PEDIATRIC /Copyright s 1981 by The American Academy of Pedodontics Vol. 3, Special Issue

Localized juvenile periodontitis (periodontosis) Dr. Newman Michael G. Newman, DOS

Abstract The following discussion will highlight recent major areas of research activity which have provided the A discussion of the recent information regarding the basis for our current understanding of this impor- terminology, clinical manifestations and epidemiology of the tant . Many reviews have been periodontal disease termed Localized Juvenile Periodontitis 5 7 (LJP) is presented in the context of newer scientific published. * advances. Emphasis is given to the microbiological and immunological parameters associated with the etiology of Terminology the disease previously referred to as Periodontosis. Newer Even though a more clear understanding of the therapeutic modalities including adjunctive antimicrobial therapy appear to offer promise in the treatment of this etiology and pathogenesis of this disease currently ex- highly destructive disease. ists, the terminology used to describe this entity has become more confusing. Confusion may result from a failure to clarify and correlate the clinical descriptors Introduction with research findings. These findings have clearly Interest in the rapidly destructive form of perio- demonstrated that specific microbiologic, immuno- dontal disease referred to as "periodontosis" has logic and histologic features can be associated with greatly increased since 1973 when the suggestion of a this disease process (Table 1). It is suggested that unique bacterial etiology was made. In preliminary these findings become incorporated into, and become findings Newman et al.1 reported that gram negative part of, the diagnostic features and then become the rods predominated at the forefront of molar incisor le- basis for classification of the disease process. Table 2 sions in patients diagnosed as having "periodontosis." lists some current terminology. The author prefers the In that study, a sampling device which permitted bac- differentiation of the molar-incisor type of bone loss terial sampling at the apical zone of the lesion was from the generalized involvement since this condition combined with newly developed methods2 of increas- can be distinctly separated on the basis of clinical cri- ing the viable recovery of plaque bacteria. Their re- teria in moderate and advanced cases. Localized Juve- port stimulated great interest among microbiologists, nile Periodontitis, (LJP), is the suggested term for the immunologists and clinicians since it suggested that molar incisor involvement. Generalized terms can be bacterial specificity may be an important etiologic fac- referred to as Juvenile Periodontitis, (JP). As with tor in this disease. any classification system there are always exceptions. In the last seven years a major world-wide research In a recent study Hormand and Frandsen8 described effort has taken place in all areas of study. Particu- three types of bone loss in patients with JP. Type I in- larly important has been the recognition that the cluded first molars and/or incisors. Type II included rapid periodontal breakdown which occurs in "perio- first molars and/or incisors and some additional teeth dontosis" may also occur during periods of exacerba- (less than 14 involved teeth) and Type III patients tion in more common adult forms of periodontitis.3'4 were generally involved. The authors referred to all Understanding more about these periods of disease ac- three types as JP. tivity may provide the basis to unraveling key fea- In 1977 Sugarman and Sugarman9 argued that the tures associated with destructive periodontal diseases term Precocious Periodontitis be used to describe both in man. Since "periodontosis" can be sharply defined localized and generalized forms. The authors argued it may be considered as an ideal model in which exac- that this terminology more clearly describes the clini- erbation and bone destruction can be more accurately cal manifestation of the disease process. In 1978 Baer predicted and studied. and Kaslick pointed out that the term "Periodon-

PEDIATRIC DENTISTRY 121 Volume 3, Special Issue Table1. Possibleetiologic factors associated with LJP. Table2. Currentterminology.

Subgingival Plaque Periodontosis Gram Negative Rods Juvenile Periodontitis PMNDysfunction *LocalizedJuvenile Periodontitis Cell Mediated Deficiency Idiopathic Juvenile Periodontitis Altered Precocious Periodontitis Gottlieb Syndrome Destructive Juvenile Periodontitis tosis’" was never intended to mean "degenerative." They suggested the etymological derivation was from * Preferred Term the Greek and properly defined the term "Pe~iodon- tosis"as meaning "an abnormal or diseased condition 4) are more typical of "inflammatory" chronic perio- of the ." It is clear that confusion over dontitis. In these cases roentgenographic evidence of terminology and definitions exist. The following dis- bone loss and periodontal probing can be used to con- cussion may help to clarify the confusion and provide firm the diagnosis of LJP. the basis for agreement. Many patterns of bone loss may occur among in- volved teeth. Maxillary first molars and incisors are affected to a higher degree than their mandibular Definition m Clinical Features counterparts. 8 There are numerous studies which have Age of Onset: The circumpubertal period appears to documented the bilateral (cross arch) symmetry be the primary time when the disease process mani- bone loss. Bone loss occurs rapidly. One study 18 has fests. 11,1. In some cases however, bone destruction can documented an average attachment loss of 4-5 be documented to occur in the mid-teen years. LJP as microns per day. described in this article, does not occur in the pre- General Health: LJP occurs in healthy patients. No pubertal child, it is a disease of the immediate preteen systemic disease occurs with this condition. When and teenage years. If rapid or unusual periodontal de- rapid periodontal destruction occurs in patients with struction occurs in young children it may be simply certain systemic conditions such as Papillon Lefevre termed, Periodontitis. syndrome or cyclic neutropenia it is called "periodon- Clinical Manifestations:Table 3 summarizes the major titis" not LJP. A recent study which examined the mi- ’4 clinical manifestations associated with LJP. The key crobiota associated with Papillon Lefevre syndrome features of early and moderate forms of the disease are demonstrated that a flora similar to adult forms of unlike the adult forms of periodontitis of similar in- periodontitis was present. The microbiota was re- volvement. Particularly important is the lack of those markably different from that seen in patients with clinical signs which result from an acute inflammatory LJP (see below). response such as: gingival erythema, edema, and Recent studies (see below) have also suggested that bleeding adjacent to involved teeth. Whenpoor oral an underlying defect in polymorphonuclear leukocytes hygiene is present plaque and may induce {PMN) may predispose affected patients to LJP. ’5 gingival inflammation. Later clinical findings (Table Clark et al. have suggested that the PMNdysfunc- tion is genetically transmitted and is re|atively mild. Table3. LJP..Early clinical findings. Affected patients have no other predisposition (as far as is known) to other infectious agents. This observa- tion does not alter the conceptual basis for defining Age Circumpubertal LJP as occurring in healthy patients. Systemic None Bone Loss Molar-- Incisor -- Bilateral Table4. LIP:Late clinica~ findings. and Symmetrical Onset and Course Insidious + Rapid Gingiva Little Clinical Inflammation Mobility and Migration Diasthemata Plaque Small Amounts Pocket Formation Microbiology Characteristic GramNeg. Flora Root Sensitivity Other Regional LymphNodes Pain UponMastication Familial Pattern Abscess Formation No Primary Teeth Involvement Plaque and Inflammation PMNDysfunction Burn Out

LOCALIZEDJUVENILE PERIODONTITIS (PERIODONTOSIS) 122 Newman Epidemiology quency in diseases affecting adult patients. One group which has received considerable atten- Incidence: A recent unpublished study conducted by tion consists of fusiform-shaped, capnophilic rods Hew and Killoy TM examined 22,000 U.S. Air Force which have the ability to glide on agar surfaces. Mem- recruits for evidence of LJP. Their findings indicated bers of this group had been called Bacteroides ochra- an overall incidence of 0.255%. Whenrace was consid- ceus, but are now designated by the genus name Cap- ered, blacks had an overall incidence of 0.410% while nocytopl~aga. ~,~.~ The creation of the new genus was caucasians had an overall incidence of 0.198%. based on the recognition of a typical "wet spreading" Sex Ratio: Hew and Killoy ~s and others reported an colony demonstrating the gliding ability of the organ- overall female to male ratio of 1.05:1. Whenracial con- isms on the solid agar surface. The organisms are not siderations were analyzed the female to male ratio anaerobic (as originally described by Newmanet al.~), amongblacks was 1.16:1, and amongcaucasians 1.19:1. but require increased carbon dioxide tension for their Horman and Frandsen ~ found that the overall female growth. The ability to glide on surfaces has long been to male ratio was 2.5:1 in their caucasian population. recognized in organisms colonizing other sites in na- When broken down according to age, younger females ture, particularly the soil. Since the oral isolates most (12-18) had a female to male ratio of 5.3:1 while older resembled the gliding aerobic genus Cy~opbaga, a new females had a ratio of 2.4:1. genus Capnocytopl~aga was proposed to include the carbon dioxide loving oral strains. ~ The genus Capno- Familial Pattern: The familial pattern of the occurrence cytopl~aga includes three species: Capnocytopl~aga of LJP is well documented. Potential genetic pre- ochracea, Capnocytopt~aga sputigena and Capnocy- disposition is very likely based on recent immunologic tophaga ging~valls. ~,~ In early publications, the Cap- studies as well as from historical data. nocytopl~aga strains’~,~ had been designated Group II. All three species have been detected in LJP lesions Etiology: TheRole of Microorganisms with total counts averaging 25% of the organisms isolated. While many details describing the microbiota of A second group of capnophilic, gram negative rods the LJP lesions have not been clarified, a number of frequently isolated from LJP lesions includes the spe- observations seem consistent (Table 5). The number cies Actinobacillus ac~inomycetemcomitans.~,~ Strains organisms in LJP lesions is less than in most forms of of this species were included in Groups III and IV in destructive periodontal disease 3 ranging from 1@-1@ one of the original descriptions of the microbiota of bacteria per pocket. This may be one to three orders LJP lesions; ~,~ The colonies are small, convex and of magnitude lower than counts of organisms in adult smooth, while the cells are short, round-ended and oc- periodontitis pockets of similar depth and associated casionally slightly curved. Strains of this species pro- bone loss. From microscopic studies of in situ plaque, duce a protein exotoxin capable of destroying poly- it appears that the organisms at the apical portion of morphonuclear~,~.~’ leukocytes and gingival fibroblasts. the pocket are loosely and sparsely attached to the The exact role that this organism, its exotoxin and the tooth surfacemT.~with little evidence of calcification. host response to the exotoxin play in the pathogenesis Clinically, the root surfaces feel hard and smooth. is under intensive investigation and is one of the most The predominant cultivable microbiota of the LJP ’,’9.~.~’ exciting avenues of research concerning this disease lesion is dominated by gram negative rods. Most entity. of the isolates from such lesions have been saccha- rolytic and capnophilic to anaerobic (Table 6). At the present time, three groups of organisms appear to be more frequently encountered in lesions of LJP pa- Table6. Changesin terminologyfor LJPassociated bacteria. tients, as well as in other patients with early onset highly destructive periodontal disease. ~ These organ- Original Current isms are not isolated in the same magnitude or fre- Classific~~°’~ tion Terminology* Table5. Microbiologicfeatures associated with LJP. ¯ GroupI ...... Anaerobic Vibrio-STB ¯ GroupII ...... Capnocytopbaga ¯ GroupIII ...... GroupIII STB& Actinobscillus Fewer bacteria ¯ GroupIV...... Actinobacillus (Y4) Unusual gram negative rods ...... Bacteroidescorrodens Major proportion of plaque -- unattached ¯ GroupV...... Eubacte~m Pathogenic~ potential in animal models Immunologicresponse * Other bacteria within groups I - V are not listed under heading Antibacterial treatment "Current Terminology" since they have not been characterized further.

PEDIATRICDENTISTRY 123 Volume3, Special Issue A third group of organisms frequently encountered Table7. Polymorphonuclearleukocytes (PMN) associated in LJP lesions includes organisms previously placed in withLJP. "periodontosis Group V.’’19,~ Strains of this group often demonstrate a type of spreading on the agar sur- face. Many isolates from Group V appear to fit de- IMPAssociation Observations scriptions of the species Eubacterium saburrheum2 Presencein lesion Histologic sections This species stains Gram positively in very young conirLrmstheir presence cultures and Gram negatively in older preparations, Imparied function In serumand gingival fluid cells are long blunt-ended rods which often produce Sensitivity to From A. actinomycetemcomitans filaments. bacterial exotoxin and other bacteria? The three groups of organisms briefly discussed above are by no means solely confined to LJP lesions or lesions of other forms of early onset destructive dis- taxis and phagocytosis) of PMNsin juvenile periodon- eases. However, their frequency of isolation and their titis (JP) patients to their first-degree relatives and proportions when isolated are clearly much higher in normal subjects. They found a marked reduction in these lesions than in lesions of adult destructive dis- the ability of patients’ neutrophils to respond to eases or healthy sites of adult patients or age-matched chemotatic agents. Peripheral monocytes from the controls. same group of patients with JP responded normally in In 1978, Allen and Brady 18 found rod-shaped similar chemotaxis experiments, suggesting that the microorganisms which were continuously present defective chemotactic response was limited to along the entire cemental surface of extracted LJP in- neutrophils and not shared by other phagocytes. The volved teeth. The cultural and anatomical association cells of the patients with JP showed markedly reduced of microorganisms associated with LJP lesions pro- (5070) bacterial phagocytic activity compared to age- vides the basis for research which may clarify the and sex-matched normal controls. exact role of these bacteria. These observations were The PMNsof siblings showed a marked reduction prerequisite to a more accurate assessment of the re- in chemotactic response in all of the siblings with JP sponse (or failure to respond) by the host to poten- and in several younger siblings with no signs of perio- tially pathogenic bacteria and/or their products. dontal disease. Older siblings with normal neutrophil ImmunologicStudies chemotaxis did not show clinical manifestations of JP. It has been concluded that reduced neutrophil chemo- Antibody: IgG antibody response to many of the sub- taxis seen in subjects with JP does not result from the gingival bacteria associated with LIP lesions has been disease; it may be inherited and predispose to the documented. ~,u.~ In particular, antibody to A. early severe bone loss seen in JP. However, these ob- actinomycetemcondtans and its leukotoxin has servations did not show to what extent compromised received the greatest attention, u,~.~,~ This response neutrophil function is a factor in determining the has been interpreted by some as a blocking effect of severity of extreme forms of periodontal disease. the leukotoxinY The antibody response to A. ac- In 1977, Clark et al.%valuated the serum chemotac- tinomycetemcomitansis also strain specific u,4! indicat- tic activity and the presence of serum chemotactic ing the possibility of virulent and avirulent strains. inhibitors in JP patients. A reduced level of comple- Gingival fluid antibodies appear to parallel anti- ment-derived chemotactic activity was demonstrated body activity in serum~ but, antibody coating of sub- in serum from four of nine patients. Serum from five gingival bacteria from LIP lesions may not occur to of the JP patients contained a heat-stable, non-dialyz- high degree? 2 These observations may provide insight able factor that markedly inhibited the chemotaxis of into the host-bacterial interactions which take place normal neutrophils. One patient who had defective in the lesion. Also, the pathogenicity of the resident chemotaxis was evaluated again after being success- flora may be enhanced since the bacterial numbers fully treated for JP. No improvement in chemotaxis would not be limited by antibody interactions occur- was observed. ring within the lesion. PolymorphonuclearLeukocytes (PMN|: The current re- Cell-Mediated Immunity: Using a non-specific immu- search investigating PMNfunctions in LIP may pro- nostimulation drug, levamisol, Budtz-Jorgensen et vide a more clear understanding of the pathogenic al. ~,~ evaluated the competency of the drug to stimu- mechanisms|8,43.~,~ involved with the disease process. late immunologic responsiveness in LIP patients. Table 7 lists the major research findings associated They concluded that LIP is associated with an in with PMNs. vitro cell-mediated deficiency. Previous studies by Cianciola et al? 3 compared the functions (chemo- Lehner et al?9 have suggested a similar deficiency.

LOCALIZEDJUVENILE PERIODONTITIS(PERIODONTOSIS) 124 Newman Treatment patients. When employed by the author, the combina- tion of surgical intervention, stablization, and sys- Since the suggestion that subgingival plaque may temic antibiotic appears to have success when the be etiologic and contribute to the destructive process patients were selected on the basis of antimicrobial in LJP, much of the treatment employed in these pa- susceptibility testing of the organisms found in the tients has been directed towards the control of the as- lesions (Figure 1). The predictability of treatment 1949 sociated bacteria. The results of treatment can be success can be enchanced (Table 9) as in other forms excellent especially when initiated early in the clinical of destructive periodontal disease in man. There is course of the disease and/or when the destructive no better treatment than prevention through early process begins late in the teen years (Table 8). Table 4 diagnosis. summarizes the current treatment modalities. The clinical course of LJP is rapid and fairly pre- dictable. However, there is a phenomenon referred to as "burn out" which is seen in many cases. Burn out refers to a sudden and unexplainable decrease in the rate of bone destruction, and is almost always seen in the mid- and late twenties. In these cases, the onset of alveolar resorption apparently occurred in the mid- to late teens rather than during the circumpubertal pe- riod. Although many theories have been postulated re- garding this phenomenon, none are based on scientific fact. The use of systemic tetracycline in patients with LJP appears to enchance treatment success in some

Table 8. Diagnostic features associated with treatment of LJP. Figure 1. Roentgenographs of 18-year-old girl treated for LJP with conventional therapy and systemic tetracycline. Patients bacteria were tested for susceptibility to tetracycline prior to treatment. Top: Diagnostic Feature Effect on Treatment Bitewing roentgenographs at age 14 demonstrating moderate bone Age of onset Late onset favors loss around remaining first molars. Bottom: Bitewing roentgeno- successful treatment graphs four years later demonstrating cessation of visable bone Depth of lesion Incipient lesions favors loss and improvement in roentgenographic picture. Clinically, treatment pocket depths were 3 mm or less in all areas. M. G. Newman, E. Montierth and R. Williams. Furcation involvement Decreases success Improves prognosis Occlusion Excessive forces Dr. Newman is adjunct associate professor, school of dentistry, University of California, The Center for the Health Sciences, Los decreases success Angeles, CA 90024. Requests for reprints should be sent to him at that address. Table 9. Treatment modalities currently used in LJP patients.

Nonsurgical References Plaque control 1. Newman, M., Williams, R., Crawford, A., Manganiello, A. D. Root planing and Socransky, S. S.: Predominant cultivable microbiota of per- iodontitis and periodontosis. III. Periodontosis, Journal of Dent Antibacterial agents Res, 52, Abst. 290,1973. Orthodontic treatment 2. Manganiello, A. D., Socransky, S. S., Smith, C., Propas, D., Occlusal adjustment Orham, V., Digon, I.: Attempts to increase viable count recovery of human supragingival , J Period Res, 12:107, Surgical 1977. Mucoperiosteal flap 3. Socransky, S. S.: Microbiology of periodontal disease — present status and future considerations, J Periodontol, 48:497,1977. Osseous grafting 4. Newman, M. G.: The role of Bacteroides melaninogenicus and Autologous tooth transplantation other anaerobes in periodontal infections, Reviews of Infectious Hemisection, root amputation Disease, 2:313,1979. Extraction 5. Newman, M. G.: Periodontosis, Journal of the Western Society ofPeriodontology, 24:5-16,1976.

PEDIATRIC DENTISTRY 125 Volume 3, Special Issue 6. Hashim, J. R., Ruben, M. P., Kramer, G. M.: Cellular and im- tor(s), IADRAbstract, 446, 1979. mune mechanisms in juvenile periodontitis, J West Soc Perio, 30. Baehni, P., Tsai, C., McArthur, W., Hammond,B., Socransky, 27:40, 1979. S. S. Taicbanan, N.: Leukotoxicity of various Actinobacillus 7. Manoucheln-Pour, M. and Bissada, N. F.: Juvenile perlodontitis actinomycetemcomitans isolates, J Dent Res Abst, 223, 1980. (periodontosis): A review of the literature, J West Soc Pe~o, 27: 31. Taichman, W. S. and Wilton, J. M. A.: Cytotoxicity of Actinoba- 86, 1979. cillas actinomycetemcomitans (Y4) Leukotoxin for gingival crev- 8. Hormand,J., Frandsen, A.: Bone loss in juvenile periodontitis, J ice PMNs,J Dent Res Abst., 224, 1980. Clin Pe~o, 6:417, 1979. 32. Nisengard, R. S., Myers, D. and Newman, M, G.: Human anti- 9. Sugerman, M. M. and Sugerman, E. F.: Precocious periodontitis: body titers to periodontosis associated microbiota, J Dent Res, A clinical entity and a treatment responsibility, Journal of Per- IADR Abstract 1977. iodontology, 48:397,409. 33. Kaslick, R. S., West, T. L., Singh, S. M., Chasens, A. I.: Serum 10. Baer, P. N. and Kaslick, R. S.: Periodontosis: A confusion of immunoglobulins in periodontosis patients, J Pe~odontol, 51: terminology, JPe~odontol, 50:153, 1979. 343, 1980. 11.Baer, P. N. and Benjamin, S.: Periodontal Disease in Cblldren 34. Nisengard, R. J., Newman, M. N., Myers, D., Horkoashi, A.: and Adoleecenta, J. B. Lipincott, 1974. Humeral responses in idiopathic juvenile peri.odontitis {perio- 12. Baer, P. N.: The case for periodontosis as a clinical entity, JPer- dontosis), J Periodontol, 51:30, 1980. iodontol, 42:516, 1971. 35. Murray, P. A., Genco, R. J.: Serum and gingival fluid antibodies 13. Waerhaug, J.: Subgingival plaque and loss of attachment in per- to A. actinomycetemcomitans in localized juvenile periodontitis, iodontosis as evaluated on extracted teeth, Journal of Pe~odon- J Dent Res, Abst. 245, 1980. tology, 48:125-130, 1977. 36. McArthur, W., Tsai, C. C., Baehni, P., Hammond,F. G., Taich- 14. Newman,M. B., Angel, I., Karge, H., Weiner, M., Grinenko, V., man, N. S. and Genco, R.: Inhibition of Y4 leukotoxic activity Schusterman, L.: Bacterial studies of the Papillon-Lefevre syn- by sera from juvenile periodontitis patients, IADR Abstract, drome, JDent Res, 56:545, 1977. 116, 1979. 15. Clark, R. A., Page, R. C. and Wilde, G.: Defective neutrophil 37. Genco, R. J., Taichman, N. A., Sadowski, L. A.: Precipitating chemotaxis in juvenile periodontitis, Infect Immun,18:694, 1977. antibodies to A. actinomycetemcomitans in localized juvenile 16. Hew, E. and Killoy, W.: The incidence of periodontosis in a periodontitis, JDent Res, Abst. 246, 1980. young military population, Unpublished study, 1979. 38. Ebersole, J. L., Frey, D. E., Taubman, M. A., Smith, D. S. and 17. Listgarten, M. A.: Structure of the microbial flora associated Genco, R. J.: Serum antibody response to A. actinomycetem- with periodontal health and disease in man, J Pe~odontol, 47:1, comitans (Y4) in periodontal disease, J Dent Res, Abst. 249, 1976. 1980. 18. Allen, A. L. and Brady, J. M.: Periodontosis: A case report with 39. Ebersole, J. L., Frey, D. E., Taubman, M. A., Smith, D. J., scanning electron microscopic observations, J Periodont, 49:415- Genco, B. F., Hammond,B. F.: Antibody response to antigens 418, 1978. from A. actinomycetemcomitans (Y4): Relatiouship to localized 19. Newman,M. G., Socransky, S. S., Savitt, E. D., Propas, D. A. juvenile periodontitis (LJP), JDent Res, Abst. 255, 1980. and Crawford, A.: Studies of the microbiology of periodontosis, 40. Hammond,B. F., Darkes, M., Tsai, C. C.: Isolation and charac- J Periodontol, 47:373-379, 1976. terization of the group antigen of Actinobacillus actinomycetem- 20. Newman, M. G. and Socransky, S. S.: Predominant cultivable comitans, J Dent Res, Abst. 973, 1980. microbiota in periodontosis, JPeHodont Res, 12:120-128, 1977. 41. Lai, G. H. and Listgarten, M. A.: Circulating antibody titers to 21. Slots, J.: The predominant cultivable organisms in juvenile per- Actinobacillus actinomycetemcomitans in pati.ents with perio- iodontosis, Scand J Dent Res, 84:1, 1976. dontal disease, J Dent Res, Abst. 975, 1980. 22. Tanner, A. C. R., Haffer, C., Bratthall, G. T., Visconti, R. A. and 42. Nisengard, R. W. and Newman,M. G.: Unpublished results. Socransky, S. S.: A study of the bacteria associated with advanc- 43. Cianciola, L. J., Genco, R., Patters, M. and McKenna,J.: Defec- ing periodontal disease in man, J Cb’n Pe~odont, 5:278-307, tive polymorphonuclear leukocyte functions in a human perio- 1979. dontal disease, Nature, 165:445, 1977. 23. Savitt, E. and Hammond,Fo B.: Capnocytophaga: new genus of 44. Altman, L. C., Page, R. C., Bowen, T., Ochs, H. and 0sterberg, gram-negative gliding bacteria III. Physiological characteristics, S.: Neutrophil and monocyte chemotaxis in patients with var- Archives Microblol, 122:29, 1979. ious forms of periodontal diseases, J Dent Res, Abst. 252, 1980. 24. Leadbetter, E. R., Holt, S. C. and Socransky, S. S.: Capnocy- 45. Lavine, W. S., Maderazo, E. G., Stolman, J., Ward, P. A., Cogen, tophaga: new genus of gram-negative gliding bacteria. I. General R. B., Greenblat, I. and Robertson, P. B.: Impaired neutrophil characteristics, taxonomic considerations and significance, Arch chemotaxis in patients with juvenile and rapidly progressing Mlcrobiol, 122:9, 1979. periodontitis, JPeriodont Res, 14:10, 1979. 25. Newman, M. G., Sutter, V. L., Pickett, M. J., Blackman, M., 46. Budtz-J~’gensen, E., Ellegaard, J., Ellegaard, B., Jorgensen, F. Greenwood, J. R., Grinenko, V. and Citron, D.: Capnocy- and Kelstrup, J.: Cell-mediated immunity in juvenile periodon- tophaga, B. ochraceus, and DF-I: seponomy, detection and iden- titis and levamisole treatment, Scand Jour of Dent Res, 86, 124- tification, J Clln Micro, In Press. 129, 1978A. 26. Williams, B. L., Hollis, D. G., Holdeman, L. V.: Synonomy of 47. Budtz-J~’gensen, E., Ellegaard, J., Ellegaard, B., Jorgensen, F. CDCcoup OF-1 with species of Capnocytophaga, J Clin Micro, and Kelstrup, J.: The effect of levamisole on experimental gingi- In Press. vitis in juvenile periodontitis, J Pe~o Res, 11:460-473, 1978B. 27. Tanner, A. C. R. and Socransky, S. S.: Unpublished data, 1979. 48. Kehner, T., Wilton, J. M. A., Ivanyi, L. and Manson, J. D.: 28. Slots, J., Reynolds, H. S., Jobbins, P. M., Genco, R. J.: Actinoba- Immunological aspects of juvenile periodontitis (periodontosis), cillus actinomytemcomitans: Selective culturing and oral ecol- J Pe~o Res, 9:261-272, 1974. ogy in patients with localized juvenile periodontitis, JDent Res, 49. Waerhaug, J.: Plaque control in the treatment of juvenile perio- Abst. 244, 1980. dontitis, J Clln PeHo,4:29, 1977. 29. Tsai, C. C., Baehm, P., Hammond,B. F., Taichman, N. S. and McArthur, W. P.: Characterization of Y4-derived leukotoxic fac-

LOCALIZEDJUVENILE PERIODONTITIS (PERIODONTOSIS) 126 Newman