Case ReportGingival and other oralmanifestations in measles virusinfection

Joseph Katz1, Marcio Guelmann2,Franci Stavropolous1 and Marc Heft1

Departments of 1Oral and Maxillofacial

Surgery and Diagnostic Sciences and2Pediatric Dentistry, College of Dentistry,

University of Florida, FL, USA

Katz J, Guelmann M, Stavropolous F, Heft M: Gingival and other oral manifestationsin measles virus infection. J Clin Periodontol 2003; 30: 665–668. r BlackwellMunksgaard, 2003.

AbstractBackground: Measles is a highly contagious, viral infectious disease affecting mainlychildren and young adults. It is characterized by high fever, maculopapular rash,keratoconjunctivitis and pathognomonic oral Koplik’s spots.

Methods: During an outbreak of measles among soldiers in the Israeli military,patients were referred to one medical center where they were also examined for oralsigns and symptoms of their illness.

Results: We present a case of measles infection with distinct oral findings. Theseincluded Koplik’s spots, various forms of ulcerations of the free mucosa, -likegingivitis and pericoronitis. All oral lesions resolved after cessation of systemicillness.

Conclusions: The measles virus is associated with a transient inhibition of the hostresponse. Immunosuppression may create the necessary condition for the proliferationof pathobacteria associated with the observed pericoronitis and the other gingivallesions.

Key words: measles; Koplik’s spots; gingivitis;pericoronitis; oral ulcerations

Accepted for publication 19 August 2002

Measles is an infection produced by aparamyxovirus that exhibits a variableprevalence and is correlated to thedegree of immunity gained in thevaccination (Neville et al. 2002). Af-fected individuals are infectious from 2days prior to developing symptoms until4 days after appearance of the rash.After an incubation period of 10–12days, the infection begins with prodro-mal symptoms of fever, malaise, coryza,conjunctivitis and cough. The well-known exanthematous rash followswithin a few days and lasts from 4 to7 days, initially involving the face(Regezi & Scuibba 1993). Commoncomplications in young children areotitis, pneumonia, bronchitis, diarrheaand encephalitis. Koplik’s spots are themost distinctive oral manifestation ofmeasles, and they develop early in thecourse of the infection. Reported oralmanifestations of measles include can-

didiasis, ulcerative gingivitis and necro-tizing stomatitis (Neville et al. 2002).The purpose of the present case report isto describe the oral and gingival man-ifestations of the measles virus in youngadult patients.

Case Report

We assessed the oral manifestations ofmeasles during an outbreak amongIsraeli military personnel. All affectedindividuals were hospitalized in onecenter where they were also evaluatedfor oral findings. The patients were ofages between 18 and 21 years and theratio of males to females was 3:1.Twenty percent of affected individualspresented with oral findings during theirillness. The present case reports findingsin a 19-year-old male who was vacci-nated for measles at the age of 9 years.

His medical history was not significant,and the dental history was positive forminor conservative treatment with noprevious gingival or periodontal invol-vement. Upon admission, the patientwas febrile (391C), fatigued, and re-ported oral pain and discomfort. Onexamination, a maculopapular rash wasnoted on the trunk of the body and theextremities (Fig. 1). Severe keratocon-junctivitis was present in both eyes (Fig.2). A few cervical and submandibularlymph nodes were enlarged and tenderbilaterally. Intraorally, tiny, white pla-que-like papules (Koplik’s spots) cov-ered the buccal mucosa, and severe oralulcerations were present on the lip (Fig.3). The marginal gingiva were inflamedwith microabscesses present in an acutenecrotizing gingivostomatitis (ANUG)-like pattern (Fig. 4). Pericoronitis wasevident bilaterally in the mandibularthird molar areas (Fig. 5). The patient

J Clin Periodontol 2003; 30: 665–668 Copyright r Blackwell Munksgaard 2003Printed in Denmark. All rights reserved

reported that the oral lesions precededthe appearance of the maculopapularskin rash and keratoconjunctivitis. Viralcultures taken from the area of theoperculum confirmed the presence ofthe measles virus. This diagnosis wasalso supported by the increased titer ofmeasles virus antibody. The fatiguedpatient was instructed to rinse with oralchlorhexidine 0.12% mouthwash twicea day and maintain a soft diet. Noantibiotic treatment was recommended.One week later, all oral lesions had

disappeared. At a month follow-up, noremaining oral signs or symptoms werepresent.

Discussion

Although the role of viruses in thepathology of gingival and periodontallesions has been recently appreciated(Contreras et al. 1999a,b, 2000), theperiodontal literature, typically, doesnot include measles infection in the

differential diagnosis of young adultgingivitis and pericoronitis associatedwith systemic diseases. Rich lymphatictissue surrounding the operculum of awisdom tooth, Waldeyer’s ring andmucosa-associated lymphoid tissue allpredispose these areas as a potentialtarget for the incubation of variousmicroorganisms associated with sys-temic manifestations. The role of humansimian virus-1 and Epstein–Barr virus(EBV) in specific forms of pericoronitisassociated with systemic disease such aserythema multiforme (Katz et al. 1999,Ayangco et al. 2001), infectious mono-nucleosis (Kadesh & Albers 1981,Benoliel & Katz 1989) and lymphoma(Dhanrajani et al. 1992), has beendescribed in the past literature. Also,as a result of immunosuppression fol-lowing a measles virus infection, Can-dida albicans-associated gingivitis wasnoted in monkeys (Choi et al. 1999).

Microbial analysis of the flora ofpericoronal pockets of mandibular thirdmolars from symptomatic pericoronitisrevealed the presence of obligate anae-robic bacteria including various Actino-myces and Prevotella species (Leung etal. 1993, Peltroche-Llacsahunaga et al.2000), and also viruses. In one report, itwas suggested that human cytomegalo-virus infects periodontal monocytes,macrophages and less frequently T-lymphocytes, and that EBV-1 infectsperiodontal B-lymphocytes (Contreraset al. 1999a,b).

Recently, we have also reported thatthe oral epithelium of patients withrecurrent aphthous stomatitis testedpositive for the presence of measlesvirus and suggested that the viralgenome might be present in the oraltissues in the form of dormant state(Czerninski et al. 2000). The measlesvirus was also associated with Crohn’sdisease, another condition characterizedwith oral lesions. (Wakefield et al.1993).

The mechanism by which the measlesvirus induces gingival pericoronal swel-ling is not clear. Like the herpes viruses,it may reduce the periodontal defenseby initiating cytotoxic or immunopatho-genic events that promote growth ofsubgingival bacteria capable of causinggingival damage (Contreras et al.1999a,b). Similarly, measles virus in-fection results in lymphopenia andreduction in CD4 T-lymphocyte percen-tage and number (Moss et al. 2002). Areduction in T-helper cells has beenassociated in the past with acute forms

Fig. 1. Maculopapular rash on the abdomen and chest of a measles patient.

Fig. 2. Keratoconjunctivitis in a measles patient.

666 Katz et al.

of periodontal disease (Katz et al. 1988)and pericoronitis associated with infec-tious mononucleosis (Benoliel & Katz1989).

The measles virus has also beenshown to induce downregulation ofCD46, which controls complement reg-ulation (Naniche et al. 1993). Thecleavage of complement was shown tobe an important immunopathologic me-chanism in the development of gingival

inflammation (Patters et al. 1989). It hasyet to be discovered if this mechanismcauses gingival inflammation in a pa-tient with a measles infection.

Zusammenfassung

Gingivale und andere orale Manifestationenvon Infektionen mit dem Masern-VirusHintergrund: Masern sind eine hochgradigansteckende virale Infektion, die vorwiegend

Kinder und junge Erwachsene befallt. Sie istcharakterisiert durch hohes Fieber, makulopa-pularen Ausschlag, Keratokonjunktivitis undpathognomonische orale Koplik-Flecken.Zielsetzung: Beschreibung der oralen undgingivalen Manifestationen des Masern-Virusbei jungen Erwachsenen.Methoden: Wahrend einer Masernepidemie beiSoldaten der israelischen Streitkrafte wurdendie Patienten an ein Medizinisches Zentrumuberwiesen, wo sie auf orale Zeichen undSymptome ihrer Erkrankung untersucht wur-den.Ergebnisse: Es wird ein Fall von Masern mitspeziellen oralen Symptomen gezeigt: Koplik-Flecken, verschiedene Formen von Ulzeratio-nen der Alveolarmukosa, der NUG ahnlicheGingivitis und Pericoronitis. Alle oralen Lasio-nen heilten nach Ende der systemischen Erk-rankung aus.Schlussfolgerungen: Eine Infektion mit demMasern-Virus geht mit einer vorubergehendenSchwachung der Wirtsabwehr einher. DieseImmunsuppression konnte die notwendigenBedingungen fur das Wachstum von pathogen-en Keimen schaffen, die mit den beobachtetenPerikoronitiden und gingivalen Lasionen asso-ziiert waren.

Resume

Manifestations gingivale et buccale dans l’in-fection virale de la rougeoleLa rougeole est une maladie infectieuse viraletres contagieuse qui affecte essentiellement lesenfants et les jeunes adultes. Elle est caracter-isee par la haute temperature, une eruptionmaculo-papulaire, une kerato-conjonctivite etdes spots de Koplik buccaux pathognomoni-ques. Durant une epidemie de rougeole parmiles soldats de l’armee israelienne, des patientsont ete referes vers un centre medical ou ils ontegalement ete examines pour les signes buccauxet les symptomes de leur maladie. Un casd’infection de rougeole avec des decouvertesbuccales distinctes est presente. Elles compren-nent : les spots de Koplik, des formes varieesd’ulcerations de la muqueuse libre, une gingi-vite genre gingivite necrotique et une pericor-onarite. Toutes les lesions buccales ont disparuapres la fin de la maladie systemique. Le virusde la rougeole est associe a une inhibitiontransitoire de la reponse immunitaire. L’im-munosuppression peut creer la condition neces-saire pour la proliferation de bacteriespathogenes associees avec la pericoronariteobservee ainsi que les autres lesions gingivales.

References

Ayangco, L., Sheridan, P. J. & Rogers, R. S.

(2001) Erythema multiforme secondary to

herpes simplex infection: a case report.

Journal of Periodontology 72, 953–957.

Benoliel, R. & Katz, J. (1989) Infectious

mononucleosis first manifestation as pericor-

onitis. Annals of Dentistry 48, 30–33.

Bustos, D., Grenon, M., Benitez, M., de

Boccardo, G., Pavan, J. & Gendelman, H.

(2001) Human papillomavirus infection in

Fig. 3. Koplik’s spots of the buccal mucosa of a measles patient. Tiny, erythematous maculaewith white necrotic centers.

Fig. 4. ANUG-like gingivitis of the anterior maxillary and mandibular incisors withmicroabscesses.

Measles and gingival involvement 667

cyclosporin-induced gingival overgrowth in

renal allograft recipients. Journal of Period-

ontology 72, 741–744.

Choi, Y. K., Simon, M. A. & Kim, D. Y. et al.

(1999) Fatal measles infection in Japanese

macaque. Veterinary Pathology 36, 594–600.

Contreras, A., Umeda, M. & Chen, C. et al.

(1999a) Relationship between herpesviruses

and adult periodontitis and periodontopathic

bacteria. Journal of Periodontology 70,

478–484.

Contreras, A., Zadeh, H. H., Nowzari, H. &

Slots, J. (1999b) Herpesvirus infection of

inflammatory cells in human periodontitis.

Oral Microbiology and Immunology 14,

206–212.

Contreras, A., Nowzari, H. & Slots, J. (2000)

Herpesviruses in periodontal pocket and

gingival tissue specimen. Oral Microbiology

and Immunology 15, 15–18.

Czerninski, R., Katz, J. & Schlesinger, M.

(2000) Preliminary evidence for an associa-

tion of measles virus antigen and CD46 virus

with recurrent aphthous ulceration. Archives

of Dermatology 136, 801–803.

Dhanrajani, P. J., Swaify, G. A. & Khateery, S.

M. (1992) Malignant lymphoma presenting

as pericoronitis. A case report. International

Journal of Oral and Maxillofacial Surgery 5,

295–296.

Kadesh, J. B. & Albers, D. (1981) Infectious

mononucleosis first manifest by mandibular

pericoronitis. General Dentistry 29, 428–429.

Katz, J., Goultchin, J., Benoliel, R. & Schle-

singer, M. (1988) T helper/T suppressor in

rapidly progressive periodontitis. Journal of

Clinical Periodontology 15, 266–288.

Katz, J., Findler, M., Marmary, Y., Askenazi,

Y. & Shemer, J. (1996) Measles, Crohn’s

disease and recurrent aphthous stomatitis.

Lancet 348, 1250–1251.

Katz, J., Livneh, A. & Shemer, J. et al. (1999)

Herpes simplex erythema multiforme

(HAEM): a clinical therapeutic dilemma.

Pediatric Denistry 21, 359–362.

Leung, W. K., Thilade, E. & Comfort, M. B. et

al. (1993) Microbiology of the pericoronal

pouch in mandibular third molar pericoroni-

tis. Oral Microbiology and Immunology 8,

306–312.

Moss, W., Ryon, J., Monze, M., Cutts, F.,

Quinn, T. & Griffin, E. (2002) Suppression of

human immunodeficiency virus replication

during acute measles. Journal of Infectious

Diseases 15, 1035–1042.

Neville, B. W., Damm, D. D., Allen, C. M. &

Bouquot, J. E. (2002) Oral and maxillofacial

pathology, 2nd edition, p. 231. Philadelphia:

Saunders.

Patters, M. R., Niekrash, C. E. & Lang, N. P.

(1989) Assessment of complement cleavage

in gingival fluid during experimental gingi-

vitis in man. Journal of Clinical Period-

ontology 16, 33–37.

Peltroche-Llacsahunaga, H., Reichhart, E. &

Schmitt, W. et al. (2000) Investigation of

infectious organisms causing pericoronitis of

the mandibular third molar. Journal of Oral

and Maxillofacial Surgery 58, 611–616.

Regezi, J. A. & Scuibba, J (1993) Oral

pathology, clinical pathologic correlation,

2nd edition, pp. 15–16. Philadelphia: Saun-

ders.

Shafer, W. G., Hine, M. K. & Levy, B. M.

(1983) A textbook of oral pathology, 3rd

edition, p. 378. Philadelphia: Saunders.

Wakefield, A. J., Pittilo, R. M. & Sim, R. et al.

(1993) Evidence of persistent measles virus

infection in Crohn’s disease. Journal of

Medical Virology 39, 345–359.

Address:

Dr. Joseph Katz

Department of Oral and Maxillofacial Surgery

and Diagnostic Sciences

College of Dentistry

University of Florida

P.O. Box 100416

Gainesville, FL 32610-0416

USA

Fax: 11 352 8460588

E-mail: jkatz@dental.ufl.edu

Fig. 5. Pericoronitis of the mandibular third molar with affected adjacent mucosa.

668 Katz et al.