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Exploring the Reasons for Delay in Treatment of Oral Cancer
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Exploring the Reasons for Delay in Treatment of Oral Cancer Zachary S. Peacock, M. Anthony Pogrel and Brian L. Schmidt JADA 2008;139(10):1346-1352 10.14219/jada.archive.2008.0046 The following resources related to this article are available online at jada.ada.org (this information is current as of October 14, 2014): Updated information and services including high-resolution figures, can be found in the online version of this article at: http://jada.ada.org/content/139/10/1346
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Exploring the reasons for delay in treatment of oral cancer Zachary S. Peacock, DMD, MD; M. Anthony Pogrel, DDS, MD, FRCS, FACS; Brian L. Schmidt, DDS, MD, PhD, FACS
pproximately 30,000 new cases of oral and pharyngeal cancer are diagnosed per year in the United States, with approximately 8,500 deaths per year,1 and the incidence may be increasing.2,3 Overall, oral and pharyngeal cancer constitutes about 2 percent of all malignancies,4 but it is the seventh most common malignancy in males.5 Despite many new investigative modalities as well as improved surgical and radiation therapies, investigators often state that overall survival has not improved significantly during the last 40 years.6 In addition, investigators frequently report that the five-year survival rate is about 50 percent.7 Recently, however, improved overall survival has been reported,8 indicating that recent advances in diagnosis, imaging and treatment may be having some effect on outcome. The largest single variable affecting survival appears to be the cancer’s stage at the patient’s initial visit.9 For stage 1 disease, the fiveyear survival rate is more than 80 percent,10 while the overall five-year survival rate for patients with
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ABSTRACT Background. Oral cancer continues to be diagnosed and treated at a late stage, which has a negative effect on outcomes. This study identified and quantified delays in diagnosis and treatment. Methods. The authors conducted a study that included all new patients seen in the Department of Oral and Maxillofacial Surgery, University of California, San Francisco, between 2003 and 2007 who had a diagnosis of squamous cell carcinoma of the oral cavity. They identified the time intervals for six stages, beginning with the time at which patients first became aware of symptoms and ending with the time at which definitive treatment began. Results. The total time from patients’ first sign or symptoms to commencement of treatment was a mean of 205.9 days (range, 52-786 days). The longest delay was from the time symptoms first appeared to the initial visit to a health care professional (mean time, 104.7 days; range, 0-730 days). Conclusions. Health care professionals need to place greater emphasis on patient education to encourage early self-referrals. Clinical Implications. Patients should be encouraged to visit a health care professional when signs or symptoms of oral cancer first develop. Key Words. Oral cancer; early diagnosis; delay in diagnosis. JADA 2008;139(10):1346-1352.
Dr. Peacock is a resident, Department of Oral and Maxillofacial Surgery, University of California, San Francisco. Dr. Pogrel is a professor and the chairman, Department of Oral and Maxillofacial Surgery, University of California, San Francisco, P.O. Box 0440, 521 Parnassus Ave., Room C-522, San Francisco, Calif., 94143-0440, e-mail “[email protected]“. Address reprint requests to Dr. Pogrel. Dr. Schmidt is an associate professor and director, Residency Training Program, Department of Oral and Maxillofacial Surgery, University of California, San Francisco.
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d T1: length of time, in days, from the time at stage 4 disease is as low as 20 percent.11-13 Patients continue to wait to visit their clinicians which the patient first became aware of sympuntil their disease has reached an advanced toms (subsequently shown to be oral cancer) to stage. This may seem surprising, given that his or her first visit to a primary care clinician lesions generally are superficial, easily visible (physician or dentist). This time often was approximate because patients tended to estimate and painful.14 time in months, but sometimes they could idenSome evidence shows that early diagnosis and tify the week or day when they first became treatment can significantly decrease morbidity aware of the cancer. associated with treatment and may improve d T2: length of time, in days, from the time overall long-term survival.15,16 This latter finding when the patient was seen by the primary care has, however, been difficult to substantiate, clinician to the time when he or she underwent a because although some studies suggest a better biopsy performed by the primary care clinician or long-term survival with early diagnosis, other the time when he or she was referred to a studies have not shown such a relationship.17 This specialist. may indicate that for some specific types of oral d T3: length of time, in days, from the time cancer, even early diagnosis may not improve when the biopsy was performed by the primary long-term prognosis. Nevertheless, it does appear care clinician or the patient was that early diagnosis and treatment referred to the time when the are preferable to delay. Some evidence shows patient was seen by the specialist. We conducted this study to identhat early diagnosis In this study, the specialist always tify the different stages at which was an oral and maxillofacial surdelay can occur within the U.S. and treatment can health care system with regard to significantly decrease geon who had an interest in head and neck pathology. diagnosis and treatment of oral morbidity associated d T4: length of time, in days, from cancer. with treatment and the time when the patient was first SUBJECTS, MATERIALS may improve overall seen by the oral and maxillofacial AND METHODS long-term survival. surgeon at the University of California, San Francisco, to the comThis study includes all patients pletion of appropriate studies and seen in the Oral and Maxillofacial investigations. Surgery Clinic, University of California, San d T5: length of time, in days, from the compleFrancisco, between Jan. 1, 2003, and Dec. 31, tion of studies and investigations to the time 2007 (60 months), with a new diagnosis of squawhen the patient’s case was presented to the head mous cell carcinoma of the oral cavity. Exclusion and neck tumor board for discussion and treatcriteria included other malignancies, recurrences, ment planning. long-standing dysplasia, proliferative verrucous d T6: length of time, in days, from case presentaleukoplakia and other premalignant conditions. tion to the head and neck tumor board to the time We chose these criteria because many of these at which definitive treatment was begun. This patients were being seen on a regular basis by a was either the first day of radiation therapy or health care professional. We also excluded the day of surgery. patients who received any part of their treatment—except for the first visit to a primary care RESULTS clinician—elsewhere because we wished to study delays within one health care facility. During the five-year study period, we identified As part of an established protocol, all patients 50 new patients with biopsy-proven squamous with head and neck cancer who are scheduled to cell carcinoma of the oral cavity who did not meet receive any type of treatment at the University of the exclusion criteria. Below are the time interval California, San Francisco, are presented to a findings: weekly multidisciplinary head and neck tumor d T1: mean time from the patient’s first board for discussion and treatment planning. becoming aware of the problem to visiting a priTherefore, we defined the time intervals estabmary care clinician, 104.7 days (range, 0-730 lished as sequential and potential areas for delay days); to occur in the system as follows: d T2: mean time from the patient’s visiting a JADA, Vol. 139
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primary care clinician to undergoing a biopsy or being referred, 35.9 days (range, 0-280 days); d T3: mean time from the biopsy or referral to actually visiting a specialist, 17.7 days (range, 0-240 days); d T4: mean time from visiting a specialist to undergoing appropriate tests, 10.1 days (range, 0-33 days); d T5: mean time from completion of tests to case presentation to the head and neck tumor board, 20.7 days (range, 1-208 days); d T6: mean time from case presentation to the head and neck tumor board to commencement of definitive treatment, 16.6 days (range, 1-76 days). The mean total time from patients’ becoming aware of their problem to commencement of definitive treatment was 205.9 days (range, 52-786 days). DISCUSSION
Oral cancer remains a public health problem, with approximately 8,500 people dying of the disease each year in the United States.1 In our study, the longest single delay in receiving treatment was from the time the patient became aware of a possible problem to his or her first visit to a primary care clinician. Other studies have confirmed this delay.18-22 The shortest time for a symptomatic patient to visit a clinician in this study was the same day that symptoms appeared, and the longest time was more than two years. Although the literature contains reports of oral cancer progressing slowly,23 in general, a delay of more than two years, as occurred in one case in this study, worsens the patient’s overall long-term prognosis and complicates the treatment. Educating patients. Health care providers must place greater emphasis on educating patients about the importance of visiting a clinician as soon as oral symptoms develop. They can visit a dentist or a physician, and the clinician should schedule an early appointment for these patients.24 Health care providers’ offices should not encourage patients to visit an emergency department, because this is not its primary function. Reasons for delay. There are a number of reasons why people do not visit clinicians soon after noticing symptoms. One is the financial barrier that exists for many patients who are at risk of developing oral cancer. Interestingly, Yu and colleagues25 recently studied 102 patients with 1348
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new diagnoses of oral cancer at the University of Toronto. They reported a mean initial delay of 21.7 weeks in visiting a health care professional, although the median delay was only 4.5 weeks. This median delay of 4.5 weeks was remarkably shorter than the median delay of 18.4 weeks found at our institution. This disparity may be explained by the fact that Canada’s health care system is publicly funded. In the United States, studies have shown that health insurance status is an important predictor of the stage at which patients with oropharyngeal cancer first visit a clinician.26 Compared with patients with private health insurance, those with no insurance and those with Medicaid had a greater likelihood of being diagnosed with overall advanced-stage cancer.26 Although it is a daunting task, the dental profession needs to find a way to eliminate financial restraints that prevent patients from seeking care when symptoms first appear. Increased access to health care, including dental care, for uninsured patients likely would allow for more frequent detection of early-stage cancers. Government agencies, universities and dental clinics have made attempts to diagnose cancer early, via population screening and the use of various visual and chemical detection methods. Routine screening of asymptomatic people in an attempt to diagnose oral cancer early is not practical and does not meet any epidemiologic guidelines for a successful screening program; attempts to implement such programs generally have not been effective.27,28 In general, for those considering a regional or national screening program, the following are needed29: d an identifiable and diagnosable disease that is an important health problem; d availability of an accepted treatment for patients with recognized disease; d a recognizable latent or early symptomatic stage; d an adequate understanding of the natural history of the disease; d a simple, cost-effective and reliable test for the disease that has acceptable rates of false-positive and false-negative findings; d a screening process that is ongoing and not a one-time project; d detection of the disease via screening that improves the outcome. Routine screening of the general population for oral cancer cannot meet the above guidelines.30
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Nevertheless, screening of certain high-risk an incisional biopsy, which again is impractical groups may result in earlier detection and earlier for the general population. The brush biopsy is treatment.31 Such high-risk groups might include intended to assess clinical lesions that may not those with alcoholism, those who smoke32,33 and otherwise have undergone a biopsy, because the those who had developed a carcinoma previously, level of suspicion for cancer in these lesions is because it is known that patients who have had a low.43,44 The brush biopsy technique has been wellmalignancy in one part of the body are more accepted by dentists and has helped detect maligliable to develop one in another site.34 In parnant and premalignant lesions in early stages ticular, Kramer and colleagues35 reported that that otherwise would have been watched or those who have had an oral carcinoma have a ignored.42 There also are anecdotal reports of greater than 9 percent overall chance of develfalse-positive45 and false-negative46 results with oping a second oral carcinoma throughout their brush biopsy techniques. To our knowledge, no lifetime, while Day and Blot36 found second pristudies have compared cytology with scalpel mary malignancies at a rate of 3.7 percent per biopsy in a large number of seemingly innocuous year. lesions identified on clinical examination that Oral cancer testing. Developing and valitypically would not undergo a biopsy.41 Further dating an acceptable test for detecting oral cancer studies are needed to clarify the sensitivity and with minimal false-positive and specificity of the brush biopsy techfalse-negative results has been nique for lesions of low suspicion. Developing and problematic. Screening via clinical A recently developed detection validating an examination alone—as can be done system, the VELscope (LED Dental, by a general dentist during the White Rock, British Columbia, acceptable test for patient’s routine dental examiCanada), is thought to enhance dendetecting oral cancer nation—or via oral health fairs tists’ ability to detect oral cancer with minimal generally has resulted in poor after the tissue in question is false-positive and detection rates, mainly because the exposed to fluorescent light. The false-negative results high-risk population does not visit premise is that abnormal cells will has been problematic. absorb fluorescent light and appear a dentist regularly or attend screenings at health fairs. In pardark, while normal mucosa will ticular, this applies to patients reflect light and glow. To date, the with a history of alcohol abuse.37 With routine effectiveness of this device has been described only in observational and case studies.47,48 screening of asymptomatic patients, examination alone may identify areas such as leukoplakia and Although it can detect abnormal tissue, it atrophy; however, a biopsy is necessary to make a remains to be seen if it can distinguish cancer diagnosis, and this is a time-consuming, uncomfrom other abnormal oral tissues, such as aphfortable and relatively expensive technique that thous ulcers. In addition, biopsy ultimately still is cannot be applied to a general population.38 required.49 Therefore, determining the true sensitivity and With routine screening of an asymptomatic specificity of a clinical examination is not possible population being unrealistic and ineffective for without comparing it with the gold standard of the detection of oral cancer,50 most cases are diagscalpel biopsy. nosed when a patient with symptoms visits a clinAdjunctive techniques. Alternative diagician. In practice, some patients may make a spenostic techniques such as chemiluminescence39 cial visit to a dentist when symptoms develop, or and toluidine blue staining40 indicate which areas some may wait until their next six-month of the oral cavity may be more suspicious than checkup before mentioning a sore or an ulcer.51 others and may direct the choice of biopsy site, Other patients may visit a primary care physibut they are useful only as an adjunct in diagcian, and this applies in particular to patients nosing existing lesions. Thus, chemiluminescence who have medical insurance but may not have and toluidine blue staining are not true screening dental insurance. Studies have shown that, in tests.41 general, physicians are capable of diagnosing oral Brush biopsy. A noninvasive biopsy such as carcinoma and referring patients appropriately,52 the brush biopsy technique can identify atypical but health care providers in oral specialties are cells,42 but any such detection must be followed by known to be better trained in this area.53 In our JADA, Vol. 139
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study, some patients had been seen by a physician or a dentist on a number of occasions with the patient complaining about a persistent oral problem before he or she finally underwent a biopsy or was referred. Self-examination. One intriguing concept in increasing awareness of oral cancer is to institute a self-examination campaign54 similar to the monthly breast self-examination campaign. A visual examination of the oral cavity in a mirror on a monthly basis would be fairly easy to perform and could result in the detection of some lesions. Patients would be instructed to lift up their tongues to view the floor of the mouth, move the tongue to the right and left of the mouth to evaluate the lateral surfaces and pull both cheeks laterally to examine the vestibules, gingivae and buccal mucosa. Self-examination has the potential to enable patients to detect asymptomatic cancers at early stages. Not only does self-examination increase the frequency with which the oral cavity is screened, but it is done at no burden to the health care system beyond patient education (for example, brochures). Patients without symptoms might visit a general dentist every six months and a physician every year. Any self-examination conducted between these intervals might result in the detection of lesions and expedite visits to health care professionals before symptoms develop. Again, the main difficulty lies in communicating this message to patients who are at greatest risk. National oral health organizations have recognized this and have increased their efforts to educate the public. In 2002, the American Dental Association received a five-year grant from the National Cancer Institute that focused on oral cancer prevention education for practicing dentists in the United States.55 More than 60 continuing education programs have been held, focusing on the key components of oral cancer prevention, including risk assessment and risk reduction for tobacco and alcohol use, chemoprevention, early detection and early diagnosis. The American Association of Oral and Maxillofacial Surgeons also has initiated a task force on early detection of oral cancer.56 Despite these efforts, the majority of consumers do not know that dentists screen for oral cancer.57,58 Through continued public educational efforts, however, patients will be better informed regarding oral cancer screenings provided by dentists. 1350
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In our study, the mean time from the initial appointment with a primary care physician or dentist to a biopsy or referral to a specialist was 35.9 days. This is longer than one would wish, particularly when we consider the fact that in some cases, there was a delay of almost 10 months from the time when the patient first visited a clinician to the time when the patient underwent a biopsy. The British National Health Service, in its guidelines for general medical practitioners,59 recommends that clinicians refer patients to specialists in the following circumstances: d any oral signs or symptoms for which a definitive diagnosis cannot be made and that do not resolve within six weeks; d unexplained oral red or white patches that are painful, swollen or bleeding; d unexplained oral ulcer present for longer than three weeks; d unexplained tooth mobility (unless the teeth are loose, clinicians may refer patients to a general dentist). Delays in referral by primary care clinicians have led to lawsuits and claims of malpractice,60,61 and some evidence shows that the number of such malpractice claims may be increasing.62 An early biopsy or referral of a patient with an unknown lesion is indicated,51 and a biopsy of an unknown lesion that does not resolve within three weeks is essential. Any patient who is referred to a specialist because of a suspicious lesion should be given an appointment as soon as possible. In our study, the mean time from referral to a specialist to actually being seen by a specialist was 17.7 days, which is appropriate. The longest delay was 240 days, and this was because of a patient-generated delay. This specific delay illustrates the need for patients to realize the potential seriousness of the problem and the wisdom of arranging and keeping early appointments. In most cases, there was an inevitable delay between the patient’s seeing the specialist and undergoing necessary tests and other investigations. These included plain radiographs, computed tomography, magnetic resonance imaging, positron emission tomography, direct and indirect laryngoscopy, triple endoscopy and appropriate laboratory tests. The longest time for these tests to be performed in our study was 33 days. In some cases, a delay was caused by the need to obtain insurance authorization for some studies. In addition, in some cases, there were delays of a
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few days in the scheduling of imaging studies. The mean delay of 10.1 days in this study appears appropriate. Head and neck tumor board. The mean delay from completion of imaging and other investigations to presentation to the head and neck tumor board was 20.7 days (range, one to 208 days). In two cases, the delays were more than 200 days, thus elevating the mean number. Again, these delays were patient-generated and resulted from patients who were difficult to contact and difficult to persuade of the importance of presentation to the head and neck tumor board. If we exclude these outliers, the mean time is reduced to 13.2 days, which is appropriate because some patients could not attend the tumor board presentation during the week after their diagnosis. Definitive treatment. The mean time from presentation to the head and neck tumor board to commencement of definitive treatment was 18.6 days, which appears appropriate because there often was a delay in obtaining insurance authorization and in scheduling an operating room (frequently two to three weeks for each). Similarly, there often was an unavoidable delay in commencing radiation therapy, because of the need to obtain insurance authorization and for any planning (such as calculating radiation dosage) that was necessary. Overall delay. The overall delay from the patient’s first becoming aware of symptoms to commencement of definitive treatment was a mean of 203.8 days, which is just less than seven months (range, more than two months to 21⁄2 years). This overall delay appears unacceptable; we would hope that the interval would be eight weeks or less. No patients in our study underwent definitive treatment in less than eight weeks. CONCLUSION
Delays in the diagnosis and treatment of oral cancer occur in a number of stages in the referral and treatment process. The longest single delay in our study occurred between the patient’s first becoming aware of symptoms and visiting a primary care clinician. Health care professionals need to place more emphasis on early selfreferrals, as well as accelerate other portions of the referral process, particularly in referrals from a primary care clinician to a specialist. Screening and self-examinations of high-risk groups might improve outcomes for patients who self-refer late
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in the course of their oral cancer. The practical issues of how high-risk people are identified, how they are screened and how often they are screened require further study. ■ Disclosure. None of the authors reported any disclosures. 1. Ries LA, Eisner MP, Kosary CL, et al, eds. SEER Cancer Statistics Review, 1975-2002. Bethesda, Md.: National Cancer Institute; 2005. “http://seer.cancer.gov/csr/1975_2002/citation.html”. Accessed Aug. 13, 2008. 2. Shiboski CH, Schmidt BL, Jordan RC. Tongue and tonsil carcinoma: increasing trends in the U.S. population ages 20-44 years. Cancer 2005;103(9):1843-1849. 3. O’Dowd A. Skin cancer is on the increase but incidence of lung cancer is falling. BMJ 2007;335(7615):322. 4. Cancer facts and figures. American Cancer Society: Atlanta; 2005. 5. Jemal A, Clegg LX, Ward E, et al. Annual report to the nation on the status of cancer, 1975-2001, with a special feature regarding survival. Cancer 2004;101(1):3-27. 6. McCann MF, Macpherson LM, Gibson J. The role of the general dental practitioner in detection and prevention of oral cancer: a review of the literature. Dent Update 2000;27(8):404-408. 7. Pisani P, Parkin DM, Bray F, Ferlay J. Estimates of the worldwide mortality from 25 cancers in 1990. Int J Cancer 1999;83(1):18-29. 8. Parker SL, Tong T, Bolden S, Wingo PA. Cancer statistics, 1997. CA Cancer J Clin 1997;47(1):5-27. 9. McGurk M, Chan C, Jones J, O’Regan E, Sherriff M. Delay in diagnosis and its effect on outcome in head and neck cancer. Br J Oral Maxillofac Surg 2005;43(4):281-284. 10. Spiro RH. Squamous cancer of the tongue. CA Cancer J Clin 1985;35(4):252-256. 11. Evans SJ, Langdon JD, Rapidis AD, Johnson NW. Prognostic significance of STNMP and velocity of tumor growth in oral cancer. Cancer 1982;49(4):773-776. 12. Mashberg A, Samit AM. Early detection, diagnosis, and management of oral and oropharyngeal cancer. CA Cancer J Clin 1989;39(2): 67-88. 13. Williams RG. The early diagnosis of carcinoma of the mouth. Ann R Coll Surg Engl 1981;63(6):423-425. 14. Scott SE, Grunfeld EA, McGurk M. The idiosyncratic relationship between diagnostic delay and stage of oral squamous cell carcinoma. Oral Oncol 2005;41(4):396-403. 15. Dolan RW, Vaughan CW, Fuleihan N. Symptoms in early head and neck cancer: an inadequate indicator. Otolaryngol Head Neck Surg 1998;119(5):463-467. 16. Vernham GA, Crowther JA. Head and neck carcinoma: stage at presentation. Clin Otolaryngol Allied Sci 1994;19(2):120-124. 17. Allison P, Locker D, Feine JS. The role of diagnostic delays in the prognosis of oral cancer: a review of the literature. Oral Oncol 1998; 34(3):161-170. 18. Brouha XD, Tromp DM, Hordijk GJ, Winnubst JA, de Leeuw JR. Oral and pharyngeal cancer: analysis of patient delay at different tumor stages. Head Neck 2005;27(11):939-945. 19. Llewellyn CD, Johnson NW, Warnakulasuriya S. Factors associated with delay in presentation among younger patients with oral cancer. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2004;97(6):707-713. 20. Onizawa K, Nishihara K, Yamagata K, Yusa H, Yanagawa T, Yoshida H. Factors associated with diagnostic delay of oral squamous cell carcinoma. Oral Oncol 2003;39(8):781-788. 21. Pitiphat W, Diehl SR, Laskaris G, Cartsos V, Douglass CW, Zavras AI. Factors associated with delay in the diagnosis of oral cancer. J Dent Res 2002;81(3):192-197. 22. Scott SE, Grunfeld EA, Main J, McGurk M. Patient delay in oral cancer: a qualitative study of patients’ experiences. Psychooncology 2006;15(6):474-485. 23. Kirita T, Kajihara A, Choudhury CR, et al. A patient with untreated tongue carcinoma surviving for 15 years. Int J Oral Maxillofac Surg 2005;34(3):324-327. 24. Diz Dios P, Padrón González N, Seoane Lestón J, Tomás Carmona I, Limeres Posse J, Varela-Centelles P. “Scheduling delay” in oral cancer diagnosis: a new protagonist. Oral Oncol 2005;41(2):142-146. 25. Yu T, Wood RE, Tenenbaum HC. Delays in diagnosis of head and neck cancers. J Can Dent Assoc 2008;74(1):61. 26. Chen AY, Schrag NM, Halpern MT, Ward EM. The impact of health insurance status on stage at diagnosis of oropharyngeal cancer.
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45. Rick GM. Oral brush biopsy: the problem of false positives. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2003;96(3):252. 46. Potter TJ, Summerlin DJ, Campbell JH. Oral malignancies associated with negative transepithelial brush biopsy. J Oral Maxillofac Surg 2003;61(6):674-677. 47. Poh CF, Zhang L, Anderson DW, et al. Fluorescence visualization detection of field alterations in tumor margins of oral cancer patients. Clin Cancer Res 2006;12(22):6716-6722. 48. Poh CF, Ng SP, Williams PM, et al. Direct fluorescence visualization of clinically occult high-risk oral premalignant disease using a simple hand-held device. Head Neck 2007;29(1):71-76. 49. Lane PM, Gilhuly T, Whitehead P, et al. Simple device for the direct visualization of oral-cavity tissue fluorescence. J Biomed Opt 2006;11(2):024006. 50. Netuveli G, Sheiham A, Watt RG. Does the “inverse screening law” apply to oral cancer screening and regular dental check-ups? J Med Screen 2006;13(1):47-50. 51. Scully C, Newman L, Bagan JV. The role of the dental team in preventing and diagnosing cancer: 3. oral cancer diagnosis and screening. Dent Update 2005;32(6):326-328, 331-332, 335-337. 52. Sohn W, Ismail AI, Kolker JL. Knowledge of oral cancer and screening practices of primary care providers at Federally Qualified Health Centers. J Public Health Dent 2005;65(3):160-165. 53. Holmes JD, Dierks EJ, Homer LD, Potter BE. Is detection of oral and oropharyngeal squamous cancer by a dental health care provider associated with a lower stage at diagnosis? J Oral Maxillofac Surg 2003;61(3):285-291. 54. Want some life saving advice? Ask your dental hygienist about oral cancer. Chicago: American Dental Hygienists’ Association; 2002. “www.adha.org/downloads/oralcancer.pdf”. Accessed Aug. 13, 2008. 55. $1 million NCI grant targets oral cancer. ADA News Sept. 16, 2002:2-3. 56. American Association of Oral and Maxillofacial Surgeons. Oral cancer. “www.aaoms.org/oral_cancer.php”. Accessed Sept. 4, 2008. 57. Stahl S, Meskin LH, Brown LJ. The American Dental Association’s oral cancer campaign: the impact on consumers and dentists. JADA 2004;135(9):1261-1267. 58. Horowitz AM, Canto MT, Child WL. Maryland adults’ perspectives on oral cancer prevention and early detection. JADA 2002;133(8):1058-1063. 59. National Collaborating Centre for Primary Care. Referral guidelines for suspected cancer in adults and children. London: Royal College of General Practitioners; 2005. 60. Hapcook CP. Risk management considerations for oral cancer. JADA 2005;136(11):1566-1567. 61. Lydiatt DD. Cancer of the oral cavity and medical malpractice. Laryngoscope 2002;112(5):816-819. 62. Rapp C. Oral cancer malpractice claims increasing. Today’s Florida Dental Association 2005;17:37-38.
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Exploring the Reasons for Delay in Treatment of Oral Cancer Zachary S. Peacock, M. Anthony Pogrel and Brian L. Schmidt JADA 2008;139(10):1346-1352 10.14219/jada.archive.2008.0046 The following resources related to this article are available online at jada.ada.org (this information is current as of October 14, 2014): Updated information and services including high-resolution figures, can be found in the online version of this article at: http://jada.ada.org/content/139/10/1346
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Exploring the reasons for delay in treatment of oral cancer Zachary S. Peacock, DMD, MD; M. Anthony Pogrel, DDS, MD, FRCS, FACS; Brian L. Schmidt, DDS, MD, PhD, FACS
pproximately 30,000 new cases of oral and pharyngeal cancer are diagnosed per year in the United States, with approximately 8,500 deaths per year,1 and the incidence may be increasing.2,3 Overall, oral and pharyngeal cancer constitutes about 2 percent of all malignancies,4 but it is the seventh most common malignancy in males.5 Despite many new investigative modalities as well as improved surgical and radiation therapies, investigators often state that overall survival has not improved significantly during the last 40 years.6 In addition, investigators frequently report that the five-year survival rate is about 50 percent.7 Recently, however, improved overall survival has been reported,8 indicating that recent advances in diagnosis, imaging and treatment may be having some effect on outcome. The largest single variable affecting survival appears to be the cancer’s stage at the patient’s initial visit.9 For stage 1 disease, the fiveyear survival rate is more than 80 percent,10 while the overall five-year survival rate for patients with
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ABSTRACT Background. Oral cancer continues to be diagnosed and treated at a late stage, which has a negative effect on outcomes. This study identified and quantified delays in diagnosis and treatment. Methods. The authors conducted a study that included all new patients seen in the Department of Oral and Maxillofacial Surgery, University of California, San Francisco, between 2003 and 2007 who had a diagnosis of squamous cell carcinoma of the oral cavity. They identified the time intervals for six stages, beginning with the time at which patients first became aware of symptoms and ending with the time at which definitive treatment began. Results. The total time from patients’ first sign or symptoms to commencement of treatment was a mean of 205.9 days (range, 52-786 days). The longest delay was from the time symptoms first appeared to the initial visit to a health care professional (mean time, 104.7 days; range, 0-730 days). Conclusions. Health care professionals need to place greater emphasis on patient education to encourage early self-referrals. Clinical Implications. Patients should be encouraged to visit a health care professional when signs or symptoms of oral cancer first develop. Key Words. Oral cancer; early diagnosis; delay in diagnosis. JADA 2008;139(10):1346-1352.
Dr. Peacock is a resident, Department of Oral and Maxillofacial Surgery, University of California, San Francisco. Dr. Pogrel is a professor and the chairman, Department of Oral and Maxillofacial Surgery, University of California, San Francisco, P.O. Box 0440, 521 Parnassus Ave., Room C-522, San Francisco, Calif., 94143-0440, e-mail “[email protected]“. Address reprint requests to Dr. Pogrel. Dr. Schmidt is an associate professor and director, Residency Training Program, Department of Oral and Maxillofacial Surgery, University of California, San Francisco.
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d T1: length of time, in days, from the time at stage 4 disease is as low as 20 percent.11-13 Patients continue to wait to visit their clinicians which the patient first became aware of sympuntil their disease has reached an advanced toms (subsequently shown to be oral cancer) to stage. This may seem surprising, given that his or her first visit to a primary care clinician lesions generally are superficial, easily visible (physician or dentist). This time often was approximate because patients tended to estimate and painful.14 time in months, but sometimes they could idenSome evidence shows that early diagnosis and tify the week or day when they first became treatment can significantly decrease morbidity aware of the cancer. associated with treatment and may improve d T2: length of time, in days, from the time overall long-term survival.15,16 This latter finding when the patient was seen by the primary care has, however, been difficult to substantiate, clinician to the time when he or she underwent a because although some studies suggest a better biopsy performed by the primary care clinician or long-term survival with early diagnosis, other the time when he or she was referred to a studies have not shown such a relationship.17 This specialist. may indicate that for some specific types of oral d T3: length of time, in days, from the time cancer, even early diagnosis may not improve when the biopsy was performed by the primary long-term prognosis. Nevertheless, it does appear care clinician or the patient was that early diagnosis and treatment referred to the time when the are preferable to delay. Some evidence shows patient was seen by the specialist. We conducted this study to identhat early diagnosis In this study, the specialist always tify the different stages at which was an oral and maxillofacial surdelay can occur within the U.S. and treatment can health care system with regard to significantly decrease geon who had an interest in head and neck pathology. diagnosis and treatment of oral morbidity associated d T4: length of time, in days, from cancer. with treatment and the time when the patient was first SUBJECTS, MATERIALS may improve overall seen by the oral and maxillofacial AND METHODS long-term survival. surgeon at the University of California, San Francisco, to the comThis study includes all patients pletion of appropriate studies and seen in the Oral and Maxillofacial investigations. Surgery Clinic, University of California, San d T5: length of time, in days, from the compleFrancisco, between Jan. 1, 2003, and Dec. 31, tion of studies and investigations to the time 2007 (60 months), with a new diagnosis of squawhen the patient’s case was presented to the head mous cell carcinoma of the oral cavity. Exclusion and neck tumor board for discussion and treatcriteria included other malignancies, recurrences, ment planning. long-standing dysplasia, proliferative verrucous d T6: length of time, in days, from case presentaleukoplakia and other premalignant conditions. tion to the head and neck tumor board to the time We chose these criteria because many of these at which definitive treatment was begun. This patients were being seen on a regular basis by a was either the first day of radiation therapy or health care professional. We also excluded the day of surgery. patients who received any part of their treatment—except for the first visit to a primary care RESULTS clinician—elsewhere because we wished to study delays within one health care facility. During the five-year study period, we identified As part of an established protocol, all patients 50 new patients with biopsy-proven squamous with head and neck cancer who are scheduled to cell carcinoma of the oral cavity who did not meet receive any type of treatment at the University of the exclusion criteria. Below are the time interval California, San Francisco, are presented to a findings: weekly multidisciplinary head and neck tumor d T1: mean time from the patient’s first board for discussion and treatment planning. becoming aware of the problem to visiting a priTherefore, we defined the time intervals estabmary care clinician, 104.7 days (range, 0-730 lished as sequential and potential areas for delay days); to occur in the system as follows: d T2: mean time from the patient’s visiting a JADA, Vol. 139
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primary care clinician to undergoing a biopsy or being referred, 35.9 days (range, 0-280 days); d T3: mean time from the biopsy or referral to actually visiting a specialist, 17.7 days (range, 0-240 days); d T4: mean time from visiting a specialist to undergoing appropriate tests, 10.1 days (range, 0-33 days); d T5: mean time from completion of tests to case presentation to the head and neck tumor board, 20.7 days (range, 1-208 days); d T6: mean time from case presentation to the head and neck tumor board to commencement of definitive treatment, 16.6 days (range, 1-76 days). The mean total time from patients’ becoming aware of their problem to commencement of definitive treatment was 205.9 days (range, 52-786 days). DISCUSSION
Oral cancer remains a public health problem, with approximately 8,500 people dying of the disease each year in the United States.1 In our study, the longest single delay in receiving treatment was from the time the patient became aware of a possible problem to his or her first visit to a primary care clinician. Other studies have confirmed this delay.18-22 The shortest time for a symptomatic patient to visit a clinician in this study was the same day that symptoms appeared, and the longest time was more than two years. Although the literature contains reports of oral cancer progressing slowly,23 in general, a delay of more than two years, as occurred in one case in this study, worsens the patient’s overall long-term prognosis and complicates the treatment. Educating patients. Health care providers must place greater emphasis on educating patients about the importance of visiting a clinician as soon as oral symptoms develop. They can visit a dentist or a physician, and the clinician should schedule an early appointment for these patients.24 Health care providers’ offices should not encourage patients to visit an emergency department, because this is not its primary function. Reasons for delay. There are a number of reasons why people do not visit clinicians soon after noticing symptoms. One is the financial barrier that exists for many patients who are at risk of developing oral cancer. Interestingly, Yu and colleagues25 recently studied 102 patients with 1348
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new diagnoses of oral cancer at the University of Toronto. They reported a mean initial delay of 21.7 weeks in visiting a health care professional, although the median delay was only 4.5 weeks. This median delay of 4.5 weeks was remarkably shorter than the median delay of 18.4 weeks found at our institution. This disparity may be explained by the fact that Canada’s health care system is publicly funded. In the United States, studies have shown that health insurance status is an important predictor of the stage at which patients with oropharyngeal cancer first visit a clinician.26 Compared with patients with private health insurance, those with no insurance and those with Medicaid had a greater likelihood of being diagnosed with overall advanced-stage cancer.26 Although it is a daunting task, the dental profession needs to find a way to eliminate financial restraints that prevent patients from seeking care when symptoms first appear. Increased access to health care, including dental care, for uninsured patients likely would allow for more frequent detection of early-stage cancers. Government agencies, universities and dental clinics have made attempts to diagnose cancer early, via population screening and the use of various visual and chemical detection methods. Routine screening of asymptomatic people in an attempt to diagnose oral cancer early is not practical and does not meet any epidemiologic guidelines for a successful screening program; attempts to implement such programs generally have not been effective.27,28 In general, for those considering a regional or national screening program, the following are needed29: d an identifiable and diagnosable disease that is an important health problem; d availability of an accepted treatment for patients with recognized disease; d a recognizable latent or early symptomatic stage; d an adequate understanding of the natural history of the disease; d a simple, cost-effective and reliable test for the disease that has acceptable rates of false-positive and false-negative findings; d a screening process that is ongoing and not a one-time project; d detection of the disease via screening that improves the outcome. Routine screening of the general population for oral cancer cannot meet the above guidelines.30
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Nevertheless, screening of certain high-risk an incisional biopsy, which again is impractical groups may result in earlier detection and earlier for the general population. The brush biopsy is treatment.31 Such high-risk groups might include intended to assess clinical lesions that may not those with alcoholism, those who smoke32,33 and otherwise have undergone a biopsy, because the those who had developed a carcinoma previously, level of suspicion for cancer in these lesions is because it is known that patients who have had a low.43,44 The brush biopsy technique has been wellmalignancy in one part of the body are more accepted by dentists and has helped detect maligliable to develop one in another site.34 In parnant and premalignant lesions in early stages ticular, Kramer and colleagues35 reported that that otherwise would have been watched or those who have had an oral carcinoma have a ignored.42 There also are anecdotal reports of greater than 9 percent overall chance of develfalse-positive45 and false-negative46 results with oping a second oral carcinoma throughout their brush biopsy techniques. To our knowledge, no lifetime, while Day and Blot36 found second pristudies have compared cytology with scalpel mary malignancies at a rate of 3.7 percent per biopsy in a large number of seemingly innocuous year. lesions identified on clinical examination that Oral cancer testing. Developing and valitypically would not undergo a biopsy.41 Further dating an acceptable test for detecting oral cancer studies are needed to clarify the sensitivity and with minimal false-positive and specificity of the brush biopsy techfalse-negative results has been nique for lesions of low suspicion. Developing and problematic. Screening via clinical A recently developed detection validating an examination alone—as can be done system, the VELscope (LED Dental, by a general dentist during the White Rock, British Columbia, acceptable test for patient’s routine dental examiCanada), is thought to enhance dendetecting oral cancer nation—or via oral health fairs tists’ ability to detect oral cancer with minimal generally has resulted in poor after the tissue in question is false-positive and detection rates, mainly because the exposed to fluorescent light. The false-negative results high-risk population does not visit premise is that abnormal cells will has been problematic. absorb fluorescent light and appear a dentist regularly or attend screenings at health fairs. In pardark, while normal mucosa will ticular, this applies to patients reflect light and glow. To date, the with a history of alcohol abuse.37 With routine effectiveness of this device has been described only in observational and case studies.47,48 screening of asymptomatic patients, examination alone may identify areas such as leukoplakia and Although it can detect abnormal tissue, it atrophy; however, a biopsy is necessary to make a remains to be seen if it can distinguish cancer diagnosis, and this is a time-consuming, uncomfrom other abnormal oral tissues, such as aphfortable and relatively expensive technique that thous ulcers. In addition, biopsy ultimately still is cannot be applied to a general population.38 required.49 Therefore, determining the true sensitivity and With routine screening of an asymptomatic specificity of a clinical examination is not possible population being unrealistic and ineffective for without comparing it with the gold standard of the detection of oral cancer,50 most cases are diagscalpel biopsy. nosed when a patient with symptoms visits a clinAdjunctive techniques. Alternative diagician. In practice, some patients may make a spenostic techniques such as chemiluminescence39 cial visit to a dentist when symptoms develop, or and toluidine blue staining40 indicate which areas some may wait until their next six-month of the oral cavity may be more suspicious than checkup before mentioning a sore or an ulcer.51 others and may direct the choice of biopsy site, Other patients may visit a primary care physibut they are useful only as an adjunct in diagcian, and this applies in particular to patients nosing existing lesions. Thus, chemiluminescence who have medical insurance but may not have and toluidine blue staining are not true screening dental insurance. Studies have shown that, in tests.41 general, physicians are capable of diagnosing oral Brush biopsy. A noninvasive biopsy such as carcinoma and referring patients appropriately,52 the brush biopsy technique can identify atypical but health care providers in oral specialties are cells,42 but any such detection must be followed by known to be better trained in this area.53 In our JADA, Vol. 139
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study, some patients had been seen by a physician or a dentist on a number of occasions with the patient complaining about a persistent oral problem before he or she finally underwent a biopsy or was referred. Self-examination. One intriguing concept in increasing awareness of oral cancer is to institute a self-examination campaign54 similar to the monthly breast self-examination campaign. A visual examination of the oral cavity in a mirror on a monthly basis would be fairly easy to perform and could result in the detection of some lesions. Patients would be instructed to lift up their tongues to view the floor of the mouth, move the tongue to the right and left of the mouth to evaluate the lateral surfaces and pull both cheeks laterally to examine the vestibules, gingivae and buccal mucosa. Self-examination has the potential to enable patients to detect asymptomatic cancers at early stages. Not only does self-examination increase the frequency with which the oral cavity is screened, but it is done at no burden to the health care system beyond patient education (for example, brochures). Patients without symptoms might visit a general dentist every six months and a physician every year. Any self-examination conducted between these intervals might result in the detection of lesions and expedite visits to health care professionals before symptoms develop. Again, the main difficulty lies in communicating this message to patients who are at greatest risk. National oral health organizations have recognized this and have increased their efforts to educate the public. In 2002, the American Dental Association received a five-year grant from the National Cancer Institute that focused on oral cancer prevention education for practicing dentists in the United States.55 More than 60 continuing education programs have been held, focusing on the key components of oral cancer prevention, including risk assessment and risk reduction for tobacco and alcohol use, chemoprevention, early detection and early diagnosis. The American Association of Oral and Maxillofacial Surgeons also has initiated a task force on early detection of oral cancer.56 Despite these efforts, the majority of consumers do not know that dentists screen for oral cancer.57,58 Through continued public educational efforts, however, patients will be better informed regarding oral cancer screenings provided by dentists. 1350
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In our study, the mean time from the initial appointment with a primary care physician or dentist to a biopsy or referral to a specialist was 35.9 days. This is longer than one would wish, particularly when we consider the fact that in some cases, there was a delay of almost 10 months from the time when the patient first visited a clinician to the time when the patient underwent a biopsy. The British National Health Service, in its guidelines for general medical practitioners,59 recommends that clinicians refer patients to specialists in the following circumstances: d any oral signs or symptoms for which a definitive diagnosis cannot be made and that do not resolve within six weeks; d unexplained oral red or white patches that are painful, swollen or bleeding; d unexplained oral ulcer present for longer than three weeks; d unexplained tooth mobility (unless the teeth are loose, clinicians may refer patients to a general dentist). Delays in referral by primary care clinicians have led to lawsuits and claims of malpractice,60,61 and some evidence shows that the number of such malpractice claims may be increasing.62 An early biopsy or referral of a patient with an unknown lesion is indicated,51 and a biopsy of an unknown lesion that does not resolve within three weeks is essential. Any patient who is referred to a specialist because of a suspicious lesion should be given an appointment as soon as possible. In our study, the mean time from referral to a specialist to actually being seen by a specialist was 17.7 days, which is appropriate. The longest delay was 240 days, and this was because of a patient-generated delay. This specific delay illustrates the need for patients to realize the potential seriousness of the problem and the wisdom of arranging and keeping early appointments. In most cases, there was an inevitable delay between the patient’s seeing the specialist and undergoing necessary tests and other investigations. These included plain radiographs, computed tomography, magnetic resonance imaging, positron emission tomography, direct and indirect laryngoscopy, triple endoscopy and appropriate laboratory tests. The longest time for these tests to be performed in our study was 33 days. In some cases, a delay was caused by the need to obtain insurance authorization for some studies. In addition, in some cases, there were delays of a
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few days in the scheduling of imaging studies. The mean delay of 10.1 days in this study appears appropriate. Head and neck tumor board. The mean delay from completion of imaging and other investigations to presentation to the head and neck tumor board was 20.7 days (range, one to 208 days). In two cases, the delays were more than 200 days, thus elevating the mean number. Again, these delays were patient-generated and resulted from patients who were difficult to contact and difficult to persuade of the importance of presentation to the head and neck tumor board. If we exclude these outliers, the mean time is reduced to 13.2 days, which is appropriate because some patients could not attend the tumor board presentation during the week after their diagnosis. Definitive treatment. The mean time from presentation to the head and neck tumor board to commencement of definitive treatment was 18.6 days, which appears appropriate because there often was a delay in obtaining insurance authorization and in scheduling an operating room (frequently two to three weeks for each). Similarly, there often was an unavoidable delay in commencing radiation therapy, because of the need to obtain insurance authorization and for any planning (such as calculating radiation dosage) that was necessary. Overall delay. The overall delay from the patient’s first becoming aware of symptoms to commencement of definitive treatment was a mean of 203.8 days, which is just less than seven months (range, more than two months to 21⁄2 years). This overall delay appears unacceptable; we would hope that the interval would be eight weeks or less. No patients in our study underwent definitive treatment in less than eight weeks. CONCLUSION
Delays in the diagnosis and treatment of oral cancer occur in a number of stages in the referral and treatment process. The longest single delay in our study occurred between the patient’s first becoming aware of symptoms and visiting a primary care clinician. Health care professionals need to place more emphasis on early selfreferrals, as well as accelerate other portions of the referral process, particularly in referrals from a primary care clinician to a specialist. Screening and self-examinations of high-risk groups might improve outcomes for patients who self-refer late
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in the course of their oral cancer. The practical issues of how high-risk people are identified, how they are screened and how often they are screened require further study. ■ Disclosure. None of the authors reported any disclosures. 1. Ries LA, Eisner MP, Kosary CL, et al, eds. SEER Cancer Statistics Review, 1975-2002. Bethesda, Md.: National Cancer Institute; 2005. “http://seer.cancer.gov/csr/1975_2002/citation.html”. Accessed Aug. 13, 2008. 2. Shiboski CH, Schmidt BL, Jordan RC. Tongue and tonsil carcinoma: increasing trends in the U.S. population ages 20-44 years. Cancer 2005;103(9):1843-1849. 3. O’Dowd A. Skin cancer is on the increase but incidence of lung cancer is falling. BMJ 2007;335(7615):322. 4. Cancer facts and figures. American Cancer Society: Atlanta; 2005. 5. Jemal A, Clegg LX, Ward E, et al. Annual report to the nation on the status of cancer, 1975-2001, with a special feature regarding survival. Cancer 2004;101(1):3-27. 6. McCann MF, Macpherson LM, Gibson J. The role of the general dental practitioner in detection and prevention of oral cancer: a review of the literature. Dent Update 2000;27(8):404-408. 7. Pisani P, Parkin DM, Bray F, Ferlay J. Estimates of the worldwide mortality from 25 cancers in 1990. Int J Cancer 1999;83(1):18-29. 8. Parker SL, Tong T, Bolden S, Wingo PA. Cancer statistics, 1997. CA Cancer J Clin 1997;47(1):5-27. 9. McGurk M, Chan C, Jones J, O’Regan E, Sherriff M. Delay in diagnosis and its effect on outcome in head and neck cancer. Br J Oral Maxillofac Surg 2005;43(4):281-284. 10. Spiro RH. Squamous cancer of the tongue. CA Cancer J Clin 1985;35(4):252-256. 11. Evans SJ, Langdon JD, Rapidis AD, Johnson NW. Prognostic significance of STNMP and velocity of tumor growth in oral cancer. Cancer 1982;49(4):773-776. 12. Mashberg A, Samit AM. Early detection, diagnosis, and management of oral and oropharyngeal cancer. CA Cancer J Clin 1989;39(2): 67-88. 13. Williams RG. The early diagnosis of carcinoma of the mouth. Ann R Coll Surg Engl 1981;63(6):423-425. 14. Scott SE, Grunfeld EA, McGurk M. The idiosyncratic relationship between diagnostic delay and stage of oral squamous cell carcinoma. Oral Oncol 2005;41(4):396-403. 15. Dolan RW, Vaughan CW, Fuleihan N. Symptoms in early head and neck cancer: an inadequate indicator. Otolaryngol Head Neck Surg 1998;119(5):463-467. 16. Vernham GA, Crowther JA. Head and neck carcinoma: stage at presentation. Clin Otolaryngol Allied Sci 1994;19(2):120-124. 17. Allison P, Locker D, Feine JS. The role of diagnostic delays in the prognosis of oral cancer: a review of the literature. Oral Oncol 1998; 34(3):161-170. 18. Brouha XD, Tromp DM, Hordijk GJ, Winnubst JA, de Leeuw JR. Oral and pharyngeal cancer: analysis of patient delay at different tumor stages. Head Neck 2005;27(11):939-945. 19. Llewellyn CD, Johnson NW, Warnakulasuriya S. Factors associated with delay in presentation among younger patients with oral cancer. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2004;97(6):707-713. 20. Onizawa K, Nishihara K, Yamagata K, Yusa H, Yanagawa T, Yoshida H. Factors associated with diagnostic delay of oral squamous cell carcinoma. Oral Oncol 2003;39(8):781-788. 21. Pitiphat W, Diehl SR, Laskaris G, Cartsos V, Douglass CW, Zavras AI. Factors associated with delay in the diagnosis of oral cancer. J Dent Res 2002;81(3):192-197. 22. Scott SE, Grunfeld EA, Main J, McGurk M. Patient delay in oral cancer: a qualitative study of patients’ experiences. Psychooncology 2006;15(6):474-485. 23. Kirita T, Kajihara A, Choudhury CR, et al. A patient with untreated tongue carcinoma surviving for 15 years. Int J Oral Maxillofac Surg 2005;34(3):324-327. 24. Diz Dios P, Padrón González N, Seoane Lestón J, Tomás Carmona I, Limeres Posse J, Varela-Centelles P. “Scheduling delay” in oral cancer diagnosis: a new protagonist. Oral Oncol 2005;41(2):142-146. 25. Yu T, Wood RE, Tenenbaum HC. Delays in diagnosis of head and neck cancers. J Can Dent Assoc 2008;74(1):61. 26. Chen AY, Schrag NM, Halpern MT, Ward EM. The impact of health insurance status on stage at diagnosis of oropharyngeal cancer.
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