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Mechanisms of Antimicrobial Activity of Calcium Hydroxide A Critical Review IEJ 1999
Mechanisms of Antimicrobial Activity of Calcium Hydroxide A Critical Review IEJ 1999
q 1999 Blackwell Science Ltd International Endodontic Journal, 32, 361±369, 1999 361
Use of calcium hydroxide in root canal Siqueira & Lopes
362 International Endodontic Journal, 32, 361±369, 1999 q 1999 Blackwell Science Ltd
Siqueira & Lopes Use of calcium hydroxide in root canal
show high solubility and thereby may diffuse more dressing. Apically, the pH of the inner dentine reached
than calcium hydroxide across the culture medium. a plateau of approximately 9.5 after 2 weeks. In the
Both bases have pronounced antibacterial activity outer dentine, although the pH began rising earlier,
(Siqueira et al. 1996b). On the other hand, high the maximum pH level was low, reaching just under 9
solubility and diffusibility increases the cytotoxic effects at 2 weeks. The pH of the cervical inner dentine
of these substances on host cells. Because of the high peaked at 10.8 after 24 h and settled to a stable pH
cytotoxicity of these substances, they are not indicated value of just above 10. The pH of the cervical outer
for use in endodontic practice. dentine reached over 9 at 2 weeks. These results
Although hydroxyl ions possess antibacterial effects, revealed that a dressing for 1 week with calcium
rather high pH values are required to destroy microor- hydroxide raised the pH of the inner dentine to ap-
ganisms. Killing of bacteria by calcium hydroxide will proximately 9.0.
depend on the availability of hydroxyl ions in solution, In certain conditions, such pH levels in dentine may
which is higher where the paste is applied. Calcium allow the survival or growth of some bacterial strains.
hydroxide exerts antibacterial effects in the root canal Bacteria vary in their pH tolerance ranges and most
as long as they retain a very high pH. If calcium grow well within a range of 6±9 pH (Padan et al.
hydroxide needs to diffuse to tissues and the hydroxyl 1981). Some strains of Escherichia coli, Proteus vulgaris,
concentration is decreased as a result of the action of Enterobacter aerogenes and Pseudomonas aeruginosa can
buffering systems (bicarbonate and phosphate), acids, survive in pH 8 or 9 (Atlas 1997). These bacterial
proteins and carbon dioxide, its antibacterial effective- species have been occasionally isolated from infected
ness may be reduced or impeded (Siqueira et al. 1998, root canals, usually causing secondary infections
Siqueira & Uzeda 1998). (Haapasalo et al. 1983, Tronstad 1992, Siren et al.
Bacteria inside dentinal tubules may constitute an 1997). Certain bacteria, such as some enterococci,
important reservoir from which root canal infection tolerate very high pH values, varying from 9 to 11.
or reinfection may occur during and after endodontic Fungi generally also exhibit a wide pH range, growing
treatment (Oguntebi 1994). Occasionally, these within a range of 5±9 pH (Atlas 1997). Strains of
remaining bacteria may cause a persistent infection Prevotella intermedia, Fusobacterium nucleatum and Por-
that jeopardizes the outcome of endodontic therapy. phyromonas gingivalis may show stable growth in
Bacteria located inside dentinal tubules are protected alkaline pH values (approximately 8.0±8.3) (Marsh
from the effects of host defence cells and molecules, et al. 1993).
systemically administered antibiotics, and chemome- The pH of the medium exerts a drastic selective
chanical preparation. Therefore, treatment strategies pressure, and only those microorganisms with
that are directed toward the elimination of tubule adaptative mechanisms are able to proliferate. Most
infection are necessary and must include proteins and other biologically important molecules
medicaments that penetrate dentinal tubules and kill have a narrow pH range of optimum activity and/or
bacteria. stability, which turns around neutrality. Bacterial
For calcium hydroxide to act effectively as an tolerance to pH changes may be because of activation
intracanal dressing, the hydroxyl ions must be able to of specific proton pumps, specific enzymatic systems
diffuse through dentine and pulpal tissue remnants. and/or buffering devices, which help to keep the
Studies have revealed that hydroxyl ions derived from internal pH practically constant (Padan et al. 1981). In
a calcium hydroxide medication do diffuse through addition to these mechanisms, some bacterial products
root dentine. Tronstad et al. (1981) reported that the generated during growth may help bacteria to
pH of the monkey dentine was elevated after neutralize the environmental pH.
intracanal medication with calcium hydroxide for Several studies have attested the inefficacy of
4 weeks. However, the pH values were decreased in calcium hydroxide in eliminating bacterial cells inside
the more distant areas from the root canal. In the root dentinal tubules. Haapasalo & érstavik (1987)
canal, the pH was greater than 12.2; circumjacent reported that a calcium hydroxide paste (Calasept,
dentine, in direct contact with calcium hydroxide, Swedia, Knivsta, Sweden) failed to eliminate, even
showed a pH varying from 8 to 11; and in the most superficially, Enterococcus faecalis in the tubules. Safavi
peripheral dentine, the pH ranged from 7.4 to 9.6. et al. (1990) demonstrated that Enterococcus faecium
Nerwich et al. (1993) investigated pH changes over remained viable in dentinal tubules after relatively
4 weeks, after application of a calcium hydroxide extended periods of calcium hydroxide/saline solution
q 1999 Blackwell Science Ltd International Endodontic Journal, 32, 361±369, 1999 363
Use of calcium hydroxide in root canal Siqueira & Lopes
treatment. érstavik & Haapasalo (1990) observed that these properties, cytotoxicity is limited to the tissue
calcium hydroxide can take up to 10 days to disinfect area in direct contact with calcium hydroxide. On
dentinal tubules infected by facultative bacteria. Heling the other hand, the low solubility and diffusibility of
et al. (1992) have found that calcium hydroxide did calcium hydroxide may make it difficult to reach a
not show any antibacterial activity against E. faecalis rapid and significant increase in the pH to eliminate
inside dentinal tubules, and failed to sterilize the bacteria located within dentinal tubules and enclosed
dentine or prevent secondary infection. Siqueira & in anatomical variations. Likewise, the tissue
Uzeda (1996) demonstrated that calcium hydroxide buffering ability controls pH changes. Because of
associated with saline solution was ineffective in these factors, calcium hydroxide is a slowly working
eliminating E. faecalis and F. nucleatum cells inside antiseptic. Prolonged exposure may allow for
dentinal tubules, even after 1 week of contact. saturation of the dentine and tissue remnants. Theo-
To be effective against bacteria located inside the retically, long-term use of calcium hydroxide may be
dentinal tubules, the hydroxyl ions from calcium necessary to obtain a bacteria-free root canal system.
hydroxide should diffuse into dentine at sufficient However, in most instances, the routine use of an
concentrations. It has been reported that dentine has intracanal medication for a long period does not
buffering ability because of the presence of proton seem to be an acceptable practice in modern
donors, such as H2PO4ÿ , H2CO3, and HCO3ÿ , in the endodontics.
hydrated layer of hydroxyapatite, which furnish The period needed for calcium hydroxide to
additional protons to keep the pH unchanged (Wang optimally disinfect the root canal system is still
& Hume 1988, Nerwich et al. 1993). Therefore, in unknown. Clinical studies using root canal sampling
order to have antibacterial effects within dentinal procedures, have revealed conflicting results. Cvek
tubules, the ionic diffusion of calcium hydroxide et al. (1976) revealed that 90% of the samples taken
should exceed the dentine buffer ability, reaching pH from root canals 3 months after medication with
levels sufficient to destroy bacteria. After short-term calcium hydroxide mixed with Ringer's solution
use of calcium hydroxide, microorganisms are showed no microbial growth. BystroÈm et al. (1985)
probably exposed to lethal levels of hydroxyl ions demonstrated that calcium hydroxide effectively
only at the tubule orifice. eliminated all microorganisms when the medicament
Another factor can also help to explain the inefficacy was maintained for 4 weeks. Reit & DaÂhlen (1988)
of calcium hydroxide in disinfecting dentinal tubules. found that infection persisted in 26% of the canals
The arrangement of the bacterial cells colonizing the after 2 weeks of dressing with calcium hydroxide.
root canal walls can reduce the antibacterial effects of SjoÈgren et al. (1991) have reported that an
calcium hydroxide, since the cells located at the intracanal medication with calcium hydroxide for
periphery of colonies can protect those located more 1 week effectively eliminated bacteria in the root
deeply inside the tubules (Siqueira et al. 1996a, canal in 100% of the cases. érstavik et al. (1991)
Siqueira & Uzeda 1996). observed the persistence of bacteria in 34.8% of the
Bacteria colonizing necrotic tissue in ramifications, root canals after 1 week of dressing. Barbosa et al.
isthmuses and irregularities are also, probably, protected (1997) reported that 12 of 45 cases (26.7%) dressed
from the action of calcium hydroxide, due to pH neutrali- with calcium hydroxide for 1 week yielded positive
zation. Therefore, a short-term dressing with calcium cultures.
hydroxide appears to eliminate mainly bacterial cells in Even cases that yield negative cultures may result in
direct contact with this substance, such as bacteria failure (SjoÈgren 1996, SjoÈgren et al. 1997). This occurs
located in the main root canal or in the circumpulpal because microorganisms may have been present in the
dentine. These areas are also commonly affected by the root canal system and escaped detection in the samples
chemomechanical procedures. that were taken. This can occur for several reasons,
The ability of a medicament to dissolve and diffuse one of which is that bacteria located in isthmuses,
in the root canal system would seem essential for its dentinal tubules and ramifications may have been in-
successful action (érstavik 1997). A saturated accessible to sampling from the main canal. In
aqueous suspension of calcium hydroxide possesses a addition, smear layer and residues of calcium
high pH, which has a great cytotoxic potential. hydroxide pastes in the root canal walls can physically
Nevertheless, this substance owes its biocompatibility limit access to bacteria during sampling procedures.
to its low water solubility and diffusibility. Because of Another reason could be that, since culture has a
364 International Endodontic Journal, 32, 361±369, 1999 q 1999 Blackwell Science Ltd
Siqueira & Lopes Use of calcium hydroxide in root canal
sensitivity to detect approximately 103±104 cells in a solubility and ideally they must not change the pH of
sample (Zambon & Haraszthy 1995), it is possible that, calcium hydroxide significantly.
at time of sampling, too few cells were present in the Most of the substances used as a vehicle for
root canal to be recovered for this method. calcium hydroxide do not have significant antibacter-
Although enterococci are not normally present or ial activities. They include distilled water, saline
are present in very low numbers in untreated cases solution and glycerine. Other substances, such as
(BystroÈm et al. 1985, Sundqvist et al. 1998), studies camphorated paramonochlorophenol (CMCP) and me-
have suggested that they are important agents in tacresylacetate, are known to possess this property.
endodontic failure. Molander et al. (1998) examined Frank (1966) recommended mixing calcium
the microbiological status of 100 root-filled teeth hydroxide with CMCP in apexification procedures.
with periradicular lesions. Facultative anaerobes pre- Some authors criticized this by considering it
dominated amongst the isolates, corresponding to unnecessary to add antimicrobial agents to calcium
69% of the identified strains. Enterococci were found hydroxide, especially those that have been shown to
in 32% of the investigated teeth. Under similar be tissue irritating (Cvek et al. 1976, Anthony et al.
conditions, MoÈ ller (1966) and Sundqvist et al. (1998) 1982).
isolated E. faecalis from 29% and 38% of canals that Recently, renewed interest has been generated
had recoverable microorganisms, respectively. It has regarding this association because of the relative ineffi-
been observed that calcium hydroxide dressing is ciency of calcium hydroxide against some microorgan-
ineffective against enterococci (Stevens & Grossman isms, such as E. faecalis. Although CMCP has
1983, BystroÈm et al. 1985, Haapasalo & érstavik pronounced in vitro antibacterial effects on anaerobic
1987, Siqueira & Uzeda 1996). Therefore, the bacteria (Ohara et al. 1993, Siqueira et al. 1996a),
frequent isolation of enterococci questions the studies have revealed that calcium hydroxide is
routine use of calcium hydroxide as an intracanal superior to it against this set of microorganisms
medication (Molander et al. 1998). (BystroÈm et al. 1985, Stuart et al. 1991, Georgopoulou
Bacteria may survive after intracanal medication for et al. 1993). However, CMCP has been reported to be
several reasons. First, bacterial strains present in the more effective in eliminating enterococci than calcium
root canal infection may be intrinsically resistant to hydroxide (Stevens & Grossman 1983, Haapasalo &
the medicament. Secondly, bacterial cells may be érstavik 1987, Siqueira et al. 1996a).
enclosed within anatomical variations inaccessible to As discussed previously, calcium hydroxide effects
the medicament. Thirdly, the medicament may be are highly dependent on the availability of hydroxyl
neutralized by tissue components and by bacterial cells ions in solution. Culture media, tissue fluids and
or products, losing its antibacterial effects. Fourthly, dentine possess buffer substances that can prevent
medicaments may remain in the root canal system for calcium hydroxide activity by causing a pH drop.
insufficient time to reach and kill bacterial cells. Siqueira & Uzeda (1996) verified that calcium
Finally, bacteria may alter their pattern of gene hydroxide/saline solution paste was ineffective in
expression after changes in the environmental eliminating E. faecalis and F. nucleatum from dentinal
conditions. This alteration may allow them to survive tubules even after 1 week of exposure. In contrast, a
in unfavourable environments. calcium hydroxide/CMCP/glycerine paste effectively
Good clinical results have been attributed to the use killed bacteria in the tubules after 1 h exposure, except
of calcium hydroxide as an intracanal medicament for E. faecalis that required 1 day of exposure. Studies
(Heithersay 1975, Tronstad 1992). Nonetheless, the using an agar diffusion test have revealed that the
antibacterial activity of calcium hydroxide is still con- calcium hydroxide/CMCP paste had pronounced anti-
troversial and it is not clear whether the benefits of bacterial activity against facultative and anaerobic
this substance are based solely upon superior antibac- bacteria, which was superior to pastes containing
terial activity (Seltzer 1988). calcium hydroxide in inert substances (Difiore et al.
1983, Siqueira et al. 1996b, 1997b, Siqueira & Uzeda
1997).
Influence of the vehicle on the
Siqueira & Uzeda (1998) evaluated the influence of
antimicrobial activity
three different vehicles on the antibacterial activity of
A plethora of substances have been used as vehicles for calcium hydroxide against four bacterial species
calcium hydroxide. Vehicles have different water commonly found in endodontic infections, using a
q 1999 Blackwell Science Ltd International Endodontic Journal, 32, 361±369, 1999 365
Use of calcium hydroxide in root canal Siqueira & Lopes
modification of the broth dilution method. Calcium 1. the small concentration of released paramono-
hydroxide/CMCP/glycerine paste rapidly killed bacteria. chlorophenol (MCP). Calcium hydroxide plus CMCP
Other calcium hydroxide pastes also killed bacteria, but yields calcium paramonochlorophenolate, which is a
required more time. These findings indicate that CMCP weak salt that progressively releases MCP and
increased the antibacterial effectiveness of the calcium hydroxyl ions to the surrounding medium (Anthony
hydroxide paste. et al. 1982). It is well known that a substance may
A number of phenolic derivatives, such as CMCP, have either beneficial or deleterious effects, depending
camphorated phenol, thymol and eugenol have been on its concentration. The low release of MCP from the
extensively used in dentistry for many years. paste might not be sufficient to have cytotoxic effects.
Phenolic compounds possess strong antibacterial 2. the denaturing effect of calcium hydroxide on
properties and halogenation intensifies their antimi- connective tissue, which may prevent the tissue
crobial activities. Phenol is believed to act by penetration of MCP, reducing its toxicity (Siqueira
disrupting lipid-containing bacterial membranes, 1997).
resulting in leakage of cellular contents. At higher 3. the fact that the effect on periradicular tissues is
concentrations, these compounds act by precipitating probably associated with the antimicrobial effect
the cytoplasmic cell proteins (O'Connor & Rubino of the paste, which allows natural healing to
1991). At lower concentrations, phenolic compounds occur without persistent infectious irritation. If
inactivate essential enzyme systems and may also the wound area is free of bacteria when the
cause bacterial cell wall lysis (Hugo & Russel 1998). transitory chemical irritation occurs, there is no
Some properties of phenolic compounds, such as low reason to believe that tissue repair would not
surface tension (Naumovich 1963) and lipid take place as the initial chemical irritant
solubility (O'Connor & Rubino 1991), confer a high decreases in intensity.
penetrability and spreading of the medicament. Thus,
Since released MCP is sufficient to exercise excellent
the calcium hydroxide/CMCP mixture possesses a
antibacterial activity, and because MCP does not
high radius of action, eliminating bacteria located in
possess selective toxicity to microorganisms, it is quite
regions more distant from the vicinity where the
acceptable that the second and/or the third hypothesis
paste was applied (Siqueira 1997).
are correct.
Alencar et al. (1997) have determined the presence
of MCP in calcium hydroxide/MCP paste after its use
for 2, 4, 7, and 14 days as intracanal dressing in dogs.
Physical barrier
Their results showed a MCP loss of approximately 50%
in the dressing after 48 h, with no further significant In addition to eliminating remaining viable bacteria
loss after longer periods. This finding indicates that the unaffected by the chemomechanical preparation of the
effects of MCP may persist in the root canal for at least root canal, intracanal medicaments have been
14 days. advocated for other reasons. They should also act as a
Endodontic infections are polymicrobial and no physicochemical barrier, precluding the proliferation of
medicament is effective against all the bacteria found residual microorganisms and preventing the reinfection
in infected root canals. Combination of two of the root canal by bacteria from the oral cavity
medicaments may produce additive or synergistic (Siqueira 1997).
effects. Evidence suggests that the association of Intracanal medicaments may prevent the
calcium hydroxide with CMCP has a broader antibac- penetration of bacteria from saliva in the root canal
terial spectrum, a higher radius of antibacterial action, basically in two ways. First, medicaments possessing
and kills bacteria faster than mixtures of calcium antibacterial properties may act as a chemical barrier
hydroxide with inert vehicles. Therefore, CMCP cannot against leakage by killing bacteria, thereby preventing
be considered a vehicle for calcium hydroxide, but an their ingress into the root canal. The root canal system
additional medicament. can become recontaminated when the number of
Although CMCP has strong cytotoxic activities bacterial cells exceeds the antibacterial activity of the
(Spangberg et al. 1979), studies have reported a medicament. In addition, saliva dilutes the medicament
favorable tissue response to calcium hydroxide/CMCP and may neutralize its effects, allowing the invasion of
mixtures (Torneck et al. 1973, Holland et al. 1979). microorganisms. Secondly, medicaments that fill the
This association probably owes its biocompatibility to: entire length of the root canal act as a physical barrier
366 International Endodontic Journal, 32, 361±369, 1999 q 1999 Blackwell Science Ltd
Siqueira & Lopes Use of calcium hydroxide in root canal
q 1999 Blackwell Science Ltd International Endodontic Journal, 32, 361±369, 1999 367
Use of calcium hydroxide in root canal Siqueira & Lopes
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