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Oral Manifestations of HIV Infection Nicoleta Vaseliu, DDS, MS, OMFSHarrison Kamiru, BDS, MS, DrPH

Mark Kabue, BDS, MS, MPH, DrPH

ObjectivesDiscuss the importance of oral and dental care 1. for patients with human immunodeficiency virus (HIV) infection.Review the classification of orofacial lesions 2. associated with HIV infection in adults and children.Describe the clinical presentation and 3. management of the most common oral manifestations of HIV infection.

Key PointsOral health care is an important part of HIV 1. primary care.Oral manifestations are common clinical findings 2. in children and adults with HIV infection.Early diagnosis and management of oral mani­3. festations is important to prevent compli cations and improve quality of life.

Importance of Oral Manifes ta­tions of HIV InfectionSince human immunodeficiency virus (HIV) infection was first described in 1981, a variety of oral conditions associated with HIV disease have been documented. Studies have shown that 70%­90% of HIV­infected individuals will develop at least one oral manifestation during the course of the disease. A review of the dental literature shows that HIV­associated orofacial lesions have been considered

• clinical indicators of HIV infection in otherwise healthy, undiagnosed individuals;

• early clinical features of HIV infection;• clinical markers for the classification and staging of

HIV disease; and• predictors of HIV disease progression.

In developed countries, HIV disease progression is monitored by two key laboratory markers: CD4+ lympho­cyte count and HIV viral load. Unfortunately, these tests are not readily available in many developing countries. There, other important clinical findings guide clinicians in the evaluation and treatment of HIV disease. Because the oral cavity is easily accessible to clinical examination, orofacial lesions associated with HIV infection may be used as clinical markers of HIV disease progression.

The advent of highly active antiretroviral therapy (HAART) in 1996 greatly reduced the mortality and morbidity of HIV­infected patients who have access to treatment. The incidence rates of many opportunistic infections associated with HIV disease have decreased, including that of HIV­associated orofacial lesions.

Evaluation of oral health status is an important part of routine health care. A thorough oral examination is important at every stage in the management of HIV disease. It is also desirable to encourage collaboration among general medical practitioners, infectious­disease doctors, general and pediatric dentists, and oral pathologists to provide the best care possible for HIV­infected patients.

Classification of Orofacial Lesions Associated with HIVThere are two main classification systems of oral lesions associated with HIV infection. The first is based on the etiology of the oral lesions. According to this system, orofacial lesions are classified as bacterial, viral, or fungal infections or as neoplastic lesions or other conditions. The second, more widely used, system—recommended by the EC Clearinghouse on Oral Problems Related to HIV Infection and WHO Collaborating Centre on Oral Manifestations of the Human Immunodeficiency Virus—classifies orofacial lesions into three groups according to the degree of their association with HIV infection.

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Tables 1 and 2 show this classification of orofacial lesions associated with HIV/AIDS in adults and children, respectively.

Clinical Presentation and ManagementOral CandidiasisOral candidiasis is the most common orofacial manifes­tation of HIV infection. Its prevalence may depend on study population, diagnostic criteria, study design, and availability of antiretroviral therapy. Reported prevalence rates have varied widely, to as high as 72% in children and 94% in adults. Oral candidiasis is also a significant predictor of HIV disease progression in both adults and children. The median time of survival from its clinical diagnosis to death is 3.4 years among HIV­infected children. The main etiologic factor of oral candidiasis is the fungus Candida albicans, although other species of Candida may be involved.

Clinical appearance. Oral candidiasis is often observed in one of the following four clinical forms: erythematous (atrophic) candidiasis, pseudomembranous candidiasis, hyperplastic candidiasis, and angular cheilitis.

Erythematous (atrophic) candidiasis appears 1. clinically as multiple small or large patches, most often localized on the tongue and/or palate (Figure 1). Pseudomembranous candidiasis (oral thrush) 2. is characterized by the presence of multiple superficial, creamy white plaques that can be easily wiped off, revealing an erythematous base (Figure 2). They are usually located on the buccal mucosa, oropharynx, and/or dorsal face of the tongue. Hyperplastic candidiasis lesions appear white and 3. hyperplastic and cannot be removed by scraping. This form of oral candidiasis is rare in HIV­infected individuals.

Table 1. Orofacial lesions associated with HIV/AIDS in adults Lesions strongly associated with HIV infection

• Candidiasis • Non­Hodgkin’s lymphoma – Erythematous • Periodontal disease – Pseudomembranous – Linear gingival erythema • Hairy leukoplakia – Necrotizing (ulcerative) gingivitis • Kaposi’s sarcoma – Necrotizing (ulcerative) periodontitis

Lesions less commonly associated with HIV infection

• Bacterial infections • Viral infections – Mycobacterium avium­intracellulare – Herpes simplex virus – Mycobacterium tuberculosis – Human papillomavirus (wart­like lesions) • Melanotic hyperpigmentation – Condyloma acuminatum • Necrotizing (ulcerative) stomatitis – Focal epithelial hyperplasia • Salivary gland disease – Verruca vulgaris – Dry mouth due to decreased salivary flow rate – Varicella zoster virus – Unilateral or bilateral swelling of the major – Herpes zoster salivary glands – Varicella • Thrombocytopenic purpura • Ulceration NOS (not otherwise specified)

Lesions seen in HIV infection

• Bacterial infections • Fungal infection other than candidiasis – Actinomyces Israel – Cryptococcus neoformans – Escherichia coli – Geotrichum candidum – Klebsiella pneumoniae – Histoplasma capsulatum • Cat­scratch disease – Mucoraceae (mucormycosis/ zygomycosis) • Drug reactions (ulcerative, erythema multiforme, – Aspergillus flavus lichenoid, toxic epidermolysis • Recurrent aphthous stomatitis • Epithelioid (bacillary) angiomatosis • Viral infections • Neurologic disturbances – Cytomegalovirus – Facial palsy – Molluscum contagiosum – Trigeminal neuralgia

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2

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Angular cheilitis is characterized by the presence 4. of erythematous fissures at the corners of the mouth. It is usually accompanied by another form of intraoral candidiasis.

Treatment. Treatment with topical and systemic antifungal agents is recommended (Table 3).

Oral Hairy Leukoplakia Oral hairy leukoplakia (OHL) is more common among HIV­infected adults than among HIV­infected children. The reported prevalence of OHL in adults is about 20%­25%, increasing as the CD4+ lymphocyte count decreases, whereas in children the prevalence is about 2%­3%. The

presence of OHL is a sign of severe immunosuppression. OHL is a significant predictor of HIV disease progression in adults. Although its etiology is not clear, OHL seems to be caused by Epstein­Barr virus infection.

Clinical appearance. OHL presents as white, thick patches that do not wipe away and that may exhibit vertical corrugations with a hairlike appearance (Figure 3). The lesions usually start on the lateral margins of the tongue and sometimes inside the cheeks and lower lip. They may be unilateral or bilateral, and they are asymptomatic. OHL is often associated with oral candidiasis.

Figure 1. Erythematous candidiasis in an HIV-infected child Figure 2. Pseudomembranous candidiasis in an HIV-infected child

Table 2. Orofacial lesions associated with pediatric HIV infection Lesions commonly associated with pediatric HIV infection

• Oral candidiasis • Parotid enlargement (swelling of the major salivary glands) – Pseudomembranous • Recurrent aphthous ulcers – Erythematous – Minor – Angular cheilitis – Major • Herpes simplex virus infection – Herpetiform • Linear gingival erythema

Lesions less commonly associated with pediatric HIV infection

• Bacterial infections of oral tissues • Viral infections • Periodontal diseases – Cytomegalovirus – Necrotizing ulcerative gingivitis – Human papillomavirus – Necrotizing ulcerative periodontitis – Molluscum contagiosum – Necrotizing stomatitis – Varicella zoster virus • Xerostomia – Herpes zoster • Seborrheic dermatitis – Varicella

Lesions strongly associated with HIV infection but rare in children

• Neoplasms – Kaposi’s sarcoma and non­Hodgkin’s lymphoma • Oral hairy leukoplakia • Tuberculosis­related ulcers

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2

3

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Treatment. OHL usually does not require any treatment, but in severe cases systemic antivirals are recommended (Table 3). When OHL is associated with oral candidiasis, therapeutic management of oral candidiasis is required.

HIV-Associated Periodontal DiseasePeriodontal (gum) disease is common among HIV­infected patients. It is characterized by bleeding gums, bad breath, pain/discomfort, mobile teeth, and some­times sores. Its reported prevalence ranges widely, between 0% and 50%. Left untreated, HIV­associated periodontal disease may progress to life­threatening infections, such as Ludwig’s angina and noma (cancrum oris).

Clinical appearance. Four forms of HIV­associated periodontal disease have been described: linear gingival erythema, necrotizing ulcerative gingivitis (NUG), necrotizing ulcerative periodontitis (NUP), and necrotizing stomatitis.

Linear gingival erythema is characterized by 1. the presence of a 2­ to 3­mm red band along the marginal gingiva, associated with diffuse

erythema on the attached gingiva and oral mucosa (Figure 4). The degree of erythema is disproportionately intense compared with the amount of plaque present on the teeth. NUG is more common in adults than in 2. children. It is characterized by the presence of ulceration, sloughing, and necrosis of one or more interdental papillae, accompanied by pain, bleeding, and fetid halitosis. NUP is characterized by the extensive and rapid 3. loss of soft tissue and teeth. Necrotizing stomatitis is thought to be a con ­4. sequence of severe, untreated NUP. It is charac­terized by acute and painful ulceronecrotic lesions on the oral mucosa that expose underlying alveolar bone.

Treatment. Management and control of HIV­associated periodontal disease begin with good daily oral hygiene. In addition to brushing, flossing and use of mouthwash solutions are effective ways to prevent and control periodontal disease. Table 3 presents various therapeutic options.

Figure 3. Oral Hairy Leukoplakia in an HIV-infected adult Figure 4. Linear Gingival Erythema in an HIV-infected adult

Figure 5. Recurrent Herpes Simplex in an HIV-infected child Figure 6. Recurrent minor Aphthous Ulcers in an HIV-infected adult

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Table 3. Therapeutic options for the most common HIV-associated oral manifestations23,34,35,36,37

Oral Lesion Treatment for Adults Treatment for Children Comments

Oral Topical Topical • Different forms of oral candidiasisCandidiasis • Nystatin (Mycostatin) • Nystatin suspension 200,000­ may occur simultaneously.(Erythematous, • Oral gel: apply gel q8h 400,000 U/day divided in 4­6 doses, • Hyperplastic candidiasis requiresPseudomembranous, or q6h, for 10­14 days for 14 days systemic treatment.and Hyperplastic) • Cream: Apply q12h, for • Clotrimazole troches 10 mg q8h or • Ketoconazole may interact with 10­14 days q6h, for 4 weeks Lopinavir­Ritonavir (Kaletra) at • Gentian violet 1% aqueous solution doses >200 mg/day. Systemic painted in the affected areas q8h • Topical fluoride should be used if • Nystatin (Mycostatin) antifungal agents are administered for long periods to counteract high 400,000­600,000 U q6h, sugar content of some antifungal for 14 days Systemic medications. • Ketoconazole (Nizoral) • Ketoconazole 3.5­6.6 mg/kg/day in • Amphotericin B may be used in 200­400 mg PO q.d. a single dose azole­resistant infections. • Fluconazole (Diflucan) • Fluconazole 6 mg/kg on day 1, then • Amphotericin B may also be 50­100 mg PO q.d. 3 mg/kg qd, up to 2 weeks available as a topical preparation. • Itraconazole (Sporanox) • Itraconazole 100 mg PO, daily for • Dentures should be removed when (Capsules or solution) children older than 3 years medication is applied. 200 mg PO qd for 7 days • Amphotericin B10 mg Prophylaxis IVq6h, for 10 days • Clotrimazole 10 mg PO q8h or q12h for long period Prophylaxis • Nystatin 100,000­400,000 U PO • Fluconazole 100 mg q12h for long period PO qwk, for long period • Fluconazole 3­6 mg/kg PO daily or weekly for long period

Angular Topical Topical • Lesions tend to heal slowlyCheilitis • Nystatin­triamcinolone • Nystatin­triamcinolone (Mycolog II) because of the repeated opening (Mycolog II) ointment ointment applied on the affected of the mouth. applied on the affected areas after meals and at bedtime areas after meals and • Clotrimazole 1% (Mycelex) cream at bedtime • Miconazole 2% cream applied q12h • Clotrimazole 1% on the affected areas, for 1­2 weeks (Mycelex) cream • Miconazole 2% cream applied q12h on the affected areas, for 1­2 weeksHerpes Simplex Systemic Systemic • Ganciclovir, Valacyclovir andVirus (HSV) • Acyclovir (Zovirax) • Acyclovir 10 mg/kg PO q4h or q6h Famciclovir are probably effective.Infection 800 mg PO q4h, • Acyclovir 10 mg/kg IV q8h • Foscarnet is the drug of choice for for 10 days • Foscarnet 24­40 mg/kg PO q8h, for Acyclovir­resistant cases. • Foscarnet 24­40 mg/kg resistant herpetic lesions • Patients taking Acyclovir should PO q8h, for resistant be instructed to drink plenty of herpetic lesions fluids. • Topical antiviral medications may be used for labial and perioral herpetic lesions.

Linear Gingival Local Local • Prophylaxis is recommended:Erythema • Scaling and root planing • Scaling and root planing brushing, flossing, and use of(LGE) • 0.12% Chlorhexidine • 0.12% Chlorhexidine gluconate mouth rinses. gluconate (Periogard, (Periogard, Peridex) 0.5 oz q12h • Antifungal agents may be useful in Peridex) 0.5 oz q12h rinse, for 30 sec. and spit the treatment of LGE. rinse, for 30 sec. and spit

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Table 3. Therapeutic options for the most common HIV-associated oral manifestations23,34,35,36,37 (continued)

Oral Lesion Treatment for Adults Treatment for Children CommentsLinear Gingival Local Local • Prophylaxis is recommended:Erythema • Scaling and root planing • Scaling and root planing brushing, flossing, and use of(LGE) • 0.12% Chlorhexidine • 0.12% Chlorhexidine gluconate mouth rinses. gluconate (Periogard, (Periogard, Peridex) 0.5 oz q12h • Antifungal agents may be useful in Peridex) 0.5 oz q12h rinse, for 30 sec. and spit the treatment of LGE. rinse, for 30 sec. and spit

Xerostomia Topical Topical • Good oral hygiene measures and • Chewing or sucking • Chewing or sucking sugarless candy diet control (control of sugar and sugarless candy • Frequent sips of water sugary foods) are recommended • Frequent sips of water • Commercial artificial saliva to prevent dental caries. • Commercial artificial substitutes • Mouth rinses with high alcohol saliva substitutes • Topical fluoride products content should be avoided due to • Topical fluoride products drying effect.

Systemic • Pilocarpine (Salagen) 5 mg PO q8h before meals; it may increase to 7.5 mg PO q8h

Parotid Systemic Systemic • Surgical removal of the parotidEnlargement (of • Non­steroidal • Non­steroidal anti­inflammatories gland may be necessary formajor salivary anti­inflammatories • Analgesics esthetic reasons.glands) • Analgesics • Antibiotics • Antibiotics • Steroids • Steroids

Oral Hairy Local Local • Recurrence often occurs after theLeukoplakia (OHL) • Podophyllin resin • Podophyllin resin 25% 1­2 applica­ treatment is discontinued. 25% 1­2 applications tions on the affected areas, at • OHL is rare in children. on the affected areas, at 1 week apart Symptomatic and extensive lesions 1 week apart • Retinoic acid (Tretinoin) may require topical treatment. • Retinoic acid (Tretinoin) • Surgical excision • OHL has been shown to disappear • Surgical excision in patients receiving zidovudine (AZT). Systemic • Acyclovir (Zovirax) 800 mg PO q4h or q6h, for 14 days • Famciclovir 500 mg PO q8h, for 5­10 days • Valacyclovir 1000 mg PO q8h, for 5­10 days

Necrotizing Local Local • Prolonged use of chlorhexidineUlcerative • Debridement of • Debridement of affected areas may cause staining of teeth, Gingivitis (NUG), affected areas • Irrigation with povidon­iodine tongue, and restorations; taste • Irrigation with povidon­ (10% Betadine) alteration; and mucosalNecrotizing iodine (10% Betadine) • 0.12% chlorhexidine gluconate desquamation and irritation.Ulcerative • 0.12% chlorhexidine (Peridex, Periogard) mouth rinse • Metronidazole should not bePeriodontitis (NUP), gluconate (Peridex, q12h given to patients taking Periogard) mouth rinse didanosine (ddI) or zalcitabineNecrotizing q12h (ddC), because it may potentiateStomatitis (NS) peripheral neuropathy.

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Table 3. Therapeutic options for the most common HIV-associated oral manifestations23,34,35,36,37 (concluded)

Oral Lesion Treatment for Adults Treatment for Children Comments

Necrotizing Systemic Systemic (See chart on previous page)Ulcerative • Metronidazole (Flagyl) • Metronidazole (Flagyl) 15­35 mg/kgGingivitis (NUG), 250 mg PO q8h or PO q8h, for 7­10 days 500 mg q12h, for 7­10 days • Clindamycin (Cleocin) 20­30 mg/kgNecrotizing • Clindamycin (Cleocin) PO q6h, for 7 daysUlcerative 150 mg PO q6h or • Amoxicillin clavulanate (Augmentin)Periodontitis (NUP), 300 mg PO q8h, for 7 days 40 mg/kg PO q8h, for 7 days • Amoxicillin clavulanate Necrotizing (Augmentin) 250 mg POStomatitis (NS) q12h, for 7 days

Oral Ulcers Topical Topical • Major aphthous ulcers usually(Recurrent • Triamcinolone in • Triamcinolone in Carboxymethyl­ require systemic steroids.Aphthous Ulcers) Carboxymethylcellulose cellulose 0.1% paste applied in a • Aphthous ulcers may be exacebated 0.1% paste thin layer q6h daily by stress. • Betamethasone • Betamethasone phosphate: • Iron, vitamin B12, and folate phosphate: – 0.5 mg tablet dissolved in 10 ml deficiencies should be ruled out. – 0.5 mg tablet dissolved mouthwash and rinse q4h • Dexamethasone elixir should be in 10 ml mouthwash – spray on ulcer (1 spray = 100 μg) used for multiple ulcers or ulcers and rinse q4h up to 800 μg not accessible for topical applica­ – spray on ulcer (1 spray • Fluocinonide (Lidex) 0.05% tion. = 100 μg) up to 800 μg ointment q4h • Thalidomide is indicated only • Fluocinonide (Lidex) • Dexamethasone elixir (0.5 mg/5ml) when recurrences are severe 0.05% ointment applied rinse and expectorate and frequent. on ulcer q4h • The treatment with Thalidomide • Dexamethasone elixir Systemic should be monitored thoroughly (0.5 mg/5ml) rinse and • Prednisone 2 mg/kg q6h, for 5­7 due to its teratogenicity. Birth expectorate days with gradual tapering control measures are required. Systemic • Prednisone starting at 30­40 mg PO daily with taper over 1 month for severe disease resistant to topical agents • Thalidomide 200 mg PO daily

Oral Warts Topical Topical • The recurrence rate is high. • Podophyllin resin 25% • Podophyllin resin 25% applications • Concurrent therapeutic approaches applications q6h for q6h for long period should be considered. long period • Surgical excision • Surgical excision • Laser ablation • Laser ablation • Cryotherapy • Cryotherapy

Systemic • Cimetidine (Tagamet) 600 mg PO q6h, for long period (months) • Interferon alfa–n3 SC/IM 3,000,000 U (1 ml) qwk, for several weeks

Abbreviations used in Table 3: PO = per os (by mouth); IV = intravenous; qd = every day; qwk = every week; q2h = every two hours; q4h = every four hours; q6h = every six hours; q8h = every 8 hours; q12h = every 12 hours.

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Noma, also known as cancrum oris, is a gangrenous condition that affects primarily children. Noma has been reported mainly in developing countries in West Africa, but cases have also been described in other parts of the world. It is a multifactorial disease. The most important risk factors are poverty, chronic malnutrition, poor oral hygiene, and severe immunosuppression. Though considered a preventable disease, noma has a case fatality rate of 70%­90% if left untreated.

Herpes Simplex Virus InfectionHerpes simplex virus (HSV) infection may be either primary (herpetic gingivostomatitis) or secondary (herpes labialis). The prevalence of oral HSV infection varies between 10% and 35% in HIV­infected adults and children. The presence of HSV infection for more than 1 month constitutes an AIDS­defining condition.

Clinical appearance. HSV infection appears as a crop of vesicles usually localized on the keratinized mucosa (hard palate, gingiva) and/or vermillion borders of the lips and perioral skin (Figure 5). The vesicles rupture and form irregular painful ulcers. They may interfere with mastication and swallowing, resulting in decreased oral intake and dehydration.

Treatment. Systemic therapy with antiviral agents is recommended (Table 3). The treatment is more effective if it is instituted in the prodromal stage of infection.

Recurrent Aphthous UlcersRecurrent aphthous ulcers (RAUs) occur in about 1%­7% of HIV­infected patients. They are painful ulcers on the nonkeratinized oral mucosa, such as labial and buccal mucosa, soft palate, and ventral aspect of the tongue. Severe recurrent aphthous lesions usually occur when the CD4+ lymphocyte count is less than 100 cells/μL. This result may be suggestive of HIV disease progression. The etiology of RAUs is not well known.

Clinical appearance. RAUs may present as minor, major, or herpetiform aphthae. Minor aphthous ulcers are ulcers less than 5 mm in diameter covered by pseudomembrane and surrounded by an erythematous halo. They usually heal spontaneously without scarring (Figure 6). Major aphthous ulcers resemble minor aphthous ulcers, but they are fewer and larger in diameter (1­3 cm), are more painful, and may persist longer. Their presence interferes with mastication, swallowing, and speaking. Healing occurs over 2­6 weeks. Scarring is common. Herpetiform

aphthous ulcers occur as a crop of many small lesions (1­2 mm) disseminated on the soft palate, tonsils, tongue, and/or buccal mucosa.

Treatment. The first line of management of RAUs is pain control and prevention of superinfection. Depending on the severity of the ulcers, topical and/or systemic steroid agents are recommended (Table 3).

Parotid Enlargement and XerostomiaParotid enlargement is commonly associated with HIV infection in children (10%­30%) and less commonly in adults. It occurs in the late course of HIV infection and is associated with a slower rate of HIV disease progression. The median time from its diagnosis to death has been reported to be 5.4 years among HIV­infected children. Lymphocytic infiltration of the salivary glands may be an etiologic factor.

Clinical appearance. Parotid enlargement occurs as unilateral or bilateral swelling of the parotid glands. It is usually asymptomatic and may be accompanied by decreased salivary flow (xerostomia or dry mouth). Problems with dry mouth in HIV­infected patients are often caused by medications that interfere with salivary secretion, such as antihistamines, antianxiety medications, antidepressants, and some antiretroviral drugs (didanosine and zalcitabine).

Treatment. Treatment is required only in severe cases and may consist of systemic analgesics, anti­inflammatories, antibiotics, and/or steroids (Table 3).

Human Papillomavirus Infection (Oral Warts)The incidence of oral warts due to human papillomavirus infection has increased dramatically since the era of HAART. The lesions are more prevalent in adults (1%­4% of cases) than in children.

Clinical appearance. Oral warts may appear cauliflower­like, spiked, or raised with a flat surface. They are asymptomatic. The most common location is the labial and buccal mucosa. The most common clinical presentation is multifocal flat lesions resembling focal epithelial hyperplasia (Heck’s disease).

Treatment. Treatment may be required for patients with multiple lesions. Topical and systemic agents and various surgical approaches are available (Table 3).

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General Management ConsiderationsTo prevent the need for expensive dental services, it is imperative to treat the oral manifestations of HIV infection at all levels of care. Personal oral hygiene practices, such as tooth brushing and use of interdental cleaning aids, are the most effective ways of maintaining good oral health.

At the primary level of oral care, prevention of oral diseases takes priority. Prevention involves improving oral hygiene awareness through health education at the individual and community levels. Oral health education messages should be made visible in all community forums. Home­based care providers should undergo training in basic oral hygiene practices so that they can impart these to patients under their care. Use of simple materials such as warm salty mouth rinse or commercial mouthwash (chlorhexidine) can improve basic oral hygiene cost­effectively. Patients whose manual dexterity is intact should be taught appropriate brushing techniques. Other adjuvant oral hygiene methods, such as flossing and use of interdental toothbrushes, will depend on the availability and affordability of supplies.

The secondary level of oral care involves visits to clinical care facilities. Depending on local resources, the health cadre available at this level may range from nursing staff at a health center to primary care physicians. In some countries, health centers may have no oral health personnel or may offer only relief of pain with analgesics and extractions. Health care workers at this level should be trained to recognize suspicious lesions that may be oral manifestations of HIV infection, and they should know when and where to refer patients to a higher level of oral care.

At the tertiary level of oral care, a dentist should be available to make definitive diagnoses of oral lesions and provide professional oral services such as prophylaxis, restorations, biopsies, and the prescription of appropriate medication.

AcknowledgmentWe thank Professor Sudeshi Naidoo, Department of Community Dentistry, Faculty of Dentistry and WHO Collaborating Centre, University of the Western Cape, South Africa, for providing the pictures of oral lesions used in this chapter.

References 1. Arendorf TM, Bredekamp B, Cloete CAC, et al. Oral

manifestations of HIV infection in 600 South African patients. J. Oral Pathol. Med. 1998;27:176­179.

2. Winfert M, Grimes RM, Lynch DP. Oral manifestations of HIV infection. Ann. Intern. Med. 1996;125:485­496.

3. Kamiru HN, Naidoo S. Oral HIV lesions and oral health behaviour of HIV positive patients attending Queen Elizabeth II Hospital, Maseru, Lesotho. SADJ 2002;57:479­482.

4. Patton LL, Phelan JA, Ramos­Gomez FJ, et al. Prevalence and classification of HIV­associated oral lesions. Oral Dis. 2002;8(Suppl 2):98­109.

5. Chapple ILC, Rout PJ, Basu MK. Gingival Kaposi’s sarcoma: the first indication of HIV infection. Dent. Update 1992;19:296­301.

6. Klein RS, Harris CA, Small CB, et al. Oral candidiasis in high­risk patients as the initial manifestations of the acquired immunodeficiency syndrome. N. Engl. J. Med. 1984;311:354­358.

7. 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 Recomm. Rep. 1993;41(RR­17):1­19.

8. Ramos­Gomez FJ, Petru A, Hilton JF. Oral manifestations and dental status in paediatric HIV infection. Int. J. Paediatr. Dent. 2000;10:3­11.

9. Magalhaes GM, Bueno DF, Serra E. Oral manifestations of HIV positive children. J. Clin. Pediatr. Dent. 2001;25:103­106.

10. Nicolatou O, Theodoridou M, Mostrou G. Oral lesions in children with perinatally acquired immunodeficiency virus infection. J. Oral Pathol. Med. 1999;28:49­53.

11. Begg MD, Lamster IB, Panageas KS. A prospective study of oral lesions and their predictive value for progression of HIV disease. Oral Dis. 1997;3:176­183.

12. Chapple ILC, Hamburger J. The significance of oral health in HIV disease. Sex Transm. Inf. 2000;76:236­243.

13. Katz MH, Mastrucci T, Leggott PJ, et al. Prognostic significance of oral lesions in children with perinatally acquired human immunodeficiency virus infection. Am. J. Dis. Child. 1993;147:45­48.

193

Oral Manifestations of HIV Infection

14. Barasch A, Safford MM, Catalanotto FA, et al. Oral soft tissue manifestations in HIV­positive vs. HIV­negative children from an inner city population: a two­year observational study. Pediatr. Dent. 2000;22:215­220.

15. Schmidt­Westhausen AM, Priepke F, Bergmann FJ, et al. Decline in the rate of oral opportunistic infections following introduction of highly active antiretroviral therapy. J. Oral Pathol. Med. 2000;29:336­341.

16. Darbyshire J. Therapeutic interventions in HIV infection—a critical review. Trop. Med. Int. Health 2000;5:A26­A31.

17. Scully C, Diz Dios P. Orofacial effects of antiretroviral therapies. Oral Dis. 2001;7:205­210.

18. Royce RA, Luckman RS, Fusaro RE, et al. The natural history of HIV­1 infection: staging classifications of disease. AIDS 1991;5:355­364.

19. EC 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;20:97­100.

20. EC Clearinghouse on Oral Problems Related to HIV Infection and WHO Collaborating Centre on Oral Manifestations of the Human Immunodeficiency Virus. Classification and diagnostic criteria for oral lesions in HIV infection. J. Oral Pathol. Med. 1993;22:289­291.

21. Ramos­Gomez FJ, Flaitz CM, Catapano P, et al.; Collaborative Workgroup on Oral Manifestations of Pediatric HIV Infection, Oral AIDS Center, University of California, San Francisco, San Francisco, California. Classification, diagnostic criteria, and treatment recommendations for orofacial manifestations in HIV­infected pediatric patients. J. Clin. Pediatr. Dent. 1999;23:85­96.

22. Kline MW. Oral manifestations of pediatric human immunodeficiency HIV infection: a review of the literature. Pediatrics 1996;97:380­388.

23. Kline MW. Cutaneous and oral manifestations of pediatric HIV infection. In Pizzo PA & Wilfert CM (Eds.): Pediatric AIDS: The Challenge of HIV Infection in Infants, Children, and Adolescents. 3rd ed. Baltimore: Williams & Wilkins, 1998.

24. Flaitz CM, Hicks MJ. Oral manifestations in pediatric HIV infection. In: Shearer WT & Hanson CI (Eds.): Medical Management of AIDS in Children. Philadelphia: Saunders, 2003.

25. Schiodt M, Pindborg JJ. AIDS and the oral cavity: epidemiology and oral manifestations of HIV infection: a review. Int. J. Oral Maxillofac. Surg. 1987;16:1­14.

26. Ramos­Gomez FJ, Hilton JF, Canchola AJ, et al. Risk factors for HIV­related orofacial soft­tissue manifestations in children. J. Pediatr. Dent. 1996;18:121­126.

27. Walling DM. Oral hairy leukoplakia: an Epstein­Barr virus­associated disease of patients with HIV. Res. Initiat. Treat Action 2000;6:10­15.

28. Lifson AR, Hilton JF, Westenhouse JL, et al. Time from seroconversion to oral candidiasis or hairy leukoplakia among homosexual and bisexual men enrolled in three prospective cohorts. AIDS 1994;8:73­79.

29. Berthold P. Noma: a forgotten disease. Dent. Clin. N. Am. 2003;47:559­574.

30. Enwonwu CO, Falkler WA, Idigbe EO, et al. Noma (cancrum oris): questions and answers. Oral Dis. 1999;5:144­149.

31. Schiodt M. Less common oral lesions associated with HIV infection: prevalence and classification. Oral Dis. 1997;3:S208­S213.

32. Clark PC, Flaitz CM, Nichols CM, et al. Oral human papillomavirus infection in HIV: clinicopathologic correlations. J. Dent. Res. 1998;77:250A.

33. Brothell DJ, Jutai DK, Hawkins RJ. An update of mechanical oral hygiene practices: evidence­based recommendations for disease prevention. J. Can. Dent. Assoc. 1998;46:295­306.

34. Gage TW, Picket FA. Mosby’s Dental Drug Reference. 6th ed. St. Louis: Mosby, 2003.

35. Naidoo S, Chikte U. HIV/AIDS—the evolving pandemic and its impact on oral health in sub­Saharan Africa. SADJ 1999;54:661­630.