Smear Layer

You might also like

Download as pdf or txt
Download as pdf or txt
You are on page 1of 9

oo ORAL SURGERY

Vol. 94 No. 6 December 2002

o ORAL MEDICINE
ORAL PATHOLOGY

REVIEW ARTICLE

Clinical implications of the smear layer in endodontics:


A review
Mahmoud Torabinejad, DMD, MSD, PhD,a Robert Handysides, DDS,b
Abbas Ali Khademi, DMD, MS,c and Leif K. Bakland, DDS,d Loma Linda, Calif
LOMA LINDA UNIVERSITY

It has been recognized for many years that root canal instrumentation produces a smear layer that covers the
surfaces of prepared canal walls. This layer contains inorganic and organic substances such as fragments of
odontoblastic processes and necrotic debris. There is a lack of agreement regarding the effect of the smear layer on the
quality of instrumentation and obturation, but the smear layer itself may be infected and may protect the bacteria
within the dentinal tubules. Various methods have been used to remove the smear layer. Conflicting results have been
obtained from numerous in vitro studies regarding the significance of the presence or the removal of the smear layer.
(Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2002;94:658-66)

Studies have shown that current methods of cleaning evidence regarding clinical implications of the smear
and shaping root canals produce a smear layer that layer in endodontics.
covers the instrumented walls.1-5 This layer contains
inorganic and organic substances that include frag- BACTERIAL PRESENCE
ments of odontoblastic processes, microorganisms, and When pathologic changes occur in the dental pulp,
necrotic materials (Fig 1).5 According to Mader et al,3 the root canal system can harbor several species of
the smear layer consists of a superficial layer on the bacteria, their toxins, and byproducts. A number of
surface of the canal wall approximately 1 to 2 ␮m in investigations have shown that pulpal and periradicular
thickness and a deeper layer packed into the dentinal pathoses do not develop without the presence of bac-
tubules to a depth of up to 40 ␮m. The components of teria.6-9 Depending on the stage of pulpal pathosis,
the smear layer can be forced into the dentinal tubules various species of bacteria can be cultured from in-
to varying distances.2,4 This can occur as a result of the fected root canals. These bacteria are predominantly
linear movement and rotation of instruments and be- gram-negative anaerobes8,10,11 that can infect the root
cause of capillary action generated between the dentinal canals by direct pulp exposures (caries or traumatic
injuries) or by coronal microleakage.12-16 Davis et al17
tubules and the smear material.4
have shown that the morphology of root canals is very
The purpose of this article was to review current
complex and that mechanically prepared canals contain
areas not accessible by currently used endodontic in-
a
Professor and Program Director, Department of Endodontics, School struments. Bacteria can be found in all areas of the root
of Dentistry, Loma Linda University. canal system and in the dentinal tubules (Fig 2).18-20
b
Assistant Professor, Department of Endodontics, School of Den-
tistry, Loma Linda University.
c
Professor of Endodontics and Vice President of Academic Affairs,
DENTINAL TUBULES
School of Dentistry, University of Isfehan, Iran. In the root, dentinal tubules extend from the pulp-
d
Professor and Chair, Department of Endodontics, School of Den- predentin junction to the intermediate dentin just inside
tistry, Loma Linda University. the cementum-dentin junction. Dentinal tubules in the
Received for publication Mar 22, 2002; returned for revision May 13,
root run a relatively straight course between the pulp
2002; accepted for publication Jul 9, 2002.
© 2002, Mosby, Inc. and the periphery in contrast to the typical S-shaped
1079-2104/2002/$35.00 ⫹ 0 7/15/128962 contours of the tubules in the tooth crown. They range
doi:10.1067/moe.2002.128962 in size from approximately 1 to 3 ␮m in diameter.21,22

658
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY Torabinejad et al 659
Volume 94, Number 6

Fig 1. The presence of smear layer on the surface of an Fig 2. The presence of several bacteria in a dentinal tubule of
instrumented root canal. Original magnification ⫻5000. a tooth with necrotic pulp. Original magnification ⫻5000.

The density or number of dentinal tubules per square smear layer opened the tubules, allowing bacteria to
millimeter varies from 4900 to 90,000.21 This density colonize in the tubules to a much higher degree
increases in an apical-coronal direction to the root (10-fold) compared with roots with an intact smear
surface and similarly in an external to internal direction layer.
from the root surface. At the cementoenamel junction, Factors such as the number and the type of bacteria,
the number of dentinal tubules has been estimated to be in addition to the length of exposure and the presence or
approximately 15,000 per square millimeter.
absence of smear layer, could influence the depth of
Available evidence shows that bacteria and its by-
penetration of bacteria into the dentinal tubules. Be-
products present in infected root canals may invade the
cause of the difficulties involved in sampling the den-
dentinal tubules.18-20,23-29 Investigators18,19 have re-
tinal tubules, the exact microflora of infected dentinal
ported the presence of bacteria in the dentinal tubules of
infected teeth at approximately half the distance be- tubules is unknown. Ørstavik and Haapasalo26 have
tween the root canal walls and the cementodentinal expressed concern regarding the effect of bacteria in the
junction. Sen et al20 examined 10 extracted human teeth dentinal tubules after inadequate root canal therapy.
with necrotic pulps under a scanning electron micro-
scope and reported bacterial penetration into the den- INTRACANAL MEDICATIONS
tinal tubules up to 150 ␮m in the apical two thirds of The removal of diseased tissue, elimination of bac-
the roots. Horiba et al23 found endotoxin within the teria present in the canals and dentinal tubules, and
dentinal walls of infected root canals. In addition, in prevention of recontamination after treatment are the
vitro studies have shown bacterial penetration into the objectives of endodontic therapy. These objectives are
dentinal tubules in experimentally inoculated root ca-
achieved by thoroughly cleaning, shaping, and disin-
nals.24-26
fecting the root canal system; by sealing the root canals
Siqueira et al27 removed the smear layer in bovine
with a 3-dimensional obturation; and by placing a coro-
teeth and inoculated them with 5 species of bacteria and
nal seal.
Enterococcus faecalis as a control. Their scanning elec-
tron microscope examination showed that all of the test Because of the complexity of root canal systems and
bacteria were able to penetrate into the dentinal tubules the current inability to instrument all aspects of canal
to varying depths. Perez et al28 found a mean penetra- wall surfaces, it is impossible to achieve complete
tion depth of 479 ␮m for Streptococcus sanguis after 28 removal or destruction of all bacteria.31,32 Byström and
days of incubation, with a maximum penetration of 737 Sundqvist31 have shown that residual bacteria in an
␮m. Peters et al29 evaluated the presence, depth of instrumented but unfilled canal can multiply to their
penetration, morphotypes, and the number of colony- original numbers within 2 to 4 days. To prevent recolo-
forming units of bacteria in the root dentin of teeth with nization of the root canals with residual bacteria, some
periapical lesions. They reported the presence of bac- authors recommend the use of intracanal medication
teria in more than half of their samples close to the and, therefore, the completion of treatment of infected
cementum. Drake et al30 showed that removal of the root canals in more than 1 visit.32-34
660 Torabinejad et al ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY
December 2002

Various medicaments have been proposed for disin- math49 examined the antibacterial effect of chlorhexi-
fection of root canals.26,35-37 The traditional phenolic or dine gluconate and sodium hypochlorite on inoculated
fixative agents include camphorated monochlorophenol human teeth in vitro. They reported a reduction in
(CMCP), formocresol, and cresatin. Iodine potassium bacterial counts but not total disinfection of the root
iodide and calcium hydroxide are the main nonphenolic canals.
intracanal medications. These medicaments are potent In an in vivo experiment, Katebzadeh et al50 showed
antibacterial agents under laboratory test conditions; that infected dog teeth that were filled experienced
however, their effectiveness in clinical use is unpredict- treatment failure more frequently than those medicated
able.38 According to some researchers, they also neu- with Ca(OH)2 before obturation. Sjögren et al51 exam-
tralize and render canal tissue remnants inert. Some ined the presence and influence of bacteria on the
medications contain aldehyde derivatives that can be long-term success of root canal therapy. Their results
used to fix fresh tissues for histologic examination; show that 40% of root canals remain infected after
however, they may not effectively fix necrotic or de- instrumentation. In addition, they reported that teeth
composed tissues.35 According to Wesselink et al,39 filled in 1 visit without the use of Ca(OH)2 experienced
fixed tissues are not inert and may become more toxic treatment failure significantly more frequently than
and antigenic after fixation. Intracanal medications those that were medicated for 1 week with Ca(OH)2
have also been used clinically to prevent posttreatment (68% vs 94%). The results of this study corroborate the
pain. Studies have shown, however, that routine use of findings of Byström et al,52 who showed improved
these materials as intracanal medication has no signif- clinical success rates after effective disinfection of root
icant effect on the prevention of pain.40-43 canals.
According to Oguntebi,44 most currently used intra-
canal medicaments have a limited antibacterial spec- Effects of smear layer on penetration of root
trum and antigenic potential. In addition, some of them canal medicaments and sealers into the dentinal
have a limited ability to diffuse into the dentinal tu- tubules
bules. In an in vitro study, Ørstavik and Haapasalo26
showed the importance of removal of the smear layer
Effects of intracanal medications on bacteria in and the presence of patent dental tubules for decreasing
dentinal tubules the time necessary to achieve the disinfecting effect of
After removal of the smear layer, Haapasalo and intracanal medications. Byström and Sundqvist53 have
Ørstavik25 inoculated the bovine incisors with E faeca- also shown that the presence of a smear layer can
lis and found penetration of these bacteria into the inhibit or significantly delay the penetration of antimi-
dentinal tubules up to 1 mm. They demonstrated that crobial agents such as intracanal irrigants and medica-
liquid CMCP completely disinfected the dentinal tu- tions into the dentinal tubules.
bules but that Ca(OH)2 was ineffective. Behnen et al45 Studies54-56 have shown better adhesion of obturation
had better success killing E faecalis with either Pulp- materials to the canal walls after removal of the smear
dent or a 10% solution of Ca(OH)2 than with the layer. Pitt Ford and Roberts57 have suggested that the
traditional thick mixes. The difference might have been failures of glass-ionomer retrograde fillings after apical
attributable to the different viscosity of various types of surgery may result from degradation of the smear layer.
Ca(OH)2 used in this experiment. Heling and Chand- Other investigators58-62 assessed the penetration depth
ler46 also inoculated dentinal tubules of bovine teeth of different sealers, including Tubliseal, AH26, Seala-
with E faecalis and then examined the disinfecting pex, Rosin, Roth’s 811, and CRCS, into the dentinal
effect of various irrigants. They found that none of the tubules. They found the penetration to be 10 to 80 ␮m
test irrigants (chlorhexidine, hydrogen peroxide, so- after removal of the smear layer, whereas no penetra-
dium hypochlorite, EDTA, or their combinations) were tion was observed with the smear layer intact.
totally effective. Siqueira and de Uzeda47 inoculated
bovine dentin cylinders with 1 facultative and 2 obli- MICROLEAKAGE OF ROOT CANAL FILLINGS
gate anaerobic bacteria and examined the disinfecting WITH AND WITHOUT A SMEAR LAYER
effect of Ca(OH)2 mixed with saline solution or CMCP The presence or absence of a smear layer may play
for 1 hour, 1 day, and 1 week. Their results showed that an important role in the adhesiveness of some sealers to
Ca(OH)2 and saline solution were ineffective in disin- the root canal walls. Studies have shown a significant
fecting the dentinal tubules after 1 week of application. increase in adhesive strength and resistance to mic-
In contrast, a mixture of Ca(OH)2 and CMCP resulted roleakage of AH26 sealer when the smear layer was
in complete disinfection of the dentinal tubules in 1 removed.63,64 Gettleman et al63 did not find any changes
day. Jeansonne and White48 and Kuruvilla and Ka- in adhesive strengths when Sultan and Sealapex sealers
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY Torabinejad et al 661
Volume 94, Number 6

were evaluated with or without the smear layer intact. addition, they reported that tetrasodium salt pH-ad-
Several investigators64-70 have shown less dye leakage justed with HCl is less expensive and just as effective
after removal of the smear layer with various obturation as the more commonly used disodium EDTA.
techniques and root canal sealers. Other investigators Aktener and Bilkay83 developed a solution of EDTA
have reported that the removal of the smear layer did and ethylenediamine to work in dual action. Their goal
not have any significant effect on the microleakage of was to see whether a single irrigating solution could be
root canals when various sealers and obturation tech- developed to remove the inorganic and the organic
niques were used.71-75 In contrast to these findings, components of the smear. They found many patent
Timpawat et al76 have reported that removal of the tubules but concluded that more research was needed to
smear layer has adverse effects on the microleakage of determine the efficacy of this combination. Goldberg
filled root canals. These conflicting results might be and Abramovich84 added a quaternary ammonium bro-
attributable to differences in the types of sealer and mide (Cetavlon) to EDTA to reduce its surface tension;
obturation techniques, the means of producing a smear this solution is called EDTAC. This addition increased
layer, and the diversity of bacteria used under various the wetting effect on the canal wall and permitted
laboratory conditions. deeper penetration of the solution into irregularities.
This combination was shown by Goldberg and Spiel-
REMOVAL OF THE SMEAR LAYER berg85 to be very effective in smear layer removal,
Despite the controversy regarding the effect of the reaching its peak effect at 15 minutes and increasing the
smear layer on the quality of instrumentation and ob- diameter of the opened dentinal tubules. Recently, Çalt
turation, several investigators1,77,78 have found that the and Serper86 reported that ethylene glycol-bis (b-ami-
smear layer itself may be infected and may protect the noethyl ether)-N,N,N’, N’-tetraacetic acid was some-
bacteria already present in the dentinal tubules. Be-
what effective in removing the smear layer without
cause of these concerns, one may deem it prudent to
inducing dentinal erosion commonly caused by EDTA
remove the initially created smear layer in infected root
(Fig 3).
canals and to allow penetration of intracanal medica-
Morgan and Baumgartner87 showed that the quantity
tions into the dentinal tubules of these teeth. Efforts to
of smear layer removed by a material is directly related
remove the smear layer have included chemical, me-
to its pH and the time of exposure. Loel58 used a 50%
chanical, and laser means. After disinfection of the root
canal system, one can recreate a new smear layer by citric acid solution to treat canal walls after instrumen-
mechanical filing of the root canal walls. tation and found better penetration of rosin sealer into
the tubules and improved adaptation of gutta-percha
than in untreated canals. Tidmarsh55 and Baumgartner
Chemical removal
et al88 also showed that 50% citric acid is an effective
The components of the smear layer are very small
irrigant to remove the smear layer from the surface of
particles with a large surface-mass ratio, which makes
prepared root canal walls. Wayman et al89 found lactic
them very soluble in acids.5 Because of this character-
acid at 50% concentration was less effective than 50%
istic, acids have been used to remove the smear layer.
citric acid for removal of the smear layer. This might be
McComb and Smith1 were the first investigators to
attributed to the viscosity of lactic acid. They also
show that REDTA (a commercial brand of EDTA) can
remove the smear layer. Goldman et al79 showed that determined that alternating use of 10% citric acid and
when used alone, REDTA removed the inorganic por- 2.5% NaOCl was a very effective method for removing
tion and left an organic layer intact in the tubules. To the smear layer.
remove this organic layer, another solvent is needed. Bitter90 reported that 25% tannic acid was effective
Sodium hypochlorite (NaOCl) has been shown to be in removing the smear layer. Sabbak and Hasanin91
very effective for this purpose. When used alone, refuted these findings and explained that tannic acid
NaOCl can dissolve pulpal remnants and predentin. increased the cross-linking of exposed collagen within
However, many studies have shown its ineffectiveness the smear layer and within the matrix of the underlying
in removing the entire smear layer when used alone. dentin, thus increasing organic cohesion to the tubules.
Goldman et al,79 Yamada et al,80 and Baumgartner and Polyacrylic acid (Durelon liquid and Fuji II liquid) at
Mader81 showed that alternating the use of EDTA and 40% was reported by Berry et al92 to be very effective
NaOCl is an effective method for smear layer removal. for removal of the smear layer. Because of its potency,
O’Connell et al82 compared the ability of various salts the application of polyacrylic acid should not exceed 30
of EDTA to remove the smear layer. They showed that seconds according to the authors’ recommendations.
all salts of EDTA were capable of removing the smear Derivatives of oxine (8-hydroxy-quinoline) were
layer from the coronal two thirds of root canals. In known to possess antiseptic qualities as early as 1895.93
662 Torabinejad et al ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY
December 2002

Fig 3. Erosion of the dentinal tubule after placement of EDTA in the root canal for 5 minutes. Original magnification ⫻5000.

Dequalinium compounds, which belong to this cause enamel and root surface demineralization.99
group, have been widely used in medicine against The surface demineralization of dentin is comparable
infections of bacteria, molds, and fungi.94 Bis-de- with that of citric acid.100 The substantivity of these
qualinium-acetate (BDA) has been shown by Kauf- antibiotics allows them to be absorbed and released
man et al94 and Kaufman95 to remove the smear layer gradually from tooth structures such as dentin and
throughout the canal, even in the apical third. BDA is cementum.100-102
well tolerated by the tissues within the periodontium The ability of the tetracycline family of antibiotics to
and has a low surface tension that allows penetration remove smear layers has also been studied. They have
into spaces that instruments cannot reach.94 BDA is been used to demineralize dentin surfaces, uncover and
also considered less toxic than NaOCl and can be widen the orifices of dentinal tubules, and expose the
used as a root canal dressing. Kaufman and Green- dentin collagen matrix. These effects provide a matrix
berg96 compared Salvizol (a commercial brand of
that stimulates fibroblast attachment and growth. Bark-
0.5% BDA) with 5.25% NaOCl and found both com-
hordar et al103 showed that doxycycline HCl (100 mg/
parable in their ability to remove organic debris, but
mL) is effective in removing the smear layer from the
only Salvizol was able to open dentinal tubules. Berg
surfaces of instrumented canals and root-end cavity
et al97 reported Salvizol to be less effective at open-
ing dentinal tubules than was REDTA. preparations. They speculated that a reservoir of active
Tetracyclines (including tetracycline-HCl, mino- antibacterial agents might be created because doxycy-
cycline, and doxycycline) are broad-spectrum antibi- cline readily attaches to dentin and can be subsequently
otics that are effective against a wide range of mi- released. Haznedaroglu and Ersev104 showed that 1%
croorganisms. Genco et al98 have suggested that tetracycline hydrochloride or 50% citric acid can be
tetracyclines significantly enhance healing after sur- used to remove the smear layer from the surfaces of
gical periodontal therapy. Tetracyclines have many instrumented root canals. Although they reported no
unique properties in addition to their antimicrobial difference between these 2 groups, it appears that the
effect. They have a low pH in concentrated solution tetracycline demineralized less peritubular dentin than
and thus can act as a calcium chelator, and they can did the 50% citric acid.
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY Torabinejad et al 663
Volume 94, Number 6

Ultrasonic removal be the access to small canal spaces with the relatively
Cameron105 produced a debris-free canal with the use large probes that are available for delivery of the laser
of a 3% NaOCl solution combined with ultrasonic beam.
instrumentation for 5 minutes after conventional canal
instrumentation. The mechanism of action for debris
CONCLUSION
removal was described as acoustic streaming by Ahmad
On the basis of the available evidence, it can be
et al.106 Acoustic streaming is maximized when the tips
concluded that current methods of root canal instru-
of the smaller instruments operate at high power and
mentation produce a layer of organic and inorganic
vibrate freely in a solution. Lumley et al107 recom-
material (smear layer) that may also contain bacteria
mended that only size 15 files be used to maximize the
and their byproducts. This layer covers the instru-
microstreaming for removal of debris.
mented walls and may prevent the penetration of int-
Cameron108 showed complete smear removal with
racanal medications into the dentinal tubules and may
4% NaOCl and ultrasonic instrumentation for 2 min-
affect close adaptation between root canal filling mate-
utes. Prati et al109 also achieved smear layer removal
with ultrasonics. Walker and del Rio110,111 in 2 separate rials and the root canal walls.
reports showed no significant difference between tap Considering the aforementioned observations, it
water and NaOCl when used with ultrasonics, but they seems reasonable to suggest that removal of the smear
reported that neither solution used with ultrasonics was layer can result in a more thorough disinfection of the
effective at any level in the canal to remove the smear root canal system and the dentinal tubules, which
layer. Baumgartner and Cuenin112 also observed that would ensure a better adaptation between the obturation
ultrasonically energized NaOCl, even at full strength, materials and the root canal walls. Current methods of
did not remove the smear layer from the root canal smear layer removal include chemical, ultrasonic, and
walls. Guerisoli et al113 evaluated the use of ultrasonics laser techniques—none of which is totally effective or
to remove the smear layer and found it necessary to use has received universal acceptance. Conflicting reports
15% EDTAC with either distilled water or 1% NaOCl exist regarding the removal of the smear layer before
to achieve the desired result. the obturation of root canals. One may deem it prudent,
because of its potential contamination, to remove the
Laser removal smear layer in teeth with infected root canals and allow
penetration of intracanal medications into the dentinal
Takeda et al114,115 found that lasers can be used to
tubules. After disinfection of the root canal system, if
vaporize tissues in the main canal, remove the smear
layer, and eliminate the residual tissue in the apical advised, one may recreate a new smear layer by cir-
portion of the root canals. Several investigators116-118 cumferential hand-filing or the use of rotary instru-
have reported that the effectiveness of lasers depends ments. To effectively disinfect the root canal system, an
on many factors, including the power level, the duration irrigant or an intracanal medication with the following
of exposure, the absorption of light in the tissue, the characteristics should be used:
geometry of the root canal, and the tip-to-target dis- 1. It should be able to completely remove the smear
tance. layer.
Dederich et al116 and Tewfik et al119 used variants of 2. It should be able to disinfect the dentin and its
the neodymium-yttrium-aluminum-garnet laser and re- tubules.
ported a range of findings from no change or disruption 3. It should have sustained antibacterial effect after
of the smear layer to actual melting and recrystalliza- use.
tion of the dentin. This pattern of dentin disruption was 4. It should allow the penetration of antimicrobial
observed in other studies with various lasers, including agents present in the solution into the dentinal
the carbon dioxide laser,117 the argon fluoride excimer tubules.
laser,120 and the argon laser.118,121 Takeda et 5. It should be nonantigenic, nontoxic, and noncarci-
al,114,115,122 using the erbium-yttrium-aluminum-garnet nogenic to tissue cells surrounding the tooth.
(Er:YAG) laser, demonstrated optimal removal of the 6. It should have no adverse effects on the physical
smear layer without the melting, charring, and recrys- properties of exposed dentin.
tallization associated with other laser types. Kimura et 7. It should have no adverse effect on the sealing
al123 demonstrated the removal of the smear layer with ability of filling materials.
an Er:YAG laser as well. Although they showed re- 8. It should not discolor the tooth.
moval of the smear layer, the photomicrograph showed 9. It should have convenient application.
destruction of the peritubular dentin. The main diffi- 10. It should be relatively inexpensive.
culty with laser removal of the smear layer continues to Clinical investigations are needed to determine the
664 Torabinejad et al ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY
December 2002

role of smear layer in the outcome of root canal ther- 24. Akpata ES, Blechman H. Bacterial invasion of pulpal dentin
wall in vitro. J Dent Res 1982;61:435-8.
apy. 25. Haapasalo M, Ørstavik D. In vitro infection and disinfection of
dentinal tubules. J Dent Res 1987;66:1375-9.
26. Ørstavik D, Haapasalo M. Disinfection by endodontic irrigants
REFERENCES and dressings of experimentally infected dentinal tubules.
1. McComb D, Smith DC. A preliminary scanning electron mi- Endod Dent Traumatol 1990;6:142-9.
croscopic study of root canals after endodontic procedures. J 27. Siqueira JF Jr, de Uzeda M, Fonseca MEF. A scanning electron
Endod 1975;1:238-42. microscopic evaluation of in vitro dentinal tubules penetration
2. Moodnik RM, Dorn SO, Feldman MJ, Levey M, Borden BG. by selected anaerobic bacteria. J Endod 1996;22:308-10.
Efficacy of biomechanical instrumentation: a scanning electron 28. Perez F, Rochd T, Lodter J-P, Calas P, Michel G. In vitro study
microscopic study. J Endod 1976;2:261-6. of the penetration of three bacterial strains into root dentin. Oral
3. Mader CL, Baumgartner JC, Peters DD. Scanning electron Surg Oral Med Oral Pathol 1993;76:97-103.
microscopic investigation of the smeared layer on root canal 29. Peters LB, Wesselink PR, Buijs JF, van Winkelhoff AJ. Viable
walls. J Endod 1984;10:477-83. bacteria in root dentinal tubules of teeth with apical periodon-
4. Cengiz T, Aktener BO, Pi’kin B. The effect of dentinal tubule titis. J Endod 2001;27:76-81.
orientation on the removal of smear layer by root canal irrig- 30. Drake DR, Wiemann AH, Rivera EM, Walton RE. Bacterial
ants. A scanning electron microscopic study. Int Endod J 1990; retention in canal walls in vitro: effect of smear layer. J Endod
23:163-171 1994;20:78-82
5. Pashley DH. Smear layer: overview of structure and function. 31. Byström A, Sundqvist G. Bacteriologic evaluation of the effi-
Proc Finn Dent Soc 1992; 88(Suppl l):215-24. cacy of mechanical root canal instrumentation in endodontic
6. Kakehashi S, Stanley HR, Fitzgerald RJ. The effects of surgical therapy. Scand J Dent Res 1981;89:321-8.
exposures of dental pulps in germ-free and conventional labo- 32. Byström A, Claesson R, Sundqvist G. The antibacterial effect of
ratory rats. Oral Surg Oral Med Oral Pathol 1965;20:340-9. camphorated paramonochlorophenol, camphorated phenol and
7. Bergenholtz G. Micro-organisms from necrotic pulp of trauma- calcium hydroxide in the treatment of infected root canals.
tized teeth. Odontol Revy 1974;25:347-58. Endod Dent Traumatol 1985;1:170-5.
8. Sundqvist G. Bacteriological studies of necrotic dental pulps 33. Chong BS, Pitt Ford TR. The role of intracanal medication in
[dissertation]. Umeå University Odontology Dissertation, No 7. root canal treatment. Int Endod J 1992;25:97-106.
University of Umeå, Sweden, 1976. 34. Heithersay GW, Hume WR, Abbot PV. Conventional root canal
9. Möller ÅJR, Fabricius L, Dahlén G, Öhman AE, Heyden G. therapy. II: intracanal medication. In: Harty FJ, editor. End-
Influence on periapical tissues of indigenous oral bacteria and odontics in clinical practice, 3rd ed. London: Wright; 1990.
necrotic pulp tissue in monkeys. Scand J Dent Res 1981;89: p. 162-85.
475-84. 35. Walton RE, Rivera EM. Cleaning and Shaping. In: Walton RE
10. Fabricius L, Dahlén G, Öhman AE, Möller ÅJR. Predominant and Torabinejad M, editors. Principles and practice of endodon-
indigenous oral bacteria isolated from infected root canals after tics, 3rd ed. Philadelphia: W. B. Saunders; 2002. p. 232-3.
varied times of closure. Scand J Dent Res 1982;90:134-44. 36. Spångberg LSW. Cellular reaction to intracoronal medica-
11. Kantz WE, Henry CA. Isolation and classification of anaerobic ments. In Grossman LI, editor. Transactions of the Fifth Inter-
bacteria from intact pulp chambers of non-vital teeth in man. national Conference on Endodontics. University of Pennsylva-
Arch Oral Biol 1974;19:91-96. nia, Philadelphia; 1973. p. 108-23.
12. Swanson K, Madison S. An evaluation of coronal microleakage 37. Masillamoni CRM, Kettering JD, Torabinejad M. The biocom-
in endodontically treated teeth. Part I. Time periods. J Endod patibility of some root canal medicaments and irrigants. Int
1987;13:56-9. Endod J 1981;14:115-20.
13. Madison S, Swanson K, Chiles S. An evaluation of coronal 38. Messer HH, Chen RS. The duration of effectiveness of root
microleakage in endodontically treated teeth. Part II. Sealer canal medicaments. J Endod 1984;10:240-5.
types. J Endod 1987;13:109-12. 39. Wesselink PR, Thoden van Velzen SK, van den Hoof A. The
14. Madison S, Wilcox LR. An evaluation of coronal microleakage tissue reaction to implantation of unfixed and glutaraldehyde
in endodontically treated teeth. Part III. In vivo study. J Endod fixed heterologous tissue. J Endod 1977;3:229-235.
1988;14:455-8. 40. Maddox DL, Walton RE, Davis CO. Incidence of posttreatment
15. Torabinejad M, Ung B, Kettering JD. In vitro bacterial pene- endodontic pain related to medicaments and other factors. J
tration of coronally unsealed endodontically treated teeth. J Endod 1977;3:447-452.
Endod 1990;16:566-9. 41. Kleier DJ, Mullaney TP. Effects of formocresol on posttreat-
16. Magura ME, Kafrawy AH, Brown CE Jr, Newton CW. Human ment pain of endodontic origin in vital molars. J Endod 1980;
saliva coronal microleakage in obturated root canals: an in vitro 6:566-9.
study. J Endod 1991;17:324-31. 42. Torabinejad M, Kettering JD, McGraw JC, Cummings RR,
17. Davis SR, Brayton S, Goldman M. The morphology of the Dwyer TG, Tobias TS. Factors associated with endodontic
prepared root canal: a study utilizing injectable silicone. Oral interappointment emergencies of teeth with necrotic pulps. J
Surg Oral Med Oral Pathol 1972;34:642-8. Endod 1988;14:261-6.
18. Ando N, Hoshino E. Predominant obligate anaerobes invading 43. Trope M. Relationship of intracanal medicaments to endodontic
the deep layers of root canal dentine. Int Endod J 1990;23:20-7. flare-ups. Endod Dent Traumatol 1990;6:226-9.
19. Armitage GC, Ryder MI, Wilcox SE. Cemental changes in teeth 44. Oguntebi BR. Dentine tubule infection and endodontic therapy
with heavily infected root canals. J Endod 1983;9:127-30. implications. Int Endod J 1994;27:218-22.
20. Sen BH, Pi’kin B, Demirci T. Observation of bacteria and fungi 45. Behnen MJ, West LA, Liewehr FR, Buxton TB, McPherson JC.
in infected root canals and dentinal tubules by SEM. Endod Antimicrobial activity of several calcium hydroxide prepara-
Dent Traumatol 1995;11:6-9. tions in root canal dentin. J Endod 2001;27:765-67.
21. Mjör IA, Nordahl I. The density and branching of dentinal 46. Heling I, Chandler NP. Antimicrobial effect of irrigant combi-
tubules in human teeth. Arch Oral Biol 1996;41:401-12. nations within dentinal tubules. Int Endod J 1998;31:8-14.
22. Garberoglio R, Brännström M. Scanning electron microscopic 47. Siqueira JF Jr, de Uzeda M. Disinfection by calcium hydroxide
investigation of human dentinal tubules. Arch Oral Biol 1976; pastes of dentinal tubules infected with two obligate and one
21:355-62. facultative anaerobic bacteria. J Endod 1996;22:674-6.
23. Horiba N, Maekawa Y, Matsumoto T, Nakamura H. A study of 48. Jeansonne MJ, White RR. A comparison of 2.0% chlorhexidine
the distribution of endotoxin in the dentinal wall of infected root gluconate and 5.25% sodium hypochlorite as antimicrobial end-
canals. J Endod 1990;16:331-4. odontic irrigants. J Endod 1994;20:276-8.
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY Torabinejad et al 665
Volume 94, Number 6

49. Kuruvilla JR, Kamath MP. Antimicrobial activity of 2.5% so- smear layer on microbial coronal leakage of gutta-percha root
dium hypochlorite and 0.2% chlorhexidine gluconate separately fillings. Int Endod J 1996;29:242-8.
and combined, as endodontic irrigants. J Endod 1998;24:472-6. 73. Saunders WP, Saunders EM. Influence of smear layer and the
50. Katebzadeh N, Hupp J, Trope M. Histological periapical repair coronal leakage of thermafil and laterally condensed gutta-
after obturation of infected root canals in dogs. J Endod 1999; percha root fillings with a glass ionomer sealer. J Endod 1994;
25:364-8. 20:155-8.
51. Sjögren U, Figdor D, Persson S, Sundqvist G. Influence of 74. Madison S, Krell KV. Comparison of ethylenediamine tetraace-
infection at the time of root filling on the outcome of endodontic tic acid and sodium hypochlorite on the apical seal of endodon-
treatment of teeth with apical periodontitis. Int Endod J 1997; tically treated teeth. J Endod 1984;10:499-503.
30:297-306. 75. Timpawat S, Sripanaratanakul S. Apical sealing ability of glass
52. Byström A, Happonen R-P, Sjögren U, Sundqvist G. Healing of ionomer sealer with and without smear layer. J Endod 1998;24:
periapical lesions of pulpless teeth after endodontic treatment 343-5.
with controlled asepsis. Endod Dent Traumatol 1987;3:58-63. 76. Timpawat S, Vongsavan N, Messer HH. Effect of removal of
53. Byström A, Sundqvist G. The antibacterial action of sodium the smear layer on apical microleakage. J Endod 2001;27:
hypochlorite and EDTA in 60 cases of endodontic therapy. Int 351-3.
Endod J 1985;18:35-40. 77. Brannström M. Smear layer: pathologic and treatment consid-
54. Abramovich A, Goldberg F. The relationship of the root canal erations. Oper Dent 1984;suppl 3:35-42.
sealer to the dentine wall. An in vitro study using scanning 78. Pashley DH. Smear layer: physiological considerations. Oper
electron microscope. J Br Endod Soc 1976;9:81– 6. Dent 1984;suppl 3:13-29.
55. Tidmarsh BG. Acid-cleansed and resin-sealed root canals. J 79. Goldman M, Goldman LB, Cavaleri R, Bogis J, Peck S-L. The
Endod 1978;4:117-21. efficacy of several endodontic irrigating solutions: a scanning
56. White R, Goldman M, Peck S-L. The influence of the smeared electron microscopic study: part 2. J Endod 1982;8:487-92.
layer upon dentinal tubule penetration by plastic filling materi- 80. Yamada RS, Armas A, Goldman M, Peck S-L. A scanning
als. J Endod 1984;10:558-62. electron microscopic comparison of a high volume final flush
57. Pitt Ford TR, Roberts GJ. Tissue response to glass ionomer with several irrigating solutions: part 3. J Endod 1983;9:137-42.
retrograde root fillings. Int Endod J 1990;23:233-8. 81. Baumgartner JC, Mader CL. A scanning electron microscopic
58. Loel DA. Use of acid cleanser in endodontic therapy. J Am evaluation of four root canal irrigation regimens. J Endod
Dent Assoc 1975;90:148-51. 1987;13:147-57.
59. Gutiérrez JH, Herrera VR, Berg EH, Villena F, Jofré A. The 82. O’Connell MS, Morgan LA, Beeler WJ, Baumgartner JC. A
risk of intentional dissolution of the smear layer after mechan- comparative study of smear layer removal using different salts
ical preparation of root canals. Oral Surg Oral Med Oral Pathol of EDTA. J Endod 2000;26:739-43.
1990;70:96-108. 83. Aktener BO, Bilkay U. Smear layer removal with different
concentrations of EDTA-ethylenediamine mixtures. J Endod
60. Pallarés A, Faus V, Glickman GN. The adaptation of mechan-
1993;19:228-31.
ically softened gutta-percha to the canal walls in the presence or
84. Goldberg F, Abramovich A. Analysis of the effect of EDTAC
absence of smear layer: a scanning electron microscopic study.
on the dentinal walls on the root canal. J Endod 1977;3:101-5.
Int Endod J 1995;28:266-9.
85. Goldberg F, Spielberg C. The effect of EDTAC and the varia-
61. Kouvas V, Liolios E, Vassiliadis L, Parissis-Messimeris S,
tion of its working time analyzed with scanning electron mi-
Boutsioukis A. Influence of smear layer depth of penetration of
croscopy. Oral Surg Oral Med Oral Pathol 1982;53:74-7.
three endodontic sealers: an SEM study. Endod Dent Traumatol
86. Çalt S, Serper A. Smear layer removal by EGTA. J Endod
1998;14:191-5. 2000;8:459-61.
62. Gençoǧlu N, Samani S, Günday M. Dentinal wall adaptation of 87. Morgan LA, Baumgartner JC. Demineralization of resected
thermoplasticized gutta-percha in the absence or presence of root-ends with methylene blue dye. Oral Surg Oral Med Oral
smear layer: a scanning electron microscopic study. J Endod Pathol Oral Radiol Endod 1997;84:74-8.
1993;19:558-62. 88. Baumgartner JC, Brown CM, Mader CL, Peters DD, Shulman
63. Gettleman BH, Messer HH, ElDeeb ME. Adhesion of sealer JD. A scanning electron microscopic evaluation of root canal
cements to dentin with and without the smear layer. J Endod debridement using saline, sodium hypochlorite and citric acid. J
1991;17:15-20. Endod 1984;10:525-31.
64. Economides N, Liolios E, Kolokuris I, Beltes P. Long-term 89. Wayman BE, Kopp WM, Pinero GJ, Lazzari EP. Citric and
evaluation of the influence of smear layer removal on the lactic acids as root canal irrigants in vitro. J Endod 1979;5:258-
sealing ability of different sealers. J Endod 1999;25:123-5. 65.
65. Kennedy WA, Walker WA, Gough RW. Smear layer removal 90. Bitter NC. A 25% tannic acid solution as a root canal irrigant
effects on apical leakage. J Endod 1986;12:21-7. cleanser: A scanning electron microscope study. Oral Surg Oral
66. Cergneux M, Ciucchi B, Dietschi JM, Holz J. The influence of Med Oral Pathol 1989;67:333-7.
the smear layer on the sealing ability of canal obturation. Int 91. Sabbak SA, Hassanin MB. A scanning electron microscopic
Endod J 1987;20:228-32. study of tooth surface changes induced by tannic acid. J Pros-
67. Vassiliadis L, Liolios E, Kouvas V, Economides N. Effect of thet Dent 1998;79:169-74.
smear layer on coronal microleakage. Oral Surg Oral Med Oral 92. Berry EA, von der Lehr WN, Herrin HK. Dentin surface treat-
Pathol Oral Radiol Endod 1996;82:315-20. ments for the removal of the smear layer: an SEM study. J Am
68. Taylor JK, Jeansonne BG, Lemon RR. Coronal leakage: effects Dent Assoc 1987;115:65-7.
of smear layer, obturation technique, and sealer. J Endod 1997; 93. Albert A, Margrath D. The choice of a chelating agent for
23:508-12. inactivating trace metals. J Biochem 1947;41:534-43.
69. Karagöz-Küçükay I, Bayirli G. An apical leakage study in the 94. Kaufman AY, Binderman I, Tal M, Gedalia I, Peretz G. New
presence and absence of the smear layer. Int Endod J 1994;27: chemotherapeutic agent for root canal treatment. Oral Surg Oral
87-93. Med Oral Pathol 1978;46:283-95.
70. Saunders WP, Saunders EM. The effect of smear layer upon the 95. Kaufman AY. The use of dequalinium acetate as a disinfectant
coronal leakage of gutta percha root filling and a glass ionomer and chemotherapeutic agent in endodontics. Oral Surg Oral
sealer. Int Endod J 1992;25:245-9. Med Oral Pathol 1981;51:434-41.
71. Evans JT, Simon JHS. Evaluation of the apical seal produced by 96. Kaufman AY, Greenberg I. Comparative study of the configu-
injected thermoplasticized gutta-percha in the absence of smear ration and the cleanliness level of root canals prepared with the
layer and root canal sealer. J Endod 1986;12:101-7. aid of sodium hypochlorite and bis-dequalinium-acetate solu-
72. Chailertvanitkul P, Saunders WP, Mackenzie D. The effect of tions. Oral Surg Oral Med Oral Pathol 1986;62:191-7.
666 Torabinejad et al ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY
December 2002

97. Berg MS, Jacobsen EL, BeGole EA, Remeikis NA. A compar- 113. Guerisoli DMZ, Marchesan MA, Walmsley AD, Lumley PJ,
ison of five irrigating solutions: A scanning electron micro- Pecora JD. Evaluation of smear layer removal by EDTAC and
scopic study. J Endod 1986;12:192-7. sodium hypochlorite with ultrasonic agitation. Int Endod J
98. Genco R, Singh S, Krygier G, Levine M. Use of tetracycline in 2002;35:418-21.
the treatment of adult periodontitis. I. Clinical studies [abstract]. 114. Takeda FH, Harashima T, Kimura Y, Matsumoto K. Efficacy of
J Dent Res 1978;57(A):266;768. Er:YAG laser irradiation in removing debris and smear layer on
99. Björvatn K. Antibiotic compounds and enamel demineraliza- root canal walls. J Endod 1998;24:548-51.
tion. An in vitro study. Acta Odontol Scand 1982;40:341-52. 115. Takeda FH, Harashima T, Kimura Y, Matsumoto K. A com-
100. Wikesjö UME, Baker PJ, Christersson LA, Genco RJ, Lyall parative study of the removal of smear layer by three endodon-
RM, Hic S, et al. A biochemical approach to periodontal re- tic irrigants and two types of laser. Int Endod J 1999;32:32-9.
generation: tetracycline treatment conditions dentin surfaces. J 116. Dederich DN, Zakariasen KL, Tulip J. Scanning electron mi-
Periodontal Res 1986;21:322-9. croscopic analysis of canal wall dentin following neodymium-
101. Baker PJ, Evans RT, Coburn RA, Genco RJ. Tetracycline and yttrium-aluminum-garnet laser irradiation. J Endod 1984;10:
its derivatives strongly bind to and are released from the tooth 428-31.
surface in active form. J Periodontol 1983;54:580-5. 117. Önal B, Ertl T, Siebert G, Müller G. Preliminary report on the
102. Björvatn K, Skaug N, Selvig KA. Tetracycline-impregnated application of pulsed CO2 laser radiation on root canals with
enamel and dentin: duration of antimicrobial capacity. Scand J AgCl fibers: a scanning and transmission electron microscopic
Dent Res 1985;93:192-7.
study. J Endod 1993;19:272-6.
103. Barkhordar RA, Watanabe LG, Marshall GW, Hussain MZ.
118. Moshonov J, Sion A, Kasirer J, Rotstein I, Stabholz A. Effect of
Removal of intracanal smear by doxycycline in vitro. Oral Surg
argon laser irradiation in removing intracanal debris. Oral Surg
Oral Med Oral Pathol Oral Radiol Endod 1997;84:420-3.
Oral Med Oral Pathol Oral Radiol Endod 1995;79:221-5.
104. Haznedaroglu F, Ersev H. Tetracycline HCl solution as a root
canal irrigant. J Endod 2001;27:738-40. 119. Tewfik HM, Pashley DH, Horner JA, Sharawy MM. Structural
105. Cameron JA. The use of ultrasonics in the removal of the smear and functional changes in root dentin following exposure to
layer: a scanning electron microscope study. J Endod 1983; KTP/532 laser. J Endod 1993;19:492-7.
9:289-92. 120. Stabholz A, Neev J, Liaw L-HL, Stabholz A, Khayat A, Tor-
106. Ahmad M, Pitt Ford TR, Crum LA. Ultrasonic debridement of abinejad M. Effect of ArF-193 nm excimer laser on human
root canals: acoustic streaming and its possible role. J Endod dentinal tubules. A scanning electron microscopic study. Oral
1987;13:490-9. Surg Oral Med Oral Pathol Oral Radiol Endod 1993;75:90-4.
107. Lumley PJ, Walmsley AD, Walton RE, Rippin JW. Effect of 121. Harashima T, Takeda FH, Zhang C, Kimura Y, Matsumoto K.
precurving endosonic files on the amount of debris and smear Effect of argon laser irradiation on instrumented root canal
layer remaining in curved root canals. J Endod 1992;18:616-9. walls. Endod Dent Traumatol 1998;14:26-30.
108. Cameron JA. The use of ultrasound for the removal of the smear 122. Takeda FH, Harashima T, Kimura Y, Matsumoto K. Compar-
layer. The effect of sodium hypochlorite concentration: SEM ative study about the removal of smear layer by three types of
study. Aust Dent J 1988;33:193-200. laser devices. J Clin Laser Med Surg 1998;16:117-22.
109. Prati C, Selighini M, Ferrieri P, Mongiorgi R. Scanning electron 123. Kimura Y, Yonaga K, Yokoyama K, Kinoshita J, Ogata Y,
microscopic evaluation of different endodontic procedures on Matsumoto K. Root surface temperature increase during Er:
dentin morphology of human teeth. J Endod 1994;20:174-9. YAG laser irradiation of root canals. J Endod 2002;28:76-8.
110. Walker TL, del Rio CE. Histological evaluation of ultrasonic
and sonic instrumentation of curved root canals. J Endod 1989;
15:49-59. Reprint requests:
111. Walker TL, del Rio CE. Histological evaluation of ultrasonic
Mahmoud Torabinejad, DMD, MSD, PhD
debridement comparing sodium hypochlorite and water. J
Endod 1991;17:66-71. Department of Endodontics
112. Baumgartner JC, Cuenin PR. Efficacy of several concentrations School of Dentistry
of sodium hypochlorite for root canal irrigation. J Endod 1992; Loma Linda University
18:605-12. Loma Linda, CA 92350

You might also like