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January 1996, Vol 122, No. 1 >
ARTICLE | January 1996

The Accurate Diagnosis of Oral Lesions in Human Immunodeficiency Virus Infection: Title and subTitle BreakImpact on Medical Staging FREE

Gustavo D. Cruz, DMD, MPH; Ira B. Lamster, DDS, MMSc; Melissa D. Begg, ScD; Joan A. Phelan, DDS; Jack M. Gorman, MD; Wafaa El-Sadr, MD, MPH
Arch Otolaryngol Head Neck Surg. 1996;122(1):68-73. doi:10.1001/archotol.1996.01890130060010
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Objective:  To compare identification of oral candidiasis (OC) and oral hairy leukoplakia (OHL) by medical examiners and oral/dental examiners and to assess the impact of these diagnoses on the medical staging of the human immunodeficiency virus (HIV).

Design:  Retrospective analysis of data collected by medical and oral/dental examiners at the baseline examination of a prospective study.

Setting:  Homosexual men and men and women who were parenteral drug users residing in New York City, enrolled in a longitudinal cohort study.

Subjects:  A total of 245 individuals participated in this study.

Main Outcome Measures:  The diagnoses of OC and OHL as recorded in the medical and oral/dental charts were analyzed retrospectively for the same medical and oral/dental evaluation visits. The medical staging of HIV infection based on that evaluation was analyzed concomitantly.

Results:  Among homosexual men, the oral/dental examiners diagnosed OC in 11% of the individuals and the medical examiners in 4%. In the same cohort, OHL was diagnosed by the oral/dental examiners in 14% of the individuals and by the medical examiners in 8%. Among the parenteral drug users the oral/dental examiners diagnosed OC in 29% of the individuals while the medical examiners made this diagnosis in 11%. In the same cohort, OHL was diagnosed by the oral/dental examiners in 9% of the individuals and by the medical examiners in 2%. The OC and OHL diagnoses affected the medical staging of 12% of the HIV-positive homosexual men and of 22% of the HIV-positive parenteral drug users. Forty percent of the HIV-positive homosexual men and 79% of the HIV-positive parenteral drug users with stage-defining oral lesions were not properly identified by the medical examiners.

Conclusions:  Specific training and a comprehensive oral examination have a significant impact on the diagnoses of OC and OHL, and on the medical staging of individuals with HIV infection.(Arch Otolaryngol Head Neck Surg. 1996;122:68-73)

REFERENCES

1 +
Budtz-Jorgensen E.  Histopathology, immunology, and serology of oral yeast infections: diagnosis of oral candidosis . Acta Odontol Scand . 1990;;48:37-43.
2 +
Greenspan JS, Greenspan D.  Oral lesions associated with HIV infection . In: Wormser GP. AIDS and Other Manifestations of HIV Infection . New York, NY: Raven Press; 1992;:489-498.
3 +
McCarthy GM.  Host factors associated with HIV-related oral candidiasis . Oral Surg Oral Med Oral Pathol . 1992;;73:181-186.
4 +
Resnick L, Herbst JS, Raab-Traub N.  Oral hairy leukoplakia . J Am Acad Dermatol . 1990;;22:1278-1282.
5 +
Greenspan D, Greenspan JS.  Significance of oral hairy leukoplakia . Oral Surg Oral Med Oral Pathol . 1992;;73:151-154.
6 +
Syrjanen S, Laine P, Happoinen RP, Niemela M.  Oral hairy leukoplakia is not a specific sign of HIV infection but related to immunosuppression in general . J Oral Pathol Med . 1989;;18:28-31.
7 +
Greenspan D, Greenspan JS, De Souza YG, Levy JA, Ungar AM.  Oral hairy leukoplakia in an HIV-negative renal transplant recipient . J Oral Pathol Med . 1989;;18:32-34.
8 +
Epstein JB, Priddy RW, Sherlock CH.  Hairy leukoplakia-like lesions in immunosuppressed patients following bone marrow transplantation . Transplantation . 1988;;46:462-464.
9 +
Mcleod RI, Long RQ, Soames JV, Ward MK.  Oral hairy leukoplakia in an HIV-negative renal transplant patient . Br Dent J . 1990;;169:208-209.
10 +
Saah AJ, Munoz A, Kuo V, et al.  Predictors of the risk of development of acquired immunodeficiency syndrome within 24 months among gay men seropositive for human immunodeficiency virus type 1: a report from the Multicenter AIDS Cohort Study . Am J Epidemiol . 1992;;135:1147-1155.
11 +
Eyster ME, Rabkin CS, Hilgartner MW, et al.  Human immunodeficiency virus–related conditions in children and adults with hemophilia: rates, relationship to CD4 counts, and predictive value . Blood . 1993;;81:828-834.
12 +
Katz MH, Greenspan D, Westenhouse J, et al.  Progression to AIDS in HIV-infected homosexual and bisexual men with hairy leukoplakia and oral candidiasis . AIDS . 1992;;6:95-100.
13 +
Coates RA, Farewell VT, Raboud J, et al.  Using serial observations to identify predictors of progression to AIDS in the Toronto Sexual Contact Study . J Clin Epidemiol . 1992;;45:245-253.
14 +
Selwyn PA, Alcabes P, Hartel D, et al.  Clinical manifestations and predictors of disease progression in drug users with human immunodeficiency virus infection . N Engl J Med . 1992;;327:1697-1703.
15 +
Palenicek J, Nelson KE, Vlahov D, Galai N, Cohn S, Saah AJ.  Comparison of clinical symptoms of human immunodeficiency virus disease between intravenous drug users and homosexual men . Arch Intern Med . 1993;;153:1806-1812.
16 +
Moniaci D, Greco D, Flecchia G, Raiteri R, Sinicco A.  Epidemiology: clinical features and prognostic value of HIV-1 related oral lesions . J Oral Pathol Med . 1990;;19:477-481.
17 +
Gardner LI, Brundage JF, McNeil JG, et al.  Predictors of HIV-1 disease progression in early- and late-stage patients: the US Army Natural History Cohort . J Acquir Immune Defic Syndr . 1992;;5:782-793.
18 +
Gillespie GM, Marino R.  Oral manifestations of HIV infection: a Panamerican perspective . J Oral Pathol Med . 1993;;22:2-7.
19 +
Rabeneck L, Crane MM, Risser JMH, Lacke CE, Wray NP.  A simple clinical staging system that predicts progression to AIDS using CD4 count, oral thrush, and night sweats . J Gen Intern Med . 1993;;8:5-9.
20 +
Greenspan D, Greenspan JS, Overby G, et al.  Risks factors for rapid progression from hairy leukoplakia to AIDS: a nested case-control study . J Acquir Immune Defic Syndr . 1991;;4:652-658.
21 +
Feigal DW, Katz MH, Greenspan D, et al.  The prevalence of oral lesions in HIV-infected homosexual and bisexual men: three San Francisco epidemiological cohorts . AIDS . 1991;;5:519-525.
22 +
Weniger BG, Quinhoes EP, Sereno AB, et al.  A simplified surveillance case definition of AIDS derived from empirical clinical data . J Acquir Immune Defic Syndr . 1992;;5:1212-1223.
23 +
Schiodt M, Bakilana PB, Hiza JF, et al.  Oral candidiasis and hairy leukoplakia correlate with HIV infection in Tanzania . Oral Surg Oral Med Oral Pathol . 1990;; 69:591-596.
24 +
Tukutuku K, Muyembe-Tramfun L, Kayembe K, Ntumba M.  Oral manifestations of AIDS in a heterosexual population in a Zaire hospital . J Pathol Med . 1990;;19:232-234.
25 +
Ketchem I, Berkowitz RJ, McIlven L, Forrester D, Rakusan T.  Oral findings in HIV-seropositive children . Pediatr Dent . 1990;;12:143-146.
26 +
Centers for Disease Control and Prevention.  1993 Revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults . MMWR Morb Mortal Wkly Rep . 1992;;41:1-19.
27 +
Royce RA, Luckmann RS, Fusaro RE, Winkelstein W.  The natural history of HIV-1 infection: staging classifications of disease . AIDS . 1991;;5:355-364.
28 +
Cooper DA, Gatell JM, Kroon S, et al.  Zidovudine in persons with asymptomatic HIV infection and CD4+ cell counts greater than 400 per cubic millimeter . N Engl J Med . 1993;;329:297-303.
29 +
Schulten EAJM, ten Kate RW, van der Waal I.  The impact of oral examination on the Centers for Disease Control classification of subjects with human immunodeficiency virus infection . Arch Intern Med . 1990;;150:1259-1261.
30 +
Thompson SH, Charles GA, Craig DB.  Correlation of oral disease with the Walter Reed staging scheme for HIV-1 seropositive patients . Oral Surg Oral Med Oral Pathol . 1992;;73:289-292.
31 +
Gorman JM, Kertzner R, Spitzer R, et al.  Development and characteristics of a medical staging system for HIV infection . Int J Meth Psychiatr Res . 1992;:2:117-124.
32 +
Cohen J.  A coefficient of agreement for nominal scales . Educ Psychol Measure . 1960;;20:37-46.
33 +
Landis JR, Koch GG.  The measurement of observer agreement for categorical data . Biometrics . 1977;;33:159-174.
34 +
Fleiss JL, Cohen J, Everitt BS.  Large sample standard errors of kappa and weighted kappa . Psychol Bull . 1969;;72:323-327.
35 +
El-Sadr W, Oleske JM, Agins BD, et al.  Evaluation and management of early HIV infection . In: Clinical Practice Guideline: No. 7 . Silver Spring, Md: Agency for Health Care Policy and Research; 1994;. Publication 94-0572.
36 +
Centers for Disease Control and Prevention.  Recommendations for prophylaxis against Pneumocystis carinii pneumonia for adults and adolescents infected with human immunodeficiency virus . MMWR Morb Mortal Wkly Rep . 1992;;41:1-11.
37 +
Phair J, Muñoz A, Detels R, et al.  The risk of Pneumocystis carinii pneumonia among men infected with human immunodeficiency virus type-1 . N Engl J Med . 1990;;322:161-165.
38 +
Phair J, Muñoz A, Detels R, Kaslow R, Rinaldo C. Letter to the editor. N Engl J Med . 1990;;322:1608.
39 +
Jewett JF, Hecht FM.  Preventive health care for adults with HIV infection . JAMA . 1993;;269:1144-1153.
40 +
US Public Health Service Task Force on Antipneumocystis Prophylaxis in Patients With Human Immunodeficiency Virus Infection.  Recommendations for prophylaxis against Pneumocystis carinii pneumonia for persons infected with human immunodeficiency virus . J Acquir Immune Defic Syndr . 1993;;6:46-55.
41 +
Montauk SL, Mandell K.  Update on drug therapy for HIV and related infections in adults . Am Fam Physician . 1992;;46:1772-1781.
42 +
Klein RS.  Prophylaxis of opportunistic infections in individuals infected with HIV . AIDS . 1989;;3( (suppl 1) ):S161-S173.
43 +
Dodd CL, Greenspan D, Katz MH, Westenhouse JL, Feigal DW, Greenspan JS.  Oral candidiasis in HIV infection: pseudomembranous and erythematous candidiasis show similar rates of progression to AIDS . AIDS . 1991;;5:1339-1343.
44 +
Tavitian A, Raufman JP, Rosenthal LE.  Oral candidiasis as a marker for esophageal candidiasis in the acquired immunodeficiency syndrome . Ann Intern Med . 1986;;104:54-55.
45 +
Porro GB, Parente F, Cernuschi M.  The diagnosis of esophageal candidiasis in patients with acquired immunodeficiency syndrome: is endoscopy necessary? Am J Gastroenterol . 1989;;84:143-146.
46 +
Connolly GM, Hawkins D, Harcourt-Webster JN, Parsons PA, Husain OAN, Gazzard BG.  Oesophageal symptoms, their causes, treatment, and prognosis in patients with the acquired immunodeficiency syndrome . Gut . 1989;;30:1033-1039.
47 +
EEC-Clearinghouse on Oral Problems Related to HIV Infection and WHO Collaborating Centre on Oral Manifestations of the Human Immunodeficiency Virus.  An update of the classification and diagnostic criteria of oral lesions in HIV infection . J Oral Pathol Med . 1991;;20:97-100.
48 +
Melnick SL, Nowjack-Raymer R, Kleinman DV, Swango PA.  A guide for epidemiological studies of oral manifestations of HIV infection . Bull World Health Organ . 1993;;71:10-13.
49 +
Greenspan JS, Barr CE, Sciubba JJ, et al.  Oral manifestations of HIV infection . Oral Surg Oral Med Oral Pathol . 1992;;73:142-144.

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1 +
Budtz-Jorgensen E.  Histopathology, immunology, and serology of oral yeast infections: diagnosis of oral candidosis . Acta Odontol Scand . 1990;;48:37-43.
2 +
Greenspan JS, Greenspan D.  Oral lesions associated with HIV infection . In: Wormser GP. AIDS and Other Manifestations of HIV Infection . New York, NY: Raven Press; 1992;:489-498.
3 +
McCarthy GM.  Host factors associated with HIV-related oral candidiasis . Oral Surg Oral Med Oral Pathol . 1992;;73:181-186.
4 +
Resnick L, Herbst JS, Raab-Traub N.  Oral hairy leukoplakia . J Am Acad Dermatol . 1990;;22:1278-1282.
5 +
Greenspan D, Greenspan JS.  Significance of oral hairy leukoplakia . Oral Surg Oral Med Oral Pathol . 1992;;73:151-154.
6 +
Syrjanen S, Laine P, Happoinen RP, Niemela M.  Oral hairy leukoplakia is not a specific sign of HIV infection but related to immunosuppression in general . J Oral Pathol Med . 1989;;18:28-31.
7 +
Greenspan D, Greenspan JS, De Souza YG, Levy JA, Ungar AM.  Oral hairy leukoplakia in an HIV-negative renal transplant recipient . J Oral Pathol Med . 1989;;18:32-34.
8 +
Epstein JB, Priddy RW, Sherlock CH.  Hairy leukoplakia-like lesions in immunosuppressed patients following bone marrow transplantation . Transplantation . 1988;;46:462-464.
9 +
Mcleod RI, Long RQ, Soames JV, Ward MK.  Oral hairy leukoplakia in an HIV-negative renal transplant patient . Br Dent J . 1990;;169:208-209.
10 +
Saah AJ, Munoz A, Kuo V, et al.  Predictors of the risk of development of acquired immunodeficiency syndrome within 24 months among gay men seropositive for human immunodeficiency virus type 1: a report from the Multicenter AIDS Cohort Study . Am J Epidemiol . 1992;;135:1147-1155.
11 +
Eyster ME, Rabkin CS, Hilgartner MW, et al.  Human immunodeficiency virus–related conditions in children and adults with hemophilia: rates, relationship to CD4 counts, and predictive value . Blood . 1993;;81:828-834.
12 +
Katz MH, Greenspan D, Westenhouse J, et al.  Progression to AIDS in HIV-infected homosexual and bisexual men with hairy leukoplakia and oral candidiasis . AIDS . 1992;;6:95-100.
13 +
Coates RA, Farewell VT, Raboud J, et al.  Using serial observations to identify predictors of progression to AIDS in the Toronto Sexual Contact Study . J Clin Epidemiol . 1992;;45:245-253.
14 +
Selwyn PA, Alcabes P, Hartel D, et al.  Clinical manifestations and predictors of disease progression in drug users with human immunodeficiency virus infection . N Engl J Med . 1992;;327:1697-1703.
15 +
Palenicek J, Nelson KE, Vlahov D, Galai N, Cohn S, Saah AJ.  Comparison of clinical symptoms of human immunodeficiency virus disease between intravenous drug users and homosexual men . Arch Intern Med . 1993;;153:1806-1812.
16 +
Moniaci D, Greco D, Flecchia G, Raiteri R, Sinicco A.  Epidemiology: clinical features and prognostic value of HIV-1 related oral lesions . J Oral Pathol Med . 1990;;19:477-481.
17 +
Gardner LI, Brundage JF, McNeil JG, et al.  Predictors of HIV-1 disease progression in early- and late-stage patients: the US Army Natural History Cohort . J Acquir Immune Defic Syndr . 1992;;5:782-793.
18 +
Gillespie GM, Marino R.  Oral manifestations of HIV infection: a Panamerican perspective . J Oral Pathol Med . 1993;;22:2-7.
19 +
Rabeneck L, Crane MM, Risser JMH, Lacke CE, Wray NP.  A simple clinical staging system that predicts progression to AIDS using CD4 count, oral thrush, and night sweats . J Gen Intern Med . 1993;;8:5-9.
20 +
Greenspan D, Greenspan JS, Overby G, et al.  Risks factors for rapid progression from hairy leukoplakia to AIDS: a nested case-control study . J Acquir Immune Defic Syndr . 1991;;4:652-658.
21 +
Feigal DW, Katz MH, Greenspan D, et al.  The prevalence of oral lesions in HIV-infected homosexual and bisexual men: three San Francisco epidemiological cohorts . AIDS . 1991;;5:519-525.
22 +
Weniger BG, Quinhoes EP, Sereno AB, et al.  A simplified surveillance case definition of AIDS derived from empirical clinical data . J Acquir Immune Defic Syndr . 1992;;5:1212-1223.
23 +
Schiodt M, Bakilana PB, Hiza JF, et al.  Oral candidiasis and hairy leukoplakia correlate with HIV infection in Tanzania . Oral Surg Oral Med Oral Pathol . 1990;; 69:591-596.
24 +
Tukutuku K, Muyembe-Tramfun L, Kayembe K, Ntumba M.  Oral manifestations of AIDS in a heterosexual population in a Zaire hospital . J Pathol Med . 1990;;19:232-234.
25 +
Ketchem I, Berkowitz RJ, McIlven L, Forrester D, Rakusan T.  Oral findings in HIV-seropositive children . Pediatr Dent . 1990;;12:143-146.
26 +
Centers for Disease Control and Prevention.  1993 Revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults . MMWR Morb Mortal Wkly Rep . 1992;;41:1-19.
27 +
Royce RA, Luckmann RS, Fusaro RE, Winkelstein W.  The natural history of HIV-1 infection: staging classifications of disease . AIDS . 1991;;5:355-364.
28 +
Cooper DA, Gatell JM, Kroon S, et al.  Zidovudine in persons with asymptomatic HIV infection and CD4+ cell counts greater than 400 per cubic millimeter . N Engl J Med . 1993;;329:297-303.
29 +
Schulten EAJM, ten Kate RW, van der Waal I.  The impact of oral examination on the Centers for Disease Control classification of subjects with human immunodeficiency virus infection . Arch Intern Med . 1990;;150:1259-1261.
30 +
Thompson SH, Charles GA, Craig DB.  Correlation of oral disease with the Walter Reed staging scheme for HIV-1 seropositive patients . Oral Surg Oral Med Oral Pathol . 1992;;73:289-292.
31 +
Gorman JM, Kertzner R, Spitzer R, et al.  Development and characteristics of a medical staging system for HIV infection . Int J Meth Psychiatr Res . 1992;:2:117-124.
32 +
Cohen J.  A coefficient of agreement for nominal scales . Educ Psychol Measure . 1960;;20:37-46.
33 +
Landis JR, Koch GG.  The measurement of observer agreement for categorical data . Biometrics . 1977;;33:159-174.
34 +
Fleiss JL, Cohen J, Everitt BS.  Large sample standard errors of kappa and weighted kappa . Psychol Bull . 1969;;72:323-327.
35 +
El-Sadr W, Oleske JM, Agins BD, et al.  Evaluation and management of early HIV infection . In: Clinical Practice Guideline: No. 7 . Silver Spring, Md: Agency for Health Care Policy and Research; 1994;. Publication 94-0572.
36 +
Centers for Disease Control and Prevention.  Recommendations for prophylaxis against Pneumocystis carinii pneumonia for adults and adolescents infected with human immunodeficiency virus . MMWR Morb Mortal Wkly Rep . 1992;;41:1-11.
37 +
Phair J, Muñoz A, Detels R, et al.  The risk of Pneumocystis carinii pneumonia among men infected with human immunodeficiency virus type-1 . N Engl J Med . 1990;;322:161-165.
38 +
Phair J, Muñoz A, Detels R, Kaslow R, Rinaldo C. Letter to the editor. N Engl J Med . 1990;;322:1608.
39 +
Jewett JF, Hecht FM.  Preventive health care for adults with HIV infection . JAMA . 1993;;269:1144-1153.
40 +
US Public Health Service Task Force on Antipneumocystis Prophylaxis in Patients With Human Immunodeficiency Virus Infection.  Recommendations for prophylaxis against Pneumocystis carinii pneumonia for persons infected with human immunodeficiency virus . J Acquir Immune Defic Syndr . 1993;;6:46-55.
41 +
Montauk SL, Mandell K.  Update on drug therapy for HIV and related infections in adults . Am Fam Physician . 1992;;46:1772-1781.
42 +
Klein RS.  Prophylaxis of opportunistic infections in individuals infected with HIV . AIDS . 1989;;3( (suppl 1) ):S161-S173.
43 +
Dodd CL, Greenspan D, Katz MH, Westenhouse JL, Feigal DW, Greenspan JS.  Oral candidiasis in HIV infection: pseudomembranous and erythematous candidiasis show similar rates of progression to AIDS . AIDS . 1991;;5:1339-1343.
44 +
Tavitian A, Raufman JP, Rosenthal LE.  Oral candidiasis as a marker for esophageal candidiasis in the acquired immunodeficiency syndrome . Ann Intern Med . 1986;;104:54-55.
45 +
Porro GB, Parente F, Cernuschi M.  The diagnosis of esophageal candidiasis in patients with acquired immunodeficiency syndrome: is endoscopy necessary? Am J Gastroenterol . 1989;;84:143-146.
46 +
Connolly GM, Hawkins D, Harcourt-Webster JN, Parsons PA, Husain OAN, Gazzard BG.  Oesophageal symptoms, their causes, treatment, and prognosis in patients with the acquired immunodeficiency syndrome . Gut . 1989;;30:1033-1039.
47 +
EEC-Clearinghouse on Oral Problems Related to HIV Infection and WHO Collaborating Centre on Oral Manifestations of the Human Immunodeficiency Virus.  An update of the classification and diagnostic criteria of oral lesions in HIV infection . J Oral Pathol Med . 1991;;20:97-100.
48 +
Melnick SL, Nowjack-Raymer R, Kleinman DV, Swango PA.  A guide for epidemiological studies of oral manifestations of HIV infection . Bull World Health Organ . 1993;;71:10-13.
49 +
Greenspan JS, Barr CE, Sciubba JJ, et al.  Oral manifestations of HIV infection . Oral Surg Oral Med Oral Pathol . 1992;;73:142-144.

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