What Is Known/What Is New
What Is Known
- Celiac disease remains undiagnosed for a long time in many adult and pediatric patients.
- Long diagnostic delays might be because of poor knowledge about the disease among healthcare professionals.
- The lack of knowledge about celiac disease might influence the adherence of patients to the gluten-free diet.
What Is New
- The knowledge about celiac disease among HCPs and patients is not satisfactory.
- Pediatric gastroenterologists have higher knowledge about celiac disease than other HCPs.
- Parents of children with celiac disease have higher knowledge about the disease than adult patients and children.
- Members of celiac disease societies and patients with recently diagnosed celiac disease have higher knowledge about the disease.
Celiac disease (CD) is a lifelong systemic autoimmune disorder, elicited by gluten and related prolamines in genetically susceptible individuals (1). Traditionally defined as gluten-related enteropathy, it is one of the most common chronic illnesses and affects about 1% of the population (2–5). It has a very diverse clinical presentation, involving intestinal, extraintestinal, and even asymptomatic presentations (1,4,6–8). Due to its genetic background, CD is more common among family members of affected individuals and is associated with a number of other conditions, including type-1 diabetes, IgA deficiency, autoimmune thyroid disease, and certain chromosomal abnormalities, such as Down syndrome, Turner syndrome, and Williams syndrome (1,9–11).
The diagnosis of celiac disease is suspected by the clinical presentation but the definitive diagnosis is based on the presence of celiac-specific autoantibodies and characteristic histological changes in the small intestinal mucosa. Recently, the European Society for Pediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN) and European Society for the Study of Celiac Disease (ESsCD) published new guidelines for the diagnosis of CD in children and adults, respectively (1,12). Despite many similarities, ESPGHAN guidelines allow pediatric gastroenterologists to diagnose the disease without intestinal biopsy when certain criteria are met (1,12,13).
The only available treatment for CD is a lifelong strict gluten-free diet, which should only be initiated after the firm confirmation of the diagnosis (1,9,14). Once on a diet, patients have to exclude all gluten-containing products, including products from wheat and wheat cultivars, rye, barley, kamut (Khorasan wheat), triticale, and bulgur. Owing to the high likelihood of cross-contamination, oats are also recommended to be avoided in many regions (15,16), regardless of the reports showing that the consumption of uncontaminated oats is well tolerated and may improve quality of life of patients (17).
Despite being one of the most common lifelong disorders, CD remains undiagnosed for a long time in many patients. Diagnostic delays in some regions exceed 10 years, which could have an important adverse effect on patients’ health and their quality of life (18–27). After confirmation of the diagnosis, high patient awareness of their condition is vital, in order to avoid the development of serious disease-related complications, which could affect various organ systems, for example, neurological, hematological, and reproductive systems. Also, psychological and psychiatric disorders could occur (4,9,28–30).
One of the possible reasons for long diagnostic delays might be poor knowledge about the disease among HCPs. Also, the lack of knowledge about CD might influence the adherence of patients to gluten-free diet, so the aim of our study was to assess the knowledge about CD among healthcare professionals (HCPs) and patients in Central Europe (CE).
METHODS
The study was carried out between the end of March 2017 and October 2019, as a part of the Focus IN CD project (CE 111), co-financed by the Interreg CE Programme. Twelve partners from 5 CE countries (Croatia, Germany, Hungary, Italy, and Slovenia) participated in the project.
Participants and Study Design
Healthcare professionals (HCPs) and CD patients or their caregivers in 5 CE countries were asked to complete the web-based questionnaire about CD (https://www.interreg-central.eu/Content.Node/surveys.html). Both questionnaires were translated to the languages of all project partners. The questionnaire for HCPs was composed of 22 questions, divided into 3 subsections—epidemiology and clinical presentation (7 questions), diagnostic procedure (6 questions), and treatment with follow-up (9 questions). The questionnaire for CD patients had 14 questions and was divided into 2 subsections—epidemiology, clinical presentation, and diagnostic procedure (7 questions), and treatment with follow-up (7 questions). All 14 questions were identical for patients and HCPs. To better compare the 2 groups, questionnaires shared the same structure and 9 questions for HCPs and patients had identical answer possibilities. In the remaining 5 questions for patients, there were fewer answer possibilities compared with the questions for HCPs. Individual questions were scored based on their complexity with 1 or 2 points. Total score for each individual subsection was calculated as the percentage of maximum score possible.
We analyzed knowledge of HCPs managing CD patients according to their specialty and assessed regional differences in knowledge among CD patients. We also analyzed the effect of the disease duration and involvement in patient support groups on the knowledge of CD patients or their caregivers.
Statistical Analysis
Statistical analysis was performed using IBM SPSS Statistics 22.0 for Windows. One-way ANOVA, multiple linear regression, Independent Samples t-test, and Pearson Correlation test were used for the analysis.
The study was approved by the National Medical Ethics Committee of the Republic of Slovenia (0120-383) and the Slovenian Research Agency (ARRS).
RESULTS
Healthcare Professionals’ Knowledge Analysis
The questionnaire was completed by 1381 HCPs (76% women, mean age 50 years) from Croatia (N = 143), Hungary (N = 670), Germany (N = 71), Italy (N = 359), and Slovenia (N = 138).
Most participants were pediatricians (42%), followed by general practitioners (31%), internal medicine specialists (6%) and other HCPs (Table 1). Almost half of HCPs (43%) have a friend or distant relative with CD, and 10% have a close relative with CD. HCPs mostly receive information about CD at seminars, lectures, and congresses (77%), from medical journals (68%), and on the internet (59%).
TABLE 1 -
Participating healthcare professionals by specialty
| Specialty |
CRO (N = 143) |
HUN (N = 670) |
GER (N = 71) |
ITA (N = 359) |
SLO (N = 138) |
Total CE (N = 1381) |
| General practitioners |
15% |
14% |
6% |
77% |
22% |
31% |
| Pediatricians |
| Primary care pediatricians |
11% |
38% |
65% |
11% |
34% |
29% |
| Pediatric gastroenterologists |
5% |
4% |
8% |
0.6% |
6% |
3% |
| Other |
34% |
10% |
4% |
2% |
8% |
10% |
| Internal medicine specialists |
| Gastroenterologists |
1% |
2% |
0 |
0.3% |
3% |
1% |
| Other |
4% |
4% |
14% |
0.3% |
12% |
5% |
| Other HCPs∗ or unclear specialty |
30% |
28% |
3% |
9% |
15% |
21% |
CRO = Croatia; HUN = Hungary; GER = Germany; ITA = Italy; SLO = Slovenia.
∗Pediatric residents, neurologists, ophthalmologists, anesthesiologists, dermatologists, dentists, infectious disease specialists, psychiatrists, dietitians
The mean score achieved by HCPs was 50.9%. Only 14% of all HCPs and 18% of pediatricians achieved more than 70% of the maximal score. More than 50% of the total score was achieved by 51% of all HCPs and 55% of pediatricians. No one answered all the questions correctly. The highest number of correct answers was found in the treatment and follow-up subsection with 77% of HCPs answering more than half of the questions correctly.
Significant differences were found between different specialties with pediatricians (mean score: 54.0%) and general practitioners (53.4%) scoring higher than internal medicine specialists (46.0%) and other HCPs (42.8%) (P < 0.001). When comparing gastroenterologists (pediatric gastroenterologists [N = 49] and internal medicine gastroenterologists [N = 20]) with primary care physicians (primary care pediatricians [N = 405] and general practitioners [N = 424]), we found that pediatric gastroenterologists (mean score: 69.4%) scored significantly higher than internal medicine gastroenterologists (54.2%) (P < 0.05), primary care pediatricians (53.4%) (P < 0.001), and general practitioners (53.4%) (P < 0.001). Analyzing the subsections of the questionnaire, we found that in the subsection on epidemiology and clinical presentation, primary care physicians (pediatrics and general practice), scored lower in comparison to gastroenterologists (pediatric and internal medicine); however, all 4 groups scored better in the treatment and follow-up subsection, with pediatric gastroenterologists reaching the highest score (Table 2).
TABLE 2 -
Results achieved by primary care physicians and gastroenterologists according to different subsections of the questionnaire
|
General practitioners (N = 424) |
Primary care pediatricians (N = 405) |
Paediatric GI (N = 49) |
Internal medicine GI (N = 20) |
| Overall mean score |
53.4% (SD ±16.5) |
53.4% (±15.5) |
69.4%∗ (±10.7) |
54.2% (±9.4) |
| Epidemiology and clinical presentation |
46.2% (SD ± 17.5) |
46.3% (±17.1) |
60.8%∗∗ (±13.8) |
51.7% (±13.6) |
| Diagnostic procedure |
40.4% (SD ± 26.2) |
39.7% (±27.8) |
63.3%∗ (±23.3) |
34.2% (±14.8) |
| Treatment and follow-up |
67.8% (SD ± 17.9) |
68.1% (±16.2) |
80.8%∗∗∗ (±15.1) |
68.5% (±14.2) |
SD = standard deviation.
∗Significant difference versus general practitioners, primary care pediatricians and internal medicine gastroenterologists (GI) (P < 0.001).
∗∗Significant difference versus general practitioners, primary care pediatricians (P < 0.001).
∗∗∗Significant difference versus general practitioners, primary care pediatricians (both P < 0.001), and internal medicine gastroenterologists (P < 0.05).
HCPs with a family member or friend with CD scored significantly higher in comparison to the others (54.9% vs 48.3%; P < 0.001). There is a negative correlation between achieved score and age of HCPs (r = −0.186; P < 0.001) and work experience of HCPs (r = −0.197; P < 0.001). Male HCPs scored significantly higher than female HCPs (54.2% vs 50.8%, P < 0.05). Multiple regression analysis showed that sex and specialty statistically significantly predict achieved score (P > 0.05).
Patients and Caregivers’ Knowledge Analysis
The questionnaire was completed by 2262 CD patients or their caregivers (39% caregivers) from Croatia (N = 131), Hungary (N = 321), Germany (N = 1311), Italy (N = 74), and Slovenia (N = 425). The majority of participants were members of patient support groups (81%), with the highest membership in Slovenia (91%), followed by Germany (88%). 10.9% of patients and caregivers, however, did not answer this question so, they were excluded from the analyses related to support groups membership. Half of the patients (51%) were diagnosed within the last 5 years.
The mean score achieved was 56.4%. Total score higher than 50% was achieved by 58% of CD patients or caregivers and 418 (18%) achieved more than 70% of maximal score. One patient answered all the questions correctly. The highest number of correct answers was found in the treatment and follow-up subsection with 84% of participants answering more than half of the questions correctly. Comparing the answers of patients and caregivers, the latter scored significantly higher than adult CD patients (58.1% vs 55.4%; P < 0.001) (Table 3).
TABLE 3 -
Results of celiac disease
patients and caregivers according to the different subsections of the questionnaire
|
Children with CD (63) |
Parents of CD patients (892) |
Adult patients (1307) |
| Overall mean score |
53.4% (SD ± 13.6) |
58.1%∗ (±13.6) |
55.4% (±13.9) |
| Epidemiology, clinical presentation and diagnosis |
39.8% (SD ± 15.1) |
43.3% (±16.4) |
42.7% (±16.3) |
| Treatment and follow-up |
70.4% (SD ± 17.1) |
76.7%∗ (±16.5) |
71.2% (±17.7) |
CD = celiac disease; SD = standard deviation.
∗Significance versus adult patients, P < 0.001.
There were significant differences between different CE countries, with German participants (58.3%) scoring significantly higher than Hungarian (53.7%; P < 0.001) and Slovenian participants (52.9%; P < 0.001). Participants from Croatia (55.6%) and Italy (55.3%) also scored higher than patients from Hungary and Slovenia; however, the difference was not significant.
Members of CD support groups scored higher compared with nonmembers (mean 58.0% vs 53.2%; P < 0.001), with significantly higher scores found in patient support group members from Germany, Hungary, and Croatia. We also found that patients who were diagnosed less than 5 years ago scored higher compared with those diagnosed more than 10 years ago (mean score 57.3% vs 54.6%; P < 0.001) (Table 4).
TABLE 4 -
Mean score according to the celiac disease patient support group membership and duration of the disease
|
CD Society membership, N (%) |
Mean score, % (SD) |
Sig |
|
|
Members |
Nonmembers |
|
| Croatia |
78 (68) |
59.4% (SD ± 12.6) |
50.8% (SD ± 11.3) |
<0.05 |
| Germany |
1052 (88) |
59.6% (±13.2) |
55.2% (±12.2) |
<0.001 |
| Hungary |
128 (45) |
55.9% (±15.9) |
51.9% (±12.4) |
<0.05 |
| Italy |
45 (67) |
58.4% (±13.0) |
55.8% (±14.9) |
NS |
| Slovenia |
325 (91) |
53.6% (±13.0) |
51.6% (±13.5) |
NS |
| Central Europe |
1628 (81) |
58.0% (±13.6) |
53.2% (±12.6) |
<0.001 |
| Diagnosed |
| <5 years ago |
774 (68) |
59.6% (±13.3) |
52.9% (±12.9) |
<0.001 |
| 5 to 10 years ago |
373 (75) |
58.0% (±12.9) |
54.8% (±12.3) |
NS |
| >10 years ago |
481 (78) |
55.5% (±14.1) |
52.5% (±11.5) |
NS |
CD = celiac disease; NS = nonsignificant.
When comparing the knowledge between patients and HCPs regarding the major gluten-containing grains, we found that patients know the harmful grains better in comparison to HCPs (see Figures 1–4, Supplementary Digital Content, https://links.lww.com/MPG/C128, https://links.lww.com/MPG/C129, https://links.lww.com/MPG/C130, https://links.lww.com/MPG/C131, which show the knowledge about harmful and safe grains among HCPs and CD patients or their caregivers). Among CD patients and their caregivers, 29% recognized all the grains correctly, contrary to the HCPs, were only 10% correctly identified all gluten-containing grains.
DISCUSSION
Our study showed that the knowledge of HCPs is not satisfactory as, on average, only half of the questions were answered correctly. This is in line with other published studies that found low knowledge of HCPs about CD (31–37). The lowest scores found in the subsection on diagnostic procedures are especially worrisome, in particular, for internal medicine gastroenterologists, who should be well aware of diagnostic options in CD patients. The opposite was found in some other studies, where gastroenterologists demonstrated higher knowledge compared with the other study groups (32,36). It is, however, important to note that pediatric gastroenterologists achieved the highest scores, which is likely to be related to a higher awareness about the burden of CD and possibly also to a greater impact of existing ESPGHAN guidelines on this group. The diagnostic procedure is, however, still poorly understood in some areas or the guidelines are not followed entirely (32,38,39). It is quite concerning that primary care physicians (pediatricians and general practitioners) scored low in the epidemiology and clinical presentation subsection, which should be well recognized, as they represent the first contact point for potential CD patients (31). Our results are, however, in line with those of Zipser et al (36), who found that family physicians’ awareness of the onset of the symptoms of illness and related diseases needs to be improved (36). In our study, better results were found in the section on treatment and follow-up, which is very important for physicians advising CD patients. Pediatric gastroenterologists showed especially good results in this section. We have also shown that with age, knowledge of HCPs about CD decreases, meaning that younger physicians know more about the disease and recognize the potential patients better. Similar, Assiri et al (31) showed in their study that young physicians performed better than seniors because of recently acquired knowledge about CD in medical schools, in comparison to the senior physicians, who were learning about CD when it was still taught to be a rare malabsorptive disorder (31). The opposite was found in the study of Barzegar et al (32), where participants with more than 10 years of work experience had better knowledge and better performance in the diagnosis and treatment of CD (32).
It is also interesting to note that physicians who have friends and/or relatives with CD scored higher, which suggests that informal learning can play an important role.
Poor knowledge among HCPs leads to the disease being underdiagnosed (32,34) and adds to the long diagnostic delays that were observed in many studies (18,19–27). Our previous study (18) found relatively short diagnostic delays in children with CD in Central Europe, which could correlate with the satisfactory knowledge of pediatric gastroenterologists in CE, demonstrated by this study.
The knowledge about CD among patients is also not satisfactory. It is worrisome that almost one fifth of patients scored less than 50% in the subsection of treatment, which should be of the highest importance for patients. We found higher knowledge among parents in comparison to adults and children with CD, especially about the treatment and follow-up, probably as they are responsible for the meals of their child and are especially careful not to do any harm. The opposite was found in other studies, where poor parental knowledge and attitude towards CD and its management were observed (40). In the United Kingdom, Tomlin et al (41) showed that only one-third of parents had good overall knowledge of CD, with better results found in understanding that a gluten-free diet is the only available treatment of the disease. In that study, however, only 33% of parents correctly identified all gluten-containing foods (41), which is slightly higher than in our study. One-third of parents thought that rye did not contain gluten, whereas 98% correctly identified gluten as a component of wheat (41). Paganizza et al (42) showed that patients’ knowledge regarding CD and gluten-free diet was generally poor and that knowledge was strongly and significantly associated with adherence to a gluten-free diet (42). Similar results were found in other studies, where adherence to the gluten-free diet was associated with having a better knowledge of CD (43,44). In our study, the benefit of membership in patient support groups was clearly demonstrated in many aspects, with members consistently performing significantly better. Also, recently diagnosed patients presented better knowledge, probably as they had learned about the disease (more) recently. Studies have shown that the education of CD patients is very important and significantly increases the knowledge of CD (45,46). Barzegar et al (45) showed that the level of knowledge and understanding of patients in terms of epidemiology, diagnosis, and treatment was significantly increased after an education program (45). Similar was shown also in the study of Connan et al (46) where knowledge about the gluten-free diet increased significantly after undergoing an e-learning module designed to educate patients and families with concurrent CD and type-1-diabetes (46).
As questionnaires used for HCPs and CD patients were almost identical, performance of both groups can be at least partially compared. We have seen that both groups performed comparably, with more than 50% of participants scoring more than 50% of all points; however, the patients scored better in the treatment and follow-up, which is somewhat expected. Among HCPs, pediatric gastroenterologists showed the highest knowledge about the treatment and follow-up and among CD patients and their caregivers, the latter scored the highest. This might be at least partially attributed to stronger cooperation between pediatric gastroenterologists and parents of newly diagnosed children.
One of the limitations of our study is not to have sufficient regional representation of HCPs in some subspecialties to be able to reliably compare results between participating countries. On the other hand, a large number of participants, both HCPs and patients, represents a strength of the study. Also, the similarity of the questionnaires gives us an option to compare both groups.
It would be interesting to know whether better knowledge of HCPs leads to shorter diagnostic delays, whether HCPs knowledge is related to their follow-up practices and whether better knowledge among HCPs leads to better compliance and knowledge among CD patients.
To conclude, the knowledge of HCPs and CD patients is not satisfactory. Further awareness-raising and learning activities are needed especially among primary care pediatricians and general practitioners to improve their knowledge. An e-learning programme, such as the one developed within the EU funded project Focus IN CD (https://www.celiacfacts.eu/focusincd-en) could serve as a valuable tool for patients, their caregivers, and practicing HCPs. Better knowledge will effectively reduce the number of unrecognized patients and unnecessary diagnostic delays, and will improve the quality of patient care and reduce health care costs in Central Europe. Similarly, patients should be better informed about their disease in order to reach higher compliance with the gluten-free diet. Patients, as well as their caregivers, should be encouraged to join patient support organizations and recommended to use available patient-oriented learning opportunities, which can play an important role in building patient self-management capacities.
Acknowledgments
The authors wish to thank all the participating physicians and celiac disease patients or their caregivers from Croatia, Germany, Hungary, Italy, and Slovenia, who answered the questionnaires, thus enabling us to do the study. We are also grateful to all the project partners who helped in designing the questionnaire and its translation to the partner languages as well as in distributing the questionnaire to the physicians and to patient support groups for distributing questionnaires to CD patients from participating regions.
REFERENCES
1. Husby S, Koletzko S, Korponay-Szabó I, et al. European Society for Paediatric Gastroenterology, Hepatology and Nutrition Guidelines for Diagnosing Coeliac Disease 2020.
J Pediatr Gastroenterol Nutr 2020; 70:141–156.
2. Catassi C, Gatti S, Fasano A. The new epidemiology of celiac disease.
J Pediat Gastroent Nutr 2014; 59:S7–9.
3. Altobelli E, Paduano R, Di Orilo F. Burden of celiac disease in Europe: a review of its childhood and adulthood prevalence and incidence as of September 2014.
Ann Ig 2014; 26:485–498.
4. Lebwohl B, Sanders DS, Green PHR. Coeliac disease.
Lancet 2018; 391:70–81.
5. Laass MW, Schmitz R, Uhlig HH, et al. The prevalence of celiac disease in children and adolescents in Germany.
Dtsch Arztebl Int 2015; 112:553–560.
6. Fasano A. Clinical presentation of celiac disease in the pediatric population.
Gastroenterology 2005; 128: (4 Suppl 1): S68–S73.
7. Rampertab DS, Pooran N, Brar P, et al. Trends in the presentation of celiac disease.
Am J Med 2006; 4:355.e19–355.e14.
8. Ravikumara M, Tuthill DP, Jenkins HR. The changing clinical presentation of coeliac disease.
Arch Dis Child 2006; 91:969–971.
9. Parzanese I, Qehajaj D, Patrinicola F, et al. Celiac disease: From pathophysiology to treatment.
World J Gastrointest Pathophysiol 2017; 8:27–38.
10. Dubé C, Rostom A, Sy R, et al. The prevalence of celiac disease in average-risk and at-risk Western European populations: a systematic review.
Gastroenterology 2005; 128:57–67.
11. Ludvigsson JF, Card TR, Kaukinen K, et al. Screening for celiac disease in the general population and in high-risk groups.
United Eur Gastroenterol J 2015; 3:106–120.
12. Al-Toma A, Volta U, Auricchio R, et al. European Society for the Study of Coeliac Disease (ESsCD) guideline for coeliac disease and other gluten-related disorders.
United European Gastroenterol J 2019; 7:583–613.
13. Husby S, Koletzko S, Korponay-Szabo IR, et al. ESPGHAN Working Group on Coeliac Disease Diagnosis, ESPGHAN Gastroenterology Committee, European Society for Pediatric Gastroenterology, Hepatology, and NutritionEuropean Society for Pediatric Gastroenterology, Hepatology, and Nutrition Guidelines for the Diagnosis of Coeliac Disease.
J Pediat Gastroent Nutr 2012; 54:136–160.
14. Theethira TG, Dennis M. Celiac disease and the gluten-free diet: consequences and recommendations for improvement.
Dig Dis 2015; 33:175–182.
15. McAllister BP, Williams E, Clarke K. A comprehensive review of celiac disease/gluten-sensitive enteropathies.
Clinic Rev Allerg Immunol 2019; 57:226–243.
16. Valitutti F, Trovato CM, Monturi M, et al. Pediatric celiac disease: follow-up in the spotlight.
Adv Nutr 2017; 8:356–361.
17. Aaltonen K, Laurikka P, Huhtala H, et al. The long-term consumption of oats in celiac disease
patients is safe: a large cross-sectional study.
Nutrients 2017; 9:611.
18. Riznik P, De Leo L, Dolinsek J, et al. Diagnostic delays in children with coeliac disease in the central European Region.
J Pediatr Gastroenterol Nutr 2019; 69:443–448.
19. Fuchs V, Kurppa K, Huhtala H, et al. Factors associated with long diagnostic delay in celiac disease.
Scand J Gastroenterol 2014; 49:1304–1310.
20. Gray AM, Papanicolas IN. Impact of symptoms on quality of life before and after diagnosis of coeliac disease: results from a UK population survey.
BMC Health Serv Res 2010; 10:1–7.
21. Green PHR, Stavropoulos SN, Panagi SG, et al. Characteristics of adult celiac disease in the USA: results of a national survey.
Am J Gastroenterol 2001; 96:126–131.
22. Navalón-Ramon E, Juan-García Y, Pinzón-Rivadeneira A. Prevalence and features of coeliac disease in the Mediterranean area of Spain.
Semergen 2016; 42:514–522.
23. Norström F, Lindholm L, Sandström O, et al. Delay to celiac disease diagnosis and its implications for health-related quality of life.
BMC Gastroenterol 2011; 11:1–8.
24. Rashid M, Cranney A, Zarkadas M, et al. Celiac disease: evaluation of the diagnosis and dietary compliance in Canadian children.
Pediatrics 2005; 116:e754–e759.
25. Rodrigo-Sáez L, Fuentes-Álvarez D, Pérez-Martínez I, et al. Differences between pediatric and adult celiac disease.
Rev Esp Enferm Dig 2011; 103:238–244.
26. Vavricka SR, Vadasz N, Stotz M, et al. Celiac disease diagnosis still significantly delayed - doctor's but not
patients’ delay responsive for the increased total delay in women.
Dig Liver Dis 2016; 48:1148–1154.
27. Pulido O, Zarkadas M, Dubois S, et al. Clinical features and symptom recovery on a gluten-free diet in Canadian adults with celiac disease.
Can J Gastroenterol 2013; 27:449–453.
28. Biagi F, Schiepatti A, Maiorano G, et al. Risk of complications in coeliac
patients depends on age at diagnosis and type of clinical presentation.
Dig Liver Dis 2017; 50:549–552.
29. Goddard CJR, Gillett HR. Complications of coeliac disease: are all
patients at risk?
Postgrad Med J 2006; 82:705–712.
30. Walker MM, Ludvigsson JF, Sanders DS. Coeliac disease: review of diagnosis and management.
Med J Aust 2017; 207:173–178.
31. Assiri AM, Saeed A, Saeed E, et al. Assessment of knowledge of celiac disease among health care professionals.
Saudi Med J 2015; 36:751–753.
32. Barzegar F, Rostami-Nejad M, Rostami K, et al. Lack of health care professional's awareness for management of celiac disease may contribute to the under diagnosis of celiac disease.
Gastroenterol Hepatol Bed Bench 2019; 12:203–208.
33. Jinga M, Popp A, Balaban D, et al. Physicians’ attitude and perception regarding celiac disease: a questionnaire-based study.
Turk J Gastroenterol 2018; 29:419–426.
34. Ress K, Harro M, Maaroos H, et al. High prevalence of coeliac disease: need for increasing awareness among physicians.
Dig Liver Dis 2007; 39:136–139.
35. Shergill S, Makharia GK. Awareness about celiac disease amongst physicians.
Indian J Gastroenterol 2017; 36:327–329.
36. Zipser RD, Farid M, Baisch D, et al. Physician awareness of celiac disease.
J Gen Intern Med 2005; 20:644–645.
37. Malik I, Kumar K, Hussain H, et al. Celiac disease: what the Indian pediatricians know about the disease.
Indian J Gastroenterol 2019; 38:263–267.
38. Paul S, Adams H, Basude D. CollaboratorsInterpretation and implementation of the revised European Society for Paediatric Gastroenterology Hepatology and Nutrition (ESPGHAN) guidelines on pediatric celiac disease amongst consultant general pediatricians in Southwest of England.
Indian J Gastroenterol 2019; 38:203–210.
39. Riznik P, Balogh M, Bódi P, et al. The use of biopsy and “no-biopsy” approach for diagnosing paediatric coeliac disease in the Central European Region.
Gastroenterol Res Pract 2019; 2019:9370397.
40. Jackson P, Glasgow J, Thom R. Parents’ understanding of coeliac disease and diet.
Arch Dis Child 1985; 60:672–674.
41. Tomlin J, Slater H, Muganthan T, et al. Parental knowledge of coeliac disease.
Inform Health Soc Care 2015; 40:240–253.
42. Paganizza S, Zanotti R, DʼOdorico A, et al. Is adherence to a gluten-free diet by adult
patients with celiac disease influenced by their knowledge of the gluten content of foods?
Gastroenterol Nurs 2019; 42:55–64.
43. Garg A, Gupta R. Predictors of compliance to gluten-free diet in children with celiac disease.
Int Sch Res Notices 2014; 2014:248402.
44. Silvester J, Weiten D, Graff L, et al. Living gluten-free: adherence, knowledge, lifestyle adaptations and feelings towards a gluten-free diet.
J Hum Nutr Diet 2016; 29:374–382.
45. Barzegar F, Rostami-Nejad M, Mohaghegh Shalmani H, et al. The effect of education on the knowledge of
patients with celiac disease.
Gastroenterol Hepatol Bed Bench 2017; 10:15–19.
46. Connan V, Marcon M, Mahmud F, et al. Online education for gluten-free diet teaching: development and usability testing of an e-learning module for children with concurrent celiac disease and type 1 diabetes.
Pediatr Diabetes 2019; 20:293–303.
