Date of current publication: April 12, 2023
Lead author: Abhiram Maddi, PhD, MS, DDS
Contributor: Stephen N. Abel, DDS, MSD
Writing group: Joseph P. McGowan, MD, FACP, FIDSA; Steven M. Fine, MD, PhD; Rona Vail, MD; Samuel T. Merrick, MD; Asa Radix, MD, MPH, PhD; Christopher J. Hoffmann, MD, MPH; Charles J. Gonzalez, MD
Committee: Dental Standards of Care Committee
Date of original publication: March 8, 2017
In some patients with HIV, immunosuppression may allow the development of oral and periodontal lesions Polvora, et al. 2018; Baccaglini, et al. 2007. Chronic periodontitis can influence systemic inflammation favoring viral replication, and periodontal pockets may serve as reservoirs for the virus Polvora, et al. 2018. Periodontal lesions associated with HIV include linear gingival erythema (LGE) and necrotizing periodontal diseases, which are subclassified as necrotizing ulcerative gingivitis (NUG), necrotizing ulcerative periodontitis (NUP), and necrotizing ulcerative stomatitis (NUS/NS). NUP and NUS/NS may represent different stages of the same pathologic process, with NUP being a more advanced stage of NUG Ryder, et al. 2012; Kaplan, et al. 2009. As the population with HIV ages, patients may develop chronic conditions that can contribute to an exacerbated or enhanced progression of chronic adult periodontitis Stabholz, et al. 2010. There is also a concern about oral hygiene care and the incidence of periodontal disease in youth with perinatally acquired HIV, who may be at higher risk for developing significant periodontal disease associated with tooth loss and HIV progression. Frequent dental care is needed to prevent potential periodontal progression in this population Ryder, et al. 2020; Moscicki, et al. 2019. Stricter periodontal recall and oral hygiene care within older/aging and perinatally infected youth are critical.
The identification of periodontal diseases may be critical even in patients receiving antiretroviral therapy (ART). While the introduction of highly active ART has significantly reduced this incidence Ntolou, et al. 2023; Mataftsi, et al. 2011, the occurrence of oral and periodontal infections despite ART may indicate the failure of ART or the development of viral resistance Mataftsi, et al. 2011. It has also been suggested that the oral microbiome of patients on ART may affect systemic and periodontal inflammation. A shift in the microbiome is most likely due to a complex relationship between HIV, ART, and aging Griffen, et al. 2019; Toljic, et al. 2018; Noguera-Julian, et al. 2017.
HIV-associated periodontal diseases, along with oral infections, are considered serious complications of HIV. The incidence of periodontal infections in patients with HIV is lower than the incidence of oral infections Ryder, et al. 2012, but the increasing severity of periodontal diseases in the aging population of patients with HIV is a concern. Thus, there is a need to closely monitor these populations for the worsening of periodontal conditions Ryder, et al. 2020; Groenewegen, et al. 2019.
Management of periodontal lesions in patients with HIV has changed little in the past 30 years Goncalves, et al. 2013; Ryder, et al. 2012. Basic periodontal therapy provided at regular periodic intervals can effectively reduce periodontal inflammation in HIV patients Valentine, et al. 2016. Removal of local irritants from the root surfaces, mechanical debridement of necrotic tissues, and appropriate use of local and systemic antibiotics remain essential components of the management of HIV-associated gingival and periodontal diseases. The interaction between bacteria and Candida may play a vital role in the etiology of periodontal lesions; therefore, the management of HIV-associated periodontal lesions involves treating both bacteria and fungi Pihlstrom, et al. 2005. Multiple factors affect response to treatment, including immune status and personal oral hygiene practices of keeping the mouth, gums, and teeth clean Alpagot, et al. 2004.
Linear Gingival Erythema (LGE)
Presentation and Diagnosis
LGE characteristically presents as a distinct 2- to 3-mm-wide linear erythematous band limited to the free gingival margin (see Appendix: Photo- and Radiographs of Periodontal Disease Associated With HIV for images).
LGE typically presents at the anterior teeth initially Cherry-Peppers, et al. 2003, with subsequent progression to the posterior dentition Ryder, et al. 2012. Clinically, it may be difficult to distinguish LGE from severe gingivitis in patients with poor plaque control. LGE lesions do not resolve or respond to conventional periodontal therapy, including plaque control, scaling, and root planing. Initial biopsy is not indicated for diagnosis unless the tissue does not heal after follow-up because no microscopic appearance specific to LGE exists. X-rays may be used to rule out alveolar bone involvement.
LGE is classified as a gingival disease of fungal origin by the American Academy of Periodontology because Candida is the primary etiological factor Armitage 1999. LGE lesions often resolve with topical and/or systemic antifungal treatment. Data are unavailable to establish whether LGE will evolve into a more severe form of periodontal disease; however, LGE may be a predecessor to the necrotizing ulcerative periodontal diseases that present in some patients with HIV Goncalves, et al. 2013. If LGE lesions do not resolve after 1 month of therapy, a biopsy may then help indicate a different diagnosis Ryder, et al. 2012.
Conventional periodontal therapy does not adequately treat LGE, likely because of the presence of yeast within the gingival tissues Patton 2000; Candida is the etiological factor. Treatment for LGE includes oral hygiene instructions and mechanical supragingival debridement using minimal pressure on soft tissue to remove plaque Herrera, et al. 2014. Oral antimicrobial rinses are effective in treating LGE. As a first-line treatment, patients should rinse twice daily with a 0.12% chlorhexidine gluconate suspension (a broad-spectrum oral antimicrobial) and be re-examined after 2 weeks. If lesions are persistent, topical antifungal medications can be used Cherry-Peppers, et al. 2003.
Necrotizing Ulcerative Gingivitis and Necrotizing Ulcerative Periodontitis (NUG/NUP)
NUG and NUP are periodontal conditions that may be present in patients who do not have HIV, but both are more commonly associated with HIV and other systemic conditions Bodhade, et al. 2011.
Because of their similar clinical appearance and treatment, most studies have tended to classify NUG and NUP together as necrotizing periodontal lesions. Additionally, Candida organisms may be present in the tissues of NUP sites among patients with HIV, which suggests that Candida may have a role in HIV-associated NUP. Because of the presence of Candida in both LGE and NUG/NUP lesions, the possibility exists that LGE is a precursor to the development of NUG/NUP lesions. NUG and NUP are considered to be on the spectrum of the same pathologic process Ryder, et al. 2012; Bodhade, et al. 2011; Patton and McKaig 1998; Robinson, et al. 1998; hence, early diagnosis and intervention will be effective in treating necrotizing periodontal diseases.
Presentation and Diagnosis
NUG, formerly referred to as acute necrotizing ulcerative gingivitis (ANUG), characteristically presents as a rapid onset of ulcerations of the interdental papilla with gingival bleeding and severe pain. Lesions are typically described as having a “punched out” appearance of the papilla, and the affected tissue appears to be covered with a fibrinous pseudomembrane (see Appendix: Photo- and Radiographs of Periodontal Disease Associated With HIV for images). Biopsy is not initially indicated for diagnosis unless the tissue does not show evidence of healing.
NUP lesions are similar in appearance to NUG lesions; however, NUP lesions extend into and destroy the alveolar bone. Patients with NUP frequently present with exposed bone, gingival recession, and tooth mobility. These clinical signs and symptoms do not necessarily involve the entire periodontium; only localized areas of the tooth-bearing bone and associated soft tissues may be affected. NUP is characterized by rapid destruction of bone that often leads to tooth loss, severe deep jaw pain, widespread soft tissue necrosis, bleeding, and fetid mouth odor. Other signs and symptoms of NUG and NUP include swelling of the regional lymph nodes, fever, and malaise. These clinical findings do not present in all patients and are considered secondary presentations of disease. The presence of NUP may be indicative of severe or worsening immunosuppression Ryder, et al. 2012; Bodhade, et al. 2011.
Treatment initiation as soon as possible following the diagnosis of acute NUG/NUP is important to alleviate pain and tissue destruction. The well-established standard of care for NUG/NUP treatment by the oral health care provider includes debridement of infected areas; scaling and root planing of the teeth as needed; and intrasulcular lavage/irrigation with either 0.12% chlorhexidine gluconate or, as an alternative, 10% povidone-iodine Herrera, et al. 2014. This standard of care is based on the principle of eliminating or reducing the microbial load by mechanically removing debris and plaque Hofer, et al. 2002. Such practices have been rigorously used over many years in the management of periodontal diseases in patients with HIV Ryder, et al. 2012; Mealey 1996; Holmstrup and Westergaard 1994; Winkler, et al. 1989. In severe cases or nonresponding conditions, systemic antimicrobials should be used as an adjunct to standard treatment Herrera, et al. 2014. Because the use of prophylactic antibiotic therapy might risk candidiasis Herrera, et al. 2014; Mealey 1996, the best option for antimicrobial therapy is metronidazole with an antifungal agent to prevent the development of a secondary manifestation of oral candidiasis. Once the acute disease is under control, definitive treatment, such as scaling and root planning as needed and therapy for pre-existing gingivitis or periodontitis, should be provided. These include adequate therapy for the pre-existing gingivitis or periodontitis, instructions on adequate oral hygiene practices at home, and supportive therapy such as periodontal recall maintenance Herrera, et al. 2014; Hofer, et al. 2002.
Broad-spectrum antibiotics are effective for the treatment of periodontal diseases in patients with HIV Murray 1994. Follow-up treatment includes daily antimicrobial rinses and systemic antibiotics, specifically metronidazole 250 mg 3 times per day, for 7 to 14 days. Metronidazole is effective as an adjunct systemic antibiotic for treating periodontal diseases in patients with HIV Winkler and Robertson 1992. If the patient cannot tolerate metronidazole, clindamycin 150 mg 4 times per day or amoxicillin-clavulanate 875 mg twice per day for 7 to 10 days may be prescribed. Extraction of affected teeth may be necessary if the bone loss is severe. The use of systemic antibiotics increases the patient’s risk of developing candidiasis; therefore, concurrent, empiric administration of an antifungal agent should be considered to maintain the balance between treatment and potential negative side effects Ryder 2000.
During the acute and healing stages of NUP, frequent recall visits are needed to administer the necessary periodontal therapies, assess tissue response, and monitor the patient’s oral hygiene performance. Periodontal maintenance is generally indicated every 3 months once the infection is controlled Ryder, et al. 2012.
Favorable treatment responses to HIV-associated periodontal disease usually occur when the disease is addressed as early as possible Ryder, et al. 2012. Patients treated for NUP may develop repeated episodes, especially when oral hygiene practices are not good. NUP can be insidious, localized, and not necessarily related to plaque. Once clinical stabilization has occurred, visits every 3 months will allow for the detection and prevention of disease recurrence at an incipient stage Ryder, et al. 2012.
Necrotizing Ulcerative Stomatitis and Necrotizing Stomatitis (NUS/NS)
Presentation and Diagnosis
Necrotizing ulcerative stomatitis and necrotizing stomatitis (NUS/NS) may be an extension of NUP into the adjacent supporting bone, leading to osteonecrosis and subsequent sequestration of the surrounding bone.
Patients may present with pronounced residual soft tissue and bony defects in the affected areas following treatment and healing of the necrotic tissues Ryder, et al. 2012; Armitage 1999; Horning and Cohen 1995. If the tissue does not heal, a soft tissue biopsy is indicated to exclude other potential diagnoses, such as the increased risk of cancer in patients with HIV Chen, et al. 2015.
When the soft tissue destruction is no longer contained to the soft tissue and bone of the oral cavity, this condition can be clinically consistent with Noma disease (also referred to as cancrum oris), which is more often seen in the pediatric population and is associated with severe or life-threatening malnourishment Feller, et al. 2014.
|PERIODONTAL DISEASE PRESCRIPTION DOSING|
Broad-spectrum antibiotics are effective for the treatment of periodontal diseases in patients with HIV Patton and McKaig 1998; Murray 1994. Metronidazole is very effective as an adjunct systemic antibiotic for treating periodontal diseases in patients with HIV Winkler and Robertson 1992. Metronidazole is effective against gram-negative bacteria that are typically involved in periodontal diseases. Augmentin can be used as an alternative if a patient has gastrointestinal problems with metronidazole. Both 0.12% chlorhexidine gluconate and 10% povidone-iodine are effective treatment modalities, and either may be used in office and at home as an antimicrobial rinse Hofer, et al. 2002. A local anesthetic may be indicated for pain management during the removal of necrotic debris, scaling, and root planing.
Chronic Pre-Existing Periodontal Disease
Chronic Pre-Existing Periodontal Disease Treatment
Presentation and Diagnosis
About half of the U.S. population >30 years of age is affected by chronic periodontal disease, and the prevalence of periodontal disease increases with age Eke, et al. 2015. No data currently exist to indicate the extent to which HIV infection may accelerate the destruction of periodontal tissues in the population with HIV. However, the occurrence of rapid attachment loss may indicate severe immunosuppression Ryder, et al. 2012; Mealey 1996. Pre-existing periodontal disease can be diagnosed by clinical characteristics and radiographic examination for bone loss as recommended by the American Academy of Periodontology American Academy of Periodontology 2000; Armitage 1999. The clinical characteristics for chronic periodontitis include the presence of periodontal pockets, clinical attachment loss, and bleeding on probing. Radiographic analysis can reveal the presence of periodontal bone loss with horizontal or vertical bony defects. Increased mobility of teeth may also be observed in association with clinical attachment loss and bone loss.
Scaling and root planing is recommended for nonsurgical treatment of periodontal disease American Academy of Periodontology 2000. A recent case-control study further reinforced that nonsurgical periodontal therapy has a beneficial effect on clinical and immunological parameters of chronic periodontitis, reduction of oral Candida counts, and improvement of HIV infection status. Patients with chronic periodontitis treated with nonsurgical periodontal therapy had an increase in CD4+ T-lymphocytes and a reduction in viral load Nobre, et al. 2019.
Surgical therapy, including flap debridement and extraction of teeth, can be performed without postoperative complications. Before surgical treatment, consultation with the patient’s physician may be indicated to obtain information regarding hematological levels of immune cells. Low neutrophil counts may indicate the adjunct use of systemic antimicrobial therapy.
Appendix: Photo- and Radiographs of Periodontal Disease Associated With HIV
Photographs courtesy of Dr. Gwen Cohen Brown and the Dental Hygiene Department of New York City College of Technology
|ALL RECOMMENDATIONS: MANAGEMENT OF PERIODONTAL DISEASE|
Chronic Pre-Existing Periodontal Disease Treatment
Guideline Information and Updates
|Intended users||New York State clinicians who provide dental care for adults with HIV|
|Last reviewed and updated||April 12, 2023|
|Original publication||March 2017|
Joseph P. McGowan, MD, FACP, FIDSA; Steven M. Fine, MD, PhD; Rona Vail, MD; Samuel T. Merrick, MD; Asa Radix, MD, MPH, PhD; Christopher J. Hoffmann, MD, MPH; Charles J. Gonzalez, MD
|Developer and funding|
See Guideline Development and Recommendation Ratings Scheme, below.
April 12, 2023
Reviewed and determined to be up to date.
|Box A1: Committee on Dental Standards of Care Leaders and Members (when this guideline was developed)
Unless noted otherwise, committee members had no disclosures of financial relationships with commercial entities
NYS Program and Consumer Liaisons
External Peer Reviewers
|Guideline Development: New York State Department of Health AIDS Institute Clinical Guidelines Program|
|Program Manager||Clinical Guidelines Program, Johns Hopkins University School of Medicine, Division of Infectious Diseases. See Program Leadership and Staff.|
|Mission||To produce and disseminate evidence-based, state-of-the-art clinical practice guidelines that establish uniform standards of care for practitioners who provide prevention or treatment of HIV, viral hepatitis, other sexually transmitted infections, and substance use disorders for adults throughout New York State in the wide array of settings in which those services are delivered.|
|Expert Committees||The NYSDOH AI Medical Director invites and appoints committees of clinical and public health experts from throughout New York State to ensure that the guidelines are practical, immediately applicable, and meet the needs of care providers and stakeholders in all major regions of New York State, all relevant clinical practice settings, key New York State agencies, and community service organizations.|
|Disclosure and Management of Conflicts of Interest||
|Evidence Collection and Review||
|Review and Approval Process||
|Recommendation Ratings Scheme|
|Strength||Quality of Evidence|
|A||Strong||1||Based on published results of at least 1 randomized clinical trial with clinical outcomes or validated laboratory endpoints.|
|B||Moderate||*||Based on either a self-evident conclusion; conclusive, published, in vitro data; or well-established practice that cannot be tested because ethics would preclude a clinical trial.|
|C||Optional||2||Based on published results of at least 1 well-designed, nonrandomized clinical trial or observational cohort study with long-term clinical outcomes.|
|2†||Extrapolated from published results of well-designed studies (including nonrandomized clinical trials) conducted in populations other than those specifically addressed by a recommendation. The source(s) of the extrapolated evidence and the rationale for the extrapolation are provided in the guideline text. One example would be results of studies conducted predominantly in a subpopulation (e.g., one gender) that the committee determines to be generalizable to the population under consideration in the guideline.|
|3||Based on committee expert opinion, with rationale provided in the guideline text.|
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