UNDERSTANDING THE DISEASE R O S E M A R Y E. D U F F V, D .D .S ., M.P.IH.; R IO H A R D A D E L S O N , D .D .S .; L IN D A C. N IESS EN , M .P .H ., M R.P.; W IL L IA M B. W E S C O T T , D .M -D., M .S .; KE ITH W A T K IN S , D .D .S .; R O B E R T R. R H V N E , D .D .S ., M .S.
I ih e D epartm ent of V eteran Affairs is the largest single source of h ealth care for U.S. patients w ith AIDS. VA Medical C enters provide medical tre a tm e n t for 7 percent of all reported U.S. AIDS cases.1 In 1983, the VA National AIDS Program Office, using the C enters for Disease Control reporting system , began tracking the im pact of AIDS on the VA health care system. The national office designs and m onitors VA AIDS surveillance reporting system s and databases. It also recommends policy guidelines and serves as a source of AIDS statistics obtained from the VAMCs. The centers report only cases w ithin the CDC definition of AIDS. This excludes persons w ith AIDS Related-Complex or those who are positive w ith the hum an immunodeficiency virus. (In this report, HIV-positive veterans are those patients who m ay or m ay not have symptoms associated w ith HIV. They haven’t yet developed ARC or AIDS.) Between 1983 and August 1990, VAMCs treated 10,129 AIDS patients.2 (For this report, HIV infection includes patients who are HIV positive, HIV positive with ARC or HIV positive w ith AIDS). Of 172 VAMCs, 152 nationwide treated
ABSTRACT
HIV g in g iv itis, p e r io d o n titis a n d oral c a n d id ia sis ran k as th e k e y oral sig n s o f HIV in fec tio n , a cco rd in g to th e VA S u rv eilla n ce P rogram . a t least one p atien t w ith AIDS. Between August 1988 and A ugust 1990, the national office received reports of about 200 new AIDS patients each m onth.2 More th a n h alf of the cases were seen in 10 VAMCs: New York; Miami; Los Angeles; Bronx, N.Y.; San Francisco; E ast Orange, N.J.; Houston; Brooklyn, N.Y.; San Ju a n , Puerto Rico; and Chicago.2 These figures coincide with those reported by the same cities in th e non-VA sector.3 Although m any veterans w ith HIV infection are eligible for dental care and seek these services a t VA facilities, m inim al data on oral signs are collected on the CDC reporting forms. As a result, the VA Office of D entistry had lim ited inform ation to determ ine the n atu re and im pact of the HIV epidemic on its dental services. Several studies also documented the im portance of collecting detailed data on the
oral condition of patien ts w ith HIV infection.4’7 These studies indicated th a t oral lesions occur not only in individuals w ith HIV infection, and th a t certain oral conditions, such as oral candidiasis and hairy leukoplakia, m ay have an im portant diagnostic role in the staging and tracking the infection.4'8 According to 1988 testim ony on oral lesions associated w ith HIV presented to the President’s Commission on the HIV Epidemic: “Intraoral lesions are among the first opportunistic infections th a t appear during and after the prodrom al period of HIV infection. In fact, 33 percent of p atients show evidence of oral lesions as the prim ary or initial m anifestations of infection.”9 Since veterans w ith HIV infection seek routine dental care for HIV-associated oral problems in dental services, the VA Office of D entistry, which advises and assists in establishing policy in dental services throughout the country, decided to establish an independent HIV Infection Oral Surveillance Program . D ata collected for this program would complement the national office data, docum ent oral h ealth problems and tre a tm e n t needs of the HIV-infected veterans JADA, Vol. 123, October 1992
57
TABLE 1
SINS No
Y e s
No.
°/o
Total1
18
1 ,7 1 0
82
2 ,0 7 6
3
2 ,0 0 8
97
2 ,0 6 1
152
7
1 ,9 0 9
93
2 ,8 6 1
124
6
1 ,9 3 9
94
2 ,0 6 3
Oral clinical impressions
No.
°/o
Hairy leukoplakia
366 53
Herpes simplex recurrent Kaposi’s sarcoma
Herpes simplex primary
ANUG
194
9
1 ,8 6 2
91
2 ,0 5 6
HIV gingivitis
452
22
1 ,6 0 9
78
2 ,0 6 1
Periodontitis
727
35
1 ,3 9 9
65
2 ,0 6 6
HIV periodontitis
171
8
1 ,8 8 5
92
2 ,0 5 6
Recurrent aphthous ulcer
119
6
1 ,9 4 1
94
2 ,0 6 0
Angular cheilitis-oral candidiasis
211
io
1 ,8 5 7
90
2 ,0 6 8
Hyperplastic-oral candidiasis
179
9
1 ,8 8 3
91
2 ,0 6 2
Pseudomembranous-oral
433
21
1 ,6 3 5
79
2 ,0 6 8
Atrophic-oral candidiasis
168
8
1 ,8 7 4
92
2 ,0 4 2
Systemic impressions
No.
°/o
No.
°/o
Total*
Lymphadenopathy
638
31
1 ,4 2 3
69
2 ,0 6 1
Diarrhea > 1 year
388
19
1 ,6 6 9
81
2 ,0 5 5
Fewer > ■ 1 month
441
21
1 ,6 1 5
79
2 ,0 5 6
HIV encephalitis including
157
8
1 ,8 7 5
92
2 ,0 3 2
candidiasis
dementia Herpes zoster
204
IO
1 ,8 3 8
90
2 ,0 4 2
HIV wasting syndrome
383
19
1 ,6 5 9
81
2 ,0 4 2
Kaposi’s sarcoma (skin)
144
7
1 ,9 0 1
93
2 ,0 4 5
Lymphoma
56
3
1 ,9 6 8
97
2 ,0 2 4
* Totals do not equal 2,191 because of incomplete data.
and provide an objective basis for policy, planning and resource allocation decisions. We describe the developm ent of this ongoing Surveillance Program and the inform ation obtained from August 1988 through December 1990. We also report on the num ber, type and p a tte rn of distribution of oral soft tissue and periodontal problems as well as the dental 58
JADA, Vol. 123, October 1992
tre a tm e n t needs of HIV patients. BACKGROUND
In the spring of 1987, representatives from the Dental Disease Prevention Activity of the CDC, the N ational In stitu te of Dental Research, the World H ealth O rganization and the VA Office of D entistry m et to design a surveillance program th a t would collect m inim al data
on oral problems and dental treatm en t needs of individuals w ith HIV infection. The following Septem ber, the VA held a one-day training program for dentists responsible for caring for HIVinfected patients in the 12 VAMCs w ith the highest reported cases of AIDS patients. Dr. Jen s Pindborg, director of the WHO Collaborative C enter of Oral M anifestations and HIV
Infection in Copenhagen, Denmark, instructed dentists how to recognize oral problems associated with HIV. VA oral pathologists showed the dentists how to use the proposed surveillance form developed by the collaborating agencies. A pilot test conducted among these 12 facilities from September 1987 through February 1988 resulted in modifying the form to resolve reporting difficulties. The VA Office of Dentistry, in July 1988, announced the implementation of the surveillance program to representatives from all 203 VAMCs and outpatient clinics. Participation in the surveillance program by dental services personnel was voluntary but highly encouraged by the VA Office of Dentistry in Washington, D.C. METHODS AND MATERIALS
In August 1988, each VA dental clinic received copies of the revised surveillance form with directions on how to complete it. All patients with HIV infection seen in dental services, such as those who were referred from other medical services, self referrals, veterans currently receiving routine dental care, and patients seeking emergency treatment would be included in the surveillance program. Participants would receive an oral examination from the examining dentist who would complete the form for submission to the VA Office of Dentistry. Since more than 900 dentists employed by the VA were potential examiners of HIVinfected patients, training was necessary beyond the original
group of staff dentists from the high AIDS census VAMCs. The VA’s Western Dental Education Center developed and distributed to every dental service offices a set of clinical slides and written descriptions of common oral signs found in HIV-positive patients. These instructional materials were designed to assist dental staff in diagnosing oral signs of HIV. To protect participants’ confidentiality, dental staff assigned each HIV-positive participant a sequential number. This number was used rather than an identifying number. General medical information such as type of HIV infection, risk factors and systemic illnesses were extracted from the participants’ medical records. In some cases, where information was not welldocumented on the medical records, dentists obtained the information through patient interviews. Dentists conducted oral examinations by recording abnormal oral soft tissue lesions and dental treatment needs. They asked the participants about other HIV-related signs, symptoms and habits. No further attempts were made to standardize the reported findings aside from provision of uniform training and materials. Dental services periodically returned completed forms to the Office of Dentistry for data entry. The Statistical Analysis System was used in analysis and report generation. RESULTS
Between August 1988 to December 1990, 2,191 HIVinfected patients were examined by VA dentists and
included in the surveillance program. These participants were examined at 115 of the 203 dental clinics. About half the patients were white (53 percent). Blacks (33 percent), Hispanics (13 percent), Asians and American Indians/Alaskan natives (0.5 percent) made up the rest. Almost all were men (99 percent) between 20 to 78 years with a mean age of 41 years and a median age of 40. Seventynine percent were between 30 to 49 years, and 14 percent were older than 50. With respect to data on HIV risk factors, 57 percent of the participants reported a history of drug use and 37 percent were homosexual/bisexuals. Sixteen percent of the participants reported two risk factors: being homosexual/bisexual and having a history of drug use. Less than 3 percent of the participants got the infection from transfusions. The study population consisted of participants at the following stages of infection: HIV positive, 62 percent; HIV positive with ARC, 10 percent; HIV positive with AIDS, 25 percent. For 4 percent, there were no data on infection stage from either the participants or their medical records. In 49 percent of the cases, examining dentists determined the type of HIV infection and risk factors from a review of the participant’s medical record. In the rest, examiners acquired this data by patient interview. Participants sought treatment in dental services for various reasons: 28 percent were referred from other medical services, 18 percent needed emergency treatment, ê percent were self-referred for JADA, Vol. 123, October 1992
59
problem s relating to the m outh and 40 percent sought routine dental care. O ral co n d itio n s. Seventytwo percent of the surveyed veterans had a t least one oral problem associated w ith HIV. Of all the participants, 46 percent had a t least one type of periodontal disease. Periodontitis and HIV gingivitis were present in 35 and 22 percent of the participants respectively. C andidiasis was the second m ost frequent oral problem. T hirty-three of all participants had a t least one type of oral candidiasis. Specifically, pseudom em branous candidiasis (thrush) was present in 21 percent. The th ird m ost frequent oral soft tissue lesions, after periodontal and fungal infections, were viral in nature. H airy leukoplakia was reported Dr. Duffy, a in 18 percent of Commander in the all HIVU.S. Public Health Service, is a dental infected education and public veterans. health officer with Of oral the Public Health Service, Health cancers, Resources Services Kaposi’s Administration, Bureau of Health sarcoma was Professions, Division seen in 6 of Associated, Dental and Public percent of all Health Professions, participants, Dental Education and more and Special Initiatives Branch. specifically, 16 Address reprint percent of the requests to Dr. Duffy at BHPr, 5600 AIDS Fishers Lane, Room participants. 8C09, Rockville, Md Looking a t 20857. HIV-positive participants, 62 percent had one or more oral condition as opposed to 80 percent of those w ith ARC and 85 percent of 60
JADA, Vol. 123, October 1992
those w ith AIDS. S y stem ic con d ition s. Oral problems were complicated by systemic conditions. N early 60 percent of the participants had one or more of the following medical complications: lym phadenopathy, 31 percent; fever for more th an a m onth, 21 percent; HIV wasting syndrome, 19 percent; and diarrhea for more th an a year, 19 percent. As the disease progressed, systemic problems increased. Ninety-five percent of the AIDS surveillance participants had one or more systemic condition compared w ith 68 percent of the participants who were HIV positive. (Five percent of the AIDS participants didn’t report a systemic condition a t the time of the oral examination. By CDC definition, systemic symptoms m ust be present for the diagnosis of AIDS.) D en tal treatm en t n eed s. Prevalent dental treatm ent needs—prophylaxis, restorative care and oral surgery—were needed in 75, 49 and 35 percent of the HIV-infected participants respectively. Preventive procedures, particularly those related to oral hygiene, were needed in 69 percent of the participants. O ther needs included periodontic and prosthodontic treatm ent. Regardless of the infection stage, 79 percent of all the participants needed some type of oral treatm ent. O ther oral com p lain ts. M any participants reported HIV-related oral signs associated w ith pain and discomfort. Thirty-five of the participants reported oral herpes (cold sores) and 29 percent reported aphthae (canker sores). Of those with
oral herpes, nearly 10 percent reported an increase of severity and Dr. Adelson is duration in the director, Minneapolis p ast six Regional Medical Education Center in m onths. Oral Minneapolis. herpes and aphthae were more prevalent in those who did not have full blown AIDS. Additional complaints included pain on swallowing, pain in the bone and blood in the m outh—59 percent reported a t least one condition. DISCUSSION
Only a percentage of all HIVinfected veterans seen in VAMCs were reported in the surveillance program. Between August 1988 and December 1990, the VA treated 5,444 AIDS patients. D uring this same period, 2,191 HIV-infected veterans were reported to the surveillance program by the VA D ental Service. Of the 2,191 participants, 520 were diagnosed w ith AIDS—nearly 10 percent of the AIDS cases seen by the VA Medical Service. The difference between the num ber of cases reported by the VA National Office and its dental service m ay result from several factors: " V eterans were eligible for medical care but not for dental care; » HIV-positive veterans were eligible for dental care b u t had no apparent oral problems and didn’t seek care; ™ The attending physician was unaw are of oral problems and didn’t refer the patient for dental care, or the patient was referred to oral care but refused it;
■■ U nderreporting of HIVinfected veterans by the dental service for various logistical reasons. As in any surveillance system requiring clinical decisions by m any exam iners, there is the potential for variable findings. These lim itations, however, are m inim al in the VA because of standardized procedures used a t all VAMCs. Surveillance data, such as medical history, risk factors and demographics, are collected from a standard m edical record. In addition, since all exam iners are fam iliar w ith VA forms, there m ay be higher compliance in completing forms and better agreem ent in the estim ation of tre a tm e n t needs. The W estern Dental Education C enter’s m anual and clinical slides on HIV-associated oral signs possibly assisted in improving th e reliability of the findings of the oral exam ination. Also, the surveillance program , in which all exam iners were dentists, avoided problems experienced by other efforts th a t used non dental personnel to perform oral exam inations. Because there were no attem pts a t standardization, nor were th ere tests of interand intra-exam iner variability completed, some variation obviously occurred. The surveillance program collects d a ta on four types of oral candidiasis—angular cheilitis, erythem atous, chronic and pseudom em branous—and two types of herpes simplex infection. Diagnosing the v ar ious types of oral candidiasis, specifically pseudomem branous and erythem atous, are im portant in helping to
determ ine the development of AIDS and in staging and tracking the disease.4'68 For the most part, different types of candida are confirmed by clinical evaluation as opposed to laboratory confirmation. As stated earlier, the two types of herpes infection are more prevalent in participants who had not developed AIDS. Why this occurred is unknown and additional research is needed. The dental tre a tm e n t needs of the veterans are extensive w ith 79 percent of the participants requiring dental care regardless of the stage of Dr. Watkins is staff infection. The dentist, Department infection stage of Veterans Affairs Medical Center, New doesn’t appear York, and clinical to affect the assistant professor, Department of Oral need for dental Medicine and treatm en t for Pathology, New York the University, College of Dentistry. participants. B ut since these d ata are not longitudinal, nor are dental records available to determ ine the dental treatm en t needs of these participants before becoming HIV positive, and it is unknow n to w hat extent these participants received dental care a t any stage of th eir lives—no conclusion can be reached. Although two other studies report on HIV-infected m ilitary personnel, they are not directly comparable to the surveillance program .8,10 These studies correlate HIV-associated oral signs w ith the W alter Reed Staging Classification System of T4-cell counts greater or less th an 400 m illim eters. The VA Oral Surveillance
Program participants were classified by stage of HIV infection. In addition, VAMCs used its own classification of HIV disease progression based on T4-cell counts g rea ter or less th an 500 mm, plus CDC criteria for AIDS. Even if the surveillance program used T4cell counts to correlate w ith oral signs, because the VAMCs used T4-cell counts greater or less th an 500 mm, the two other studies on m ilitary personnel still wouldn’t be comparable. Also, the VA Surveillance Program reports on veterans only. Thompson and others10 reported on all active duty personnel while Swango and others8 reported on veterans, active duty personnel and dependents. Thus, the type of population examined is different. The surveillance program reported observing more HIVassociated oral signs th a n the other studies.810 The veterans who participated in the program were eligible for dental care and actively sought oral health care. They were not selected from the overall VA HIV-positive population. Studies have identified patients through m ilitary testing.810 They were not necessarily seeking dental treatm ent. As a resu lt of this selection bias, the oral care needs of the surveillance participants Dr. Niessen is chair may be of Preventive and inflated. The Community Dentistry at Baylor College of study Dentistry, Dallas. population represents a higher proportion of AIDS participants th a n the study populations in the other JADA, Vol. 123, October 1992
61
two reports.810 As a result, there m ay be a higher prevalence of HIV-associated Dr. Wescott is chief, oral signs Dental Service and because of the Oral Pathologist, DVA Medical Center, distribution of San Francisco and study adjunct professor, populations by Department of Stomatology, the stage of Division of Oral disease. Pathology, University of As new HIVCalifornia School of positive Dentistry, San patients seek Francisco. dental care from the VA, they will undoubtedly develop HIVrelated system ic and oral problems, increasing the burden on dental services. The burden m ay take the form of additional tim e or costs for personnel, supplies and drugs. Many routine dental procedures may become more complex and intensive as the patient becomes more ill. Through the surveillance program, the VA Office of D entistry can estim ate b e tte r the future needs of the HIV-positive veterans who will seek dental care. The large population of U.S. veterans provides a unique opportunity to monitor HIVinfected individuals. The VA health care system saw more th an 4 million patients in 1988, of which 525,000 were seen in dental services. Of those 525,000 p atients seen in the dental clinics, some are or will become HIV positive. Many of these p atients will receive all th eir h ealth care w ithin VAMCs.
62
JADA, Vol. 123, October 1992
The VA D ental Service has the unique ability to monitor and track oral health in various stages of HIV infection. As the HIV infection continues to increase and affect U.S. veterans, the surveillance program will enable the VA Office of D entistry to gather inform ation on oral health and tre a tm e n t needs of this population. SUMMARY AND CONCLUSIONS
D ata from the VA Surveillance Program show a population w ith considerable need for oral h ealth services. Oral care is required for problems directly related to HIV and routine dental care. Complicating the provisions of dental care are significant systemic problems. D entistry’s involvement in the treatm en t of patients with HIV includes: controlling Dr. Rhyne is director, VA Medical Center, pain and Grand Junction, suffering, and Colo. assisting patients w ith nutritional problems by m aintaining a functional oral environment. The inform ation gathered through the surveillance program helps plan m anagem ent strategies and policy to care for the growing num ber of HIV-infected veterans. The VA also hopes th a t data collected through the program provide more
understanding of this disease and dentistry’s role in caring for the victims. ■ The informed consent of all hum an subjects who participated in the experim ental investigation reported or described in this m anuscript was obtained after the natu re of the procedure and possible discomforts and risks have been explained fully. The authors th a n k the VA Office of D entistry and Dental Service for their cooperation and support for th is report and R alph Eskenazi, B.S., program analyst, VA Central Office, and Lawrence Seitz, Ph.D., m athem atical statistician, Prevention Research Branch, National Institute of Drug Abuse, for th eir assistance in the development of the VA HIV Infection O ral Surveillance Program. 1. An update on AIDS. VA P ract 1988:41;104. 2. D epartm ent of V eterans Affairs Central Office, AIDS Program Office, AIDS Gram, January/February/M arch 1991. 3. HIV/AIDS Surveillance; U.S. AIDS cases reported through Jan u ary 1991. U.S. D epartm ent of H ealth and H um an Services. Public H ealth Service Centers for Disease Control C enter for Infectious Diseases. Division of HIV/AIDS. Issued February 1991. 4. G reenspan D, G reenspan JS. M anagem ent of th e oral lesions of HIV infection. JADA 1991;122(9):26-32. 5. C handrasekar PH, Molinari JA. Oral candidiasis: forerunner of acquired immune deficiency syndrome. O ral Surg Oral Med Oral Pathol 1985;60(5):532-4. 6. G reenspan JS , G reenspan D, H earst N, et al. Relation of oral hairy leukoplakia to infection w ith th e hum an immunodeficiency virus and th e risk of developing AIDS. J Infect Dis 1987;155(3):475-81. 7. Klein RS, H arris CA, Sm all CB, Moll B, Lesser M, Friedland GH. O ral candidiasis in high-risk patients as th e initial m anifestations of AIDS. N Engl J Med 1984;311(6):354-8. 8. Swango PA, Kleinman DV, Konzelman JL. HIV and periodontal health: a study of m ilitary personnel with HIV. JADA 1991;122(8):49-54. 9. Rogers VC. Testim ony before the president’s commission on HIV epidemic. Ja n u ary 14, 1988. U.S. Government Printing Office 1988:214-701. 10. Thompson SH, Glen AC, Craig DB. Correlation of oral disease with the W alter Reed staging scheme for HIV-1 seropositive patients. O ral S urg Oral Med O ral Pathol 1992;73(3):289-92.
I ih e D epartm ent of V eteran Affairs is the largest single source of h ealth care for U.S. patients w ith AIDS. VA Medical C enters provide medical tre a tm e n t for 7 percent of all reported U.S. AIDS cases.1 In 1983, the VA National AIDS Program Office, using the C enters for Disease Control reporting system , began tracking the im pact of AIDS on the VA health care system. The national office designs and m onitors VA AIDS surveillance reporting system s and databases. It also recommends policy guidelines and serves as a source of AIDS statistics obtained from the VAMCs. The centers report only cases w ithin the CDC definition of AIDS. This excludes persons w ith AIDS Related-Complex or those who are positive w ith the hum an immunodeficiency virus. (In this report, HIV-positive veterans are those patients who m ay or m ay not have symptoms associated w ith HIV. They haven’t yet developed ARC or AIDS.) Between 1983 and August 1990, VAMCs treated 10,129 AIDS patients.2 (For this report, HIV infection includes patients who are HIV positive, HIV positive with ARC or HIV positive w ith AIDS). Of 172 VAMCs, 152 nationwide treated
ABSTRACT
HIV g in g iv itis, p e r io d o n titis a n d oral c a n d id ia sis ran k as th e k e y oral sig n s o f HIV in fec tio n , a cco rd in g to th e VA S u rv eilla n ce P rogram . a t least one p atien t w ith AIDS. Between August 1988 and A ugust 1990, the national office received reports of about 200 new AIDS patients each m onth.2 More th a n h alf of the cases were seen in 10 VAMCs: New York; Miami; Los Angeles; Bronx, N.Y.; San Francisco; E ast Orange, N.J.; Houston; Brooklyn, N.Y.; San Ju a n , Puerto Rico; and Chicago.2 These figures coincide with those reported by the same cities in th e non-VA sector.3 Although m any veterans w ith HIV infection are eligible for dental care and seek these services a t VA facilities, m inim al data on oral signs are collected on the CDC reporting forms. As a result, the VA Office of D entistry had lim ited inform ation to determ ine the n atu re and im pact of the HIV epidemic on its dental services. Several studies also documented the im portance of collecting detailed data on the
oral condition of patien ts w ith HIV infection.4’7 These studies indicated th a t oral lesions occur not only in individuals w ith HIV infection, and th a t certain oral conditions, such as oral candidiasis and hairy leukoplakia, m ay have an im portant diagnostic role in the staging and tracking the infection.4'8 According to 1988 testim ony on oral lesions associated w ith HIV presented to the President’s Commission on the HIV Epidemic: “Intraoral lesions are among the first opportunistic infections th a t appear during and after the prodrom al period of HIV infection. In fact, 33 percent of p atients show evidence of oral lesions as the prim ary or initial m anifestations of infection.”9 Since veterans w ith HIV infection seek routine dental care for HIV-associated oral problems in dental services, the VA Office of D entistry, which advises and assists in establishing policy in dental services throughout the country, decided to establish an independent HIV Infection Oral Surveillance Program . D ata collected for this program would complement the national office data, docum ent oral h ealth problems and tre a tm e n t needs of the HIV-infected veterans JADA, Vol. 123, October 1992
57
TABLE 1
SINS No
Y e s
No.
°/o
Total1
18
1 ,7 1 0
82
2 ,0 7 6
3
2 ,0 0 8
97
2 ,0 6 1
152
7
1 ,9 0 9
93
2 ,8 6 1
124
6
1 ,9 3 9
94
2 ,0 6 3
Oral clinical impressions
No.
°/o
Hairy leukoplakia
366 53
Herpes simplex recurrent Kaposi’s sarcoma
Herpes simplex primary
ANUG
194
9
1 ,8 6 2
91
2 ,0 5 6
HIV gingivitis
452
22
1 ,6 0 9
78
2 ,0 6 1
Periodontitis
727
35
1 ,3 9 9
65
2 ,0 6 6
HIV periodontitis
171
8
1 ,8 8 5
92
2 ,0 5 6
Recurrent aphthous ulcer
119
6
1 ,9 4 1
94
2 ,0 6 0
Angular cheilitis-oral candidiasis
211
io
1 ,8 5 7
90
2 ,0 6 8
Hyperplastic-oral candidiasis
179
9
1 ,8 8 3
91
2 ,0 6 2
Pseudomembranous-oral
433
21
1 ,6 3 5
79
2 ,0 6 8
Atrophic-oral candidiasis
168
8
1 ,8 7 4
92
2 ,0 4 2
Systemic impressions
No.
°/o
No.
°/o
Total*
Lymphadenopathy
638
31
1 ,4 2 3
69
2 ,0 6 1
Diarrhea > 1 year
388
19
1 ,6 6 9
81
2 ,0 5 5
Fewer > ■ 1 month
441
21
1 ,6 1 5
79
2 ,0 5 6
HIV encephalitis including
157
8
1 ,8 7 5
92
2 ,0 3 2
candidiasis
dementia Herpes zoster
204
IO
1 ,8 3 8
90
2 ,0 4 2
HIV wasting syndrome
383
19
1 ,6 5 9
81
2 ,0 4 2
Kaposi’s sarcoma (skin)
144
7
1 ,9 0 1
93
2 ,0 4 5
Lymphoma
56
3
1 ,9 6 8
97
2 ,0 2 4
* Totals do not equal 2,191 because of incomplete data.
and provide an objective basis for policy, planning and resource allocation decisions. We describe the developm ent of this ongoing Surveillance Program and the inform ation obtained from August 1988 through December 1990. We also report on the num ber, type and p a tte rn of distribution of oral soft tissue and periodontal problems as well as the dental 58
JADA, Vol. 123, October 1992
tre a tm e n t needs of HIV patients. BACKGROUND
In the spring of 1987, representatives from the Dental Disease Prevention Activity of the CDC, the N ational In stitu te of Dental Research, the World H ealth O rganization and the VA Office of D entistry m et to design a surveillance program th a t would collect m inim al data
on oral problems and dental treatm en t needs of individuals w ith HIV infection. The following Septem ber, the VA held a one-day training program for dentists responsible for caring for HIVinfected patients in the 12 VAMCs w ith the highest reported cases of AIDS patients. Dr. Jen s Pindborg, director of the WHO Collaborative C enter of Oral M anifestations and HIV
Infection in Copenhagen, Denmark, instructed dentists how to recognize oral problems associated with HIV. VA oral pathologists showed the dentists how to use the proposed surveillance form developed by the collaborating agencies. A pilot test conducted among these 12 facilities from September 1987 through February 1988 resulted in modifying the form to resolve reporting difficulties. The VA Office of Dentistry, in July 1988, announced the implementation of the surveillance program to representatives from all 203 VAMCs and outpatient clinics. Participation in the surveillance program by dental services personnel was voluntary but highly encouraged by the VA Office of Dentistry in Washington, D.C. METHODS AND MATERIALS
In August 1988, each VA dental clinic received copies of the revised surveillance form with directions on how to complete it. All patients with HIV infection seen in dental services, such as those who were referred from other medical services, self referrals, veterans currently receiving routine dental care, and patients seeking emergency treatment would be included in the surveillance program. Participants would receive an oral examination from the examining dentist who would complete the form for submission to the VA Office of Dentistry. Since more than 900 dentists employed by the VA were potential examiners of HIVinfected patients, training was necessary beyond the original
group of staff dentists from the high AIDS census VAMCs. The VA’s Western Dental Education Center developed and distributed to every dental service offices a set of clinical slides and written descriptions of common oral signs found in HIV-positive patients. These instructional materials were designed to assist dental staff in diagnosing oral signs of HIV. To protect participants’ confidentiality, dental staff assigned each HIV-positive participant a sequential number. This number was used rather than an identifying number. General medical information such as type of HIV infection, risk factors and systemic illnesses were extracted from the participants’ medical records. In some cases, where information was not welldocumented on the medical records, dentists obtained the information through patient interviews. Dentists conducted oral examinations by recording abnormal oral soft tissue lesions and dental treatment needs. They asked the participants about other HIV-related signs, symptoms and habits. No further attempts were made to standardize the reported findings aside from provision of uniform training and materials. Dental services periodically returned completed forms to the Office of Dentistry for data entry. The Statistical Analysis System was used in analysis and report generation. RESULTS
Between August 1988 to December 1990, 2,191 HIVinfected patients were examined by VA dentists and
included in the surveillance program. These participants were examined at 115 of the 203 dental clinics. About half the patients were white (53 percent). Blacks (33 percent), Hispanics (13 percent), Asians and American Indians/Alaskan natives (0.5 percent) made up the rest. Almost all were men (99 percent) between 20 to 78 years with a mean age of 41 years and a median age of 40. Seventynine percent were between 30 to 49 years, and 14 percent were older than 50. With respect to data on HIV risk factors, 57 percent of the participants reported a history of drug use and 37 percent were homosexual/bisexuals. Sixteen percent of the participants reported two risk factors: being homosexual/bisexual and having a history of drug use. Less than 3 percent of the participants got the infection from transfusions. The study population consisted of participants at the following stages of infection: HIV positive, 62 percent; HIV positive with ARC, 10 percent; HIV positive with AIDS, 25 percent. For 4 percent, there were no data on infection stage from either the participants or their medical records. In 49 percent of the cases, examining dentists determined the type of HIV infection and risk factors from a review of the participant’s medical record. In the rest, examiners acquired this data by patient interview. Participants sought treatment in dental services for various reasons: 28 percent were referred from other medical services, 18 percent needed emergency treatment, ê percent were self-referred for JADA, Vol. 123, October 1992
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problem s relating to the m outh and 40 percent sought routine dental care. O ral co n d itio n s. Seventytwo percent of the surveyed veterans had a t least one oral problem associated w ith HIV. Of all the participants, 46 percent had a t least one type of periodontal disease. Periodontitis and HIV gingivitis were present in 35 and 22 percent of the participants respectively. C andidiasis was the second m ost frequent oral problem. T hirty-three of all participants had a t least one type of oral candidiasis. Specifically, pseudom em branous candidiasis (thrush) was present in 21 percent. The th ird m ost frequent oral soft tissue lesions, after periodontal and fungal infections, were viral in nature. H airy leukoplakia was reported Dr. Duffy, a in 18 percent of Commander in the all HIVU.S. Public Health Service, is a dental infected education and public veterans. health officer with Of oral the Public Health Service, Health cancers, Resources Services Kaposi’s Administration, Bureau of Health sarcoma was Professions, Division seen in 6 of Associated, Dental and Public percent of all Health Professions, participants, Dental Education and more and Special Initiatives Branch. specifically, 16 Address reprint percent of the requests to Dr. Duffy at BHPr, 5600 AIDS Fishers Lane, Room participants. 8C09, Rockville, Md Looking a t 20857. HIV-positive participants, 62 percent had one or more oral condition as opposed to 80 percent of those w ith ARC and 85 percent of 60
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those w ith AIDS. S y stem ic con d ition s. Oral problems were complicated by systemic conditions. N early 60 percent of the participants had one or more of the following medical complications: lym phadenopathy, 31 percent; fever for more th an a m onth, 21 percent; HIV wasting syndrome, 19 percent; and diarrhea for more th an a year, 19 percent. As the disease progressed, systemic problems increased. Ninety-five percent of the AIDS surveillance participants had one or more systemic condition compared w ith 68 percent of the participants who were HIV positive. (Five percent of the AIDS participants didn’t report a systemic condition a t the time of the oral examination. By CDC definition, systemic symptoms m ust be present for the diagnosis of AIDS.) D en tal treatm en t n eed s. Prevalent dental treatm ent needs—prophylaxis, restorative care and oral surgery—were needed in 75, 49 and 35 percent of the HIV-infected participants respectively. Preventive procedures, particularly those related to oral hygiene, were needed in 69 percent of the participants. O ther needs included periodontic and prosthodontic treatm ent. Regardless of the infection stage, 79 percent of all the participants needed some type of oral treatm ent. O ther oral com p lain ts. M any participants reported HIV-related oral signs associated w ith pain and discomfort. Thirty-five of the participants reported oral herpes (cold sores) and 29 percent reported aphthae (canker sores). Of those with
oral herpes, nearly 10 percent reported an increase of severity and Dr. Adelson is duration in the director, Minneapolis p ast six Regional Medical Education Center in m onths. Oral Minneapolis. herpes and aphthae were more prevalent in those who did not have full blown AIDS. Additional complaints included pain on swallowing, pain in the bone and blood in the m outh—59 percent reported a t least one condition. DISCUSSION
Only a percentage of all HIVinfected veterans seen in VAMCs were reported in the surveillance program. Between August 1988 and December 1990, the VA treated 5,444 AIDS patients. D uring this same period, 2,191 HIV-infected veterans were reported to the surveillance program by the VA D ental Service. Of the 2,191 participants, 520 were diagnosed w ith AIDS—nearly 10 percent of the AIDS cases seen by the VA Medical Service. The difference between the num ber of cases reported by the VA National Office and its dental service m ay result from several factors: " V eterans were eligible for medical care but not for dental care; » HIV-positive veterans were eligible for dental care b u t had no apparent oral problems and didn’t seek care; ™ The attending physician was unaw are of oral problems and didn’t refer the patient for dental care, or the patient was referred to oral care but refused it;
■■ U nderreporting of HIVinfected veterans by the dental service for various logistical reasons. As in any surveillance system requiring clinical decisions by m any exam iners, there is the potential for variable findings. These lim itations, however, are m inim al in the VA because of standardized procedures used a t all VAMCs. Surveillance data, such as medical history, risk factors and demographics, are collected from a standard m edical record. In addition, since all exam iners are fam iliar w ith VA forms, there m ay be higher compliance in completing forms and better agreem ent in the estim ation of tre a tm e n t needs. The W estern Dental Education C enter’s m anual and clinical slides on HIV-associated oral signs possibly assisted in improving th e reliability of the findings of the oral exam ination. Also, the surveillance program , in which all exam iners were dentists, avoided problems experienced by other efforts th a t used non dental personnel to perform oral exam inations. Because there were no attem pts a t standardization, nor were th ere tests of interand intra-exam iner variability completed, some variation obviously occurred. The surveillance program collects d a ta on four types of oral candidiasis—angular cheilitis, erythem atous, chronic and pseudom em branous—and two types of herpes simplex infection. Diagnosing the v ar ious types of oral candidiasis, specifically pseudomem branous and erythem atous, are im portant in helping to
determ ine the development of AIDS and in staging and tracking the disease.4'68 For the most part, different types of candida are confirmed by clinical evaluation as opposed to laboratory confirmation. As stated earlier, the two types of herpes infection are more prevalent in participants who had not developed AIDS. Why this occurred is unknown and additional research is needed. The dental tre a tm e n t needs of the veterans are extensive w ith 79 percent of the participants requiring dental care regardless of the stage of Dr. Watkins is staff infection. The dentist, Department infection stage of Veterans Affairs Medical Center, New doesn’t appear York, and clinical to affect the assistant professor, Department of Oral need for dental Medicine and treatm en t for Pathology, New York the University, College of Dentistry. participants. B ut since these d ata are not longitudinal, nor are dental records available to determ ine the dental treatm en t needs of these participants before becoming HIV positive, and it is unknow n to w hat extent these participants received dental care a t any stage of th eir lives—no conclusion can be reached. Although two other studies report on HIV-infected m ilitary personnel, they are not directly comparable to the surveillance program .8,10 These studies correlate HIV-associated oral signs w ith the W alter Reed Staging Classification System of T4-cell counts greater or less th an 400 m illim eters. The VA Oral Surveillance
Program participants were classified by stage of HIV infection. In addition, VAMCs used its own classification of HIV disease progression based on T4-cell counts g rea ter or less th an 500 mm, plus CDC criteria for AIDS. Even if the surveillance program used T4cell counts to correlate w ith oral signs, because the VAMCs used T4-cell counts greater or less th an 500 mm, the two other studies on m ilitary personnel still wouldn’t be comparable. Also, the VA Surveillance Program reports on veterans only. Thompson and others10 reported on all active duty personnel while Swango and others8 reported on veterans, active duty personnel and dependents. Thus, the type of population examined is different. The surveillance program reported observing more HIVassociated oral signs th a n the other studies.810 The veterans who participated in the program were eligible for dental care and actively sought oral health care. They were not selected from the overall VA HIV-positive population. Studies have identified patients through m ilitary testing.810 They were not necessarily seeking dental treatm ent. As a resu lt of this selection bias, the oral care needs of the surveillance participants Dr. Niessen is chair may be of Preventive and inflated. The Community Dentistry at Baylor College of study Dentistry, Dallas. population represents a higher proportion of AIDS participants th a n the study populations in the other JADA, Vol. 123, October 1992
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two reports.810 As a result, there m ay be a higher prevalence of HIV-associated Dr. Wescott is chief, oral signs Dental Service and because of the Oral Pathologist, DVA Medical Center, distribution of San Francisco and study adjunct professor, populations by Department of Stomatology, the stage of Division of Oral disease. Pathology, University of As new HIVCalifornia School of positive Dentistry, San patients seek Francisco. dental care from the VA, they will undoubtedly develop HIVrelated system ic and oral problems, increasing the burden on dental services. The burden m ay take the form of additional tim e or costs for personnel, supplies and drugs. Many routine dental procedures may become more complex and intensive as the patient becomes more ill. Through the surveillance program, the VA Office of D entistry can estim ate b e tte r the future needs of the HIV-positive veterans who will seek dental care. The large population of U.S. veterans provides a unique opportunity to monitor HIVinfected individuals. The VA health care system saw more th an 4 million patients in 1988, of which 525,000 were seen in dental services. Of those 525,000 p atients seen in the dental clinics, some are or will become HIV positive. Many of these p atients will receive all th eir h ealth care w ithin VAMCs.
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The VA D ental Service has the unique ability to monitor and track oral health in various stages of HIV infection. As the HIV infection continues to increase and affect U.S. veterans, the surveillance program will enable the VA Office of D entistry to gather inform ation on oral health and tre a tm e n t needs of this population. SUMMARY AND CONCLUSIONS
D ata from the VA Surveillance Program show a population w ith considerable need for oral h ealth services. Oral care is required for problems directly related to HIV and routine dental care. Complicating the provisions of dental care are significant systemic problems. D entistry’s involvement in the treatm en t of patients with HIV includes: controlling Dr. Rhyne is director, VA Medical Center, pain and Grand Junction, suffering, and Colo. assisting patients w ith nutritional problems by m aintaining a functional oral environment. The inform ation gathered through the surveillance program helps plan m anagem ent strategies and policy to care for the growing num ber of HIV-infected veterans. The VA also hopes th a t data collected through the program provide more
understanding of this disease and dentistry’s role in caring for the victims. ■ The informed consent of all hum an subjects who participated in the experim ental investigation reported or described in this m anuscript was obtained after the natu re of the procedure and possible discomforts and risks have been explained fully. The authors th a n k the VA Office of D entistry and Dental Service for their cooperation and support for th is report and R alph Eskenazi, B.S., program analyst, VA Central Office, and Lawrence Seitz, Ph.D., m athem atical statistician, Prevention Research Branch, National Institute of Drug Abuse, for th eir assistance in the development of the VA HIV Infection O ral Surveillance Program. 1. An update on AIDS. VA P ract 1988:41;104. 2. D epartm ent of V eterans Affairs Central Office, AIDS Program Office, AIDS Gram, January/February/M arch 1991. 3. HIV/AIDS Surveillance; U.S. AIDS cases reported through Jan u ary 1991. U.S. D epartm ent of H ealth and H um an Services. Public H ealth Service Centers for Disease Control C enter for Infectious Diseases. Division of HIV/AIDS. Issued February 1991. 4. G reenspan D, G reenspan JS. M anagem ent of th e oral lesions of HIV infection. JADA 1991;122(9):26-32. 5. C handrasekar PH, Molinari JA. Oral candidiasis: forerunner of acquired immune deficiency syndrome. O ral Surg Oral Med Oral Pathol 1985;60(5):532-4. 6. G reenspan JS , G reenspan D, H earst N, et al. Relation of oral hairy leukoplakia to infection w ith th e hum an immunodeficiency virus and th e risk of developing AIDS. J Infect Dis 1987;155(3):475-81. 7. Klein RS, H arris CA, Sm all CB, Moll B, Lesser M, Friedland GH. O ral candidiasis in high-risk patients as th e initial m anifestations of AIDS. N Engl J Med 1984;311(6):354-8. 8. Swango PA, Kleinman DV, Konzelman JL. HIV and periodontal health: a study of m ilitary personnel with HIV. JADA 1991;122(8):49-54. 9. Rogers VC. Testim ony before the president’s commission on HIV epidemic. Ja n u ary 14, 1988. U.S. Government Printing Office 1988:214-701. 10. Thompson SH, Glen AC, Craig DB. Correlation of oral disease with the W alter Reed staging scheme for HIV-1 seropositive patients. O ral S urg Oral Med O ral Pathol 1992;73(3):289-92.
