Management of Periodontal Disease

Introduction

Dental Standards of Care Committee, January 2017

In some patients with HIV infection, immunosuppression may allow the development of oral and periodontal lesions [Baccaglini et al. 2007]. Periodontal lesions associated with HIV infection 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 [Kaplan et al. 2009; Ryder et al. 2010]. 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].

The identification of periodontal diseases may be critical even in patients receiving ART. While the introduction of highly-active antiretroviral therapy (ART) has significantly reduced this incidence [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]. HIV-associated periodontal diseases, along with oral infections, are considered serious complications of HIV infection. The incidence of periodontal infections in patients with HIV is lower than the incidence of oral infections [Ryder et al. 2010].

Management of periodontal lesions in patients with HIV has changed little in the past 30 years [Ryder et al. 2010; Gonçalves et al. 2013]. 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 important components in the management of HIV-associated gingival and periodontal diseases. The interaction between bacteria and Candida may play a key role in the etiology of periodontal lesions; therefore, 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].

References

Alpagot T, Duzgunes N, Wolff LF, et al. Risk factors for periodontitis in HIV patients. J Periodontal Res 2004;39(3):149–57. [PubMed]

Baccaglini L, Atkinson JC, Patton LL, et al. Management of oral lesions in HIV-positive patients. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2007:103 Suppl:S50.e1–23. [PubMed]

Gonçalves LS, Gonçalves BM, Fontes TV. Periodontal disease in HIV-infected adults in the HAART era: Clinical, immunological, and microbiological aspects. Arch Oral Biol 2013;58(10):1385–96. [PubMed]

Kaplan JE, Benson C, Holmes KK, et al. Guidelines for prevention and treatment of opportunistic infections in HIV-infected adults and adolescents: Recommendations from CDC, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America. MMWR Recomm Rep 2009;58(RR-4):155, 160–61. [PubMed]

Mataftsi M, Skoura L, Sakellari D. HIV infection and periodontal diseases: an overview of the post-HAART era. Oral Dis 2011;17(1):13-25. [PubMed]

Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet 2005;366(9499):1809–20. [PubMed]

Ryder MI, Nittayananta W, Coogan M, et al. Periodontal disease in HIV/AIDS. Periodontol 2000 2012;60(1):78–97. [PubMed]

Stabholz A, Soskolne WA, Shapira L. Genetic and environmental risk factors for chronic periodontitis and aggressive periodontitis. Periodontol 2000 2010;53:138–53. [PubMed]

Valentine J, Saladyanant T, Ramsey K, et al. Impact of periodontal intervention on local inflammation, periodontitis, and HIV outcomes. Oral Dis 2016;22 Suppl 1:87–97. [PubMed]

Linear Gingival Erythema (LGE)

Dental Standards of Care Committee, January 2017

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 Infection 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 and root planing and scaling. 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 [Gonçalves et al. 2013]. If LGE lesions do not resolve after 1 month of therapy, biopsy may then help indicate a different diagnosis [Ryder et al. 2012].

Treatment

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 for 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].

References

Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999;4(1):1–6. [PubMed]

Cherry-Peppers G, Daniels CO, Meeks V, et al. Oral manifestations in the era of HAART. J Natl Med Assoc 2003;95(2 Suppl 2):21S-32S. [PubMed]

Gonçalves LS, Gonçalves BM, Fontes TV. Periodontal disease in HIV-infected adults in the HAART era: Clinical, immunological, and microbiological aspects. Arch Oral Biol 2013;58(10):1385–96. [PubMed]

Herrera D, Alonso B, de Arriba L, et al. Acute periodontal lesions. Periodontal 2000 2014;65(1):149–77. [PubMed]

Patton LL. Sensitivity, specificity, and positive predictive value of oral opportunistic infections in adults with HIV/AIDS as markers of immune suppression and viral burden. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;90(2):182–88. [PubMed]

Ryder MI, Nittayananta W, Coogan M, et al. Periodontal disease in HIV/AIDS. Periodontol 2000 2012;60(1):78–97. [PubMed]

Necrotizing Ulcerative Gingivitis and Necrotizing Ulcerative Periodontitis (NUG/NUP)

Dental Standards of Care Committee, January 2017

Necrotizing ulcerative gingivitis (NUG) and necrotizing ulcerative periodontitis (NUP) are periodontal conditions that may be present in patients who do not have HIV infection, but both are more commonly associated with HIV infection 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 [Bodhade et al. 2011; Ryder et al. 2012; Patton et al. 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 Infection 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 a 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 [Bodhade et al. 2011; Ryder et al. 2012].

Treatment

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 infection [Ryder et al. 2012; Winkler et al. 1989; Holmstrup and Westergaard 1994; Mealey 1996]. In severe cases or in 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 development of a secondary manifestation of oral candidiasis. Once the acute disease is under control, definitive treatment, such as root planning and scaling 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 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 four 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. 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 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 detection and prevention of disease recurrence at an incipient stage [Ryder et al. 2012].

References

Bodhade AS, Ganvir SM, Hazarey VK. Oral manifestations of HIV infection and their correlation with CD4 count. J Oral Sci 2011;53(2):203–11. [PubMed]

Herrera D, Alonso B, de Arriba L, et al. Acute periodontal lesions. Periodontal 2000 2014;65(1):149–77. [PubMed]

Hofer D, Hämmerle CH, Grassi M, et al. Long-term results of supportive periodontal therapy (SPT) in HIV-seropositive and HIV-seronegative patients. J Clin Periodontal 2002;29(7):630–37. [PubMed]

Holmstrup P, Westergaard J. Periodontal diseases in HIV-infected patients. J Clin Periodontal 1994;21(4):270–80. [PubMed]

Lucartorto FM, Franker CK, Maza J. Postscaling bacteremia in HIV-associated gingivitis and periodontitis. Oral Surg Oral Med Oral Pathol 1992;73(5):550-54. [PubMed]

Mealey BL. Periodontal implications: Medically compromised patients. Ann Periodontal 1996;1(1):256–321. [PubMed]

Murray PA. Periodontal diseases in patients infected by human immunodeficiency virus. Periodontal 2000 1994;6:50–67. [PubMed]

Patton LL, McKaig R. Rapid progression of bone loss in HIV-associated necrotizing ulcerative stomatitis. J Periodontal 1998;69(6):710–16. [PubMed]

Robinson PG, Sheiham A, Challacombe SJ, et al. Gingival ulceration in HIV infection. A case series and case control study. J Clin Periodontal 1998;25(3):260–67. [PubMed]

Ryder MI, Nittayananta W, Coogan M, et al. Periodontal disease in HIV/AIDS. Periodontol 2000 2012;60(1):78–97. [PubMed]

Ryder MI. Periodontal management of HIV-infected patients. Periodontal 2000 2000;23(1):85–93. [PubMed]

Winkler JR, Murray PA, Grassi M, et al. Diagnosis and management of HIV-associated periodontal lesions. J Am Dent Assoc 1989;119(Suppl):25S–34S. [PubMed]

Winkler JR, Robertson PB. Periodontal disease associated with HIV infection. Oral Surg Oral Med Oral Pathol 1992;73:145–50. [PubMed]

Necrotizing Ulcerative Stomatitis and Necrotizing Stomatitis (NUS/NS)

Dental Standards of Care Committee, January 2017

Presentation and Diagnosis

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 [Armitage 1999; Ryder et al. 2012; Horning and Cohen 1995]. If the tissue does not heal, 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].

Treatment

Broad spectrum antibiotics are effective for treatment of periodontal diseases in patients with HIV [Murray 1994; Patton and McKaig 1998]. 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 the patients have 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]. Local anesthetic may be indicated for pain management during removal of necrotic debris, scaling, and root planing.

References

Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999;4(1):1–6. [PubMed]

Chen CH, Chung CY, Wang LH, et al. Risk of cancer among HIV-infected patients from a population-based nested case-control study: implications for cancer prevention. BMC Cancer 2015;15:133. [PubMed]

Feller L, Altini M, Chandran R, et al. Noma (cancrum oris) in the South African context. J Oral Pathol Med 2014;43(1):1–6. [PubMed]

Hofer D, Hämmerle CH, Grassi M, et al. Long-term results of supportive periodontal therapy (SPT) in HIV-seropositive and HIV-seronegative patients. J Clin Periodontal 2002;29(7):630–37. [PubMed]

Horning GM, Cohen ME. Necrotizing ulcerative gingivitis, periodontitis, and stomatitis: clinical staging and predisposing factors. J Periodontal 1995;66(11):990-8. [PubMed]

Murray PA. Periodontal diseases in patients infected by human immunodeficiency virus. Periodontal 2000 1994;6:50–67. [PubMed]

Patton LL, McKaig R. Rapid progression of bone loss in HIV-associated necrotizing ulcerative stomatitis. J Periodontal 1998;69(6):710–16. [PubMed]

Ryder MI, Nittayananta W, Coogan M, et al. Periodontal disease in HIV/AIDS. Periodontol 2000 2012;60(1):78–97. [PubMed]

Winkler JR, Robertson PB. Periodontal disease associated with HIV infection. Oral Surg Oral Med Oral Pathol 1992;73:145–50. [PubMed]

Chronic Pre-Existing Periodontal Disease

Dental Standards of Care Committee, January 2017

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 [Armitage 1999; Academy of Periodontology 2000]. 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.

Treatment

Scaling and root planing is recommended for nonsurgical treatment of periodontal disease [Academy of Periodontology 2000]. Surgical therapy, including flap debridement and extraction of teeth, can be performed without postoperative complications. Prior to surgical therapy, 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.

References

Academy of Periodontology. Parameters of care. J Periodontol 2000;71(5 Suppl): i–ii, 847–83. [PubMed]

Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999;4(1):1–6. [PubMed]

Eke PI, Dye BA, Wei L, et al. Update on prevalence of periodontitis in adults in the United States: NHANES 2009 to 2012. J Periodontol 2015;86(5):611–22. [PubMed]

Mealey BL. Periodontal implications: Medically compromised patients. Ann Periodontal 1996;1(1):256–321. [PubMed]

Ryder MI, Nittayananta W, Coogan M, et al. Periodontal disease in HIV/AIDS. Periodontol 2000 2012;60(1):78–97. [PubMed]

All Recommendations

Dental Standards of Care Committee, January 2017

NYSDOH AIDS Institute Committee on Dental Standards of Care

Committee Leadership

Stephen N. Abel, DDS, MSD, Committee Chair
University at Buffalo-SUNY
New York, New York

Guidelines Program Leadership

Bruce D. Agins MD, MPH, Medical Director
New York State Department of Health AIDS Institute
New York, New York

Christopher J. Hoffman, MD, MPH, Principal Investigator
Clinical Guidelines Program
Johns Hopkins University School of Medicine
Baltimore, Maryland

Contributing Members

Victor M. Badner, DMD, MPH
North Bronx Healthcare Network
Bronx, New York

Mary Therese Biltucci, RDH, MA
University of Rochester
Rochester, New York

Stanley J. Boyd, DMD
Healthy Chelsea Dentistry
New York, New York

Gwen Cohen Brown, DDS, FAAOMP
New York City College of Technology
Brooklyn, New York

Dolores Cottrell-Carson, DDS, MSHA
New York State Board for Dentistry
Albany, New York

Maria de los Angeles Figueroa, DMD
Bronx-Lebanon Hospital Center
Bronx, New York

Robert D. Kelsch, DMD
Northwell Health
Manhasset, New York

Michael A. Kozlowski, DDS
Unity Dental Group
Rochester, New York

Abhiram Maddi, DDS, MSc, PhD
School of Dental Medicine, University at Buffalo
Buffalo, New York

 Kareem J. Merrick, DDS
Harlem Unity Community Clinic
New York, New York

Calix Ramos-Rodriguez, DMD
Lutheran Medical Center
Brooklyn, New York

Miriam R. Robbins, DDS, MS
Winthrop University Hospital
Mineola, New York

Dara J. Rosenberg, DDS, MS, MPH
St. Barnabas Hospital
Bronx, New York

Terrence T. Thines, DDS, MS
SUNY Upstate Medical University
Syracuse, New York

New York State Program and Consumer Liaisons

Mary J. D’Silva, DDS, Department of Corrections and Community Supervision Liaison
Albany, New York

Britta Viereckl-Prast, DMD, Department of Corrections and Community Supervision Liaison
Bedford Hills, New York

Jahlove Serrano, Consumer Advisor
NYSDOH AIDS Institute Consumer Advisory Committee
New York, New York

AIDS Institute Staff and Liaisons

Tracy Hatton, MPH, Guidelines Program

Lyn C. Stevens, MS, NP, ACRN, Office of the Medical Director

External Peer Reviewers

John T. Grbic, DMD, MMSc
Columbia University Medical Center
New York, New York

Mark I. Ryder, DMD
University of California San Francisco School of Dentistry
San Francisco, California

Appendix: Photo- and Radiographs of Periodontal Disease Associated with HIV Infection

November 2016

Photographs courtesy of Dr. Gwen Cohen Brown and the Dental Hygiene Department of New York City College of Technology

Patient with linear gingival erythema (LGE)

Patient with necrotizing ulcerative periodontitis (NUP)

Patient with linear gingival erythema (LGE) and necrotizing ulcerative periodontitis (NUP)

Patient with necrotizing ulcerative gingivitis (NUG)

Patient with localized bone loss