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RESEARCH
Qualitative Research
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
DEBORAH NOLAN-CLARK; LINDA C. TAPSELL, PhD, MHPEd; RONG HU, MSc; DUG YEO HAN, PhD;
LYNNETTE R. FERGUSON, MSc, DPhil (Oxon), DSc
ABSTRACT
Background Dairy products have been perceived as having
the potential to cause adverse effects in individuals with
Crohn’s disease (CD) and are often avoided, potentially
increasing the risk of osteoporosis and related morbidity
associated with inadequate dietary calcium intake.
Objective To evaluate the self-reported effects of dairy
products on CD symptoms and to determine whether
these effects differed between types of dairy products
consumed and disease state or location.
Design Secondary analysis of dietary survey and clinical
data from participants in the Genes and Diet in Inflam-
matory Bowel Disease study based in Auckland, New
Zealand.
Subjects/setting One hundred and sixty-five men and
women diagnosed with CD for which both dietary survey
data and clinical information were available.
Statistical analyses performed ␹2
analysis was conducted to
assess whether significant differences in the proportions
of responses relating to a worsening of CD symptoms
from individual dairy products were evident between in-
dividuals with active or quiescent CD, or ileal or colonic
disease locations. Odds ratios with confidence interval
were calculated to determine whether CD location was
associated with risk of any type of adverse reaction to
milk products. Logit scales were utilized to depict self-
reported CD symptoms associated with individual dairy
product consumption for ileal and colonic CD patients.
Results Dairy products had no effect on self-reported CD
symptoms for most people. Dairy products with a high fat
content were most frequently reported to worsen per-
ceived CD symptoms. Clinically, self-reported CD activity
status did not influence responses to dairy products; how-
ever, colonic inflammation was more frequently associ-
ated with adverse CD effects in comparison to ileal CD
involvement.
Conclusions Research outcomes question the necessity of
dairy product avoidance in CD patients and illustrate the
highly individual nature of dairy product tolerance in this
clinical population.
J Am Diet Assoc. 2011;111:1165-1172.
C
rohn’s disease (CD) is a debilitating form of inflam-
matory bowel disease that can affect any location of
the gastrointestinal tract, resulting in considerable
morbidity (1). The incidence of CD in a New ZealandϪ
based 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 Zealand
population.
Dairy products have often been perceived as having the
potential to cause adverse effects in individuals with CD
and so are often avoided, potentially increasing the risk of
osteoporosis and related morbidity associated with inad-
equate dietary calcium intake.
There are several hypotheses proposed to explain this
perceived adverse effect. Perhaps the most frequently
reported theory relates to the prevalence of lactose intol-
erance in CD patients. A higher prevalence of lactose
malabsorption, as diagnosed by hydrogen breath testing,
in individuals with CD has been reported in comparison
to controls (3). Allergy to major milk proteins may be
another reason that a small number of CD patients report
adverse effects from dairy products (4). In addition, indi-
viduals with CD might be susceptible to secondary lactose
D. 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 and
Director, Smart Foods Centre, University of Wollongong,
Wollongong, NSW, Australia. R. Hu and D. Y. Han are
statisticians, Discipline of Nutrition, University of Auck-
land, Auckland, New Zealand. L. R. Ferguson is pro-
gram leader, Nutrigenomics New Zealand and Head of
the 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.au
Manuscript accepted: January 5, 2011.
Copyright © 2011 by the American Dietetic
Association.
0002-8223/$36.00
doi: 10.1016/j.jada.2011.05.004
© 2011 by the American Dietetic Association Journal of the AMERICAN DIETETIC ASSOCIATION 1165
intolerance. During the periods of the acute gastrointes-
tinal inflammation characteristic of CD, quantities of lac-
tase, the lactose digesting enzyme, may decline in the
duodenal mucosa, resulting in the gastrointestinal dis-
comfort associated with lactose maldigestion (5). Thus,
disease state (active or quiescent) can affect response to
dairy products in this clinical population.
Disease location may further influence tolerance to
dairy 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 colonic
CD (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 region
of the gastrointestinal tract may have difficulties with
lactose intolerance and, thus, perceive that adverse CD
symptoms are associated with consumption of dairy prod-
ucts.
The aim of this study was to evaluate the self-reported
effects of dairy products on CD symptoms and to deter-
mine whether these perceived effects differed between
types of dairy products consumed, disease state, or loca-
tion. The identification of dairy-mediated effects on CD
symptoms may facilitate the provision of more targeted
dietary advice on dairy products for this clinical popula-
tion.
METHODS
This study was based on a secondary analysis of dietary
survey and clinical data from 165 adults with CD. All
subjects were white participants in the Genes and Diet in
Inflammatory 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 of
dietary and clinical data was available.
The original study was approved by the New Zealand
Multi-Region Human Ethics Committee (MEC/04/12/
011). Access to the data for this secondary analysis met
ethical approval and all information utilized was coded to
protect the anonymity of participants.
Clinical Data
Clinical information including age, inflammatory bowel
disease 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 part
of the Genes and Diet in Inflammatory Bowel Disease
study. Individuals with a latest Montreal classification of
L1, indicating ileal involvement, were grouped into the
Ileal Involvement group. Although individuals with a
classification of L2, indicating isolated colonic involve-
ment, were classified as the Colonic Involvement group.
To ensure that effects observed could be attributable to
either colonic or ileal disease locations, individuals with a
classification of L3 and L4 (indicating ileocolonic and
upper gastrointestinal disease in the presence of classifi-
cations of L1 to L3, respectively (9), were excluded from
this part of the analysis.
Additional clinical information was sought from the
dietary questionnaire whereby subjects self-reported cur-
rent disease activity status (active or quiescent).
Dietary Data
For 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 this
study was developed in conjunction with CD patients and
aimed 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 in
a subset of CD patients with consistent results indicating
good survey reliability. All data were cross-checked inde-
pendently by two researchers to ensure accuracy. The
complete dietary questionnaire is described in more de-
tail elsewhere (7).
Self-reported data on effects of dairy products were
extracted from this dietary questionnaire, which required
participants to indicate whether particular foods items
made their inflammatory bowel disease condition “defi-
nitely worse,” “probably worse,” “had no effect,” “probably
better,” or “definitely better.” Subjects reporting that par-
ticular dairy products made their condition either “defi-
nitely” or “probably worse” were categorized as having
CD symptom worsening associated with consumption of
that food. Similarly, those reporting a “definitely” or
“probably better” effect of a particular dairy product on
their CD condition were categorized as having a benefi-
cial effect on CD symptoms from consuming that food.
Several open-ended questions within the questionnaire
were also analyzed to determine qualitative information
about perceived effects on CD condition associated with
particular 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 about
the frequency and nature of having any form of adverse
reaction (such as nausea or bloating) to milk products
was 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 consuming
milk products?
● Have you seen a health professional about your reac-
tions to milk products (if applicable)?
● Have you been formally diagnosed with an intolerance
or allergy?
Data Analysis
Qualitative data (including reports on symptoms of ad-
verse reactions to dairy products and of symptomatic
differences from different types of dairy products con-
sumed) were categorized accordingly and the proportion
of individuals responding to each category was calcu-
lated.
␹2
analysis was conducted to assess whether substan-
tial differences in the proportions of responses relating to
a worsening of CD symptoms from individual dairy prod-
1166 August 2011 Volume 111 Number 8
ucts were evident between individuals with active or qui-
escent CD, or ileal or colonic disease locations. Odds
ratios with confidence interval were calculated to deter-
mine whether CD location was associated with a risk of
having any type of adverse reaction to milk products.
Results were considered statistically significant at
PϽ0.05.
For interpretation of data grouped by disease location
(ileal vs colonic), logit scales were utilized to create a clear
visual representation of self-reported CD symptoms asso-
ciated with consumption of individual dairy products
while addressing the issue of the variance of proportions
between the groups.
All analyses were conducted using SPSS (V15.0 1989-
2006, SPSS Inc, Chicago IL), R (2009, R Development
Core Team, Vienna, Austria, http://www.R-project.org.ref),
and SAS (V9.1, 2003, SAS Institute, Cary, NC) statistical
software packages.
RESULTS
Dietary and clinical data were available for 165 patients
with CD (mean ageϭ48.8Ϯ16.3 years). The study sample
was predominantly female (males, nϭ49; mean ageϭ
50.6Ϯ17.8 years; females, nϭ116; mean ageϭ48.0Ϯ15.6
years).
Clinical Profiles
Of the study sample, 80 patients (48.5%) reported that
their CD was currently active and 82 (49.7%) identified
their CD as being in the quiescent phase. Three patients
did not answer this survey question. There was no differ-
ence between the sexes in the proportion reporting an
active CD period at the time of survey completion
(␹2
ϭ0.38, Pϭ0.54).
Data were available for 160 patients on the latest Mon-
treal classification indicating the location of CD. Isolated
ileal disease involvement was present for 32.7% of the
study sample, while 27.9% displayed evidence of isolated
colonic involvement (Table 1).
There was no significant difference between males and
females in terms of CD location (␹2
ϭ0.98; Pϭ0.81).
Effects of All Dairy Products on Self-Reported CD Symptoms
Forty-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 adverse
event 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 isolated
event.
A formal diagnosis of lactose intolerance was reported
for 11 patients (6.7% of the study population). A total of
41 CD patients described adverse symptoms experienced
after consumption of milk products (Figure 1).
As an aside to these data, naturopaths were listed as
the health practitioner most frequently sought for advice
regarding 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 one
individual reported seeking advice in relation to dairy
product intolerance from a registered dietitian.
Associations Between Individual Dairy Products and Self-
Reported CD Symptoms
No effect on CD symptoms was reported to be associated
with the consumption of butter, standard cow’s milk, and
reduced-fat cow’s milk in 71.5%, 55.2%, and 58.2% of all
patients, respectively. Dairy products most frequently
reported to worsen CD symptoms were cream (43.6%), ice
cream (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 favorable
effects on CD symptoms. The response to this question
was quite varied (Table 2).
Cheese
When asked whether the type of cheese may influence CD
symptoms, 26.1% of participants responded positively.
The flavor strength of the cheese was most frequently
Table 1. Latest subject Montreal classifications for location of
Crohn’s disease (CD) (nϭ160)
Montreal classification
for CD location Group Males Females
4™™™™™™™™™™ n (%) ™™™™™™™™™™3
L1 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 upper
disease
9 (5.5) 3 (6.1) 6 (5.2)
Figure 1. Adverse symptoms reported by Crohn’s disease patients
after consumption of dairy products (nϭ41). Some patients reported
more 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
reported as influencing tolerance, with 15 patients re-
porting that increased strength cheese decreased toler-
ance. Richer/soft cheeses were reported to worsen CD
symptoms for nine patients, with a preference for feta
and edam cheese varieties reported by eight and seven
patients, respectively. Cheeses with a lower fat content
were reported to increase tolerance (nϭ6), as did hard
cheeses (nϭ5) and plain cheeses without added herbs
(nϭ3). Melted cheese was associated with worsening CD
symptoms for four patients.
Yogurt
In total, 23.0% of respondents reported that the type of
yogurt consumed may also be a key factor relating to
whether it would be tolerated. Patients reported that
yogurts containing live cultures such as acidophilus were
most beneficial to CD symptoms (nϭ19), while natural
yogurt was preferable to sweetened alternatives for 11
patients. A preference for reduced-fat yogurt was re-
ported (nϭ9), with yogurt lacking seeds or fruit preferred
by an additional 4.8% (nϭ8) of individuals.
Disease Activity and Self-Reported Effect of Dairy Products on
CD Symptoms
There were no significant differences in the proportion of
individuals reporting a worsening of CD symptoms asso-
ciated with the consumption of individual dairy products
between patients in the active or quiescent CD state
(Table 3).
Site of Disease and Self-Reported Effect of Dairy Products on
CD Symptoms
Likewise, no significant differences were detected be-
tween self-reported CD symptoms associated with con-
sumption of individual dairy products and ileal or colonic
disease location (data not shown). However, considerably
fewer patients with ileal disease activity reported ever
having any type of adverse reaction to dairy products
compared to those with colonic disease involvement
(␹2
ϭ5.90; Pϭ0.015; odds ratioϭ0.32; 95% confidence in-
terval: 0.13 to 0.82; Pϭ0.017).
Logit scales of self-reported improvement or worsening
of 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 item
CD symptoms
worse
No difference to
CD symptoms
CD symptoms
better
Question not
answered
4™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™ n (%) ™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™3
Standard 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 item
CD Symptoms Worse No Difference in CD Symptoms
Active CD
(n‫)08؍‬
Quiescent CD
(n‫؍‬ 82)
Active CD
(n‫)08؍‬
Quiescent CD
(n‫؍‬ 82) ␹2
analysis
4™™™™™™™™™™™™™™™™™™™™™™™™™™™™ n ™™™™™™™™™™™™™™™™™™™™™™™™™™3
Standard cow’s milk 21 30 45 43 (␹2
ϭ1.28; Pϭ0.26)
Reduced-fat cow’s milk 14 15 46 48 (␹2
ϭ0.004; Pϭ0.95)
Butter 15 9 57 61 (␹2
ϭ1.61; Pϭ0.20)
Custard 17 14 50 54 (␹2
ϭ0.48; Pϭ0.51)
Goat’s milk 7 4 13 13 (␹2
ϭ0.58; Pϭ0.45)
Sheep’s milk 5 6 13 13 (␹2
ϭ0.64; Pϭ0.80)
Ice cream 31 30 45 47 (␹2
ϭ0.053; Pϭ0.82)
Yogurt 16 14 46 47 (␹2
ϭ0.14; Pϭ0.71)
Cheese 27 29 46 47 (␹2
ϭ0.02; Pϭ0.883)
Cream 36 36 35 35 (␹2
ϭ0.00; Pϭ1.00)
1168 August 2011 Volume 111 Number 8
tinal (ileal) or colonic CD involvement are displayed in
Figure 2A and B. Only dairy products with at least one
reported beneficial/adverse effect on CD symptoms can be
plotted 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 individuals
with colonic involvement.
A
Standard Milk
Reduced-Fat Milk
Custard
Ice Cream
Yogurt
Cheese
Cream
1% %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 symptoms
IncreasingperceivedimprovementofCDsymptoms
B
Standard Milk
Reduced-Fat Milk
Butter Custard
Yogurt
Cheese
1% %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 symptoms
IncreasingperceivedimprovementofCDsymptoms
Figure 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
DISCUSSION
This analysis of self-reported effects of dairy products on
CD symptoms has clearly illustrated the extent of varia-
tion in perceived tolerance to these items within this
clinical population.
Most importantly, the majority of the study sample
reported that consumption of dairy products made no
difference to CD symptoms. This finding reinforces the
need to determine tolerance to dairy products in CD pa-
tients before encouraging widespread avoidance of this
food group, an idea that may still be encouraged by some
physicians and many alternative health consultants. Al-
though it may be pertinent to avoid some dairy products
for CD patients with congenital hypolactasia or during
periods of active disease, unnecessary avoidance of all
dairy products by this clinical group without appropriate
nutrition support may have deleterious consequences.
Individuals with CD are more susceptible to osteoporosis
(10). Prolonged corticosteroid use to induce remission of
inflammation has been demonstrated to reduce bone min-
eral density in CD patients (11). CD itself may be an
independent risk factor for osteoporosis (12), with an
increase in proinflammatory cytokines associated with
disease pathogenesis mediating excessive bone resorption
(13). According to the National New Zealand Nutrition
Survey (14), milk, cheese, and other dairy products were
the highest food contributors of dietary calcium in the
New 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 bowel
disease, and increased dairy product consumption has
been reported to retard bone loss (16). Eliminating dairy
products as the highest contributor of dietary calcium
from the diet may further exacerbate risk of osteoporosis
and related morbidity in individuals with CD in New
Zealand.
Intermittent secondary lactose intolerance may be ex-
perienced by some individuals with CD during periods of
active gastrointestinal inflammation (5). Formally diag-
nosed lactose intolerance was reported for only a small
proportion of the study sample. However, symptoms con-
sistent with lactose maldigestion, including bloating, di-
arrhea, and gas (17), were the most frequently reported
adverse 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 of
this nature is often sought as an adjunct to conventional
medical therapies in an effort to establish a sense of
control over this debilitating condition (19). This practice
was evident in this clinical population, whereby naturo-
paths were the most frequently used source of advice for
issues with dairy product tolerance. Ensuring accurate
advice 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 in
patients with CD (20). Thus, for individuals reporting
adverse CD effects associated with the consumption of
dairy 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 associated
with 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 study
sample reporting a worsening of CD symptoms associated
with its consumption. The perceived adverse effects may
relate to the high fat content of this item. High dietary fat
intakes decrease gastric emptying rates (21). In addition,
disorders in gastrointestinal motility have been observed
in this clinical population, with affected individuals more
likely to experience gastric hypomotility than controls
(22). This is particularly pertinent as gastric hypomotility
is associated with delayed gastric emptying (23). Effects
of dietary-fatϪmediated decreases in gastric emptying
after consumption of dairy products rich in fat may be
more 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 product
consumption in this study.
It should also be noted that cream, like many other
foods, is rarely consumed in isolation and generally forms
a component of a meal. Thus, there is a possibility that
perceived worsening of CD symptoms assigned to partic-
ular foods may relate to the cuisine context in which
these items are consumed rather than the food item itself.
However, other dairy products containing higher
amounts of fat, including ice cream and cheese, were also
associated with a perceived worsening of CD symptoms in
a larger number of patients in comparison to their lower
fat dairy counterparts. Furthermore, reduced-fat cheese
and yogurt varieties were perceived as more tolerable.
These findings illustrate that the fat content of dairy
products may be a key factor influencing tolerance in this
clinical population.
Of interest was the finding that butter, a dairy product
that 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 being
consumed in quantities great enough to influence gastric
stasis in the study sample. Conversely, butter contains a
relatively high proportion of conjugated linoleic acid,
which has been implicated in the amelioration of inflam-
mation in experimental models of inflammatory bowel
disease, particularly in relation to colitis (24). Thus, the
lack of perceived worsening of CD symptoms associated
with butter consumption may be the result of this conju-
gated linoleic acidϪmediated anti-inflammatory effect.
Probiotic-containing yogurt has been demonstrated to
attenuate markers of inflammation in individuals with
inflammatory bowel disease (25).The dairy product most
frequently associated with having self-reported beneficial
effects 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 of
individuals than had experienced beneficial effects from
it. A limitation of the survey used for analysis was that it
failed to distinguish between CD effects experienced from
1170 August 2011 Volume 111 Number 8
probiotic yogurt and nonprobiotic varieties. An analysis
of qualitative responses indicated that for individuals
experiencing a difference in CD symptoms dependent on
the type of yogurt consumed, those containing live cul-
tures and probiotics were most frequently associated with
beneficial effects. Thus, probiotic yogurts appeared to
benefit individuals with CD in preference to yogurt with-
out live cultures; however, this is an area that requires
further research, and a placebo effect cannot be ruled out.
It was expected from previous observations (7) that
goat and sheep milk may result in less perceived worsen-
ing of CD symptoms than their bovine counterparts. Goat
milk in particular contains oligosaccharides, which have
demonstrated anti-inflammatory effects in rat models of
inflammatory bowel disease (26). In addition, sheep and
goat’s milk contain higher proportions of medium chain
triglycerides 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 of
individuals reported beneficial effects on CD symptoms
associated with consumption of these milk products, with
a slightly greater proportion reporting symptom worsen-
ing. However, because the majority of individuals did not
answer this question, indicating that they did not con-
sume these items, it was not possible to determine the
true effect of goat and sheep milk on CD symptoms. Given
emerging evidence to suggest a potentially beneficial role
for sheep and goat milks in relation to CD symptoms,
evaluating the true effects of these products may be an
important area for future research.
The lactose content of the individual dairy products did
not seem to influence self-reported CD symptoms in this
study sample. Cow’s milk, which contains a considerably
greater amount of lactose per serving than cream, ice
cream, or cheese (17), was associated with comparatively
less perceived symptom worsening. In addition, lactose
tolerance may be influenced by gastrointestinal transit
time, with higher-fat milk products traveling less rapidly
throughout the small intestine, affording lactase a
greater opportunity for lactose digestion (17). Thus, if
lactose was a key factor relating to CD symptoms in this
study sample, reduced-fat cow’s milk would have been
associated with less favorable CD symptoms than its
standard counterpart. As this was not the case, it appears
that the lactose content of individual dairy products does
not have a major impact on CD symptoms. In contrast,
qualitative responses regarding the types of cheese and
yogurt consumed, which may influence tolerance, indi-
cate a lactose effect in a small proportion of the study
sample. The preference for yogurt containing live bacte-
ria previously outlined may be associated with tolerance
to 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 comparison
to soft cheeses. Hard cheeses contain slightly less lactose
than soft varieties, such as cream cheese (17), and so may
be better tolerated by individuals with lactose maldiges-
tion.
In this study, disease activity (active vs quiescent) did
not appear to influence perceived effects of dairy products
on CD symptoms, with a similar proportion of individuals
reporting either adverse or beneficial dairy-mediated ef-
fects on CD symptoms irrespective of disease activity.
This finding challenges the necessity of dairy avoidance
during active CD. However, as disease activity was sub-
jectively reported, these findings should be interpreted
with caution.
Reference to the logit scales developed in this analysis
illustrate that individuals with isolated colonic inflam-
mation appeared to have an increase in perceived adverse
CD symptoms associated with the consumption of re-
duced-fat cow’s milk, custard, sheep’s milk, and yogurt in
comparison to those with isolated small intestinal (ileal)
involvement. This was an unexpected finding, as it was
anticipated that individuals with small intestinal inflam-
mation would be more likely to have issues with lactose
and, thus, dairy product tolerance, given that lactase
lines 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 investigation
and may relate to functional differences in gut microbiota
among individuals with CD affecting varied locations
throughout the gastrointestinal tract.
A possible explanation for the unexpected outcomes
observed in relation to dairy product tolerance in this
study may be attributable to individual genetic variation.
Although clear genomic loci, such as NOD2 and IL23R,
have been repeatedly associated with CD in genome-wide
association studies (30), there is a paucity of evidence in
relation to genetic factors that may influence tolerance to
dairy products in individuals with this inflammatory con-
dition. Future research efforts should consider the impact
of genetic interactions on dairy product tolerance in CD to
conclusively address the research question.
This study was limited by the subjective nature of the
dietary questionnaire used and the relatively small size
of the CD sample, which make it difficult to extrapolate
findings to the wider CD community. In addition, infor-
mation relating to the specific macronutrient composition
or processing methods used for each of the dairy products
included within this study was not acquired. Results ob-
tained may only be applicable to this study sample and
may not apply to individuals consuming dairy products
that differ greatly from the generic food composition of
New Zealand dairy products. Furthermore, information
about the quantity of dairy food items required to elicit
effects on self-reported CD symptoms was not collected in
the dietary questionnaire. Quantification of such items
may provide further insight into the factors that can
influence tolerance to dairy products in this clinical pop-
ulation, in particular whether there is a threshold of
consumption that must be achieved in order to influence
perceived symptoms. Despite these limitations, this is the
first study to assess the perceived effects of dairy prod-
ucts on CD symptoms, taking into account both clinical
and qualitative data, and provide some important in-
sights for both future research and dietetics practice
within this clinical population.
CONCLUSIONS
In conclusion, within this study sample of CD patients in
Auckland, New Zealand, dairy products in general had no
August 2011 ● Journal of the AMERICAN DIETETIC ASSOCIATION 1171
effect on self-reported CD symptoms for most people.
When analyzed according to type of dairy product, items
with a high fat content were most frequently reported to
worsen perceived CD symptoms. The lactose content of
individual dairy products did not influence self-reported
CD symptoms for the majority of patients. Clinically, CD
activity status did not influence responses to dairy prod-
ucts; however, site of disease appeared to have an effect.
Colonic inflammation was more frequently associated
with an increase in reported adverse CD effects from
dairy product consumption in comparison to ileal CD
involvement. Results from this exploratory study rein-
force the idea that that “one size does not fit all” when it
comes to making dietary recommendations relating to
dairy product consumption for individuals with CD. Fu-
ture research should consider the identification of genetic
variants that might further explain tolerance to dairy
products 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 received
through an Australian Endeavour Research Fellowship
to support travels to New Zealand to collaborate with
Nutrigenomics New Zealand at the University of Auck-
land. However, as this study was based on a secondary
analysis of existing data, no additional funds were uti-
lized.
Deborah Nolan-Clark is a recipient of an Australian
Endeavour Research Fellowship. The authors would like
to acknowledge the participants of the present study and
thank Philippa Dryland and Virginia Parslow for assis-
tance with the provision of dietary questionnaires. Nu-
trigenomics New Zealand is a collaboration between
AgResearch Ltd, Plant and Food Research and The Uni-
versity of Auckland and is largely funded by the Founda-
tion for Research, Science and Technology.
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1172 August 2011 Volume 111 Number 8

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  • 1. RESEARCH Qualitative Research 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 DEBORAH NOLAN-CLARK; LINDA C. TAPSELL, PhD, MHPEd; RONG HU, MSc; DUG YEO HAN, PhD; LYNNETTE R. FERGUSON, MSc, DPhil (Oxon), DSc ABSTRACT Background Dairy products have been perceived as having the potential to cause adverse effects in individuals with Crohn’s disease (CD) and are often avoided, potentially increasing the risk of osteoporosis and related morbidity associated with inadequate dietary calcium intake. Objective To evaluate the self-reported effects of dairy products on CD symptoms and to determine whether these effects differed between types of dairy products consumed and disease state or location. Design Secondary analysis of dietary survey and clinical data from participants in the Genes and Diet in Inflam- matory Bowel Disease study based in Auckland, New Zealand. Subjects/setting One hundred and sixty-five men and women diagnosed with CD for which both dietary survey data and clinical information were available. Statistical analyses performed ␹2 analysis was conducted to assess whether significant differences in the proportions of responses relating to a worsening of CD symptoms from individual dairy products were evident between in- dividuals with active or quiescent CD, or ileal or colonic disease locations. Odds ratios with confidence interval were calculated to determine whether CD location was associated with risk of any type of adverse reaction to milk products. Logit scales were utilized to depict self- reported CD symptoms associated with individual dairy product consumption for ileal and colonic CD patients. Results Dairy products had no effect on self-reported CD symptoms for most people. Dairy products with a high fat content were most frequently reported to worsen per- ceived CD symptoms. Clinically, self-reported CD activity status did not influence responses to dairy products; how- ever, colonic inflammation was more frequently associ- ated with adverse CD effects in comparison to ileal CD involvement. Conclusions Research outcomes question the necessity of dairy product avoidance in CD patients and illustrate the highly individual nature of dairy product tolerance in this clinical population. J Am Diet Assoc. 2011;111:1165-1172. C rohn’s disease (CD) is a debilitating form of inflam- matory bowel disease that can affect any location of the gastrointestinal tract, resulting in considerable morbidity (1). The incidence of CD in a New ZealandϪ based 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 Zealand population. Dairy products have often been perceived as having the potential to cause adverse effects in individuals with CD and so are often avoided, potentially increasing the risk of osteoporosis and related morbidity associated with inad- equate dietary calcium intake. There are several hypotheses proposed to explain this perceived adverse effect. Perhaps the most frequently reported theory relates to the prevalence of lactose intol- erance in CD patients. A higher prevalence of lactose malabsorption, as diagnosed by hydrogen breath testing, in individuals with CD has been reported in comparison to controls (3). Allergy to major milk proteins may be another reason that a small number of CD patients report adverse effects from dairy products (4). In addition, indi- viduals with CD might be susceptible to secondary lactose D. 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 and Director, Smart Foods Centre, University of Wollongong, Wollongong, NSW, Australia. R. Hu and D. Y. Han are statisticians, Discipline of Nutrition, University of Auck- land, Auckland, New Zealand. L. R. Ferguson is pro- gram leader, Nutrigenomics New Zealand and Head of the 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.au Manuscript accepted: January 5, 2011. Copyright © 2011 by the American Dietetic Association. 0002-8223/$36.00 doi: 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 the duodenal mucosa, resulting in the gastrointestinal dis- comfort associated with lactose maldigestion (5). Thus, disease state (active or quiescent) can affect response to dairy products in this clinical population. Disease location may further influence tolerance to dairy 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 colonic CD (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 region of the gastrointestinal tract may have difficulties with lactose intolerance and, thus, perceive that adverse CD symptoms are associated with consumption of dairy prod- ucts. The aim of this study was to evaluate the self-reported effects of dairy products on CD symptoms and to deter- mine whether these perceived effects differed between types of dairy products consumed, disease state, or loca- tion. The identification of dairy-mediated effects on CD symptoms may facilitate the provision of more targeted dietary advice on dairy products for this clinical popula- tion. METHODS This study was based on a secondary analysis of dietary survey and clinical data from 165 adults with CD. All subjects were white participants in the Genes and Diet in Inflammatory 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 of dietary and clinical data was available. The original study was approved by the New Zealand Multi-Region Human Ethics Committee (MEC/04/12/ 011). Access to the data for this secondary analysis met ethical approval and all information utilized was coded to protect the anonymity of participants. Clinical Data Clinical information including age, inflammatory bowel disease 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 part of the Genes and Diet in Inflammatory Bowel Disease study. Individuals with a latest Montreal classification of L1, indicating ileal involvement, were grouped into the Ileal Involvement group. Although individuals with a classification of L2, indicating isolated colonic involve- ment, were classified as the Colonic Involvement group. To ensure that effects observed could be attributable to either colonic or ileal disease locations, individuals with a classification of L3 and L4 (indicating ileocolonic and upper gastrointestinal disease in the presence of classifi- cations of L1 to L3, respectively (9), were excluded from this part of the analysis. Additional clinical information was sought from the dietary questionnaire whereby subjects self-reported cur- rent disease activity status (active or quiescent). Dietary Data For 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 this study was developed in conjunction with CD patients and aimed 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 in a subset of CD patients with consistent results indicating good survey reliability. All data were cross-checked inde- pendently by two researchers to ensure accuracy. The complete dietary questionnaire is described in more de- tail elsewhere (7). Self-reported data on effects of dairy products were extracted from this dietary questionnaire, which required participants to indicate whether particular foods items made their inflammatory bowel disease condition “defi- nitely worse,” “probably worse,” “had no effect,” “probably better,” or “definitely better.” Subjects reporting that par- ticular dairy products made their condition either “defi- nitely” or “probably worse” were categorized as having CD symptom worsening associated with consumption of that food. Similarly, those reporting a “definitely” or “probably better” effect of a particular dairy product on their CD condition were categorized as having a benefi- cial effect on CD symptoms from consuming that food. Several open-ended questions within the questionnaire were also analyzed to determine qualitative information about perceived effects on CD condition associated with particular 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 about the frequency and nature of having any form of adverse reaction (such as nausea or bloating) to milk products was 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 consuming milk products? ● Have you seen a health professional about your reac- tions to milk products (if applicable)? ● Have you been formally diagnosed with an intolerance or allergy? Data Analysis Qualitative data (including reports on symptoms of ad- verse reactions to dairy products and of symptomatic differences from different types of dairy products con- sumed) were categorized accordingly and the proportion of individuals responding to each category was calcu- lated. ␹2 analysis was conducted to assess whether substan- tial differences in the proportions of responses relating to a 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. Odds ratios with confidence interval were calculated to deter- mine whether CD location was associated with a risk of having any type of adverse reaction to milk products. Results were considered statistically significant at PϽ0.05. For interpretation of data grouped by disease location (ileal vs colonic), logit scales were utilized to create a clear visual representation of self-reported CD symptoms asso- ciated with consumption of individual dairy products while addressing the issue of the variance of proportions between the groups. All analyses were conducted using SPSS (V15.0 1989- 2006, SPSS Inc, Chicago IL), R (2009, R Development Core Team, Vienna, Austria, http://www.R-project.org.ref), and SAS (V9.1, 2003, SAS Institute, Cary, NC) statistical software packages. RESULTS Dietary and clinical data were available for 165 patients with CD (mean ageϭ48.8Ϯ16.3 years). The study sample was predominantly female (males, nϭ49; mean ageϭ 50.6Ϯ17.8 years; females, nϭ116; mean ageϭ48.0Ϯ15.6 years). Clinical Profiles Of the study sample, 80 patients (48.5%) reported that their CD was currently active and 82 (49.7%) identified their CD as being in the quiescent phase. Three patients did not answer this survey question. There was no differ- ence between the sexes in the proportion reporting an active CD period at the time of survey completion (␹2 ϭ0.38, Pϭ0.54). Data were available for 160 patients on the latest Mon- treal classification indicating the location of CD. Isolated ileal disease involvement was present for 32.7% of the study sample, while 27.9% displayed evidence of isolated colonic involvement (Table 1). There was no significant difference between males and females in terms of CD location (␹2 ϭ0.98; Pϭ0.81). Effects of All Dairy Products on Self-Reported CD Symptoms Forty-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 adverse event 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 isolated event. A formal diagnosis of lactose intolerance was reported for 11 patients (6.7% of the study population). A total of 41 CD patients described adverse symptoms experienced after consumption of milk products (Figure 1). As an aside to these data, naturopaths were listed as the health practitioner most frequently sought for advice regarding 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 one individual reported seeking advice in relation to dairy product intolerance from a registered dietitian. Associations Between Individual Dairy Products and Self- Reported CD Symptoms No effect on CD symptoms was reported to be associated with the consumption of butter, standard cow’s milk, and reduced-fat cow’s milk in 71.5%, 55.2%, and 58.2% of all patients, respectively. Dairy products most frequently reported to worsen CD symptoms were cream (43.6%), ice cream (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 favorable effects on CD symptoms. The response to this question was quite varied (Table 2). Cheese When asked whether the type of cheese may influence CD symptoms, 26.1% of participants responded positively. The flavor strength of the cheese was most frequently Table 1. Latest subject Montreal classifications for location of Crohn’s disease (CD) (nϭ160) Montreal classification for CD location Group Males Females 4™™™™™™™™™™ n (%) ™™™™™™™™™™3 L1 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 upper disease 9 (5.5) 3 (6.1) 6 (5.2) Figure 1. Adverse symptoms reported by Crohn’s disease patients after consumption of dairy products (nϭ41). Some patients reported more 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 CD symptoms for nine patients, with a preference for feta and edam cheese varieties reported by eight and seven patients, respectively. Cheeses with a lower fat content were reported to increase tolerance (nϭ6), as did hard cheeses (nϭ5) and plain cheeses without added herbs (nϭ3). Melted cheese was associated with worsening CD symptoms for four patients. Yogurt In total, 23.0% of respondents reported that the type of yogurt consumed may also be a key factor relating to whether it would be tolerated. Patients reported that yogurts containing live cultures such as acidophilus were most beneficial to CD symptoms (nϭ19), while natural yogurt was preferable to sweetened alternatives for 11 patients. A preference for reduced-fat yogurt was re- ported (nϭ9), with yogurt lacking seeds or fruit preferred by an additional 4.8% (nϭ8) of individuals. Disease Activity and Self-Reported Effect of Dairy Products on CD Symptoms There were no significant differences in the proportion of individuals reporting a worsening of CD symptoms asso- ciated with the consumption of individual dairy products between patients in the active or quiescent CD state (Table 3). Site of Disease and Self-Reported Effect of Dairy Products on CD Symptoms Likewise, no significant differences were detected be- tween self-reported CD symptoms associated with con- sumption of individual dairy products and ileal or colonic disease location (data not shown). However, considerably fewer patients with ileal disease activity reported ever having any type of adverse reaction to dairy products compared to those with colonic disease involvement (␹2 ϭ5.90; Pϭ0.015; odds ratioϭ0.32; 95% confidence in- terval: 0.13 to 0.82; Pϭ0.017). Logit scales of self-reported improvement or worsening of 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 item CD symptoms worse No difference to CD symptoms CD symptoms better Question not answered 4™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™ n (%) ™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™™3 Standard 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 item CD Symptoms Worse No Difference in CD Symptoms Active CD (n‫)08؍‬ Quiescent CD (n‫؍‬ 82) Active CD (n‫)08؍‬ Quiescent CD (n‫؍‬ 82) ␹2 analysis 4™™™™™™™™™™™™™™™™™™™™™™™™™™™™ n ™™™™™™™™™™™™™™™™™™™™™™™™™™3 Standard cow’s milk 21 30 45 43 (␹2 ϭ1.28; Pϭ0.26) Reduced-fat cow’s milk 14 15 46 48 (␹2 ϭ0.004; Pϭ0.95) Butter 15 9 57 61 (␹2 ϭ1.61; Pϭ0.20) Custard 17 14 50 54 (␹2 ϭ0.48; Pϭ0.51) Goat’s milk 7 4 13 13 (␹2 ϭ0.58; Pϭ0.45) Sheep’s milk 5 6 13 13 (␹2 ϭ0.64; Pϭ0.80) Ice cream 31 30 45 47 (␹2 ϭ0.053; Pϭ0.82) Yogurt 16 14 46 47 (␹2 ϭ0.14; Pϭ0.71) Cheese 27 29 46 47 (␹2 ϭ0.02; Pϭ0.883) Cream 36 36 35 35 (␹2 ϭ0.00; Pϭ1.00) 1168 August 2011 Volume 111 Number 8
  • 5. tinal (ileal) or colonic CD involvement are displayed in Figure 2A and B. Only dairy products with at least one reported beneficial/adverse effect on CD symptoms can be plotted 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 individuals with colonic involvement. A Standard Milk Reduced-Fat Milk Custard Ice Cream Yogurt Cheese Cream 1% %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 symptoms IncreasingperceivedimprovementofCDsymptoms B Standard Milk Reduced-Fat Milk Butter Custard Yogurt Cheese 1% %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 symptoms IncreasingperceivedimprovementofCDsymptoms Figure 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. DISCUSSION This analysis of self-reported effects of dairy products on CD symptoms has clearly illustrated the extent of varia- tion in perceived tolerance to these items within this clinical population. Most importantly, the majority of the study sample reported that consumption of dairy products made no difference to CD symptoms. This finding reinforces the need to determine tolerance to dairy products in CD pa- tients before encouraging widespread avoidance of this food group, an idea that may still be encouraged by some physicians and many alternative health consultants. Al- though it may be pertinent to avoid some dairy products for CD patients with congenital hypolactasia or during periods of active disease, unnecessary avoidance of all dairy products by this clinical group without appropriate nutrition support may have deleterious consequences. Individuals with CD are more susceptible to osteoporosis (10). Prolonged corticosteroid use to induce remission of inflammation has been demonstrated to reduce bone min- eral density in CD patients (11). CD itself may be an independent risk factor for osteoporosis (12), with an increase in proinflammatory cytokines associated with disease pathogenesis mediating excessive bone resorption (13). According to the National New Zealand Nutrition Survey (14), milk, cheese, and other dairy products were the highest food contributors of dietary calcium in the New 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 bowel disease, and increased dairy product consumption has been reported to retard bone loss (16). Eliminating dairy products as the highest contributor of dietary calcium from the diet may further exacerbate risk of osteoporosis and related morbidity in individuals with CD in New Zealand. Intermittent secondary lactose intolerance may be ex- perienced by some individuals with CD during periods of active gastrointestinal inflammation (5). Formally diag- nosed lactose intolerance was reported for only a small proportion of the study sample. However, symptoms con- sistent with lactose maldigestion, including bloating, di- arrhea, and gas (17), were the most frequently reported adverse 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 of this nature is often sought as an adjunct to conventional medical therapies in an effort to establish a sense of control over this debilitating condition (19). This practice was evident in this clinical population, whereby naturo- paths were the most frequently used source of advice for issues with dairy product tolerance. Ensuring accurate advice 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 in patients with CD (20). Thus, for individuals reporting adverse CD effects associated with the consumption of dairy 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 associated with 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 study sample reporting a worsening of CD symptoms associated with its consumption. The perceived adverse effects may relate to the high fat content of this item. High dietary fat intakes decrease gastric emptying rates (21). In addition, disorders in gastrointestinal motility have been observed in this clinical population, with affected individuals more likely to experience gastric hypomotility than controls (22). This is particularly pertinent as gastric hypomotility is associated with delayed gastric emptying (23). Effects of dietary-fatϪmediated decreases in gastric emptying after consumption of dairy products rich in fat may be more 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 product consumption in this study. It should also be noted that cream, like many other foods, is rarely consumed in isolation and generally forms a component of a meal. Thus, there is a possibility that perceived worsening of CD symptoms assigned to partic- ular foods may relate to the cuisine context in which these items are consumed rather than the food item itself. However, other dairy products containing higher amounts of fat, including ice cream and cheese, were also associated with a perceived worsening of CD symptoms in a larger number of patients in comparison to their lower fat dairy counterparts. Furthermore, reduced-fat cheese and yogurt varieties were perceived as more tolerable. These findings illustrate that the fat content of dairy products may be a key factor influencing tolerance in this clinical population. Of interest was the finding that butter, a dairy product that 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 being consumed in quantities great enough to influence gastric stasis in the study sample. Conversely, butter contains a relatively high proportion of conjugated linoleic acid, which has been implicated in the amelioration of inflam- mation in experimental models of inflammatory bowel disease, particularly in relation to colitis (24). Thus, the lack of perceived worsening of CD symptoms associated with butter consumption may be the result of this conju- gated linoleic acidϪmediated anti-inflammatory effect. Probiotic-containing yogurt has been demonstrated to attenuate markers of inflammation in individuals with inflammatory bowel disease (25).The dairy product most frequently associated with having self-reported beneficial effects 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 of individuals than had experienced beneficial effects from it. A limitation of the survey used for analysis was that it failed to distinguish between CD effects experienced from 1170 August 2011 Volume 111 Number 8
  • 7. probiotic yogurt and nonprobiotic varieties. An analysis of qualitative responses indicated that for individuals experiencing a difference in CD symptoms dependent on the type of yogurt consumed, those containing live cul- tures and probiotics were most frequently associated with beneficial effects. Thus, probiotic yogurts appeared to benefit individuals with CD in preference to yogurt with- out live cultures; however, this is an area that requires further research, and a placebo effect cannot be ruled out. It was expected from previous observations (7) that goat and sheep milk may result in less perceived worsen- ing of CD symptoms than their bovine counterparts. Goat milk in particular contains oligosaccharides, which have demonstrated anti-inflammatory effects in rat models of inflammatory bowel disease (26). In addition, sheep and goat’s milk contain higher proportions of medium chain triglycerides 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 of individuals reported beneficial effects on CD symptoms associated with consumption of these milk products, with a slightly greater proportion reporting symptom worsen- ing. However, because the majority of individuals did not answer this question, indicating that they did not con- sume these items, it was not possible to determine the true effect of goat and sheep milk on CD symptoms. Given emerging evidence to suggest a potentially beneficial role for sheep and goat milks in relation to CD symptoms, evaluating the true effects of these products may be an important area for future research. The lactose content of the individual dairy products did not seem to influence self-reported CD symptoms in this study sample. Cow’s milk, which contains a considerably greater amount of lactose per serving than cream, ice cream, or cheese (17), was associated with comparatively less perceived symptom worsening. In addition, lactose tolerance may be influenced by gastrointestinal transit time, with higher-fat milk products traveling less rapidly throughout the small intestine, affording lactase a greater opportunity for lactose digestion (17). Thus, if lactose was a key factor relating to CD symptoms in this study sample, reduced-fat cow’s milk would have been associated with less favorable CD symptoms than its standard counterpart. As this was not the case, it appears that the lactose content of individual dairy products does not have a major impact on CD symptoms. In contrast, qualitative responses regarding the types of cheese and yogurt consumed, which may influence tolerance, indi- cate a lactose effect in a small proportion of the study sample. The preference for yogurt containing live bacte- ria previously outlined may be associated with tolerance to 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 comparison to soft cheeses. Hard cheeses contain slightly less lactose than soft varieties, such as cream cheese (17), and so may be better tolerated by individuals with lactose maldiges- tion. In this study, disease activity (active vs quiescent) did not appear to influence perceived effects of dairy products on CD symptoms, with a similar proportion of individuals reporting either adverse or beneficial dairy-mediated ef- fects on CD symptoms irrespective of disease activity. This finding challenges the necessity of dairy avoidance during active CD. However, as disease activity was sub- jectively reported, these findings should be interpreted with caution. Reference to the logit scales developed in this analysis illustrate that individuals with isolated colonic inflam- mation appeared to have an increase in perceived adverse CD symptoms associated with the consumption of re- duced-fat cow’s milk, custard, sheep’s milk, and yogurt in comparison to those with isolated small intestinal (ileal) involvement. This was an unexpected finding, as it was anticipated that individuals with small intestinal inflam- mation would be more likely to have issues with lactose and, thus, dairy product tolerance, given that lactase lines 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 investigation and may relate to functional differences in gut microbiota among individuals with CD affecting varied locations throughout the gastrointestinal tract. A possible explanation for the unexpected outcomes observed in relation to dairy product tolerance in this study may be attributable to individual genetic variation. Although clear genomic loci, such as NOD2 and IL23R, have been repeatedly associated with CD in genome-wide association studies (30), there is a paucity of evidence in relation to genetic factors that may influence tolerance to dairy products in individuals with this inflammatory con- dition. Future research efforts should consider the impact of genetic interactions on dairy product tolerance in CD to conclusively address the research question. This study was limited by the subjective nature of the dietary questionnaire used and the relatively small size of the CD sample, which make it difficult to extrapolate findings to the wider CD community. In addition, infor- mation relating to the specific macronutrient composition or processing methods used for each of the dairy products included within this study was not acquired. Results ob- tained may only be applicable to this study sample and may not apply to individuals consuming dairy products that differ greatly from the generic food composition of New Zealand dairy products. Furthermore, information about the quantity of dairy food items required to elicit effects on self-reported CD symptoms was not collected in the dietary questionnaire. Quantification of such items may provide further insight into the factors that can influence tolerance to dairy products in this clinical pop- ulation, in particular whether there is a threshold of consumption that must be achieved in order to influence perceived symptoms. Despite these limitations, this is the first study to assess the perceived effects of dairy prod- ucts on CD symptoms, taking into account both clinical and qualitative data, and provide some important in- sights for both future research and dietetics practice within this clinical population. CONCLUSIONS In conclusion, within this study sample of CD patients in Auckland, New Zealand, dairy products in general had no August 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, items with a high fat content were most frequently reported to worsen perceived CD symptoms. The lactose content of individual dairy products did not influence self-reported CD symptoms for the majority of patients. Clinically, CD activity status did not influence responses to dairy prod- ucts; however, site of disease appeared to have an effect. Colonic inflammation was more frequently associated with an increase in reported adverse CD effects from dairy product consumption in comparison to ileal CD involvement. Results from this exploratory study rein- force the idea that that “one size does not fit all” when it comes to making dietary recommendations relating to dairy product consumption for individuals with CD. Fu- ture research should consider the identification of genetic variants that might further explain tolerance to dairy products 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 received through an Australian Endeavour Research Fellowship to support travels to New Zealand to collaborate with Nutrigenomics New Zealand at the University of Auck- land. However, as this study was based on a secondary analysis of existing data, no additional funds were uti- lized. Deborah Nolan-Clark is a recipient of an Australian Endeavour Research Fellowship. The authors would like to acknowledge the participants of the present study and thank Philippa Dryland and Virginia Parslow for assis- tance with the provision of dietary questionnaires. Nu- trigenomics New Zealand is a collaboration between AgResearch Ltd, Plant and Food Research and The Uni- versity of Auckland and is largely funded by the Founda- tion for Research, Science and Technology. References 1. Veloso FT, Ferreira JT, Barros L, Almeida S. 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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 disease population. Mutat Res. 2010;690:123-138. 8. Satsangi J, Silverberg MS, Vermeire S, Colombel JF. The Montreal classification 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 Montreal World Congress of Gastroenterology. 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Osteoporosis in inflammatory bowel disease: 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, Roche J. Dietary modification with dairy products for preventing vertebral bone 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 Complement Altern Med. 2006;6:19. 19. Jamieson AE, Fletcher PC, Schneider MA. Seeking control through the determination of diet: A qualitative investigation of women with irritable bowel syndrome and inflammatory bowel disease. Clin Nurse Spec. 2007;21:152-160. 20. O’Sullivan M, O’Morain C. Nutrition in inflammatory bowel disease. 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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 rats with 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 intestinal mucosa in inflammation. Mutat Res. 2010;690:64-70. 28. Park YW, Juárez M, Ramos M, Haenlein GFW. Physico-chemical characteristics of goat and sheep milk. Small Rumin Res. 2007;68:88- 113. 29. Adolfsson O, Meydani SN, Russell RM. Yogurt and gut function. Am J Clin Nutr. 2004;80:245-256. 30. Van Limbergen J, Wilson DC, Satsangi J. The genetics of Crohn’s disease. Annu Rev Genomics Hum Genet. 2009;10:89-116. 1172 August 2011 Volume 111 Number 8