Section 1 Rationale for disease management

Biological and clinical rationale for vital pulp therapy

K Gulabivala, Y-L Ng

The aim of this chapter is to outline the biological basis for prevention and
management of pulp disease. A rational approach to the treatment of
disease requires an understanding of the pathological process, which in
turn, demands knowledge of the normal anatomy and physiology of the
involved tissues (see Chapter 1). Given the low-compliance encapsulation
of the pulp and its apparent fragility as a tissue, it was once believed that
relatively minor events could precipitate pulp necrosis and infection. Yet,
the pulp shows remarkable resilience and ability to repair and survive an
aggressive oral environment and generally unsympathetic dental interventions. Clearly the pulpdentine complex is adapted for such survival and
this chapter explores the interplay between host mechanisms and restorative factors that determine the direction of the outcome.

FUNCTIONS OF THE PULP

The functions of the pulp are stated to be formative (dentine) and defensive
(through the pulpdentine complex, inflammatory and immune responses).
Once the tooth is fully formed, the pulp mainly serves a defensive function.
The pulp is not a vestigial organ, as indicated by the definite change in the
rate at which dentine is deposited once tooth formation is complete. Hypothetically, if secondary dentine deposition continued at the rate of primary
dentine formation, the almost complete obliteration of the pulp would
result in a tooth with very different mechanical properties. By inference,
the raison dtre of the pulp and dentine must be to provide a tooth with
the resilient characteristics necessary for withstanding masticatory load.
Note that the tooth is considered the hardest structure in the body and
referred to as a non-compliant environment from a fluid dynamics perspective. Yet, from a mechanical perspective, dentine can flex at a microstrain
level, detectable by sensitive strain gauges. This microscopic deformation
of the tooth under occlusal load must, by the principle of homeostatic
mechanisms, be detectable by proprioceptors in the pulp; however, direct
evidence for the existence of proprioceptors in the pulp is absent. The
presence of A fibres, which serve a proprioceptive function, offers an
attractive, if partial, explanation for the apparently greater susceptibility
of pulpless teeth to fracture.
Defence reactions are essential for the survival of the pulp. The most
obvious and widely described defence reactions include: the initial inflammatory response in the pulp; blockage of the involved dentinal tubules by
large molecular substances in the transudate; the sclerosis of the dentinal
tubules by mineral deposition and formation of peritubular dentine; and,
finally, the laying down of secondary and tertiary dentine (Fig. 2.1).
The pulpdentine complex has been thought of as a sensory organ that
warns against developing disease (e.g. caries or other forms of surface
tooth tissue loss) by eliciting pain. In this role, the warning system is not
effective given the proportion of teeth whose pulps become irreversibly
inflamed apparently without prior pain. The recently exposed dentine may
become sensitive over a few days but, thereafter, as the pulp recovers, the
sensitivity too would subside.
The first line of sensory defence involves stimulation of the lowthreshold cutaneous-type A nerve fibres, responsible for the sensation of
the characteristic sharp, lancinating dentinal pain elicited by stimulating
dentine by probing, air blast, hyperosmotic fluids, extreme temperatures
or occlusal loading (in the cracked tooth syndrome). Inflammation in the

vicinity of the exposed tubules reduces their threshold and leads to hyperalgesia or hypersensitivity. In addition, it also allows stimulation of the
higher threshold C fibres that are responsible for the deep-seated, less
localized, duller, throbbing pain associated with pulpitis. Stimulation of
proprioceptive A nerve fibres may forewarn the owner of impending
overloading of the tooth.
In addition to sensory defences, the inflammatory response of the pulp
contributes to recruitment of the full array of non-specific and specific
immunological responses (see Chapter 3). This system protects the pulpal
soft tissue against external molecular or microbial assault. An extremely
important function of the pulpdentine complex, which often works simultaneously with inflammation, is secondary (reactionary) or tertiary (reparative) dentine formation (Fig. 2.2) together with dentinal tubule sclerosis
(calcification) (Fig. 2.3) to block off further ingress of noxious factors. It
is likely that severe inflammation may interfere with the dentinal response
by disturbing the odontoblastic function.
Reparative processes within the pulpdentine complex mimic developmental processes. During tooth formation, molecular signals (growth
factors) between epithelial and mesenchymal cells control the induction
of odontoblast differentiation. The growth factors have a profound effect
on various cellular activities and are found throughout the body. A subclass
of these molecules, called the transforming growth factor-beta (TGF-)
family, is responsible for signalling odontoblast differentiation. The differentiated odontoblasts synthesize and secrete the TGF-s together with
other growth factors and sequester them into the dentine matrix, which
then becomes calcified. The subsequent dissolution of the dentine matrix
as a result of caries, tooth surface loss or restorative procedures releases
these molecules again to exert their influence on healing. TGF- molecules
released by mild dentinepulp injury diffuse along a concentration gradient down the dentinal tubules, against the outward flow of dentinal fluid,
and stimulate viable odontoblasts to lay down reactionary dentine. Injury
that is severe enough to damage odontoblasts irreversibly requires their
replacement from the pulpal mesenchymal cell pool. This is a lengthier
and more complex process requiring the migration and differentiation of
new cells followed by secretion of a new matrix. The resulting dentine is,
therefore less well organized and known as reparative dentine (see Fig.
2.1). An important factor that may interfere with the reparative process is
a continuing microbial challenge as a result of coronal leakage, as well as
the toxicity of any restorative material, which would both intensify the
inflammatory process (Fig. 2.4).

CAUSES OF PULP INJURY

The pulp may be injured in a variety of direct and indirect ways. These
are summarized in Table 2.1 (Figs 2.52.7). The pulp may be injured
either by interference with its blood supply or by damage to, or through,
the pulpdentine complex. Direct interference with the blood supply
may occur in acute (impact) or chronic (occlusal) traumatic injuries.
Injuries through the pulpdentine complex may occur by: (1) induction
of cracks or fractures in the tooth structure (through acute or chronic
traumatic injuries); (2) exposure of dentine through natural (attrition,
abfraction), dietary (attrition, erosion), parafunctional (attrition, abrasion),
habitual (attrition, abrasion), pathological (caries, resorption) or iatrogenic

2014 Elsevier Ltd. All rights reserved.

34 Biological and clinical rationale for vital pulp therapy

Fig. 2.1 Primary (A) and irregular

secondary (B) dentine

Fig. 2.2 Secondary dentine

deposition caused by caries and its
treatment

Fig. 2.3 Sclerosed dentinal tubules

(arrowed)

Fig. 2.4 Bacteria in dentinal tubules

(low-power view)

Fig. 2.5 Effect of attrition on dentine

Fig. 2.6 Effect of caries on the pulp: A = inflamed

pulp tissue

(operative or cosmetic) processes; or (3) direct exposure and damage to

the pulp.
Exposure of dentine through any of the mentioned processes would
induce direct physical injury to odontoblastic processes and the cell body.
The disruption would cause the tight junctions between odontoblasts to
separate and be pushed away centrally into the pulp; this would allow
pathways of fluid flow from the pulp to open up. Equally, the pulp would
then be open to stimulation by microbial factors by diffusion, albeit against
the tide of outward flowing dentinal fluid. The degree of such exposure to
flowing or diffusing substances would be dependent on the surface area of
exposure, permeability of the dentinal tubules and depth of dentine damage.
The permeability of dentinal tubules is affected by several factors, including involvement in the carious process, physiological response, pathological response, exposure to acidic oral environment, calcification, and
coverage by restorative materials. The rate of damage to the dentine,
whether carious or non-carious, may also influence the ability of the pulp
to defend itself. The dentine reputedly has a strong buffering capacity
against the inflow of bacterial substances by binding them to the walls of
the tubules.
The physiopathological mechanisms in place, namely, inflammation,
outflow of dentinal fluid, temporary blockage of tubules by protein molecules, followed later by mineralization (dentinal sclerosis) and formation
of reactionary dentine help to close off the avenues of direct pulp exposure,
in time. If such closure were not possible because of a precompromised
pulp unable to generate the reparative response, then the unrelenting inflow

Fig. 2.7 Effect of cavity preparation on the pulp

of microbial stimulants would eventually lead to chronic inflammation and

pulpal demise. The mechanism for such progression may begin with an
accumulation of polymorphonuclear leucocytes (PMNs) at the boundary
of the pulpdentine complex with migration of these phagocytic cells into
the dentinal tubules. Observation of this phenomenon was originally misinterpreted as aspiration of odontoblasts. This would be followed by
migration of macrophages, particularly if an irritating or allergenic material had been deployed.
These would then be followed by the specific response, including T and
B lymphocytes. The chances of pulp necrosis may be enhanced when the
accumulation of PMNs is profuse.
Protection of the pulpdentine complex is, therefore dependent on coverage of the exposed dentine using restorative materials. Such coverage
may simply aim to provide a protective layer or simultaneously replace
the missing tissue, restoring form, function, aesthetics and speech. The
complexity and invasiveness of the restorative procedures may in turn also
induce further damage to the pulp, but this is seen as a necessary calculated
risk in order to afford the final protection, just as it is in any elective
surgery. It is, however, important to appreciate the damaging effect of
restorative procedures. A key initial problem is the manner by which the
material is attached to the tooth structure; whether this involves mechanical or chemical retention, each has its advantages and disadvantages.
The relative importance of the different factors causing pulp injury,
when restorative procedures are employed, has been debated at length and
the emphasis has changed from one set of factors to another. In the 1950s

Biological and clinical rationale for vital pulp therapy 35

Fig. 2.8 Migration of

PMNs into the tubules
as a result of injury

Table 2.1 Pulp injury

Relation to treatment

Damaging agent

Studies

Preoperative factors

Cervical exposed
dentine (genetically
determined)
Tooth surface loss
(acquired) erosion
Attrition
Abrasion
Abfraction

Ten Cate 1994

Caries

Brannstrom & Lind 1965

Lundy & Stanley 1969

Tronstad & Langeland 1971
Meister etal. 1980
Rosenberg 1981
Stanley etal. 1983
Reeves & Stanley 1966
Massler 1967
Langeland 1987

Trauma

Andreasen & Andreasen 1994

Tooth subluxation or
avulsion
Tooth fracture
Enamel
Dentine pulp exposure
Periodontal disease

Seltzer etal. 1963

Mazur etal. 1964
Rubach & Mitchell 1965
Bender & Seltzer 1972
Langeland etal. 1974
Czarnecki & Schilder 1979
Dongari & Lambrianidis 1988

Intraoperative factors

Tooth preparation

Marsland & Shovelton 1957

Intracoronal

Shovelton & Marsland 1958

Extracoronal

Langeland 1959

Iatrogenic pulp
exposure

Hartnett & Smith 1961

Morrant & Kramer 1963

Fig. 2.9 Direct injury to odontoblasts

Hamilton & Kramer 1967

Marsland & Shovelton 1970
Morrant 1977
Turner etal. 1989
Ohshima 1990

Postoperative factors

Other restorative
procedures
Local anaesthesia

Langeland & Langeland 1965

Pin placement

Cotton & Siegel 1978

Cavity cleaning

Spangberg etal. 1982

Impression taking

Kim etal. 1984

Temporization

Plamondon etal. 1990

Electrosurgery

Nixon etal. 1993

Orthodontics

Odor etal. 1994

Restorative materials

Cox 1987

Dentine liners

Cox etal. 1987

Temporary materials

Qvist 1993

Permanent materials

Jontell etal. 1995

Katsuno etal. 1995
Gwinnett & Tay 1998
Smith etal. 2002

Microbial microleakage
Any preoperative factor

Brannstrom & Nyborg 1971

Suzuki etal. 1973

Vojinovic etal. 1973

Bergenholtz etal. 1982
Browne & Tobias 1986
Mejare etal. 1987

and 1960s, the effect of restorative procedures and toxic restorative materials (silicate and zinc phosphate restorative materials) was uppermost in
the minds of researchers. Controlled animal and human histological studies
at the end of the 1960s and early 1970s revealed that pulp injury caused
by restorative procedures and toxic restorative materials was reversible

provided that microbial leakage at the interface between restorative material and dentine was controlled. Even exposed pulps dressed with such
materials healed over time, provided that persistent injury, due to microbial
microleakage was eliminated, which in these studies, was often achieved
with a barrier of zinc oxide/eugenol cement. There is evidence, however,
that resin particles propelled into the pulp may induce a foreign body
response. They may also interfere with the immune defence of the pulp
and weaken its potential to defend against bacterial challenge.
Current understanding of the complex interplay between size of cavity,
remaining dentine thickness (see Figs 2.6, 2.7), restorative material, microbial leakage and pulp inflammation, remains hazy, but a large part may be
attributed to the presence of bacteria in the cavity (Qvist etal., 1989). The
degree of injury to the pulp and its ability to survive is dictated in large
part by the amount of remaining dentine, viable odontoblasts, and integrity
of the neuroinflammatory and immune responses. It is important to preserve as much dentine as possible as it provides a natural buffer to further
injury. Cutting deeper cavities or crown preparations increases the number
of dentinal tubules involved, reduces the survival of odontoblasts and
increases the degree of pulp inflammation and migration of PMNs into the
tubules (Fig. 2.8). The injury to the pulp is probably due to a combination
of direct injury to odontoblasts (Fig. 2.9) and the pulp by dehydration, heat
generation (Fig. 2.10), and microbial and chemical factors reaching the
pulp (Fig. 2.11). Heat generation may be influenced by bur type (diamond
or tungsten, large or small), rotation speed (type of hand-piece), duration
and nature of bur contact (intermittent or continuous, high or low interfacial pressure, bur stalling), cutting technique (slot versus surface removal),
vibration and adequacy of coolant spray. Although it is difficult to quantify
the threshold of dentine thickness critical to pulp survival, less than
0.25mm results in severe inflammation. Additionally, teeth with cavities

36 Biological and clinical rationale for vital pulp therapy

Fig. 2.10 Incandescence caused by

dry cutting of dentine

Fig. 2.11 Bacteria (a) lining the surface of cut dentine (high-power view), (b) in dentinal
tubules

Fig. 2.13 Localized pulp

inflammation

Fig. 2.12 Microleakage under (a) well-filled and (b) poorly-filled restorations

contaminated by microbial leakage have even more severe pulp

inflammation.
Restorations fail and are associated with postoperative complications,
most frequently as a result of the effects of microbial microleakage (Fig.
2.12). The postoperative complications include:

dentine hypersensitivity
marginal staining
restoration corrosion or degradation
secondary caries
pulp inflammation and death.
Microbial leakage is enhanced in larger cavities where there is a greater
marginal interface exposed to the oral environment. There is also a greater
potential for tooth deformation under load, causing increased strain at the
marginal junction and making breakdown in the marginal integrity between
restoration and cavity, more likely. The choice of restorative material also
influences the degree of microbial leakage. Zinc oxide/eugenol is the most
effective material for preventing microbial leakage, although resinmodified glass ionomer cements may also be useful in this regard. Enamelbonded or dentine-bonded composites, counterintuitively do not always
perform well in preventing microbial leakage; a distinction should be made
between bonding and a microbial seal. Bonded restorations are rarely
sealed along their entire boundary at placement because of factors, such
as material properties, manipulation variables and setting-related dimensional changes. Furthermore, in function, the restoration may lose bonding
integrity due to mechanical, chemical and thermal stresses and strains, all
of which could facilitate nano- or microleakage.

Factors, such as restorative material, cavity dimensions and design,

acid-etching and microbial leakage all influence the degree of pulp inflammation. A complex interplay between these variables leads to damage of
the pulp. The emphasis on microbial leakage in no way reduces the potential role of restorative procedures and materials in the demise of the pulp.
In clinical practice, teeth undergoing treatment may have a history of
previous treatment and, therefore, pulp inflammation, which may go undiagnosed if asymptomatic. It is, therefore, entirely possible that restorative
intervention, however minimal, superimposed upon pre-existing pulp
inflammation or fibrosis may be sufficient to tip the balance and cause its
apparent sudden death, necrosis, infection and symptoms.
Open dentinal tubules may provide a persistent pathway for bacteria and
their products leading to persistent chronic inflammation of the pulp and
ultimately to its demise. Open dentinal tubules associated with a healthy
pulp do, however, offer some resistance to bacterial invasion compared to
those in a non-vital pulp. The period of time it may take for the pulp to
die has not been defined but, depending on the initial condition, nature of
the continuing stimulus, and the pulp response, it may sometimes take
many months, if not years. In contrast, the clinical impression can be that
the transition from pulpitis to apical periodontitis may take place over a
matter of days. In such cases, it is likely that asymptomatic pulpitis was
incumbent for an indeterminate period beforehand.

SEVERE INFLAMMATORY AND DEGENERATIVE CHANGES

IN THE PULP

SPREAD OF PULPAL INFLAMMATION

If a localized zone of dentinal tubules remains patent following odontoblast injury, only the associated portion of the pulp will be inflamed (Fig.
2.13). The process of inflammation spread from this localized site to the

Biological and clinical rationale for vital pulp therapy 37

Fig. 2.14 Severe inflammation

affecting most of the pulp

Fig. 2.15 (a) Pulp chamber containing vital pulp tissue; (b) radiograph of the
same tooth, showing periapical area around palatal root before opening into
the pulp

Fig. 2.16 (a) Longitudinal section of tooth, showing a large round

stone in the pulp chamber; (b) calcified stone in the pulp chamber

rest of the pulp is not fully understood. It is presumably related to the

ability of the pulp to close off dentinal tubules by the action of replacement
odontoblasts from undifferentiated mesenchymal cells. If this fails to wall
off the source of inflammation, then it would become persistent and
chronic. It can be envisaged that the greater the number of adjacent dentinal tubules involved and the greater the degree of odontoblast injury, the
larger the volume of pulp tissue affected by inflammation. The localized
response may or may not progress to more severe inflammation depending
on stemming of the provoking factors. Progression of the inflammation
may produce a range of histological pictures, including areas of chronic
inflammation coexisting with microabscesses, gross PMN accumulation
and partial necrosis (Fig. 2.14). Unfortunately, all these histological pictures of pulp disease have a poor correlation with clinical signs and symptoms; in 50% of cases, the pulp remains asymptomatic. This makes clinical
diagnosis of the state of the pulp extremely difficult as the tissues are
hidden from direct view and examination. Adding to the complexity of
this diverse picture is the finding that, in some cases (usually young
patients), even in the presence of vital healthy pulp tissue in the roots
(Fig. 2.15a), there may be radiographic evidence of periapical change
(Fig. 2.15b) associated with coronal pulp inflammation. A reasonably clear
distinction between different states of the pulp can only be made between
vital (albeit inflamed) and completely necrotic pulps using currently available pulp tests.
Under the specific condition of traumatic impact injuries, sudden severance of the blood supply can result in total necrosis of the pulp without
any intervening infection, inflammation or subsequent radiographic periapical change. Such change would then only become evident in the event

of subsequent infection of the necrotic pulp. Such pulps have been shown
to remain uninfected for up to 6 years.

DYSTROPHIC PULP CALCIFICATION

A common finding in the pulp in all age groups is the presence of dystrophic calcification or pulp stones. These are more common in teeth with
diseased pulps but may also be found in unerupted teeth. The precise
stimulus for calcification is unknown but may be presumed to be mediated
via the mechanisms stimulated by growth factors and leading to odontogenesis from mesenchymal cells. A recent theory suggests a role for
nanobacteria or particles but this remains far from widely accepted so far.
There are two types of calcifications; those which are smooth and rounded
are formed by concentric laminations and found commonly in the coronal
pulp (Fig. 2.16a), whereas the irregular calcifications without laminations
are found more commonly in the radicular pulp (Fig. 2.17a). These may
sometimes take the shape of rods or leafs. The laminated stones grow in
size by the addition of collagen fibrils to their surface (Fig. 2.16b), whereas
the irregular type of pulp stones form by calcification of pre-existing collagen fibre bundles (Fig. 2.17b). Some regard the calcifications as a dystrophic change, but these calcifications are not always found in association
with degenerative changes. The main clinical significance of pulp calcification lies in the technical difficulty it can cause during root-canal treatment. Sometimes the calcification may be extensive enough to almost
obliterate the pulp space (Fig. 2.18). These changes may make the location
and negotiation of canals difficult. Furthermore, dislodged stones may be
pushed apically to cause a blockage. Irregular calcification in the canal

38 Biological and clinical rationale for vital pulp therapy

Fig. 2.17 (a) Longitudinal section of tooth: note irregular calcification in the
root canal; (b) irregular calcifications in the radicular pulp

Fig. 2.18 (a,b) Examples of almost complete obliteration of pulp space by

calcification

also has the potential to harbour bacteria and make their elimination more
difficult.

PRINCIPLES OF PULP DISEASE PREVENTION

AND TREATMENT
It may be concluded from the foregoing that the fundamental principle of
pulp disease prevention is prevention of exposure of dentine, minimal
removal of this precious tissue and prevention of access of the underlying
pulp tissue to direct or indirect injury. More particularly, persistent microbial assault is to be avoided. Approaches to prevent caries are well known,
including prevention of occlusal caries by using fissure sealants, fluoride
delivered through various means, control of the frequency of intake and
residence of refined carbohydrates in the mouth and plaque control. These
approaches have had qualified success because of issues of patient
compliance.
Despite such efforts and even if they were completely effective, it is
evident that physiological and pathological conditions, as well as unpredictable life events, would not allow prevention of exposure of dentine for
very long. The increasingly longer life spans conferred by protected
western lifestyles, along with the inevitable wear and tear of teeth, are
likely sooner or later to lead to exposed dentine and an increase in the
prevalence and incidence of pulpal and periapical disease. Teeth, it seems,
are not designed to meet the demands of parafunction precipitated by
stressful modern lifestyles, nor are they designed to withstand the onslaught
of acidic foods, drinks and regurgitation precipitated by poor feeding
habits and other gastrointestinal problems. It is true that ancient man also

suffered from attrition albeit more due to function than parafunction,

however, by all accounts theirs was a shorter life span. Tooth surface
loss has become an endemic problem in modern society (prevalence
was 15% in 2009) but it is also coupled with much longer life spans.
This will therefore create a challenge for the dental profession in the
future (The UK Information Centre For Health And Social Care. Adult
Dental Health Survey 2009; http://www.hscic.gov.uk/pubs/dentalsurveyfull
report09 Accessed June 2013).
Coverage of exposed dentine with restorative materials, as a principle
of treatment, either with or without bonding, has failed because no material
seems capable of establishing and maintaining a permanent bond for the
life of the tooth. It is fortunate that the innate healing mechanisms of the
pulpdentine complex have evolved to prevail over most of the compromising conditions, under which teeth are placed during their life spans.
Instead, the principle of prevention and treatment will, in the future,
need to focus on finding effective ways to control microbial colonization
of tooth surfaces and ingress to the pulp. This will need to be coupled with
an understanding of the natural innate defence mechanisms inherent in the
pulp better to harness them to manage incipient disease. This also means
the discovery of better and more effective ways to detect pulpal disease at
an early stage. Tooth integrity must be preserved through conservative
management of any dental disease. By the same token, the epidemic of
contemporary cosmetic dentistry must be resisted or else more conservative means found to meet the demand for preconceived and standardized
aesthetic dental form.
Developments in conservative management of caries have taken us
away from the rigid adoption of Blacks principles of cavity preparation,
which having served the populations well for their time, have been succeeded by new cavity design principles. These are predicated upon a better
understanding of the natural history of caries, its biology, tooth biomechanics and properties of dental materials. Two main approaches have been
tried; the first involves an adaptation of fissure sealing for caries treatment
(as opposed to prevention); and the second, the so-called Atraumatic
Restorative Technique. The aim of placing sealants over caries therapeutically is to arrest active non-cavitated lesions. Previous studies found that
caries beneath the sealant did not progress as long as the sealant was intact.
The number and viability of microorganisms in infected dentine were also
found to reduce significantly when there was no communication with the
oral environment. Atraumatic restorative treatment has been actively promoted by the World Health Organization as a viable approach to meet the
need for treatment of dental caries in underserved populations that mainly
receive extractions when seeking dental care. Atraumatic restorative treatment uses manual excavation of dental caries without the need for anaesthesia and the use of expensive equipment and restores the cavity with
glass ionomer cement that bonds to the tooth structure and releases fluoride
to stimulate remineralization.

RATIONALE FOR VITAL PULP THERAPY

When prevention and conservative management have failed to protect
teeth and the dentine surface begins to encroach on the pulp, means need
to be found to protect or regenerate the pulpdentine complex. Procedures
designed to preserve or regenerate the pulpdentine complex of compromised teeth have been labelled, indirect pulp capping, direct pulp capping
and pulpotomy. To this traditional list may be added the new category of
regenerative pulp therapy and perhaps even regenerative tooth replacement in the future. The rationale behind and consequences of these procedures should be properly understood before they are used.
A potentially compromised pulp may present itself in a variety of ways.
The pulp may be breached or nearly breached because of caries, tooth

Biological and clinical rationale for vital pulp therapy 39

Fig. 2.19 Necrotic/inflamed pulp

below pulp exposure

surface loss, acute traumatic injury or cavity preparation. In each case, the
operator has to estimate the pre-existing state of the pulp, the extent of
pulp injury and the degree of microbial contamination. In the case of an
acute or chronic (tooth surface loss) traumatic injury, the hard tissue wound
is clearly seen and its history will reveal the extent of damage at the
surface. The nature of the acute injury will give an indication of the probable damage to the pulp and its chances of success. When dealing with a
deep carious lesion, the picture is less clear as the extent of the carious
lesion in its proximity to the pulp will not be obvious. Its acute or chronic
nature will provide some insight into the degree of pulp injury as judged
by loss of odontoblasts and inflammation. Estimation of the degree of
damage is made by a number of clinical assessments. The first assessment
is to judge the histological state of the pulp. This judgement is made on
the history of pain, examination findings, pulp tests and radiographs. The
poor correlation between the histopathology of the pulp and clinical signs
and symptoms leaves the operator with an educated guess. Despite this, it
has often been stated that teeth exhibiting no history of pain or signs of
periapical disease and a positive response to pulp tests stand a good chance
of success following vital pulpal therapy. Conversely, teeth exhibiting
severe throbbing, spontaneous pain, made worse by hot stimuli and keeping
the patient awake may not fare well using this approach. The second
assessment is to estimate the proximity of the carious lesion to the pulp
and, lastly, to guess the extent to which the superficial pulp may be necrotic
and contaminated by bacteria (Fig. 2.19).
The aim of the treatment is to remove as much of the infected hard or
soft tissue as possible and to restore the tooth with a bacteria-tight restoration in order to preserve the health of the residual pulp tissue, leaving it
inflammation-free.
The differences between the procedures labelled indirect pulp capping,
direct pulp capping and pulpotomy reside mainly in the depth and extent
of injury to the pulp and, consequently, the burden of recovery. Each more
radical procedure confers greater damage on the residual pulp calling upon
higher tissue regeneration demands for recovery. In the case of the indirect
pulp cap, by definition, the dentine should be intact, even if it is thin. There
may be damage to the odontoblasts but the potential for recovery of the
pulpdentine complex should be the highest. In the case of the vital pulp
therapies, the essential dentine barrier is missing, so the emphasis is on an
adequately healthy, albeit inflamed pulp, to regenerate the dentine barrier
through stimulation and differentiation of pulp stem cells to secrete and
mineralize a new functional tertiary dentine layer. In successful cases, the
newly formed pulpdentine complex may be almost indistinguishable
from the remaining dentine (Fig. 2.20). If the pulp is too inflamed or
fibrotic, there may be insufficient capacity to regenerate, in which attempts

Fig. 2.20 A pulpotomized tooth with

almost normal looking odontoblastic
layer and relatively uninflamed pulp.
Note the inclusions in the dentine
coronal to the pulpotomy

at repair may create a calcific barrier but may not possess the structural
integrity or full defensive ability of a normal pulpdentine complex. Such
deficient barriers may eventually succumb to the effects of microbial colonization, whereas a fully functional pulpdentine complex would eventually lead to an inflammation-free pulp. Judging the outcome (regeneration/
repair/non-healing) is somewhat subjective, with opinions varying about
the amount of time given from 6 weeks to 6 months.

REGENERATIVE PULP THERAPY

This is a relatively newly tried approach with a limited evidence-base. It
is supported only by case reports/series, many of which have involved
mandibular premolars devitalized by occlusal wear or breach of a dens
evaginatus, leaving the root incompletely formed. The cases involved have
periapical lesions and sometimes even suppuration. The proposed management consists of conventional access under rubber dam isolation, flushing
of the root canal using a dilute sodium hypochlorite solution, followed by
dressing with a mixture of antibiotic (ciprofloxacin, metronidazole, minocycline) or calcium hydroxide paste within the coronal half to threequarters of the canal. The latter helps to control the infection without
damaging any mesenchymal stem cells in the periapical tissues containing
the residue of the formative dental papilla. Once the infection is controlled,
the paste is removed and the canal debrided. Bleeding is then induced by
over-instrumentation of the periapical tissues or the residual dental papilla,
to encourage the influx of stem/mesenchymal cells. The tooth is then
dressed with mineral trioxide aggregate (MTA) over the blood clot and
permanently restored. Follow up of such cases has demonstrated resolution
of the periapical lesion, thickening of the root walls internally, as well as
continued root growth with evidence of continued deposition of hard tissue
within the root. However, the outcome of continued root development is
not as predictable as increased thickening of the canal walls. Crown discoloration produced by the minocycline is an undesirable outcome. Histology on dog teeth undergoing this procedure suggests that, in some cases,
the new tissue is dentine-like and, in other cases, it is cementum-like with
the invasion of bone and periodontal ligament into the root canal. The latter
are not pulp parenchymal tissues, suggesting that the outcome is not
always tissue regeneration but wound repair.

ASSESSMENT OF SUCCESS OF VITAL PULP

THERAPY PROCEDURES
All cases of vital pulp therapy should be followed up to determine outcome.
An initial assessment at between 6 and 12 weeks is recommended,

40 Biological and clinical rationale for vital pulp therapy

Fig. 2.21 Calcific bridge

formation

Fig. 2.23 (a) Complete root formation following pulpotomy; (b) elective
devitalization following completion of root formation

Fig. 2.22 (a,b) Root formation continues after successful pulpotomy

followed by 6- and 12-monthly reviews. At each review, a history of

symptoms is obtained and an examination carried out to assess tenderness
to palpation of adjacent soft tissues, tenderness to pressure and percussion
of the tooth, signs of radiographic pulpal and periapical changes and
responses to pulp tests. However, pulp tests may not be as fruitful in pulpotomized teeth. In the case of pulp capping and pulpotomy, additional
tests include checking the presence and integrity of the calcific barrier
(Fig. 2.21) radiographically and by removal of the dressing and direct
probing. Although an initial examination at 6 weeks has been suggested,
this can be modified by the radiographic assessment. If there is no evidence
of a complete bridge formation, the treatment is considered to be a failure
and conventional root canal treatment must be considered. In addition, in
the case of incompletely formed roots, there should be radiographic evidence of progressing root formation (Fig. 2.22). Once root formation is
complete, some believe that it is desirable to carry out root-canal treatment
in order to avoid the complications of continued calcification of the rootcanal system, which may render the procedure more difficult at a later
stage (Fig. 2.23). This is not, however, a universally accepted axiom and
many consider that the residual pulp would be healthy (see Fig. 2.20) and
should only be removed if restorative requirements for restorative retention dictate so.

PROBABILITY OF SUCCESS OF VITAL PULP

THERAPY PROCEDURES

CONSERVATIVE MANAGEMENT OF CARIES

Fissure sealing of occlusal caries
The approach of sealing occlusal caries appears to be at least partially
successful; a recent study (Bakhshandeh etal., 2011) reporting that 7.4%

of sealants for occlusal caries were partially or totally lost and 7.5% of
those sealants retained had caries progression underneath.

Atraumatic restorative therapy (ART)

According to a recent meta-analysis (de Amorim etal., 2011), the pooled
survival rates of single-surface ART restorations using high-viscosity glass
ionomer in permanent teeth were 85% (95% CI: 77%, 91%) and 80% (95%
CI: 76%, 83%) over the first 3 and 5 years, respectively. The pooled oneyear survival rate for multiple-surface restorations was 80% (95% CI:
76%, 83%).

Indirect pulp capping (one-step versus

step-wise excavation)
A clinical trial (Bjorndal etal., 2010) including only adult permanent teeth
reported pulpal exposure to be a complication during the final excavation
in 18% of cases, and 74% of carious teeth undergoing a step-wise excavation procedure remained vital and free of periapical disease at one year
postoperatively. The age of patients, presence of preoperative pain and
pulpal exposure during excavation were significant prognostic factors.

Direct pulp capping

A systematic review (Aguilar & Linsuwanont, 2011), including 10 studies
published between 1971 and 2010, reported the pooled success rates of
direct pulp capping using calcium hydroxide or MTA as the capping material in permanent teeth with cariously exposed pulps to be as follows: 88%
at 6 months to 1 year, 95% at 12 years, 88% at 23 years, and 73% at 3
years or more, postoperatively. MTA was found to be superior to calcium
hydroxide and teeth with immature apices were associated with significantly more successful outcomes.

Pulpotomy
A systematic review (Aguilar & Linsuwanont, 2011) reported that partial
(six studies) or full (seven studies) pulpotomies using calcium hydroxide
or MTA in permanent teeth with carious pulpal exposure achieved a more
predictable outcome than direct pulp capping, and sustained high pooled
success rates: 9899%; 9399%, respectively. The outcome was not influenced by the capping material or the maturity of the root apex.

Biological and clinical rationale for vital pulp therapy 41

FACTORS AFFECTING OUTCOME OF VITAL

PULP THERAPY
The most important factors affecting the outcome of vital pulp therapy are:
the maturity of the root apex, pre-existing health of the pulp; adequate
removal of infected hard or soft tissues; careful operative technique to
avoid damage to residual pulp tissues; and elimination of microbial leakage
around the final restoration. It can be difficult to gauge the health of the
residual pulp as it is a matter of subjective assessment and relies on experience in pulp diagnosis. The degree of pulp bleeding upon exposure is a
more reliable tool to judge the status of the pulp than the preoperative
clinical signs and symptoms. Continued bleeding after 10 minutes, even
after rinsing with sodium hypochlorite solution, may suggest that the
residual pulp was still heavily inflamed and a complete pulpectomy may
be a more effective treatment modality. Removal of infected tissue is a
matter of subjective experience but may be aided by various dyes. The
final factor is reliant upon the correct choice of restorative material and its
adequate manipulation to prevent leakage.
Factors, such as age and health of the patient, size and nature (carious
or traumatic) of pulp exposure, and its duration of exposure to the oral
environment (up to 48 hours) do not in themselves compromise outcomes
of vital pulp therapy.

FUTURE APPROACHES TO PULP REGENERATION AND

VITAL PULP THERAPY
Innovation should by definition recognize the flaws and potential in current
approaches. It is evident that high success rates can be achieved in vital
pulp therapy but that predictability is uncertain because of flaws in the
manner in which the main predictors can be judged clinically. The main
predictors are: (1) the preoperative health of the pulp; (2) elimination of
source of inflammation; (3) treatment to provide the optimal conditions
for healing and tissue regeneration; (4) exclusion of future microbial microleakage. Innovation should therefore focus on ways to enhance predictability and operator performance in each of these areas. That is, it is
necessary to have better methods for judging the health of the remaining
pulp, that infection can be eliminated or controlled predictably, that a more
biologically based and predictable means of ensuring healing and regeneration is found, and that bacterial microleakage can be more predictably
excluded.
It has been suggested that extension of adhesive dentistry to pulp
capping may be one innovation but, while short-term studies show reasonable early tissue responses, this approach does not actually deal with the
main areas for improvement cited above. Given the extensive clinical data
currently available for the conventional approaches, described above, it is
premature to abandon these procedures in favour of such new methods
that, as yet, have little evidence to support them.
Another putative innovation is the use of MTA (Fig. 2.24) as a pulp
capping agent given its biocompatibility with pulpal and periapical tissues.
While the evidence for pulpal healing of healthy pulp tissue is good, this
approach again fails to address the key innovation parameters. It may
perhaps facilitate better healing but this seems fortuitous rather than by
design.
A promising approach to engineering more effective healing and regeneration would be to adopt biomimetic approaches that recruit natural
growth factors and stem cells to stimulate regeneration and healing
with the use of scaffolds as necessary. These approaches may be used to
regenerate both the pulp and the pulpdentine complex. Potential regenerative endodontic techniques, which have been investigated include: root
canal regeneration via blood clotting; postnatal stem cell therapy; pulp

Fig. 2.24 Mineral trioxide aggregate

(MTA)

implantation; scaffold implantation; injectable scaffold delivery; threedimensional cell printing; and gene delivery.
The ultimate would be the in vitro growth of teeth and their implantation
into the mouth to order, however, this seems decades away.
REFERENCES AND FURTHER READING
Aguilar, P., Linsuwanont, P., 2011. Vital pulp therapy in vital permanent teeth with
cariously exposed pulp: a systematic review. J Endod 37 (5), 581587.
Andreasen, J.O., Andreasen, F.M., 1994. Text book and colour atlas of traumatic injuries
to the teeth, 3rd ed. Mosby, Munksgaard, Denmark.
Bakhshandeh, A., Qvist, V., Ekstrand, K.R., 2011. Sealing occlusal caries lesions in
adults referred for restorative treatment: 2-3 years of follow-up. Clin Oral Investig 16
(2), 521529.
Banchs, F., Trope, M., 2004. Revascularization of immature permanent teeth with apical
periodontitis: new treatment protocol? J Endod 30, 196200.
Barnes, D.E., 1996. Foreword: Proceedings of the International Association of Dental
Research Symposium on Minimal Intervention Techniques for Dental Caries. J Public
Health Dent 56 (3 Spec No), 131.
Baume, L.J., Holz, J., 1981. Long term clinical assessment of direct pulp capping. Int
Dent J 31, 251260.
Bender, I.B., Seltzer, S., 1972. The effect of periodontal disease on the pulp. Oral Surg
33, 458474.
Bergenholtz, G., 2000. Evidence for bacterial causation of adverse pulpal responses in
resin-based dental restorations. Crit Rev Oral Biol Med 11 (4), 467480.
Bergenholtz, G., Cox, C.F., Loesche, W.J., et al., 1982. Bacterial leakage around dental
restorations: its effect on the dental pulp. J Oral Pathol 11 (6), 439450.
Bjrndal, L., Reit, C., Bruun, G., et al., 2010. Treatment of deep caries lesions in adults:
randomized clinical trials comparing stepwise vs. direct complete excavation, and
direct pulp capping vs. partial pulpotomy. Eur J Oral Sci 118 (3), 290297.
Brannstrom, M., Lind, P.O., 1965. Pulpal response to early dental caries. J Dent Res 44,
10451050.
Brannstrom, M., Nyborg, H., 1971. The presence of bacteria in cavities filled with
silicate cement and composite resin materials. Swed Dent J 64, 149155.
Brannstrom, M., Nyborg, H., 1977. Pulpal reaction to polycarboxylate and zinc
phosphate cements used with inlays in deep cavity preparations. J Am Dent Assoc 94,
308310.
Browne, R.M., Tobias, R.S., 1986. Microbial microleakage and pulpal inflammation: a
review. Endod Dent Traumatol 2, 177183.
Byers, M.R., Taylor, P.E., Khayat, B.G., et al., 1990. Effects of injury and inflammation
on pulpal and periapical nerves. J Endod 16, 7884.
Byers, M.R., Swift, M.L., Wheeler, E.F., 1992. Reaction of sensory nerves to dental
restorative procedures. Proc Finn Dent Soc 88 (Suppl. 1), 7382.
Cotton, W.R., Siegel, R.L., 1978. Human pulpal response to citric acid cavity cleanser.
J Am Dent Assoc 96, 639644.
Cox, C.F., 1987. Biocompatibility of dental materials in the absence of bacterial
infection. Oper Dent 12 (4), 146152.
Cox, C.F., 1994. Evaluation and treatment of bacterial microleakage. Am J Dent 7,
293295.
Cox, C.F., Suzuki, S., 1994. Re-evaluating pulp protection: calcium hydroxide liners vs
cohesive hybridization. J Am Dent Assoc 125, 823831.
Cox, C.F., Keall, C.L., Ostro, E., et al., 1987. Biocompatibility of surface sealed dental
materials against exposed pulps. J Prosthet Dent 57 (1), 18.
Cvek, M., 1978. A clinical report on partial pulpotomy and capping with calcium
hydroxide in permanent incisors with complicated crown fracture. J Endod 4,
232237.
Czarnecki, R.T., Schilder, H., 1979. A histological evaluation of the human pulp in teeth
with varying degrees of periodontal disease. J Endod 5, 242253.
de Amorim, R.G., Leal, S.C., Frencken, J.E., 2012. Survival of atraumatic restorative
treatment (ART) sealants and restorations: a meta-analysis. Clin Oral Investig 16 (2),
429441.
Dongari, A., Lambrianidis, T., 1988. Periodontally derived pulpal lesions. Endod Dent
Traumatol 4, 4954.
Felton, D., Bergenholtz, G., Cox, C.F., 1989. Inhibition of bacterial growth under
composite restorations following gluma pretreatment. J Dent Res 68 (3), 491495.

42 Biological and clinical rationale for vital pulp therapy

Fuller, E., Steele, J., Watt, R., et al., 2011. Oral health and function a report from The
Adult Dental Health Survey 2009. The information centre for health and social care.
http://www.hscic.gov.uk/pubs/dentalsurveyfullreport09 (accessed June 2013).
Gwinnett, A.J., Tay, F., 1998. Early and intermediate time response of the dental pulp to
an acid etch technique in vivo. Am J Dent 11, S35S44.
Hamilton, A.I., Kramer, I.R.H., 1967. Cavity preparation with and without waterspray.
Br Dent J 123, 281285.
Handelman, S.L., Leverett, D.H., Solomon, E.S., et al., 1982. Use of adhesive sealants
over occlusal carious lesions: radiographic evaluation. Community Dent Oral
Epidemiol 9 (6), 256259.
Handelman, S.L., 1982. Effect of sealant placement on occlusal caries progression. Clin
Prev Dent 4 (5), 1116.
Handelman, S.L., Washburn, F., Wopperer, P., 1976. Two-year report of sealant effect on
bacteria in dental caries. J Am Dent Assoc 93, 967970.
Hartnett, J.E., Smith, W.F., 1961. The production of heat in the dental pulp by use of the
air turbine. J Am Dent Assoc 63, 210214.
Haskell, E.W., Stanley, H.R., Chellemi, J., et al., 1978. Direct pulp capping treatment: a
long-term follow-up. J Am Dent Assoc 97, 607612.
Horsted, P., Sondergaard, B., Thylstrup, A., et al., 1985. A retrospective study of direct
pulp capping with calcium hydroxide compounds. Endod Dent Traumatol 1, 2934.
Iways, S., Ikawa, M., Kubota, M., 2001. Revascularization of an immature permanent
tooth with apical periodontitis and sinus tract. Dent Traumatol 17, 185187.
Jontell, M., Hanks, C.T., Bratel, J., et al., 1995. Effects of unpolymerized resin
components on the function of accessory cells derived from the rat incisor pulp.
J Dent Res 74 (5), 11621167.
Katsuno, K., Manabe, A., Itoh, K., et al., 1995. A delayed hypersensitivity reaction to
dentine primer in the guinea-pig. J Dent 23 (5), 295299.
Kidd, E.A., Fejerskov, O., 2008. The control of disease progression: Non-operative
treatment. In: Fejerskov, O., Kidd, E., Nyvad, B., Baelum, V., (Eds.), Dental caries:
the disease and its clinical management, 2nd ed. Blackwell Munksgaard Ltd, San
Francisco, pp. 252255.
Kim, S., Edwall, L., Trowbridge, H., et al., 1984. Effects of local anaesthetics on pulpal
blood flow in dogs. J Dent Res 63, 650652.
Kramer, I.R.H., 1959. Pulp changes of non-bacterial origin. Int Dent J 9, 435450.
Langeland, K., 1959. Histologic evaluation of pulp reactions to operative procedures.
Oral Surg Oral Med Oral Pathol 12, 12351248.
Langeland, K., 1961. Effect of various procedures on the human dental pulp. Oral Surg
Oral Med Oral Pathol 14, 210233.
Langeland, K., 1987. Tissue response to dental caries. Endod Dent Traumatol 3,
149171.
Langeland, K., Langeland, L.K., 1965. Pulpal reactions to crown preparations,
impression, temporary crown fixation and permanent cementation. J Prosthet Dent 15,
129142.
Langeland, K., Rodrigues, H., Dowden, W., 1974. Periodontal disease, bacteria and
pulpal histopathology. Oral Surg 37, 252270.
Lundy, T., Stanley, H.R., 1969. Correlation of pulpal histopathology and clinical
symptoms in human teeth subjected to experimental irritation. Oral Surg Oral Med
Oral Pathol 27 (2), 187201.
Marsland, E.A., Shovelton, D.S., 1957. The effect of cavity preparation on the human
dental pulp. Br Dent J 102 (6), 213222.
Marsland, E.A., Shovelton, D.S., 1970. Repair in the human dental pulp following
cavity preparation. Arch Oral Biol 15, 411423.
Massler, M., 1967. Pulpal reaction to dental caries. Int Dent J 17, 441460.
Mazur, B., Kaplowitz, B., Massler, M., 1964. Influence of periodontal disease on the
dental pulp. Oral Surg 17, 592603.
Meister, F., Brown, R.J., Gerstein, H., 1980. Endodontic involvement resulting from
dental abrasion or erosion. J Am Dent Assoc 101, 651653.
Mejare, B., Mejare, I., Edwardsson, S., 1979. Bacteria beneath composite resotorations
a culturing and histological study. Acta Odontol Scand 37, 267275.
Mejare, I., Mejare, B., Edwardson, S., 1987. Effect of a tight seal on survival of bacteria
in saliva-contaminated cavities filled with composite resin. Endod Dent Traumatol 3,
69.
Mejare, I., Cvek, M., 1993. Partial pulpotomy in young permanent teeth with deep
carious lesions. Endod Dent Traumatol 9, 238242.
Morrant, G.A., 1977. Dental instrumentation and pulpal injury: Part 1. J Br Endod Soc
10, 38; Part 2. J Br Endod Soc 10, 5562.
Morrant, G.A., Kramer, I.R.H., 1963. The response of the human pulp to cavity
preparations using turbine handpieces. Br Dent J 115, 99110.
Murray, P.E., Lumley, P.J., Smith, A.J., 2002a. Preserving the vital pulp in operative
dentistry: 2. Guidelines for successful restoration of unexposed dentinal lesions. Dent
Update 29, 127135.
Murray, P.E., Lumley, P.J., Smith, A.J., 2002b. Preserving the vital pulp in operative
dentistry: 3. thickness of remaining cavity dentine as a key mediator of pulpal injury
and repair responses. Dent Update 29, 172179.

Murray, P.E., Lumley, P.J., Hafez, A.A., et al., 2002c. Preserving the vital pulp in
operative dentistry: 4. Factors influencing successful pulp capping. Dent Update 29,
225234.
Nair, P.N.R., Schroeder, H.E., 1995. Number and size spectra of non-myelinated axons
of human premolars. Anat Embryol 192, 3541.
Nixon, C.E., Saviano, J.A., King, G.J., et al., 1993. Histomorphometric study of dental
pulp during orthodontic tooth movement. J Endod 19, 1316.
Odor, T.M., Pitt Ford, T.R., McDonald, F., 1994. Effect of inferior alveolar nerve block
anaesthesia on the lower teeth. Endod Dent Traumatol 10, 144148.
Ohshima, H., 1990. Ultrastructural changes in odontoblasts and pulp capillaries
following cavity preparation in rat molars. Arch Histol Cytol 53 (4), 423438.
Phantumvanit, P., Songpaisan, Y., Pilot, T., et al., 1996. Atraumatic restorative treatment
(ART): a three-year community field trial in Thailand survival of one-surface
restorations in the permanent dentition. J Public Health Dent 56 (3), 141145.
Pissiotis, E., Spngberg, L.S., 1994. Dentin permeability to bacterial proteins in vitro. J
Endod 20 (3), 118122.
Plamondon, T.Y., Walton, R., Graham, C., et al., 1990. Pulp response to the combined
effects of cavity preparation and periodontal ligament infection. Oper Dent 18, 8693.
Qvist, V., Stoltze, K., Qvist, J., 1989. Human pulp reactions to resin restorations
performed with different acid-etch restorative procedures. Acta Odontol Scand 47 (5),
253263.
Qvist, V., 1993. Resin restorations: leakage, bacteria, pulp. Endod Dent Traumatol 9,
127152.
Rakich, D.R., Wataha, J.C., Lefebvre, C.A., et al., 1999. Effect of dentin bonding agents
on the secretion of inflammatory mediators from macrophages. J Endod 25 (2),
114117.
Reeves, R., Stanley, H.R., 1966. The relationship of bacterial penetration and pulpal
pathosis in carious teeth. Oral Surg 22 (1), 5965.
Rosenberg, P.A., 1981. Occlusion, the dental pulp, and endodontic treatment. Dent Clin
North Am 25, 423437.
Rubach, W.C., Mitchell, D.F., 1965. Periodontal disease, accessory canals and pulp
pathosis. J Periodontol 36, 3438.
Rykke, M., 1992. Dental materials for posterior restorations. Endod Dent Traumatol 8,
139148.
Santini, A., 1983. Assessment of the pulpotomy technique in human first permanent
mandibular molars. Br Dent J 155, 151154.
Seltzer, S., Bender, I.D., Ziontz, M., 1963. The interrelationship of pulp and periodontal
disease. Oral Surg 16, 289301.
Shovelton, D.S., 1976. Pulp Protection. J Br Endod Soc 9, 57.
Shovelton, D.S., Marsland, E.A., 1958. A further investigation of the effect of cavity
preparation on the human dental pulp. Br Dent J 103, 1627.
Shovelton, D.S., Friend, L.A., Kirk, E.E.J., et al., 1971. The efficacy of pulp capping
materials a comparative trial. Br Dent J 130, 385391.
Smith, A.J., Murray, P.E., Lumley, P.J., 2002. Preserving the vital pulp in operative
dentistry: 1. A biological approach. Dent Update 29, 6469.
Spangberg, L.S., Robertson, P.B., Levy, B.M., 1982. Pulp effects of electrosurgery
involving based and unbased cervical amalgam restorations. Oral Surg 59 (6),
678685.
Stanley, H.R., 1996. Trashing the dental literature misleading the general practitioners.
A point of view. Guest editorial. J Dent Res 75 (9), 16241626.
Stanley, H.R., Pereira, J.C., Spiegel, E., et al., 1983. The detection and prevalence of
reactive and physiology sclerotic dentine, reparative dentine and dead tracts beneath
various types of dental lesions according to tooth surface and age. J Pathol 12,
257289.
Suzuki, M., Goto, G., Jordan, R.E., 1973. Pulpal response to pin placement. J Am Dent
Assoc 87, 636640.
Ten Cate, A.R., 1994. Oral histology development, structure and function, 4th ed.
Mosby, St Louis.
Tronstad, L., Langeland, K., 1971. Effect of attrition on subjacent dentin and pulp.
J Dent Res 51, 1730.
Trowbridge, H.O., 1981. Pathogenesis of pulpitis resulting from dental caries. J Endod
7, 5260.
Turner, D.F., Marfurt, C.F., Sattelberg, C., 1989. Demonstration of physiological barrier
between pulpal odotoblasts and its perturbation following routine restorative
procedures: a horse-radish tracing study in the rat. J Dent Res 68, 12621268.
Vant Spijker, A., Rodriguez, J.M., Kreulen, C.M., et al., 2009. Prevalence of tooth wear
in adults. Int J Prosthodont 22 (1), 3542.
Vojinovic, O., Nyborg, H., Brannstrom, M., 1973. Acid treatment of cavities under resin
fillings. Bacterial growth in dentinal tubules and pulpal reactions. J Dent Res 52 (6),
11891193.
Zeng, J., Yang, F., Zhang, W., et al., 2011. Association between dental pulp stones and
calcifying nanoparticles. Int J Nanomedicine 6, 109118.