Clinical and Legal Issues Impacting on Dental Care

Australian Dental Journal The ofﬁcial journal of the Australian Dental Association

Australian Dental Journal 2012; 57: 256–270 REVIEW doi: 10.1111/j.1834-7819.2012.01715.x

HIV and dentistry in Australia: clinical and legal issues impacting on dental care

AT McLean,* EK Wheeler, S Cameron, D Baker

*St Vincent’s Hospital, Fitzroy, Victoria. Australasian Society for HIV Medicine, Darlinghurst, New South Wales.

ABSTRACT The number of people in Australia living with HIV is growing. This reﬂects a consistent rate of new HIV infections combined with an increased life expectancy of people with HIV. Dentists are ideally positioned to identify, manage and treat HIV-associated oral manifestations and have a responsibility to themselves and to their patients to be up-to-date with the evolving area of HIV and related issues. Those issues include medico-legal implications associated with HIV diagnosis and treatment. This article provides a review of the current clinical and medico-legal aspects of HIV in Australia. The oral manifestations of HIV can be divided into ﬁve categories: microbiological infections (fungal, bacterial and viral); oral neoplasms; neurological conditions; other oral conditions that may be associated with HIV infection; and oral conditions associated with HIV treatment. Current treatment options in the scope of general dental practice are outlined. Medico-legal issues related to the management of patients with HIV are explored, including rights of the patient regarding disclosure of HIV status; an algorithm for the management of a patient with signs or symptoms indicating possible HIV infection, including referral pathways; and an algorithm for dealing with patient management and referral issues. Keywords: Bacterial, dental, fungal, HIV, legal. Abbreviations and acronyms: ADA = Australian Dental Association; AIDS = acquired immune deficiency syndrome; ASHM = Australasian Society for HIV Medicine; cART = combination antiretroviral therapy; CMV = cytomegalovirus; EBV = Epstein-Barr virus; HHV = human herpesvirus; HHV4 = human herpesvirus 4; HHV8 = human herpesvirus 8; HIV = human immunodeficiency virus; HSV = herpes simplex virus; HZ = herpes zoster; KS = Kaposi’s sarcoma; MCV2 = molluscum contagiosum virus 2; NHL = non-Hodgkin’s lymphoma; OHL = oral hairy leukoplakia; VZV = varicella zoster virus. (Accepted for publication 17 May 2012.)

reflecting Bell’s estimate.5 HIV is present in saliva, INTRODUCTION however it is not considered a risk factor for transmis- Currently in Australia there are more than 21 300 sion because of the low levels of HIV and endogenous people living with human immunodeficiency virus antiviral factors present in saliva.6–8 There is no (HIV), with approximately 1000 people newly infected evidence that HIV can be transmitted by contact with each year.1 The number of people living with HIV tears, sweat, urine or faeces.3,4 infection continues to rise as improved antiretroviral Dentists can play a key part in the diagnosis and treatments mean people live longer, often for decades, management of patients with HIV. Research has following HIV infection.2 demonstrated that early identification of HIV is an HIV is transmitted by exposure to HIV-infected important factor in maximizing positive outcomes for bodily fluids or tissues by way of unprotected sex, individual patients and for preventing ongoing trans- re-using drug-injecting equipment and vertical mission.9 Unfortunately, indications for HIV testing are transmission from mother-to-child.3,4 In Australia, often missed.9 Dentists should not underestimate the male-to-male sex remains the dominant mode of contribution they can make in the diagnosis of HIV by transmission.1 Transmission via medical procedures is way of its oral manifestations. Due to the complexity of uncommon4 as the risk of HIV transmission after HIV infection and its associated complications, a team percutaneous exposure to HIV-infected blood is 0.3%, approach to the management of HIV is ideal, with

256 ª 2012 Australian Dental Association Clinical and legal issues impacting on dental care dentists as important contributors to this multidisci- Oral lesions may be present at all stages of HIV plinary approach. infection (Fig. 1). However, it should be emphasized The potential for dentists to play a proactive role in that HIV-associated oral lesions are not pathogno- HIV diagnoses and treatment is complicated by the monic as it is possible to find such conditions in significant patient, social and legal implications related immunocompetent people without HIV infection.11 to this particular disease. Such advice is based on Similar to systemic HIV-associated pathology, oral awareness that HIV based discrimination remains lesions presenting during HIV infection are more likely prevalent across health services. Notably HIV Futures to occur with a high viral load or a reduced CD4 cell 6 surveyed over 1000 HIV positive individuals and count.12–19 Oral manifestations of the seroconversion found 26% had experienced less favourable treatment illness may include oral ulcers, oral candidiasis, oral from their health services and 10% had experienced herpes and tonsillitis and, uncommonly, gingivitis and discrimination due to their HIV status.10 Thus, HIV stomatitis.20,21 Multiple factors such as the failure of service organizations advise HIV positive individuals to normal immune surveillance and HIV-related immuno- ‘think carefully’ before disclosing HIV status to dental suppression increase the risk of neoplasia throughout professionals. the course of HIV infection.22 It is illegal for dentists to discriminate on the basis of disease. HIV status should not affect the decision to Treatment of HIV infection provide treatment, however knowing the HIV status of a patient does allow the dentist to provide more The aim of treatment is to suppress HIV infection and comprehensive dental care as HIV and HIV-associated allow immune recovery to optimize health.23 Ulti- disease significantly impacts on oral health. It is mately, such treatment will prevent or lessen the important that Australian dentists do not become likelihood of HIV-related complications and may complacent about HIV and instead keep abreast of prevent advanced HIV disease or acquired immune current HIV medicine and wider issues to ensure deficiency syndrome (AIDS). Current treatments are optimal outcomes for their patients. usually very successful with current life expectancy from diagnosis of a young person projected to be almost 40 years.24 Oral pathophysiology of HIV infection Treatment of HIV infection involves the use of HIV infection causes an immunodeficient state by combinations of antiretroviral medications, currently gradually impairing humoral and cell-mediated immu- referred to as combination antiretroviral therapy nity. This allows new pathogens to more readily infect (cART). cART is instituted based on the monitoring and cause disease, and this disease is usually more of disease progression. Current guidelines recommend severe and widespread. Pre-existing or latent conditions starting treatment when an individual’s CD4 cell count held dormant by a functioning immune system can be declines to 350 cells ⁄ lL or there is a diagnosis of an re-activated. Also opportunistic infections may develop, AIDS-defining illness with treatment aiming to produce a process whereby normally non-pathogenic organisms an undetectable viral load of less than 20–75 HIV gain the ability to cause disease. copies ⁄ mL of plasma.25

KS = Kaposi’s sarcoma; PJP = pneumcystis jirovecii pneumonia; OHL = oral hairy leukoplakia; NHL = non-Hodgkin’s lymphoma; MAC = Mycobacterium avium complex; CMV = cytomegalovirus; TB = tuberculosis; NUP = necrotizing ulcerative periodontitis; HZ = Herpes zoster. Fig. 1 Natural history of HIV infection – the various stages of HIV infection depicting the development of different opportunistic infections with advanced immunodeﬁciency and the impact of antiretroviral therapy on CD4 cell count recovery. Adapted from: Sasadeusz J, Locarnini S, Kidd M, Bradford D, Danta M. HIV, HBV, HCV and STIs: Similarities and Differences. In: Bradford D, Hoy J, Matthews G, et al., eds. HIV, Viral Hepatitis and STIs: A Guide for Primary Care. Sydney: Australasian Society for HIV Medicine, 2008:18.

ª 2012 Australian Dental Association 257 AT McLean et al.

Impact of HIV treatment on oral conditions erythema is now classed as a periodontal condition of fungal origin.30 Oral manifestations may occur with the progression of Fungal infections may appear at any time throughout HIV infection in patients without medical treatment or HIV infection, however they are more prevalent when intervention, however most people with HIV infection the CD4 cell count falls to below 500 cells ⁄ lL.12,14,19,20 in Australia start a treatment regimen prior to signif- Ninety per cent of patients with advanced HIV disease icant immune impairment. The impact of cART are affected with oral candidiasis at some point during generally results in a marked reduction in viral load, their disease.28 However cART results in a significant which in turn enables the immune system to return reduction of oral candidiasis, such that rates range from to adequate surveillance of the oral environment with 0% to 16.7%.18,19 cART has changed the prevalence oral manifestations often resolving. Occasionally, some patterns of oral lesions associated with HIV infection, conditions such as aphthous ulceration may persist so candidiasis is no longer the most common condi- while HIV-related periodontal diseases may recur, even tion.18,19 When diagnosing oral candidiasis, it must be in the presence of adequate viral control. Co-factors remembered that many fungal species, in particular such as stress and smoking have been suggested to have C. albicans, are commensal organisms, so the isolation a role in their re-emergence.26 of fungal organisms is not diagnostic of a disease state. Although introduction of cART often improves oral Any suspicious lesions should be considered a candidate health and stabilizes oral conditions, some complica- for biopsy. tions may result from therapy. Generally, there appear Pseudomembranous candidiasis is evident by the to be few significant oral side effects associated with presence of creamy white or yellow plaques found on any particular HIV medication but the combination any of the intraoral surfaces (Fig. 2) which, when of potent antiretroviral drugs with other medications scraped, reveal an erythematous or bleeding mucosal commonly results in xerostomia and dry lips. Often surface. It may cause no symptoms or mild to moderate there will be persistent cracking at the anterior com- pain or burning and is usually intermittent, however missure, and xerostomia can facilitate dental decay and may be chronic. The diagnosis is clinical, although affect oral function. when uncertain or there is a lack of response to treatment, microscopy, culture or biopsy may be Clinical aspects of HIV-associated oral manifestations needed. A periodic acid Schiff staining of a cytological smear may show candidal hyphae. Oral conditions associated with HIV infection and the Erythematous candidiasis causes patchy red or ery- development of advanced HIV disease can be divided thematous areas that may become atrophic. It is often 27 into five major groups: microbiological infections associated with oral appliances, may become diffuse, (fungal, bacterial, viral), oral neoplasms, neurological and is commonly found on the hard palate, the dorsum conditions, other oral conditions that may be associated of the tongue and occasionally on the buccal mucosa. with HIV infection, and oral conditions associated with Similar to pseudomembranous candidiasis, there may HIV treatment. be no symptoms or mild to moderate pain or burning. Other co-infections and conditions associated with Erythematous candidiasis is usually intermittent, how- HIV infection, which are significant to dentists, are ever it may become chronic, especially when related to syphilis, tuberculosis, persistent generalized lymph- dentures. A history and examination is sufficient for adenopathy, gastro-oesophageal reflux disease and diagnosis, although in cases where there is an uncertain odynophagia.

Fungal infections Mycoses or fungal infections are often the ﬁrst and can be the most prevalent conditions affecting the oral mucosal surfaces of patients with HIV infection.11,13,19,28,29 The main fungal pathogen involved in oral disease is Candida albicans, however numerous other fungi have been reported as pathogens.11 Atypical or systemic mycoses can have oral manifestations, but these are beyond the scope of this paper. The classic forms of oral candidiasis described below include pseudomembranous candidiasis, erythematous candidiasis, angular cheilitis and chronic hyperplastic candidiasis. Linear gingival Fig. 2 Pseudomembranous candidiasis of the buccal mucosa.

258 ª 2012 Australian Dental Association Clinical and legal issues impacting on dental care diagnosis or poor response to treatment, sampling for risk of dental decay associated with the use of this microscopy and culture or biopsying may be necessary. agent. Oral candidiasis can be treated with 2.5 mL of Chronic hyperplastic candidiasis is associated with miconazole 2% gel dropped on the tongue and kept in smoking, local factors, blood group antigen secretor the mouth for as long as possible before swallowing.31 status and nutritional deficiencies (iron and vitamins A, This should be taken after meals (four times a day) for B1 and B2).32 The lesions are generally considered 14 to 21 days.31 Another treatment option is ampho- premalignant and may demonstrate dysplasia.32 Clini- tericin B, one lozenge slowly dissolved in the mouth cally, they may appear as speckled or homogenous four times a day for 14 to 21 days.31 It should be noted rough white patches that are irregular, unable to be antifungals commonly interact with other medications. wiped off and are indistinguishable from a leukoplakia. An important interaction is the potentiation of warfarin Chronic hyperplastic candidiasis is long-standing and by miconazole. most commonly found on the buccal mucosa, near the Commonly associated with a concurrent infection labial commissures, with less frequent involvement of with Staphylococcus aureus, angular cheilitis may be the palate or tongue where it can be confused with oral evident in addition to fungal lesions in the mouth. hairy leukoplakia. It is usually asymptomatic, although Angular cheilitis, found at the labial commissures, speckled lesions are more likely to cause discomfort. causes an erythematous lesion with red or white fissures Lesions can be clinically diagnosed but due to their or ulcers (Fig. 3). It is asymptomatic or only causes mild premalignant status and the similarity in appearance to to moderate pain ⁄ burning, of intermittent duration but malignant lesions, a biopsy to define and characterize may become chronic. Diagnosis is clinical however the lesion is ideal. A definitive diagnosis should be occasionally, taking a swab for microscopy and culture, sought and ongoing monitoring is necessary. Depend- or a biopsy, may be appropriate if there is an uncertain ing on the histopathology, further treatment or referral diagnosis or the lesion does not respond well to may be necessary. Topical or systemic antifungals and therapy. For angular cheilitis, treat oral candidiasis as surgical therapies are treatment options.32 above and in addition recommend miconazole 2% Treatment for oral candidiasis with topical antifungals cream or gel topically, four times daily to the angles of can be initiated by a general dentist, however prescribing the mouth for at least 14 days, or nystatin 100 000 systemic antifungal therapy is beyond the scope of units ⁄ g cream topically, two to three times daily to the practise for a general dentist. Any lesion that is atypical angles of the mouth for at least 14 days.31 Nystatin or refractory should be considered a candidate for biopsy liquid is sweetened with sucrose, resulting in a potential and histopathological examination. Local or systemic host factors, predisposing to the fungal infections, should be identified and treated. These include a review of current medications, denture fit and hygiene, deficiencies in vitamin A, B1, B2, B9, B12 and iron and conditions that cause immunocompromise, such as diabetes. There is developing resistance to antifungal medications, therefore where fluconazole-resistant forms of candidiasis are present, e.g. Candida glabrata and Candida krusie, mouthwash with ketoconazole can prove effective. If an inadequate response to topical medication is seen after two weeks, increasing the frequency and ⁄ or the dose of medication may be necessary and vacuum- formed treatment trays can be fabricated to hold the antifungal medicament against the infected tissues. For recalcitrant infections, referral to a medical practitioner or a dental specialist such as an oral medicine specialist is required for prescription of systemic antifungals such as ketoconazole, fluconazole or itraconazole. Linear gingival erythema is a gingival condition of immunosuppressed people. Growing evidence supports the theory of a fungal origin for this condition.33,34 It is classified by the American Academy of Periodontology as a disease of fungal aetiology.30 The lack of response of linear gingival erythema to oral hygiene measures and conventional periodontal therapy is important in Fig. 3 Angular cheilitis. diagnosis.35

ª 2012 Australian Dental Association 259 AT McLean et al.

Initially, the lesions present as discrete petechiae on examined and are implicated in the pathogenesis of the gingival margin, which then coalesce into a 1–3 mm chronic periodontitis in people with HIV infection.35 wide, intensely erythematous band. This condition is Necrotizing ulcerative gingivitis (Fig. 4) presents unlike gingivitis induced solely by dental plaque in that with pain, ulceration and gingival bleeding. The lesion the erythema associated with linear gingival erythema is does not involve the alveolar bone35 and is character- disproportionate to any local factors, such as plaque ized by punched out, ulcerated and erythematous and calculus. It is found along the marginal gingivae interdental papillae covered by a greyish necrotic and may be localized or generalized and usually has slough. It is found on the gingival tissues, particularly no significant symptoms, however the gingivae may be the interdental papillae and causes moderate to severe tender and bleed easily. Diagnosis is clinical and by pain, bleeding and fetor oris. Systemic features such as response to oral hygiene and periodontal therapy. The fever, malaise and lymphadenopathy may be present. recommended management for linear gingival erythema Necrotizing ulcerative gingivitis has a sudden onset and is discussed below. short duration, although may be progressive in some cases. Necrotizing ulcerative periodontitis (Fig. 5) presents Bacterial infections similarly to necrotizing ulcerative gingivitis, except the There is a wide range of bacterial pathogens that cause lesion involves the alveolar bone, and potentially, oral disease in patients with HIV infection. This section gingival recession and tooth mobility.35 Onset is sudden considers bacterial periodontal infections associated and the condition can be rapidly progressive. It causes with HIV infection, as well as syphilis and tuberculosis, ulcerated and erythematous gingival and periodontal which are bacterial, non-periodontal infections. tissues. The interdental papillae are covered by a For dentists, one of the most significant oral mani- greyish necrotic slough. Symptoms are the same as festations of HIV-associated bacterial infections is those for necrotizing ulcerative gingivitis. periodontal pathology. In the past, questions regarding Necrotizing ulcerative stomatitis involves an exten- the association of periodontal disease and HIV infec- sive area of oral ulceration, tissue necrosis and ery- tion were raised,39 however further research has thema that extends from the gingivae into the adjacent confirmed the association.44 This pathology falls into mucosa and may involve bone, leading to osteonecrosis three groups: linear gingival erythema, necrotizing and sequestration. It is evident on the periodontal periodontal diseases and accelerated progression of tissues and may extend into the maxillary or mandib- chronic periodontitis. ular bone, with the same symptoms and duration as Linear gingival erythema is primarily a fungal disease necrotizing ulcerative periodontitis. and is discussed above, however it is worth mentioning here as linear gingival erythema may represent a precursor condition to necrotizing ulcerative periodontal diseases associated with HIV infection.35,36 The necrotizing diseases of the periodontium include necrotizing ulcerative gingivitis, periodontitis and stomatitis. The prevalence of necrotizing periodontal diseases associated with HIV infection has reduced with the introduction of modern antiretroviral therapy.35 The reported rates vary from 0.6% to 11%.18,19,37 Necro- tizing ulcerative gingivitis and periodontitis are classi- Fig. 4 Necrotizing ulcerative gingivitis. fied together as related conditions30 and are diagnosed through clinical findings. Necrotizing ulcerative gingivitis, periodontitis and stomatitis are believed to be related, however the exact relationship between the conditions has yet to be fully delineated.28,35 Particu- larly spirochetes, but the usual periodontal pathogens, are believed to be important in the pathogenesis of necrotizing ulcerative gingivitis and periodontitis.38,39 The exact role of Candida species remains to be determined in ulcerative periodontal diseases associated with HIV infection.35 HIV infection seems to enhance the progression of chronic periodontitis.40,41 The periodontopathic bacteria, fungi such as Candida and viruses such as human herpesvirus (HHV) have been Fig. 5 Necrotizing ulcerative periodontitis.

260 ª 2012 Australian Dental Association Clinical and legal issues impacting on dental care

Currently, there is inadequate information to provide syphilis. The significance of syphilis in the context of dentists with evidence-based guidelines for the man- HIV infection is complex. Syphilis and HIV co-facilitate agement of periodontal infections in people with transmission and there are many similarities in the HIV.42,43 Periodontal diseases should be treated as appearance of syphilitic and HIV-associated lesions. they would in people without HIV infection, with The treatment of syphilis, as well as other sexually removal of plaque, calculus and necrotic tissue.35,42,44 transmissible infections, will decrease HIV trans- Excellent home oral hygiene should be encouraged and mission risk. If syphilis is suspected, referral to a smoking cessation recommended. Adjunctive therapies medical practitioner for investigation and treatment is and the prescription of systemic antibiotics should be appropriate. considered on a case-by-case basis.35,42,44 Adjunctive Tuberculosis (TB) is caused by Mycobacterium therapies include irrigation and rinsing with 10% tuberculosis.46 The atypical mycobacteria are beyond povidine iodine or alternatively 15 mL chlorhexidine the scope of this document. People with HIV infection 0.12%–0.2% mouthwash, rinsed in the mouth for one may develop TB via primary infection, reactivation of minute, 8 to 12 hourly.31 Chlorhexidine should only be latent infection and re-infection with new strains. TB is used on a short-term basis as prolonged periods of use rare in Australian-born people but much more common may cause discolouration of teeth and restorations. in those born, or who have lived, in countries of high Narrow spectrum antibiotics, such as metronidazole TB prevalence.46 Occasionally, TB may present as (400 mg orally [or for a child; 10 mg ⁄ kg up to chronic ulcers with a grey-yellow slough in the mouth 400 mg], 12 hourly for five days31), are preferable to which, when examined histologically, demonstrate the broad spectrum antibiotics, to reduce the likelihood presence of granulomas or granulomatous inflamma- of overgrowth of commensals and antibiotic resis- tion. There may also be lymphadenopathy in the head tance.35,44 The use of antifungals may be considered and neck. TB can occur at any CD4 cell level, however due to the implication of fungal microorganisms in the frequency and severity of disease is inversely periodontal disease pathogenesis,35 and this should proportional to the CD4 cell level. TB presents only be managed by medical practitioners and dental significant infection control issues. If the patient has specialists. The initial treatment options for linear active disease then transmission based precautions are gingival erythema should be standard periodontal necessary and, if possible, dental treatment should be therapy plus adjunctive therapies, such as 10% povi- postponed. If a patient has suspected TB, referral to a dine iodine or 0.12%–0.2% chlorhexidine, and con- medical practitioner for investigation and management sideration of the use of antifungals or antibiotics.35 If a is necessary. dentist feels inadequately equipped to manage periodontitis in people with HIV or if they fail to control Viral infections the disease, then referral to a periodontist, a general practice dentist with an interest in HIV infection or a There are seven groups of viruses that commonly cause specialized clinic at a major hospital, is required. oral lesions. Patients co-infected with HIV and with any Syphilis is caused by the bacterium Treponema of these viruses are at increased risk of developing oral pallidum, subspecies pallidum. Syphilis causes primary, conditions.27 The viral groups include herpes simplex secondary and tertiary disease and atypical presenta- virus (HSV 1 and 2), varicella zoster virus (VZV), tions of syphilis are common. The primary lesion of cytomegalovirus (CMV), human papilloma virus (HPV syphilis develops after a few weeks and is characterized many subtypes), Epstein-Barr virus (EBV), molluscum by the chancre, which presents as an asymptomatic, contagiosum virus 2 (MCV2) and human herpesvirus 8 clean-based, shallow but indurated ulcer.45 Chancres (HHV8).28 may be found in the mouth and are sometimes In a person with HIV infection, co-infection with associated with regional lymphadenopathy.45 The sec- these viruses may manifest in the oral cavity in a typical ondary manifestations of syphilis take a few months to manner, similar to the pattern of infection seen in an develop and most commonly involve lymphadenopathy immunocompetent person. However, the infections are and a systemic rash, usually red-brown in colour but more likely to be unusual, severe, widespread and often variable. Oral features include diffuse erythema recurrent. Also, the viruses can be involved in the or mucous patches, which fuse to form snail track formation of neoplasms and oral lesions that would be ulcers. Tertiary syphilis can present as neurosyphilis, considered unconventional in an immunocompetent cardiovascular syphilis and gummas. Gummas may person. The prevalence of oral viral infections increases occur in the mouth and the lesions range in size from with reducing CD4 cell count.12,17,19 The viral infec- microscopic to a number of centimetres in diameter. tions may be primary infections or a reactivation of Gummas are chronic, asymptomatic, indurated nodular latent infections due to reduced immune surveillance.28 or ulcerative lesions. Atrophic glossitis and syphilitic The oral manifestations of viral co-infections with HIV leukoplakia are other oral manifestations of tertiary are discussed below. Treatment of viral infections, on

ª 2012 Australian Dental Association 261 AT McLean et al. the whole, should be done by a medical practitioner or valaciclovir, can reduce illness severity and complica- dental specialist. tions. HZ in the ophthalmic (V1) distribution of the HSV has two main types, type 1 and type 2. HSV, trigeminal nerve requires ophthalmological referral to when it appears on the lips, is known as herpes labialis minimize ocular complications. or a cold sore. Primary HSV infection may be very In people with HIV infection, CMV can present with severe, whereas recurrent infections are usually less a wide array of complications such as gastrointestinal severe. Disseminated infection and herpes encephalitis tract ulceration, hepatitis, encephalitis, retinitis, leuko- is possible. Herpes labialis presents as multiple small penia and respiratory infections.28,48 There is a rela- vesicles or ulcers on the lips and may include adjacent tionship between CMV infection and xerostomia in skin. Intraoral HSV infection presents as small, round people with HIV infection48 and relapse after treatment vesicles that rupture, leaving shallow ulcers that can is common.28 CMV causes punched out ulcers from coalesce. The lesions are superimposed on an inflamed, millimetres to several centimetres in diameter that can erythematous base. In people with HIV infection, erode deep into tissues. These ulcers are mainly found recurrent HSV infection is common.47 on the palate or gingiva, but occasionally the buccal Lesions occur on the lips and anywhere in the oral mucosa, tongue and pharynx. The oral ulcers can cause cavity. In the mouth, HSV is commonly found on mild to severe pain and xerostomia, and the duration is keratinized epithelium, including hard palate, gingiva variable. Biopsy and culture may be used in diagnosis. and dorsum of the tongue, but in people with HIV Medical practitioners may prescribe antiviral medica- infection it can sometimes be found on non-keratinized tion such as ganciclovir or foscarnet to treat CMV epithelium.28 Prodromal symptoms may be present infection. before the rapid onset of lesions, persisting for A variety of benign mucocutaneous lesions are 7–14 days causing mild to severe pain. They may be induced by the HPVs, including verruca vulgaris, localized or widespread, involving the entire oral cavity condyloma acuminatum, focal epithelial hyperplasia and lips. Fever, lymphadenopathy and other symptoms (Heck’s Disease) and squamous papilloma. Verruca may occur, especially with a primary infection. A vulgaris is connected with HPV types 1, 2 and 7.49 diagnosis can be made from history and examination, Condyloma acuminatum is associated with HPV or if uncertain, a swab for PCR analysis can be types 6 and 11.49 HPV types 13 and 32 are linked to performed. focal epithelial hyperplasia.49 Multiple HPV strains No treatment for HSV is required if symptoms are are linked with oropharyngeal squamous cell mild, although treatment of symptoms may be neces- carcinoma.47,50 sary. Severe or recurrent infections should be treated by Verruca vulgaris, also known as the common wart, a medical practitioner or dental specialist with topical may present as multiple, large and disfiguring lesions in and ⁄ or oral antiviral medications such as aciclovir, conjunction with HIV infection, but most commonly famciclovir or valaciclovir. the presentation is typical (Fig. 6).47 There may be VZV is the herpes virus that causes the primary single or multiple cauliflower-like growths with a white infection known as chicken pox and can reactivate from or pink surface. Lesions of varying diameter, either a latent state to cause herpes zoster (HZ) or shingles. sessile or pedunculated, are found anywhere in the oral The pattern of VZV infection is generalized in primary cavity but more commonly seen on the labial mucosa. infection, however HZ infection is usually uniderma- Usually asymptomatic, lesions may be present for years. tomal but can be multidermatomal or dissemi- Commonly a clinical diagnosis is sufficient, however a nated.28,47 VZV infection can be recurrent.47 biopsy is definitive. Intraorally, VZV presents as a roughly linear erup- Condyloma acuminatum, also known as the venereal tion of herpetiform vesicles or bullae that ulcerate and wart, is characteristically found on anogenital mucosa, may coalesce. Extraorally, the vesicles can ulcerate and however warts may also be seen on oral mucosa and form a crust or scab. The vesicles or ulcers are bordered may present as multiple, large and disfiguring lesions in by erythema and their distribution corresponds to a association with HIV infection.47 Condyloma acumin- branch of a sensory nerve, such as the trigeminal nerve. atum may present as single or multiple lesions of There may be prodromal symptoms present and the varying sizes, which are soft and have a pink to grey rash causes mild to severe pain. The duration of VZV is appearance. Often multiple nodules coalesce to form usually 10–14 days, although infections can become pedunculated or sessile papillary growths. They can chronic and leave scarring. A diagnosis may be made on be found on any mucosal surface, particularly the clinical findings, although a swab for PCR analysis may ventral tongue, gingiva, labial mucosa and palate. be performed if diagnosis is uncertain. Although the lesions are normally asymptomatic, the In the setting of immunocompromise, urgent review condition is often chronic. Diagnosis is made on clinical of VZV for consideration of treatment is required. findings, however for a definitive diagnosis, biopsy is Antiviral medications, such as aciclovir, famciclovir or recommended.

262 ª 2012 Australian Dental Association Clinical and legal issues impacting on dental care

Fig. 7 Oral hairy leukoplakia on the lateral surface of the tongue.

Fig. 6 Verruca vulgaris of the retromolar region. OHL is a chronic condition and diagnosis is possible with clinical findings and ⁄ or biopsy. Specific treatment is not indicated due to the benign and asymptomatic Management of condyloma acuminatum can be by a nature of OHL. Modern therapies such as cART and general dentist with experience in this area. Otherwise topical treatments can reduce the prevalence of OHL in consider referral to a medical practitioner, such as a patients with HIV infection.37,55 OHL usually resolves dermatologist or to an oral medicine specialist or oral following the introduction of effective antiretroviral and maxillofacial surgeon for treatment, if warranted. therapy, although it may recur after stopping treat- Medical and surgical treatment may be appropriate ment.56 depending on the site, characteristics and number.49 MCV is a poxvirus. There are four types of MCV, Options include excision, electrosurgery, cryosurgery, however MCV2 is responsible for orofacial disease in 28 CO2 laser, topical podophyllin resin ⁄ interferon alpha patients with HIV infection. MCV is spread by direct injections,49 podophyllotoxin, salicylic acid, tricholor- skin-to-skin contact and involves flesh coloured domes, acetic acid, bichloroacetic acid or imiquimod.47 2–6 mm in size or larger, with a central umbilication. EBV is also known as human herpesvirus type 4 MCV can be found anywhere on the body and pruritis (HHV4). EBV has been connected to infectious mono- is the most prevalent symptom. Infections last for nucleosis, Burkitt’s lymphoma, non-Hodgkin’s lym- months although can become chronic. Diagnosis for phoma and nasopharyngeal carcinoma.28 The chief MCV is clinical, with a biopsy rarely required. No manifestation of EBV in people with HIV infection is treatment is necessary for MCV, although it usually oral hairy leukoplakia (OHL), and so EBV and OHL responds well to cryotherapy. Other treatments such as will be discussed together. EBV has been linked to oral curettage, cantharidin and imiquimod can be tried. ulceration in patients with advanced HIV infection.51 Referral to a medical practitioner or dental specialist EBV is found mainly in B lymphocytes but also in for treatment is recommended. epithelial cells and salivary gland tissue.52 OHL is HHV8 infection has been implicated in oral ulcera- induced and maintained by repeated direct infection tion in patients with HIV infection51 and HIV infection of the epithelial cells by EBV in the saliva52 and is in conjunction with HHV8 infection has a strong associated with EBV and immunosuppression. OHL association with the development of Kaposi’s sarcoma has rarely been reported in immunocompetent people (KS; see below for more information). HHV8 is without HIV infection53 and may be considered a transmitted by exposure to contaminated body fluids. marker of disease progression.17 As CD4 cell counts fall in the context of HIV infection, OHL is increasingly Oral neoplasms found and it is common when the CD4 count drops below 150 cells ⁄ lL.27 Reported rates of OHL in There are two common malignancies associated with untreated patients with HIV infection range from HIV infection that may have oral involvement: KS and 0% to 24%,12–14,19,54 however actual rates may be non-Hodgkin’s lymphoma (NHL). KS and NHL were greater.11,28 OHL lesions present as whitish, elevated, the most common forms of cancer associated with non-removable patches of variable size (Fig. 7). HIV infection in the pre-antiretroviral era but with Characteristically, the surface of the lesion has vertical treatment, cancers not associated with advanced HIV ridges but smooth lesions can occur. Lesions are found infection are now more prevalent than KS and NHL.57 on the lateral borders of the tongue and sometimes they At present there is insufficient evidence to establish a may extend onto the ventral and dorsal surfaces of the direct relationship between oral squamous cell carci- tongue and occasionally on the buccal mucosa. noma and HIV infection, although there are a limited

ª 2012 Australian Dental Association 263 AT McLean et al. number of studies suggesting a connection between the are increasing.50 HIV infection in association with EBV two diseases.11 Management of oral neoplasms should can induce NHL. AIDS-related NHL is B-cell derived, be by medical practitioners or oral and maxillofacial with 70% of cases systemic and 30% primarily surgeons with appropriate experience. General dentists involving the central nervous system.61 Presentation can play a limited role in holistic treatment of oral varies according to histological type and extra-nodal neoplasms, but should be guided by their medical involvement is common. colleagues. NHL symptoms are generalized (B-symptoms) and KS was the most common malignancy associated include fever, night sweats and weight loss. Intraorally, with HIV infection,58 however rates have significantly NHL is a diffuse, rapidly proliferating, red-purple mass, decreased with cART.59 In 22% of cases, oral mani- which often occurs on the palatal-retromolar complex. festations are the initial presentation and a majority Confirmation of NHL is by biopsy which is best carried will have oral involvement at some point.58 KS is an out by a medical practitioner or dental specialist. endothelial cell malignancy associated with HHV8 and Following confirmation, referral to appropriate medical HIV infection.60 There are a number of different forms specialists for consideration of treatment options is of the disease but all are believed to represent aspects of warranted. NHL is chronic without treatment and the same pathological process. KS presents initially as a medical management may include surgical resection, symptomatic red macule which enlarges to form a red- chemotherapy, radiotherapy or palliation. It should be blue plaque (Fig. 8). These plaques may grow into realized that there can be many oral complications of lobulated nodules that potentially ulcerate and some- radiotherapy and chemotherapy. times cause pain. The lesions can be red, purple, blue or brown in colour and range from flat macules to Neurological conditions ulcerated nodular masses. KS can be found on the skin or mucous membranes and, in the mouth, KS most There are many neurological conditions associated commonly involves the hard palate, followed by the with HIV infection and cART. These conditions may gingiva and buccal mucosa. have a direct or indirect impact on the oral cavity and KS lesions are chronic unless treated and diagnosis is include sensory neuropathy, e.g. trigeminal neuralgia, usually based on clinical and histopathological findings. and motor neuropathy, such as facial nerve palsy. Any treatment related to intraoral KS should be Another condition of relevance to dentists is undertaken only in conjunction with the patient’s HIV-associated neurocognitive disorders, e.g. HIV- medical team. Biopsy carries a significant risk of associated dementia. haemorrhage as the lesions are extremely vascular and this should be avoided by the general dental practi- Other oral conditions that may be associated with HIV tioner. Often commencement of cART can lead to infection spontaneous resolution of these lesions. Systemic chemotherapy, intra-lesional chemotherapy and radiother- Hyperpigmentation, aphthous ulceration and xerosto- apy are treatment modalities that may be employed. mia have been documented as occurring in the context However, it should be realized that there can be many of HIV infection, however at this stage the relationship oral complications of radiotherapy and chemotherapy. between these conditions and HIV is yet to be fully Rates of HIV-associated NHL decreased with cART, delineated. however overall rates of NHL have continued to rise as In a review of seven studies, hyperpigmentation was a large proportion of NHL is not related to advanced found at a rate of 2.2% of people living with HIV.62 HIV infection and background levels of this malignancy The exact cause of this low level of hyperpigmentation is uncertain, however it may be attributable to the combined effects of HIV infection and cART. There are three types of aphthous ulcers: major, minor and herpetiform. The ulcers are of uncertain origin but immune mechanisms are implicated in the pathogenesis, as well as local and systemic factors. Deficiencies in iron, folate and vitamin B12 may predispose individuals to recurrent aphthous ulcers.63 The ulcers may be preceded by prodromal symptoms and may cause considerable discomfort. Generally, biopsies are not helpful in diagnosing aphthous ulceration as diagnosis can be made with a degree of certainty with a thorough history and examination. Fig. 8 Kaposi’s sarcoma. However, a biopsy may be necessary when the clinical

264 ª 2012 Australian Dental Association Clinical and legal issues impacting on dental care diagnosis is not certain and can be used to determine in adults but more commonly in children.62 Xerostomia other causes for the ulceration, e.g. malignancy. can reduce quality of life and lead to many dental Major aphthous ulcers are characterized by a number complications. Along with the usual management of ulcers, each of which are greater than 10 mm in options for xerostomia, consultation with the treating diameter, on any keratinized or non-keratinized oral medical practitioner may be relevant, to discuss mucosa, such as the lips, cheeks, tongue, palate and whether medications can be altered to improve the side pharynx. Lasting longer than 30 days, they may appear effect profile. Consideration should be given to the at monthly intervals and heal with scarring. referral to an oral medicine specialist for assessment Minor aphthous ulcers are found on non-keratinized of suitability for pilocarpine, a salivary stimulant, oral mucosa, such as the lips, cheeks and lateral tongue, although there are risks of adverse effects.31 and are a collection of ulcers, each less than 10 mm in diameter. Lasting one to two weeks, they usually heal Oral conditions associated with HIV treatment without scarring and can recur every one to four months. HIV medications can cause a taste disturbance. Dry lips Herpetiform aphthous ulcers are identified by larger are associated with HIV treatment, particularly the numbers of ulcers, each 1–2 mm in diameter, which protease inhibitor, indinavir. The cracking and crusting may occur anywhere but generally tend to be found on of the lips can be extremely uncomfortable and the non-keratinized oral mucosa (lips, cheeks, tongue, unaesthetic. Protective creams designed for use on the palate, floor of mouth and pharynx). These ulcers last lips, such as papaya-based lip ointments can be helpful for 10–30 days and may recur at monthly intervals. in alleviating this condition. Dental management of aphthous ulcers involves Other conditions associated with HIV treatment recommending that the patient avoid any specific include xerostomia, oral ulceration, erythema multi- triggers such as stress, poor diet or trauma. A review forme (Stevens–Johnson syndrome), lichenoid reactions of medications may also be suitable to reduce the risk of and hyperpigmentation. There is the potential that medications contributing to aphthous ulcers. Topical many drugs prescribed by dentists may interact with agents may reduce ulcer severity and recurrence, cART, therefore medications should always be pre- however evidence is limited for most interventions.64,65 scribed in consultation with the patient’s medical Management of mild lesions includes topical anaes- practitioner(s). thetic agents (lignocaine gel 2% topically every three hours31) and the use of chlorhexidine gel (chlorhexidine HIV and tooth decay 0.05% topically every three hours).31 Lignocaine gel must be used with caution in patients with cardiac, Dental caries can cause a significant burden of disease hepatic or renal disease.31 Topical corticosteroids and affect quality of life for people with HIV infec- (betamethasone dipropionate 0.05% ointment applied tion.66 Access to dental care improves oral hygiene and topically to the lesion twice a day after meals,31 or quality of life in people with advanced HIV infection. triamcinolone acetonide 0.1% paste applied topically Xerostomia, the most important factor in the develop- to the lesions three times a day after meals) may also be ment of dental caries, can be directly linked to HIV considered. infection or its treatment. The most serious complica- Severe ulceration or ulceration in the context of tion of dental caries is the occurrence of a potentially neutropenia necessitates specialist review. Ulceration life-threatening infection, which is an important con- that is unresponsive to topical treatments can be trialled sideration in immunocompromised people. Limiting on systemic corticosteroids or thalidomide following a tooth decay through the usual methods, with consider- review by a medical specialist.65 Corticosteroids are ation given to patient, dietary and dental factors, is associated with a real risk of side effects, although recommended. topical corticosteroids rarely have systemic side effects. As a result, side effects should be regularly monitored Medico-legal implications of HIV management in when using both topical and systemic corticosteroids. Australia Medical management of aphthous ulcers should include haematological investigations to exclude anaemia or Medico-legal issues related to the management of haematinic deficiency. patients can be complex and decisions must not be Xerostomia affects 2–10% of people with HIV taken lightly. The following provides an overview of infection. 62 The cause of xerostomia is multifactorial some central considerations applicable to the and can include a CD8 lympho-cytosis syndrome management of HIV-infected patients, however it is related to HIV infection, side effects of medications or not legal advice. In cases involving individual patients, opportunistic infections of the salivary tissue. Enlarge- dental practitioners should seek independent legal ment of salivary glands occurs at a rate of less than 1% recommendations.

ª 2012 Australian Dental Association 265 AT McLean et al.

Confidentiality Discrimination People with HIV infection are not required by law to All healthcare professionals are bound by legislation disclose their HIV status to dentists, doctors or other that makes it illegal to discriminate on the basis of HIV healthcare professionals. HIV service organizations status. HIV is covered by both Commonwealth and encourage people with HIV infection to consider state ⁄ territory legislation. The Commonwealth Disabil- disclosure when having a medical examination, treat- ity Discrimination Act not only protects people living ment or procedure as there is the potential for HIV with HIV, but also people believed to have HIV and medication and related conditions to affect other people who associate with people living with HIV or treatments or therapies. However, services advise that believed to be HIV-infected. As dentists should such decisions must be made carefully given many maintain standard infection control procedures at all people living with HIV have experienced stigma and times, a person’s HIV status should have no influence discrimination from healthcare professionals following on a dentist’s level of precaution or infection control disclosure.67 practices. When a person discloses his or her HIV positive status, dentists and all other healthcare professionals Management of symptoms indicative of HIV infection have a broad duty under state, territory or federal privacy laws to ensure confidentiality is maintained. A team approach should be adopted for any HIV- That duty extends to the collection, storage and associated oral manifestation, however the approach protection of health records. Dental practices should to the management of a patient with a suspected employ procedures to only grant access to information HIV-associated lesion should differ depending on to those people who are authorized to have access, in whether or not the patient’s HIV status is known. order to use or disclose the information for the purpose The algorithm in Fig. 9 highlights the different for which it was collected. Of equal importance are processes. Medical practitioners, mainly infectious security measures to prevent unauthorized access to the disease specialists or immunologists, deal with most records and where practicable, procedures for storing of the HIV cases in Australia. There are general the information in a way that the identity of the person medical practitioners who have further training in is not readily apparent from the face of the record, e.g. HIV medicine and are qualified to prescribe medica- by the use of identification codes. Procedures for tion for HIV in primary care. Dental specialists such destroying the records to protect the privacy of the as those in oral medicine or oral and maxillofacial information, where the record is not to be retained, surgery are likely to be the best equipped to deal with must also be in place. the oral manifestations of HIV. Other dental spe- Principles governing the use and disclosure of cialists and general dentists, especially those with an health information are set out in the Commonwealth interest in HIV medicine can play a role in the Privacy Act. In short, healthcare workers must not treatment of the oral diseases associated with HIV. disclose a person’s health information without There is a limited but important role for the general consent except in a very limited number of circum- dental practitioner to treat the oral manifestations of stances, which include instances where an organiza- HIV infection, however it is important they practise tion reasonably believes that the use or disclosure is within their scope of practice and seek advice or refer necessary to lessen or prevent a serious and imminent when uncertain about management. threat to an individual’s life, health or safety, or a If the patient has disclosed that he or she is HIV serious threat to public health or public safety. Such positive, the dental management of HIV-associated instances include the case of needle-stick injury where oral manifestations should occur in consultation with a healthcare professional is aware of a patient’s HIV the patient’s medical practitioners and relevant dental positive status and a healthcare worker has been specialists, where appropriate. If a patient is found to exposed in circumstances where there is a real risk of have oral manifestations indicative of HIV but has not transmission. In this situation, if it is not possible to disclosed that he or she is HIV positive, a different conceal the identity of the source patient who has approach is required. Such a situation may arise refused to consent to disclosure, disclosure may be because a person is not HIV-infected, is unaware they relevant. Another scenario regards a particular are HIV-infected, or has chosen not to disclose their instance of care where there is a need to know the known HIV positive status. The dentist should infection status for treatment purposes of benefit communicate his or her concerns to the patient about to the patient (e.g. in an emergency or if the patient the potential significance of any suspicious lesion. is unconscious). This should not, however, detract Importantly, that information should be framed from the observance of standard infection control within the context that all oral manifestations of precautions.68 HIV are not pathognomonic. It is important to

266 ª 2012 Australian Dental Association Clinical and legal issues impacting on dental care

When an HIV-associated lesion is found

Review and recheck the medical history

Patient's HIV status unknown Patient is HIV positive

Advise patient of the provisional diagnosis Advise the patient of the provisional diagnosis and the association between the lesion and HIV infection or other conditions. Explain that lesions known to be associated with HIV can Carry out any urgent treatment as needed by † occur in healthy people the patient

Carry out any urgent treatment as needed by the patient†

Recommend referral to The patient should Suggest that if the their general medical be advised that there HIV test is positive, practitioner as soon as is a potential for it may be beneficial possible for a full check-up HIV transmission, if to make a review and an HIV test with informed positive, and should appointment with consent. A referral avoid behaviour you to explain the ‡ letter should be given to which has a risk of impact of HIV the patient, and permission HIV transmission infection on oral should be obtained to send (unprotected sex health and potential a copy of the referral letter and sharing injecting management to the patient’s medical drug use equipment) options § practitioner

Follow-up with the patient after 7 days to ensure he or she has presented to a GP or sexual health clinic

A referral letter‡ should be Investigate the lesion as required or consider given to the patient and referring the patient for assessment permission should be obtained to send a copy to the specialist who will Manage the patient as indicated but if you do manage the lesion.§ If the not feel qualified then consider referral patient agrees, a copy of the referral letter should also be sent to the patient’s medical practitioner(s)

†Any treatment should be initiated in consultation with the patient’s general medical practitioner and/or with specialists as necessary. ‡A referral letter should contain patient details, reason for referral, examination findings, diagnosis, and details of treatment. §If a patient declines referral for follow-up or to have a referral sent to their general medical practitioner or specialist, then it is necessary to consult with a senior colleague and obtain a medico- legal opinion about the necessary steps that should be undertaken to follow-up the patient. There may be circumstances, although rare, where a breach of confidentiality is legally permissible in order to have the patient adequately followed up. Fig. 9 Algorithm for the management of oral manifestations indicative of HIV infection. provide the patient with a sense of concern, support, positive. Patient support services are available through understanding and care and to reassure the patient state and territory AIDS councils. about conﬁdentiality. If a patient declines a referral for follow-up or to The dentist should recommend the patient visits their have a referral sent to a GP or specialist, it will be general medical practitioner (GP) or local sexual health necessary to consult with a senior colleague and obtain clinic for assessment of risk factors indicating HIV a medico-legal opinion. There may be circumstances testing is required, as per the National HIV Testing where a breach of conﬁdentiality is legally permissible if Policy.68 Until HIV status is known, the patient should a patient is unwilling to seek further medical advice ⁄ be advised to avoid behaviours that could potentially care but doing so is necessary to ensure adequate result in HIV transmission if they are in fact HIV follow-up of a patient’s symptoms, to access medical

ª 2012 Australian Dental Association 267 AT McLean et al. care for him ⁄ her self and ⁄ or to ensure others are not put implications associated with HIV diagnosis and at risk of HIV infection. The National HIV Testing treatment. Policy68 states that HIV testing should be voluntary and based on informed consent. Forcing a person to be tested for HIV is considered highly invasive, and ACKNOWLEDGEMENTS consequently such actions are covered by public health Thank you to Iain Stewart Brady and colleagues from legislation. Such orders are extremely rare. Instead, the HIV ⁄ AIDS Legal Centre Inc. for guidance, state health departments generally rely on formal Dr Wayne Sherson for reviewing the original content public health mechanisms to manage people with and Dr Liz Coates and Dr Sharon Liberali for providing HIV infection who are at risk of transmitting the the source material and images. The information infection to others. Under those mechanisms, there is a contained in the review article is based on the profession strong commitment to assist healthcare providers to based booklet, Dentists and HIV, developed by the manage challenging and difficult cases with as little Australasian Society for HIV Medicine (ASHM) in 2011 intervention as possible. There is unlikely to be and funded by the Australian Government Department pressure to disclose confidential information about a of Health and Ageing. The original resource is available patient in the first instance, with healthcare workers at www.ashm.org.au/dentistsHIV. frequently remaining responsible for the patients about whom they contact. In general, healthcare providers should not hesitate to contact their health department DISCLOSURE for support and guidance from their state expert panel All authors of this paper were employed by the on those who may place others at risk of HIV Australasian Society for HIV Medicine (ASHM) to infection. develop the original resource (Dentists and HIV ) from which this review article is adapted from. Support and referral pathways

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