Effect of Sonic and Mechanical Toothbrushes on Subgingival Microbial Flora: a Comparative in Vivo Scanning Electron Microscopy Study of 8 Subjects

Isa ni Research

Effect of sonic and mechanical toothbrushes on subgingival microbial flora: A comparative in vivo scanning electron microscopy study of 8 subjects

Karen B, Williams, MS, RDHVCharles M, Cobb, DDS, PhDVHeidi J. Taylor, MS, Alan R. Brown, DDSVKimberly Krust Bray, MS,

Objedives; The purpose of this initial study was to evaluafe fhe effects of bcfii a sonic and a mechanical focfhbrush versus fhe effects of no freatment on depth of subgingival penetrafion of epifhelial and footh- assooiafed bacferia. Method and materials: Eight adult subjects exhibiting advanced chronic pericdontitis with at leasf 3 single-rocfed feeth thaf were in separate sextanfs wiffi facial pockefs a 4 mm and s 8 mm and fhaf required exfraction consfituted the expérimentai sample. Teeth were either subjected to 15 seconds of brushing wifh a mechanical toothbrush or a sonic tocfhbrush or leff untreated. The tesf toofh and fhe associafed soft fissue wall of the periodonfai pocket were removed as a single unit. Samples were processed and coded for blind examinafion by scanning elecfron microsoopy. Distribufionai and morpho- logic characferisfics of dominanf bacteria wifh specific emphasis on spirochetes were evaluafed for boffi epithelial- and foofh-associafed plaque. Results: No differences were found in morphotypes or disfribu- fional and aggregafional characteristics of epifhelial-associafed microbes in the f- to 3-mm subgingival zone befween fhe mechanical and sonic tocf h bru s h-freated groups and the control group. Both toothbrush groups featured disrupfion of microbes fhat extended up to 1 mm subgingivally. Roof surfaces on the sonic-treated samples appeared plaque-free at low magnificafion; however, af 4,70Dx, afhin layer of mixed morphofypes and intact spirochefes was found supragingivally and slighfly subgingivally. In comparison, mechanical brush samples feafured incompletely removed plaque, bofh supragingivally and subgingivally, wifh intact spirochetes presenf on subgingival root surfaces. Conclusion: Results suggest similar effecfs for bcfh sonic and mechanical toothbrushes on epifhelial- and footh-as so dated bacferial plaque in periodontal pockets and adjacenf root surfaces fhaf extend up to 1 mm subgingivally. Furfher, the presence of infact subgingival spirochefes suggesfs limifed exposure fo acousfical or mechanical energy from fhe foofhbrushes evaluafed, (Quintessence int2001:32:147-154)

Key words: mechanical, scanning microscopy, sonic, spirochefes, subgingival microflora, toofhbrush

lthough host response may be responsible for the CLINICAL RELEVANCE: The present study compares Atissue degradation associated with inflammatory the abilify of sonic and mechanical toothbrushes fo dis- periodontal disease, plaque remains the primary initia- rupf subgingival plaque af increasing depths within perio- tor or trigger,'"^ The most common form of periodon- dontal pockefs by examining fhe pockef soft tissue wall tal disease, chronic periodontitis, has been reported to and fhe associafed roof surface in 8 subjects. affect over 30% oí the adult population, with severe disease reported in T>/(i to 13% of adults,'''-* Periodontal therapy is directed toward the reduc- 'Direcfor of Ciinical and ApplieO Research, Scfiool of Denfistry, University tion and subsequent control of pathogenic bacterial of Missouri—Kansas City, Kansas City, Missouri. species. In order for periodontal therapy to be effec- ^Department of Periodonlics, School of Denfistry, University ot Missouri- Kansas City, Kansas City, Missouri. tive, a long-term commitment to oral hygiene is required of the patient.^-'' Currently, the principal ^Formerly, Deparfment of Dental Hygiene, School of Dentisfry, University ot Missouri—Kansas City, Kansas City, Missouri; presentiy, US Civii Service, means for the prevention and control of periodontal Vicenza, Itaiy, disease involves the systematic and efficient removal of 'Cral and Maxilloiacia! Surgery, School of Denfisfry, Universify of supragingival and suhgingival plaque hy oral hygiene, Missouri—Kansas Cify, Kansas City, Missouri, through mechanical and/or chemical means,''-'' ^Division ol Oenfai Hygiene, School of Denfisfry, University ot Missouri- While toothbrushing remains the single most Kansas Cify, Kansas City, Missouri. widely practiced personal plaque control method, Reprint requesfs; Or Charies M, Cobb, Departmenl of Periodontics, Sohool of Dentistry, Universify of Missouri—Kansas City, 650 East 25th there remains some controversy and a lack of defini- Streef, Kansas City, Missouri 6410B, E-mail; [email protected] tive evidence to clearly demonstrate the superiority of

Quinfessence International 147 • Wiilianis et al

any one toothbrush design or mode of action.'^"^i^ mechanical toothbrushes versus no treatment on depth Many individuals do not achieve tbe level of cleaning of subgingivai penetration and on aggregation cbarac- required for periodontal bealtb as evidenced by tbe teristics of epitbelial- and tootb-associated bacteria in levels of gingivitis and periodontal disease found in 8 subjects witb advanced cbronic periodontitis. tbe population.^'-^'^ A variety of electrically powered toothbrusbes has been developed to assist individuals in removing dental plaque. Short-term studies are METHOD AND MATERIALS divided on tbe issue of superiority wben it comes to tbe comparison of electric tootbbrushes^""^^ with their A total of 8 subjects over tbe age of 18 in good general manual counterparts.^^"" bealth were selected from the available pool of In the last decade, new toothbrushes that generate patients at the University of Missouri-Kansas City acoustical energy have been developed. Sonic tootb- School of Dentistry. Subjects were selected based on brusbes use a bigh frequency bristle motion, in addi- tbeir scheduled treatment of multiple extractlotis for tion to their scrubbing or plaque-removing activity, to advanced chronic periodontitis. All participants pre- create dynamic fluid activity.^^ Various in vitro studies sented with a minimum of 3 nonfurcated teeth in sep- suggest the sonic tootbbrusb bas tbe potential to lift arate sextants with poeket depths of £ 4 mm and £ 8 and disperse plaque bacteria up to 4 mm beyond tbe mm on facial surfaces of teeth scheduled for extrac- pbysical reach of the bristle tips tbrougb tbe generation. Prior to enrollment, subjects completed a med- tion of acoustical energy.'^""'" ical bistory form and were excluded from tbe study for Sonic toothbrusbes utilize solid state electronic a history of diabetes, blood dyscrasia, liver and kidney microcircuitry and an electromagnetic driver to disease, immunosuppression, bepatitis B or C, HIV achieve rapid bristle movement tbat produces mild infection, anticoagulant tberapy or cbronic use of cavitation in fluid as well as fluid streaming.-" •'^ Bristles non-steroid al anti-inflammatory medications, vibrate at 250 or 260 Hz (depending on tbe sonic rbeumatic fever, beart defects, and implant prostbesis brush), creating mild cavitation and bubble activity, or any other conditions necessitating propbylactic and move at 500 to 520 brusb strokes per second. In antibiotic therapy. In addition, subjects were excluded tbeory, attached plaque is removed not only by tbe for a bistory of antibiotic tberapy in tbe previous 3 direct action of tbe bristles, but also by tbe eftect of tbe montbs, evidence of oral/esophageal candidiasis, and vibrations carried in oral fluids. Tbis process is referred use of a sonic tootbbrush or any periodontal instru- to as acoustic microstreaming. Acoustic microstream- mentation in the previous 6 months. Tbe study was ing is characterized by the production of bydro- approved by the University of Missouri-Kansas City dynamic sbear stresses (bubble activity) and is tbought Institutional Review Board for Human Research, and to lift and disperse plaque from tbe teetb.^^-^*''"''*^ qualified subjects signed an informed consent form No clinical studies have demonstrated this "beyond prior to treatment. tbe bristles" effect In vivo; bowever, previous in vitro Premolars, canines and/or incisors from different studies bave shown acoustic energy is capable of dam- sextants scheduled for extraction due to advanced aging adherent bacteria on bydroxyapatite-coated chronic periodontitis were selected. All specimens disks.^^-'ä Tbe clinical relevance of these laboratory were free of cervical caries lesions, damage to dentinal results remains questionable due to tbe dynamics of surfaces, and periapicai or periodontal abscesses. brushing in the oral eavity. The ability of sonic vibra- The study was conducted as a 1-faetor within sub- tions to transmit througb a medium of crevicular fluid ject design. Subjects contributed at least 1 tooth to and into tbe subgingivai environment remains each treatment cell. Only one treatment was randomly unproven. Bristle contact with tbe oral soft and hard assigned per sextant to prevent overlapping treatment tissues may dampen tbe effects of sonic vibrations. effects. In some circumstances where multiple teeth Additionally, it can be hypothesized that pre-existing met entry criteria and were adjaeent in the mouth, 2 plaque accumulations, particularly if heavy, as well as samples were enrolled in the sonic and mechanical the viscosity of saliva may alter acoustical transmis- toothbrush group. All teeth were obtained from sion and potential effectiveness. patients with planned treatment of multiple extractions The in vivo effectiveness of sonic toothbrusbes to due to advanced chronic periodontal disease. At base- generate dynamic fluid activity that ¡nfluetices subgin- line, based on pretreatment gingival and plaque givai epithelial- and tooth-associated bacteria remains mdices, probing depths, and evidence of interproximai unknown. No studies have been published tbat exam- radiographie bone loss, there were no discernible dif- ine the in vivo subgingivai effects of sonic tootb- ferences in supragingival plaque level or gi-oival con- brushes. The purpose of this in vivo investigation was dition for tbe selected teetb. Teetb witbin t - object to qualitatively evaluate the effects of sonic and were randomly assigned to receive brusbing

148 Voiume 32, Numoer 2. 2U01 Williams et al a mecbanical toothbrusb (Plaque Remover 3000, aggregation cbaracteristics. Specific empbasis was Teledyne WaterPik) or a sonic tootbbrusb (Sensonic, given to the presence of intact spirochetes in each of Teledyne WaterPik) or were left untreated (to serve as tbe defined subgingival regions. Tbe 2 primary out- a control). Tbe toothbrushes were selected because come variables of interest were; (1) presence of intact tbey bad identical brusb bead design, thus eliminating spirochetes ranging from tbe gingival margin or CEJ to tbe potential differences from bristle type and head the most apical aspect of tbe poeket; and (2j morpho- configuration. All subjects were given brief, standard- logic cbaracteristics of dominant bacteria and distribu- ized tootbbrushing instructions for each toothbrusb tion of epitbelial- and tootb-associated microbes (eg, prior to use. A timed 15-second brushing period was single versus aggregate versus uniform dispersion). established for the 2 treatment groups. The sextant Spirochetes were used as marker organisms to assess assignment and sequencing of tootbbrusbing was ran- tbe potential of acoustical energy penetration in tbe domized. Immediately following tbe patient's timed periodontal pocket. Previous researcb bas demon- tootbbrushing, the control and treatment teetb were strated tbat spirocbetes are highly susceptible to struc- obtained by a combination of tooth extraction and tural damage when exposed to low levels of acoustical excisional biopsy under local anesthesia. An American energy.''^'"'' A total of 198 SEM photomicrographs were Board certified oral and maxillofacial surgeon per- taken of the 48 specimens. Representative photographs formed a reverse bevel incision in such a way tbat were selected to emphasize observations obtained dur- wben the tooth was extracted, tbe soft tissue wall of ing the qualitative data collection. tbe periodontal pocket was removed and kept intact witb tbe accompanying tootb. A total of 24 specimens consisting of teetb and RESULTS tbeir associated gingivae (n = 24 teeth and n = 24 gingival specimens) were processed for examination by Tbe distribution of tooth type to each of tbe treatment scanning electron microscopy (SEM). The specimens regimens was relatively equivalent witb respect to tbe were distributed equally among the 3 treatment proportion of incisors, canines, and single-rooted pre- groups, ie, 8 tooth and 8 gingival specimens per treat- molars in eacb group. Bacterial morpbotypes in tbe ment group. Specimens were fixed in 2.5% glutaralde- zone approximately 0.5 to 1.0 mm apical from the gin- hyde in 0.1 M sodium cacodylate buffer at pH 7.4 and gival margin of mechanical and sonic toothbrusb- stored at 4°C for 4 hours. Tbe specimens were buffer- treated teetb in the groups consisted of a sparse distri- rinsed with 0.1 M sodium cacodylate buffer at pH 7.4 bution of cocci, isolated sbort rods, and an occasional and placed on a shaking table for 5 minutes. intact spirochete (Figs 1 to 3). In contrast, control sam- Postfixation of tbe specimens consisted of P/o osmium ples exbibited numerous aggregates and/or a uniform tetroxide in a dark area. Tbe soft tissue was separated dispersion of a variety of mierobial morphotypes in tbe from the tooth under a dissecting microscope and same region (Fig 4). In tbe region s 1 mm below tbe mounted to facilitate viewing of the soft tissue pocket gingival margin, specimens in all groups demonstrated wall. Tootb samples were mounted next to their corre- m i crou Iceration witb numerous aggregations of mixed sponding soft tissues to allow examination and com- bacterial morphotypes. Gcneraliy, sucb ulcerated parison. All specimens were dehydrated tbrougb epitbelium exhibited clumping of erytbrocytes and var- ascending grades of ethanol followed by sputter coat- ious inftammatory ceils. The most notable finding was ing witb 200 Â of gold palladium. Specimens were tbe similarity in morphotype, distribution, and aggrega- examined in a SEM (Pbilips, Model 515), and pbo- tion characteristics of epiÜielial-associated microbes in tomicrograpbs were made for analysis. tbe 1- to 3-mm subgingival zone, for mechanical and Using tbe micrometer bar on the SEM, landmarks sonie tootbbrusb-treated groups (Figs 5 and 6). were selected on each specimen to represent subgingi- Evaluation of mechanical and sonic toothbrush-treated val regions of 0 fo 2 mm, 3 to 4 mm, and > 5 mm to samples revealed a routine and generaiized disruption permit selections of comparable areas for viewing. Soft of plaque that extended no greater than 1 mm subgin- tissue specimens were systematically examined, mov- givally. Spirocbetes present at all levels of tbe soft tis- ing from tbe gingival margin to the base of tbe pocket. sue pocket wall exhibited intact morpbology suggesting Teeth were examined in a similar manner from the a lack of exposure to acoustical or mecbanical energy. cementoenamei junction (CE|) to the plaque-free zone. Tooth surfaces exposed to the mecbanical and sonic All specimens were coded to permit evaluation by one toothbrusbes exhibited differences in tooth-associated experienced examiner who was blind to the treatment plaque. Supragingival and sbghtly subgingivai sample assignment. Specimens were photographed at various areas treated witb tbe sonic brush had the gross magnifications, and the blind examiner dictated notes appearance of being plaque-free witb a polisbed regarding observations on microbial morpbotypes and appearance when evaluated at £ 25 x magnification

Quintessenoe internationai 149 • Wiiiiamsetal

Fig 1 Low magnitioation overview ot the coronai 3 mm zone ot a Fig 2 Residuai cocci iocated within the coronal 0.5- to 1-mm pocket soft tissue waii from a sonic toothbrush-treated specimen. zone of the pocket soft lissue wall after treatment wilh the sonic Note tiiat tfie coronal 1 mm zone appears to exiiibit iess debris toothbrush. Bar = 10 |jm: originai magnification, 5,000>c, than ttie apical 2 mm. Bar = 1 mm; original magnitication, 27,6x,

Fig 3 Cocci located with the coronal 0.5- to t-mm zone of the Fig 4 Coronai 0 5- to 1-mm zone of an untreated controi speoi- poci^et soft tissue waii (oliowing treatment with the mechanical men teaturing numerous spirochetes and fusoform bacteria Bar = tooliibrusti Bar = 10 |jrn; originai magnification, 2,öODx. 10 Mm: originai magnification, 4,200x,

(Fig 7). However, examination at higher magnification by a thick, organized plaque with numerous morpho- revealed the presence of a thin but uniform layer of ti^pcs, including spirochetes (Fig 10), As with the soft plaque consisting of mixed morpbotypes including tissue samples, spirochetes present on subgingival root intact spirochetes (Fig 7 inset). Root surfaces subgingi- surfaces exhibited an intact morphology, suggesfing no vally beyond the first millimeter showed dense trtasses direct effect of mechanical and/or acoustical energy. of aggregate organisms, suggesting no effect other than that achieved by direct bristle contact (Fig 8 and inset). Root surfaces in the mechanical brush-treated group DISCUSSION examined at £ 25x magnification featured incompletely removed plaque, both supragingivally and sub- The purpose of this investigation was to ev gingivally {Fig 9), Control samples were characterized • te the effects of a sonic and electric toothbrush -=is no

150 Volume 32, Number 2, Wiiliams et al •

Fig 5 Subgingpvai zone ot 1- to 3-mm from a soniG Fig 6 View ol a mectianicai tact h brush-treated specimen at the 1 • toothbrush-treated specimen showing intact spiroclietes, short to 3-mm subgingivai zone showing an aggiegation of mixed bacte- and medium iength rods, and cocci. Bar = 10 |jm: originai magni- nal morptiotypes, irciuding cocci, spirocheies. anä short and tication, 3,700x. medium iength rods. Bar = 10 pm: originai magnitication, 3.860x.

Fig 7 Low magnitication view ol ¡fie root surlace ol a sonic tooth- Fig 8 Root surtaces from scnic foothbrusti-treated specimens brusii-treated specimen showing what appears to be a reiativeiy generaiiy exhibited a heavy mass of baoteriai piaque in the 1- to ciean surtace. However, at higher magnification [insell. the sur- 3-mm zone that featured a wide range of micrcbiai motpholypes face exhibits a iayer of diverse miorobial morphotypes in the coro- (inset). Bar = 0.1 mm; originai magnification. 356x, inset: bar = 5 nal 0 5- to 1-mm zone. Bar = 1 mm; originai magnification, 2t,2x. pm: onginal magnification. 3,22Ox Inset, oar = 5 |jm; original magnification, 4,700X. treatment on epithelial- and tooth-associated bacteria cal significance of the dynamic fluid action in patients with untreated periodontal disease. While (microstreaming) on the attached subgingival biofilm some authors have suggested that low frequency located beyond tbe pbysical reach of the bristles. acoustic energy generated by a sonic toothbrush The present study demonstrates that 15 seconds of reduces the adherence of bacteria to saliva-treated exposure to the acoustical energy generated by a sonic hydroxyapatite disks, that damaged bacterial fimbria tootbbrush or direct disruption from a mechanical plays an important role in bacterial adherence, and tootbbrush has a trend toward modifying the epithelial that adherent bacteria is reduced due to dynamic fluid associated bacteria of human periodontai pockets up action, none of these findings bas been observed out- to approximately 1 mm subgingivally in patients with side laboratory settings.'^•^^••'^ It is interesting to note advanced chronic periodontitis. In tbe context of this that none of these studies has demonstrated the cJini- study, subjects lacking tbe benefits of routine scaling,

Quintessence Internationai 151 • Wiiiiamsetal

Fig 9 Root surlace ol a specimen Irom ihe mechanicai looth- Fig 10 Root surface oí an untreafed controi speoirren teaLuring a brush-freated group showing a fhick aocumuiation of microbiai thick mat ot microbiai piaque in the subgingivai t- to 3-mm zone, plaque in fhe subgingivai f- tb 3-mni zone. Bar = 0.1 mm; original Eniargemenf at right shows tiie surtace piaque fo be cornprised of magnification, 925x. cocci ana iong filamentous rods. Bar = 50 um: originai magnification, 1,630X. Righf photo bar - 50 |jm; original magnification, 4,900 X.

root planing, and regular periodontal maintenance penetration of the bristles and/or acoustical energy showed minimal disruption in periodontal pockets beyond the gingival margin. These results are in agree- after a 1-time 15-second treatment with a sonic or ment with previous research that demonstrated the mechanical toothbrush. capacity of toothbrush bristles to penetrate into the Additionally, the lack of surface alteration of spiro- gingival sulcus with ranges from 0,70 + 0,44 mm to chetes present in the most coronal aspect of the 1,40 ± 0,66 mm, depending on the design of the tooth- pocket suggests acoustical energy did not penetrate brush and bristles or the angle at which the bristles are subgingivally. Previous research has demonstrated that held to the teeth,*« direct exposure to sonic energy generated by a sonic Gross evaluation of the supragingival zotie of sonic toothbrush disrupts the structural integrity of T denti- brush-treated tooth samples gave the impression of a cola, in vitro,•'^ It was hypothesized that the presence plaque-free, polished surfaee compared to the of flaccid tissues and higher levels of gingival crevicu- mechanical toothbrush-treated teeth. This observed lar fluid (GCF) present in inflammation in this patient difference at lower magnification may have resulted population might have made the subgingival area from the discrepancies in brush stroke cycles between more accessible to acoustical microstreaming in the meehanical and sonic brushes (approximately 2,800 specimens, thus facilitating a "beyond-the-bristles" versus 30,000 strokes). The higher number of brush effect. The similarities in distribution of both the sub- cycles coupled with the lighter pressure required to gingival organisms and presence of intact spirochetes prevent attenuation of bristle action may have resulted in the 2 toothbrush-treated groups suggests that the in a slightly different scrubbing efficiency for the sonic slight effect observed £ 1 mm subgingivally is likely brush. However, examination at a higher magnifica- limited to the physical penetration of toothbrush bris- tion revealed both groups had biofllms consisting of tles. The lack of additional advantage for the sonic mixed morphotypes, including nonaltered spirochetes. brush may be a result of insufficient GCF to transmit If the rapid brush strokes and generated acoustical the acoustic energy subgingivaily. The average quantity energy created efficiency for the sonic brushes, one of GCF present in a 5-mm pocket, approximately 0.5 would expect to see compelling differences in clinical ^L*^'*' is likely too meager to transmit the generated parameters. Although several studies have shown the acoustic energy wavelength. sonic hrush to significantly reduce plaque, gingival Similarly, the difference between mechanical and bleeding, and gingival index scores compared with sonic toothbrushes on supragingival and subgingival manual hrushing,'^'-"« these results have not trans- plaque of root surfaces was minimal. The presence of lated to comparable efficacy when comparir • sonic to dense masses of organisms with intact spirochetes mechanical brushing,^--^^ It should be noted • •( stud- beyond the ^ 1 mm subgingival zone suggests minimal ies evaluating the effects of mechanical .

152 Volume 32, Number 2, 2001 Wiiiiams el al • toothbrusbes versus manual tootbbrusbes bave sbown REFERENCES similar proportional decreases in various clinical para- meter measurements in all treatment groups. 1. Loe H, Tlieilade E, Jensen SE. Experimental gingivilis iti Tbis study did not address the effect of sonic tooth- man. J Periotlontol 1965;36:177-187, brushes on human periodontal pockets and tooth sur- 2. Socransky SS, Haffajee AD. The bacterial etiology of faces for patients receiving regular professional and destructive periodontal disease. Current concepts. J Peri- odontol 1992;63;322-331. self-maintenance care. Clearly, the design of the study 3. Brown LJ, Loe H. Prevalence, extent, severity and progres- limited the population to individuals requiring multi- sion of periodontal disease. Periodontol 2000 1993;2:57-71. ple extraction for advanced periodontal disease. Con- 4. Socransky SS, Haffajee AD. 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Treating plaque-associated gin- imal wben compared to no treatment control samples. givitis. In: Wilson TG, Kornman KS (eds]. Fundatnentals of Both brushes demonstrated a disruptive effect on sub- Periodontics. Chicago: Qtj int esse nee, 1996:330. gingivai microflora s 1 mm, and in all samples, spiro- 13. Drisko CH. Non-antiblotie plaque eontrol. In: Newtnan chetes present in tbe most coronal zone subgingivally HN, Wilson M (eds). Dental Plaque Revisited: Oral Biofilms were intact witb no structural cbanges evident. Results in Health and Disease. Cardiff, UK: BioLine, 1999:523-548. of this study, based on a limited number of subjects (n 14. Cobb CM. Non-surgical pocket tberapy: Mechanical. Ann Periodontoi 1996;1.443-490. = 8), do not support a clinically evident "beyond tbe 15. Cobb CM. Modern methods for the mechanical control of bristles" effect favoring the sonic toothbrusb. subgingivai plaque. In: Newman HN, Wilson M (eds). Dental Plaque Revisited: Oral Biofilms in Healtb and Disease. Cardiff, UK: BioLine, 1999:457-502, CONCLUSION 16. Forgas-Brockmart LB, Carter-Hanson C, Killoy WJ. The effects of an ultrasonic toothbrush on plaque accumulation and gingival inflammation. J Clin Periodontol 1998; In tbe group of 8 test subjects, similar effects were 25:375-379. acbieved by the sonic and meebanical tootbbrusbes on 17. Issacs RL, Beiswanger BE, Rosenfield ST, Crawford JL, Mau epithelial-associated bacterial plaque in periodontal MS, Eckert GJ, Warren PR. A crossover clinical investiga- pockets up to 1 mm subgingivally. Similar effects were tion of tbe safety and effieacy of a new oscillating/rotating acbieved by tbe sonic and meebanical toothbrushes on electric tootbbrusb and a bigh frequency electric tootbbrush. tooth root-associated bacterial plaque up to 1 mm AmIDentl998;ll:7-12, subgingivally, Tbe presence of intact subgingivally 18. Bader HI, Boyd RL. 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