Content, quality, and readability of website information on dental care for patients with cancer

Content, quality, and readability of website information on dental care for patients with cancer

Accepted Manuscript Content, Quality, and Readability of Website Information on Dental Care for Cancer Patients L.L. Patton, S.F. George, R.P. Hollowe...

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Accepted Manuscript Content, Quality, and Readability of Website Information on Dental Care for Cancer Patients L.L. Patton, S.F. George, R.P. Hollowell PII:

S2212-4403(14)00419-2

DOI:

10.1016/j.oooo.2014.03.019

Reference:

OOOO 894

To appear in:

Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology

Received Date: 26 January 2014 Revised Date:

12 March 2014

Accepted Date: 22 March 2014

Please cite this article as: Patton L, George S, Hollowell Jr. R, Content, Quality, and Readability of Website Information on Dental Care for Cancer Patients, Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology (2014), doi: 10.1016/j.oooo.2014.03.019. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Content, Quality, and Readability of Website Information on Dental Care for Cancer Patients

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Patton LL, George SF, Hollowell Jr. RP.

Dr. Lauren L. Patton is Professor, Chair and Director of the General Practice Residency

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Program, Department of Dental Ecology, UNC School of Dentistry Chapel Hill, NC. Dr.

Stephanie F. George is Second year Chief Resident, General Practice Residency, Department of

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Dental Ecology, NC School of Dentistry, Chapel Hill, NC. Dr. Robert P. Hollowell Jr., is Adjunct Professor, Department of Dental Ecology, UNC School of Dentistry and Clinic and General Practice Residency Director, Department of Dentistry, Carolinas Medical Center,

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Charlotte, NC.

Correspondence: Lauren L. Patton, DDS Professor and Chair, Department of Dental Ecology,

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School of Dentistry, University of North Carolina, CB 7450, Chapel Hill, NC, 27599-7450, USA Tel: + (919) 537 3582, Fax: +(919)537 3586; Email: [email protected]

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Key Words: internet, cancer, oral health, oral complications, health education, health literacy

There are no disclosures.

Accepted as Oral Presentation Abstract for 2014 American Association of Dental Research meeting. Word count abstract=150; Word count complete manuscript=3900; 2 figures; 3 tables; 35 references; no supplementary elements.

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Abstract: Objective: This study assessed content, quality and readability of patient-directed internet

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materials about dental care support and oral toxicities/complications of cancer therapy.

Study Design: 32 websites meeting inclusion criteria from a Google search using terms

“cancer>dental>care” were categorized for parameters of content, JAMA benchmarks for

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website quality, display of Health on the Net (HON) seal, and Flesch Reading Ease Score

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(FRES).

Results: Treatment modalities included radiation therapy, chemotherapy, stem cell transplantation, and surgery. Dental care was discussed before, during, and/or after cancer treatment. The most common oral toxicities/complications discussed were xerostomia, rampant

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caries, and mucositis. Only 1 site met all 4 JAMA benchmarks; 2 displayed the HON seal; only 9% were written at the 9th grade and none at the 6th to 7th grade FRES reading level.

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Conclusion: Websites addressing dental care for cancer patients are broad in content, yet limited

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in quality and are written at difficult reading levels.

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Introduction:

Treatment of head and neck cancers, other mucosal and solid organ tumors, and hematologic

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malignancies often has implications for oral health. Oral toxicities and/or complications can occur as a result of surgery and radiation therapy for head and neck cancers, chemotherapy, or hematopoetic stem cell transplantation (HSCT).1 Common toxicities and/or complications of

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cancer treatment include mucositis, pain, dysphagia, limited jaw opening and trismus, salivary dysfunction and xerostomia, acute exacerbation of chronic dental and periodontal infections,

and speech and masticatory dysfunction.1

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mucosal candidal and herpetic infections, neurosensory deficits, bone and soft tissue necrosis,

It is estimated that in the United States (U.S.) as of January 1, 2012, there were over 250,000 oral

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cavity and pharynx cancer survivors (185,240 men and approximately 93,000 women).2 Due to the permanent morbidity of surgery and radiation therapy to the head and neck region, preventive dental care is important for patients with oral cavity and pharynx cancers who are at high risk for

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late complications, such as xerostomia, radiation caries, and trismus. Additionally in 2012, 40,250 new oral cavity and pharynx cancer diagnoses were estimated in the U.S.,2 providing

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ample opportunity for patients to experience acute cancer treatment toxicities, such as mucositis. Advances in HSCT for hematologic malignancies have led to increasing survivorship and susceptibility to late complications such as xerostomia, dental caries, secondary oropharyngeal squamous cell carcinomas and oral mucosal effects of graft versus host disease (GVHD).3

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Patient education and communication with members of the dental and medical cancer care team can prepare the patient before, during and after cancer treatment to prevent and manage acute toxicities and adverse sequelae of treatment and ultimately lead to improved patient health

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outcomes, quality of life, and patient satisfaction. While interpersonal communication is

considered by many patients and professionals to be a preferred technique for patient education, healthcare providers use multiple communication techniques, with 20% of pediatric dentists and

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information for supplemental patient education.4

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15% of general dentists in Maryland in 2010 referring patients to the internet or other sources of

Patients themselves are seeking health information directly on the web. The Pew Research Center’s Internet and American Life Project’s investigation conducted in 2012 of American’s online health information seeking behaviors reported that 81% of U.S. adults use the internet;

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72% of internet users say they have looked online for health information of one kind or another in the past year; and 77% of the online health seekers say they began at a search engine such as Google, Bing, or Yahoo, with another 13% saying they began at a specific health information

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site such as WebMD.5 Online health information consumers were looking on their own behalf 39% of the time, 39% of the time on behalf of someone else, and 15% of the time on both their

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own and someone else’s behalf.5 These patients, or their caregivers, are health consumers who participate fully in their medical care by gathering information using electronic communication tools such as the internet. In a study in 2002, 31% of patients with head and neck cancer at a Toronto, Canada comprehensive cancer center reported they had already been e-health users and one of their two primary desired uses of the computer was to learn about side effects of treatment.6 This trend will increase in the future and a patient’s ability to effectively use internet

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health information will depend in part on the manner in which the educational materials are presented (quality), the patient’s or caregiver’s ability to locate information (availability), and

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their ability to effectively comprehend and make use of the information (usability).7

It is important for dental providers caring for patients with cancer to be aware of the cancerrelated oral health information available on the internet, so they can guide their patients toward

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higher quality internet resources, thus allowing them to become better educated healthcare

consumers. Thus this study aimed to determine the type, breadth, quality and readability of

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patient-directed materials on the internet available to educate about oral toxicities and/or complications of cancer therapy and to support oral health throughout cancer care.

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Methods:

A search using terms “cancer>dental>care” in the Google search engine was conducted on September 23, 2013. The first 50 websites were evaluated for patient education materials. All

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links were active. Sites were excluded if they were video only, password protected, scientific articles or books, or the content was not patient-focused or not relevant. After sites were

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excluded, 32 websites remained for further analysis. Assessment of exclusion criteria and website content and quality was conducted independently by 2 dentist reviewers with experience in managing dental care for cancer patients (LP and SG or LP and RH). Consensus was reached where discrepancy existed.

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Websites were categorized according to sponsorship or affiliation including: nonprofit organizations, university or medical centers, commercial or corporate sites, private medical and dental practices, and government sites. Websites were assessed for content. Cancer type

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discussed on the website page was categorized as head/neck, nonspecific, or other specific. Cancer treatment types included: radiation therapy, chemotherapy, HSCT, surgery, or

unspecified. Treatment toxicities and/or complications were categorized as: xerostomia,

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mucositis, radiation caries, osteoradionecrosis, bisphosphonate related osteonecrosis of the jaws (BRONJ), trismus, surgical defect, fungal disease, bacterial disease, viral disease, bleeding,

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neurotoxicity, functional disability (including eating, tasting speaking or swallowing), taste alteration, nutritional compromise, pain or other. Dental care timing discussed included: before, during, after, or unspecified. Oral care aspects discussed were categorizes as: oral hygiene, extractions, prophylaxis/cleaning, fluorides, saliva substitutes or stimulants, mucositis

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preventives/treatments, diet/nutrition, hyperbaric oxygen therapy, denture care, anti-infective rinses, and tooth remineralizing agents.

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Quality of websites was assessed with two tools. The Journal of the American Medical Association (JAMA) Benchmarks8 for quality of electronic content which has 4 core standards to

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be met: 1. Authorship: Authors and contributors, their affiliations and relevant credentials are provided; 2. Attribution: References and sources for all content should be clearly listed and copyright noted; 3. Disclosure: Website “ownership” is prominently and fully disclosed along with sponsorship, advertising, underwriting, commercial support and potential conflicts of interest; 4. Currency: Date the content was posted and updated is listed. Websites were assessed for a total score out of 4 points and attainment of the individual benchmark parameters. Website

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display of the Health on the Net (HON) seal was assessed. The HONcode certification,9 launched in 1995 by a nongovernmental organization, is an ethical standard with 8 principles aimed at offering quality health information on the internet. It is awarded to websites that comply with the

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code and thus demonstrates the intent of the website to publish transparent information that can be viewed as a reliable source of healthcare information on the internet.

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Websites were assessed for readability using the Flesch Reading Ease Score (FRES).10 The formula for the updated FRES is: Score = 206.835 – (1.015 x ASL) – (84.6 x ASW). Where:

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Score = position on a scale of 0 (difficult) to 100 (easy). ASL = average sentence length (the number of words divided by the number of sentences). ASW = average number of syllables per word (the number of syllables divided by the number of words).11 FRES scores of 0-30 are very difficult to read (College graduate estimated level), 30-50 are difficult to read (estimated 13th to

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16th grade level) and 50-60 are fairly difficult to read (estimated 10th -12th grade level). Scores of 60-70 are at the standard style and of reading level at the 8th to 9th grade level. Scores of 70-80 and 80-90 are fairly easy and easy to read, and estimated at the 7th grade and 6th grade level,

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respectively.11 For ease of analysis, website informational text content was placed in an online readability calculator tool for FRES analysis (http://www.online-

Results:

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utility.org/english/readability_test_and_improve.jsp).

The search yielded 37,300,000 hits. Of the first 50 websites, 18 met exclusion criteria for the following reasons: 12 had content not relevant to cancer, 2 had content not patient-education focused, 2 were scientific journal articles or books, 1 was a YouTube video patient story with no 7

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transcript, and 1 was password protected. Sponsorship or site hosting of the 32 included websites was as follows: 31% from non-profit organizations; 25% from university/medical centers; 22% from commercial or corporate sites, including media; 6% from private practices of which 3 were

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the same CAESY Patient Education System oral cancer module (Patterson Dental Supply, Inc., St. Paul, MN); and 6% from the U.S. government.

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The type of cancer(s), treatment modalities, and dental care timing around cancer treatment discussed on the website are shown in Table 1. Nonspecific cancers and head and neck cancers

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comprised the focus of patient education in the majority of sites. Radiation therapy (84%) and chemotherapy (78%) were the most commonly referenced. The majority discussed all 3 timing periods, before, during, and after treatment.

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Figure 1 shows the percentage of specific acute toxicities and late complications of cancer treatment covered by the sites. More than half of websites discussed cancer treatment toxicities and/or complications of xerostomia-84%, rampant/radiation caries-78%, mucositis-59%, pain-

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59%, and bacterial infections-56%. Figure 2 shows the aspects of dental care management covered in the website page. Half or more of websites discussed the need for pretreatment dental

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exam-72%, the importance of oral hygiene-59%, use of fluorides-50%, and use of saliva substitutes-50%.

Table 2 shows the website content assessed with the JAMA benchmarks criteria. Of note, only 1 site met all 4 JAMA benchmarks indicating the best quality, while the majority met only one or no criteria. The most commonly met benchmark was Disclosure. Only 2 sites displayed the

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HON seal; these were http://lymphoma.about.com/od/symptoms/a/Dental-Care-During-CancerTreatment.htm and http://www.everydayhealth.com/oral-head-and-neck-cancer/dental-care.aspx.

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Table 3 shows the average and range of FRES scores by site sponsorship group. Overall, the average FRES score was 43.03, with text considered to be difficult to read and requiring a high school education or greater. Only 3 sites (9%) were written at the 9th grade FRES reading level

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and none were at the recommended 6th -7th grade reading level. Among the sites, those with corporate/commercial and nonprofit sponsorship had higher average FRES scores, representing

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content written at lower reading levels than the university/medical center, private practice or government sites.

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Discussion:

These findings begin to show a picture of broad dental care information related to cancer treatment that is available to the public on the internet via the most widely used search engine in

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the U.S. It is encouraging that most websites discussed dental care timing before, during, and after cancer treatment and that topics covered the primary cancer treatment modalities. Most

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(83%) head and neck squamous cell carcinoma patients presenting for treatment at a U.S. comprehensive cancer center desired additional information, including topics such as how to stay healthy after treatment-75%, head and neck cancer and its treatment options- 54%, changes in swallowing and speaking following treatment- 52% and strategies for making eating and speaking easier- 46%.12 Delivery preferences varied with 25% wanting to receive information at multiple time points: 39% at diagnosis, 31% during treatment, 34% during the first 1-3 months

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following treatment, and 14% over 3 months after treatment.12 Information to support patient needs throughout the course of treatment was identified in this internet search study. Further, most patients preferred a delivery format (i.e., pamphlets, booklets, digital video disc, internet

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program) that could be viewed at the patient’s convenience, with the internet being the preferred mode of those listed.12

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Our use of a search engine for our study follows the internet search behavior of cancer patients. A study in St. Louis in 2007 found that 71% of patients who searched for cancer information

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primarily use a search engine as the tool of choice compared to only 13% who went directly to specific cancer-related websites (such as American Cancer Society 78%, WebMD 43%, National Cancer Institute 37%, People Living with Cancer 10%, and the American Society of Clinical Oncology 10%) alone and 14% used both search engines and specific websites.13

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While our study did not investigate patient or provider health education behaviors directly, studies have shown that cancer patients, and even more so their caregivers who are generally family members, prefer internet information to leaflets and booklets and are most interested in

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having their hospital doctor provide guidance to web resources.14 Only 8% of radiation oncology internet using patients in a Canadian study reported that they had received recommended web-

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links about their condition from the cancer team, yet 44% wished they had received recommendations, leading authors to conclude that lack of direction from their care team was the primary obstacle to transforming patients who wished to become e-patients, but had not independently searched for links.15

Providing cancer patients with a series of links to reliable healthcare websites written at the patient level of comprehension covering dental care topics (before, during and after cancer 10

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treatment) would be a time-efficient way of providing patients with supplementary health information that they can trust. Clinicians who provide reliable information, spare patients ineffective and sometime misleading web browsing. Consistent with findings of analyses of head

cancer patients with variable accuracy can be found on the web.

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and neck cancer information on the internet,16,17 a wide variety of dental care information for

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People receive health information from many different sources such as health professionals, friends and family, public and social media (in the forms of print, video, audio, and internet),

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schools and libraries, public and private sector organizations, product labels, and pamphlets. Varying sources of health information may present different, incomplete, biased, and possibly conflicting information forcing health information seekers to confront a complex and potentially overwhelming set of health messages. While technology as an essential tool for improving health

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literacy, internet based health education materials, including those targeting cancer patients, are often difficult to navigate and written at a reading level too high for most readers,18-21 as the average high school graduate typically reads at a 7th to 8th grade level and only 12% of U.S.

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adults have proficient health literacy.22 Aiming for the 6th to 7th grade reading level is

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recommended to make health education materials easy to read.23

Reading levels of patient education materials in this study were found to be set at a level too high for the average reader, consistent with studies involving print materials for oral cancer education24 and internet based patient education materials for dental and otolaryngology conditions and/or procedures such as dental implants;25 endodontic procedures;26 acoustic neuroma;20 facial fractures;27 and endoscopic sinus surgery.28 In contrast, a wide range of

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readability scores were obtained, equating to reading ages from 4th grade to university graduate level, with a mean reading age at the 8th to 9th grade level for family education materials

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regarding cleft lip and palate.29

In our study, web materials from all sponsors were written at higher educational levels than recommended, with government and university/medical center website materials being

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particularly difficult to read on average. This is consistent with studies of patient internet education materials from mid-Atlantic academic otolaryngology departments;30 major

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otolaryngology association websites;31 and the American Academy of Otolaryngology- Head and Neck Surgery Foundation.32 Patient education materials in 2012 from the otolaryngology specialty group, American Academy of Otolaryngology-Head and Neck Surgery, were reported

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to reflect a FRES score of 46,33 similar to our average of 43.

Beyond reading level, other elements impact the suitability of cancer education print and webbased materials, such as: content, literacy demand graphics, layout/typography, learning

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stimulation, and cultural appropriateness.21 In a comparison of English and Spanish language web sites with oral cancer information focusing on clinical presentation, etiology, and risk

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factors, the Spanish language sites were found to be of lower quality, possibly placing Hispanic patients at a disadvantage.34

There are several limitations of this study: The Google search was done on one day, and the dynamic nature of web searches with active use of search engine optimization tools means that the order of the top sites on search engine results pages can vary day to day, so the top 50 sites

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revealed on the date this web search was conducted will likely differ from the top 50 sites appearing on other days of the calendar year.35 Only websites in the English language were searched, prohibiting generalization to internet patient education materials written in other

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languages. Use of different search terms may lead to different results. The Google search

algorithm is updated periodically and updates may impact search results. In addition, industry websites often use a technique of search engine optimization to favorably position their website

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relative to others within search engines such as Google, making it more likely that the web searcher will find the industry site in the early hits. In this study, we did not search beyond the

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landing page identified by the search to other linked pages that might have added additional depth of information. This study took a simple search strategy that the authors believe would likely be the approach a patient would have taken to find information on this topic. Use of the FRES as a reading assessment tool is limited by its focus on word and sentence character length

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rather than use of common versus uncommon words. Our research design did not provide the opportunity to assess cancer patients’ internet health searching practices, reading levels, or health literacy. Also we did not compare site content for technical accuracy to gold standard literature,

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so the technical accuracy was not assessed.

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Given the increasing patient interest in web-based health information materials and the diversity of information available on the internet to support cancer patients with oral toxicities and/or complications, public and private creators of internet health-content need to constantly improve the readability of their materials and be accountable for the accuracy of the content. Professionals need to be diligent in searching for and recommending to their cancer patients

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web-materials that can promote and support positive oral health outcomes and improve oral

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health quality of life.

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2. Siegel R, DeSantis C, Virgo K, Stein K, Mariotto A, Smith T, et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin 2012;62:220-41.

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3. Majhail NS, Rizzo JD. Surviving the cure: long term followup of hematopoietic cell transplant recipients. Bone Marrow Transplant 2013;48:1145-51.

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4. Maybury C, Horowitz AM, Wang MQ, Kleinman DV. Use of communication techniques by Maryland dentists. J Am Dent Assoc 2013;144:1386-96.

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http://www.pewinternet.org/Reports/2013/Health-online.aspx (accessed 12/25/2013) 6. Lea J, Lockwood G, Ringash J. Survey of computer use for health topics by patients with head and neck cancer. Head Neck 2005;27:8-14.

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14. James N, Daniels H, Rahman R, McConkey C, Derry J, Young A. A study of information seeking by cancer patients and their carers. Clin Oncol (R Coll Radiol) 2007;19:356-62. 15. Katz JE, Roberge D, Coulombe G. The cancer patient's use and appreciation of the internet and other modern means of communication. Technol Cancer Res Treat 2013 Aug

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18. Misra P, Kasabwala K, Agarwal N, Eloy JA, Liu JK. Readability analysis of internetbased patient information regarding skull base tumors. J Neurooncol 2012;109:573-80. 19. Neuhauser L, Kreps GL. Online cancer communication: meeting the literacy, cultural and linguistic needs of diverse audiences. Patient Educ Couns 2008;71:365-77.

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23. U.S. Department of Health and Human Services National Institutes of Health, U.S.

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National Library of Medicine. How to Write Easy-to-Read Health Materials. Bethesda, MD. 2013. Available at http://www.nlm.nih.gov/medlineplus/etr.html (accessed 12/25/2013).

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24. Chung V, Horowitz AM, Canto MT, Siriphant P. Oral cancer educational materials for the general public: 1998. J Public Health Dent 2000;60:49-52.

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25. Jayaratne YS, Anderson NK, Zwahlen RA. Readability of websites containing information on dental implants. Clin Oral Implants Res 2013 Oct 22. doi: 10.1111/clr.12285. [Epub ahead of print] 26. Woodmansey K. Readability of educational materials for endodontic patients. J Endod 2010;36:1703-6.

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27. Sanghvi S, Cherla DV, Shukla PA, Eloy JA. Readability assessment of internet-based patient education materials related to facial fractures. Laryngoscope 2012;122:1943-8. 28. Cherla DV, Sanghvi S, Choudhry OJ, Liu JK, Eloy JA. Readability assessment of

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Internet-based patient education materials related to endoscopic sinus surgery. Laryngoscope 2012;122:1649-54.

29. Antonarakis GS, Kiliaridis S. Internet-derived information on cleft lip and palate for

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families with affected children. Cleft Palate Craniofac J 2009;46:75-80.

30. Svider PF, Agarwal N, Choudhry OJ, Hajart AF, Baredes S, Liu JK, et al. Readability

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assessment of online patient education materials from academic otolaryngology-head and neck surgery departments. Am J Otolaryngol 2013;34:31-5.

31. Eloy JA, Li S, Kasabwala K, Agarwal N, Hansberry DR, Baredes S, et al. Readability assessment of patient education materials on major otolaryngology association websites.

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Otolaryngol Head Neck Surg 2012;147:848-54.

32. Kasabwala K, Agarwal N, Hansberry DR, Baredes S, Eloy JA. Readability assessment of patient education materials from the American Academy of Otolaryngology--Head and

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Neck Surgery Foundation. Otolaryngol Head Neck Surg 2012;147:466-71. 33. Agarwal N, Hansberry DR, Sabourin V, Tomei KL, Prestigiacomo CJ. A comparative

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analysis of the quality of patient education materials from medical specialties. JAMA Intern Med 2013;173:1257-9. 34. Irwin JY, Thyvalikakath T, Spallek H, Wali T, Kerr AR, Schleyer T. English and Spanish oral cancer information on the internet: a pilot surface quality and content evaluation of oral cancer web sites. J Public Health Dent 2011;71:106-16.

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35. Dunne S, Cummins NM, Hannigan A, Shannon B, Dunne C, Cullen W. A method for the design and development of medical or health care information websites to optimize

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search engine results page rankings on Google. J Med Internet Res 2013;15:e183.

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Figure Legends

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Figure 2: Percentage of Specific Aspects of Dental Care Discussed

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Figure 1: Percentage of Specific Cancer Treatment Toxicities and/or Complications Discussed

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Table 1: Type of Cancer, Treatment Modalities, and Dental Care Timing Around Cancer Treatment Discussed on the Website (n=32)

13 (41%) 11 (34%) 5 (16%) 2 (6%) 1 (3%)

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27 (84%) 25 (78%) 10 (31%) 5 (16%) 3 (9%)

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Number (%)

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Parameter Cancer Type Discussed Only Nonspecific sites Nonspecific sites and Head/Neck Only Head/Neck Only Other (breast and esophageal) Nonspecific and Other (lymphoma) Cancer Treatment Modalities Discussed Radiation Therapy Chemotherapy Hematopoietic Stem Cell Transplantation Surgery Unspecified Dental Care Timing Around Cancer Treatment Before During After Unspecified

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22 (69%) 22 (69%) 17 (53%) 3 (9%)

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Table 2: Website Content Assessed with JAMA Benchmarks Criteria Number of JAMA Benchmarks Met Websites, number (%) None (Worst Quality) 3 (9%) One 16 (50%) Two 5 (16%) Three 7 (22%) Four (Best Quality) 1 (3%) Specific Benchmark Met 4 (13%) Authorship 6 (19%) Attribution 29 (91%) Disclosure 12 (38%) Currency

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Sponsorship (n) Average FRES score (range) Non-Profit Organization (10) 45.84 (32.73-65.12) University/Medical Center (8) 38.91 (16.18-58.71) Commercial/Corporate (7) 47.39 (31.54-66.38) Private Practice (5) 43.25 (16.52-55.22) Government (2) 29.69 (24.53-34.85) All sites 43.04 (16.52-66.38) FRES- Flesch Reading Ease Score

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Table 3. Readability (FRES score) by Site Sponsorship

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Statement of Clinical Relevance.

Given the increasing cancer patient interest in web-based health information materials and the diversity of information available on the internet, professionals need to be diligent in searching

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for and recommending websites that can promote and support positive oral health outcomes.

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