Invited author

Tissue response to dental caries

Langeland K. Tissue response to dental caries. Endod Dent Kaare Langeland
Traumatol 1987; 3: 149-71. Department of Endodontics, John Dempsey Hospi-
tal, University of Connecticut Health Center, Far-
Abstract - Caries still represents the most widespread hutnan dis- mington, Connecticut, USA

ease. The pulp tissue sequelae of dentin caries are of utmost im-
portance, because prevention ofpulpal damage considerably re-
duces the need for extensive restorations and endodontic therapy.
There is, however, considerable disagreement in the literature re-
garding how early the pulpal response to caries can be detected. The
material in this article, gathered from the author's and his co-
authors' earlier investigations, deals with pulp reactions from in-
itial caries to increasingly extensive caries; caries in combination
with attrition; the effect of carious dentin in experimental cavities of
intact dentin; the effect of medicaments, restorative procedures
and materials, and indirect pulp capping in the treatment of deep
caries; microbiologic aspects of dentin caries; diagnosis criteria for
treatment; light and electron microscopic study of teeth with cari-
ous exposure; periodontal disease and root caries in the geriatric
population; pulp biopsies of teeth with periapical lesions, and the
breakdown ofthe remaining pulp and its periapical sequelae. Pul-
pal reactions to initial caries detected as early as bacteria reach the
dentinal tubules arc also discussed. As in medium and deep caries,
this can be reversible following the removal ofthe infected dentin,
except for irritation dentin and calcifications on the canal walls or
free in the lumen. Bacteria remaining in dentinal tubules combined Key words: caries, coronal and radicular; micro-
with iatrogcnesis may be the reason for pulpal disintegration under organisms; inflammation, pulpal and periradicular;
calcification; immune response; pain/no pain; pulp,
deep restorations. Indirect pulp capping is not an acceptable pro-
vitai and non-vital; pulp capping, indirect and direct.
cedure. Pain (or lack thereof) is not a predictable indicator ofthe
Kaare Langeland, DDS, PhD, Department of Endo-
inflammatory stage ofthe pulp. Root caries must be treated early to dontics, John Dempsey Hospital, University of
prevent pulpal destruction. Vital pulp tissue can he found in the Connecticut Health Center, Farmington, CT 06032,
roots of teeth with periapical radiolucencies that will ultimately USA.
show the presence of bacteria. Accepted for publication 12 March 1987.

Caries - despite all prophylactic measures - is still
the most widespread human disease. Akhough die
disease has heen considerahly reduced in the popula-
tions of the West, caries causes tooth destruction of
considerable significance, placing great demands on
human labor and materials. According to the 1979
ADA Survey of Dental Practice (1) approximately
200 million fillings, 35 million single crowns, and 10
rnillion bridges were performed. In addition, there
were 50 million extractions. Almost everything per-
formed in the first 3 categories is caries-related. It is
also relevant that 17,390,000 endodontic treatments
vvere carried out that year. Furthermore, in the endo-
dontic clinic ofthe University of Connecticut Health
Center, approximately 90% of all endodontic ther-
apy is carried out in teeth that were restoratively
treated previously. Which part of the pulpal break-
down is caries-related (recurrent caries), of iatro-
genic nature, or due to the cumulative effect of all
irritants can only be speculated. The reasons for the
50 million extractions are not given in the ADA sur-
vey; it is ndt known whether the teeth were treated
earlier or if the reason for the extraction is caries or
periodontal disease. It can be assumed that before an
individual has reached 40 years of age most extrac-
tions are due to caries, whereas after 40 the extrac-
tions are mostly due to periodontal disease or a com-
bination of both. Particularly in the geriatric popula-
tion, root caries has taken on major proportions and
presents a difficult treatment problem. Thus, caries
continues to represent a practical and socio-medical
problem of great economic importance. In this re-
gard the pulpal sequelae of dentin caries are of par-
ticular interest because prevention of pulpal damage

149
Langeland
considerably reduces the need for extensive restora-
tions, and endodontic therapy and its sequelae.
There is disagreement in the literature regarding
how early the pulpal response to caries can be detect-
ed (2-6). This is due to lack of acknowledgement of
the proficiency of the available histologic method-
ology. Enamel and dentin caries may be siinul-
taneously demonstrated in ground sections. How-
ever, the technique of producing ground sections to-
tally destroys the pulp and will not allow any
observations of soft tissue and its cells. On the other
hand, demineralization of mature teeth ~ for the pro-
duction of paraffin or Em sections - leads to elimin-
ation ofthe enamel. Thus, enamel caries and pulpal
reaction cannot be demonstrated simultaneously in
the same section (7,8). However, it was earfier point-
ed out that the presence of a few infiammatory cells
in the pulp of clinically intact teeth could be due to
clinically undetected caries or doubtful conditions
subjacent to a discolored occlusal fissure (9, 10).
Material and metheds
The material upon which this article is based has ap-
peared in a number of earlier investigations. Readers
interested in the details of clinical and histopatholo-
gic methodology and how these may clarify aspects
of distinct disagreement are referred to those publi-
cations. The investigations deal with: reactions to in-
itial caries (7) and to increasingly extensive caries
(11); caries in combination with attrition (12); re-
actions to the effect of carious dentin in
experimental cavities of intact dentin (13) (with the
intent of developing a reproducible model for the
evaluation of restorative procedures and materials);
reactions to the eflect of medicaments ranging from
silver nitrate and camphorated monoclorophenol to
penicillin and corticosteroids, and reactions to re-
storative procedures and materials in carious cavities
(14—20); and reactions to indirect capping in the
treatment of deep carious lesions (21). Further inves-
tigations deal with: the microbiologic aspects of den-
tin caries and their pulpal sequelae (22); the diagnos-
tic criteria for the treatment of caries-
induced pupitis (23); the light and electron micro-
scopic study of teeth with carious exposures (24);
periodontal disease and root caries in the geriatric
populadon (25); pulp biopsies in teeth with peri-
apical radiolucencies related to caries (26); and the
breakdown ofthe remaining pulp and its periapical
sequelae involving endodontic therapy (27-29).
These studies encompass more than 2,000 teeth. The
patients represent a cross-section of the population
from children all the way through to the geriatric
population.
In order to obtain sections of reproducible quality,
methods and criteria as used and described in the
150
quoted references are essential (7, 8, 10-18, 22, 24,
26).
Observations
In teeth with only early indications of clinical caries
such as a discoloration of an occlusal fissure or of an
approximate surface, a minor accumulation of in-
fiammatory cells could be observed where the dentin
tubules involved with caries terminated in the pulp.
Clinically, a sharp probe did not catch, and radio-
grams did not reveal any interproximal caries. Upon
extraction there could be discoloration ofthe proxi-
mal surfaces, but no macroscopically observable loss
of enamel. However, in typical selected histologic sec-
tions taken from the area of a discolored fissure or
discolored interproximal surface, micro-organisms
were only present in the superficial end of the in-
volved dentinal tubules.
It should be noted that very minute (if any)
changes had occurred in the predentin at this stage
of development, and there could be a slightly reduced
odontoblast layer where the involved dentinal tu-
bules terminated in the pulp. Bacterial stains (e.g..
Brown & Brenn) demonstrated the presence of bac-
teria in the peripheral end of the dentinal tubules,
and also in their side branches. It is evident that de-
mineralization of the tubule walls had not taken
place, but it was not necessary for the penetration of
the bacteria, the diameter of which does not exceed
that ofthe side branches ofthe tubules (Fig. 1). Both
Brown & Brenn and PAS/Alcian Blue demonstrated
distinctive stain changes confined to the content of
the tubules pulpal to the bacteria. Tubules in the
same area that were not invaded by bacteria did not
show these typical color changes. Neither the remain-
ing matrix ofthe peri tubular nor intertubular dentin
was involved in this color change.
Caries progress occurred by increases in depth and
in width. Bacteria advanced towards the pulp while
widening the surface area and undermining the en-
amel. In general, the severity ofthe pulpal response
also increased with a significant increase in the num-
ber of infiammatory cells.
In addition, a marked increase in dystrophic calci-
fication occurred in the pulp chamber, in the root
canal, and on the canal walls. The calcification could
become so extensive that it took up a major part of
the pulp chamber, narrowed the root canals, and
made the walls extremely irregular (Fig. 2). This
makes endodontic therapy — if necessary afterwards
- more difficult and may, as an end result, jeopardize
or worsen prognosis.
Recording the severity ofthe pulpal response was
totally dependent on the direction and location of
the sections and their relation to the carious area as
demonstrated in a molar with deep caries: 596 sec-
 Tissue response te dental caries

Fig. J- Tooth with discolored occlusal ri.s.sure, but no attachment of a sharp probe, and thus diagnosed a.s no clinical caries.
A. Histologieally, presence of bacteria in some dentinal tubules (horizontal arrows) and where these tubules terminate in the pulp,
a concentration of cells in the odontoblast layiM" (oblique arrows, orig. mag. x 32).
B. Organic debris and bacterial plaque in the occlusal lissure (vertical arrow in A, orig. mag. x250).
C. Bacteria in debris in oeelusal fissure in B (orig. mag. x 1000). -i i l • r
D. Bacteria in the peripheral end of the adjacent dentinal tubules and their side branches. Note tlie dearly discernible cliains oi
bacteria in side branehes (orig. mag. x 1000).
E. From area ofleft arrow in A: small concentration ofehronic inllammatory eells (orig. mag. x 250).

151
Fig. 2. Maiidibular fust molar, medium to deep caries. No previous uoi- present pain.
A. Section, through center of pulp ehamber and the root canal of distal root, ofT center of mesial root. Ofthe 3.5 mm across the
pulp chamber of this seetion, 2.7 mm is occupied by calcifications (between horizontal arrows). No orifice, and only part ofthe root
canal ofthe mesial root, but an area of resorption outside the main canal (vertical arrow). Circumferential apposition on the canal
walls causes narrowness and irregularity of canal (horizontal lower arrows, orig. mag. x 8).
B. From area of middle horizontal arrow in A: free ealcification surrounded by ehronic inflammatorv cells and fibroblasts (orie mac
x250). • • \ b- b-
C. From dense cell concentration in A: small and large lymphoeytes, plasma eells, macrophages, and fibroblasts (orig. mag. x 630).
D. Amorphous dystrophie calcification from pulp chamber: left top arrow in A, free in pulp ehamber (orig. mag. x 63).
E. Calcification attached to the pulp chamber floor in A. Distance to pulp chamber eeiling 0.1 mm (orig. mag. x 63).
Clinical consideraliom. Although ealeifications occur frequently, even in the \m\p of impaeted teeth, they are pathologic entities. They
occur by deposition of calcium salts in dead and dying tissue. The capability of pulp tissue to respond to injury is reduced by the
same volume as the calcifications. When endodontic therapy finally becomes necessary, they render the canal irregular and twisted,
eausing difficulties in establishing optimal working length and obtaining the smooth clean canal wall required for adequate obturation!

152
 Tissue response te dental caries

Fig. 3- Photomoniagc from one tooth where caries penetration involves approximately 3/4 of the dentin thickness (but not the
irritation dentin) may explain the discrepancy among authors in regard to onset and extent of inllammatory response to canes.
A. The farthest penetration of bacteria into the dentinal tubules is indicated by horizontal arrows. The dividing area between prmiaiy
dentin and irritation dentin (the "calciolraumatic line") is indicated by vertical arrows, pointing upwards. In the subjacent pulp, a
concentration of cells is seen exclusively in the right part.
B. Healthy non-inflamed pulp tissue typical of approximately 200 sections cut in lhc left part of this pulp. , ..
C. Inflammatory reaction remote from the odontoblast layer, typical of approximately 200 sections cut in the area pomtc-d out wit
oblique arrow. Note: no inflammatory cells can be seen between the odontoblast layer on top and the concentration ol cells centra y.
D. From area of the vertical downward arrow in right part of A. Dense concentration of primarily chronic mllammatory c
throughout the odontoblast layer adjacent to the termination of the involved dentinal tubules. • 1 t in
Clinical considerations. If seetions had been cut exclusively in the area of B, the diagnosis would have been deep caries, out o
inflammation. If they had been cut in the area of C, the diagnosis would have been deep earies, but no 5°'''"'^'^f'°"."'^7;''!f"- ,^
inflammation and the termination of the involved dentinal tubules. Only sections including the area in L» wouia gi\e uit us,
answer, that an inflammation is caused by deep caries. Thus, different and contradictory results may be arrived at depenaing upon
direction and number of sections, unless seetions are cut throughout the entire pulp chamber.

153
 Langeland

Fig. 4. Mandibular flrst molar. Deep caries treated with indirect pulp capping, permanently leaving soft leathery dentin under the
restoration. The remaining "leathery" carious dentin was treated with 10% AgNOj, the carious lesion covered with a thick mix of zinc
oxide eugenol, and the tooth restored with oxyphosphate cement and amalgam. The observation period was 32 months. The patient had
no previous nor present pain.
A. Cavity floor, irritation dentin and adjacent pulp. Extensive layer of solid irritation dentin, but total lack of formation in area under coronal pulp (horizontal
arrows) where there are AgNO3 particles and pulp tissue remnants. Dense concentration of cells in coronal part of pulp chamber, a. Empty space (artifact)
due to liquefaction necrosis in vivo, and washing out of liquefied tissue during histologic processing. Density of cells tapers oil'to normal with increasing distance
from carious lesion (orig. mag. x 16).
B. From irregular irritation dentin. Note AgNO3 particles in crosscut dentinal tubules and in adjacent odontoblast layer with di.sintegrating ncutropliilic
leukocytes (orig. mag. x 1000).
C. From area of dense irritation dentin: AgNO;i in dentinal tubules on both sides of calciotraumatic line (vertical arrow in A), and in soft tissue inclusions of
the irritation dentin.
D. Mostly neutropbilie leukocytes along empty spaee a in A. These are the cells responsible for the condition described in A.
E. AgNO] particles in pulp and concentrated in cells along vessels (orig. mag. x 1000).
Clinical consideralions. Although precipitation of calcium salts occurs in dentinal tuhulcs during the carious process, tubules remain open to penetration, and
even a thick layer of irritation dentin docs not ]5rotect the pulp against irritation and destruction. Absence of pain does not indicate absence of inllammation
154 and destruction. Contrary to Fusayama and Jordan ct al., no carious dentin may be left under a restoration.
 Tissue response to dentai caries

Fig. 5. Premolar ol young individual demonstrating the cumulative elfecl of caries restored with a composite lilliii". The patient had
severe pam, whieh disappeared upon restoration of the cavity and then reappeared after several tnonths
A. Pulp horns seem solidly filled with irritation dentin, which generally is thought to protect the pulp from injury Note onenines in the dentin (arrows) (orig.
mag. x25). r r j j ^ 8
B . Less than I mm away, pulp tissue remaining in buccal pulp horn, and lemaining pulp tissue in palatal pulp horn (arrows) (orig. mag. x 25).
C . from spaces pointed out with arrows in A. These spaces contain soft tissue with neutrophilic leukocytes as evidence of communication with the pulp tissue
S centrally. Smce the half-hie of neutrophilic leukoeytes is only 7 h, this is fmal evidence of movement ofthe disintegration products ofthe dentinal tubules -
I bacterial to.xins, monomer, catalysts, tissue lluid, and odontoblast processes - from the periphery, and a chemotactic movement of neutrophilic leukocytes
5 from the pulp tissue into the space where irritation products occur.
I D . From the coronal pulp. Large numbersofneutrophilic leukoeytes, lymphocytes, and plasma cells. The inflammatory response-particularly the neutrophilie
leukocytes, which have to be renewed constantly - emphasizes the fact that the pulp has not been protected against the irritants penetrating from the surface,
and that the irritation is continuous.
Clinical comideratiom. The cuniulative effect of caries and iatrogenesis eaused by a eomposite material can, in the long run, cause total pulp destruetion, leading
to the necessity of endodontic therapy and its sequelae. Prevention of pulpal damage (an endodontic objective) by early and correct treatment prevents this
costly proeedure.

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