- Email: [email protected]
Treatment modalities and medication recommended by health care professionals for treating recurrent herpes labialis
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1.4 percent of the elderly population at the time of examination.4 Although there is no cure for RHL, numerous clinical trials have been conducted to find better forms of treatment and medica tions for this disease. Research also is being conducted to determine how the virus establishes or maintains a dormant state and reactivates itself within the sensory ganglia. 48
JADA, Vol. 135, January 2004 Copyright ©2004 American Dental Association. All rights reserved.
I
old sores, also known as recurrent herpes labialis, or RHL, are caused by a herpes simplex type 1 virus that remains dormant in the sensory ganglia until it is reactivated by triggers such as sun exposure, stress, and illness or trauma. RHL is a viral infection that affects an esti mated one-third of the world’s population1 and can cause pain, disfigurement and embarrassPharmacists ment to the patient. In a Swedish population of people between birth and 60 years are more likely of age, it was noted that 26.6 percent than dentists reported having a history of RHL and and physicians 19.45 percent reported having a recurrent to see episode during the past two years.2 A customers study of more than 20,000 Swedes had RHL at the when they reported that 3.1 percent time of assessment.3 More recently, a have cold German study reported that RHL was sores. reported in 1.3 percent of the adult and
T
G. WAYNE RABORN, D.D.S., M.S.; KAREN S. CHAN, B.Sc., R.D.H.; MICHAEL GRACE, Ph.D.
Background. The authors conducted a survey to determine how health care professionals respond to A D A J patients’ inquiries about ✷ ✷ cold sores, also known as recurrent herpes labialis, and their choices of treatN C U U ment modalities and IN G ED A medications. RT ICLE Methods. The authors mailed a one-page, pretested survey to a random sample of dentists, pharmacists and family physicians in Alberta, Canada. After receiving ethics approval from the University of Alberta, Edmonton, the authors mailed 998 surveys. The response rate was 51 percent. Results. Topical antiviral medication was the most common treatment recommended (63 percent). Over-the-counter medication was the first choice for pharmacists (83 percent) as compared with dentists (15 percent) and physicians (16 percent). Emotional stress (60 percent) was reported by patients to be the most common trigger, and pain or discomfort (81 percent) was their primary concern. Acyclovir ointment was the most common antiviral drug recommended or prescribed by health care professionals (60 percent), and cost was the major reason they gave for not recommending or prescribing antiviral drugs (73 percent). Conclusions. The authors found variation in treatment modalities and recommendations by each health profession, despite the fact that patients reported similar triggers and concerns. This may be due to individual patient need and the health care professional’s lack of knowledge. Practice Implications. Survey results may serve as a reference for health care professionals to use to determine how their choices of medications and treatment modalities compare with those of other practitioners. Professionals should know the benefits and limitations of all therapies, discuss them with the patients and select a treatment. CON
Treatment modalities and medication recommended by health care professionals for treating recurrent herpes labialis
ABSTRACT
IO N
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Antiviral drugs are the main mode of treatThe confidential survey consisted of four short ment prescribed for RHL.5 These drugs can be demographic questions and nine questions perused as an intermittent, suppressive or topical taining to the frequency of cold sore inquiries, form of therapy. A range of over-the-counter, or patient concerns, treatment modalities, and the OTC, medications may be recommended to relieve prescribing or recommending of antiviral drugs or cold sore symptoms. Various forms of alternative OTC medications. Participants selected their therapy also are available for people who have answers from choices given (multiple responses cold sores. were allowed) or wrote their own responses based Treatment modalities for RHL are numerous, on their experiences as immunocompetent people. and many clinical trials have been conducted to We encouraged participants to provide additional show the effectiveness of different comments. forms of treatment.6-14 It should be We entered the survey responses well-known in the health care cominto a database with each demoNo research has munity what types of treatment and graphic factor and possible been conducted to medications can be used, but no response entered as “yes,” “no,” determine which research has been conducted to “not applicable” or “blank.” We medications and types placed many of the “other” determine which are being prescribed or recommended in everyday responses that were synonymous of treatment are practice. Through a postal questionwith the remaining choices probeing prescribed or naire survey, we sought to detervided into the appropriate caterecommended in mine how dentists, pharmacists and gory. When many respondents gave everyday practice. family physicians respond to similar responses in the “other” inquiries about cold sores and what category, we treated the similar were their choices of treatment response as a new separate catemodalities and medications. We also wanted to gory. Not all respondents ranked their choices find out what treatment strategies are most suitwhen they selected more than one, so we did not able in a practical setting, as health care profestabulate a ranking of responses. The total persionals communicate directly with people who centages for each question could be more or less have cold sores. than 100 percent, as we allowed respondents to give multiple responses and some respondents METHODS left questions blank. We designed and conducted the survey to maximize validity and response rates.15,16 With approval from the University of Alberta Health Research Ethics Board, we mailed a pretested and modified one-page survey to a random sample of active dentists, pharmacists and physicians in the province of Alberta, Canada. We included prestamped return envelopes and enclosed a cover letter that included the names of the researchers in case participants had questions or concerns. The cover letter also explained the purpose of the survey, that ethics approval had been granted and that we had the cooperation of professional societies. A proportionate random sample of 201 dentists, 398 pharmacists and 399 physicians was chosen from computerized databases provided by the professional groups for each of health care professions. No follow-up surveys were mailed to the selected health care professionals, as the surveys had no codes printed on them and participants’ names were not required.
RESULTS
The response rate overall was 51 percent; it was 41 percent for dentists, 60 percent for pharmacists and 48 percent for physicians (Table 1). Twenty-nine percent of the dentists were women, and 69 percent were men. Among pharmacists, 46 percent were women, and 47 percent were men, while among physicians, 33 percent were women, and 58 percent were men. The lengths of time in practice for the three professional groups were similar and averaged 17 years ± 11 years standard deviation. Ninety percent of the dentists, 53 percent of the pharmacists and 66 percent of the physicians came from urban areas (50,000 people or more). Not all respondents provided information for each demographic category. The frequency of receiving patients’ inquiries about cold sores was most prevalent for pharmacists; 30 percent were asked for information more than 10 times per month (Table 2). Dentists and
JADA, Vol. 135, January 2004 Copyright ©2004 American Dental Association. All rights reserved.
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R E S E A R C H
TABLE 1
lactic antiviral therapy (44 percent) DEMOGRAPHICS BY PROFESSIONAL GROUP.* and stress reduction (41 percent) were PHYSICIANS DENTISTS PHARMACISTS TOTAL VARIABLE recommended. 510 (51) These choices were 240 (60) 187 (48) Response Rate 83 (41) (n [%]) similar for the dentist, pharmacist and Sex (n [%]) physician groups. 110 (46) 196 (38) Female 62 (33) 24 (29) Treatment modal112 (47) 277 (54) Male 108 (58) 57 (69) ities recommended for patients who 17 ± 11 17 ± 11 Years in Practice ± 17 ± 12 17 ± 10 Standard Deviation inquired about cold sores would, of Practice Location (n [%]) necessity, differ for each patient, and, 327 (64) Urban† 124 (66) 128 (53) 75 (90) consequently, each 148 (29) 95 (40) Rural 6 (7) 47 (25) health care profes* Respondents were able to select more than one option for some questions, which is why the overall percentage for sional may have some categories may not equal 100 percent. made different rec† Urban: Areas with populations of 50,000 people or more. ommendations TABLE 2 based on individual patient needs COLD SORE INQUIRIES FROM PATIENTS.* (Figure 1, page 52). NUMBER OF DENTISTS PHYSICIANS TOTAL PHARMACISTS Topical antiviral INQUIRIES (N [%]) (N [%]) (N [%]) (N [%]) therapy was the 132 (71) 92 (38) 295 (58) One to Five per 71 (86) most common recMonth ommendation, with 51 (27) 71 (30) 128 (25) Six to 10 per Month 6 (7) physicians (80 percent) and dentists 3 (2) 72 (30) 76 (15) More Than 10 per 1 (1) Month (72 percent) making it their top choice. 4 (2) 12 (2) Never 1 (1) 7 (8) OTC medications * Respondents were able to select more than one option for some questions, which is why the overall percentage for were the first choice some categories may not equal 100 percent. of pharmacists (83 percent), with denphysicians, however, received this number of tists (15 percent) and physicians (16 percent) requests infrequently. When we asked members being less likely to recommend the OTC medicaof all three professional groups about cold sores, tions. Oral antiviral therapy was recommended more than 90 percent indicated that they received by 57 percent of physicians, 35 percent at least one inquiry per month. of dentists and 24 percent of pharmacists. Home The primary concerns about and trigger factors remedies were chosen 5 to 9 percent of the time, for cold sores, as reported by patients, were simiand dentists were twice as likely to select the lar for each health care group (Table 3). Sixty per“other” category than were pharmacists or cent of patients cited emotional stress, 47 percent physicians. cited illness or trauma and 45 percent cited sun Antiviral medications prescribed or recomexposure. The major patient concerns reported mended by health care professionals are shown in were pain or discomfort (81 percent), social Figure 2 (page 52). Fifty-eight percent of dentists, stigma (61 percent) and transmission risk (15 69 percent of pharmacists and 51 percent of percent). physicians said acyclovir ointment was their first Health care professionals’ recommendations for choice of antiviral drug. Acyclovir cream (31 persuppression of recurrent lesions are provided in cent), oral acyclovir (31 percent), famciclovir (21 Table 4. Use of sunscreen (48 percent), prophypercent) and valacyclovir (16 percent) were other 50
JADA, Vol. 135, January 2004 Copyright ©2004 American Dental Association. All rights reserved.
R E S E A R C H
common choices. TABLE 3 OTC medicaPATIENT-REPORTED TRIGGER FACTORS FOR AND tions recomPRIMARY CONCERN ABOUT COLD SORES.* mended by health care proPHARMACISTS PHYSICIANS VARIABLE DENTIST TOTAL (N [%]) (N [%]) (N [%]) (N [%]) fessionals are shown in Figure Trigger Factor 3. Lipactin gel cold sore treat304 (60) 117 (63) 135 (57) 52 (64) Emotional stress ment (Novartis 238 (47) 102 (55) 103 (43) 33 (41) Illness or trauma Consumer 226 (45) 82 (44) 108 (45) 36 (44) Sun exposure Health Canada, Mississauga, 58 (11) 24 (13) 28 (12) 6 (7) None Ontario, 41 (8) 11 (6) 25 (11) 5 (6) Canada) was rec- Other Primary Concern ommended most (50 percent), and Pain or discomfort 412 (81) 158 (85) 188 (79) 66 (81) it was chosen 308 (61) 97 (52) 171 (72) 40 (49) Social stigma primarily by 74 (15) 39 (21) 26 (11) 9 (11) Transmission risk pharmacists (87 percent). Zilactin Other 5 (1) 2 (1) 1 (1) 2 (2) cold sore treat* Respondents were able to select more than one option for some questions, which is why the overall percentage for ment (Zila, some categories may not equal 100 percent. Phoenix) was recommended TABLE 4 the second most (22 percent). RECOMMENDATIONS FOR SUPPRESSION OF RECURRENT Dentists (55 per- LESIONS.* cent) and physiPHYSICIANS RECOMMENDATION DENTIST TOTAL PHARMACISTS cians (71 per(N [%]) (N [%]) (N [%]) (N [%]) cent) were less 238 (48) 83 (46) Use of Sunscreen 131 (55) 24 (30) likely to recommend OTC treat- Prophylactic 218 (44) 100 (56) 89 (38) 29 (36) Antiviral Therapy ment than were pharmacists 203 (41) 38 (48) 68 (38) Stress Reduction 97 (41) (> 80 percent). 57 (11) 7 (9) 18 (10) Other 32 (14) Reasons for 7 (4) Nothing 6 (3) 9 (11) 22 (4) not prescribing antiviral drugs * Respondents were able to select more than one option for some questions, which is why the overall percentage for some categories may not equal 100 percent. were cost (73 percent), with more than 80 percent of pharmacists and physiserious consequences. Prescription medication, cians citing this as a factor (Figure 4, page 53). OTC treatments and home remedies are commonLack of effectiveness (29 percent), antiviral drug place internationally, but most people who have resistance (14 percent) and side effects (10 perRHL look for preventive measures or an approach cent) were less likely to be an issue. Dentists’ that reduces healing time and minimizes pain. number one reason for not prescribing antiviral They also look for advice from those in a position drugs was lack of effectiveness (45 percent). of experience and knowledge such as dentists and physicians. However, given that RHL may be a DISCUSSION secondary issue when patients have contact with their dentists or physicians, they are more likely While RHL is a low-grade infection, it is to ask pharmacists who are more accessible when extremely widespread and sometimes can have their need is immediate. This pattern is borne out JADA, Vol. 135, January 2004 Copyright ©2004 American Dental Association. All rights reserved.
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PERCENTAGE
R E S E A R C H
90 80 70 60 50 40 30 20 10 0
Dentists Pharmacists Physicians
Topical Over-the Antiviral counter Therapy Medications
Oral Home Antiviral Remedies Therapy
None
Other
TREATMENT
Figure 1. Treatment modalities recommended by health care professionals.
80 70
PERCENTAGE
60 50
Dentists
40
Pharmacists Physicians
30 20 10 0 Acyclovir Ointment
Acyclovir Cream
Oral Famciclovir Valacyclovir Acyclovir
Other
Penciclovir
ANTIVIRAL DRUG
PERCENTAGE
Figure 2. Antiviral drugs prescribed or recommended by health care professionals.
100 80
Dentists
60 40
Pharmacists
20
Physicians
0 Lipactin Gel
None
Zilactin
Other
Cepacol Viractin Gel
OVER-THE-COUNTER MEDICATION
Figure 3. Over-the-counter medications recommended by health care professionals. Lipactin gel is manufactured by Novartis Consumer Health Canada, Mississauga, Ontario, Canada; Zilactin is manufactured by Zila, Phoenix; Cepacol Viractin gel manufactured by Combe, White Plains, N.Y.
by our findings, as pharmacists reported being asked questions about cold sores much more frequently than did dentists and physicians, though all groups received inquiries on a regular basis. This is in contrast to another study in which people who had cold sores reported having sought treatment from a physician (54 percent) more often than from a dentist (17 percent) or pharmacist (29 percent).17 Treatments recommended by each group of 52
health care professionals in our study varied; dentists’ and physicians’ first preference was topical antiviral therapy, whereas pharmacists said they recommended OTC medications more often. As pharmacists are unable to prescribe medications, and as people are likely to approach pharmacists while they have a cold sore, the need for immediate action may account for pharmacists’ tendency to recommend OTC products. Professionals are affected by their scope of responsibility and patient goals; therefore, pharmacists may prefer OTC treatments, while dentists are more concerned about specific dental problems, and physicians are geared toward providing treatment. A survey in the United Kingdom showed that patients had a positive attitude toward their physicians when the physicians discussed and recommended OTC drugs, but patients were more hostile toward OTC drug recommendations made by pharmacists.18 Since an increasing variety of OTC products are available and, therefore, the potential for drug interactions is rising, dentists and physicians should inquire about OTC drug usage more frequently before prescribing antiviral drugs. Docosonal, the first OTC medication approved by the U.S. Food and Drug Administration for the treatment of RHL, was not available in Alberta at the time this survey was conducted. The trigger factors reported by patients to each professional health care group were similar. Emotional stress was the factor reported most often, while illness or trauma and sun exposure were mentioned with almost equal frequency. Contrary to our findings, patients in other studies have reported that sun exposure (63 percent) was the major trigger as compared with stress (15 percent).17 This implies that patients have set ideas as to what causes their cold sores (usually based on recurrent patterns), while they have different expectations of each group of health care professionals. Dentists, pharmacists and physicians reported that the primary concern (81 percent) for patients seeking treatment was pain or discomfort. Social stigma was of concern to patients, with 61 percent telling their health care providers that it was a major issue. This suggests that health care professionals should not focus on treating only the disease but that they should consider the patient’s needs on a psychological level as well. Each professional group’s first choice of a prescribed or recommended medication was acyclovir ointment. Acyclovir cream and oral acyclovir were
JADA, Vol. 135, January 2004 Copyright ©2004 American Dental Association. All rights reserved.
R E S E A R C H
PERCENTAGE
prescribed or recommended equally as the second most common antiviral 90 drug choice. Acyclovir therapy was 80 reported by patients in a small study 70 in the United Kingdom to be the most 60 Dentists 50 common treatment modality.17 In our Pharmacists 40 Physicians study, famciclovir was the next most 30 common medication, and it was 20 chosen primarily by physicians who 10 were more than twice as likely to pre0 Cost Lack of Antiviral Side Other scribe this medication than were pharEffectiveness Drug Effects Resistance macists and seven times as likely than REASON were dentists. A similar pattern emerged for valacyclovir. Health care professionals’ selecting penciclovir Figure 4. Health care professionals’ reasons for not prescribing antiviral was almost nonexistent, as, despite a drugs. report of positive results in a recent penciclovir study,19 it is not available and obtaining appropriate survey samples in Canada. through randomization. The response rate for The main OTC medication recommended (50 dentists was lower than that of the other two percent) was Lipactin gel; it was recommended groups. Therefore, given that we sampled a primarily by pharmacists (87 percent). Zilactin smaller number of dentists to conform to the fact was the next choice, but it was chosen by 50 perthat their population was one-half the size of the cent less of the respondents. Fifty-four percent of other groups, the variability of their overall dentists and 69 percent of physicians did not recresponses would be greater. The response rate of ommend OTC treatment. The pattern for recomdentists to postal questionnaires can vary from 17 mending OTC treatment is understandable, given to 100 percent, depending on the questionnaire that pharmacists are more likely than dentists subject, incentives offered and the length of the and physicians to see customers when they have questionnaire.20 The lower response rate from cold sores. dentists may be because they are less likely to The primary reason pharmacists and physiencounter questions from patients about cold cians cited for not prescribing antiviral drugs was sores. cost. For dentists, the primary reason they cited In addition, the survey form was limited, owing for not prescribing antiviral drugs was lack of to space and timing considerations. We encoureffectiveness, with cost being a secondary issue. aged participants to be flexible, and this was This may be because dentists are less likely to be noticeable in the response patterns and from comprescribing the drugs than are physicians, and ments made by 13 percent of respondents. Participharmacists are more aware of prices because pants contributed valuable information and interthey receive payment at time of purchase. As esting anecdotal asides (particularly those who drug coverage is optional on Alberta health care had had cold sores), which could provide assistinsurance plans, some patients are underinsured, ance for further surveys or focus groups. which means they have to pay more of drug costs Few similar surveys have been conducted to out of pocket. With cost being the major reason determine trends and patterns of treatment for not prescribing antiviral drugs, our findings among these three health professions. One study suggest that health care professionals are sensiused the same method of a mailed questionnaire tive toward financial concerns when providing to determine attitudes of general practitioners, treatment. pharmacists and consultant geriatricians on the Although the response rate to this survey was use of sugar-free and sugar-containing medicines very high compared with those of other surveys of for the elderly.21 health care professionals, the validity of the The development and marketing of new drugs results still can be an issue, despite the fact that or OTC products are dependent on surveys of conwe followed appropriate methodologies such as sumers and health care professionals. Informaobtaining accurate lists, conducting pilot projects tion from surveys can contribute to clinical guideJADA, Vol. 135, January 2004 Copyright ©2004 American Dental Association. All rights reserved.
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ment of Dentistry, University of Alberta, Edmonton, Alberta, Canada, and Medivir AB, Huddinge, Sweden.
Dr. Raborn is a professor, Department of Dentistry, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta, Canada T6G 2N8, e-mail “wayne. [email protected]”. Address reprint requests to Dr. Raborn.
Ms. Chan is a practicing dental hygienist in Calgary, Alberta, Canada.
Dr. Grace is a clinical professor, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta, Canada.
lines, while making professionals more aware of consumers’ needs. Physicians and pharmacists have their own respective knowledge bases, and an improved partnership between these professions can help provide optimal drug therapy that is more cost-effective.22 With the increasing need for interdisciplinary collaboration, it is important that dentists, pharmacists and physicians communicate with one another to achieve quality patient care. The overall response rate of 51 percent shows a clear interest in the issue of cold sores, enough that RHL should be a topic for continuing education programs. The willingness of so many professionals to cooperate demonstrates that they encounter people who have cold sores on a regular basis, and they would like to be better informed to assist these patients. CONCLUSIONS
The response rate for this survey was high, which suggests that there is considerable interest in RHL and its treatment. With pharmacists being more likely to receive cold sore inquiries and with ease of purchase and lower costs being important factors, the market for OTC drugs is greater than that for prescription antiviral drugs. As additional studies emerge that clearly show a significant improvement in preventing or controlling the size of cold sore lesions or lessening the length of term and pain, it will be important to share the information via refereed journals and continuing education courses and in the training of undergraduate health care professionals. ■ This project has been funded in part by GlaxoSmithKline, Mississauga, Ontario, Canada; the Associate Dean’s Research Fund, Depart-
54
1. Boon R, Bacon TH, Robey HL, et al. Antiviral susceptibilities of herpes simplex virus from immunocompetent subjects with recurrent herpes labialis: a UK-based survey. J Antimicrob Chemother 2000; 46:324-5. 2. Lowhagen GB, Bonde E, Eriksson B, Nordin P, Tunback P, Krantz I. Self-reported herpes labialis in a Swedish population. Scand J Infect Dis 2002;34(9):664-7. 3. Axell T, Liedholm R. Occurrence of recurrent herpes labialis in an adult Swedish population. Acta Odontol Scand 1990;48(2):119-23. 4. Reichart PA. Oral mucosal lesions in a representative crosssectional study of aging Germans. Community Dent Oral Epidemiol 2000;28(5):390-8. 5. Esmann J. The many challenges of facial herpes simplex virus infection. J Antimicrob Chemother 2001;47(supplement T1):17-27. 6. Evans TG, Bernstein DI, Raborn GW, Harmenberg J, Kowalski J, Spruance SL. Double-blind, randomized, placebo-controlled study of topical 5% acyclovir-1% hydrocortisone cream (ME-609) for treatment of UV radiation-induced herpes labialis. Antimicrob Agents Chemother 2002;46(6):1870-4. 7. Spruance SL, Rowe NH, Raborn GW, Thibodeau EA, D’Ambrosio JA, Bernstein DI. Peroral famciclovir in the treatment of experimental ultraviolet radiation-induced herpes simplex labialis: a double-blind, dose-ranging, placebo-controlled, multicenter trial. J Infect Dis 1999;179(2):303-10. 8. Raborn GW, Martel AY, Grace MG, McGaw WT. Oral acyclovir in prevention of herpes labialis: a randomized, double-blind, multicentered clinical trial. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;85(1):55-9. 9. Raborn GW, Martel AY, Grace MG, McGaw WT. Herpes labialis in skiers: randomized clinical trial of acyclovir cream versus placebo. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1997;84(6):641-5. 10. Raborn GW, McGaw WT, Grace M, Percy J, Samuels S. Herpes labialis treatment with acyclovir 5% modified aqueous cream: a doubleblind randomized trial. Oral Surg Oral Med Oral Pathol 1989; 67(6):676-9. 11. Raborn GW, McGaw WT, Grace M, Houle L. Herpes labialis treatment with acyclovir 5 per cent ointment. J Can Dent Assoc 1989;55(2): 135-7. 12. Raborn GW, McGaw WT, Grace M, Percy J. Treatment of herpes labialis with acyclovir: review of three clinical trials. Am J Med 1988;85(2A):39-42. 13. Raborn GW, McGaw WT, Grace M, Tyrrell LD, Samuels SM. Oral acyclovir and herpes labialis: a randomized, double-blind, placebocontrolled study. JADA 1987;115(1):38-42. 14. McGaw T, Raborn W, Grace M. Analgesics in pediatric dental surgery: relative efficacy of aluminum ibuprofen suspension and acetaminophen elixir. ASDC J Dent Child 1987;54(2):106-9. 15. Fink A. The survey kit. Thousand Oaks, Calif.: Sage; 1995:2-56. 16. Barclay S, Todd C, Finlay I, Grande G, Wyatt P. Not another questionnaire! Maximizing the response rate, predicting non-response, and assessing non-response bias in postal questionnaire studies of GPs. Fam Pract 2002;19(1):105-11. 17. Lamey PJ, Biagioni PA. Patient recognition of recrudescent herpes labialis: a clinical and virological assessment. J Dent 1996;24(5):325-7. 18. Bradley CP, Riaz A, Tobias RS, Kenkre JE, Dassu DY. Patient attitudes to over-the-counter drugs and possible professional responses to self-medication. Fam Pract 1998;15(1):44-50. 19. Raborn GW, Martel AY, Lassonde M, Lewis MAO, Boon R, Spruance SL. Worldwide Topical Penciclovir Collaborative Study Group. Effective treatment of herpes simplex labialis with penciclovir cream: combined results of two trials. JADA 2002;133:303-9. 20. Tan RT, Burke FJT. Response rates to questionnaires mailed to dentists: a review of 77 publications. Int Dent J 1997;47:349-54. 21. Baqir W, Maguire A. Doctors’ and pharmacists’ attitudes to the use of sugar-free and sugar-containing medicines in the elderly. Int J Pharm Pract 2001;9(3):177-84. 22. Hindmarsh K. Optimal drug therapy: the role of the pharmacist in bridging the gap between knowledge and action. Can J Clin Pharmacol 2001;8(supplement A):53A-4A.
JADA, Vol. 135, January 2004 Copyright ©2004 American Dental Association. All rights reserved.
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1.4 percent of the elderly population at the time of examination.4 Although there is no cure for RHL, numerous clinical trials have been conducted to find better forms of treatment and medica tions for this disease. Research also is being conducted to determine how the virus establishes or maintains a dormant state and reactivates itself within the sensory ganglia. 48
JADA, Vol. 135, January 2004 Copyright ©2004 American Dental Association. All rights reserved.
I
old sores, also known as recurrent herpes labialis, or RHL, are caused by a herpes simplex type 1 virus that remains dormant in the sensory ganglia until it is reactivated by triggers such as sun exposure, stress, and illness or trauma. RHL is a viral infection that affects an esti mated one-third of the world’s population1 and can cause pain, disfigurement and embarrassPharmacists ment to the patient. In a Swedish population of people between birth and 60 years are more likely of age, it was noted that 26.6 percent than dentists reported having a history of RHL and and physicians 19.45 percent reported having a recurrent to see episode during the past two years.2 A customers study of more than 20,000 Swedes had RHL at the when they reported that 3.1 percent time of assessment.3 More recently, a have cold German study reported that RHL was sores. reported in 1.3 percent of the adult and
T
G. WAYNE RABORN, D.D.S., M.S.; KAREN S. CHAN, B.Sc., R.D.H.; MICHAEL GRACE, Ph.D.
Background. The authors conducted a survey to determine how health care professionals respond to A D A J patients’ inquiries about ✷ ✷ cold sores, also known as recurrent herpes labialis, and their choices of treatN C U U ment modalities and IN G ED A medications. RT ICLE Methods. The authors mailed a one-page, pretested survey to a random sample of dentists, pharmacists and family physicians in Alberta, Canada. After receiving ethics approval from the University of Alberta, Edmonton, the authors mailed 998 surveys. The response rate was 51 percent. Results. Topical antiviral medication was the most common treatment recommended (63 percent). Over-the-counter medication was the first choice for pharmacists (83 percent) as compared with dentists (15 percent) and physicians (16 percent). Emotional stress (60 percent) was reported by patients to be the most common trigger, and pain or discomfort (81 percent) was their primary concern. Acyclovir ointment was the most common antiviral drug recommended or prescribed by health care professionals (60 percent), and cost was the major reason they gave for not recommending or prescribing antiviral drugs (73 percent). Conclusions. The authors found variation in treatment modalities and recommendations by each health profession, despite the fact that patients reported similar triggers and concerns. This may be due to individual patient need and the health care professional’s lack of knowledge. Practice Implications. Survey results may serve as a reference for health care professionals to use to determine how their choices of medications and treatment modalities compare with those of other practitioners. Professionals should know the benefits and limitations of all therapies, discuss them with the patients and select a treatment. CON
Treatment modalities and medication recommended by health care professionals for treating recurrent herpes labialis
ABSTRACT
IO N
E
T
S
A
E
2
R
R E S E A R C H
Antiviral drugs are the main mode of treatThe confidential survey consisted of four short ment prescribed for RHL.5 These drugs can be demographic questions and nine questions perused as an intermittent, suppressive or topical taining to the frequency of cold sore inquiries, form of therapy. A range of over-the-counter, or patient concerns, treatment modalities, and the OTC, medications may be recommended to relieve prescribing or recommending of antiviral drugs or cold sore symptoms. Various forms of alternative OTC medications. Participants selected their therapy also are available for people who have answers from choices given (multiple responses cold sores. were allowed) or wrote their own responses based Treatment modalities for RHL are numerous, on their experiences as immunocompetent people. and many clinical trials have been conducted to We encouraged participants to provide additional show the effectiveness of different comments. forms of treatment.6-14 It should be We entered the survey responses well-known in the health care cominto a database with each demoNo research has munity what types of treatment and graphic factor and possible been conducted to medications can be used, but no response entered as “yes,” “no,” determine which research has been conducted to “not applicable” or “blank.” We medications and types placed many of the “other” determine which are being prescribed or recommended in everyday responses that were synonymous of treatment are practice. Through a postal questionwith the remaining choices probeing prescribed or naire survey, we sought to detervided into the appropriate caterecommended in mine how dentists, pharmacists and gory. When many respondents gave everyday practice. family physicians respond to similar responses in the “other” inquiries about cold sores and what category, we treated the similar were their choices of treatment response as a new separate catemodalities and medications. We also wanted to gory. Not all respondents ranked their choices find out what treatment strategies are most suitwhen they selected more than one, so we did not able in a practical setting, as health care profestabulate a ranking of responses. The total persionals communicate directly with people who centages for each question could be more or less have cold sores. than 100 percent, as we allowed respondents to give multiple responses and some respondents METHODS left questions blank. We designed and conducted the survey to maximize validity and response rates.15,16 With approval from the University of Alberta Health Research Ethics Board, we mailed a pretested and modified one-page survey to a random sample of active dentists, pharmacists and physicians in the province of Alberta, Canada. We included prestamped return envelopes and enclosed a cover letter that included the names of the researchers in case participants had questions or concerns. The cover letter also explained the purpose of the survey, that ethics approval had been granted and that we had the cooperation of professional societies. A proportionate random sample of 201 dentists, 398 pharmacists and 399 physicians was chosen from computerized databases provided by the professional groups for each of health care professions. No follow-up surveys were mailed to the selected health care professionals, as the surveys had no codes printed on them and participants’ names were not required.
RESULTS
The response rate overall was 51 percent; it was 41 percent for dentists, 60 percent for pharmacists and 48 percent for physicians (Table 1). Twenty-nine percent of the dentists were women, and 69 percent were men. Among pharmacists, 46 percent were women, and 47 percent were men, while among physicians, 33 percent were women, and 58 percent were men. The lengths of time in practice for the three professional groups were similar and averaged 17 years ± 11 years standard deviation. Ninety percent of the dentists, 53 percent of the pharmacists and 66 percent of the physicians came from urban areas (50,000 people or more). Not all respondents provided information for each demographic category. The frequency of receiving patients’ inquiries about cold sores was most prevalent for pharmacists; 30 percent were asked for information more than 10 times per month (Table 2). Dentists and
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TABLE 1
lactic antiviral therapy (44 percent) DEMOGRAPHICS BY PROFESSIONAL GROUP.* and stress reduction (41 percent) were PHYSICIANS DENTISTS PHARMACISTS TOTAL VARIABLE recommended. 510 (51) These choices were 240 (60) 187 (48) Response Rate 83 (41) (n [%]) similar for the dentist, pharmacist and Sex (n [%]) physician groups. 110 (46) 196 (38) Female 62 (33) 24 (29) Treatment modal112 (47) 277 (54) Male 108 (58) 57 (69) ities recommended for patients who 17 ± 11 17 ± 11 Years in Practice ± 17 ± 12 17 ± 10 Standard Deviation inquired about cold sores would, of Practice Location (n [%]) necessity, differ for each patient, and, 327 (64) Urban† 124 (66) 128 (53) 75 (90) consequently, each 148 (29) 95 (40) Rural 6 (7) 47 (25) health care profes* Respondents were able to select more than one option for some questions, which is why the overall percentage for sional may have some categories may not equal 100 percent. made different rec† Urban: Areas with populations of 50,000 people or more. ommendations TABLE 2 based on individual patient needs COLD SORE INQUIRIES FROM PATIENTS.* (Figure 1, page 52). NUMBER OF DENTISTS PHYSICIANS TOTAL PHARMACISTS Topical antiviral INQUIRIES (N [%]) (N [%]) (N [%]) (N [%]) therapy was the 132 (71) 92 (38) 295 (58) One to Five per 71 (86) most common recMonth ommendation, with 51 (27) 71 (30) 128 (25) Six to 10 per Month 6 (7) physicians (80 percent) and dentists 3 (2) 72 (30) 76 (15) More Than 10 per 1 (1) Month (72 percent) making it their top choice. 4 (2) 12 (2) Never 1 (1) 7 (8) OTC medications * Respondents were able to select more than one option for some questions, which is why the overall percentage for were the first choice some categories may not equal 100 percent. of pharmacists (83 percent), with denphysicians, however, received this number of tists (15 percent) and physicians (16 percent) requests infrequently. When we asked members being less likely to recommend the OTC medicaof all three professional groups about cold sores, tions. Oral antiviral therapy was recommended more than 90 percent indicated that they received by 57 percent of physicians, 35 percent at least one inquiry per month. of dentists and 24 percent of pharmacists. Home The primary concerns about and trigger factors remedies were chosen 5 to 9 percent of the time, for cold sores, as reported by patients, were simiand dentists were twice as likely to select the lar for each health care group (Table 3). Sixty per“other” category than were pharmacists or cent of patients cited emotional stress, 47 percent physicians. cited illness or trauma and 45 percent cited sun Antiviral medications prescribed or recomexposure. The major patient concerns reported mended by health care professionals are shown in were pain or discomfort (81 percent), social Figure 2 (page 52). Fifty-eight percent of dentists, stigma (61 percent) and transmission risk (15 69 percent of pharmacists and 51 percent of percent). physicians said acyclovir ointment was their first Health care professionals’ recommendations for choice of antiviral drug. Acyclovir cream (31 persuppression of recurrent lesions are provided in cent), oral acyclovir (31 percent), famciclovir (21 Table 4. Use of sunscreen (48 percent), prophypercent) and valacyclovir (16 percent) were other 50
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R E S E A R C H
common choices. TABLE 3 OTC medicaPATIENT-REPORTED TRIGGER FACTORS FOR AND tions recomPRIMARY CONCERN ABOUT COLD SORES.* mended by health care proPHARMACISTS PHYSICIANS VARIABLE DENTIST TOTAL (N [%]) (N [%]) (N [%]) (N [%]) fessionals are shown in Figure Trigger Factor 3. Lipactin gel cold sore treat304 (60) 117 (63) 135 (57) 52 (64) Emotional stress ment (Novartis 238 (47) 102 (55) 103 (43) 33 (41) Illness or trauma Consumer 226 (45) 82 (44) 108 (45) 36 (44) Sun exposure Health Canada, Mississauga, 58 (11) 24 (13) 28 (12) 6 (7) None Ontario, 41 (8) 11 (6) 25 (11) 5 (6) Canada) was rec- Other Primary Concern ommended most (50 percent), and Pain or discomfort 412 (81) 158 (85) 188 (79) 66 (81) it was chosen 308 (61) 97 (52) 171 (72) 40 (49) Social stigma primarily by 74 (15) 39 (21) 26 (11) 9 (11) Transmission risk pharmacists (87 percent). Zilactin Other 5 (1) 2 (1) 1 (1) 2 (2) cold sore treat* Respondents were able to select more than one option for some questions, which is why the overall percentage for ment (Zila, some categories may not equal 100 percent. Phoenix) was recommended TABLE 4 the second most (22 percent). RECOMMENDATIONS FOR SUPPRESSION OF RECURRENT Dentists (55 per- LESIONS.* cent) and physiPHYSICIANS RECOMMENDATION DENTIST TOTAL PHARMACISTS cians (71 per(N [%]) (N [%]) (N [%]) (N [%]) cent) were less 238 (48) 83 (46) Use of Sunscreen 131 (55) 24 (30) likely to recommend OTC treat- Prophylactic 218 (44) 100 (56) 89 (38) 29 (36) Antiviral Therapy ment than were pharmacists 203 (41) 38 (48) 68 (38) Stress Reduction 97 (41) (> 80 percent). 57 (11) 7 (9) 18 (10) Other 32 (14) Reasons for 7 (4) Nothing 6 (3) 9 (11) 22 (4) not prescribing antiviral drugs * Respondents were able to select more than one option for some questions, which is why the overall percentage for some categories may not equal 100 percent. were cost (73 percent), with more than 80 percent of pharmacists and physiserious consequences. Prescription medication, cians citing this as a factor (Figure 4, page 53). OTC treatments and home remedies are commonLack of effectiveness (29 percent), antiviral drug place internationally, but most people who have resistance (14 percent) and side effects (10 perRHL look for preventive measures or an approach cent) were less likely to be an issue. Dentists’ that reduces healing time and minimizes pain. number one reason for not prescribing antiviral They also look for advice from those in a position drugs was lack of effectiveness (45 percent). of experience and knowledge such as dentists and physicians. However, given that RHL may be a DISCUSSION secondary issue when patients have contact with their dentists or physicians, they are more likely While RHL is a low-grade infection, it is to ask pharmacists who are more accessible when extremely widespread and sometimes can have their need is immediate. This pattern is borne out JADA, Vol. 135, January 2004 Copyright ©2004 American Dental Association. All rights reserved.
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PERCENTAGE
R E S E A R C H
90 80 70 60 50 40 30 20 10 0
Dentists Pharmacists Physicians
Topical Over-the Antiviral counter Therapy Medications
Oral Home Antiviral Remedies Therapy
None
Other
TREATMENT
Figure 1. Treatment modalities recommended by health care professionals.
80 70
PERCENTAGE
60 50
Dentists
40
Pharmacists Physicians
30 20 10 0 Acyclovir Ointment
Acyclovir Cream
Oral Famciclovir Valacyclovir Acyclovir
Other
Penciclovir
ANTIVIRAL DRUG
PERCENTAGE
Figure 2. Antiviral drugs prescribed or recommended by health care professionals.
100 80
Dentists
60 40
Pharmacists
20
Physicians
0 Lipactin Gel
None
Zilactin
Other
Cepacol Viractin Gel
OVER-THE-COUNTER MEDICATION
Figure 3. Over-the-counter medications recommended by health care professionals. Lipactin gel is manufactured by Novartis Consumer Health Canada, Mississauga, Ontario, Canada; Zilactin is manufactured by Zila, Phoenix; Cepacol Viractin gel manufactured by Combe, White Plains, N.Y.
by our findings, as pharmacists reported being asked questions about cold sores much more frequently than did dentists and physicians, though all groups received inquiries on a regular basis. This is in contrast to another study in which people who had cold sores reported having sought treatment from a physician (54 percent) more often than from a dentist (17 percent) or pharmacist (29 percent).17 Treatments recommended by each group of 52
health care professionals in our study varied; dentists’ and physicians’ first preference was topical antiviral therapy, whereas pharmacists said they recommended OTC medications more often. As pharmacists are unable to prescribe medications, and as people are likely to approach pharmacists while they have a cold sore, the need for immediate action may account for pharmacists’ tendency to recommend OTC products. Professionals are affected by their scope of responsibility and patient goals; therefore, pharmacists may prefer OTC treatments, while dentists are more concerned about specific dental problems, and physicians are geared toward providing treatment. A survey in the United Kingdom showed that patients had a positive attitude toward their physicians when the physicians discussed and recommended OTC drugs, but patients were more hostile toward OTC drug recommendations made by pharmacists.18 Since an increasing variety of OTC products are available and, therefore, the potential for drug interactions is rising, dentists and physicians should inquire about OTC drug usage more frequently before prescribing antiviral drugs. Docosonal, the first OTC medication approved by the U.S. Food and Drug Administration for the treatment of RHL, was not available in Alberta at the time this survey was conducted. The trigger factors reported by patients to each professional health care group were similar. Emotional stress was the factor reported most often, while illness or trauma and sun exposure were mentioned with almost equal frequency. Contrary to our findings, patients in other studies have reported that sun exposure (63 percent) was the major trigger as compared with stress (15 percent).17 This implies that patients have set ideas as to what causes their cold sores (usually based on recurrent patterns), while they have different expectations of each group of health care professionals. Dentists, pharmacists and physicians reported that the primary concern (81 percent) for patients seeking treatment was pain or discomfort. Social stigma was of concern to patients, with 61 percent telling their health care providers that it was a major issue. This suggests that health care professionals should not focus on treating only the disease but that they should consider the patient’s needs on a psychological level as well. Each professional group’s first choice of a prescribed or recommended medication was acyclovir ointment. Acyclovir cream and oral acyclovir were
JADA, Vol. 135, January 2004 Copyright ©2004 American Dental Association. All rights reserved.
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PERCENTAGE
prescribed or recommended equally as the second most common antiviral 90 drug choice. Acyclovir therapy was 80 reported by patients in a small study 70 in the United Kingdom to be the most 60 Dentists 50 common treatment modality.17 In our Pharmacists 40 Physicians study, famciclovir was the next most 30 common medication, and it was 20 chosen primarily by physicians who 10 were more than twice as likely to pre0 Cost Lack of Antiviral Side Other scribe this medication than were pharEffectiveness Drug Effects Resistance macists and seven times as likely than REASON were dentists. A similar pattern emerged for valacyclovir. Health care professionals’ selecting penciclovir Figure 4. Health care professionals’ reasons for not prescribing antiviral was almost nonexistent, as, despite a drugs. report of positive results in a recent penciclovir study,19 it is not available and obtaining appropriate survey samples in Canada. through randomization. The response rate for The main OTC medication recommended (50 dentists was lower than that of the other two percent) was Lipactin gel; it was recommended groups. Therefore, given that we sampled a primarily by pharmacists (87 percent). Zilactin smaller number of dentists to conform to the fact was the next choice, but it was chosen by 50 perthat their population was one-half the size of the cent less of the respondents. Fifty-four percent of other groups, the variability of their overall dentists and 69 percent of physicians did not recresponses would be greater. The response rate of ommend OTC treatment. The pattern for recomdentists to postal questionnaires can vary from 17 mending OTC treatment is understandable, given to 100 percent, depending on the questionnaire that pharmacists are more likely than dentists subject, incentives offered and the length of the and physicians to see customers when they have questionnaire.20 The lower response rate from cold sores. dentists may be because they are less likely to The primary reason pharmacists and physiencounter questions from patients about cold cians cited for not prescribing antiviral drugs was sores. cost. For dentists, the primary reason they cited In addition, the survey form was limited, owing for not prescribing antiviral drugs was lack of to space and timing considerations. We encoureffectiveness, with cost being a secondary issue. aged participants to be flexible, and this was This may be because dentists are less likely to be noticeable in the response patterns and from comprescribing the drugs than are physicians, and ments made by 13 percent of respondents. Participharmacists are more aware of prices because pants contributed valuable information and interthey receive payment at time of purchase. As esting anecdotal asides (particularly those who drug coverage is optional on Alberta health care had had cold sores), which could provide assistinsurance plans, some patients are underinsured, ance for further surveys or focus groups. which means they have to pay more of drug costs Few similar surveys have been conducted to out of pocket. With cost being the major reason determine trends and patterns of treatment for not prescribing antiviral drugs, our findings among these three health professions. One study suggest that health care professionals are sensiused the same method of a mailed questionnaire tive toward financial concerns when providing to determine attitudes of general practitioners, treatment. pharmacists and consultant geriatricians on the Although the response rate to this survey was use of sugar-free and sugar-containing medicines very high compared with those of other surveys of for the elderly.21 health care professionals, the validity of the The development and marketing of new drugs results still can be an issue, despite the fact that or OTC products are dependent on surveys of conwe followed appropriate methodologies such as sumers and health care professionals. Informaobtaining accurate lists, conducting pilot projects tion from surveys can contribute to clinical guideJADA, Vol. 135, January 2004 Copyright ©2004 American Dental Association. All rights reserved.
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ment of Dentistry, University of Alberta, Edmonton, Alberta, Canada, and Medivir AB, Huddinge, Sweden.
Dr. Raborn is a professor, Department of Dentistry, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta, Canada T6G 2N8, e-mail “wayne. [email protected]”. Address reprint requests to Dr. Raborn.
Ms. Chan is a practicing dental hygienist in Calgary, Alberta, Canada.
Dr. Grace is a clinical professor, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Alberta, Canada.
lines, while making professionals more aware of consumers’ needs. Physicians and pharmacists have their own respective knowledge bases, and an improved partnership between these professions can help provide optimal drug therapy that is more cost-effective.22 With the increasing need for interdisciplinary collaboration, it is important that dentists, pharmacists and physicians communicate with one another to achieve quality patient care. The overall response rate of 51 percent shows a clear interest in the issue of cold sores, enough that RHL should be a topic for continuing education programs. The willingness of so many professionals to cooperate demonstrates that they encounter people who have cold sores on a regular basis, and they would like to be better informed to assist these patients. CONCLUSIONS
The response rate for this survey was high, which suggests that there is considerable interest in RHL and its treatment. With pharmacists being more likely to receive cold sore inquiries and with ease of purchase and lower costs being important factors, the market for OTC drugs is greater than that for prescription antiviral drugs. As additional studies emerge that clearly show a significant improvement in preventing or controlling the size of cold sore lesions or lessening the length of term and pain, it will be important to share the information via refereed journals and continuing education courses and in the training of undergraduate health care professionals. ■ This project has been funded in part by GlaxoSmithKline, Mississauga, Ontario, Canada; the Associate Dean’s Research Fund, Depart-
54
1. Boon R, Bacon TH, Robey HL, et al. Antiviral susceptibilities of herpes simplex virus from immunocompetent subjects with recurrent herpes labialis: a UK-based survey. J Antimicrob Chemother 2000; 46:324-5. 2. Lowhagen GB, Bonde E, Eriksson B, Nordin P, Tunback P, Krantz I. Self-reported herpes labialis in a Swedish population. Scand J Infect Dis 2002;34(9):664-7. 3. Axell T, Liedholm R. Occurrence of recurrent herpes labialis in an adult Swedish population. Acta Odontol Scand 1990;48(2):119-23. 4. Reichart PA. Oral mucosal lesions in a representative crosssectional study of aging Germans. Community Dent Oral Epidemiol 2000;28(5):390-8. 5. Esmann J. The many challenges of facial herpes simplex virus infection. J Antimicrob Chemother 2001;47(supplement T1):17-27. 6. Evans TG, Bernstein DI, Raborn GW, Harmenberg J, Kowalski J, Spruance SL. Double-blind, randomized, placebo-controlled study of topical 5% acyclovir-1% hydrocortisone cream (ME-609) for treatment of UV radiation-induced herpes labialis. Antimicrob Agents Chemother 2002;46(6):1870-4. 7. Spruance SL, Rowe NH, Raborn GW, Thibodeau EA, D’Ambrosio JA, Bernstein DI. Peroral famciclovir in the treatment of experimental ultraviolet radiation-induced herpes simplex labialis: a double-blind, dose-ranging, placebo-controlled, multicenter trial. J Infect Dis 1999;179(2):303-10. 8. Raborn GW, Martel AY, Grace MG, McGaw WT. Oral acyclovir in prevention of herpes labialis: a randomized, double-blind, multicentered clinical trial. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1998;85(1):55-9. 9. Raborn GW, Martel AY, Grace MG, McGaw WT. Herpes labialis in skiers: randomized clinical trial of acyclovir cream versus placebo. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1997;84(6):641-5. 10. Raborn GW, McGaw WT, Grace M, Percy J, Samuels S. Herpes labialis treatment with acyclovir 5% modified aqueous cream: a doubleblind randomized trial. Oral Surg Oral Med Oral Pathol 1989; 67(6):676-9. 11. Raborn GW, McGaw WT, Grace M, Houle L. Herpes labialis treatment with acyclovir 5 per cent ointment. J Can Dent Assoc 1989;55(2): 135-7. 12. Raborn GW, McGaw WT, Grace M, Percy J. Treatment of herpes labialis with acyclovir: review of three clinical trials. Am J Med 1988;85(2A):39-42. 13. Raborn GW, McGaw WT, Grace M, Tyrrell LD, Samuels SM. Oral acyclovir and herpes labialis: a randomized, double-blind, placebocontrolled study. JADA 1987;115(1):38-42. 14. McGaw T, Raborn W, Grace M. Analgesics in pediatric dental surgery: relative efficacy of aluminum ibuprofen suspension and acetaminophen elixir. ASDC J Dent Child 1987;54(2):106-9. 15. Fink A. The survey kit. Thousand Oaks, Calif.: Sage; 1995:2-56. 16. Barclay S, Todd C, Finlay I, Grande G, Wyatt P. Not another questionnaire! Maximizing the response rate, predicting non-response, and assessing non-response bias in postal questionnaire studies of GPs. Fam Pract 2002;19(1):105-11. 17. Lamey PJ, Biagioni PA. Patient recognition of recrudescent herpes labialis: a clinical and virological assessment. J Dent 1996;24(5):325-7. 18. Bradley CP, Riaz A, Tobias RS, Kenkre JE, Dassu DY. Patient attitudes to over-the-counter drugs and possible professional responses to self-medication. Fam Pract 1998;15(1):44-50. 19. Raborn GW, Martel AY, Lassonde M, Lewis MAO, Boon R, Spruance SL. Worldwide Topical Penciclovir Collaborative Study Group. Effective treatment of herpes simplex labialis with penciclovir cream: combined results of two trials. JADA 2002;133:303-9. 20. Tan RT, Burke FJT. Response rates to questionnaires mailed to dentists: a review of 77 publications. Int Dent J 1997;47:349-54. 21. Baqir W, Maguire A. Doctors’ and pharmacists’ attitudes to the use of sugar-free and sugar-containing medicines in the elderly. Int J Pharm Pract 2001;9(3):177-84. 22. Hindmarsh K. Optimal drug therapy: the role of the pharmacist in bridging the gap between knowledge and action. Can J Clin Pharmacol 2001;8(supplement A):53A-4A.
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