Advice ofthis nature is often sought as an adjunct to conventionalmedical therapies in an effort to establish a sense ofcontrol over this debilitating condition (19). This practicewas evident in this clinical population, whereby naturo-paths were the most frequently used source of advice forissues with dairy product tolerance. Ensuring accurateadvice in relation to dairy product consumption is imper-ative to preventing micronutrient deficiencies in this clin-ical population. Appropriate dietetic intervention is in-strumental in ensuring optimal bone mineral density inpatients with CD (20). Thus, for individuals reportingadverse CD effects associated with the consumption ofdairy products, dietetic intervention should be encour-aged as part of the continuum of care.In this study sample, individual dairy product toler-ance was highly variable. In fact, the majority of individ-uals experienced no effect on CD symptoms associatedwith each of the individual dairy products under ques-tion. An exception to this finding was evident for cream,with the highest proportion of individuals in the studysample reporting a worsening of CD symptoms associatedwith its consumption. The perceived adverse effects mayrelate to the high fat content of this item. High dietary fatintakes decrease gastric emptying rates (21). In addition,disorders in gastrointestinal motility have been observedin this clinical population, with affected individuals morelikely to experience gastric hypomotility than controls(22). This is particularly pertinent as gastric hypomotilityis associated with delayed gastric emptying (23). Effectsof dietary-fatϪmediated decreases in gastric emptyingafter consumption of dairy products rich in fat may bemore pronounced in individuals with CD. Symptoms as-sociated with delayed gastric emptying include nausea,abdominal pain, and bloating (23), all of which were fre-quently reported as adverse effects after dairy productconsumption in this study.It should also be noted that cream, like many otherfoods, is rarely consumed in isolation and generally formsa component of a meal. Thus, there is a possibility thatperceived worsening of CD symptoms assigned to partic-ular foods may relate to the cuisine context in whichthese items are consumed rather than the food item itself.However, other dairy products containing higheramounts of fat, including ice cream and cheese, were alsoassociated with a perceived worsening of CD symptoms ina larger number of patients in comparison to their lowerfat dairy counterparts. Furthermore, reduced-fat cheeseand yogurt varieties were perceived as more tolerable.These findings illustrate that the fat content of dairyproducts may be a key factor influencing tolerance in thisclinical population.Of interest was the finding that butter, a dairy productthat contains a very high proportion of fat, was not re-ported to worsen self-reported CD symptoms for the ma-jority of individuals. It may be that butter is not beingconsumed in quantities great enough to influence gastricstasis in the study sample. Conversely, butter contains arelatively high proportion of conjugated linoleic acid,which has been implicated in the amelioration of inflam-mation in experimental models of inflammatory boweldisease, particularly in relation to colitis (24). Thus, thelack of perceived worsening of CD symptoms associatedwith butter consumption may be the result of this conju-gated linoleic acidϪmediated anti-inflammatory effect.Probiotic-containing yogurt has been demonstrated toattenuate markers of inflammation in individuals withinflammatory bowel disease (25).The dairy product mostfrequently associated with having self-reported beneficialeffects on CD symptoms in this study was yogurt. How-ever, yogurt was also found to be associated with a wors-ening of CD symptoms for a slightly greater number ofindividuals than had experienced beneficial effects fromit. A limitation of the survey used for analysis was that itfailed to distinguish between CD effects experienced from1170 August 2011 Volume 111 Number 8
  • 7. probiotic yogurt and nonprobiotic varieties. An analysisof qualitative responses indicated that for individualsexperiencing a difference in CD symptoms dependent onthe type of yogurt consumed, those containing live cul-tures and probiotics were most frequently associated withbeneficial effects. Thus, probiotic yogurts appeared tobenefit individuals with CD in preference to yogurt with-out live cultures; however, this is an area that requiresfurther research, and a placebo effect cannot be ruled out.It was expected from previous observations (7) thatgoat and sheep milk may result in less perceived worsen-ing of CD symptoms than their bovine counterparts. Goatmilk in particular contains oligosaccharides, which havedemonstrated anti-inflammatory effects in rat models ofinflammatory bowel disease (26). In addition, sheep andgoat’s milk contain higher proportions of medium chaintriglycerides than cow’s milk, which may enhance digest-ibility (27). Finally, like butter, sheep milk contains rel-atively high amounts of conjugated linoleic acid (28),which may further ameliorate gastrointestinal inflamma-tion (24). In this study, only a very small proportion ofindividuals reported beneficial effects on CD symptomsassociated with consumption of these milk products, witha slightly greater proportion reporting symptom worsen-ing. However, because the majority of individuals did notanswer this question, indicating that they did not con-sume these items, it was not possible to determine thetrue effect of goat and sheep milk on CD symptoms. Givenemerging evidence to suggest a potentially beneficial rolefor sheep and goat milks in relation to CD symptoms,evaluating the true effects of these products may be animportant area for future research.The lactose content of the individual dairy products didnot seem to influence self-reported CD symptoms in thisstudy sample. Cow’s milk, which contains a considerablygreater amount of lactose per serving than cream, icecream, or cheese (17), was associated with comparativelyless perceived symptom worsening. In addition, lactosetolerance may be influenced by gastrointestinal transittime, with higher-fat milk products traveling less rapidlythroughout the small intestine, affording lactase agreater opportunity for lactose digestion (17). Thus, iflactose was a key factor relating to CD symptoms in thisstudy sample, reduced-fat cow’s milk would have beenassociated with less favorable CD symptoms than itsstandard counterpart. As this was not the case, it appearsthat the lactose content of individual dairy products doesnot have a major impact on CD symptoms. In contrast,qualitative responses regarding the types of cheese andyogurt consumed, which may influence tolerance, indi-cate a lactose effect in a small proportion of the studysample. The preference for yogurt containing live bacte-ria previously outlined may be associated with toleranceto lactose for some individuals, given that these organ-isms perform the activity of lactase (29), enhancing di-gestibility. Similarly, several individuals reported a pref-erence for hard cheeses, such as cheddar, in comparisonto soft cheeses. Hard cheeses contain slightly less lactosethan soft varieties, such as cream cheese (17), and so maybe better tolerated by individuals with lactose maldiges-tion.In this study, disease activity (active vs quiescent) didnot appear to influence perceived effects of dairy productson CD symptoms, with a similar proportion of individualsreporting either adverse or beneficial dairy-mediated ef-fects on CD symptoms irrespective of disease activity.This finding challenges the necessity of dairy avoidanceduring active CD. However, as disease activity was sub-jectively reported, these findings should be interpretedwith caution.Reference to the logit scales developed in this analysisillustrate that individuals with isolated colonic inflam-mation appeared to have an increase in perceived adverseCD symptoms associated with the consumption of re-duced-fat cow’s milk, custard, sheep’s milk, and yogurt incomparison to those with isolated small intestinal (ileal)involvement. This was an unexpected finding, as it wasanticipated that individuals with small intestinal inflam-mation would be more likely to have issues with lactoseand, thus, dairy product tolerance, given that lactaselines the small intestinal mucosa (6). Furthermore, An-nese and colleagues (22) reported that most severe gas-trointestinal motility disorders occur in Crohn’s ileitis.This unexpected finding warrants further investigationand may relate to functional differences in gut microbiotaamong individuals with CD affecting varied locationsthroughout the gastrointestinal tract.A possible explanation for the unexpected outcomesobserved in relation to dairy product tolerance in thisstudy may be attributable to individual genetic variation.Although clear genomic loci, such as NOD2 and IL23R,have been repeatedly associated with CD in genome-wideassociation studies (30), there is a paucity of evidence inrelation to genetic factors that may influence tolerance todairy products in individuals with this inflammatory con-dition. Future research efforts should consider the impactof genetic interactions on dairy product tolerance in CD toconclusively address the research question.This study was limited by the subjective nature of thedietary questionnaire used and the relatively small sizeof the CD sample, which make it difficult to extrapolatefindings to the wider CD community. In addition, infor-mation relating to the specific macronutrient compositionor processing methods used for each of the dairy productsincluded within this study was not acquired. Results ob-tained may only be applicable to this study sample andmay not apply to individuals consuming dairy productsthat differ greatly from the generic food composition ofNew Zealand dairy products. Furthermore, informationabout the quantity of dairy food items required to eliciteffects on self-reported CD symptoms was not collected inthe dietary questionnaire. Quantification of such itemsmay provide further insight into the factors that caninfluence tolerance to dairy products in this clinical pop-ulation, in particular whether there is a threshold ofconsumption that must be achieved in order to influenceperceived symptoms. Despite these limitations, this is thefirst study to assess the perceived effects of dairy prod-ucts on CD symptoms, taking into account both clinicaland qualitative data, and provide some important in-sights for both future research and dietetics practicewithin this clinical population.CONCLUSIONSIn conclusion, within this study sample of CD patients inAuckland, New Zealand, dairy products in general had noAugust 2011 ● Journal of the AMERICAN DIETETIC ASSOCIATION 1171
  • 8. effect on self-reported CD symptoms for most people.When analyzed according to type of dairy product, itemswith a high fat content were most frequently reported toworsen perceived CD symptoms. The lactose content ofindividual dairy products did not influence self-reportedCD symptoms for the majority of patients. Clinically, CDactivity status did not influence responses to dairy prod-ucts; however, site of disease appeared to have an effect.Colonic inflammation was more frequently associatedwith an increase in reported adverse CD effects fromdairy product consumption in comparison to ileal CDinvolvement. Results from this exploratory study rein-force the idea that that “one size does not fit all” when itcomes to making dietary recommendations relating todairy product consumption for individuals with CD. Fu-ture research should consider the identification of geneticvariants that might further explain tolerance to dairyproducts in this clinical population.STATEMENT OF POTENTIAL CONFLICT OF INTEREST:No potential conflict of interest was reported by the au-thors.FUNDING/SUPPORT: Funding has been receivedthrough an Australian Endeavour Research Fellowshipto support travels to New Zealand to collaborate withNutrigenomics New Zealand at the University of Auck-land. However, as this study was based on a secondaryanalysis of existing data, no additional funds were uti-lized.Deborah Nolan-Clark is a recipient of an AustralianEndeavour Research Fellowship. The authors would liketo acknowledge the participants of the present study andthank Philippa Dryland and Virginia Parslow for assis-tance with the provision of dietary questionnaires. Nu-trigenomics New Zealand is a collaboration betweenAgResearch Ltd, Plant and Food Research and The Uni-versity of Auckland and is largely funded by the Founda-tion for Research, Science and Technology.References1. Veloso FT, Ferreira JT, Barros L, Almeida S. Clinical outcome ofCrohn’s disease: Analysis according to the Vienna classification andclinical activity. Inflamm Bowel Dis. 2001;7:306-313.2. Gearry RB, Richardson A, Frampton CMA, Collett JA, Burt MJ,Chapman BA, Barclay ML. High incidence of Crohn’s disease inCanterbury, New Zealand: Results of an epidemiologic study. In-flamm Bowel Dis. 2006;12:936-943.3. Barrett JS, Irving PM, Shephard SJ, Muir JG, Gibson PR. Compari-son of the prevalence of fructose and lactose malabsorption acrosschronic intestinal disorders. Aliment Pharmacol Ther. 2009;30:165-174.4. Knoflach P, Park BH, Cunningham R, Weiser MM, Albini B. Serumantibodies to cow’s milk proteins in ulcerative colitis and Crohn’sdisease. Gastroenterology. 1987;92:429-485.5. von Tirpitz C, Kohn C, Steinkamp M, Geerling I, Maier V, Möller P,Adler G, Reinshagen M. Lactose intolerance in active Crohn’s diseaseclinical value of duodenal lactase analysis. J Clin Gastroenterol. 2002;34:49-53.6. Vesa TH, Marteau P, Korpela, R. Lactose intolerance. J Am Coll Nutr.2000;19(suppl):165S-175S.7. Triggs CM, Munday K, Hu R, Fraser AG, Gearry RB, Barclay ML,Ferguson LR. Dietary factors in chronic inflammation: Food toler-ances and intolerances of a New Zealand Caucasian Crohn’s diseasepopulation. Mutat Res. 2010;690:123-138.8. Satsangi J, Silverberg MS, Vermeire S, Colombel JF. The Montrealclassification of inflammatory bowel disease: Controversies, consen-sus, and implications. Gut. 2006;55:749-753.9. Silverberg MS, Satsangi J, Ahmad T, Arnott IDR, Bernstein CN,Brant SR, Caprilli R, Colombel JF, Gasche C, Geboes K, Jewell DP,Karban A, Loftus EV, Pena AS, Riddell RH, Sachar DB, Schreiber S,Steinhart AH, Targan SR, Vermeire S, Warren BF. Towards an inte-grated clinical, molecular and serological classification of inflamma-tory bowel disease: Report of a working party of the 2005 MontrealWorld Congress of Gastroenterology. Can J Gastroenterol. 2005;19(suppl A):5A-36A.10. Héla S, Nihel M, Faten L, Monia F, Boubaker J, Azza F, SlaheddineS. Osteoporosis and Crohn’s disease. Joint Bone Spine. 2005;72:403-407.11. Yang YX, Lichtenstein GR. Corticosteroids in Crohn’s disease. Am JGastroenterol. 2002; 97:803-823.12. Ghosh S, Cowen S, Hannan WJ, Ferguson A. Low bone mineraldensity in Crohn’s disease, but not in ulcerative colitis, at diagnosis.Gastroenterology. 1994;107:1031-1039.13. Manolagas SC, Jilka RL. Bone marrow, cytokines, and bone remod-eling—Emerging insights into the pathophysiology of osteoporosis.N Engl J Med. 1995;332:305-311.14. Russel DG, Parnell WR, Wilson NC, Faed J, Ferguson E, Herbison P,Horwath C, Nye T, Reid P, Walker R, Wilson B. NZ Food: NZ People.Key Results of the 1997 National Nutrition Survey. Wellington, NewZealand: Ministry of Health; 1999.15. Abitbol V, Mary JY, Roux C, Soulé JC, Belaiche J, Dupas JL, GendreJP, Lerebours E, Chaussade S. Osteoporosis in inflammatory boweldisease: Effect of calcium and vitamin D with or without fluoride.Aliment Pharmacol Ther. 2002;16:919-927.16. Baran D, Sorensen A, Grimes J, Lew R, Karellas A, Johnson B, RocheJ. Dietary modification with dairy products for preventing vertebralbone loss in premenopausal women: A three-year prospective study.J Clin Endocrinol Metab. 1990;70:264-270.17. Riitta K. Symptoms of lactose intolerance. Scand J Nutr. 2001; 45:171-173.18. Joos S, Rosemann T, Szecsenyi J, Hahn EG, Willich SN, Brinkhaus B.Use of complementary and alternative medicine in Germany—A sur-vey of patients with inflammatory bowel disease. BMC ComplementAltern Med. 2006;6:19.19. Jamieson AE, Fletcher PC, Schneider MA. Seeking control throughthe determination of diet: A qualitative investigation of women withirritable bowel syndrome and inflammatory bowel disease. Clin NurseSpec. 2007;21:152-160.20. O’Sullivan M, O’Morain C. Nutrition in inflammatory bowel disease.Best Pract Res Clin Gastroenterol. 2006;20:561-573.21. Gentilcore D, Chaikomin R, Jones KL, Russo A, Feinle-Bisset C,Wishart JM, Rayner CK, Horowitz, M. Effects of fat on gastric emp-tying of and the glycemic, insulin, and incretin responses to a carbo-hydrate meal in type 2 diabetes. J Clin Endocrinol Metab. 2006;91:2062-2067.22. Annese V, Bassotti G. Napolitano G, Usai P, Andriulli A, VantrappenG. Gastrointestinal motility disorders in patients with inactiveCrohn’s disease. Scand J Gastroenterol. 1997;32:1107-1117.23. Chen JDZ, Zhiyue L, Pan J, McCallum RW. Abnormal gastric myo-electrical activity and delayed gastric emptying in patients withsymptoms suggestive of gastroparesis. Dig Dis Sci. 1996;41:1538-1545.24. Bassaganya-Riera J, Hontecillas R, Beitz DC. Colonic anti-inflamma-tory mechanisms of conjugated linoleic acid. Clin Nutr. 2002;21:451-459.25. Lorea Baroja M, Kirjavainen PV, Hekmat S, Reid G. Anti-inflamma-tory effects of probiotic yogurt in inflammatory bowel disease pa-tients. Clin Exp Immunol. 2007;149:470-479.26. Daddaoua A, Puerta V, Requena P, Martínez-Férez A, Guadix E,Sánchez de Medina F, Zarzuelo A, Suárez MD, Boza JJ, Martínez-Augustin O. Goat milk oligosaccharides are anti-inflammatory in ratswith hapten-induced colitis. J Nutr. 2006;136:672-676.27. Russ A, Barnett M, McNabb W, Andersen R, Reynolds G, Roy N.Post-weaning effects of milk and milk components on the intestinalmucosa in inflammation. Mutat Res. 2010;690:64-70.28. Park YW, Juárez M, Ramos M, Haenlein GFW. Physico-chemicalcharacteristics of goat and sheep milk. Small Rumin Res. 2007;68:88-113.29. Adolfsson O, Meydani SN, Russell RM. Yogurt and gut function. Am JClin Nutr. 2004;80:245-256.30. Van Limbergen J, Wilson DC, Satsangi J. The genetics of Crohn’sdisease. Annu Rev Genomics Hum Genet. 2009;10:89-116.1172 August 2011 Volume 111 Number 8