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Inflammatory bowel disease: An evaluation of health information on the internet

AIM To evaluate the quality and accuracy of websites written to the public on inflammatory bowel disease (IBD) (Crohn's disease and ulcerative colitis) and assess their readability level. METHODS Google™, Bing™, and Yahoo™ search engines were searched independently by three researchers in December 2014. Only English-language websites were selected on the basis of predetermined inclusion and exclusion criteria. Researchers independently evaluated the quality of each website by using the DISCERN and the HONcode instruments. The readability levels were calculated using two formulas; the Flesch-Kincaid Grade Level Index, and the Coleman-Liau Readability Index. The agreement between the evaluators was calculated using Cohen kappa coefficient. RESULTS Eighty-four websites were finally identified. Scores varied from a minimum DISCERN score of 18 to a maximum of 68 [mean ± SD, 42.2 ± 10.7; median = 41.5, interquartile range, interquartile range (IQR) = 15.8] and a minimum score of HONcode of 0.14 and a maximum of 0.95 (mean ± SD, 0.16 ± 0.19; median = 0.45, IQR = 0.29). Most of these websites were reviewed in 2014 and 2015 (n = 51). The creators of these websites were: universities and research centers (n = 25, 30%), foundations and associations (n = 15, 18%), commercial and pharmaceutical companies (n = 25, 30%), charities and volunteer work (n = 9, 10%), and non-university educational bodies (n = 10, 12%). The Flesch-Kincaid Grade Level readability score (mean ± SD) was 11.9 ± 2.4 and the Coleman-Liau Readability Index score was 12.6 ± 1.5. Significant correlation was found between the two readability scores (R2 = 0.509, P = 0.001). The overall agreement between evaluators measured by Cohen kappa coefficient was in the range of 0.804-0.876; rated as "Good". CONCLUSION The DISCERN and the HONcode scores of websites varied and the readability levels of most websites were above the public readability level. The study highlights the areas that need further improvement and development in patient education online materials about IBD.


INTRODUCTION
Inflammatory bowel disease (IBD) refers to two chronic inflammatory disorders, Crohn's disease and ulcerative colitis. Both are life long, relapsing disorders of unknown etiology; possibly the result of interaction between genetic and environmental factors [1] . The diagnosis of these disorders is based on clinical features, endoscopy, and histological changes [2] . Crohn's disease may affect any part of the gastrointestinal tract but most commonly affects the distal ileum and proximal colon. The disease is characterized by inflammatory changes involving all the layers of the affected regions. In contrast, ulcerative colitis is characterized by continuous ulceration starting in the rectum and limited to the colonic mucosa [3] . IBD occurs worldwide with the highest incidence in developed countries mainly North America, United Kingdom and northern Europe. The incidence of ulcerative colitis in North America is approximately 19.5 per 100000 person years and 243 per 100000 person years in Europe while the incidence of Crohn's disease in North America is approximately 20.2 per 100000 person years and 12.7 per 100000 person years in Europe [4] . The aims of treatment are to induce remission in active disease and to maintain remission/prevent relapse. Therapeutic modalities include lifestyle modification, nutritional support, and medications. Surgery is reserved for the treatment of complications or when the medical therapy is ineffective. In addition to other complications, patients with IBD are at a higher risk of developing colorectal cancer. Therefore, patients have to undergo to regular checkup for early detection of the development of colon cancer [5] .
With this information in mind, patients with IBD, as it is the case with other chronic diseases, usually seek information about the nature of the disease, its causes, investigations needed to diagnose the disease and therapeutic options. The advances in treatment modalities and options, and the increasing desire for patients to participate in decision-making about treatment choices necessitate the need for resources to support these decisions. Nowadays, patients have increasingly used the Internet as a source of health information because of its global accessibility, speed, and cost effectiveness [6] . Approximately 80% of the Internet users look for medical or health-related information through the Internet [7] . The topics most searched were information about specific disease or medical condition, treatment options, diet and nutrition, exercise and fitness and medications [7] . The increasing use of the Internet embraces a variety of aspects of topics searched, which gives the person an opportunity to investigate their questions from several resources. However, with the abundance of such information there is concern about the quality, accuracy, and readability level of the information available on the Internet about health care [8] . Therefore, the aims of this study were: to evaluate the quality, and accuracy of web-based information about IBD using two instruments, the DISCERN and the HONcode, as well as calculate the readability level by using two formulas, the Flesch-Kincaid Grade Level Index, and the Coleman-Liau Readability Index. The rationales for the study were to assess the educational usefulness of web-based information on IBD particularly their quality, accuracy and areas of deficiencies that need improvement. Also to assess whether these resources are easily read and understood by the public. Therefore our research questions are: (1) for the websites targeting the public and patients with IBD, what is the accuracy and the quality of these information resources? and (2) does the readability level of these online resources match with the recommended level for the public?

Search design
In this study we assessed websites written for patients and the public on IBD by searching three search engines (Google™, Bing™ and Yahoo™), the selection of these three search engines was based on current statistical information that showed that these engines are the most searched by the public for health information [9] . The quality and accuracy of information provided on websites were assessed using two instruments: the DISCERN (www.discern.org.uk) and HONcode (www.hon.ch/HONcode/) instrument. Details about these instruments and the justification for selecting them are discussed later. The readability of the websites was assessed using two methods: the Flesch-Kincaid Grade Readability Level and the Coleman-Liau Readability Index. After piloting the work and ensuring satisfactory use of these instruments by researchers, the work was carried out to assess the quality of websites. The Institutional Review Board, College of Medicine King Saud University, has approved the project and the approval number: F06/2014.

Searching the internet
Using the following key words: "inflammatory bowel disease", "Crohn's disease", "ulcerative colitis", "inflammatory bowel disease patient information", "Crohn's disease patient information", and "ulcerative colitis patient information", three search engines (Google™, Bing™ and Yahoo™) were searched. Researchers independently from 1 to 20 December 2014 conducted the search. Information for each website was recorded; these included: website title, website URL, name of creator, year of publication on the Internet, last date updated, and the objectives of the website. This information about each website was collected using the following online meter: http://whois.domaintools.com/. The data collected were evaluated on the bases of the inclusion and the exclusion criteria.

Inclusion and exclusion criteria
The inclusion criteria included: (1) websites covering public education about Crohn's disease, ulcerative colitis or IBD; and (2) websites focusing on patient education and in the English language. The excision criteria comprised: (1) websites addressing doctors or health professionals; (2) lectures, and advertisement on IBD; (3) websites in languages other than English; and (4) presentations at conferences.

Assessing accuracy and quality of information
Two instruments were used in assessing the quality and accuracy of information provided, namely the DISCERN instrument and the HONcode instrument. These two instruments have been widely used in the literature in assessing information on the Internet particularly health related issues and patients' education online resources [8,[10][11][12] . More details about these two instruments can be summarized as follows: DISCERN instrument: This instrument is a standardized set of criteria for judging the quality of health information and is written for the public to assess treatment options [8,[10][11][12] . The DISCERN instrument was created by the University of Oxford, and the project was funded by the British Library and the National Health Service (NHS) Research & Development Programme [13] The instrument consists of 15 questions plus an overall quality rating question. The questions can be grouped under the three key topics as follows: Questions 1 to 8 addressing reliability, Questions 9 to 15 addressing specific detail about the information provided and treatment choices, and Q16 covering the overall quality rating [14] . The instrument has been used to assess healthcare-related websites and online resources. For example, the quality of patients' information on surgical treatment of haemorrhoids [12] , and colorectal cancer information [11] .
HONcode instrument: The Health on the Net (HON) Foundation, a non-profit, and non-government organization created this instrument in 1995. The instrument focuses on key questions on the provision of health information available on the Net, and provides a code of conduct addressing eight principles: (1) authoritative (indicates the qualifications of the authors); (2) complementarity (Information should support, not replace, the doctor-patient relationship); (3) privacy (Respect the privacy and confidentiality of personal data submitted to the site by the visitor); (4) attribution [cite the source(s) of published information, date medical and health pages]; (5) justifiability (site must back up claims relating to benefits and performance); (6) transparency (Accessible presentation, accurate email contact); (7) financial disclosure (Identify funding sources); and (8) advertising policy (Clearly distinguish advertising from editorial content) [15][16][17] . To earn HONcode certification, a website must conform to the eight principles of the HONcode of Conduct. An HONcode expert then assesses the candidate website using precise guidelines for each principle. Recently, the HON Foundation has developed an automated system to assist in detecting a website's HONcode conformity. Therefore, the automated assistance in conducting HONcode reviews can expedite the current time-consuming tasks of HONcode certification and ongoing surveillance. A recent study showed that there is concordance between automated and expert manual compliance detection for the criteria [18] . In this research we have used the electronic system available at: http://www.readabilityformulas.com/free-readabilityformula-tests.php.
The HONcode has been widely used in the literature in assessing health-related websites [19] . The two instruments, the DISCERN and HONcode, do not exactly cover the same issues/topics, although there are some overlaps. Therefore, using these two instruments with these differences in mind could provide a better evaluation of the websites.

Piloting the study
The aims of piloting the study were: (1) to introduce the two instruments to the researchers and orient them on how to use each instrument in assessing the websites; and (2) identify difficulties facing the researchers on applying the two instruments and the sources of disagreements among them. Such exercise prior to the implementation of the two instruments was vital for ensuring optimal use of the instruments and maximizing the degree of agreement among evaluators when they apply these two instruments in the actual research. The piloting part was conducted as follows: (1) approximately 10 websites other than those identified for the research study were evaluated independently by three researchers using the two instruments; (2) the results of their evaluation were discussed with the aim to identify sources for difficulties/disagreements; (3) the identified differences were resolved after discussing them reaching to a solution; and (4) the same process was repeated on another 10 websites until the agreement between the researchers reached to an optimal level [20] .

Conduction of the study
Along with the same approach described under piloting the study, the researchers evaluated the websites identified by applying the two instruments on each website and giving a score. The process was conducted by each researcher independently first by applying the DISCERN instrument then the HONcode instrument. The results of the assessment were placed on an Excel sheet for each researcher. The degree of agreement was measured using Cohen kappa coefficient [21] .

Calculating website readability
The aims of calculating readability level of websites was to assess if they were written at the readability level of the general public and patients; should not exceed the 6 th grade readability level [22,23] . Two methods were used to calculate readability: The Flesch-Kincaid Grade Level Index [24] , and the Coleman-Liau Readability Index [25,26] . It was decided to use these two methods rather than one method so that we can compare the readability scores and examine if there were an agreement between the two methods, and hence strengthening the outcomes of our readability assessment and our conclusions. The two methods can be summarized as follows: Flesch-Kincaid grade level index: This test helps in indicating how difficult a reading passage in the English language to understand. The test was developed by Rudolf Flesch and finalized by J Peter Kincaid for use by 1679 March 7, 2017|Volume 23|Issue 9| WJG|www.wjgnet.com the United States Navy, hence the name of the test [24] . The test is based on the word length and the sentence length and is based on the following formula: 0.39 × [(total words)/(total sentences)] + 11.8 × [(total syllables)/(total words)] - 15.59 This method has been widely used in assessing the readability of websites and educational material [27] . Coleman-Liau readability index: This test differs from the above method in relying on characters instead of syllables per word. It enables the users however to grade the readability level. It has been widely used in assessing the readability of educational material [27] . We used a free online calculator (www.readabilityformulas.com) to calculate the readability level using the two readability methods. As per instructions provided by the website, the top, middle and bottom 150-200 words of each website were placed in the calculator and then the text readability was checked by calculating the number of sentences, words, syllables, and characters in the sample. A sufficient sample size of four to five full sentences; approximately 200-500 words in total were used. The scores recorded for each website were placed on an Excel sheet and reviewed by two other researchers before conducting final analysis for the means and standard deviations.

Grouping the websites under five categories
Assessment of the identified websites revealed variability in their creators. These can be grouped into 5 categories: (1) university, affiliated hospitals, and research centres; (2) foundations and associations; (3) commercial and pharmaceutical companies; (4) charities and volunteer works; and (5) non-university educational bodies such as colleges, academies, and councils. The grouping of websites under these five categories was carried out by researchers independently and was reviewed in a meeting for any disagreements.

Statistical analysis
The collected data were placed on an Excel Sheet (Microsoft Excel for Mac 2011, Microsoft Corporation, Redmond, WA, United States). All analysis was conducted by using SPSS software (SPSS Statistics version 22 for Mac, IBM Corporation, Armonk, NY, United States). For the data collected from measuring website accuracy, and the readability scores, the means, standard deviations, the median and interquartile range (IQR) were calculated. Pearson correlation studies and P-values for significance were calculated to examine if there were correlations between the scores obtained from the two readability methods [28] . A P-value of < 0.05 was considered significant. The agreement between the evaluators measured by the degree of inter-rater agreement using Cohen kappa coefficient was also carried out using SPSS software. This has been interpreted as "Poor", if the results in the range: 0.21-0.40; "Fair" 0.41-0.60; "Moderate" 0.61-0.80; "Good" 0.81-1.00.

General information about websites
The search of the three databases, Google™, Bing™ and Yahoo™, resulted in the identification of 300 websites. After the duplicates were removed we ended with 210 websites. On applying the inclusion and exclusion criteria, 84 websites were finally identified and included in the study (Figure 1). Table 1 summarizes the general information about the 84 websites, including: website title, URL, author/ownership, year created, last updated, number of pages, number of tables, images and illustrations. The oldest two websites were created by the Of the 84 websites, 60 websites comprised 1-5 pages, 16 websites had 6-10 pages, 8 had more than 11 pages. The website titled Crohn's disease by the University of Maryland medical center had the highest number of pages, 20 pages. The number of tables varied from zero to 6. Out of the 84 websites only 24 websites used tables to explain their content. The total number of tables in these websites was 55. The number of images varied from zero to 27. Out of the 84 websites only 42 websites had images to explain the content. The total number of images in these websites was 141. Again the number of illustrations varied from zero to 10. Out of the 84 websites, only 28 had illustrations to explain the content. The total number of illustrations was 53.

DISCERN and the HONcode scores of websites
In order to calculate the accuracy of the websites, we used two instruments, the DISCERN and the HONcode instruments.      It is interesting to note that the website, Crohn's Disease, the National Institute of Diabetes and Digestive and Kidney Diseases was ranked number one as per the two instruments. Seven websites in total were among the top ten websites as per both the DISCERN and the HONcode scores. Nine out of the ten websites were created in United State. Table 3 summarizes the grouping of the 84 websites under five categories on the basis of the website creators. Universities and research centers created 25 (%), professional foundations and associations created 15 (%), commercial and pharmaceutical companies created 25 (%), charities and volunteers contributed to 9 (%), non-university educational bodies such as colleges, academies, councils, WebMed contributed to 10 (%). Further analysis revealed that there was no significant differences in the DISCERN scores between the groups (P = 0.472) but the HONcode scores were different (P = 0.041). Examples of content deficiencies or scientific content inaccuracies and suggestions for improvement are shown on Table 4. Table 2 summarizes the readability scores calculated by using two methods, the Flesch-Kincaid Grade Level Index and Coleman-Liau Readability Index. The minimum score for the Flesch-Kincaid Grade Level Index was 6.7 for the website Crohn's Disease Symptoms and Treatment, United States news Wellness, while the maximum score was 20.3 for the website Crohn's Disease, UPMC Life Changing Medicine. Out of the 84 websites, 28 received a mean of 6.7 to 10.9, fortysix received a mean of 11.0 to 14.5, and ten websites received a mean of 15.7 to 20.3. The overall mean score for the 84 websites was 11.9 ± 2.4. For the Coleman-Liau Readability Index the minimum score was 9.0 for the website Crohn's Disease, Bupa, while the maximum score was 16 for the website Inflammatory Bowel Disease, Fact Sheet, Womenshealth. Out of the 84 websites, eleven received a mean score of 9.0 to 10.9, thirty-nine received a score of 11.0 to 12.7, and thirty-four received a score of 13.0 to 16.0. The overall mean score for the 84 websites was 12.6 ± 1.5.

Readability level of websites
Significant correlation was found between the Flesch-Kincaid Grade Level index scores and the Coleman-Liau Index scores (R² = 0.509, P < 0.001) ( Figure 2). Table 5 summarizes the inter-rater agreement between evaluators for the DISCERN instrument items. The overall Cohen kappa scores were in the range of 0.804-0.876.

DIsCUssION
Several studies pointed to continuous progress from paper to electronic and online-based patient education [29,30] . The aims of the study were to evaluate the quality and accuracy of information available on IBD websites and calculate the readability level using two methods. To maximize the yield of the search, we searched three search engines commonly used by the public seeking information related to healthcare. The study showed that the 84 websites identified were created by universities, affiliated hospitals and research centers, professional foundations and associations, commercial and pharmaceutical companies created, charities and volunteers, as well as non-university educational bodies (such as colleges, academies, councils, and WebMed). The involvement of universities, affiliated hospitals, and research centers is directed at health information exchange as well as public and patient education with the aim to improve the quality of care, engage the patient in the decisionmaking processes and the journey of treatment as well as enhance patient's awareness about the nature of their illness. Such educational approaches while having multiple impacts on the patients' healthcare; it can also help in reducing the costs of treatment [31] . The current move from paper-based to online health care education may be related to the progressive increases in the use of the Internet by the public and patients [32] . Furthermore, Morgan et al [33] showed that patients with genetic and chronic diseases have great interest 1691 March 7, 2017|Volume 23|Issue 9| WJG|www.wjgnet.com Nothing is mentioned about treatment of Crohn's disease. Symptoms may include abdominal pain, typically in the right lower quadrant, diarrhoea, some blood may be present in stools, fatigue. In more severe disease fever, and weight loss may be present. Some patients may have nausea, and abdominal distention together with abdominal pain.
It is worth to mention that Crohn's disease is a lifelong illness (chronic disease). People who have Crohn's will experience periods of flare-ups, when their symptoms are active, and other times when their symptoms go into remission.
Up to 30% of patients may have changes in the area around the anus including anal fistulas (internal tracts connecting the anal lumen with the skin around the anus), abscess, skin tags, and anal fissures. About 10%-20% of patients also have joint pains, lower back pain, skin rash known as erythema nodosum, and eye changes. (images showing some of these changes will enhance this part). A section discussing investigations should be added. In addition to detailed medical history, the treating doctor will initiate the evaluation by testing for infectious conditions that can cause inflammation of the colon, screen for endocrine-metabolic disorders such as excessive activity of the thyroid gland. Therefore biochemical tests and stool tests are needed.
Endoscopic evaluation (colonoscopy) should be carried out in patients who have symptoms suggestive of inflammatory bowel disease and no evidence for an infection to explain symptoms. Small bowel images, computed tomography (CT) enterography may also be needed.
Nutritional changes, medical and surgical treatment should be briefly discussed. in participating in clinical studies and a desire to understand information discussed during reviewing their healthcare provider. These patients may have more questions after they leave the doctor's clinic and usually tend to search the Internet for answers [33] . Compared to paper-based health education, the Internet appears to provide a wider range of answers and options. However, the quality of information provided and the readability level remain as areas of concern [8,34] .  As per this study, the DISCERN and the HONcode scores varied. However, no significant differences in the DISCERN scores were found between the groups but when the groups were compared on the basis of the HONcode scores, the difference was significant. A weak correlation was found between the DISCERN scores and the HONcode scores (R 2 = 0.217). The results are consistent with the variability of the DISCERN scores of websites in each group and the fact that the two instruments are not measuring the same characteristics [25] . Interestingly, seven out of the top 10 websites on IBD scored higher on both the DISCERN and the HONcode scales. Looking into the readability levels of these seven websites, the readability using the Flesch-Kincaid Grade level was in the range 11 to 15, while for the Coleman-Liau Readability Index the range was 12 to 15. This indicates that even the top 7 websites had a readability level not adjusted to the public level.
Out of the 84 websites, only 17 displayed the HONcode certificate. A recent study found that only three websites out of 78 showed HONcode certificates [35] . Although the number of websites granted a HONcode certificate is small yet there is no correlation between the calculated HONcode scores and having a certificate on the website. Absence of the HONcode certificate from a website doesn't necessarily indicate poor quality of the website. This is because the process of issuing the HONcode is based on a voluntary application for the certificate. Therefore, it is possible that the owners/authority responsible for these websites did not apply for the HONcode certificate.
The readability scores were calculated by using two methods, the Flesch-Kincaid Grade Level Index and Coleman-Liau Readability Index. The moderate correlation between the Flesch-Kincaid Grade Level index scores and the Coleman-Liau Index scores is consistent with other work [20] and indicates that the results from the two calculations are consistent. The findings show that the majority of the studies had a readability level equivalent to year 11 and 12. However, the national reading grade level average has been estimated to be about the 6 th -grade [36] and the general agreement is that the reading level for patient information materials should not exceed this level and be no less than what a 4 th -grade is capable of reading [37] . With these findings in mind, there is a need for editing the content of most websites identified and adjusting the reading levels to meet the recommended reading levels for the public.
This study has a number of strengths; first, we searched three different search engines commonly used by the public seeking health-related information with the aim to maximize the yield of the search. Second, we used two instruments the DISCERN and the HONcode to measure the accuracy of contents. Both instruments have been widely used in assessing online health information material. Third, three evaluators independently conducted the evaluation and the inter-rater agreement among the assessors was within the accepted limits. Finally, the readability was measured by using two different methods. However, this study is not without limitations; the study is just a representation of websites identified at the time of the search. Only websites in the English language were included, and there is the possibility that there are other websites in other languages that match with our inclusion criteria and were not included. A multinational study may be needed to identify any differences if any and resolve gaps in this area. Therefore, despite all efforts and the plans considered, we may have missed some websites.
The results of this study may be of value to general practitioners, physicians, gastroenterologists, nurses, and allied health professionals, the public and medical students interested in online education material on IBD. The top 10 websites with the highest DISCERN and the HONcode scores identified from this study provide examples of educationally useful websites that can be recommended by treating physicians to their patients. However, their readability level was above the recommended level for the public and they may be suitable for educated patients only.

Future directions
This study highlights a number of future directions in research in the area of Internet-based patient education particularly patients with IBD. These can be summarized as follows: First, planning for creating online educational material for the public and patients with IBD necessitates more care for innovation, content accuracy and readability level to match the recommended needs of the public. Second, more work is needed to enhance the use of images, illustrations, and videos in improving the educational usefulness of websites on IBD and engage the patients and the public using such online resources. The use of these educational tools should aim at explaining difficult concepts, and enhancing understanding of the message given. As shown from this study the use of these educational tools was deficient in most websites. Third, future research should aim at assessing the impact of using Internet education and health literacy in patients with IBD and whether such resources have made impacts on number of hospital admissions, costs associated with poor health literacy, effective health education techniques, and how poor health literacy influences management outcome in these patients.
In conclusion, health literacy about IBD and the use of Internet as a medium for education appears to be increasing. Universities, research centers, commercial and pharmaceutical companies, professional foundations and associations were the major contributors to online resources written for the public and patients. Several deficiencies in the content were observed and most websites failed to meet the recommendations set by the National Institute of Health and American Medical Association that patients resources should be written about the 6 th -grade level. Effective use of diagrams, illustrations, videos, and tables to explain difficult concepts should be encouraged. Revising the websites and resolving the gap between the readability of written health information and the literacy skills of the public will improve the purpose of these websites and make them a useful healthcare resource to patients with IBD.

aCKNOwLeDGMeNTs
The authors would like to thank Dr. Sarah Azer of Box Hill hospital for her kind review of the manuscript.

Background
Patients with inflammatory bowel disease (IBD), as it is the case with other chronic diseases, seek information about the nature of their disease. The increasing use of the Internet embraces the significance of online resources educating patients and the public.

Research frontiers
With the abundance of information there is concern about the quality, accuracy and readability level of information available on the web, thus it might be useful to assess the quality of these resources, identify specific deficiencies and examine whether these websites meet the recommendations of national bodies.

Innovations and breakthrough
The goal of this paper is to use comprehensive analysis to assess the quality of websites, accuracy of content and readability levels of websites on IBD dedicated to patients and the public.

Applications
The study highlights a number of future directions in the area of Internetbased patient education particularly patients with IBD and raises the need for improving such resources particularly in relation to specific areas identified in the study.

Terminology
Scientific accuracy and quality of content were evaluated using two standardised instruments widely used in research. The readability level was calculated on the bases of word length, sentence length and syllables.

Peer-review
This paper is an interesting evaluation of quality, accuracy, and readability of websites dedicated to the public. It is a novelty and represents a beginning point for judging and improving websites dedicated to IBD.