Pulp-dentin biology in restorative dentistry.

Part 4: Dentai cariesCiiaracteristics of iesions and puipai reactions

Lars Bjrndal, DDS, PhDVIvar A, Mjr, BSD, MSD, MD, DrOdont^
The infectious disease dental caries resuifs in lesions thai may affect enamel, dentin, puip, and cementum. If a caries lesion has progressed to the stage at which it requires restorative intervention, it is important that the ciinician understand the tissue changes in the dentin that are iikeiy to have taken place during lesion development. Until the present, no major distinction between the restorative treatment of active (rapldiy progressing] and arrested (slowly progressing) lesions has been made, despite the faot that the two conditions exhibit major differences in tissue changes in the puip-dentin complex. Intralubuiar changes and tertiary dentin formation will affect the outcome of the restorative treatment. In unaffected dentir and in rapidly progressing lesions, permeabie tubules persist, and when the preparation of carious teeth results in the opening of unaffected dentin, greater care must be taken in ali phases of the restorative procedures than if the dentin is impermeable. An active, deep iesion can be changed to an arrested lesion by a two-step excavation approach. Optimal assessment ot the prevailing ciinical conditions can only be made on the basis of thorough knowledge of the biology of the pulp-dentin organ. (Quintessence Int 2001:32:

717-736)
Key words: caries lesion, demineralization, dentin, enamel, odontoblasts, pulp, remineraiization, stepwise excavation, tertiary dentin

he infectious disease dental caries results in lesions that affect enamel, dentin, and pulp, and cementum if the root portion of the tooth is involved. These lesions will be referred to as caries lesions. They are characterized by demineralization of the hard tissues of the tooth, accompanied by tissue changes in the affected primary dentin and inflammatory reactions in the puip. ITie reasons for dental restorative treatments differ, and it is important to be aware of the actual cause for each individual treatment. When preventive, nonoperative treatment fails, restorative treatment of dental caries is needed to remove necrotic and infected demineralized dentin to arrest further progression. Removal of tissue usually also involves enamel and dentin that have not been affected by caries. Thus, routine restorative procedures are performed partly in

'Associate Professor, Department of Cafiology and Endodontics, School of Dentistry, Faculty of Health Sciences, Unrversity of Copenhagen, Copenhagen, Denmark. 'Protessor, Academy 100 Eminent Scholar, Department of Operative Dentistry, University of Florida, College ot Dentistry, Gainesuille, Florida; NIOM, Scandinavian institute ct Dental Matenais, Hasium, Non^ay. Reprint r e q u e s t s : Dr Lars Bjarndai, Depaitmenf ot Cariology and Endodontics, Facuity of Health Sciences, Nerre All 20, DK-2200 Copenhagen N, Denmark. This is one ot seven articles in a series emphasizing a blologio approach to restorative dentistry through an understanding of file pulp-dentin compiex.

sound, unaffected dentin. Intact teeth may likewise he used as abutment teeth for fixed partial dentures. Furthermore, restorations are frequently replaced because of failure and sometimes because of cosmetic demands made by the patient.' The conditions for restorative therapy are, therefore, quite different from tooth to tooth, not only as a result of variable pathoses and associated tissue changes, including age-related changes, but also because of variations in the size and activity of the individual caries lesion. To optimize the profession's understanding of these differences, the present review will focus on the gradual development from early enamel lesions to deep dentin involvement and the associated ptilpal reactions. The development of caries lesions is not a one-way process of demineralization, but an intermittent course of demineralization interspersed with mineral uptake or remineraliiation,^'^ The key factor in the development of caries lesions is the presence of microbial, acid-producing plaque on the surface of tbe tooth. The metabolism of the plaque varies depending on many factors, including dietary intake and oral hygiene, which explains the cycle of demineralization and remineraiization. A progressing lesion is referred to as an active lesion. In the enamel, it has a dull, white, opaque appearance (Pig 1). In the dentin, a soft, yellowish or light to dark brown discoloration of the demineralized tissue prevails (Fig 2). 717

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Fig 1 Active primary enamei iesion represented by a wbiie, auii mesiai surface on a mandibular first moiar The lesion has been made isible tollowing exfoiiation of tbe primary second molar

Fig 2 Yeilow emineraiized denlin in an aoliue, progressing iesion, made visible iolioming the removai of undermined enamel in the maxiiiary lirst premolar. No denlin has yet been excavated, and a gentle touch with an explorer reveis penetration and ioosening of a fragment of demineraiized tissue

Fig 3 Arrested approximai iesion on a mandibular molar with cavitation iocated in the enamel. Tine surfaoe is shiny and discolored. The adjacent tootii has been extracted; the resuitant change in the cariogenic environmenf has allowed the lesion to become arrested.

Fig 4 Exposed, siowiy progressing iesion in a maxiilary premolar The demineraiized dentin has a dark appearance. The adjacent tooth has been extracted, causing a change in the cariogenic environment. As a result, the iesion has become inactivated or arrested.

Fig 5 Secondary caries in a second moiar. deveioping gingivaiiy adjacent fo fhe resforation. Apart from its location, it is basicaily similar to a primary lesion.

The process may be permanently stalled under favorable conditions, a condition referred to as arrested caries. Depending on the extent of the injury produced by the caries, arrested lesions will have a varied appearance, ranging from a shiny, white, opaque or discolored spot in the enamel (Fig 3) to a hard, dark dentinal surface exposed to the oral environment (Fig 4), Different types of caries lesions have heen described; primary, secondary (rcurrent), and remaining lesions. This article will focus on primary lesions. Coronal caries starts on intact tooth surfaces, and the early enamei lesion will be described to the extent required to understand the reactions in the dentin and pulp. Secondary lesions, often referred to as secondary caries, develop adjacent to restorations. Apart from their location at the margin of restorations (Fig 5),
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Bjarndai/Mjr Fig 6 (Lett) Ground section of a subsurface enamei iesion viewed in poiarized iight after it has been imbibed in mater. The thickness ol tine sudace zone is greater in [he central part of (he iesion than in the peripheral par!. (Original mag nil i cat ion x30.) Fig 7 (Rigi^t) Microradiograph of an undemineraiized section ot a tooth through a root surlace canes lsion. The subsurface lesion phenomenon is shown in cementum. Note the increased mineraiization in the dentin subjacent to the iesion. {Original magnification x3.)

they are basically similar to primary lesions^'^ and will not be discussed separately in this article. Remaining caries represents part of the caries lesion left behind in the preparation or at the enamel margin of a preparation when a restoration is placed.
PRIMARY ENAMEL LESIONS

The classic description of the morphogenesis of the primary enamel lesions starts with the so-called white-spot lesion, defined as the first macroscopic sign of caries-induced demineralization^ (Fig 1). When a white-spot lesion is viewed histologically, an apparently well-mineralized surface zone is seen overlying a subsurface demineralization. All initial caries lesions characteristically progress as subsurface lesions, irrespective of whether they begin in enamel (Fig 6), experimentally exposed coronal dentin,' or cementum. A microradiograph of a root surface lesion developing as a subsurface process is sbown in More than 50 years ago, the mterpretation of the enamel subsurface phenomenon centered around evidence for a stronger and more resistant composition of the surface enamel.^-i^ Later in vitro studies'^ described the formation and maintenance of an apparently well-mineralized intact surface layer as an integral part of the remineralization of the enamel, including possible "repair" processes.'^ However, controversial information has been publisbed over the years concerning the nature of the surface layer and
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the subsurface lesion. Scanning electron microscopy has shown that the surface layer is not intact but has a surface dissolution pattern with widened intercrystalline spaces, which explains the dull clinical appearance of active lesions.'6 Moreover, arrested lesions show no specific evidence of reprecipitated "repair" crystals in the surface layer.'' On the other hand, signs of wear may be noted, which explains the shiny surface found on some arrested enamel lesions. Because the chemical dynamics of the development of natural enamel lesions involve ongoing sequences of mineral dissolution and uptake, remineralization becomes an integral component in the understanding of the structural characteristics of the caries lesion. Eurthermore, it is important to understand that the remineralization cannot act as an isolated repair mechanism. Mineral uptake from saliva, including additional fluoride from enamel or topically applied fluoride, is a contributing factor in tbe development of tbe structural appearance of the lesion. Although the composition of surface enamel is somewhat different from that of the subjacent enamel, including a relatively bigb fluoride content, it is important to note that, if the surfaee enamel is removed, a subsurface lesion will still develop.'^''^ Thus, the special characteristics of surface enamel are properties acquired as a result of exposure to the oral environment. The organic pellicle, about 1 pm thick, covers all intraoral surfaces, including the hard tissues. It plays a significant role in the development of subsurface lesions. The pellicle is the substrate on whicb bacteria will attach and form plaque. If the pellicle is removed, 719

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eg, by polishing witb pumice or by grinding, it will start to re-form quickly in vivo (in minutes rather tban hours) because of adsorption of proteins from the saliva. However, because subsurface lesions can be induced in vitro,i'''2 tbe presence of a peilicle is not essential for tbeir development. Mueb researcb bas been done on artificially initiated lesions, especially in relation to factors that affect the remineralization of lesions. An intraoral cariogenicity test using hovine enamel bas also been developed.^' Tbe artificially induced lesions do simulate the subsurface characteristics of enamel lesions, but tbese lesions are demineralizations and not true caries lesions. Tbe clinical relevance of tbe results obtained must, tberefore, be interpreted cautiously. A series of bistologic and ultrastructural cbanges occur in vivo during tbe initiation of active enamel caries lesions before tbe well-recognized signs of a wbite-spot lesion can be discerned.22 Tbere is a close relationsbip between tbe activity of a time-controlled microbial, acid-producing plaque and tbe degree of demineralization. As the demineralization deepens, the area of the surface zone also increases. Similarly, quantitative analysis of natural approximal lesions^^ shows that the greatest degree of tissue porosity always follows the direction of the enamel rods from the deepest point of penetration to the surface. Measurements of the thickness of tbe surface zone indicate that it increases with lesion progression. The thickness of the central part of the surface zone is typically greater than that observed in tbe peripberal part of the same lesion, indicating that the surface zone and the subsurface demineralization are closely correlated to each other (see Fig 6). The early caries lesion on approximal surfaces takes on a conical sbape, wbich projects into a triangular shape in a two-dimensional ground section wben viewed in reflected light (Fig 8). If allowed to progress, the lesion will reach the dentinoenamel junction [Fig 9) and continue into the dentin (Fig 10}. In all areas, the lesion advanees in a direction parallel to the enamel rods, and the depth of demineralization will vary depending on the time each rod has been subjected to tbe caries attack." Although tbe lesion evolves as a unit. Its particular shape may be best understood if eacb enamei rod is envisioned as developing individually, as a "minilesion.''^" The oldest, deepest part is located in the center and the youngest, shallowest part is at the periphery. In tbis way, the conical sbape of the enamel lesion is estahlished. The practical implication of this pattern of development is that the peripheral extent of tbe subsurface enamel lesion always represents the total area of the lesion throughout the thickness of the enamel.
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However, the depth of demineralization for each minilesion, ie, the individual rod lesion, is c'iffcitnt, so that the oldest, central part is the most ^idvanced. Thus, when projected along the enamel rod:., the total extent of the lesion is similar toward the dentinoenamel junetion as it is toward the outer imlace at any given time. However, the depth of deniineralization varies (Fig 10). Consequently, the effect on the dentin is less marked at the periphery than it is at the central part of the lesion. Tbe conical shape of the advancing enamel lesion is best illustrated on smooth surfaces, eg, on approximal surfaces just below tbe contact points wbere lesions usually start (Fig 8).^' Tbe anatomic configuration of tbe enamel on occlusal surfaces with tbe groove-fossa system, including pits and fissures, makes it somewhat difficult to follow tbe direction of the rods. Lesions also develop baek to back as it were, on the two walls of a groove, or at the entrance of a fissure.^^ As they advance and finally merge at the dentinoenamel junction, tbe actual origin on the surfaee is sometimes hard to establish. Thus, early occlusal lesions may be difficult to discern clinically, but tbey can be detected after careful cleaning and air drying of grooves and fissures, and tbey can be treated successfully witb noninvasive techniques.25,37

ENAMEL-DENTIN LESIONS

Reviews of the histopatbology of carles have typically focused on either early stages in the enamel^ or advanced lesions witb bacterial invasion and destruction of dentin.2s Clinically, tbe terms enamel caries and dentinal caries bave been interpreted as two independent entities. However, effects on dentin may already be seen at early stages of enamel lesions (Fig 8), prior to surface breakdown and bacterial invasion. Histoiogic evidence shows that the first alteration in dentin is a hypermineralized zone that develops even before tbe enamel lesion reaches the dentinoenamel junction.25.M Subsequent demineralization of tbe dentin is initiated when the enamel lesion reacbes the dentinoenamel juncfion. It appears tbat tbe initial demineralization never takes place in sound dentin but is actually a demineralization of affected bypermineralized tissue and corresponds to the deepest part of tbe enamel rods affected by the caries, ie, tbose along the central part of the lesion (Fig 9), As the lesion progresses, the involvement of dentin becomes greater (Figs 10 and 11), The dentin demineralization and the dentin hypermineralization never exeeed the area corresponding to the limits of tbe outer enamel lesion; ie, they do not spread beyond the enamel rods affected by the caries
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B0rndal/Mjor Figs 8 to 11 Ground sections through the central part ot tour progressive stages ol approximai enamei iesions i'lewed in reliected iigiit (Originai magmtication y2 5.)

Fig 8 Note the trianguiar shape ot the enamei lesion before il oontacts ttie dentinoenamei junction and ttie subjacent initial hypermineralizaticn ct the dentin.

Fig 9 When ttie enamel lesion oontacts the aftected dentin, more pronounced dentin changes are fcund. but they are limiled in extent to those in the enamel lesion.

Fig 10 As Ihe lesion progresses further, the extent of the dentinal lesion corresponds to that of the peripheral enamel lesion.

Fig 11 When enamei cavitation oocurs, similar relationships prevail between the extent of the enamei iesion and the subjacent reaoticns in dentin The extent of the dark brownish discoloration of the demineraiizcd dentin is limited to the surtace area of enamei rods affected by the caries iesion.

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lesion. However, as indicated in the discussion of the development of the enamel lesion, not all rods are affected at the same time and, therefore, to the same extent. Thus, the reactions of dentin reflect the changes occurring in enamel, giving rise to two principal alterations in the dentin tissue; First, when demineralization involving groups of rod and inter-rod enamel approaches the inner third of the enamel and progresses toward the dentinoenamei unction, tnineral alterations can be detected intratubularly in the dentin. Second, when demineralization of enamel reaches the dentinoenamel junction, demineralization uf the dentin starts, and some of the dissolved minerals will reprecipitate following the pH-dependent gradients within the enamel lesion. In general, the youtigest part of the lesion is found peripherally, both in enamel and dentin. This particular reaction pattern has resulted in the notion that there is a laterai spread of caries lesions al the dentinoenamel junction, based largely on the clinical and radiographie appearance of approximal iesions. This concept of the spread of caries lesions is accentuated because the mantle dentin normally has a relatively lower degree of mineralization at the dentinoenamel junction than in the bulk of the coronal circumpulpal dentin.^f* However, at precavitated stages of caries, the lesions follow the hasic rules of dentinai permeability, demonstrating that the primary dentinai tubules are the most significant routes for solute diffusion through the dentin.^i The belief that caries lesions spread at the dentinoenamel junction has led to the conviction that cavity preparations must be completed beyond the extent of even preeavitated enamel lesions in order to eliminate undermined enamel prior to restoration, but the outer periphery of the enamel lesion actually determines the extent of the dentin lesion.'' No true "lateral spread" of the lesion occurs as it reaches the dentinoenamel junction, and consequently no sound enamel is undermined during precavitated stages of enamel lesion progression. Even eavitation restricted to the enamel shows the same type of enamel-dentin lesion appearance, in which there is no uncontrolled spreading pattern (see Fig 11). In addition, recent quantitative histologie evidence has shown that the progress of occiusal enamel lesions at the dentinoenamel junction is basically similar to that of lesions on flat surfaces,^Slowly progressing lesions In slowly progressing caries lesions, increased mineralization of the subjacent dentin is normal (see Fig 7). This is a typical reaction in primary dentin to a mild or moderate external stimuli of any sort. In addition to the increased mineral content of the primary
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, ^ ' ' tertiary dentinogenesis will take pl;"*^ subjacent to the affected dentin.^^ The structure of the tertiary dentin can be related to the activity of the lesion, in that the more active the lesion, the more irregular the structure of the tertiary dentin.^'' This variation in structure may also be related to reactionary and reparative variants of tertiary dentin,*" The initial changes in primary dentin involve secretion of the highly mineralized peritubular dentin that reduces the diameter of the tubules. This secretion takes place prior to dentinai demineralization, Intratubular mineral deposits within the demineralized dentin may also obturate the tubules. These deposits represent reprecipitations o some of the minerals dissolved by the acids that have caused the lesion to develop. They are significant defense mechanisms because they reduce the permeability of the dentin, which in turn reduces the opportunities for ingress of bacterial antigens and agents that may cause inflammatory reactions in the pulp.'"-'^ The permeability of dentin subjaeent to caries lesions in teeth from individuals 20 to 28 years of age was only 14% of that in unaffected dentin in individuals from the same age group."^ In the 45- to 69-year age group, all dentinai samples subjaeent to caries lesions were impermeable according to the methods used. Deposition of intratubular mineral crystals was shown in the affected dentin. Similar mineral deposits in the tubules subjacent to caries lesions in dentin have been shown to be composed of hydroxyapatite and whitoekite crystals.-*^ The positive effect of intratubular precipitation of mineral crystals as a defense mechanism must be emphasized. They are reprecipitated during sequences of varying pH gradients in the lesion. In slowly progressing lesions, these changes are pronounced because the demineralization is not aggressive. The intratubular crystals per se do not actually cause the arrest of the lesion. Instead they should be considered to be a consequence of the caries activity and a positive effect of preventive measures such as removal of the microbial, acid-producing plaque covering the lesion. The application of individually based preventive measures, including professional plaque removal, has shown that lesions can be successfully arrested,'^ if caries still develops under these conditions, slowly progressing lesions are the most common outcome in populations with an adequate exposure to fluoride,''^ eg, through the use of fluoridated toothpaste twice daily. If no additional preventive treatment is employed, lesions in permanent teeth may take 5 to 6 years to develop to a stage that requires removal of damaged tissues followed by the placement of restorations. These lesions tend to remain without clinical symptoms through most of their development.
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patients, were often not considered. These limitations in information make it difflcult to assess the data. A Rampant caries, coupled with inadequate oral hygiene summary of pulpal and dentinal reactions to caries, and inadequate exposure to fluoride, results in active based mainly on demineraiized sections from a large and rapidly progressing lesions, botb in enamel and number of teeth, has been published.^' dentin. Tbe dentinal reactions associated witb slowly It is difflcult, and somewbat clinically irrelevant, to progressing caries do not prevail to tbe same extent. base discussions of the caries-related histopathology of Breakdown of the affected enamel and dentin wiil the pulp on stained, demineraiized sections uniess deoccur in months, rather than years, and will result in tailed, chronologic knowledge of the changes in tbe changes in tbe odontohlast-predentin region, inciuding dentin and the rate of progression of the lesions has destruction of the odontohlasts and lack of formation been developed. of tertiary dentin. Despite all the uncontrolled factors in reports of The subjacent pulpal tissue will react to the transpulpal reactions to caries, some broad conclusions mission of microhial products through a permeable can he drawn; The pulp subjacent to deep caries ledentin hy releasing or activating mediators from polysions sbows tbe presence of cbronic inflammatory exmorphonuclear and mononuclear leuiiocytes, includudate, including lymphocytes, macrophages, and ing lymphocytes and macrophages or blood plasma. plasma cells.^w.^" Formation of tertiary dentin usually These reactions will initiate the complex inflammatory takes place on the pulpal aspect of the affected events leading to either reversible or irreversihle stages tubules. The localized increase in dentin thickness is of pulpitis, which may or may not he associated with often accompanied by a reduced odontoblastic layer sensitivity or pain. in the aflected area. If tbe odontoblasts are destroyed, tertiary dentin The depth of hacterial penetration into the dentin will form under favorable conditions. Tbis bard tissue, has been claimed to be decisive for the degree of inespecially that formed initially, is often atubular and flammatory reaction, and, whenever the bacteria reach may have cellular inclusions, deflned as fibrodentin'^ the tertiary dentin, severe pulpitis prevails."^"'^' The or interface dentin.-*'^ The healing process will be en- pulpal reactions are well delimited and localized to hanced if the cariogenic environment is removed or the aflected dentin. In tbis respect, histopathologically, altered, and the sequence may then be followed by the the pulpal lesions correspond to the houndaries of the differentiation of new, secondary odontoblast-like locally increased tissue fluid pressure associated with cells that lay down new tubular matrix, also defined as pulpal inflammation.^^ The importance of neurogenic reparative dentin.^" If, however, the lesion is allowed involvement in pulpal reactions to caries has also been to progress, the pulp may become infected and permademonstrated.^' Growth factors present in the deniin nently damaged, requiring endodontic treatment prior are also released during demineralization.S'' They may to restoration. be important in tbe initiation of defense mechanisms such as formation of tertiary dentin.^^ The onset of pulpal reactions to caries has been rePULPAL REACTIONS ported to occur early, but the phenomenon has been difficuft to study because the enamel is lost when tbe Extensive research has been published on pulpal reacsections are prepared for routine histopatbologic extions in teeth subjected to caries.^i-" Much emphasis amination of the dentin and pulp. The relationship to has been placed on the correlation of clinical sympthe lesion is then lost. The localization of noncavitated toms and the bistopathologic condition of tbe pulp to and cavitated approximai enamel lesions has been allow classification of the degree of pulpitis for use in studied in newly erupted teeth after grooves were pretreatment planning. No universally accepted classiflpared through the enamel into dentin in areas not afcation system has ever been establisbed, mainly fected by caries.52 This approach allowed location of because of marked variation in reactions noted but the site of the lesion and aided in estabhshing the dialso because of the varied interpretation of the rection of the histologie sectioning. The affected histopatbology. enamel with the lesion in situ was dissected free from the dentin prior to the demineralization required for As time progressed, the criteria for evaluation routine histologie sectioning. Undemineralized secgreatly improved as researchers hegan to differentiate tions were then prepared from these pieces of enamel between histologie artifacts and tissue reactions.^'' for microradiographic examination. Thus, the degree However, because the publications largely comprised of ceiiuiar infiltration and tertiary dentin formation case reports, the extent of the lesions varied. Usually could he correlated to the extent of the enamel lesion no information on the caries activity or progresston with a fair degree of accuracy. was available, and otber factors, such as the age of the
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Rapidiy progressing lesions

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Pulpal changes were found subjacent to enamel lesions without cavitation in 50 of 74 teeth. In 33 of the teeth with pulpal reactions, the caries lesions were limited to the enamel. Pulpal reactions were even noted subjacent to shallow white-spot lesions.^^ Problems associated with studies of pulpal reactions to caries, such as the use of demineralized teeth, direction of sectioning, location of the lesion after sectioning, caries activity of the lesion, and the age of the patients, have already been mentioned. In addition, no or only Hmited cbaracterization of the tissue changes in the dentin has been undertaken in routine pulpal studies, either clinically or histopathologically in relation to the mineral content of the dentin. Significant tissue changes in the primary dentin, such as obturation of the tubules and the resulting reduced dentin permeability, have largely been disregarded. The reason that undemineralized and demineralized sections are not studied at the same time is mainly because of the difficulties involved in studying the organic and the inorganic phases of the tissues in their normal relationship, ie, in the undemineralized state. The dentin will be markedly different in rapidly progressing or "acute" lesions than it will in arrested or "chronic" lesions. This technical problem in preparing sections of teeth for light microscopy can be overcome,^^'^^ but the loss of tissue during the preparation of the sections represents a major problem for detailed analyses of the entire tooth. With this reservation, the use of undemineralized tooth sections of the central, and therefore most advanced, part of a caries lesion makes it possible to obtain overview sections showing concomitant cbanges within the enamel, dentin, and the corresponding pulp (Eigs 12 to 15). Such a technique was used to carefully examine and histologically classify 36 clinically welldefined enamel caries lesions without cavitation, based on increasing depths of the lesions.^' Computerized histomorphometric analysis revealed that the involved odontobiasts in active enamel lesions reaching the dentinoenamel junction were significantly smaller than were odontobiasts at tbe control site. No significant changes in the size of odontobiasts were noted subjacent to arrested lesions of similar depths. In addition, cellular proliferation in the cellfree zone was noted, whereas this was not observed in arrested lesions. Thus, the odontobiasts and subodontobiastic cells are activated early in the progress of the caries lesion, just as they react rapidly to the removal of cariogenic plaque.3' Changes in the subodontobiastic region also occur early, and these changes might include the eariy onset of neurogenic inflammatory reactions (Figs 16 and 17). The chronology of the initiation of the odontoblastic response to caries lesions has not been established
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with any degree of certainty. However, wlien undemineralized sections are examined, the first indications of cellular reactions (Fig 18) are noted in active lesions involving more than a quarter of the thickness of the enamel.3' These active lesions do not show any discernible alterations in dentin mineralization (Fig 19). Concomitantly with the formation of hyp^ rmineralized dentin, the homogeneity of the predentin may be altered, and a change in the organization of the collagen fibrils prevails (Eig20). Diagrams of these stages are shown in Eigs 21 and 22. As soon as the noncavitated enamel lesion causes demineralization of the affected dentin, evidence of tertiary dentin may be noted at the pulp-dentin border, involving the primary odontobiasts, also deflned as reactionary dentin^^ (Fig 23). Eventually these cells are lost and the number of tubular structures decreases in the tertiary dentin {Fig 24), The adjacent cells are fibroblast-like, with nonpolarized nuclei, and atubular tertiary dentin is laid down (Fig 25). In contrast, the tertiary dentin in slowly progressing lesions resembles that of tbe physiologic secondary dentin (Fig 26). This dentin has the potential for normal tissue changes as a result of mild to moderate stimulation from chronic caries lesions. As previously illustrated, this can take place where an adjacent tooth has been extracted (see Figs 3 and 4) or in areas where growth conditions for the microbial ecosystem are reduced. Eigures 27 to 29 show the principal changes during stages of slowly progressing caries. During the last 20 years, much emphasis has been placed on the permeability of the dentin in the assessment of pulp-dentin reactions,^ with good reason. The initial ports of entry to the pulp for bacteria, bacterial antigens, toxic, and allergenic components are the dentinal tubules. Therefore, studies are needed to evaluate both the inorganic and the organic phases of dentin in the same sample to correlate with caries and restorative procedures. Furthermore, studies of the immune system of the pulp have clarified some of the defense mechanisms of the pulp. Specifically, in relation to carious dentin, increased accumulation of immunocompetent cells has been demonstrated in the pulpal tissue, as shown in Figs 21 and 22.^^ Attention has been paid to the dendritic cells of the pulp. They are present along the odontoblastic layer even before the onset of external injuries, Therefore, immunocompetent cells are important during the initial exposure of antigens to the pulp.'i These cells have not been observed following the formation of tertiary dentin.'^ The importance of interactions among immunocompetent cells, release of neurogenic peptides, and vascular changes related to caries and restorative dentistry will be important areas of research in the future.
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Bjarndal/Mji Figs 12 to 15 Central part ol an occlusal lesion on a biseoted loolh. (Original magnificalton x5 From B|0rndal et al.3' Reprinted with permission.^

Fig 12 Photograph of the lesion before tfiin sectiOhs were prepared.

Fig 13 Thm, undemineralized sec(ion viewed in tfie light microsoope.

Fig 14 Thin, undemineralized seclion viewed microradiographically The dentin demineraiization (DD] is restricted to the oontact area of the enamel lesion (HD] Hyper mi ne rail zed dentin.

Fig 15 Example of lesioh (X] and control () areas. The hypermineraiized dentin appears diffrent, depending on the microscopic lechnique employed. Note the difference in appearanoes of Ifie lesion and unaffected controi areas, and compare those appearances fc those shown with (he microradiographic technique (Fig 13) and another iight microscopic technique (Fig 14).

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srndal/lvljr Fig 16 (Left) Odontoblast (O)-pijde'iiiii [PD] region, correspcndiog to that 'il unafleoted dentin (Y) in Fig t5. [Tciuidine blue-p/ronin stajn; original magnification X5O.]

Fig 17 (High!) Odontobiast (Oj-prc-dentin (PD) .'egion, corresponding to the iesicn area (X) in Fig 15. subjacent to a nonoavitaied, active caries iesicn (Toiuidine btue-pyronin stain; origilai magnilioation x50 )

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Fig 18 Reduced odontobiastic (0) layei and reduced predentin width subjacent to an active caries iesion that has not reached the dentinoenamei junction The ceil-free zone is present subjacent to the odontcbiasts (dotted lines) Extent of the affected dentin. (Toluidine biuepyronin stain; original magnification x50.]

Fig 19 Ccmpcsite microradiograph of an undernineraiized section adjacent to that shown in Fig 18. There is no difference in degree cf mineralization of the inner dentin of affected and unaffected dentin. (Onginal magnification x50.)

Fig 20 High magnification of the odontoblast (O)-predentin (PD region subjaoeni to an aclive enamei lesion. The homogeneity of the predentin is aitered, and the organization of the coiiagen fibriis has changed The odontobiasts are reduced in height and number. (Toluidine biue-pyronin stain; original magnification x90D.)

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 Bjorndal/Mjr Figs 21 to 23 Schematio representation of progression of an active, noncavitaled canes lesion (red areas)CanoQer\ic plaque.

Fig 21 Cellular changes in the pulp are noted even betre alteration in dentin mineralization, (inset) Details ot cellular proliteration into the cell-free zone. Dendritic-1 ike cells (yeilow cells) are present, and tnese are also found in unaffected areas. (CT) Central Irauerse line representing the oldest part of the enamel lesion

Fig 22 As the enamel lesion approaoties dentin, hypermineraiized dentin (gray area) is cbserved corresponding to tne central traverse line (CT). (inset) Changes in the odontobiast-predentin and subodontoblasiic regions.

Fig 23 As dentin demineraiization starts (orange area), formation ot tertiary, or reactionary, dentin is iniiiated. The tirst-formed reactionary dentin develops into an atubular fibrcderttin type, also referred to as interface dentin. (inset) Reduced number of odontoblasts (red oelts) in the tertiary dentin.

Fig 24 Central lesicn area showing tertiary dentin A distinct interface separates the crihodentin (D) from the partly atubuiar tertiary dentin (TD). Fibre blast-1 ike ceils, not odcntobiasts, line the atubular dertin. (Toluidine blue-pyronin stain; original magnificalion x90D.) Fig 25 Microradiograph of mainly atubular tertiary dentin (TD) subjacent to an active lesion. (D) Dentin. (Original magnification x20,) Fig 26 Microradiograph cl lubular tertiary dentin (TD) subjacent to a slowly progressing lesion. Note the continuity of tubules from physiologic secondary dentin (SD) to tertiary dentin and the variation in rsiodensity between secondary dentin and tertiary dentin, (Original magnification X2O.)

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Figs 27 and 28 Schematic representation of arrested, slowly progressing lesions. Dendritic-like cells (yellow cells) are present, and they can also be found in unaflecled areas.

Fig 27 During the early stages of the enamel lesion, no changes are visible in the dentin. and no cellular changes are present in the pulp, (inset) Details of the normal structure in the odontoblastic region. (CT) Central traverse line representing the oldest part of the enamel lesion.

Fig 28 As the enamel lesion approaches the dentin, hypermmeralized dentin is observed subjacent to the deepest part of the lesion (CT). Changes are also taking plaoe in the odontoblast-predentin region, but the subodontoblastio region appears unaffected. (inset)Jhe homogeneity of the predentin is altered,

Fig 29 Schematic representation cf the tooth's condition after the tooth adjacent to an aotive lesion is extracted. Cavitation has occurred, and it is covered by cariogenic plaque (red area). Note the discolored, demineraiized dentin (brown area) and adjacent hypermineralized dentin (gray area), f/nsef; Tertiary dentin subjacent to the lesion with marked reduction in both the number and height of odontoblasts.

Moreover, the fate of the odontoblasts during caries progression still remains to be answered in detail. Major changes during progression of cavitated enamel lesions are summarized in Figs 30 to 32. During rapid lesion progression, accumulation of immunocompetent cells is observed in conjunction with reduced numbers of primary odontoblasts (Fig 30). If tertiary dentin eventually develops, it is usually formed as an atubular dentin (Fig 31). During stages of well-defined dentin exposure, it becomes relevant to comment on the spread of the advanced iesion, which tends to occur along the dentinoenamel junction (Fig 32). Black^^ described the phenomenon as "backward decay of the enamel," because the enamel becomes demineraiized both from the ad728

vancing dentin lesion and from the outside. Undemineralized sections at this stage of progression clearly show the spreading pattern as a large, growing zone that somewhat masks the outlines of the initial dentin reactions that occur prior to cavitation (Figs 33 to 35). The accumulation of inflammatory cells is particularly great whenever the bacteria associated with the caries process reach the tertiary dentin subjacent to the lesion.53 5761 ^t this stage, major intradentinal defense mechanisms have been depleted; ie, obturated tubules have opened and the interface dentin has been destroyed. The stage corresponds to the histopathologic condition of severe pulpal inflammation, and the chances for healing are minimal. Pulpal infection and necrosis may be the end result. Endodontic treatment is then necessary prior to restorative treatment. This sequence of events is characteristic of active and rapidly progressing deep lesions that may exhibit no or only minor defense reactions in primary dentin and minimal formation of atubular tertiary dentin subjacent to the lesion.

CLINICAL DIAGNOSIS

Important signs and symptoms indicative of caries include tbe presence of microbial acid-producing plaque, the surlace characteristics of the lesion, including the degree of cavitation, discoloration, consistency, and wetness of the involved dentin, and subjective symptoms such as pain and hypersensitivity,^'^''''^s These factors must all be taken into consideration during the evaluation of the caries status of any lesion.
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BJ0rndal/Mjr Figs 30 to 32 Schematic representation of changes in the dentin and pulp associated with the progression of a cavitated lesion with cariogenic plaque (re area) in the cavfty and with extensive dentin demineralization (orange area) and minimal reactions in primary dentin.

Fig 30 During rapid progression of the lesion, odontobiasts are absent subjacent to the lesion and accumulation of immunocompetent cells, including dendritic-like cells (yellow cells), is observed, (inset) Details of the predentin area with dendritic cells and immunocompetent cells (round cells).

Fig 31 Active caries iesion has reached into the dentin (red area), and bacteria penetrate the dentin. C/nsef) Tertiary dentin initially develops as atubular dentin and later as tubular dentin, with no dendritic-like cells present.

A very important element in the diagnosis of the pulpal pathosis associated with caries is the rate of progression of the lesion. In clinics with regularly attending patients, lesion progression can usually be established. However, in many situations the rate of progression cannot be ascertained, and clinicians must rely on an overall gross risk assessment based on the existing conditions and the past history of restorative treatment. The most common pattern of caries development today, in a dentally alert population, tends to be slow progression of lesions. Present-day restorative treatment should, therefore, be less aggressive than in the past, when lesions progressed more rapidly, resulting in irreversible pulpal involvement at early stages of the disease. However, in individuals with poor oral care and in populations with active disease, as was typical in the "pre-uoride era," irreversible pulpal lesions may still develop quickly. Therefore, an appropriate treatment choice for such selected patients today may be to attempt a stepwise excavation procedure to allow the pulp to heal prior to the final restoration. While such procedures are in progress, it is important to explain to the patient the advantages of preventive and noninvasive dental care. Dentinal lesions without clinical symptoms that are hard, dry, and dark brown are typically arrested or slowly progressing lesions, and the depth of the demineralized dentin is often limited. Bacteria may remain in the dentinal tubules of such lesions.^-^^ xhey may not require surgical intervention and restoration, except for esthetic reasons to replace lost tissues in advanced cases to restore function, but such lesions should be kept under observation.
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Fig 32 Following rapid, extensive cavitation of enamel and dentin, a spread of the lesion occurs along the deminerazed dentinoenamel junction. An increased accumulation of inflammatory cells is noted.

Rapidly progressing lesions that are soft, wet, and light yellow are often painful, and the demineralization will penetrate deep into the dentin. Although early development of hypermineralized dentin also prevails in these lesions, the relative importance of intratubular deposits in acting as a barrier against bacteria and toxic or allergenic agents is low. These lesions must, therefore, receive immediate clinical attention. All stages between the characteristic arrested lesion and the active lesion may be found. This situation makes treatment planning a challenge. There is no infallible way to predict future development of any caries lesion, and, as previously pointed out,^ it might not be enough to focus on a single lesion parameter.
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Frgs 33 to 35 Tooth bisected through the central par of an active lesion in a closed environment. (Original rnagnification x5. From B|0rnaal and Darvann.-^^* Reprinfed with permission )

Fig 33 Photograph of the lesion before thin sections were prepared. Note the heavy accumulation of plaque on the dentin in the cavity.

Fig 34 Section from the tooth viewed in the light microscope

Fig 35 Seotion from the tooth viewed microradiographically. Zones of higher radiopacity are visible at the periphery of and within the demineralized dentin

Instead, attention to the specific site of the lesion within the oral cavity, including evaluation of the lesion's history, may give relevant information and may indicate why the lesion has either progressed slowly or rapidly. Because the caries process is dynamic, longitudinal review of any lesion can be beneficial in assessing its status. Microbial ecosystems have been defined in terms of closed or open environments."*' The occlusal cavitated lesion represents a closed, active environment, whereas the open ecosystem is typically noted on smooth surfaces (Fig 36). The open lesions are vulnerable locations for cariogenic plaque, because it may be more easily disturbed by mechanical and physical masticatory forces and toothbrushing than the protected closed ecosystem located in occlusal and proximal cavitated lesions {Fig 37). If the enamel breaks down during any stage in the development of a cavitated lesion, the environment of the lesion changes dramatically {Fig 38). This situation may provide a self-cleansing surface. An active lesion may then become arrested, ie, a conversion from a closed to an open environment takes place, The softest parts of the demineralized dentin may then be lost as a result of function and wear. The remaining parts may remineralize. Clinically, this situation presents itself as exposed, shiny, dark, hard dentin. The clinical tools presently available to preoperatively diagnose caries lesions in relatively inaccessible locations, such as occlusal surfaces and interproximal areas, are inaccurate and crude. They include visual inspection of discoloration and staining (which may occur for different reasons and are not synonymous with caries), "explorer catch" (an explorer will catch in
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any narrow crevice, carious or not), and radiography, which also leaves much to be desired in the diagnosis of caries lesions.^'^ Extensive research to develop new and improved diagnostic tools^" has so far not led to development of methods that have received wide acceptance by practitioners. The clinical experience of the practitioner, including knowledge of the caries pathology, and the visual assessments of an individual's caries situation over time, are at present the optimal base for treatment planning that will benefit the patient in the long term.
Hidden caries

Clinical terms that indicate some of the problems involved in assessing caries lesions are sometimes introduced. An example is the term hidden caries, which is diagnosed radiographically as an extensive dentinal lesion that cannot be detected clinically. Tbe important point in this context is what the practitioner expected to find. If the answer is a cavitated lesion, then the expression "hidden" seems logical because it represents a surprising element to the examiner.**' On the basis of epidcmioiogic data, it has been suggested that the morphology of approximal lesions may have changed, which in turn leads to ^'hidden" dentinal caries.f^^ The morphologic change may possibly be explained as follows: A progressing, noncavitated enamel lesion eventually becomes associated with demineralization of dentin, because the basic histopathologic nature requires that the enamel lesion reach the dentinoenamel junction before the dentin becomes demineralized. In addition, lesions are progressing much more slowly than previously;
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Fig 36 Siowly progressing canes lesion m an open environment on the buccal surface of a mandibular canine, Noe the dark color of Ihe dentin in tfie Fig 37 Active caries lesion in a closed environment on the mesial surface of tfie maxillary first molar.

therefore, destruction of dentin can be more pronounced prior to the cavitation stage. Thus, the potential for extensive dentin destruction exists even in the absence of clinically detectable lesions. Use of the term hidden occlusal caries or hidden dentinal caries shouid be changed and related to the histopathology rather than just an expression of a surprising element for the practitioner, ie, of caries found under apparently intact enamel. Clinically, attention should focus on careful examination and measurement of the enamel lesion's size, which basically iticludes the cleaning and drying of the teeth,232^8 supplemented by radiographie examination at regular intervals. In addition, future acceptance of promising diagnostic tools**''^ as aids in the diagnostic process must also be considered.
Deep lesions

It is of prime clinical importance to evaluate the extent of any caries lesion, but especially deep caries lesions, and to assess the pathosis involved. The possibility of development of irreversible, symptomless pulpitis looms in the background. Presently, no routine equipment is available clinically for noninvasive measurements of the degree of inflammation in the pulp. This means that the treatment of deep lesions is based on information collected from indirect methods, including subjective information from the patient and assessment of his or her caries risk and progression of the lesion, and on techniques for estimating pulpal sensitivity and vitality as well as radiology, A combined evaluation of the collected data leads to the best possible diagnosis and treatment plan.^f'
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Fig 38 Schematic representation of the condition m an untreated lesion where slowing of the lesion's progression may occur, provided that the enamel breaks off or s removed, (dotted line) Position of the overlying undermined enamel of an active lesion in a closed environment. Whenever the undermined enamel breaks down, the lesion is opened, and a change in the conditions for bacterial growth occurs, leading to an altered cariogenic environment and a slower progression of the lesion.

9 have described the states of pulpal pathosis as reversible/asymptomatic pulpitis and irreversible/symptomatic pulpitis, but these diagnoses are empirically based. For decades, different classifications of pulpal reactions related to caries and varying opinions regarding treatment strategies have existed for the treatment of asymptomatic deep caries lesions.'^ The most common, but rather radical, approach involves a one-step excavation procedure, even if the possible
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outcome is pulpal exposure, followed by either a pulpcapping procedure''" or a pulpectomy. Another approach involves a stepwise excavation aiming to prevent perforation of the pulp.^'
REMOVAL OF CARIOUS TISSUE

The clinical handling and excavation of necrotic, infected, and demineralized dentin must be based on knowledge of pulp-dentin biology. Softened carious dentin is traditionally removed by hand excavation or with burs in a dental handpiece run at extremely low speed, to prevent overextension of the preparation, Overextension within the dentinai cavity will open unaffected dentinai tubules, which are more permeable than the tubules subjacent to the carles lesion.52 Thus, the periphery of any prepared caries lesion must be given partieular attention, because this location runs a high risk for invasion of bacteria through permeable dentin. The effeet of such overextension was noted in an experimental series in which the defense mechanisms at the pulp-dentin interface were challenged.^^ Whenever the cavity preparation was aecidentally extended beyond the original size, localized, peripheral pulpal reactions were noted. A randomized clinical trial for testing a stepwise excavation procedure versus more radical pulpal treatment procedures has never been carried out on permanent teeth, and for ethical reasons that might even be difficult to achieve today. Such an experimental approach has been employed in primary teeth.si The results showed that a stepwise excavation procedure was more successful than a single and final excavation procedure for rapidly progressing lesions in thai fewer pulpa! complications developed after the treatment. A few recent studies have taken this information into account and examined the stepwise excavation, performed on permanent teeth by pedodontists"*" or general practitioners.^' One of these studies included a subsequent follow-up examination,^^ which is important because pulpal necrosis can typically develop without clinical symptoms. In the follow-up study, 4 of 84 teeth examined showed necrotic pulp at the 3- to 4-year recall, indicating a success rate of 92%, Thus, a two-step approach for the treatment of selected deep caries lesions can successfully be performed in general practice, but it requires the time and dedication of both the clinician and the patient. Alternative excavation techniques have come and gone, and some have reappeared after some time. Airabrasive and ultrasonic techniques and chemomechanical approaches that use sodium hypochlorite or enzymes to further dissolve the affected dentin for easy removal are among these methods.^''^^ These
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techniques have never received wide accej by clinicians, but, in comparison with the relativL., .rude bur concept, the chemomechanicai approach represents a more specific, but slower, approach to the removal of demineralized dentin. The use of dyes to detect remaining carious dentm in cavity preparations has been suggested,^^ Evidence was presented to indicate that the dye (basic fuchsm) could differentiate between demineralized infected dentin and the deeper demineralized noninfected dentin. Because the noninfected, demineralized vital dentin has the potential for remineraiization, it may not have to he removed.i"o However, the use of cariesdetecting dyes may lead to excessive removal of dentin in a preparation,loi including the mantle dentin at the dentinoenamel junction, which is normally relatively poorly mineralized. It is universally accepted that all soft, carious dentin should be removed prior to restoration. However, the need for removal of all carious dentin has been seriously challenged by the results of a longterm clinical study.i^ In this study, gross ocelusal caries was sealed into the tooth witii resin-hased materials. After 10 years, no progression of the lesions had occurred. The results may have been dependent on a complete seahng of the lesion from the oral environment, and they also require confirmation in other clinical studies. Reminerahzation of carious dentin after calcium hydroxide treatment has also been shown in an in vivo experimental study. ^^^ However, at the present time, it is considered appropriate to remove all soft, carious tissue prior to restoration. Similarly, even if the stepwise excavation approach is employed to prevent perforation to the pulp, all soft dentin is removed after treatment intervals varying from 3 to 6 months. The basic concept in the two-step approach to restorative treatment is to change an active lesion (Fig 39) into a slowly progressing lesion. Because of the marked alteration of the cariogenic environment gained during the first exeavation procedure, the remaining demineralized dentin changes properties during the treatment interval toward those of arrested lesions (Fig 40). In principle, the process is similar to the conversion of lesion activity that occurs following the breakdown of undermined enamel in untreated lesions (see Fig 38). Clinically, the wet, soft, and yellowish infected demineralized dentin (Fig 41) is turned into dry, dark brown, harder, and less infected demineralized dentin (Fig 42), according to recent microbiologie data,'"'' Clinically, the dentin "dries out," resulting in a tissue that may be excavated without exposing the puip. The philosophy during the final excavation, however, follows the same rules as for a single excavation procedure, ie.
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arndal/Mjr rigs 39 and 40 Cnanges tnat take place as a resuH ot stepwise excavation. Tne aim is to cnange an active lesion into a slowly progressing lesion Fig 39 (Left) (dotted iine) Amount ot carious dentin removed during the initial treatment. Fig 40 (Rigiit) Because of tne marked aiteration of the cariogenic environment gained during the first excavation procedure and the placement of a provisional restoration (mde yelloiiv area), the retained demineraiized dentin changes its properties during the treatment intervai toward those of an arrested, siowiy progressing iesion (dark brown).

Fig 41 Maxillary first premolar wiin a deep canes lesion subjected to a stepwise exoavation procedure, snown after me initial excavation and jusl prior to the application ol a provisional restotatron. Tne remaining demineraiized dentin is wet, soft, and yellow-orange, but it wiil be covered by a provisional restoration for 6 months.

Fig 42 Same premolar shown in Fig 41, 6 months foliowing the initiai treatment. The tooth is shown after removal of the provisionai restoration and just pnor lo the final excavation ol the remaining demineraiized dentin. The dentin on the puipai lioor of Ihe iesion now appears dry, is dark brown, and is harder than it was at the initial treatment.

all soft dentin must be removed to obtain optimal conditiorts for the future permanent restoration. Such a twostep excavation process will add to the cost of the restorative treatment.
CONCLUDING REMARKS

Dental caries, presenting as primary and secondary lesions, is by far the most common reason for inserting restorations- Despite the fact that the disease is preventable, restorative dentistry represents the major workload in general denial practice in many populations. It is the obligation of the practitioner to inform patients of the advantages of preventive dentistry in the management of dental caries. It is also the clinician's responsibility to monitor the situation and take the tiecessary steps to encourage compliance with the
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preventive programs prescribed. Tbe patient is accountable for adbcrence to tbe established preventive plan, but for a variety of reasons some patients may not be capable of accepting responsibility for tbis part of tbeir orai bealth. If for any reason prevention fails, restorative treatment is required. Assessment of lesion progression is an essential part of caries diagnosis and management. The rate of caries progression on a population basis is typically described as either a decreasing or an increasing factor, but sucb information must be interpreted with caution in relation to an individual patient. Tbus, tbe rate of caries progression witbin tbe patient can only bc determined by comparing tbe condition of the specific lesion environment at different time intervals, and it is a decided advantage for the patient to receive continuity of care by the same clinician over extended periods of time. Oniy in tbis way can an accurate "cariogenic 733

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profile" for the individual patient be estahlished and realistic preventive strategies he developed. If caries lesions progress to the stage at which they require restorative intervention, it is important to understand the tissue changes in the dentin that are likely to have taken place during lesion development. Intratuhular changes and tertiary dentin formation will affect the outcome of the restorative treatment. Evaluation of such tissue responses should enter into the treatment planning. Until the present, no major distinction hetween the restorative treatment of active (rapidly progressing) and arrested (slowly progressing) lesions has been prescrihed, despite the fact that the two conditions represent major differences in tissue change in the puip-dentin complex. Where open, permeable dentinal tubules persist, or when the preparation results in the opening of unaffected dentin, greater care must be taken in all phases of the restorative procedures than is necessary if the dentin is impermeable. An optimal assessment of the prevailing clinical conditions can only he made on the basis of thorough knowledge of the hiology of the pulpdentin organ.

ACKNOWLEDGMENTS
The aiilhors would like to thLink Dr A. J. Smith. Prolessor and Chairman, Unit of Oral Biology. School of Dentistry. University of Birmingham. Birmingham, England, for reviewing the manuscript. A Guest Research Fellowship from the Research Council of Norway, partly in support of Ivar A. Mjr's Faculty Developmental Leave al NIOM, Scandinavian Instilute of Dental Materials, is gratefully acknowledged.

REFERENCES 1. Mjr IA, Moorliead JE, Dahl JE. Reasons for replacement of restorations Jti permanent teeth in general dental practice. Int Dent I 2000;50: 360-36. 2. Silvcrslone LM, Hicks MJ, Feathcrstone MJ. Dynamic factors affecting lesion initiation and progression in hutnan detital enamel. Part I. The dynamic nature of enamel caries. Quintessence Int 1988,19:683-711. 3. Larsen MJ, Bruun C. Caries Chemistry and fluorideMechanisms of action. In: Thyistrup A, Fcjcrslov O (eds): Textbook of Clinical Cariology. Copetihagen: Munksgaard, 1994:231-257 4. zer L. The Relation Between Gap Size, Microbial AcctJmulation and the Structural Features of Natural Caries in Extracted Teeth With Class II Amalgam Restorations. A Stereo- And Polarized Light Microscopic Study [thesis]. Copenhagen: University of Copenhagen, 1997. 5. Mjr IA, Toffenetti F. Secondary caries; A literature review with case reports. Quintessence Int 2000;31:165-179. 6. Silverstone LM. Structure of carious enamel, including tbe early lesion. Oral Sei Rev 1973;3:100-160.

1. Mjr IA. Histoiogic studies of human coronal v- "^ ' lowing cavity preparations and exposure of ground i jcets tn vivo. Arch Oral Biol 1967; 12:247-263. 8. Furseth R, Johanscn E. A microradiographic comparison of sound and carious human dental cementum. Arch Oral Biol 1968:13:1197-1206. 9 Thewlis J Tbe structure of teetb as shown by x-ray examination. Spec Rep Ser Med Res 1940;238:l-82. 10. Hals E, Mrch T, Sand HE Effect of lactate buffers on dental enarnel in vilro observed in polarizing microscope. Acta Odontol Scand 1955;13:85-122. 11. Darling AI. Resistance of the enamel to dental caries, J Dent Res 1963;42:488-496. 12. Bmdevold F. McCann HG, Gren P. Caries resistance as related to the chemistry of the enamel. In: Wolstenholme GEW (ed). Caries Resistant Teeth. London: Churchill, 1965: 121-140. 13. Groeneveld A, Theuns HM, Kalter PGE. Microradiography of developing artificial dentai caries-like lesions in man. Arch Oral Biol 1978;23:75-83. 14. Itidd EAM, Thyistrup A, Fejerskov O. Tbe histopatbology of enamel caries in fluorosed deciduous teeth. Caries Res 1981;15:346-352. 15. Arends J, Christoffersen J. The nature of early caries iesions in enamel. ] Dent Res 1986;65:2-11. 16 Holmen L, Tbylstrup A, 0gaard B, Kragh F. A scanning electron microscopic study of progressive stages of enamel caries in vivo. Caries Res 1985;19:355-367 17 Holmen L, Thyistrup A, Artun J. Ciinical and bistological features observed during arrestment of active enamel carious lesions in vivo. Caries Res 1987;21:546-554. 18. von der Fehr FR. A study of carious lesions produced in vivo in unabraded, abraded, exposed, and F-treated human enamel surfaces, with emphasis on the x-ray dense outer layer. Arcb Gral Biol 1967;12:797-814. 19. Silverstone LM. Reminerahzation phenomena. Caries Res 1977;U(suppi l):59-84. 20. Koulourides T, Cameron B. Enamel remineralization as a factor in tbe pathogenesis of dental caries. J Oral Patbol 1980:9:255-269. 21. Koulourides T, Bodden R, Keller S, Manson-Hing L, Lastra J, Housch T Cariogenicity of nine sugars tested with an intraoral device in man. Caries Res 1976; 10:427-441. 22. Thyistrup A, Bruun C, Holmen L. In vivo caries modelsMechanisms for caries initiation and arrestment. Adv Dent Res 1994;8:144-157 23. BJBmdal L, Thyistrup A. A structural analysis of approximal enamel caries lesions and subjacent dentin reactions. Eur J Oral Sei 1995;103:25-31. 24. Bjorndai L. Cariesltesionens tidlige udvilding i emalje og pulpa-dentinorganet [thesisj. Copenhagen: University of Copenhagen, 1991. 25. Ekstrand KR, Bjorndai L. Structural analyses of plaque and caries in relation to the morpbology of tbe groove-fossa system on erupting mandibular third molars. Caries Res 1997;31:336-348. 26. Carvalho JC, Tbylstrup A, Ekstrand KR. Results after 3 years of non-operative occlusal caries treatment of erupting permanent first molars. Community Dent Oral Epidemiol 1992;20:187-192.

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