research

13/20

University of Florida

Nutrition and Disease II

Research Assignment

Oriana Carrasco

1. In your own words, describe celiac disease and the primary treatment/therapy for celiac disease.

Celiac disease is commonly known as an autoimmune response after the ingestion of gluten. As a celiac patient, digesting food that contains gluten will cause the small intestine to be super sensitive and that will lead to a serious difficulted digestion process causing abdominal pain. There is not and specific treatment for celiac disease yet, the only thing that would be effective is having a completely gluten free diet.

2. Article 1

a) What was the author’s purpose for conducting this study?

They created a survey that was designed to assess information to evaluate further treatment and adherence – But why did they create the survey? What question were they trying to answer?

b) Describe the participants in this study

Socioeconomic: specifically made to study how activities are presented in the social environment and how it is shaped by social processes depending on region and other factors.

Demographic: Data provided by participants to find a determination. Missing details in results section of characteristics of participants. This question is asking you to describe the actual people that participated in the project. Example, sex, race, types of diseases, etc.

c) What is treatment burden? How did this study assess “treatment burden”?

Treatment burden is defined as the load of healthcare for patients with severe diseases, in this case, with celiac disease. Sometimes it can be contradictory having lack of adherence and negative outcomes from patients carrying the disease. Stata was implemented to drive statistic analysis. What tool, or type of tool/survey was used to measure treatment burden?

d) What How was adherence to a gluten free diet and presence of celiac symptoms measured?

Poor adherence was identified and there are some important factors that should be considered when concluding the adherence. Maintaining a gluten free diet is difficult, “restrictions” everywhere, limited food and lack of education regarding this disease are causing a bad adherence to it. Concerns with prices is also an important factor that should be considered, eating outside while being on a gluten free diet is barely impossible and preparation of that type of food in our house sometimes could be even more expensive.

Symptoms are strong if diet is not followed, based on proper experience. Abdominal pain could take you to the ER due to the intolerable heartburn that is caused by gluten. This question is asking specifically for the names of the surveys also.

e) What were the overall primary findings of the study? What characteristics of participants with celiac disease were associated with increased adherence to a gluten free diet? Decreased adherence to a gluten free diet?

The primary goal of the article was to evaluate the patient perception of the disease and to evaluate how treatment burden was with comparison of other serious diseases. Asking primary findings rather than goal. So essentially, what did they find?

Characteristics of participants – ? this information is missing? So what is different about patients with celiac disease that adhere to a gluten free diet versus those that do not adhere well?

In order to have a good adherence, diet must be followed. Females showed on the statistics a higher adherence to a gluten free diet. However, it remains poor. It is hard to maintain a gluten free diet since that is the only way to take care of celiac disease, some aspects were mentioned below but besides those, lack of time is also a factor that does not contribute to a good adherence.

f) Figures

Treatments between GERD and CD are different in every aspect. The main difference of those diseases referring to treatment is the daily diet that should be followed. GERD is caused by acid reflux. Therefore, protein inhibitors or receptor blocker medication should be used, there also numerous of medicines that can be used to help with the heartburn. It is important to know that a gluten free diet is suggested but no obligatory as it is on patients with celiac disease which technically explain the difference in treatment burden.

Personally, I was surprised that patients with celiac disease reported importance of treatment higher that all other conditions. A few years ago, I had to maintain a gluten free diet for 3 months because of an abdominal pain that I was experimenting after eating bread, pasta or crackers, it was very hard to follow a strict gluten free diet for 3 months that I could never imagine how hard it should be to cut gluten completely out of our diet.

Article 2

1. What was the authors primary purpose for conducting this study?

To study the outcome of individuals living with a gluten free diet since there are concerns about how the cut of those aliments can cause some type of anxiety or fatigue. Be more specific here. So in additional to anxiety and fatigue – what else were they looking to learn and do with the information?

2. Describe the participants in the study

– Demographic: data provided by participants

-Medical: age, gender, ethnicity, self-described race missing details

3) How are participants categorized as “hypervigilant” or not?

Cooking at home and using the internet sites in a positive way potentially increased the hypervigilance. Also, negative results came back too, and more empathy should be implemented to people with CD since it can cause severe depression or anxiety, we all should be alert of mental health. -Happy people are healthy people. They used very specific criteria from dietary recalls to classify participants as “hypervigilant” or not – what was this information?

4) Primary finding of the study

Highlights on potential negative consequences after a severe/strict gluten free diet.

5) Main barriers and facilitators for adults and tens

For adults, they stated that eating out caused some worries as cross contamination and not feeling good when they were asked about their diet. Limitations of restaurants and distrust of the gluten free menu which is key to feel safe while eating out of their home. On the other hand, they showed some important facilitators as having friends who gave them the support needed and having helpful apps or internet sited.

Facilitator aspects for teens were basically the same as the ones that adults mentioned. Some words as “embarrassed” came in and when it comes to barriers with teens, the most common was that they were scared of how their diet was going to be affected while in college.

Application

1) You are a healthcare provider that regularly counsels/treats patients with celiac disease. How would you use this information to tailor your approach/advice/treatment plan for your celiac disease patients?

Treating a patient will always be challenging and when it comes to diseases related to mental health, it should be taken care more carefully than anything. As a provider, I would work with my patient from the beginning of their journey as a celiac disease patient in combination with a psychologist to conduct the best treatment. I would approach to my patient in a unique manner where he/she will feel safe and not embarrassed about the situation. Trying to find out as many choices of food that I am aware of in order to make it easier. Sometimes not engaging with the patient will make them feel uncomfortable and that will lead to a failure plan which is the opposite of what we are looking for. Concluding a diet together as a team, evaluating favorite type of food and finding substitutes is a great idea. Is not about “cutting” everything out for their meal but finding the best match to make them feel that they are not missing everything.

THE RED SECTION

The American Journal of GASTROENTEROLOGY VOLUME 109 | SEPTEMBER 2014 www.amjgastro.com

nature publishing group1304

Celiac disease (CD) is a chronic immune-mediated enteropathy

triggered by gluten-containing foods. Th e prevalence is estimated

to be 1:70 – 1:300, and the only treatment is life-long adherence to

a gluten-free diet (GFD) ( 1 – 5 ). Prior studies estimate adherence

to the GFD to be as low as 36 – 45 % ( 6 – 8 ). CD diff ers from many

other chronic diseases because dietary changes are the only current

therapy for disease management. Poor dietary compliance is the

leading cause of ongoing symptoms in participants with CD ( 9 ).

Th is is especially concerning considering the numerous poten-

tial complications of untreated CD, including reduction in bone

mineral density, malignancy, and increased mortality rate ( 3,10,11 ).

Adherence to GFD has been associated with improvements in

quality of life( 12 – 15 ), bone mineral density ( 16 – 21 ), fatigue ( 22 ),

infertility ( 23 – 26 ), adverse pregnancy outcomes ( 27 – 29 ), and risk

of lymphoproliferative malignancy ( 30,31 ).

Th ere are multiple potential factors accounting for low dietary

adherence in CD, including limited availability and higher cost

of gluten-free foods ( 32 – 34 ), reduced enjoyment of food ( 35 ),

and social isolation when dining out ( 35,36 ). Although there are

many unique features of the GFD that may reduce adherence, it

Patient Perception of Treatment Burden Is High
in Celiac Disease Compared With Other Common
Conditions

Sveta Shah , MD 1 , 2 , Mona Akbari , MD, MPH 1 , 2 , Rohini Vanga , MD 1 , Ciaran P. Kelly , MD 1 , Joshua Hansen , MS 1 , Th immaiah Th eethira , MD 1 ,

Sohaib Tariq , MD 1 , Melinda Dennis , MS, RD, LDN 1 and Daniel A. Leffl er , MD, MS 1

OBJECTIVES: The only treatment for celiac disease (CD) is life-long adherence to a gluten-free diet (GFD). Non-

compliance is associated with signs and symptoms of CD, yet long-term adherence rates are poor.

It is not known how the burden of the GFD compares with other medical treatments, and there are

limited data on the socioeconomic factors infl uencing treatment adherence. In this study, we com-

pared treatment burden and health state in CD compared with other chronic illnesses and evaluated

the relationship between treatment burden and adherence.

METHODS: Survey was mailed to participants with CD, gastroesophageal refl ux disease (GERD), irritable bowel

syndrome, infl ammatory bowel disease, hypertension (HTN), diabetes mellitus (DM), congestive heart

failure, and end-stage renal disease (ESRD) on dialysis. Surveys included demographic information

and visual analog scales measuring treatment burden, importance of treatment, disease-specifi c

health status, and overall health status .

RESULTS: We collected surveys from 341 celiac and 368 non-celiac participants. Celiac participants reported

high treatment burden, greater than participants with GERD or HTN and comparable to ESRD. Con-

versely, patients with CD reported the highest health state of all groups. Factors associated with high

treatment burden in CD included poor adherence, concern regarding food cost, eating outside the

home, higher income, lack of college education, and time limitations in preparing food. Poor adherence

in CD was associated with increased symptoms, income, and low perceived importance of treatment.

CONCLUSIONS: Participants with CD have high treatment burden but also excellent overall health status in compari-

son with other chronic medical conditions. The signifi cant burden of dietary therapy for CD argues

for the need for safe adjuvant treatment, as well as interventions designed to lower the perceived

burden of the GFD.

SUPPLEMENTARY MATERIAL is linked to the online version of the paper at http://www.nature.com/ajg

Am J Gastroenterol 2014; 109:1304–1311; doi: 10.1038/ajg.2014.29; published online 1 July 2014

1 Celiac Center and Department of Gastroenterology, Beth Israel Deaconess Medical Center , Boston , Massachusetts , USA ; 2 The fi rst two authors contributed

equally to this work and are co-fi rst authors . Correspondence: Daniel A. Leffl er, MD, MS , Celiac Center and Department of Gastroenterology, Beth Israel

Deaconess Medical Center , 330 Brookline Ave. , Boston , Massachusetts 02215 , USA . E-mail: dleffl er@caregroup.harvard.edu

THE RED SECTION

© 2014 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY

1305

is generally accepted that adherence is better with well-circum-

scribed treatments, such as medication administration, than

with health behaviors including dietary advice ( 37 ). Currently,

treatment of CD is limited exclusively to lifestyle modifi cation,

which may contribute to poor adherence and elevated treat-

ment burden in comparison with many other chronic illnesses;

however, this hypothesis has not been rigorously evaluated.

Close follow-up with a physician, dietician, and support group

are routinely recommended in order to monitor and improve

dietary adherence ( 38,39 ), although the evidence for these inter-

ventions is limited.

To improve the quality of life and treatment adherence in CD,

a robust understanding of the burden of the GFD and the factors

that infl uence adherence is necessary. However, relevant data

on this topic are limited ( 40 ) and in most studies have lacked

a validated measure of adherence. Th e objective of this study

was to compare the treatment burden in CD with that of other

chronic illnesses and identify factors associated with treatment

burden and GFD adherence as measured by a validated survey

tool ( 41 ).

METHODS

Study subjects . Th e study population consisted of participants

evaluated at the Celiac Center at Beth Israel Deaconess Medical

Center or who visited primary care clinics associated with Beth

Israel Deaconess Medical Center in Boston, MA. Th is study was

approved by the Beth Israel Deaconess Medical Center Commit-

tee on Clinical Investigations.

Survey development and measures . Th e survey was designed

to assess socioeconomic and demographic information, meas-

ures evaluating treatment burden and adherence, and specifi c

questions relating health and treatment barriers. Visual analog

scales (VAS) have been used to study burden of disease across

a multitude of disorders, including gastroesophageal refl ux

disease (GERD), Crohn ’ s disease, irritable bowel syndrome

(IBS), diabetes, and congestive heart failure (CHF) ( 42 – 46 ). We

adapted these existing surveys for the current study. Partici-

pants were asked to rate four domains on a scale of 0 – 100: (i)

diffi culty in following treatment; (ii) perceived importance of

following treatment; (iii) disease-specifi c health; and (iv) overall

health (see Supplementary Appendix 1 online). Th e question-

naire was fi rst assessed for comprehensiveness and clarity by

patients with and without CD before being sent to participants.

For diffi culty in following treatment, a score of 0 indicated that

treatment is “ very easy ” and a score of 100 indicated that treat-

ment is “ very diffi cult ” . For importance of following treatment,

0 indicated “ not important ” and 100 indicated “ very important. ”

For disease-specifi c health and overall health, 0 indicated “ worst

imaginable ” and 100 indicated “ best imaginable ” health states.

In addition to the VAS scales, participants with CD also com-

pleted the Celiac Dietary Adherence Test, a validated measure

of adherence to the GFD ( 41 ), and the Celiac Symptoms Index,

to measure CD symptoms ( 47 ).

Celiac cohort . To be eligible for participation in the celiac cohort,

individuals had to be > 18 years of age with biopsy-confi rmed CD

for more than 3 months, have a valid US home address, and have

cognitive ability and English profi ciency suitable for independent

completion of the surveys.

Non-celiac cohorts . To be eligible for participation, individuals

had to have cognitive ability and English profi ciency suitable

for independent completion of the surveys, be > 18 years of age,

and have a valid US address. Participants were chosen on the

basis of one of seven chronic illnesses including hypertension

(HTN), diabetes mellitus (DM), CHF, end-stage renal disease

(ESRD) requiring dialysis, GERD, IBS, and infl ammatory bowel

disease (IBD). Diagnoses were preliminarily identifi ed through

International Classifi cation of Diseases, 9th edition codes and

confi rmed in all cases through independent review of the medi-

cal record. Th e presence of multiple illnesses did not preclude

inclusion. In these scenarios, participants were included only in

the illness diagnosis fi rst used for identifi cation.

Statistical analysis . Univariate statistics were used to evalu-

ate cohort means and s.d. Missing data were handled by cohort

response means. Student ’ s t -statistic and one-way analysis of

variance compared means between two groups and across three

or more groups, respectively. Post hoc scheff e multiple compari-

son test was used to evaluate the diff erences between each pair

of means. Stepwise linear regression analysis controlling for age

and gender was used to determine predictors of treatment bur-

den, GFD adherence, and perceived importance of treatment for

the celiac cohort. A P value of < 0.05 was considered statistically

signifi cant. All analyses were performed using Stata (StataCorp

LP; College Station, TX).

RESULTS

Characteristics of study participants . Of 773 surveys mailed

to CD participants, 341 (45 % ) responded. Mean age at diagnosis

was 42.98 years (95 % confi dence intervals (CI): 41.35, 44.61) and

mean age at time of the survey was 51.14 years (95 % CI: 49.53,

52.75). Participants had followed a GFD for a mean of 85.49

months (95 % CI: 77.63, 93.46). Of the 1,288 surveys mailed out to

non-CD participants, 368 (29 % ) responded. Baseline characteris-

tics are listed in Table 1 .

Celiac responders were younger than those with HTN ( P < 0.001),

GERD ( P = 0.001), DM ( P < 0.001), and CHF ( P < 0.001) and older

than those with IBD ( P = 0.008). Th ere was no diff erence in age

between the celiac cohort and those with ESRD ( P = 0.112) or IBS

( P = 0.903). Celiac responders were more likely to be women com-

pared with all other cohorts (HTN, P < 0.001; GERD, P < 0.001;

ESRD, P = 0.006; DM, P < 0.001; CHF, P = 0.003; IBD, P < 0.001;

IBS, P = 0.004) and were more likely to identify as Caucasian com-

pared with those with HTN ( P < 0.001), GERD ( P < 0.001), ESRD

( P < 0.001), DM ( P < 0.001), CHF ( P < 0.001), but not with IBD

( P = 0.052) or IBS ( P = 0.092). Celiac responders were more likely

to report education of college or greater compared with those

THE RED SECTION
The American Journal of GASTROENTEROLOGY VOLUME 109 | SEPTEMBER 2014 www.amjgastro.com

1306

with HTN ( P < 0.001), GERD ( P = 0.015), ESRD ( P = 0.001), DM

( P < 0.001), CHF ( P < 0.001), but not with IBD ( P = 0.817) or IBS

( P = 0.647). Celiac responders were less likely to report income less

than $ 75,000 compared with those with HTN ( P < 0.001), ESRD

( P = 0.001), DM ( P < 0.001), or CHF ( P < 0.001), but not compared

with GERD ( P = 0.055), IBD ( P = 0.455), or IBS ( P = 0.579).

Celiac responders were less likely to visit specialists compared

with all other diagnoses (GERD, P = 0.006; ESRD, P < 0.001; DM,

P < 0.001; CHF, P < 0.001; IBD, P < 0.001; and IBS, P < 0.001),

except for those with HTN ( P = 0.105). Celiac responders were also

less likely to visit their primary care physician compared with par-

ticipants with ESRD ( P = 0.002), DM ( P < 0.001), CHF ( P < 0.001),

GERD ( P = 0.050), and IBS ( P -value = 0.011), but not when com-

pared with HTN ( P = 0.055) and IBD ( P = 0.948).

Treatment burden . Th e mean reported burden of following a

GFD was 44.90 points on the VAS (0: very easy and 100: very dif-

fi cult). In univariate regression analysis, patient factors that were

signifi cantly associated with increased treatment burden were

poor adherence to GFD ( P < 0.001), increased severity of current

celiac symptoms ( P = 0.001), time limitations for the research,

purchase and preparation of foods ( P = 0.001), diffi culty with eat-

ing outside the home ( P = 0.005), concern with the cost of food

( P = 0.001), lack of college education ( P = 0.004), and hospitaliza-

tions within the past year ( P = 0.006). In the multivariate linear

regression model controlling for age and gender, time limitations

for the research, purchase and preparation of foods ( P = 0.010),

diffi culty with eating outside the home ( P = 0.023), concern with

food cost ( P = 0.012), lack of college education ( P = 0.010), and

poor adherence ( P < 0.001) remained signifi cantly associated with

increased treatment burden. Income > $ 200,000 ( P = 0.017) was

also signifi cant in multivariate analysis, but increased severity of

current celiac symptoms and hospitalizations were not ( Table 2 ).

Treatment burden, perceived treatment importance, disease-

specifi c health, and overall health were compared between all

medical conditions assessed. Figures 1 – 4 graphically depict these

results. Th e reported treatment burden for CD of 44.90 was higher

than all other groups in aggregate (mean: 33.01, P < 0.001). CD

also had the highest reported treatment burden of all conditions

assessed with the exception of ESRD, although this only reached

statistical signifi cance for HTN (mean: 23.50, P < 0.001) and

GERD (mean score: 21.34, P < 0.001). Treatment burden was

highest overall for ESRD (mean: 56.41), followed by CD, DM

(mean: 41.74), IBS (mean: 40.38), CHF (mean: 38.46), and IBD

(mean: 31.91).

Adherence to GFD . Th e mean Celiac Dietary Adherence Test

score in the CD cohort was 11.93 (95 % CI: 11.55, 12.31). In uni-

variate linear regression, poor adherence was associated with

income < $ 200,000 ( P = 0.047), unemployed status ( P = 0.050),

increased severity of current celiac symptoms ( P < 0.001), lower

perceived importance of treatment ( P < 0.001), and greater

treatment burden ( P < 0.001). In the multivariate model,

income < $ 200,000 ( P = 0.045), increased severity of current celiac

symptoms ( P < 0.001), and lower perceived importance of treat-

ment ( P < 0.001) remained associated with poor adherence aft er

controlling for age and gender ( Table 3 ).

Perceived importance of following the GFD . Most participants

reported high importance of following a GFD, with a mean score

for treatment importance of 93.80 (95 % CI: 91.83 – 95.77). In uni-

variate linear regression, diffi culty with eating outside the home

( P = 0.026), female gender (94.89 vs. 90.29, P = 0.050), greater

adherence ( P < 0.001), and increased severity of current celiac

symptoms ( P = 0.024) were associated with higher perceived

importance of following a GFD. Only greater adherence ( P < 0.001)

and increased severity of current celiac symptoms ( P < 0.001) con-

tinued to have signifi cance in the multivariate linear regression

model ( Table 4 ). In comparison with other diseases, only ESRD

rated treatment as more important (mean score: 94.67); however,

the diff erence was only statistically signifi cant between CD and

IBS (mean score: 79.42, P = 0.016). Mean perceived importance of

Table 1 . Baseline characteristics of celiac and non-celiac cohorts

CD HTN DM CHF ESRD GERD IBD IBS

Number of participants 341 75 69 41 18 61 67 37

Mean age, years (s.e.) 51.14 (0.81) 63.27 (1.37) 64.03 (1.31) 70.58 (2.07) 56.61 (4.27) 57.84 (1.62) 46.13 (1.90) 50.59 (0.81)

% Female, (c) 76.26 (0.02) 45.95 (0.06) 38.24 (0.06) 53.66 (0.08) 44.44 (0.12) 40.00 (0.06) 46.97 (0.06) 52.78 (0.36)

% Caucasian, (s.e.) 96.77 (0.01) 80.00 (0.05) 70.59 (0.06) 68.29 (0.07) 61.11 (0.12) 77.96 (0.05) 93.73 (0.03) 88.89 (0.05)

% Income a < $ 75,000, (s.e.) 36.50 (0.03) 57.33 (0.06) 69.56 (0.06) 87.80 (0.05) 88.89 (0.08) 40.98 (0.06) 41.79 (0.06) 41.67 (0.08)

% No college education (s.e.) 26.71 (0.02) 48.00 (0.06) 56.52 (0.06) 56.10 (0.08) 66.67 (0.11) 42.62 (0.06) 28.36 (0.06) 30.56 (0.08)

Mean specialist visits per

year (s.e.)

0.75 (0.03) 0.48 (0.12) 1.65 (0.21) 2.34 (0.23) 4.39 (0.24) 1.26 (0.21) 2.51 (0.17) 1.82 (0.24)

Mean PCP visits per year (s.e.) 2.19 (0.08) 2.54 (0.16) 3.13 (0.18) 3.61 (0.24) 3.28 (0.36) 2.60 (0.16) 2.18 (0.18) 2.85 (0.28)

CD, celiac disease; CHF, congestive heart failure; DM, diabetes mellitus; ESRD, end-stage renal disease; GERD, gastroesophageal refl ux disease; HTN, hypertension; IBD,

infl ammatory bowel disease; IBS, irritable bowel syndrome.

a Income in US dollars.

THE RED SECTION
© 2014 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY

1307

treatment was 90.14 for DM, 88.89 for HTN, 88.83 for CHF, 87.95

for IBD, and 86.49 for GERD. Th e reported perceived importance

of treatment for CD of 93.80 was higher than all other groups in

aggregate (mean: 87.90, P < 0.001).

Overall and disease-specifi c health . Participants with CD rated

disease-specifi c health higher than any other group, with a mean

score of 81.61 (0: “ worst imaginable health state ” and 100: “ best

imaginable health state ” ). Th is score was signifi cantly higher

than that for ESRD (mean: 59.44, P = 0.003), IBS (mean: 65.20,

P = 0.003), CHF (mean score: 65.80, P = 0.002), and DM (mean:

71.22, P = 0.028). Disease-specifi c health was higher than that

of the other chronic medical conditions as well, including HTN

(mean: 76.82), GERD (mean: 74.56), and IBD (mean: 74.34),

but did not reach statistical signifi cance. Th e reported disease-

specifi c health for CD of 81.61 was higher than all other groups in

aggregate (mean: 71.72, P < 0.001).

Overall

CHF

DM

ESRD

HTN

IBS

IBD

GERD

CD

10 20 30 40 50 60 70 80

Visual analog scale

Figure 1 . Treatment burden of CD in comparison with non-celiac chronic

illnesses. * CD, celiac disease; CHF,congestive heart failure; DM, diabetes

mellitus; ESRD, end-stage renal disease; GERD,gastroesophageal

refl ux disease; HTN, hypertension; IBD,infl ammatory bowel disease;

IBS,irritable bowel syndrome. * * VAS (visual analog scale): score of

0 = very easy; score of 100 = very diffi cult. * * * Mean scores: CD 44.9

(s.d.: 30.9), GERD 21.3 (s.d.: 25.3), HTN 23.5 (s.d.: 25.7), IBD 31.9

(s.d.: 27.7), CHF 38.5 (s.d.: 31), IBS 40.4 (s.d.: 24.4), DM 41.7 (s.d.:

30.4), and ESRD 56.4 (s.d.: 31.9). * * * * On the basis of results of

post hoc multiple comparisons, treatment burden was statistically

signifi cant for the following groups: CD vs. GERD ( P value < 0.001), CD

vs. HTN ( P value < 0.001), GERD vs. ESRD ( P value 0.01), and GERD

vs. DM ( P value 0.04). Error bars represent 95 % confi dence intervals.

Overall
CHF
DM
ESRD
HTN
IBS
IBD
GERD
CD

60 8070 90 100

Visual analog scale

Figure 2 . Perceived importance of treatment of CD in comparison with

non-celiac chronic illnesses. * CD,celiac disease; CHF, congestive heart

failure; DM, diabetes mellitus; ESRD, end-stage renal disease; GERD,

gastroesophageal refl ux disease; HTN, hypertension; IBD, infl ammatory

bowel disease; IBS, irritable bowel syndrome. * * VAS (visual analog scale):

score of 0 = not important at all; score of 100 = very important. * * * Mean

scores: CD 93.8 (s.d.: 18.6), HTN 88.9 (s.d.: 20.4), GERD 86.5 (s.d.:

19.7), IBD 88.0 (s.d.: 19.9), CHF 88.8 (s.d.: 22.4), IBS 79.4 (s.d.: 25.5),

DM 90.1(s.d.: 20.4), and ESRD 94.7 (s.d.: 14.2). * * * * On the basis of

results of post hoc multiple comparisons, the importance of treatment

was statistically signifi cant for the following groups: CD vs. IBS ( P value

0.016). Error bars represent 95 % confi dence intervals.

Table 2 . Celiac patient factors associated with high GFD treatment burden

Univariate analysis Multivariate analysis

β coeffi cient 95 % CI β coeffi cient 95 % CI

Time limitations 14.21 6.09, 22.33 10.41 2.51, 18.31

Eating outside the home 12.64 3.82, 21.46 10.13 1.44, 18.82

Concern regarding food cost 11.41 4.63, 18.18 8.91 1.94, 15.88

No college education 10.78 3.48, 18.09 9.73 2.33, 17.14

Hospitalization in the past year 9.01 2.62, 15.39 NS NS

Poor GFD adherence 2.42 1.54, 3.31 1.77 0.82, 2.72

Increased celiac symptoms 0.61 0.27, 0.96 NS NS

Income a > $ 200,000 NS NS 11.51 2.08, 20.94

CI, confi dence intervals; NS, not signifi cant.

a Income in US dollars.

THE RED SECTION
The American Journal of GASTROENTEROLOGY VOLUME 109 | SEPTEMBER 2014 www.amjgastro.com

1308

compared with 31.71 ( P = 0.89) in those not on biologic therapy.

Disease-specifi c health and overall health were 76.40 and 79.80,

respectively, compared with 73.96 ( P = 0.778) and 76.11 ( P = 0.576)

for those not on biologic therapy. When compared with IBD

participants not on biologics, celiac participants reported greater

disease-specifi c health (73.96 vs. 81.61, P = 0.036), treatment burden

(mean diff erence: 31.71 vs. 44.90, P = 0.002), and perceived impor-

tance of treatment (mean diff erence: 87.26 vs. 93.80, P = 0.027).

No diff erence was observed between IBD participants on biologic

therapy and celiac participants for disease-specifi c health (76.40

vs. 81.61, P = 0.479), treatment burden (33.00 vs. 44.90, P = 0.243),

and importance of treatment (92.11 vs. 93.80, P = 0.808).

Similarly, participants with CD rated overall health higher than

any other group, with a mean score of 77.97. Overall health was

signifi cantly greater for CD compared with ESRD (mean: 55.44,

P = 0.001) and CHF (mean: 57.80, P < 0.001), but it did not reach

signifi cance for HTN (mean: 72.44), GERD (mean: 71.62), IBD

(mean: 76.66), or IBS (mean: 70.54). Th e reported overall health

for CD of 77.97 was higher than all other groups in aggregate

(mean: 69.93, P < 0.001).

In subgroup analysis, we further characterized IBD patients on

the basis of the use of biologic therapy and DM patients on the basis

of the use of insulin. Fift een percent of IBD participants reported

taking biologics, and in this group treatment burden was 33.00

Overall
CHF
DM
ESRD
HTN
IBS
IBD
GERD
CD

50 60 8070 90

Visual analog scale

Figure 3 . Perceived disease-specifi c health of CD in comparison with

non-celiac chronic illnesses. * CD, celiac disease; CHF, congestive heart

failure; DM, diabetes mellitus; ESRD, end-stage renal disease; GERD,
gastroesophageal refl ux disease; HTN, hypertension; IBD, infl ammatory
bowel disease; IBS, irritable bowel syndrome. * * VAS (visual analog scale):

score of 0 = best imaginable health, score of 100 = worst imaginable health.

* * * Mean scores: CD 81.6 (s.d.: 18), GERD 74.6 (s.d.: 18.4), HTN 76.8

(s.d.: 18.4), IBD 74.3 (s.d.: 24.9), CHF 65.8 (s.d.: 19.4), IBS 65.2 (s.d.:

20.7), DM 71.2 (s.d.: 22.7), and ESRD 59.4 (s.d.: 22.2). * * * * On the basis

of results of post hoc multiple comparisons, disease-specifi c health was

statistically signifi cant for the following groups: CD vs. IBS ( P value 0.003),

CD vs. ESRD ( P value 0.003), CD vs. DM ( P value 0.028), and CD vs. CHF

( P value 0.002). Error bars represent 95 % confi dence intervals.

Overall
CHF
DM
ESRD
HTN
IBS
IBD
GERD
CD

50 60 8070

Visual analog scale

Figure 4 . Perceived overall health state of CD in comparison with non-celiac

chronic illnesses. * CD, celiac disease; CHF, congestive heart failure; DM,

diabetes mellitus; ESRD, end-stage renal disease; GERD, gastroesophageal

refl ux disease; HTN, hypertension; IBD, infl ammatory bowel disease; IBS,

irritable bowel syndrome. * * VAS (visual analog scale): score of 0 = best

imaginable health, score of 100 = worst imaginable health. * * * Mean scores:

CD 78 (s.d.: 16.7), GERD 71.6 (s.d.: 21.6), HTN 72.4 (s.d.: 20.9), IBD 76.7

(s.d.: 19.1), CHF 57.8 (s.d.: 21.2), IBS 70.5 (s.d.: 18.1), DM 69.9 (s.d.: 23),

and ESRD 55.4 (s.d.: 17.8). * * * * On the basis of results of post hoc multiple

comparisons, overall health was statistically signifi cant for the following

groups: CD vs. ESRD ( P value 0.001), CD vs. CHF ( P value < 0.001), IBD

vs. ESRD ( P value 0.014), IBD vs. CHF ( P value 0.001), and HTN vs. CHF

( P value 0.029). Error bars represent 95 % confi dence intervals.

Table 3 . Celiac patient factors associated with poor adherence to GFD

Univariate analysis Multivariate analysis
β coeffi cient 95 % CI β coeffi cient 95 % CI

Income a < $ 200,000 1.90 0.04, 3.76 0.92 (0.02, 1.81)

Unemployed 1.43 (0.002, 2.87) NS NS

Worse symptoms 0.17 (0.13, 0.20) 0.19 (0.15, 0.22)

Lower perceived treatment importance 0.07 (0.05, 0.09) 0.09 (0.07, 0.11)

Greater treatment burden 0.03 (0.02, 0.04) NS NS

CI, confi dence intervals; GFD, gluten-free diet; NS, not signifi cant.

a Income in US dollars.

THE RED SECTION
© 2014 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY

1309

Th irty-two percent of diabetic participants reported taking

insulin. Treatment burden (45.00 vs. 40.43, P = 0.583), disease-

specifi c health (70.82 vs. 71.41, P = 0.920), and overall health

(67.50 vs. 71.06, P = 0.554) did not diff er for diabetics on insu-

lin compared with those not on insulin. When compared with

diabetics not on insulin, celiac participants reported greater

disease-specifi c health (71.41 vs. 81.61, P = 0.004). Treatment

burden (40.43 vs. 44.90, P = 0.346) and perceived importance

of treatment (87.72 vs. 93.80, P = 0.101) did not diff er between

diabetics not on insulin and celiac participants. Disease-specifi c

health (70.82 vs. 81.61, P = 0.060), treatment burden (45.00 vs.

44.90, P = 0.989), and treatment importance (95.32 vs. 93.80,

P = 0.374) did not diff er between diabetics on insulin and celiac

participants.

DISCUSSION

Adherence to a GFD is the only treatment for CD, and failure to

adequately treat is associated with morbidity. However, GFD adher-

ence remains poor (40,48), and studies examining factors that

aff ect treatment burden and GFD adherence are limited ( 36,38,49 ).

We sought to evaluate predictors of adherence and treatment bur-

den, and to compare treatment burden in CD with other chronic

diseases.

Our results demonstrate that celiac participants report a

remarkably high treatment burden. In our study, celiac partici-

pants reported greater treatment burden than those with HTN

and GERD and comparable to participants with CHF and ESRD.

Th is underscores the diffi culty of following the GFD and puts the

high treatment burden of CD into context for practitioners who

oft en have more experience with other diseases. Greater diffi culty

with treatment implies a need for nondietary interventions, as

well as the need for patients to regularly follow-up with clini-

cians, dieticians, and other allied health professionals, whereas

our data and others ’ ( 50 ) suggest that patients with CD actually

see physicians less oft en than those with other chronic medical

conditions.

Our results also show that treatment burden is a predictor of

poor adherence to a GFD. Th ose who report higher burden of

following a GFD were more likely to have poor adherence to a

GFD. An exception to this was in participants with high reported

household income. Th ese individuals were likely to report high

treatment burden but were able to overcome this and demon-

strate greater adherence to the GFD. Although our study was not

designed to evaluate this relationship in detail, we hypothesize that

low education increases burden owing to diffi culty in managing

the complexity of the GFD, whereas high income increases bur-

den owing to diffi culty in following the diet during frequent travel

and social outings. Similar to prior studies ( 41 ), celiac participants

with poor GFD adherence had greater severity of symptoms likely

because of gluten exposure. Although the majority of participants

reported overall high perceived importance of the GFD, the fi nd-

ing that participants who felt the GFD was not very important to

their health had poor adherence is logical and refl ects the internal

validity of the survey measures.

It is encouraging to note that despite having reported quite a

high treatment burden in CD when compared with other chronic

medical conditions, participants with CD also reported a high

disease-specifi c and overall health. It is notable that CD patients

reported greatest disease-specifi c health, yet reported higher treat-

ment burden compared with all other diseases except ESRD. Th e

high burden of treatment may also be addressed by focusing on

other alternative treatments such as novel medical therapy or even

complementary alternative medicine ( 51 ).

Despite the use of validated measures and the relatively large

size, we recognize a number of limitations. Th e data were collected

from a dedicated CD center at a major teaching hospital, which

potentially limits the generalizability of the fi ndings. In addition,

there was a substantial nonresponse rate that may bias results if

respondents diff er signifi cantly from nonrespondents; however, in

the CD cohort, respondent demographics were not signifi cantly

diff erent from nonrespondents. ( Supplementary Table S1 online)

In addition, the response rate of 45 % for the CD patients compared

with 29 % for non-CD patients raises the possibility of diff erential

selection between these groups, which could bias results. Finally,

although the VAS has been widely used and validated in other dis-

ease states ( 42 – 46 ), it is possible that the VAS may not measure the

full spectrum of treatment burden, importance of treatment, and

health state. In addition, participants were asked to rate treatment

burden and health state without knowledge of the other disease

states with which they were compared. Although there is value in

asking patients to rate their health compared with another distinct

health state, it is diffi cult for individuals to gauge the impact of

conditions they do not have. For this reason, we chose to use the

Table 4 . Celiac patient factors associated with higher perceived importance of following GFD

Univariate analysis Multivariate analysis

β coeffi cient 95 % CI β coeffi cient 95 % CI

Eating out 6.06 0.74, 11.38 NS NS

Female gender 4.60 0.01, 9.19 NS NS

Greater adherence 1.92 1.40, 2.43 2.71 2.19, 3.23

Worse symptoms 0.24 0.03, 0.45 0.70 0.51, 0.89

CI, confi dence intervals; GFD, gluten-free diet; NS, not signifi cant.

THE RED SECTION
The American Journal of GASTROENTEROLOGY VOLUME 109 | SEPTEMBER 2014 www.amjgastro.com

1310

13 . Nachman F , Maurino E , Vazquez H et al. Quality of life in celiac disease
patients: prospective analysis on the importance of clinical severity at
diagnosis and the impact of treatment . Dig Liver Dis 2009 ; 41 : 15 – 25 .

14 . Nachman F , del Campo MP , Gonzalez A et al. Long-term deterioration
of quality of life in adult patients with celiac disease is associated with
treatment noncompliance . Dig Liver Dis 2010 ; 42 : 685 – 91 .

15 . Mustalahti K , Lohinierni S , Laippala P et al. Improvement of the quality
of life of silent celiac disease patients during the gluten-free diet warrents
screening . Gastroenterology 2000 ; 118 : A369 .

16 . Vasquez H , Mazure R , Gonzalez D et al. Risk of fractures in celiac disease
patients: a cross-sectional, case-control study . Am J Gastroenterol 2000 ;
95 : 183 – 9 .

17 . Valdimarsson T , Lofman O , Toss G et al. Reversal of osteopenia with diet
in adult coeliac disease . Gut 1996 ; 38 : 322 – 7 .

18 . Sategna-Guidetti C , Grosso SB , Grosso S et al. Th e eff ects of 1-year gluten
withdrawal on bone mass, bone metabolism and nutritional status in
newly-diagnosed adult coeliac disease patients . Aliment Pharmacol Th er
2000 ; 14 : 35 – 43 .

19 . Mustalahti K , Collin P , Sievanen H et al. Osteopenia in patients with
clinically silent coeliac disease warrants screening . Lancet 1999 ; 354 : 744 – 5 .

20 . Meyer D , Stavropolous S , Diamond B et al. Osteoporosis in a north american
adult population with celiac disease . Am J Gastroenterol 2001 ; 96 : 112 – 9 .

21 . Ciacci C , Maurelli L , Klain M et al. Eff ects of dietary treatment on bone
mineral density in adults with celiac disease: factors predicting response .
Am J Gastroenterol 1997 ; 92 : 992 – 6 .

22 . Siniscalchi M , Iovino P , Tortora R et al. Fatigue in adult coeliac disease .
Aliment Pharmacol Th er 2005 ; 22 : 489 – 94 .

23 . Sher KS , Mayberry JF . Female fertility, obstetric and gynaecological history
in coeliac disease: a case control study . Acta Paediatr 1996 ; 412 : 76 – 7 .

24 . Rujner J . Age at menarche in girls with celiac disease . Ginekol Polska
1999 ; 70 : 359 – 62 .

25 . Ferguson R , Holmes GK , Cooke WT . Coeliac disease, fertility, and
pregnancy . Scand J Gastroenterol 1982 ; 17 : 65 – 8 .

26 . Bona G , Marinello D , Oderda G . Mechanisms of abnormal puberty in
coeliac disease . Horm Res 2002 ; 57 (Suppl 2) : 63 – 5 .

27 . Norgard B , Fonager K , Sorensen HT et al. Birth outcomes of women with
celiac disease: a nationwide historical cohort study . Am J Gastroenterol
1999 ; 94 : 2435 – 40 .

28 . Ludvigsson JF , Montgomery SM , Ekbom A . Celiac disease and risk of
adverse fetal outcome: a population-based cohort study . Gastroenterology
2005 ; 129 : 454 – 63 .

29 . Ciacci C , Cirillo M , Auriemma G et al. Celiac disease and pregnancy
outcome . Am J Gastroenterol 1996 ; 91 : 718 – 22 .

30 . Lebwohl B , Granath F , Ekbom A et al. Mucosal healing and risk for lym-
phoproliferative malignancy in celiac disease: a population-based cohort
study . Ann Intern Med 2013 ; 159 : 169 – 75 .

31 . Ludvigsson JF . Mortality and malignancy in celiac disease . Gastrointest
Endosc Clin N Am 2012 ; 22 : 705 – 22 .

32 . Stevens L , Rashid M . Gluten-free and regular foods: a cost comparison .
Can J Diet Pract Res 2008 ; 69 : 147 – 50 .

33 . Singh J , Whelan K . Limited availability and higher cost of gluten-free foods .
J Hum Nutr Diet 2011 ; 24 : 479 – 86 .

34 . Lee AR , Ng DL , Zivin J et al. Economic burden of a gluten-free diet . J Hum
Nutr Diet 2007 ; 20 : 423 – 30 .

35 . Whitaker JK , West J , Holmes GK et al. Patient perceptions of the burden
of coeliac disease and its treatment in the UK . Aliment Pharmacol Th er
2009 ; 29 : 1131 – 6 .

36 . Edwards George JB , Leffl er DA , Dennis MD et al. Psychological correlates
of gluten-free diet adherence in adults with celiac disease . J Clin Gastro-
enterol 2009 ; 43 : 301 – 6 .

37 . DiMatteo MR . Variations in patients ’ adherence to medical recommenda-
tions: a quantitative review of 50 years of research . Med Care 2004 ; 42 : 200 – 9 .

38 . Leffl er DA , Edwards-George J , Dennis M et al. Factors that infl uence
adherence to a gluten-free diet in adults with celiac disease . Dig Dis Sci
2008 ; 53 : 1573 – 81 .

39 . Leffl er D . Celiac disease diagnosis and management: a 46-year-old woman
with anemia . JAMA 2011 ; 306 : 1582 – 92 .

40 . Hall NJ , Rubin G , Charnock A . Systematic review: adherence to a gluten-
free diet in adult patients with coeliac disease . Aliment Pharmacol Th er
2009 ; 30 : 315 – 30 .

41 . Leffl er DA , Dennis M , Edwards George JB et al. A simple validated gluten-
free diet adherence survey for adults with celiac disease . Clin Gastroenterol
Hepatol 2009 ; 7 : 530 – 6 , 6.e1 – 2 .

common and well-validated anchors such as of “ best imaginable

health ” and “ worst imaginable health ” .

In conclusion, participants with CD report a remarkably high

treatment burden similar to participants with ESRD and higher

than many other chronic medical conditions. Conversely, CD

participants in general reported high disease-specifi c health state,

which suggests that despite good long-term health outcomes CD

patients struggle with treatment. Th is study underscores both the

limitations of the GFD as lone treatment and the need for attention

to patient perceptions of recommended therapies ( 51 ). As the CD

population expands and new therapies are proposed, attention to

burden of treatment and disease will be vital for providing optimal

care for this population.

CONFLICT OF INTEREST

Guarantor of the article : Daniel A. Leffl er, MD, MS.

Specifi c author contributions: Study design and execution, analysis

and interpretation of data, draft ing of the manuscript, and critical

revision of the manuscript for important intellectual content of the

manuscript: Sveta Shah and Mona Akbari; study execution: Rohini

Vanga, Joshua Hansen, Th immaiah Th eethira, and Sohaib Tariq;

study design and execution, interpretation of data, and critical

revision of the manuscript for important intellectual content of

the manuscript: Ciar á n P. Kelly; study design, execution, and

enrollment: Melinda Dennis; study concept, design and execution,

interpretation of data, and critical revision of the manuscript for

important intellectual content of the manuscript: Daniel A. Leffl er.

Financial support: Th is work was supported by Shire Th erapeutics,

Prometheus Laboratories, Alba Pharmaceuticals, and Alvine

Th erapeutics (D.A.L.).

Potential competing interests: None.

REFERENCES
1 . Lohi S , Mustalahti K , Kaukinen K et al. Increasing prevalence of coeliac

disease over time . Aliment Pharmacol Th er 2007 ; 26 : 1217 – 25 .
2 . Fasano A , Berti I , Gerarduzzi T et al. Prevalence of celiac disease in at-risk

and not-at-risk groups in the United States: a large multicenter study .
Arch Int Med 2003 ; 163 : 286 – 92 .

3 . Farrell RJ , Kelly CP . Celiac sprue . N Engl J Med 2002 ; 346 : 180 – 8 .
4 . Rubio-Tapia A , Ludvigsson JF , Brantner TL et al. Th e prevalence of celiac

disease in the United States . Am J Gastroenterol 2012 ; 107 : 1538 – 44 ; quiz 7, 45 .
5 . Gujral N , Freeman HJ , Th omson AB . Celiac disease: prevalence, diagnosis,

pathogenesis and treatment . World J Gastroenterol 2012 ; 18 : 6036 – 59 .
6 . Vahedi K , Mascart F , Mary JY et al. Reliability of antitransglutaminase

antibodies as predictors of gluten-free diet compliance in adult celiac
disease . Am J Gastroenterol 2003 ; 98 : 1079 – 87 .

7 . Hogberg L , Grodzinsky E , Stenhammar L . Better dietary compliance in
patients with coeliac disease diagnosed in early childhood . Scand J
Gastroenterol 2003 ; 38 : 751 – 4 .

8 . Bardella MT , Molteni N , Prampolini L et al. Need for follow up in coeliac
disease . Arch Dis Child 1994 ; 70 : 211 – 3 .

9 . Leffl er DA , Dennis M , Hyett B et al. Etiologies and predictors of diagnosis
in nonresponsive celiac disease . Clin Gastroenterol Hepatol 2007 ; 5 :
445 – 50 .

10 . Ludvigsson JF , Montgomery SM , Ekbom A et al. Small-intestinal histo-
pathology and mortality risk in celiac disease . JAMA 2009 ; 302 : 1171 – 8 .

11 . Leffl er D , Kelly CP . Celiac disease: what the last few years have taught us .
In: Howden CW (ed). Advances in Digestive Diseases . AGA Institute Press:
Bethesda, MD, USA , 2007 , pp. 49 – 56 .

12 . Tontini GE , Rondonotti E , Saladino V et al. Impact of gluten withdrawal on
health-related quality of life in celiac subjects: an observational case-control
study . Digestion 2010 ; 82 : 221 – 8 .

THE RED SECTION
© 2014 by the American College of Gastroenterology The American Journal of GASTROENTEROLOGY

1311

42 . Wilcox AR , Dragnev MC , Darcey CJ et al. A new tool to measure the
burden of Crohn’s disease and its treatment: do patient and physician
perceptions match? Infl amm Bowel Dis 2010 ; 16 : 645 – 50 .

43 . Liu JY , Woloshin S , Laycock WS et al. Symptoms and treatment burden of
gastroesophageal refl ux disease: validating the GERD assessment scales .
Arch Int Med 2004 ; 164 : 2058 – 64 .

44 . Janssen MF , Lubetkin EI , Sekhobo JP et al. Th e use of the EQ-5D preference-
based health status measure in adults with Type 2 diabetes mellitus .
Diab Med 2011 ; 28 : 395 – 413 .

45 . Ekman I , Granger B , Swedberg K et al. Measuring shortness of breath in
heart failure (SOB-HF): development and validation of a new dyspnoea
assessment tool . Eur J Heart Fail 2011 ; 13 : 838 – 45 .

46 . Bushnell DM , Martin ML , Ricci JF et al. Performance of the EQ-5D in
patients with irritable bowel syndrome . Value Health 2006 ; 9 : 90 – 7 .

47 . Leffl er DA , Dennis M , Edwards George J et al. A validated disease-specifi c
symptom index for adults with celiac disease . Clin Gastroenterol Hepatol
2009 ; 7 : 1328 – 34 , 34.e1 – 3 .

48 . Pietzak MM . Follow-up of patients with celiac disease: achieving compli-
ance with treatment . Gastroenterology 2005 ; 128 (4 Suppl 1) : S135 – 41 .

49 . Ciacci C , Cirillo M , Cavallaro R et al. Long-term follow-up of celiac
adults on gluten-free diet: prevalence and correlates of intestinal damage .
Digestion 2002 ; 66 : 178 – 85 .

50 . Herman ML , Rubio-Tapia A , Lahr BD et al. Patients with celiac disease
are not followed up adequately . Clin Gastroenterol Hepatol 2012 ; 10 :
893 – 899. e1 .

51 . Aziz I , Evans KE , Papageorgiou V et al. Are patients with coeliac disease
seeking alternative therapies to a gluten-free diet? J Gastrointestin Liver Dis
2011 ; 20 : 27 – 31 .

Vol.:(0123456789)

1 3

Digestive Diseases and Sciences

https://doi.org/10.1007/s10620-018-4936-4

O R I G I N A L A R T I C L E

Hypervigilance to a Gluten‑Free Diet and Decreased Quality of Life
in Teenagers and Adults with Celiac Disease

Randi L. Wolf1  · Benjamin Lebwohl2 · Anne R. Lee2 · Patricia Zybert1 · Norelle R. Reilly2 · Jennifer Cadenhead1 ·
Chelsea Amengual1 · Peter H. R. Green2

Received: 6 November 2017 / Accepted: 16 January 2018
© Springer Science+Business Media, LLC, part of Springer Nature 2018

Abstract
Background and Aims Avoidance of gluten is critical for individuals with celiac disease (CD), but there is also concern that
“extreme vigilance” to a strict gluten-free diet may increase symptoms such as anxiety and fatigue, and therefore, lower
quality of life (QOL). We examined the associations of QOL with energy levels and adherence to, and knowledge about, a
gluten-free diet.
Methods This is a cross-sectional prospective study of 80 teenagers and adults, all with biopsy-confirmed CD, living in a
major metropolitan area. QOL was assessed with CD-specific measures. Dietary vigilance was based on 24-h recalls and an
interview. Knowledge was based on a food label quiz. Open-ended questions described facilitators and barriers to maintain-
ing a gluten-free diet.
Results The extremely vigilant adults in our sample had significantly lower QOL scores than their less vigilant counterparts
[(mean (SD): 64.2 (16.0) vs 77.2 (12.2), p = 0.004]. Extreme vigilance was also associated with greater knowledge [5.7
(0.7) vs 5.1 (0.8), p = 0.035]. Adults with lower energy levels had significantly lower overall QOL scores than adults with
higher energy levels [68.0 (13.6) vs 78.9 (13.0), p = 0.006]. Patterns were similar for teenagers. Cooking at home and using
internet sites and apps were prevalent strategies used by the hypervigilant to maintain a strict gluten-free diet. Eating out
was particularly problematic.
Conclusion There are potential negative consequences of hypervigilance to a strict gluten-free diet. Clinicians must consider
the importance of concurrently promoting both dietary adherence and social and emotional well-being for individuals with
CD.

Keywords Celiac disease · Quality of life · Adherence · Gluten-free diet · Teenagers · Adults

Abbreviations
CD Celiac disease
CDAT Celiac disease adherence test
DF Degrees of freedom

NJ New Jersey
NY New York
NYC New York City
QOL Quality of life

* Randi L. Wolf
wolf@tc.columbia.edu

Benjamin Lebwohl
bl114@cumc.columbia.edu

Anne R. Lee
arl2004@cumc.columbia.edu

Patricia Zybert
paz4@tc.columbia.edu

Norelle R. Reilly
nr2268@cumc.columbia.edu

Jennifer Cadenhead
jwc2151@tc.columbia.edu

Chelsea Amengual
chelsea.amengual@gmail.com

Peter H. R. Green
pg11@cumc.columbia.edu

1 Department of Health and Behavior Studies, Program
in Nutrition, Teachers College, Columbia University, 525
West 120th Street, Box 137, New York, NY 10027, USA

2 Department of Medicine, Celiac Disease Center, Columbia
University Medical Center, Harkness Pavilion, 180 Fort
Washington Avenue, New York, NY 10032, USA

http://orcid.org/0000-0002-8155-3082

http://crossmark.crossref.org/dialog/?doi=10.1007/s10620-018-4936-4&domain=pdf

Digestive Diseases and Sciences

1 3

RDN Registered dietitian nutritionist
SDE Standardized dietitian evaluation
GF Gluten free

Introduction

Celiac disease (CD) is an autoimmune disorder featuring
duodenal villous atrophy triggered by dietary gluten, a
protein present in wheat, barley, and rye. CD affects multi-
ple systems in the body and can manifest with a variety of
symptoms, including diarrhea, abdominal pain, peripheral
neuropathy, anemia, and infertility [1, 2]. The prevalence of
CD has increased up to fivefold in the United States since
1950, and diagnosis rates continue to rise, a consequence of
parallel trends of increased prevalence and improved aware-
ness and testing [3–5].

Current guidelines for the management of CD specify
lifelong adherence to a strict gluten-free diet [6, 7]. For the
majority of patients, strict avoidance of gluten is the only
treatment proven to result in clinical, serologic, and histo-
logic improvement [8–10]. Observational studies using duo-
denal mucosal healing as a marker suggest that adherence to
a gluten-free diet can decrease risk of long-term complica-
tions such as osteoporotic fracture and lymphoproliferative
malignancy [11, 12].

Since the level at which gluten is harmless is not known
for the individual with CD, avoidance of all gluten (from
food, beverages medications, and supplements) is the current
standard of care [6, 7]. Managing such a restrictive diet is
challenging, and treatment burden can be high [13–17]. Indi-
viduals with CD must learn what foods to eat, what foods to
avoid, hidden sources of gluten, and how to navigate a com-
plex food environment and a lifetime of social situations.

While better adherence to a gluten-free diet has been
associated with better quality of life (QOL) [18–22], there
is also concern that “extreme vigilance” to a gluten-free diet
may increase symptoms, such as anxiety and fatigue, and,
therefore, lower QOL. In other words, there may be a cost
to hypervigilance for some individuals with CD when fol-
lowing a strict gluten-free diet.

This study examines the associations of CD-specific QOL
with energy level and adherence to, and knowledge about, a
gluten-free diet. We also explore specifics of how QOL may
be affected by describing qualitative barriers and facilitators
to maintaining a gluten-free diet. Our purpose is to inform
future nutrition education strategies which can promote a
strict gluten-free diet while helping to maximize QOL for
teenagers and adults with CD.

Methods

Design

We performed a cross-sectional prospective study of adult
and teenaged patients with CD, focusing on QOL and its
correlates. The study was approved by the Institutional
Review Boards at the Columbia University Medical Center
and at Teachers College Columbia University.

Setting and Participants

The study was conducted at the Celiac Disease Center of
Columbia University in New York City. Inclusion crite-
ria required that participants be at least 13  years of age,
self-report a duodenal biopsy-confirmed diagnosis of
CD ≥ 1 year prior, and be willing to participate in three
visits (one in person and two via telephone) over a 1-month
period. We considered 13–17 year olds to be teenagers and
those 18  years and older to be adults. Exclusion criteria
included serum or self-diagnosed CD (without biopsy), a CD
diagnosis < 1 year prior, and age < 13 years old. The teenag- ers received a $25 Amazon gift card for their participation.

Enrollment

Enrollment occurred between March and August 2016.
Our target goal was 30 adults and 30 teenagers. Enrollment
exceeded our expectations. All affiliates (~ 5000 members)
of the Celiac Disease Center of Columbia University (which
includes a mix of patients, family members, and those with
an interest in CD) were emailed initially asking about their
interest in the study. Two additional follow-up emails specif-
ically targeted teenagers. Those interested were assessed for
eligibility by telephone. Among the 123 respondents to the
email invitation (78 adults; 45 teenagers), 43 were ineligible
(28 adults, 15 teenagers) and 80 were eligible and enrolled
(50 adults and 30 teenagers). Among the 28 ineligible adults,
6 were ineligible due to not having a duodenal biopsy to con-
firm CD, 20 for never scheduling an appointment, and 2 for
other reasons. Among the 15 ineligible teenagers, 11 were
ineligible for not having a duodenal biopsy to confirm CD, 3
for never scheduling an appointment, and 1 for other reasons.

Data Collection and Measures

Demographic and Medical History Variables

Age (date of birth), gender (male, female), self-described
ethnicity (Hispanic, non-Hispanic), self-described race
(White, African-American, Asian, Other), education

Digestive Diseases and Sciences
1 3

(highest level/grade achieved), and home residence (based
on zip code) were assessed. Medical history variables
included years since CD diagnosis, affiliation of their gas-
troenterologist (Celiac Center of Columbia University vs
Other), and visits with a registered dietitian, now referred to
as a registered dietitian nutritionist (RDN) (currently, once
only, more than once, never).

Celiac Disease‑Specific Quality of Life

CDQOL

CD-specific quality of life (CDQOL) in adults was assessed
using a 20-item validated survey instrument [23]. Partici-
pants answered questions with Likert scales where 1 = not
at all, 2  =  slightly, 3  =  moderately, 4  =  quite a bit, and
5 = a great deal. Answers were transformed and combined
to obtain an overall score and four clinically relevant sub-
scales: dysphoria (4 items), limitations (9 items), health con-
cerns (5 items), and inadequate treatment (2 items). Dys-
phoria items measured the extent to which individuals feel
depressed, frightened, or overwhelmed by CD. Limitation
items measured the extent to which individuals feel limited
by CD when eating out with others, socializing, and trave-
ling. Health concern items measured the extent to which
individuals feel worried about long-term health outcomes
of CD for themselves or other family members. Inadequate
treatment items measured the extent to which individuals
feel there are enough treatment options for their CD. Each
final score had a possible range of 0–100 with higher scores
suggesting a higher degree of QOL.

CDPQOL

CD-specific pediatric quality of life (CDPQOL) in teenag-
ers was assessed using a 17-item validated survey instru-
ment [24]. Participants answered questions with Likert
scales where 0 = never, 1 = almost never, 2 = sometimes,
3 = often, 4 = almost always. Answers were transformed
and combined to obtain an overall score and four clinically
relevant subscales: social (7 items), uncertainty (3 items),
isolation (4 items), and limitations (3 items). Social items
measured self-esteem and the extent to which individuals
feel they are not understood or a burden. Uncertainty items
measured the extent to which individuals are worried about
college, their future, and getting older with CD. Isolation
items measured the extent to which individuals feel different
from their family and friends because of their CD. Limita-
tion items measured the extent to which individuals avoid
parties or feel nervous about eating at a friend’s house. Each
final score had a possible range of 0–100 with higher scaled
scores suggesting a higher degree of QOL.

Dietary Adherence and Vigilance

Dietary adherence was assessed using the Standardized
Dietitian Evaluation (SDE) instrument [25] which utilizes
evaluations from trained Masters students in nutrition. Three
24-h dietary recalls collected over a 1-month period and an
interview were reviewed for quantity and frequency of glu-
ten exposure (e.g., uses celiac-friendly restaurants or asks
thorough questions when dining out, has eliminated cross-
contamination potential in kitchen.) each recorded on a 6
point Likert scale ranging from 1 (excellent adherence) to 6
(not currently following a gluten-free diet).

Participants were divided into two groups: the “extremely
vigilant” and the “less vigilant.” Participants that received
an excellent adherence score for all 3 days of 24 h dietary
recalls were considered to be “extremely vigilant” (i.e., only
scores of 1 for all categories). All others were considered to
be “less vigilant” (scores of 2–6 for any of the categories on
any of the 3 days of 24 h dietary recalls).

Energy Level

One item from the Celiac Disease Adherence Test (CDAT)
[25] was used to classify participant’s energy level. Partici-
pants were asked the extent to which they were bothered by
low energy over the past 4 weeks with 1 = none of the time,
2 = a little of the time, 3 = some of the time, 4 = most of the
time, and 5 = all of the time. Those who responded ≥ 3 were
considered to have “lower energy” and those who responded
1 or 2 were considered to have “higher energy.”

Knowledge

Knowledge about gluten-containing ingredients was
assessed with a food label quiz developed by Leffler et al.
[25]. Participants were shown a modified food label and
asked to identify ingredients that contained or possibly con-
tained gluten. Individuals received 1 point for each of the
6 (out of 22) ingredients correctly identified as potentially
containing gluten. Scores could range from 0 (lower knowl-
edge) to 6 (higher knowledge).

Facilitators and Barriers

To assess barriers, participants were asked, “What do you
see as the major challenges to following a strict gluten free
diet?” To assess facilitators, participants were asked, “What
do you see as the things that help make it easy to follow a
strict gluten free diet?” Interviewers allowed participants
to spontaneously report whatever came to mind and then
probed to elicit further detail. All handwritten notes were
analyzed for major themes according to the methodology
described by Braun and Clarke [26]. Sample responses were

Digestive Diseases and Sciences
1 3

selected as representative of each theme. Some common
themes were apparent immediately (e.g., dislikes having to
ask questions, worrying about cross-contamination). Others
emerged after multiple readings. Some themes, not necessar-
ily common, were highlighted because of extreme specificity
(e.g., lack of labels for medications, makeup as a barrier;
other family members with CD as a facilitator).

Statistical Analysis

Means and standard deviations are presented for continu-
ous data, frequencies, and percentages for categorical data.
T-tests were used to assess group differences in QOL, knowl-
edge, and/or adherence between those with higher versus
lower energy levels and those that were extremely versus less
vigilant in following a strict gluten-free diet. Barriers and
facilitators are described with sample responses. Chi-square
tests with continuity correction were used to assess group
differences in frequency of barrier and facilitator themes.

Adults and teenagers were analyzed separately. We consid-
ered p < 0.05 as statistically significant.

Results

Characteristics of Study Sample

Table 1 shows the characteristics of our study sample of
50 adults and 30 teenagers. For adults, the mean age was
50.7 years and mean years since diagnosis was 11.7. The
sample of adults was mostly female (84.0%), white (94.0%),
with 68% holding college or advanced degrees. The major-
ity resided in New Jersey (NJ) (38.0%) or New York City
(NYC) (34.0%) and had gastroenterologists affiliated with
the Celiac Center at Columbia University (82.0%). Only
16% were currently seeing a RDN. For teenagers, the mean
age was 15.7 and mean years since diagnosis was 6.0. The
sample of teenagers was also mostly female (80%) and white
(96.7%). The majority (73.3%) were still in high school.

Table 1 Demographic and
patient characteristics of study
sample

BMI body mass index, NJ New Jersey, NYC New York City, NYS New York State, CT Connecticut, LI
Long Island, RDN Registered Dietitian Nutritionist

Adults (n = 50) Teenagers (n = 30)

Age, mean (SD) 50.7 (17.8) 15.7 (1.5)
BMI, mean (SD) 23.3 (3.4) 20.0 (2.4)
Years since diagnosis, mean (SD) 11.7 (10.8) 6.0 (4.6)
 1–4 8 (16.3) 14 (46.7)
 5–10 21 (42.9) 10 (33.3)
 > 10 20 (40.8) 6 (20.0)

Female gender (n, %) 42 (84.0) 24 (80.0)
Race (n, %)
 White 47 (94.0) 29 (96.7)
 Other 3 (6.0) 1 (3.3)

Education
 Middle school – 7 (23.3)
 High school 4 (8.0) 22 (73.3)
 Some college 12(24.0) 1 (3.3)
 College graduate 14 (28.0)
 Postgraduate 20 (40.0)

Residence (based on zip code) (n, %)
 NJ 19 (38.0) 10 (33.3)
 NYC 17 (34.0) 8 (26.7)
 Westchester 9 (18.0) 7 (23.3)
 Others (NYS, CT LI) 5 (10.0) 5 (16.7)

Gastroenterologist affiliated with Celiac Center 41 (82.0) 23 (76.7)
Visits with RDN
 RDN currently 8 (16.0) 8 (26.7)
 RDN past only (once) 25 (50.0) 11 (36.7)
 RDN past only (more than once) 12 (24.0) 2 (6.7)
 RDN never 5 (10.0) 9 (30.0)

Digestive Diseases and Sciences
1 3

Most resided in NJ (33.3%) or NYC (26.7%) and had gastro-
enterologists affiliated with the Celiac Center of Columbia
University (76.7%). A little over one-quarter were currently
seeing an RDN.

Differences in CD‑Specific QOL, Knowledge,
and Adherence by Energy Level

Table 2 shows differences in CD-specific QOL, knowledge,
and adherence by energy level. For adults, the overall mean
(SD) CDQOL score was 74.1 (14.2) which corresponds
to a good QOL [23]. Adults with lower energy levels had
significantly lower overall CD-specific QOL scores than
adults with higher energy levels [68.0 (13.6) vs 78.9 (13.0),
p = 0.006]. A similar pattern was seen for 2 of the 4 sub-
scales. Thus, for adults, lower energy level was associated
with more dysphoria (p = 0.024) and more reported limita-
tions (p = 0.002). Adults with lower energy level also dis-
played greater knowledge (5.6 (0.6) vs 5.0 (0.9), p = 0.012).

For teenagers, the overall mean (SD) CDPQOL score was
70.1 (14.9) which also corresponds to a good QOL [24].
Those with lower energy levels had significantly lower over-
all CDPQOL scores than teens with higher energy levels
(59.2 (16.7) vs 73.5 (13.0), p = 0.024). A similar pattern was
seen for 2 of the 4 subscales (social and isolation). Thus, for
teenagers, lower energy levels were associated with more
social concerns (p = 0.026) and greater feelings of isolation

(p = 0.017). Teenagers with lower energy levels also dis-
played greater knowledge (5.4 (0.5) vs 4.7 (0.9), p = 0.057),
although this association was not statistically significant.

Differences in CD‑Specific QOL and Knowledge
by Dietary Vigilance Level

Table 3 shows differences in CD-specific QOL and knowl-
edge by level of dietary vigilance. Extremely vigilant adults
(n = 12) had significantly lower overall QOL scores and
subscales than adults who were less vigilant [64.2 (16.0)
vs 77.2 (12.2), p = 0.004]. Adults that were extremely vigi-
lant displayed more dysphoria (p = 0.016), more reported
limitations (p = 0.004), and more concerns about inadequate
treatment (p = 0.012). At the same time, extreme vigilance
was also associated with greater knowledge [5.7 (0.7) vs 5.1
(0.8), p = 0.035]. The same patterns were not evident among
teenagers among whom there were no significant differences
by level of dietary vigilance.

Barriers and 

Facilitators

Table 4 summarizes major themes that arose from the open-
ended barrier and facilitator questions about maintaining
a strict gluten-free diet. Sample responses for each theme
are shown in Tables 5 (barriers) and 6 (facilitators). Bar-
rier responses fell into two main categories: those related

Table 2 Celiac disease-specific quality of life (QOL)a, knowledgeb, and adherencec in adults and teenagers by energy level

a Higher CDPQOL (adults) or CDPQOL (teenagers) scores and subscales suggest higher degree of QOL; Scales 0–100
b Higher knowledge scores suggest higher knowledge; Scale 0–6
c Higher adherence scores suggest lower adherence; Scale 1–6

Adults Higher energy (n = 28) Lower energy (n = 22) Total (n = 50) t p

Overall CD-QOL (0–100) 78.9 (13.0) 68.0 (13.6) 74.1 (14.2) 2.9 0.006
Subscales
Dysphoria 95.1 (9.1) 88.1 (12.2) 92.0 (11.0) 2.3 0.024
Limitations 76.4 (16.5) 61.1 (16.8) 69.7 (18.2) 3.2 0.002
Health concerns 71.8 (18.7) 66.8 (20.7) 69.6 (19.5) 0.9 0.377
Inadequate treatment 74.6 (22.7) 61.9 (27.9) 69.0 (25.7) 1.8 0.084
Knowledge 5.0 (0.9) 5.6 (0.6) 5.2 (0.8) − 2.6 0.012
Adherence (SDE) 1.4 (0.5) 1.2 (0.2) 1.3 (0.4) 2.0 0.056

Teenagers Higher energy (n = 23) Lower energy (n = 7) Total (n = 30) t p

Overall CDPQOL 73.5 (13.0) 59.2 (16.7) 70.1 (14.9) 2.4 0.024
Subscales
Social 73.6 (15.1) 58.2 (15.1) 70.0 (16.3) 2.4 0.026
Uncertainty 69.6 (21.1) 67.9 (12.2) 69.2 (19.2) 0.2 0.841
Isolation 78.5 (12.9) 59.8 (27.4) 74.2 (18.6) 2.5 0.017
Limitations 70.3 (21.3) 52.4 (29.5) 66.1 (24.2) 1.8 0.086
Knowledge 4.7 (0.9) 5.4 (0.5) 4.9 (0.9) − 2.0 0.057
Adherence (SDE) 1.3 (0.3) 1.3 (0.2) 1.3 (0.3) 0.0 0.988

Digestive Diseases and Sciences
1 3

to eating out and those related to gluten-free products (or
the lack thereof). For adults, the main barriers to eating out
included constant worries about cross-contamination (34%),
distrust of the gluten-free menu designation (30%), dislike of
having to constantly ask questions related to their diet and/
or advocate for safe food (30%), limited restaurant choices
(24%) dismissive or uninformed wait staff (22.0%), and the
general perception that gluten free is a fad or weight loss
diet (16%). Themes related to gluten-free products included
missing specific foods like pizza, bread, or pasta (38%), the
added expense of gluten-free options (22%), and the need
for better label laws for both food (16%) and pharmaceuti-
cals and makeup (16%). Less common, but described, were
concerns about gluten-free foods being unhealthy (12%) and
unpalatable (10%). There were no significant differences
between the 12 “extremely vigilant” adults and their less
vigilant counterparts, but, for nine of twelve barrier themes,
percentages were higher among the extremely vigilant. The
distribution of barrier themes was similar for teenagers,
although adults were more likely to mention lack of label
laws (16.0 vs 0.0%, χ2 = 3.7, df = 1, p = .054).

For adults, the main facilitator themes that emerged were
having supportive friends and family (70%), having more
gluten-free product options (52%), cooking at home versus
eating out (48%), having more gluten-free restaurant options
(36%), increased general awareness of the public about CD
(26%), and having helpful apps and internet sites (20%).
Less common, but described, were facilitators related to hav-
ing improved label laws (14%), having resources from the
Celiac Disease Center or from support groups (10%), and
having other family members with CD that related to their

needs (4%). The 12 “extremely vigilant” adults were more
likely than their less vigilant peers to mention helpful apps/
internet sites (50.0 vs 10.5%, χ2 = 6.6, df = 1, p = .010) and
were nearly significantly more likely to mention cooking
at home versus eating out (75.5 vs 39.5%, χ2 = 3.3, df = 1,
p = .069). For nine of ten facilitator themes, percentages
were higher among the “extremely vigilant” adults. The dis-
tribution of facilitator themes was similar for teens. Adults
were nearly significantly less likely to mention supportive
family/friends (70.0 vs 90.0%, χ2 = 3.2, df = 1, p = .072).

In the context of being asked about barriers, 56% of
adults and 70% of teens explicitly referenced the adverse
social impact of adhering to a gluten-free diet. Words that
came up included “misunderstood,” “embarrassed,” “differ-
ent,” “stigmatized,” “left out,” “awkward,” “guilty.” Some
suspected they were not invited to events or homes because
of their dietary restrictions. Others dreaded having to explain
their situation to new friends. There was resentment for the
fact that they could not be “spontaneous” like their peers and
that they often had to bring their own lunch or snacks. Three
teens expressed apprehension at having to manage their own
diet when they went away to college.

Discussion

This study is the first we are aware of that highlights the
potential negative consequences of hypervigilance to a strict
gluten-free diet for individuals with CD. The extremely vigi-
lant adults in our sample (i.e., those who consistently ate at
celiac-friendly restaurants, asked thorough questions when

Table 3 Celiac disease-specific quality of life (QOL)a and knowledgeb in adults and teenagers by vigilance level

a Higher CD-QOL (adults) or CDPQOL (teenagers) overall scores and subscales suggest higher degree of QOL; Scales 0–100
b Higher knowledge scores suggest higher knowledge; Scale 0–6

Adults Extremely vigilant
(n = 12)

Less vigilant (n = 38) Total (n = 50) t p

Overall CDQOL 64.2 (16.0) 77.2 (12.2) 74.1 (14.2) − 3.0 0.004
Subscales 85.4 (15.8) 94.1 (8.2) 92.0 (11.0) − 2.5 0.016
Dysphoria 56.7 (18.2) 73.8 (16.3) 69.7 (18.2) − 3.1 0.004
Limitations 65.0 (20.4) 71.1 (19.3) 69.6 (19.5) − 0.9 0.36
Health concerns 53.1 (25.1) 74.0 (24.0) 69.0 (25.7) − 2.6 0.012
Inadequate treatment knowledge 5.7 (0.7) 5.1 (0.8) 5.2 (0.8) 2.2 0.035

Teenagers Extremely vigilant
(n = 7)

Less vigilant (n = 23) Total (n = 30) t p

Overall CDOPQOL 74.6 (14.2) 68.8 (15.2) 70.1 (14.9) 0.9 0.38
Subscales 72.5 (16.7) 69.3 (16.5) 70.0 (16.3) 0.4 0.66
Social 66.7 (27.6) 69.9 (16.6) 69.2 (19.2) − 0.4 0.70
Uncertainty 83.9 (7.1) 71.2 (20.1) 74.2 (18.6) 1.6 0.12
Isolation 75.0 (15.2) 63.4 (26.0) 66.1 (24.2) 1.1 0.27
Limitations knowledge 5.1 (0.7) 4.8 (0.9) 4.9 (0.9) 0.9 0.39

Digestive Diseases and Sciences
1 3

dining out, eliminated cross-contamination potential in their
home kitchen.) had significantly lower QOL scores than their
less vigilant counterparts. Our qualitative data suggested
that cooking at home (as opposed to eating out) and using
internet sites and apps to facilitate gluten avoidance were
particularly prevalent strategies used by the hypervigilant to
maintain a strict gluten-free diet. The qualitative data also
highlighted the particulars that make eating out problematic
for individuals with CD.

Our findings are in contrast with several others that found
better dietary adherence to be associated with higher QOL
scores [18–21] or that found no association [27, 28]. Incon-
sistent findings may, in part, be due to differences in quality

of life instruments (generic vs CD specific), differences in
dietary adherence instruments (self-report vs RDN or health
professional opinion base on the dietary data), or geographic
location. In this study, we used validated celiac-specific
quality of life measures (CDQOL and CDPQOL) and relied
on nutrition professionals’ opinions about participant’s vigi-
lance based on interviews and 24-h recall data (as opposed
to self-reported perceptions of subject’s own dietary adher-
ence). For example, one participant perceived herself to be
extremely vigilant (i.e., reporting that she “never” had glu-
ten over the past month), but her interview and 24-h recalls
revealed a major source of cross-contamination (e.g., pulling
the croutons off of her Caesar salad before eating it). By

Table 4 Percentage of
respondents mentioning main
barrier and facilitator themes
for adhering to strict gluten-
free (GF) diet (based on
qualitative data) for adults and
teens: comparison of extremely
vigilant (EV) versus less
vigilant (LV) respondents

a Adults: pizza (8%), fast food options (16%), bread (10%), beer/vodka (10%), pasta (6%), dessert (4%),
breakfast options (6%), Chinese food (10%), Italian food (2%), teens: pizza (13%), snacks (13%), bread
(7%), pasta (7%), dessert (7%), breakfast options (3%), Chinese food (3%), Italian food (3%)
b Adult versus teen total p  <  .10: lack of label laws χ2  =  3.7, df  =  1, p  =  .054; supportive family/friends χ2 = 3.2, df = 1, p = .072 c EV versus LV p < .10: cooking at home versus eating out χ2 = 3.3, df = 1, p = .069; helpful apps/internet sites χ2 = 6.6, df = 1, p = .010

Adults Teens

EVa LVa Total EVa LVa Total

Barriers
Eating out
 Risk of cross-contamination 41.7 31.6 34.0 28.6 43.5 40.0
 Untrustworthy GF menus 33.3 28.9 30.0 28.6 17.4 20.0
 Need to ask questions/prepare ahead/advocate 33.3 28.9 30.0 42.9 30.4 33.3
 Limited restaurant choices 16.7 26.3 24.0 42.9 26.1 30.0
 Dismissive/uninformed wait staff 33.3 18.4 22.0 0.0 13.0 10.0
 Faddishness undermining seriousness 16.7 15.8 16.0 28.6 8.7 13.3
 Percentage reporting ≥ 1 eating out theme 83.3 71.0 74.0 85.7 87.0 86.7

GF products
 Missing specific foods (e.g., pizza, bread, pasta)a 41.7 36.8 38.0 57.1 39.1 43.3
 Added expense of GF foods 16.7 23.7 22.0 14.3 17.4 16.7
 Lack of label lawsb 16.7 15.8 16.0 0.0 0.0 0.0
 Determining gluten in pharmaceuticals/makeup 25.0 13.2 16.0 0.0 4.3 3.3
 Unhealthy GF foods 16.7 10.5 12.0 0.0 0.0 0.0
 Unpalatable GF foods 0.0 13.2 10.0 14.3 13.0 13.3
 Percentage reporting ≥ 1 GF products theme 75.0 71.1 72.0 71.4 47.8 53.3

Facilitators
Supportive family/friendsb 83.3 65.8 70.0 85.7 91.3 90.0
Accessibility of GF products 50.0 52.6 52.0 71.4 43.5 50.0
Cooking at home versus eating out 75.0 39.5 48.0c 71.4 43.5 50.0
Accessibility of GF restaurant options 33.3 36.8 36.0 14.3 56.5 46.7
Increased general knowledge/awareness 41.7 21.1 26.0 28.6 4.3 10.0
Helpful apps/internet sites 50.0 10.5 20.0c 42.9 21.7 26.7
Improved labeling 25.0 10.5 14.0 0.0 4.3 3.3
Celiac Center or support groups 8.3 10.5 10.0 0.0 4.3 3.3
Having other family members with celiac disease 0.0 5.3 4.0 14.3 13.0 13.3
Percentage reporting ≥ 1 facilitators 100.0 100.0 100.0 100.0 100.0 100.0

Digestive Diseases and Sciences
1 3

classifying participants’ vigilance level based on nutrition
professional’s opinion, we can more confidently assert that
the “extremely vigilant” group were truly those taking the
greatest precautions to avoid all sources of gluten.

Our data provide insights into the ways individuals with
CD struggle with eating out. Seventy-four percent of adults
and 86.7% of teens mentioned one or more barriers to adher-
ing to a gluten-free diet that were related to eating out. The
increasing popularity of the gluten-free diet in non-celiac
individuals [29] in the U.S. has created a variety of chal-
lenges for those with CD. The seriousness of gluten expo-
sure may now be dismissed at restaurants for being “trendy,”
forcing CD individuals to advocate even harder. Our find-
ings are in contrast to those conducted in Europe where the
gluten-free diet is recognized, even in restaurants, as a medi-
cal necessity for CD [18, 27]. Furthermore, while increasing
numbers of restaurants offer gluten-free menu options, it

is unclear what steps are taken to ensure that food service
staff handles food properly and with regular monitoring and
quality control. We found the desire to take advantage of
increased restaurant options, combined with the distrust of
menus and ill-informed wait staff, to be a source of consider-
able frustration and anxiety for our participants. For those
who were extremely vigilant, the frustration is reflected in
their reliance upon cooking at home as opposed to eating
out.

Our qualitative data also provide insights into prevalent
facilitators to staying gluten free. Supportive family and
friends, increased accessibility of gluten-free products,
apps and internet sites, and the benefits of cooking were
particularly appreciated. Adults who were extremely vigi-
lant particularly relied upon cooking at home versus eat-
ing out, and helpful apps and internet sites, more so than
their less vigilant counterparts. We believe identification

Table 5 Sample responses for barriers to adhering to strict gluten-free (GF) diet (based on qualitative data)

Barrier

Risk of cross-contamination The salad bar was marked as GF but was near croutons and stuff—it mixes!
Salad with side of bread or ice cream with cookies can come automatically. Will ask to send

back unless obvious the foods did not come in contact
Untrustworthy gluten-free menus The menu said GF and I got sick most times I was there

Many menus will say they are GF but clearly they are not (e.g., a salad that has pita bread,
dressing that’s not GF

Need to ask questions/prepare ahead/advocate You have to constantly be aware, especially in public settings. It feels like you are constantly
advocating. Having to be prepared all the time carrying snacks, checking restaurants ahead of
time, etc. Keeping other people educated can be exhausting. There is a lot of anxiety going to
a restaurant –being in line asking questions—I don’t want to hold up the line

Limited restaurant choices I wish places like Duncan Donuts or Starbucks were more considerate and have gluten free
snacks; big chains should have more options

I feel like I have to go to same restaurants all the time that I know are safe
Dismissive or uninformed wait staff For example, I was at pizza restaurant and asked about the fryer. I learned it was used for

gluten-containing foods so I didn’t order anything fried. Instead, I ordered the GF broccoli
pizza and later realized the broccoli was fried. I was upset that the staff wasn’t knowledge-
able enough to know I shouldn’t have had broccoli on the pizza despite having asked a lot of
questions

Faddishness undermining seriousness Restaurants complain that they are providing GF foods to people who don’t seem to be consist-
ent about needing to eat GF

Going out to eat is a problem especially because it’s a fad diet and not everyone takes it seri-
ously

Missing specific foods (e.g., pizza, bread, pasta) I can’t find good bread! All are small, bad texture
There are some commercial products like goldfish and ice cream cakes that don’t yet have a GF

option or the GF options don’t approximate it
Added expense of gluten-free foods My food costs have doubled

The cost of gluten free flours for baking are expensive
The restaurants that are safe are very expensive

Lack of label laws It is frustrating that in the US it is often difficult to know if foods/products contain gluten.
In South Africa everything is labeled containing gluten/not containing gluten. Ireland also
labels everything

Safety of pharmaceuticals or makeup It’s hard finding soaps and shampoos that are GF. In public restrooms, I don’t like to use the
soap—I’m never sure if should bring own

Unhealthy gluten-free foods Most gluten free products are junk food and poor diet quality
It is difficult to get adequate nutrients on a GF diet, specifically fiber and whole grains

Unpalatable gluten-free foods Sometimes I don’t tell the restaurant I am GF or I get steamed/boiled chicken that is really bad

Digestive Diseases and Sciences
1 3

of these facilitators can inform future educational efforts
to increase adherence to a gluten-free diet.

Our results suggest the importance of ongoing involve-
ment of a registered dietitian nutritionist (RDN) with
celiac patients, involvement that persists beyond the ini-
tial diagnosis [6, 7]. Conversations to promote dietary
adherence and ensure a high quality of life will take time
and cannot be done in a single visit. Our data, as well as
the literature, suggest that regular dietitian follow-up falls
short of guidelines. Of particular concern was that only
16% of adults and 26.7% of teenagers in our sample were
currently seeing a RDN. Most had a visit with a RDN
when first diagnosed, but without follow-up. Several had
never had a visit with a RDN. Our participants reported
relying on the internet for guidance, despite the fact that
most popular CD websites have been shown to be insuf-
ficiently accurate, comprehensive, or trustworthy [30].
Lack of insurance and/or limited availability of dietitians
specialized in CD were not likely to be problems for our
study population. The NIH consensus development con-
ference on CD advised that patients undergo consultation
with a skilled RDN and continuous long-term follow-up by
a multidisciplinary team. It appears that these guidelines
are rarely met among our participants who were contacted
via a celiac disease center email list [31].

From a clinician’s perspective, we believe our find-
ings have clinical relevance. In our study, adults who were
extremely vigilant versus less vigilant differed by at least
10 points on the overall CDQOL scale, as well as the dys-
phoria CDQOL subscale. And those who were extremely
vigilant versus less vigilant differed by approximately 20
points on the limitations and inadequate treatment CDQOL
subscales. When the CD-QOL instrument was validated, a
difference of approximately 10 points lower on the CD-QOL
scale was enough to move individuals into a worse category
of self-rated health, psychological distress, functional status,
or pain. For example, differences of 10 points on the CD-
QOL scale differentiated those that had low versus mid-level
psychological distress; differences of 20 points on the CD-
QOL scale differentiated those that had low versus high-
level psychological distress. Similar patterns were found
for the others scales. Thus, the hypervigilance described in
our sample (e.g., bringing their own dishes to restaurants or
other homes; thorough and repeated questioning at restau-
rants) may come with a meaningful and relevant cost.

This study has several limitations. First, it was conducted
at a single CD referral center, the sample sizes were small
and the population was demographically homogeneous. Sec-
ond, the design was cross sectional and not longitudinal.
While we found that “extreme vigilance” (in adults only)

Table 6 Sample responses to facilitators to adhering to strict gluten-free (GF) diet (based on qualitative data)

Facilitators

Supportive family and friends My family is a big help. We are strictly GF at home—no one is allowed to bring anything gluten
into the home

My boyfriend has switched to a mostly GF diet
My mom calls places ahead to see what I can eat—she’ll even go in a restaurant kitchen! My mom

is highly skilled at questioning the waiter!
Accessibility of GF products GF pretzels—years ago they didn’t exist!

There are just more products now, sections in food stores are larger, the quality and taste are better
Cooking at home versus eating out I cook so I don’t have to worry

I cook which makes it easier
I cook a lot so I have a good sense of what ingredients to ask about at restaurants (e.g., chicken

broth)
I have always cooked so I just cook differently now and then I know it’s safe

Accessibility of GF restaurant options Now you can go anywhere and eat out—you can get steak, chicken, GF pasta and pizza. It’s gotten
a lot easier over the years

Increased general knowledge and awareness Being GF is more known now in big cities. More mainstream. More available
Being GF is more common now so people make the connection
More restaurants are familiar, especially when traveling

Helpful apps and internet sites FindMeGlutenFree
Scanning bar codes

Improved labeling At least labels now say if a product contains wheat
Labeling laws now list the common allergies

Celiac Center or support groups Meeting with nutritionists at the Celiac Center and at school provides support
My support group, which is no longer together, was helpful adapting to diet. I am very grateful for

the network/community
Having other family members with CD Most of my family is Celiac so even at extended family gatherings there are a lot of options. I have

a cousin with celiac so that makes it more acceptance at family functions. My aunt makes two
turkeys on Thanksgiving

Digestive Diseases and Sciences
1 3

and low energy (in adults and teens) were associated with
lower CD-specific QOL, we cannot say if “extreme vigi-
lance” causes lower energy and QOL or if lower QOL and
energy lead to extreme vigilance. We speculate that, in some
individuals, extreme vigilance to a strict gluten-free diet may
be creating anxiety and stress leading to a lower QOL. This
anxiety and stress, may, in turn, lead to lack of sleep and
even depression, which may lead to low energy levels or
fatigue. The relationships need to be explored prospectively
to determine the direction of causality. Third, our measure
of energy level was limited to a single item on the CDAT.
A more extensive questionnaire on symptoms would have
been preferable. Fourth, vigilance was based on 24-h recalls
which rely on participant’s memory of what they ate and the
precautions they took to avoid gluten. Thus, there was the
potential for misclassification on level of vigilance. Finally,
our exploration of barriers to and facilitators of maintain-
ing a gluten-free diet were based on open-ended questions.
Themes were overlapping and it is likely that different peo-
ple were expressing the same idea, but with different choices
of words. When considering the percentages reporting each
theme, it must be kept in mind that study subjects were
not given the opportunity to agree or disagree with each
statement.

Our data illustrate the critical need to develop and evalu-
ate nutrition education strategies that promote increased
adherence to a gluten-free diet while, at the same time,
taking care to maintain high QOL. Given the seriousness
of poor adherence and psychological burden, it is surpris-
ing that there is so little research conducted on alternative
approaches to improve gluten-free diet adherence and QOL.
In fact, only five behavioral intervention studies have been
reported with CD patients [32–36] of which only one [35]
targeted adherence and two targeted QOL [34, 36]. Possible
future directions would be to explore interventions that com-
bine visits to a RDN (i.e., standard of care) with strategies
designed to address barriers associated with eating out (e.g.,
portable gluten sensor monitoring or promotion of skills to
combat the perception that gluten free is only a fad). Inter-
ventions that promote cooking skills could decrease reliance
on eating out. Since over 80% of participants reported the
importance of supportive friends and family, it is important
to determine the impact of family-centered nutrition educa-
tion when promoting dietary adherence. Ultimately, we need
longitudinal studies to test the best level of dietary adherence
that can avoid symptoms, intestinal damage, and long-term
complications, yet maximize energy levels and quality of
life for the celiac population. We also need to determine
the significance of potential sources of cross-contamination
for the risk of ingesting small quantities of gluten. Until
then, we must advocate for a strict gluten-free diet with the
caveat that, for some, such hypervigilance comes at a cost
that needs to be supported and addressed.

Conclusion

In this prospective, cross-sectional study, we identified
potential negative consequences of hypervigilance to a strict
gluten-free diet for individuals with CD. Clinicians need
to be aware of the importance of promoting both dietary
adherence and quality of life. While patients must be encour-
aged to continue following a strict 100% gluten-free diet, we
hope that our findings highlight the importance of clinicians
addressing both adherence to a strict gluten-free diet while
concurrently addressing emotional and social well-being
while caring for their patients with celiac disease. Our find-
ings suggest that there may be a cost to such hypervigilance
and interventions that promote both strict adherence and
maximize quality of life are urgently needed.

Acknowledgments Supported by the Provost Investment Fund at
Teachers College Columbia University and in part by Columbia Uni-
versity’s CTSA Grant No. UL1 TR000040 from NCATS/NIH.

Author’s contribution RW, BL, AL, NR, and PG conceptualized and
designed the study. JC and CA collected data and contributed to con-
ceptualization of the qualitative analyses. PZ managed and analyzed
the data. All authors (RW, BL, AL, PZ, NR, JC, CA, PG) reviewed and
commented on multiple drafts of the manuscript, and all played a key
role in the interpretation of study results.

Funding This study was funded by the Provost Investment Fund at
Teachers College Columbia University and in part by Columbia Uni-
versity’s CTSA Grant No. UL1 TR000040 from NCATS/NIH.

Compliance with ethical standards

Conflicts of interest RW, BL, AL, PZ, NR, JC, CA declare that they
have no conflicts of interest. PG serves on the Advisory board of Im-
musanT, Cellimmune and ImmunogenX.

Ethical approval All procedures performed in this study involving
human participants were in accordance with ethical standards of the
institutional review boards at both Columbia University Medical Center
and Teachers College, Columbia University and with the 1964 Helsinki
Declaration and its later amendments or comparable ethical standards.

Informed consent Written informed consent was obtained from all
individual participants included in the study.

References

1. Green PHR, Krishnareddy S, Lebwohl B. Clinical manifestations
of celiac disease. Dig Dis. 2015;33:137–140.

2. Abu Daya H, Lebwohl B, Lewis SK, et  al. Celiac disease
patients presenting with anemia have more severe disease than
those presenting with diarrhea. Clin Gastroenterol Hepatol.
2013;11:1472–1477.

3. Rubio-Tapia A, Kyle RA, Kaplan EL, et al. Increased prevalence
and mortality in undiagnosed celiac disease. Gastroenterology.
2009;137:88–93.

Digestive Diseases and Sciences
1 3

4. Rubio-Tapia A, Ludvigsson JF, Brantner TL, et al. The preva-
lence of celiac disease in the United States. Am J Gastroenterol.
2012;107:1538–1544.

5. Lohi S, Mustalahti K, Kaukinen K, et  al. Increasing preva-
lence of coeliac disease over time. Aliment Pharmacol Ther.
2007;26:1217–1225.

6. Rubio-Tapia A, Hill ID, Kelly CP, et al. American College of
Gastroenterology. ACG guidelines: diagnosis and management
of celiac disease. Am J Gastroenterol. 2013;108:656–676.

7. Ludvigsson JF, Bai JC, Biagi F, et  al. BSG Coeliac Disease
Guidelines Development Group; British Society of Gastroen-
terology. Diagnosis and management of adult coeliac disease:
guidelines from the British Society of Gastroenterology. Gut.
2014;64:1210–1228.

8. Hornell A. Effects of a gluten-free diet on gastrointestinal symp-
toms in celiac disease. Am J Clin Nutr. 2007;85:160–166.

9. Fabiani E, Catassi C. International Working Group. The serum
IgA class anti-tissue transglutaminase antibodies in the diagno-
sis and follow-up of coeliac disease: results of an international
multi-center study. International Working Group on Eu-tTG. Eur
J Gastroenterol Hepatol. 2001;13:659–665.

10. Catassi C, Fabiani E, Iacono G, et al. A prospective, double-blind,
placebo-controlled trial to establish a safe gluten threshold for
patients with celiac disease. Am J Clin Nutr. 2007;85:160–166.

11. Lebwohl B, Granath F, Ekbom A, et al. Mucosal healing and risk
for lymphoproliferative malignancy in celiac disease: a popula-
tion-based cohort study. Ann Intern Med. 2013;159:169–175.

12. Meyer D, Stavropolous S, Diamond B, et al. Osteoporosis in a
North American adult population with celiac disease. Am J Gas-
troenterol. 2001;96:112–119.

13. Lee AR, Diamond B, Ng D, et al. Quality of life of individuals
with celiac disease: survey results from the United States. J Hum
Nutr Diet. 2012;25:233–238.

14. Ciacci C, D’Agate C, DeRosa A, et al. Self-rated quality of life in
celiac disease. Dig Dis Sci. 2003;48:2216–2220.

15. Zarkadas M, Dubois S, Maclsaac K, et al. Living with coeliac
disease and a gluten-free diet: a Canadian perspective. J Hum Nutr
Diet. 2013;26:10–23.

16. Shah S, Akbari M, Vanga R, et al. Patient perception of treatment
burden is high in celiac disease compared with other common
conditions. Am J Gastroenterol. 2014;109:1304–1311.

17. Zignone F, Swift GL, Card TR, et al. Psychological morbidity of
celiac disease: a review of the literature. United Eur Gastroenterol
J. 2014;3:136–145.

18. Casellas F, Rodrigo L, Lucendo AJ, et al. Benefit of health-related
quality of life of adherence to gluten-free diet in adult patients
with celiac disease. Rev Esp Enferm Dig. 2015;107:196–201.

19. Usai P, Minerba L, Marini B, et al. Case control study on health-
related quality of life in adult coeliac disease. Dig Liver Dis.
2002;34:547–552.

20. Hauser W, Stallmach A, Caspary WF, et al. Predictors of reduced
health-related quality of life in adults with coeliac disease. Aliment
Pharmacol Ther. 2007;25:569–578.

21. Nachman F, Planzer del Campo M, Gonzalez A, et al. Long-term
deterioration of quality of life in adult patients with celiac dis-
ease is associated with treatment noncompliance. Dig Liver Dis.
2010;42:685–691.

22. White LE, Bannerman E, Gillett PM. Coeliac disease and the
gluten free diet: a review of the burdens; factors associated with
adherence and impact on health-related quality of life, with spe-
cific focus on adolescence. J Hum Nutr Diet. 2016;29:593–606.

23. Dorn SD, Hernandez L, Minayas MT, et al. The development and
validation of a new coeliac disease quality of life survey (CD-
QOL). Aliment Pharmacol Ther. 2009;31:666–675.

24. Jordan NE, Li Y, Magrini D, et al. Development and validation
of a celiac disease quality of life instrument for North American
children. J Pediatr Gastroenterol Nutr. 2013;57:477–486.

25. Leffler DA, Dennis M, Edwards JB, et  al. A simple validated
gluten-free diet adherence survey for adults with celiac disease.
Clin Gastroenterol Hepatol. 2009;7:530–536.

26. Braun V, Clarke V. What can “thematic analysis” offer health
and wellbeing researchers? Int J Qual Stud Health Well-being.
2014;9:26152.

27. Barratt SM, Leeds JS, Sanders DS. Quality of life in coeliac dis-
ease is determined by perceived degree of difficulty adhering to
a gluten-free diet, not the level of dietary adherence ultimately
achieved. J Gastrointest Liver Dis. 2011;20:241–245.

28. Hopman EGD, Koopman HM, Maarten Wit J, et al. Dietary com-
pliance and health-related quality of life in patients with coeliac
disease. Eur J Gastroenterol Hepatol. 2009;21:1056–1061.

29. Half of Americans Think Gluten-Free Diets are Fad While 25%
Eat Gluten-Free Foods. Minten Group, Ltd. http://www.minte
l.com/press -centr e/food-and-drink /half-of-ameri cans-think -glute
n-free-diets -are-a-fad-while -25-eat-glute n-free-foods . Accessed
July 25, 2017.

30. McNally SL, Donohue MC, Newton KP, et al. Can consumers
trust web-based information about celiac disease? Accuracy,
comprehensiveness, transparency, and readability of informa-
tion on the internet. Interact J Med Res. 2012;1:e1. https ://doi.
org/10.2196/ijmr.2010.

31. NIH Consensus Development Conference on Celiac Disease.
https ://conse nsus.nih.gov/2004/2004c eliac disea se118 html.htm.
Accessed July 28, 2017.

32. Addolorato G, DeLorenzi G, Abenavoli L, et al. Psychological
support counselling improves gluten-free diet compliance in coe-
liac patients with affective disorders. Aliment Pharmacol Ther.
2004;20:777–782.

33. Meyer KG, Fasshauer M, Nebel IT, et al. Comparative analysis
of conventional training and a computer-based interactive train-
ing program for celiac disease patients. Patient Educ Couns.
2014;54:353–360.

34. Ring Jacobsson L, Friedrichsen M, Al G, et al. Does a coeliac
school increase psychological well-being in women suffering
from coeliac disease, living on a gluten-free diet? J Clin Nurs.
2012;21:766–775.

35. Sainbury K, Mullan B, Sharpe L. A randomized controlled trial
of an online intervention to improve gluten-free diet adherence in
celiac disease. Am J Gastroenterol. 2013;108:811–817.

36. Haas K, Martin A, Park KT. Text message intervention (TEACH)
improves quality of life and patient activation in celiac dis-
ease: a randomized clinical trial. J Pediatr. 2017;. https ://doi.
org/10.1016/j.jpeds .2017.02.062.

http://www.mintel.com/press-centre/food-and-drink/half-of-americans-think-gluten-free-diets-are-a-fad-while-25-eat-gluten-free-foods

http://www.mintel.com/press-centre/food-and-drink/half-of-americans-think-gluten-free-diets-are-a-fad-while-25-eat-gluten-free-foods

http://www.mintel.com/press-centre/food-and-drink/half-of-americans-think-gluten-free-diets-are-a-fad-while-25-eat-gluten-free-foods

https://doi.org/10.2196/ijmr.2010

https://doi.org/10.2196/ijmr.2010

https://consensus.nih.gov/2004/2004celiacdisease118html.htm

https://doi.org/10.1016/j.jpeds.2017.02.062

https://doi.org/10.1016/j.jpeds.2017.02.062

• Hypervigilance to a Gluten-Free Diet and Decreased Quality of Life in Teenagers and Adults with Celiac Disease

Abstract
Background and Aims
Methods
Results
Conclusion
Introduction
Methods
Design
Setting and Participants
Enrollment
Data Collection and Measures
Demographic and Medical History Variables
Celiac Disease-Specific Quality of Life
CDQOL
CDPQOL
Dietary Adherence and Vigilance
Energy Level
Knowledge
Facilitators and Barriers
Statistical Analysis
Results
Characteristics of Study Sample
Differences in CD-Specific QOL, Knowledge, and Adherence by Energy Level
Differences in CD-Specific QOL and Knowledge by Dietary Vigilance Level
Barriers and Facilitators
Discussion
Conclusion
Acknowledgments
References