journal of the american dental association:...
TRANSCRIPT
T he featured Cover Story of the July 2000 Journal of the American DentalAssociation (JADA) is a 13 page article authored by John Featherstone, M.Sc.,Ph.D., Professor and Chair, Department of Preventive and Restorative Dental
Sciences and Department of Dental Public Health and Hygiene, University of California,San Francisco.
If that sounds like a mouthful, it is. And that is exactly what Dr. Featherstone delivers.
Following in the footsteps of 16 other cited articles that he has either authored or co-authored, Featherstone reminds the reader (in this case the dues-paying members of the American Dental Association) that fluoride’s preventive action is topical ratherthan systemic.
Before you begin jumping up and down in delight or horror, depending on whether youare an avid promoter of using the public water for mass medication or a modern-dayKeeper-of-the-Well, hold your horses.
Featherstone continues to give water fluoridation credit for helping reduce tooth decay– not because it is ingested – but because, he states, fluoridated water and otherfluoride-containing beverages, foods, and oral care products contribute to the dailytopical application of fluoride by bathing the teeth.
In his article, The Science and Practice of Caries Prevention, Featherstone concludesthat fluoride is a key agent in battling caries, but that it is accomplished by three
principal topical mechanisms of action: inhibition of demineralization,enhancement of remineralization, and inhibition of bacterial enzymes. He notes that remineralization of early lesions also requires calcium andphosphate, which are derived primarily from saliva and plaque fluid.
Featherstone makes it clear, as he has in other publications, that fluorideincorporated during tooth development is insufficient to play a significantrole in caries protection. He cites, as an example of the weak pre-eruptiveeffects of fluoride, a study of two groups of Okinawa nursing studentswhich showed that there was no difference in caries status between those
who had received fluoridated water only until about 5 to 8 years of age (and nonethereafter) and those who had never received fluoridated drinking water.
“Importantly, this means that fluoride incorporated during tooth mineral developmentat normal levels of 20 to 100 ppm (even in areas that have fluoridated drinking wateror with the use of fluoride supplements) does not measurably alter the solubility of themineral,” writes Featherstone. “Even when the outer enamel has higher fluoride levels,such as 1000 ppm, it does not measurably withstand acid-induced dissolution anybetter than enamel with lower levels of fluoride.”
This is not new information to those who have thoroughly researched the issue, nor is itnew for Dr. Featherstone to write or lecture on this and many other findings with thesame results. Dr. Featherstone was a featured speaker at the 1997 Canadian conferenceon controlled-dose fluoride supplements at which he reminded representatives ofCanada’s dental and medical stakeholders of the reports given at their 1992 conferenceon the same subject. These reports indicated that ingested fluoride cannot raise thefluoride concentration in the glanular saliva sufficient to meet the bacterial challengepresent in the oral cavity.
Contact: Jeff Green
(800) 728-3833
Citizens for SafeDrinking Water
1010 University Avenue # 52
San Diego, CA 92103
JOURNAL OF THE AMERICAN DENTAL ASSOCIATION:
Ingested fluoride does not reduce tooth decay, action is topical
Featherstone makes it clear, as he has in other publications,
that fluoride incorporatedduring tooth development is
insufficient to play a significantrole in caries protection.
As a consequence of that conference, the Canadian Dental Association no longerrecommends fluoride supplements if a child brushes his teeth twice a day withfluoridated toothpaste, and if individual practitioners are determined to increasefluoride exposure for high caries-risk patients in non fluoridated regions, CDArecommends that supplements be used as topical lozenges rather than swallowed.
With a title as all-inclusive-sounding as The Science and Practice of CariesPrevention, it is all too easy to erroneously dismiss its importance by pointing to what was not covered, such as irrigation devices, baby bottle tooth decay, and early childhood exposure to oral infections from primary care givers; yet many readers may be surprised at the introduction of other topics that may warrant their further exploration.
Other detractors may be angered by the avoidance of any mention about whatconstantly bathing the teeth with fluoride will do for total fluoride exposure and theconsequences to every other organ and systemic function; but alas the dental industryhas no responsibilities in other health arenas, so this publication may never be seen asthe appropriate venue for that discussion.
And yes, one topic that is glaring by its omission in a dental discussion is theincidence of dental fluorosis, which has risen to include 66.5% of ourchildren in fluoridated communities displaying the visible signs of fluorideoverdose on at least one tooth.
So why is this article so important? Contrary to promotional brochuresprinted by the dental trade organizations touting the safety and effectivenessof fluoride at virtually any exposure level, previous articles published by JADA
warned of high concentrations of fluoride in chicken and other baby foods, andadvised dentists to warn parents to restrict children’s consumption of fruit juicesbecause of fluoride pesticide residues. Once again the Journal of the American DentalAssociation has confirmed that the dental community is not all of one mind, that theportrayal of the oral ingestion of fluoride as magically-effective but never-unsafe cannow be corrected by the dental association membership.
It matters not whether Featherstone does or does not have the proof for his contentionthat 1 ppm in the water flowing past the teeth plays any significant role in cariesreduction compared to the 1000 ppm in fluoridated tooth paste. The true questionremains:
Will an informed public, a deliberative body such as a water board or citycouncil, or health professional with no other axe to grind than the overallwell-being of their patient, continue to support the forced everydayingestion of a substance that is functional only as a topical application?
Ingested fluoride does not reduce tooth decay, cont.
Once again the Journal ofthe American Dental
Association has confirmedthat the dental community
is not all of one mind…
JADA, Vol. 131, July 2000 887
C O V E R S T O R Y
THE SCIENCE AND PRACTICEOF CARIES PREVENTIONJOHN D.B. FEATHERSTONE, M.SC, PH.D.
A B S T R A C T
Background and Overview. Dentalcaries is a bacterially based disease. Whenit progresses, acid produced by bacterialaction on dietary fermentable carbohy-drates diffuses into the tooth and dis-solves the carbonated hydroxyapatite min-eral—a process called demineralization.Pathological factors including acidogenicbacteria (mutans streptococci and lacto-bacilli), salivary dysfunction, and dietarycarbohydrates are related to caries pro-gression. Protective factors—whichinclude salivary calcium, phosphate andproteins, salivary flow, fluoride in saliva,and antibacterial components or agents—can balance, prevent or reverse dentalcaries.Conclusions. Caries progression orreversal is determined by the balancebetween protective and pathological fac-tors. Fluoride, the key agent in battlingcaries, works primarily via topical mech-anisms: inhibition of demineralization,enhancement of remineralization andinhibition of bacterial enzymes.Clinical Implications. Fluoride in drink-ing water and in fluoride-containingproducts reduces caries via these topicalmechanisms. Antibacterial therapy mustbe used to combat a high bacterial chal-lenge. For practical caries managementand prevention or reversal of dentalcaries, the sum of the preventive factorsmust outweigh the pathological factors.
Although the prevalence of dental
caries in children has declined
markedly over the last 20 years in
most countries in the Western world,
the disease continues to be a major problem for both adults
and children everywhere.
The trends in caries in U.S. children during the last 30
years were recently summarized1 on the basis of results of
four national surveys.2-6 By the late 1980s, although
approximately 75 percent of children aged 5 to 11 years
were caries-free, about 70 percent of the 12- to 17-year-olds
still had caries. Approximately 25 percent of children and
adolescents in the 5- to 17-year age range accounted for 80
percent of the caries in permanent teeth. By age 17 years,
however, 40 percent of the population accounted for 80 per
cent of the caries.1-6 These findings illustrate the need for
management of caries by individual risk assessment and
for measures more specifically directed to high-risk people
and populations.
Although these prevalence rates still leave much to be
desired, the overall caries prevalence in children has
indeed declined in the United States. Smaller epidemiolog-
ic studies in recent years indicate, however, that the
decline in caries has not continued during the 1990s and
that it may have plateaued.6
ARTICLE 1
888 JADA, Vol. 131, July 2000
The reasons for the reduc-tions in caries prevalence dur-ing the last 20 years are diffi-cult to pinpoint. Strong evi-dence exists, however, that thenear universal use of fluoridecontaining products such asdentifrice, mouthrinses and top-ical gels applied in the dentaloffice have been major contribu-tors.7,8 Earlier caries reductionsof 40 to 70 percent (before the1970s) had resulted from thefluoridation of public water sup-plies in many communities.9-12
Dental caries in adults alsocontinues to be a major prob-lem, as illustrated by a recentU.S. survey.l3 The surveyreported that 94 percent of alldentate adults (aged 18 yearsor older) had evidence of treated or untreated coronal caries.
Caries obviously still is amajor problem in adults, aswell as children, and we needan improved approach to pre-vention and therapy. This arti-cle reviews and summarizes thescientific basis for and practiceof successful intervention inthe caries process.
THE CARIES PROCESS
Bacterial plaque and acidproduction. The caries processis now well-understood; much ofit has been described extensivelyin the dental literature. Somedetails of the caries processremain to be unraveled, but, ingeneral, we understand theprocess well enough to initiatebetter-targeted methods of cariesprevention and intervention.
The mechanism of dentalcaries formation is essentiallystraightforward.1 Plaque on thesurface of the tooth consists of abacterial film that producesacids as a byproduct of itsmetabolism.14,15 To be specific,certain bacteria within the
plaque are acidogenic—that is,they produce acids when theymetabolize fermentable carbo-hydrates.12,14,15 These acids candissolve the calcium phosphatemineral of the tooth enamel ordentin in a process known asdemineralization.16-18 If thisprocess is not halted or re-versed via remineralization—the redeposition of mineral viasaliva—it eventually becomes afrank cavity.
Dental caries of the enameltypically is first observed clini-cally as a so-called “white-spotlesion.” This is a small area ofsubsurface demineralizationbeneath the dental plaque. The
Any fermentable carbohy-drate (such as glucose, sucrose,fructose or cooked starch) canbe metabolized by the acido-genic bacteria and create theaforementioned organic acids asbyproducts.22 The acids diffusethrough the plaque and into theporous subsurface enamel (ordentin, if exposed), dissociatingto produce hydrogen ions asthey travel.17,23 The hydrogenions readily dissolve the miner-al, freeing calcium and phos-phate into solution, which candiffuse out of the tooth. Mostimportantly, lactic acid dissoci-ates more readily than theother acids, producing hydrogenions that rapidly lower the pHin the plaque.’7 As the pH islowered, acids diffuse rapidlyinto the underlying enamel ordentin.
The two most importantgroups of bacteria that predom-inantly produce lactic acid arethe mutans streptococci and thelactobacilli.’4 Each group con-tains several species, each ofwhich is cariogenic. Mutansstreptococci include Strep-tococcus mutans and S. sobrinus. The lactobacilli speciesalso are prolific producers oflactic acid and appear in plaquebefore caries is clinicallyobserved.24 25 These two groupsof bacteria, either separately ortogether, are the primarycausative agents of dentalcaries.
HOW FLUORIDECOMBATS THECARIES PROCESS
The ability of fluoride to pre-vent and arrest caries has beenresearched extensively. Fluo-ride has three principal topicalmechanisms of action:� inhibiting bacterial metabo-lism after diffusing into the
body of the subsurface lesionmay have lost as much as 50percent of its original mineralcontent and often is covered byan “apparently intact surfacelayer.”’19 The surface layer formsby remineralization. Theprocess of demineralization con-tinues each time there is carbo-hydrate taken into the mouththat is metabolized by the bac-teria. The saliva has numerousroles, including buffering (neu-tralizing) the acid and reminer-alization by providing mineralsthat can replace those dissolvedfrom the tooth during deminer-alization.1,20,21
The mutansstreptococci andthe lactobacilli,either separatelyor together, are
the primarycausative agents of
dental caries.
COVER STORY
JADA, Vol. 131, July 2000 889
bacteria as the hydrogen fluo-ride, or HF, molecule when theplaque is acidified;� inhibiting demineralizationwhen fluoride is present at thecrystal surfaces during an acidchallenge;� enhancing remineralizationand thereby forming a low-solubility veneer similar to theacid-resistant mineral fluorap-atite, or FAP, on the remineralized crystals.
Inhibiting bacterialmetabolism. Several investiga-tors have studied the possibleeffects of fluoride on oral bacte-ria.26-28 The most significantfinding reported is that the ionized form of fluoride, or F-, cannot cross the cell wall andmembrane but can rapidly trav-el into the cariogenic bacterialcells in the unchanged form asHF. 26-28
When the pH in the plaquefalls as the bacteria produceacids, a portion of the fluoridepresent in the plaque fluid thencombines with hydrogen ions toform HF and rapidly diffusesinto the cell, effectively drawingmore HF from the outside.1,26-28
Once inside the cell, the HF dis-sociates, acidifying the cell andreleasing fluoride ions thatinterfere with enzyme activityin the bacterium. For example,fluoride inhibits enolase, anenzyme necessary for the bacte-ria to metabolize carbohydrates.As fluoride is trapped in thecell, the process becomes cumu-lative.
In summary, fluoride fromtopical sources is converted par-tially to HF by the acid that thebacteria produce and diffusesinto the cell, thereby inhibitingessential enzyme activity.
Inhibiting demineraliza-tion. The mineral of our teeth(enamel, cementum, dentin)
and bones is a carbonatedhydroxyapatite29 that can beapproximately represented bythis simplified formula:
Ca10-x(Na)x(PO4)6-y(CO3)z
(OH)2-u(F)u
The substitutions in thehydroxyapatite crystal lattice(the arrangement of atoms andions in the crystal) occur as themineral is first laid down dur-
ing tooth development, with thecarbonate (CO3) ion in particu-lar causing major disturbancesin the regular array of ions inthe crystal lattice.30,31 Duringdemineralization, the carbonateis lost, and during remineral-ization it is excluded from thenewly formed mineral. The cal-cium-deficient, carbonate-richregions of the crystal are espe-
Figure 1. High-resolution electron microscope images (magnificationapproximately x2,000,000) of individual enamel crystals. The blacklines are rows ot calcium atoms, which are visualized by this technique. A. Normal enamel crystal showing white patches (arrows),which are calcium-deticient and carbonate-rich detect regions.B. Demineralized crystal trom the body ot a natural caries lesionshowing “large” hexagonal holes coinciding with the “small” detectregions seen in normal enamel. (Adapted trom Featherstone and col-leagues.30,31)
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890 JADA, Vol. 131, July 2000
cially susceptible to attack bythe acid hydrogen ions duringdemineralization, as has beenshown by several investigators.21,29-33 High-resolution lat-tice imaging, which imagescrystals almost to atomic reso-lution (viewed at aboutx2,000,000 magnification), wasused to illustrate the appear-ance of hexagonal holes in theearly stages of enamel crystaldissolution in dental caries(Figure 1), which coincided withthe calcium-deficient, carbon-ate-substituted regions of thecrystal.30-33
The carbonated hydroxyap-atite, or CAP, of our teeth ismuch more soluble in acid thanhydroxyapatite, or HAP(HAP = Ca10(PO4)6(OH)2), andthat in turn is much more solu-ble than fluorapatite, or FAP(FAP = Ca10(PO4)6F2),21 in which
the OH- ion in pure hydroxyap-atite is completely replaced byan F- ion. The resulting mineralFAP is highly resistant to disso-lution by acid.
Fluoride inhibits demineral-ization. Sound enamel, exceptin its outer few micrometers,generally contains fluoride atlevels of about 20 to 100 partsper million, or ppm, dependingon the fluoride ingestion duringtooth development.34 Teeth inchildren who lived in areaswith fluoridated drinking waterduring tooth development havefluoride content toward thehigher end of this range. Theouter few micrometers of en-amel can have fluoride levels of1,000 to 2,000 ppm.34
Fluoride in the solution sur-rounding CAP crystals has beenshown to be much more effec-tive in inhibiting demineraliza-
tion than fluoride incorporatedinto the crystals at the levelsfound in enamel.21,35 Ten Cate,21
Nelson and colleagues35 andFeatherstone and colleagues35,37
found no measurable reductionin the acid solubility of synthet-ic CAP (3 percent CO3 byweight, comparable to that ofdental enamel mineral) withabout 1,000 ppm fluoride incor-porated. Importantly, thismeans that fluoride incorporat-ed during tooth mineral devel-opment at normal levels of 20to 100 ppm (even in areas thathave fluoridated drinking wateror with the use of fluoride sup-plements) does not measurablyalter the acid solubility of themineral. Even when the outerenamel has higher fluoride lev-els, such as 1,000 ppm, it doesnot measurably withstand acid-induced dissolution any betterthan enamel with lower levelsof fluoride. Only when fluorideis concentrated into a new crys-tal surface during remineraliza-tion is it sufficient to beneficial-ly alter enamel solubility. Thefluoride incorporated develop-mentally—that is, systemicallyinto the normal tooth mineral—is insufficient to have a measur-able effect on acid solubility.21,38
In contrast to the lack ofeffect of fluoride incorporatedinto the CAP crystals of toothmineral developmentally, as lit-tle as 1 ppm in the acid solutionreduced the dissolution rate ofCAP to a rate equivalent tothat of HAP.36 Further increas-es in fluoride in the acid solu-tion in contact with the CAPmineral surface decreased thesolubility rate logarithmically.These results indicate that iffluoride is present in the aque-ous solution surrounding thecrystals, it is adsorbed stronglyto the surface of CAP carbonat-
Figure 2. Typical pH curves for normal subJocts with normal salivaryflow and for subjects with xerostomia (mean for each group) afteringestion of sucrose. A curve for ingestion of a sugar-free sweetenedproduct is shown for comparison. (Reproduced from Featherstone1
with permission of the publisher. Copyright © 1999, Munksgeard.)
8
7
6
5
4
3
2
1
00 5 10 15 20 25 30
TIME (MINUTES)
Subjects withnormal salivary flow
who ingestedsucrose
Subjects withxerostomia
who ingestedsucrose
Subjectswho ingesteda sugar-free
sweetened product
pH
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JADA, Vol. 131, July 2000 891
ed apatite (enamel mineral)crystals and thus acts as apotent protection mechanismagainst acid dissolution of thecrystal surface in the tooth'ssubsurface region. If fluoride isin the plaque fluid at the timethat the bacteria generate acid,it will travel with the acid intothe subsurface of the tooth and,therefore, adsorb to the crystalsurface and protect it againstbeing dissolved.
In summary, fluoride presentin the water phase at low levelsamong the enamel or dentincrystals adsorbs to these crystalsurfaces and can markedlyinhibit dissolution of tooth min-eral by acid.21,36 Fluoride thatacts in this way comes from theplaque fluid via topical sourcessuch as drinking water andfluoride products. Fluorideincorporated during toothdevelopment is insufficient toplay a significant role in cariesprotection. Fluoride is neededregularly throughout life to pro-tect teeth against caries.
Enhancing remineraliza-tion. As the saliva flows overthe plaque and its componentsneutralize the acid, raising thepH (Figure 2), demineralizationis stopped and reversed. Thesaliva is supersaturated withcalcium and phosphate, whichcan drive mineral back into thetooth.21,39 The partially deminer-alized crystal surfaces withinthe lesion act as “nucleators,”and new surfaces grow on thecrystals (Figure 3). Theseprocesses constitute remineral-ization—the replacement ofmineral in the partially de-mineralized regions of the cari-ous lesion of enamel or dentin(including the tooth root).20,21
Fluoride enhances remineral-ization by adsorbing to the crys-tal surface and attracting calci-
um ions, followed by phosphateions, leading to new mineralformation. The newly formed“veneer” excludes carbonateand has a composition some-
where between HAP and FAPas described above (Figure 4).FAP contains approximately30,000 ppm F and has a verylow solubility in acid. The new
Figure 3. High-resolution electron microscope images (magnificationapproximately x2,000,000) of individual enamel crystals that visualizeremineralization at the atomic level. The black lines are rows of calci-um atoms, which are visualized by this technique. A. Normal enamelcrystal dissected from the inner region of enamel, showing “small”white patches of calcium-deficient, carbonate-rich regions. B. Crystalon which a “remineralized” surface veneer has been grown after treat-ment with fluoride, calcium and phosphate. (Adapted fromFeatherstone and colleagues, 1981.30)
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892 JADA, Vol. 131, July 2000
remineralized crystal now willbehave like low-solubility FAPrather than the highly solubleCAP of the original crystalsurface.36
In summary, fluoride in solu-tion from topical sources en-hances remineralization byspeeding up the growth of anew surface on the partiallydemineralized subsurface crys-tals in the caries lesion. Thenew crystal surface veneer isFAP-like, with much lower sol-
ubility than the original CAPtooth mineral. Subsequent acidchallenges must be quite strongand prolonged to dissolve theremineralized enamel.
Saliva and caries. Saliva hasa critical role in the preventionor reversal of the caries process;it provides calcium, phosphate,proteins that maintain super-saturation of calcium in theplaque fluid, proteins and lipidsthat form a protective pellicleon the surface of the tooth, anti-
bacterial substances andbuffers.40 The saliva compo-nents neutralize the acids pro-duced by bacterial metabolismin the plaque, raise the pH andreverse the diffusion gradientfor calcium and phosphate.Thereby, they return calciumand phosphate to the subsur-face lesion, where these ionscan regrow new surfaces on thecrystal remnants that were pro-duced by demineralization.These so-called “remineralized”crystals have a veneer of muchless soluble mineral. Saliva alsoclears carbohydrates and acidsfrom the plaque.
In the case of salivary dys-function,41 all of the above bene-fits of saliva are reduced oreliminated (as is illustratedpartially in Figure 2 by the pHprofile of the subjects withxerostomia).
THE CARIES BALANCE
Fluoride’s three extensivelystudied and documented princi-pal mechanisms of action relyon the presence of fluoride insaliva, in the plaque at thetooth surface and in the fluidamong the crystals in the sub-surface of the enamel or dentin.The clinical effects of fluoride,therefore, can be optimized byusing delivery methods thatbring fluoride to the surface ofthe tooth and into the plaquerather than incorporating fluo-ride into the tooth mineral crys-tals during tooth development.These topical delivery methodsare equally applicable to adultsand children and include fluo-ride in beverages and foods,dental products and drinkingwater. The benefits of continu-ally providing low levels of fluo-ride in the saliva and plaquefrom the aforementioned topicalsources are described more fully
Enamel crystal =carbonated apatite
ACIDPartly dissolved
crystal
Remineralization
Ca10(PO4)6 (F)2 =fluorapatitelike
coating on crystals Crystalnucleus
Calcium +phospate+ fluoride
Protective Factors
Salivary flow and componentsProteins, antibacterial componentsand agentsFluoride, calcium and phosphateDietary components: protective
Pathological Factors
Reduced salivary functionBacteria: mutans streptococci, lactobacilliDietary components: frequency carbohydrates
NO CARIES CARIES
Figure 4. Schematic representation of demineralizetion followed byremineralization in the caries process. if remineralization is successful,the final result is a crystal with a surface veneer of “fluorapatitelike”mineral of low solubility. (Reproduced from Featherstone1 with permis-sion of the publisher. Copyright ©1999, Munksgaard.)
Figure 5. The caries balance: a schematic diagram of the balancebetween pathological and protective factors in the caries process.(Reproduced from Featherstone1 with permission of the publisher.Copyright ©1999, Munksgaard.)
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JADA, Vol. 131, July 2000 893
in a recent review article.1
Pathological and protec-tive factors in the caries bal-ance. Caries progression, asopposed to reversal, consists ofa delicate balance between theaforementioned factors—name-ly, a bacterially generated acidchallenge and a combination ofdemineralization inhibition andreversal by remineralization.l,42
The balance between pathologi-cal factors (such as bacteria andcarbohydrates) and protectivefactors (such as saliva, calcium,phosphate and fluoride) is adelicate one that swings eitherway several times daily in mostpeople (Figure 5).
Protective factors. Saliva isessential for the protection ofthe tooth against dental cariesand provides many natural pro-tective factors summarized ear-lier,40,41 including calcium, phos-phate, antibacterial componentsand other proteins with variousfunctions. Extrinsic antibacteri-al agents such as chlorhexidinealso can be considered as pro-tective factors in this balance,as can fluoride from externalsources. The mechanisms ofaction of fluoride described inthis article apply primarily tofluoride from topical sources;systemically incorporated fluo-ride has only a minor role inprotecting against dental caries.This conclusion is supported notonly by laboratory data asdescribed previously, but alsoby epidemiologic studies. Forexample, a four-year study inEngland found a 27 percentlower caries incidence amongchildren who were 12 years oldwhen water fluoridation beganin their communities, relativeto the incidence in control sub-jects of the same age in nonfluo-ridated areas.43 This was a well-conducted study, and it clearly
showed the posteruptive (topi-cal) effects of fluoride in thedrinking water. Other studieshave illustrated the weak pre-eruptive effects of fluoride. Forexample, in two groups ofOkinawa nursing students aged18 to 22 years, there was no dif-ference in caries status betweenthose who had received fluori-dated water only until about 5to 8 years of age (and nonethereafter) and those who hadnever received fluoridateddrinking water.44
The cariostatic effects of fluo-ride are, in part, related to thesustained presence of low con-centrations of ionic fluoride inthe oral environment,l,21,38
derived from foods and bever-ages, drinking water and fluo-ride-containing dental productssuch as toothpaste. Prolongedand slightly elevated low con-centrations of fluoride in thesaliva and plaque fluid decreasethe rate of enamel demineral-ization and enhance the rate ofremineralization.21,36,38,45-48 Forexample, fluoride at 0.04 ppmin saliva can enhance reminer-alization. Remineralization ofearly lesions also requires calci-
um and phosphate, which arederived primarily from salivaand plaque fluid.
Pathological factors. Patho-logical factors obviously includecariogenic bacteria and the fre-quency of ingestion of ferment-able carbohydrates that sustainthese bacteria. The importanceof mutans streptococci (whichincludes S. mutans and S.sobrinus) in the development ofdental caries has been reviewedextensively.12,14,15,49,50 Numerouscross-sectional studies inhumans have shown that great-er numbers of mutans strep-tococci and lactobacilli in salivaor plaque are associated withhigh caries rates.15,25,49,51-54
Longitudinal studies haveshown that an increase overtime in numbers of both ofthese bacterial groups isassociated with caries onsetand progression.24,55,56
CARIES INTERVENTION
The methods of caries interven-tion can be summarized by join-ing the principal components ofthe caries process with theinterventional possibilities(Table).
Cariogenic bacteria andhigh bacterial challenge.Dental caries is a transmissible,bacterially generated disease.There is the mistaken beliefthat drilling out a caries lesionand placing a restoration elimi-nates the bacteria and therebystops caries progression. Al-though traditional restorativework may eliminate the bacte-ria at the site of the restoration,the remainder of the mouth isleft untouched, caries continuesunchecked in the remainder ofthe mouth and recolonizationcommences rapidly at themargins.57
It is logical, therefore, to use
There is a mistaken belief that drilling out a caries lesion and placing arestoration
eliminates the bacteria and thereby stops
caries progression.
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894 JADA, Vol. 131, July 2000
antibacterial therapy—such astreatment with chlorhexidinegluconate rinse—as a caries-preventive measure. Althoughthis has been proposed formany years58-60 and used in sev-eral European countries, anantibacterial approach almostnever is used in the UnitedStates for the prevention of theprogression of dental caries.
One of the difficulties in per-suading clinicians to use theantibacterial approach is thatthere have not been rapid andaccurate methods of determin-ing the levels of cariogenic bac-teria in the mouth. Further-more, although numerousstudies have indicated thatmutans streptococci and lacto-bacilli definitely are risk factorsfor dental caries, there is no
one-to-one direct correlationbetween levels of these bacteriaand caries progression.24,49
However, it now is well-estab-lished that high levels ofmutans streptococci, high levelsof lactobacilli or both constitutea “high bacterial challenge.”24
This bacterial challenge can bebalanced by the protective fac-tors described earlier, whichinclude salivary components—especially calcium, phosphateand fluoride—and the amountof saliva present.42
Figure 5 illustrates the bal-ance between pathological fac-tors (including cariogenic bacte-ria, reduced salivary functionand frequency of use of fer-mentable carbohydrates) andprotective factors. If thesepathological and protective fac-
tors are in balance, caries doesnot progress. If they are out ofbalance, caries either progressesor reverses.
Antibacterial therapy forcaries control. Currently, themost successful antibacterialtherapy against cariogenic bac-teria is treatment by chlorhexi-dine gluconate rinse or gel.47,61
Chlorhexidine is available byprescription in the UnitedStates. Studies have shown thata daily dose of chlorhexidinerinse for two weeks canmarkedly reduce the cariogenicbacteria in the mouth and that,as a result, recolonization takesplace in three to six monthsrather than immediately.58 Inpatients with high levels of bac-teria, therefore, chlorhexidinetreatments at three-month
SUMMARY: THE CARIES PROCESS AND METHODS OF CARIES INTERVENTION.
CARIES COMPONENT INTERVENTION METHOD
Bacteria Antibacterial therapy such as treatment with chlorhexidine gluconate (see text.)
Carbonated Hydroxyapatite Make the mineral less soluble by transforming it to other crystalline forms such as hydroxy-apatite without carbonate (future caries-preventative treatments by specific laser irradia-tion will enable this to be done69,70)
Fermentable Carbohydrates Reduce the frequency of ingestion; substitute with noncariogenic sweeteners (this method is well-accepted and used in patient education.
Recommend use of sugar-free chewing gum, which reduces frequency of fermentable carbo-hydrate ingestion and also enhances remineral-ization
Organic Acids Produced by Neutralize the acid by providing extra buffer-Oral Bacteria ing or enhancing saliva; sugar-free gum assists
in this as well
Saliva Enhance the saliva flow and function
Fluoride Exploit its known effects on bacteria, inhibi-tion of demineralization and enhancement ofremineralization by using “topical” fluoridedelivery by means of dental products, drinkingwater, beverages and foods
TABLE
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JADA, Vol. 131, July 2000 895
intervals are indicated.The problem faced by clini-
cians is how to determine, in atimely fashion, whether thebacterial challenge is high,medium or low. For manyyears, commercial “dip slides”have been available in Europe,and they recently becameavailable in the UnitedStates.58 A saliva sample istaken from the patient andincubated on the dip slide; twodays later, a result is providedof the levels of S. mutans andlactobacilli bacteria in themouth.58 Although these slidesare a major advance in conven-ience and are the best toolsavailable at the time of thiswriting, it has been shownthat this technology is notwell-correlated with tradition-al bacterial plating. It is antic-ipated that methods of rapidchairside assessment of bacter-ial challenge, based on molecu-lar biology, will be available inthe future.
Several investigators haveexplored the possibility ofusing modern molecular biolo-gy for better and more rapidmethods of bacterial assess-ment,62 but they were unableto overcome a number of com-plications. An exciting devel-opment is work by Shi and col-leagues,63 who recently pub-lished a method using species-specific monoclonal antibodiesthat recognize the surface ofcariogenic bacteria. With thistechnology, it is not necessaryto split open the bacterial cellsto assess the internal DNA orRNA. These probes can betagged either with a fluo-rescent molecule or with amarker that can be measuredquantitatively in a simplespectrophotometer.
It is anticipated that these
probes will be available com-mercially in the near future,and that clinicians will be ableto use them chairside andobtain results within a fewminutes. This will enable clini-cians to determine the quanti-tative levels of bacteria in apatient’s mouth while he orshe is in the operatory and tofactor these numbers into anoverall risk assessment ofcaries for that patient. It isenvisaged that computer pro-grams will be available thatwill include the assay num-bers, as well as other data.The practitioner will receiveguidance as to the level of
caries risk and what regimenor regimens to use to preventfurther caries and to reducethe bacterial challenge. Withthe new monoclonal antibodyprobes, the levels of bacteriaand success of the interventioncould readily be followed overtime. This is an exciting, inno-vative tool that may becomewidely used and acceptedwithin a few years.
CARIES RISKASSESSMENT
Several studies have attempt-ed to determine risk factorsthat can be reliably used to
assess the level of risk ofcaries progression in individ-ual patients. Studies still areunder way, and there is nodefinitive formula yet avail-able. The status of risk assess-ment was summarized, how-ever, by the authors of a spe-cial supplement to TheJournal of the AmericanDental Association in 1995;this publication can be used asa guide until more definitiveinformation is available.64
Figure 5 represents a basis fordetermining caries risk withthe information currentlyavailable.
It has been established thathigh-risk patients includethose who have a high bacteri-al challenge, which may con-sist of a combination of highnumbers of mutans streptococ-ci, lactobacilli or both.Although fluoride has excel-lent properties in terms of bal-ancing caries challenge, if thechallenge is too high, thenfluoride—even at increasedconcentrations, with increaseduse or both—cannot balancethat challenge. Therefore, inthe case of high bacterial chal-lenge, the bacterial infectionmust be dealt with, typicallywith a chlorhexidine rinse, aswell as the enhancement ofsalivary action by topicaldelivery of fluoride. Theseprinciples apply equally wellto adults and children.Accurate detection of earlycaries can increase the relia-bility of caries risk assess-ment, particularly if thosemeasurements are made atthree- or six-month intervalsand caries progression can bemeasured. In the case of cariesprogression, obviously, inter-vention is needed either anti-bacterially, with fluoride or
Methods ofrapid chairsideassessment of
bacterialchallenge, based
on molecularbiology, will beavailable in the
future.
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896 JADA, Vol. 131, July 2000
with other techniques, some ofwhich are described in the fol-lowing material.
Caries management byrisk assessment. As thecaries risk assessmentmethodologies are refined, wewill have more definitive bio-logical and chemical riskassessment measures to guideclinical decision making.These measures form thebasis for assessing the direc-tion in which the caries bal-ance is likely to move for aparticular patient. Earlycaries detection, especially inocclusal surfaces, is an essen-tial part of caries managementby risk assessment.
Caries management by riskassessment now is receivingconsiderable attention, andsoftware programs are beingdeveloped that will aid practi-tioners in assessing risk andlead them to the use of cur-rent and new technologies byspecifying treatments recom-mended for the various riskcategories.59,60 As we move intothe future, tooth restorations
will become less and lessdesirable as a treatment andwill be used only as a finalresort when new interventionmeasures have failed or whenpeople have not participatedin caries intervention pro-grams such as those indicatedpreviously.
CARIES MANAGEMENTTOOLS FOR THE FUTURE
Several technological advance-ments are currently close toclinical reality and will beembraced if they are provensuccessful.
Assessment of bacterialchallenge by chairsidemolecular probes. The useof chairside bacterial probesfor assessing a patient’s cario-genic bacterial challenge willbe an essential component ofcaries management by riskassessment.
Caries immunization. Ina program of caries manage-ment by risk assessment, it islogical that all available toolsshould be used. One such toolthat has been investigated for
many years is an immuniza-tion against caries. There aremany obstacles to the successof immunization, as caries isnot a systemic infection thatcan be dealt with simply byadministering a specific anti-biotic. The infection must bedealt with in the mouth, wherethe internal body fluids do notpass and, therefore, the normalimmune response is not rele-vant. However, IgA that is pro-duced by the saliva naturallycan interfere with the coloniza-tion of the surface of the toothby specific bacteria.
Recent studies by Ma andcolleagues65,66 have illustratedthe effectiveness of specific IgAin the inhibition of recoloniza-tion of mutans streptococci.The next logical step is to usethis technology as one of thetools for caries intervention. Itis possible to use geneticallyengineered plants, such astobacco or alfalfa, to produceimmunoglobulins.66,67 A study isin progress at the University ofCalifornia, San Francisco, totest IgA that has been pro-duced using genetically engi-neered tobacco plants. At presstime, the results were notknown, but if the trial is suc-cessful, this IgA can be appliedto the teeth after chlorhexidinetreatment has removed the car-iogenic bacteria, with the aimof inhibiting future recoloniza-tion by mutans streptococci.
Early caries detectionand intervention. Successfuluse of the innovative methodsdescribed here for caries inter-vention will require accuratemethods for the early detectionof dental caries in enameland dentin. Early-detectionmethods such as fluorescence,optical coherence tomography,electrical impedance and
Pulp
Dentin
Enamel
Pulsed laser light with highabsorption coefficient
Removes carious tissue;minimal heat deposition
Walls of preparation heatedto 800-900 C
Heat conduction
Pulp temperature rise < 4 C
Fiqure 6. Schemaffc diagram showing the potenffal use of specificlasers for precise removal of carious enamel and modification of thesurrounding enamel for prevention of further caries progression afterrestoration. The laser would be set first to remove a minimum of cari-ous tissue. Then the walls and base of the cavity preparation would betreated with the laser to inhibit subsequent caries progression.(Reproduced from Featherstone71 with the permission of the publisher.Copyright ©2000 Indiana University School of Dentistry.)
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ultrasonography are likely tobecome available for use by cli-nicians in the near future.68 Itwill be possible to detectlesions in the occlusal surfaceand to determine whether theyhave progressed into the dentinand, if so, how far. This is notpossible with current radio-graphic technology.
Once new methods are intro-duced for the early detection ofcaries, they can be used in twoopposing fashions. Clinicianswith traditional training arelikely to use these methods tointervene physically at an ear-lier stage with cariouslesions—drilling, filling andplacing restorations. This out-come is of concern, as manymore restorations would beplaced than may be necessary,which weakens the tooth struc-ture. Early detection and inter-vention by placing a restorationalso does not take advantage ofthe body's natural protectivemechanisms of inhibition ofdemineralization and enhance-ment of remineralization viasaliva.
Alternatively, early detectionof caries can be used as anopportunity to promote re-mineralization via salivaryenhancement, use of topicalfluoride and chlorhexidine andmeticulous oral hygiene. Inaddition, as innovative meth-ods for early caries interven-tion are introduced, the needfor restorations may be elimi-nated for many patients, there-by preserving the tooth struc-ture and halting or reversingprogression of dental caries.
Caries prevention bylaser treatment. In May 1997,the U.S. Food and DrugAdministration approved theuse of an erbium:yttrium-aluminum-garnet, or Er:YAG,
laser for use on teeth. This wasthe first approval for laser useon dental hard tissues. Thisapproval by the FDA was forthis particular laser to be usedfor the removal of dental cariesand the cutting of sound tissuebefore the placement of restora-tions. This event has usheredin a new era for lasers in den-tistry. Since then, other lasershave been approved for thesame purpose, and additionalhard-tissue uses are likely tobe approved in the future,including the use of lasers forthe inhibition of progression ofdental caries by altering thecomposition of surface enamel
or dentin mineral.Kantorowitz and colleagues69
and Featherstone and col-leagues70 have studied theeffects of lasers on hard tissuesfor almost 20 years. The overallobjective of these studies is toestablish the scientific basis forthe choice of laser parametersthat can be used clinically forthe prevention, removal ortreatment of caries lesions.Their studies have demonstrat-ed that specific pulsed carbondioxide, or CO2, laser treat-ment of dental enamel caninhibit subsequent carieslikeprogression in a severe de-
mineralization-remineraliza-tion model in the laboratory byup to 85 percent. They havedemonstrated that carbonate islost from the CAP mineral ofthe tooth during specific laserirradiation, making the miner-al highly resistant to dissolu-tion by acid. Although theyhave demonstrated in the labo-ratory, using pH cycling mod-els, that as little as 20 pulses of100 microseconds each can pro-duce a preventive effect similarto daily use of fluoride denti-frice, these promising andexciting results have not yetbeen tested in human mouths.70
For practical purposes, itwould be desirable to develop alaser that can remove carioustissue and subsequently beused to treat the walls of thearea from which carious tissueis removed to make themresistant to subsequent carieschallenge71 (Figure 6). Friedand colleagues72 recently pub-lished a report on a new CO2
laser that efficiently removescarious tissue. After caries anda minimal amount of surround-ing tissue are removed, it willbe possible to change the laserparameters to perform caries-preventive treatment on thesame area. This would be fol-lowed by placement of a resin-based composite restoration,thereby inhibiting subsequentcaries around that restoration.For example, if an early oc-clusal lesion was detected (bythe new methods described pre-viously) that was deemed to bebeyond hope of remineraliza-tion, this lesion could be con-servatively removed with anappropriate laser. Then thesurrounding cavity preparationwalls could be treated for cariesprevention by the laser and asmall conservative restoration
As innovativemethods forearly cariesintervention
are introduced,the need for
restorations maybe eliminated formany patients.
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898 JADA, Vol. 131, July 2000
placed. The cavity walls will behighly resistant to acid attackand therefore resistant to sec-ondary caries. Providing bacter-ial intervention via chlorhexi-dine rinse was also part of thetreatment in the same patient,future caries would be unlikely.
SUMMARY ANDCONCLUSIONS
The mechanism of dental cariesis well-established to the pointwhere new approaches arebeing made for caries preven-tion based on a scientific under-standing of the processesinvolved. Several existingmethodologies are available toenable successful managementof dental caries by risk assess-ment. Understanding the bal-ance between pathological fac-tors and protective factors isthe key. Beyond the well-established and currently usedmethods, some innovative andexciting techniques have shownearly research successes thatmost likely will be used forearly caries intervention in thefuture. These methods includefluoride therapy for inhibition ofdemineralization and enhance-ment of remineralization, mole-cular probes for the quantita-tive detection of cariogenic bac-teria at chairside, computerizedcaries risk assessment pro-grams, genetically engineeredIgA for inhibition of recoloniza-tion of cariogenic bacteria, spe-cific lasers for conservativeremoval of carious tissue andspecific lasers for the preven-tion of caries progression.
The use of these technologieswill require extensive retrainingof clinical dentists. But it willdramatically alter the way inwhich dentists diagnose, inter-vene, treat and manage caries,with major benefits to the oral
health of their patients. �
Dr. Featherstone is a professor and thechair, Department of Preventive andRestorative Dental Sciences and Departmentof Dental Public Health and Hygiene,University of California, San Francisco, 707Parnassus Ave., Box 0758, San Francisco,Calif. 94143, e-mail “[email protected]”.Address reprint requests to Dr.Featherstone.
The author sincerely acknowledges contri-butions from numerous colleagues over manyyears to much of the work reviewed here.
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