o o o

Vol. 94 No. 6 December 2002

ORAL SURGERY 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. Conicting results have been obtained from numerous in vitro studies regarding the signicance 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 and shaping root canals produce a smear layer that covers the instrumented walls.1-5 This layer contains inorganic and organic substances that include fragments of odontoblastic processes, microorganisms, and necrotic materials (Fig 1).5 According to Mader et al,3 the smear layer consists of a supercial layer on the surface of the canal wall approximately 1 to 2 m in thickness and a deeper layer packed into the dentinal tubules to a depth of up to 40 m. The components of the smear layer can be forced into the dentinal tubules to varying distances.2,4 This can occur as a result of the linear movement and rotation of instruments and because of capillary action generated between the dentinal tubules and the smear material.4 The purpose of this article was to review current
Professor and Program Director, Department of Endodontics, School of Dentistry, Loma Linda University. b Assistant Professor, Department of Endodontics, School of Dentistry, Loma Linda University. c Professor of Endodontics and Vice President of Academic Affairs, School of Dentistry, University of Isfehan, Iran. d Professor and Chair, Department of Endodontics, School of Dentistry, Loma Linda University. Received for publication Mar 22, 2002; returned for revision May 13, 2002; accepted for publication Jul 9, 2002. 2002, Mosby, Inc. 1079-2104/2002/$35.00 0 7/15/128962 doi:10.1067/moe.2002.128962
a

evidence regarding clinical implications of the smear layer in endodontics. BACTERIAL PRESENCE When pathologic changes occur in the dental pulp, the root canal system can harbor several species of bacteria, their toxins, and byproducts. A number of investigations have shown that pulpal and periradicular pathoses do not develop without the presence of bacteria.6-9 Depending on the stage of pulpal pathosis, various species of bacteria can be cultured from infected root canals. These bacteria are predominantly gram-negative anaerobes8,10,11 that can infect the root canals by direct pulp exposures (caries or traumatic injuries) or by coronal microleakage.12-16 Davis et al17 have shown that the morphology of root canals is very complex and that mechanically prepared canals contain areas not accessible by currently used endodontic instruments. Bacteria can be found in all areas of the root canal system and in the dentinal tubules (Fig 2).18-20 DENTINAL TUBULES In the root, dentinal tubules extend from the pulppredentin junction to the intermediate dentin just inside the cementum-dentin junction. Dentinal tubules in the root run a relatively straight course between the pulp and the periphery in contrast to the typical S-shaped contours of the tubules in the tooth crown. They range in size from approximately 1 to 3 m in diameter.21,22

658

ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY Volume 94, Number 6

Torabinejad et al 659

Fig 1. The presence of smear layer on the surface of an instrumented root canal. Original magnication 5000.

Fig 2. The presence of several bacteria in a dentinal tubule of a tooth with necrotic pulp. Original magnication 5000.

The density or number of dentinal tubules per square millimeter varies from 4900 to 90,000.21 This density increases in an apical-coronal direction to the root surface and similarly in an external to internal direction from the root surface. At the cementoenamel junction, the number of dentinal tubules has been estimated to be approximately 15,000 per square millimeter. Available evidence shows that bacteria and its byproducts present in infected root canals may invade the dentinal tubules.18-20,23-29 Investigators18,19 have reported the presence of bacteria in the dentinal tubules of infected teeth at approximately half the distance between the root canal walls and the cementodentinal junction. Sen et al20 examined 10 extracted human teeth with necrotic pulps under a scanning electron microscope and reported bacterial penetration into the dentinal tubules up to 150 m in the apical two thirds of the roots. Horiba et al23 found endotoxin within the dentinal walls of infected root canals. In addition, in vitro studies have shown bacterial penetration into the dentinal tubules in experimentally inoculated root canals.24-26 Siqueira et al27 removed the smear layer in bovine teeth and inoculated them with 5 species of bacteria and Enterococcus faecalis as a control. Their scanning electron microscope examination showed that all of the test bacteria were able to penetrate into the dentinal tubules to varying depths. Perez et al28 found a mean penetration depth of 479 m for Streptococcus sanguis after 28 days of incubation, with a maximum penetration of 737 m. Peters et al29 evaluated the presence, depth of penetration, morphotypes, and the number of colonyforming units of bacteria in the root dentin of teeth with periapical lesions. They reported the presence of bacteria in more than half of their samples close to the cementum. Drake et al30 showed that removal of the

smear layer opened the tubules, allowing bacteria to colonize in the tubules to a much higher degree (10-fold) compared with roots with an intact smear layer. Factors such as the number and the type of bacteria, in addition to the length of exposure and the presence or absence of smear layer, could inuence the depth of penetration of bacteria into the dentinal tubules. Because of the difculties involved in sampling the dentinal tubules, the exact microora of infected dentinal tubules is unknown. rstavik and Haapasalo26 have expressed concern regarding the effect of bacteria in the dentinal tubules after inadequate root canal therapy. INTRACANAL MEDICATIONS The removal of diseased tissue, elimination of bacteria present in the canals and dentinal tubules, and prevention of recontamination after treatment are the objectives of endodontic therapy. These objectives are achieved by thoroughly cleaning, shaping, and disinfecting the root canal system; by sealing the root canals with a 3-dimensional obturation; and by placing a coronal seal. Because of the complexity of root canal systems and the current inability to instrument all aspects of canal wall surfaces, it is impossible to achieve complete m and removal or destruction of all bacteria.31,32 Bystro Sundqvist31 have shown that residual bacteria in an instrumented but unlled canal can multiply to their original numbers within 2 to 4 days. To prevent recolonization of the root canals with residual bacteria, some authors recommend the use of intracanal medication and, therefore, the completion of treatment of infected 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 disinfection of root canals.26,35-37 The traditional phenolic or xative agents include camphorated monochlorophenol (CMCP), formocresol, and cresatin. Iodine potassium iodide and calcium hydroxide are the main nonphenolic intracanal medications. These medicaments are potent antibacterial agents under laboratory test conditions; however, their effectiveness in clinical use is unpredictable.38 According to some researchers, they also neutralize and render canal tissue remnants inert. Some medications contain aldehyde derivatives that can be used to x fresh tissues for histologic examination; however, they may not effectively x necrotic or decomposed tissues.35 According to Wesselink et al,39 xed tissues are not inert and may become more toxic and antigenic after xation. Intracanal medications have also been used clinically to prevent posttreatment pain. Studies have shown, however, that routine use of these materials as intracanal medication has no significant effect on the prevention of pain.40-43 According to Oguntebi,44 most currently used intracanal medicaments have a limited antibacterial spectrum and antigenic potential. In addition, some of them have a limited ability to diffuse into the dentinal tubules. Effects of intracanal medications on bacteria in dentinal tubules After removal of the smear layer, Haapasalo and rstavik25 inoculated the bovine incisors with E faecalis and found penetration of these bacteria into the dentinal tubules up to 1 mm. They demonstrated that liquid CMCP completely disinfected the dentinal tubules but that Ca(OH)2 was ineffective. Behnen et al45 had better success killing E faecalis with either Pulpdent or a 10% solution of Ca(OH)2 than with the traditional thick mixes. The difference might have been attributable to the different viscosity of various types of Ca(OH)2 used in this experiment. Heling and Chandler46 also inoculated dentinal tubules of bovine teeth with E faecalis and then examined the disinfecting effect of various irrigants. They found that none of the test irrigants (chlorhexidine, hydrogen peroxide, sodium hypochlorite, EDTA, or their combinations) were totally effective. Siqueira and de Uzeda47 inoculated bovine dentin cylinders with 1 facultative and 2 obligate anaerobic bacteria and examined the disinfecting effect of Ca(OH)2 mixed with saline solution or CMCP for 1 hour, 1 day, and 1 week. Their results showed that Ca(OH)2 and saline solution were ineffective in disinfecting the dentinal tubules after 1 week of application. In contrast, a mixture of Ca(OH)2 and CMCP resulted in complete disinfection of the dentinal tubules in 1 day. Jeansonne and White48 and Kuruvilla and Ka-

math49 examined the antibacterial effect of chlorhexidine gluconate and sodium hypochlorite on inoculated human teeth in vitro. They reported a reduction in bacterial counts but not total disinfection of the root canals. In an in vivo experiment, Katebzadeh et al50 showed that infected dog teeth that were lled experienced treatment failure more frequently than those medicated with Ca(OH)2 before obturation. Sjo gren et al51 examined the presence and inuence of bacteria on the long-term success of root canal therapy. Their results show that 40% of root canals remain infected after instrumentation. In addition, they reported that teeth lled in 1 visit without the use of Ca(OH)2 experienced treatment failure signicantly more frequently than those that were medicated for 1 week with Ca(OH)2 (68% vs 94%). The results of this study corroborate the ndings of Bystro m et al,52 who showed improved clinical success rates after effective disinfection of root canals. Effects of smear layer on penetration of root canal medicaments and sealers into the dentinal tubules In an in vitro study, rstavik and Haapasalo26 showed the importance of removal of the smear layer and the presence of patent dental tubules for decreasing the time necessary to achieve the disinfecting effect of intracanal medications. Bystro m and Sundqvist53 have also shown that the presence of a smear layer can inhibit or signicantly delay the penetration of antimicrobial agents such as intracanal irrigants and medications into the dentinal tubules. Studies54-56 have shown better adhesion of obturation materials to the canal walls after removal of the smear layer. Pitt Ford and Roberts57 have suggested that the failures of glass-ionomer retrograde llings after apical surgery may result from degradation of the smear layer. Other investigators58-62 assessed the penetration depth of different sealers, including Tubliseal, AH26, Sealapex, Rosin, Roths 811, and CRCS, into the dentinal tubules. They found the penetration to be 10 to 80 m after removal of the smear layer, whereas no penetration was observed with the smear layer intact. MICROLEAKAGE OF ROOT CANAL FILLINGS WITH AND WITHOUT A SMEAR LAYER The presence or absence of a smear layer may play an important role in the adhesiveness of some sealers to the root canal walls. Studies have shown a signicant increase in adhesive strength and resistance to microleakage of AH26 sealer when the smear layer was removed.63,64 Gettleman et al63 did not nd any changes in adhesive strengths when Sultan and Sealapex sealers

ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY Volume 94, Number 6

Torabinejad et al 661

were evaluated with or without the smear layer intact. Several investigators64-70 have shown less dye leakage after removal of the smear layer with various obturation techniques and root canal sealers. Other investigators have reported that the removal of the smear layer did not have any signicant effect on the microleakage of root canals when various sealers and obturation techniques were used.71-75 In contrast to these ndings, Timpawat et al76 have reported that removal of the smear layer has adverse effects on the microleakage of lled root canals. These conicting results might be attributable to differences in the types of sealer and obturation techniques, the means of producing a smear layer, and the diversity of bacteria used under various laboratory conditions. REMOVAL OF THE SMEAR LAYER Despite the controversy regarding the effect of the smear layer on the quality of instrumentation and obturation, several investigators1,77,78 have found that the smear layer itself may be infected and may protect the bacteria already present in the dentinal tubules. Because of these concerns, one may deem it prudent to remove the initially created smear layer in infected root canals and to allow penetration of intracanal medications into the dentinal tubules of these teeth. Efforts to remove the smear layer have included chemical, mechanical, and laser means. After disinfection of the root canal system, one can recreate a new smear layer by mechanical ling of the root canal walls. Chemical removal The components of the smear layer are very small particles with a large surface-mass ratio, which makes them very soluble in acids.5 Because of this characteristic, acids have been used to remove the smear layer. McComb and Smith1 were the rst investigators to show that REDTA (a commercial brand of EDTA) can remove the smear layer. Goldman et al79 showed that when used alone, REDTA removed the inorganic portion and left an organic layer intact in the tubules. To remove this organic layer, another solvent is needed. Sodium hypochlorite (NaOCl) has been shown to be very effective for this purpose. When used alone, NaOCl can dissolve pulpal remnants and predentin. However, many studies have shown its ineffectiveness in removing the entire smear layer when used alone. Goldman et al,79 Yamada et al,80 and Baumgartner and Mader81 showed that alternating the use of EDTA and NaOCl is an effective method for smear layer removal. OConnell et al82 compared the ability of various salts of EDTA to remove the smear layer. They showed that all salts of EDTA were capable of removing the smear layer from the coronal two thirds of root canals. In

addition, they reported that tetrasodium salt pH-adjusted with HCl is less expensive and just as effective as the more commonly used disodium EDTA. Aktener and Bilkay83 developed a solution of EDTA and ethylenediamine to work in dual action. Their goal was to see whether a single irrigating solution could be developed to remove the inorganic and the organic components of the smear. They found many patent tubules but concluded that more research was needed to determine the efcacy of this combination. Goldberg and Abramovich84 added a quaternary ammonium bromide (Cetavlon) to EDTA to reduce its surface tension; this solution is called EDTAC. This addition increased the wetting effect on the canal wall and permitted deeper penetration of the solution into irregularities. This combination was shown by Goldberg and Spielberg85 to be very effective in smear layer removal, reaching its peak effect at 15 minutes and increasing the diameter of the opened dentinal tubules. Recently, C alt and Serper86 reported that ethylene glycol-bis (b-aminoethyl ether)-N,N,N, N-tetraacetic acid was somewhat effective in removing the smear layer without inducing dentinal erosion commonly caused by EDTA (Fig 3). Morgan and Baumgartner87 showed that the quantity of smear layer removed by a material is directly related to its pH and the time of exposure. Loel58 used a 50% citric acid solution to treat canal walls after instrumentation and found better penetration of rosin sealer into the tubules and improved adaptation of gutta-percha than in untreated canals. Tidmarsh55 and Baumgartner et al88 also showed that 50% citric acid is an effective irrigant to remove the smear layer from the surface of prepared root canal walls. Wayman et al89 found lactic acid at 50% concentration was less effective than 50% citric acid for removal of the smear layer. This might be attributed to the viscosity of lactic acid. They also determined that alternating use of 10% citric acid and 2.5% NaOCl was a very effective method for removing the smear layer. Bitter90 reported that 25% tannic acid was effective in removing the smear layer. Sabbak and Hasanin91 refuted these ndings and explained that tannic acid increased the cross-linking of exposed collagen within the smear layer and within the matrix of the underlying dentin, thus increasing organic cohesion to the tubules. Polyacrylic acid (Durelon liquid and Fuji II liquid) at 40% was reported by Berry et al92 to be very effective for removal of the smear layer. Because of its potency, the application of polyacrylic acid should not exceed 30 seconds according to the authors recommendations. Derivatives of oxine (8-hydroxy-quinoline) were 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 magnication 5000.

Dequalinium compounds, which belong to this group, have been widely used in medicine against infections of bacteria, molds, and fungi.94 Bis-dequalinium-acetate (BDA) has been shown by Kaufman et al94 and Kaufman95 to remove the smear layer throughout the canal, even in the apical third. BDA is well tolerated by the tissues within the periodontium and has a low surface tension that allows penetration into spaces that instruments cannot reach.94 BDA is also considered less toxic than NaOCl and can be used as a root canal dressing. Kaufman and Greenberg96 compared Salvizol (a commercial brand of 0.5% BDA) with 5.25% NaOCl and found both comparable in their ability to remove organic debris, but only Salvizol was able to open dentinal tubules. Berg et al97 reported Salvizol to be less effective at opening dentinal tubules than was REDTA. Tetracyclines (including tetracycline-HCl, minocycline, and doxycycline) are broad-spectrum antibiotics that are effective against a wide range of microorganisms. Genco et al98 have suggested that tetracyclines signicantly enhance healing after surgical periodontal therapy. Tetracyclines have many unique properties in addition to their antimicrobial effect. They have a low pH in concentrated solution and thus can act as a calcium chelator, and they can

cause enamel and root surface demineralization.99 The surface demineralization of dentin is comparable with that of citric acid.100 The substantivity of these antibiotics allows them to be absorbed and released gradually from tooth structures such as dentin and cementum.100-102 The ability of the tetracycline family of antibiotics to remove smear layers has also been studied. They have been used to demineralize dentin surfaces, uncover and widen the orices of dentinal tubules, and expose the dentin collagen matrix. These effects provide a matrix that stimulates broblast attachment and growth. Barkhordar et al103 showed that doxycycline HCl (100 mg/ mL) is effective in removing the smear layer from the surfaces of instrumented canals and root-end cavity preparations. They speculated that a reservoir of active antibacterial agents might be created because doxycycline readily attaches to dentin and can be subsequently released. Haznedaroglu and Ersev104 showed that 1% tetracycline hydrochloride or 50% citric acid can be used to remove the smear layer from the surfaces of instrumented root canals. Although they reported no difference between these 2 groups, it appears that the tetracycline demineralized less peritubular dentin than did the 50% citric acid.

ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY Volume 94, Number 6

Torabinejad et al 663

Ultrasonic removal Cameron105 produced a debris-free canal with the use of a 3% NaOCl solution combined with ultrasonic instrumentation for 5 minutes after conventional canal instrumentation. The mechanism of action for debris removal was described as acoustic streaming by Ahmad et al.106 Acoustic streaming is maximized when the tips of the smaller instruments operate at high power and vibrate freely in a solution. Lumley et al107 recommended that only size 15 les be used to maximize the microstreaming for removal of debris. Cameron108 showed complete smear removal with 4% NaOCl and ultrasonic instrumentation for 2 minutes. Prati et al109 also achieved smear layer removal with ultrasonics. Walker and del Rio110,111 in 2 separate reports showed no signicant difference between tap water and NaOCl when used with ultrasonics, but they reported that neither solution used with ultrasonics was effective at any level in the canal to remove the smear layer. Baumgartner and Cuenin112 also observed that ultrasonically energized NaOCl, even at full strength, did not remove the smear layer from the root canal walls. Guerisoli et al113 evaluated the use of ultrasonics to remove the smear layer and found it necessary to use 15% EDTAC with either distilled water or 1% NaOCl to achieve the desired result. Laser removal Takeda et al114,115 found that lasers can be used to vaporize tissues in the main canal, remove the smear layer, and eliminate the residual tissue in the apical portion of the root canals. Several investigators116-118 have reported that the effectiveness of lasers depends on many factors, including the power level, the duration of exposure, the absorption of light in the tissue, the geometry of the root canal, and the tip-to-target distance. Dederich et al116 and Tewk et al119 used variants of the neodymium-yttrium-aluminum-garnet laser and reported a range of ndings from no change or disruption of the smear layer to actual melting and recrystallization of the dentin. This pattern of dentin disruption was observed in other studies with various lasers, including the carbon dioxide laser,117 the argon uoride excimer laser,120 and the argon laser.118,121 Takeda et al,114,115,122 using the erbium-yttrium-aluminum-garnet (Er:YAG) laser, demonstrated optimal removal of the smear layer without the melting, charring, and recrystallization associated with other laser types. Kimura et al123 demonstrated the removal of the smear layer with an Er:YAG laser as well. Although they showed removal of the smear layer, the photomicrograph showed destruction of the peritubular dentin. The main difculty with laser removal of the smear layer continues to

be the access to small canal spaces with the relatively large probes that are available for delivery of the laser beam. CONCLUSION On the basis of the available evidence, it can be concluded that current methods of root canal instrumentation produce a layer of organic and inorganic material (smear layer) that may also contain bacteria and their byproducts. This layer covers the instrumented walls and may prevent the penetration of intracanal medications into the dentinal tubules and may affect close adaptation between root canal lling materials and the root canal walls. Considering the aforementioned observations, it seems reasonable to suggest that removal of the smear layer can result in a more thorough disinfection of the root canal system and the dentinal tubules, which would ensure a better adaptation between the obturation materials and the root canal walls. Current methods of smear layer removal include chemical, ultrasonic, and laser techniquesnone of which is totally effective or has received universal acceptance. Conicting reports exist regarding the removal of the smear layer before the obturation of root canals. One may deem it prudent, because of its potential contamination, to remove the smear layer in teeth with infected root canals and allow penetration of intracanal medications into the dentinal tubules. After disinfection of the root canal system, if advised, one may recreate a new smear layer by circumferential hand-ling or the use of rotary instruments. To effectively disinfect the root canal system, an irrigant or an intracanal medication with the following characteristics should be used: 1. It should be able to completely remove the smear layer. 2. It should be able to disinfect the dentin and its tubules. 3. It should have sustained antibacterial effect after use. 4. It should allow the penetration of antimicrobial agents present in the solution into the dentinal tubules. 5. It should be nonantigenic, nontoxic, and noncarcinogenic to tissue cells surrounding the tooth. 6. It should have no adverse effects on the physical properties of exposed dentin. 7. It should have no adverse effect on the sealing ability of lling materials. 8. It should not discolor the tooth. 9. It should have convenient application. 10. It should be relatively inexpensive. Clinical investigations are needed to determine the

664 Torabinejad et al

ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY December 2002

24. Akpata ES, Blechman H. Bacterial invasion of pulpal dentin wall in vitro. J Dent Res 1982;61:435-8. 25. Haapasalo M, rstavik D. In vitro infection and disinfection of dentinal tubules. J Dent Res 1987;66:1375-9. 26. rstavik D, Haapasalo M. Disinfection by endodontic irrigants and dressings of experimentally infected dentinal tubules. Endod Dent Traumatol 1990;6:142-9. 27. Siqueira JF Jr, de Uzeda M, Fonseca MEF. A scanning electron microscopic evaluation of in vitro dentinal tubules penetration by selected anaerobic bacteria. J Endod 1996;22:308-10. 28. Perez F, Rochd T, Lodter J-P, Calas P, Michel G. In vitro study of the penetration of three bacterial strains into root dentin. Oral Surg Oral Med Oral Pathol 1993;76:97-103. 29. Peters LB, Wesselink PR, Buijs JF, van Winkelhoff AJ. Viable bacteria in root dentinal tubules of teeth with apical periodontitis. J Endod 2001;27:76-81. 30. Drake DR, Wiemann AH, Rivera EM, Walton RE. Bacterial retention in canal walls in vitro: effect of smear layer. J Endod 1994;20:78-82 31. Bystro m A, Sundqvist G. Bacteriologic evaluation of the efcacy of mechanical root canal instrumentation in endodontic therapy. Scand J Dent Res 1981;89:321-8. 32. Bystro m A, Claesson R, Sundqvist G. The antibacterial effect of camphorated paramonochlorophenol, camphorated phenol and calcium hydroxide in the treatment of infected root canals. Endod Dent Traumatol 1985;1:170-5. 33. Chong BS, Pitt Ford TR. The role of intracanal medication in root canal treatment. Int Endod J 1992;25:97-106. 34. Heithersay GW, Hume WR, Abbot PV. Conventional root canal therapy. II: intracanal medication. In: Harty FJ, editor. Endodontics in clinical practice, 3rd ed. London: Wright; 1990. p. 162-85. 35. Walton RE, Rivera EM. Cleaning and Shaping. In: Walton RE and Torabinejad M, editors. Principles and practice of endodontics, 3rd ed. Philadelphia: W. B. Saunders; 2002. p. 232-3. 36. Spngberg LSW. Cellular reaction to intracoronal medicaments. In Grossman LI, editor. Transactions of the Fifth International Conference on Endodontics. University of Pennsylvania, Philadelphia; 1973. p. 108-23. 37. Masillamoni CRM, Kettering JD, Torabinejad M. The biocompatibility of some root canal medicaments and irrigants. Int Endod J 1981;14:115-20. 38. Messer HH, Chen RS. The duration of effectiveness of root canal medicaments. J Endod 1984;10:240-5. 39. Wesselink PR, Thoden van Velzen SK, van den Hoof A. The tissue reaction to implantation of unxed and glutaraldehyde xed heterologous tissue. J Endod 1977;3:229-235. 40. Maddox DL, Walton RE, Davis CO. Incidence of posttreatment endodontic pain related to medicaments and other factors. J Endod 1977;3:447-452. 41. Kleier DJ, Mullaney TP. Effects of formocresol on posttreatment pain of endodontic origin in vital molars. J Endod 1980; 6:566-9. 42. Torabinejad M, Kettering JD, McGraw JC, Cummings RR, Dwyer TG, Tobias TS. Factors associated with endodontic interappointment emergencies of teeth with necrotic pulps. J Endod 1988;14:261-6. 43. Trope M. Relationship of intracanal medicaments to endodontic are-ups. Endod Dent Traumatol 1990;6:226-9. 44. Oguntebi BR. Dentine tubule infection and endodontic therapy implications. Int Endod J 1994;27:218-22. 45. Behnen MJ, West LA, Liewehr FR, Buxton TB, McPherson JC. Antimicrobial activity of several calcium hydroxide preparations in root canal dentin. J Endod 2001;27:765-67. 46. Heling I, Chandler NP. Antimicrobial effect of irrigant combinations within dentinal tubules. Int Endod J 1998;31:8-14. 47. Siqueira JF Jr, de Uzeda M. Disinfection by calcium hydroxide pastes of dentinal tubules infected with two obligate and one facultative anaerobic bacteria. J Endod 1996;22:674-6. 48. Jeansonne MJ, White RR. A comparison of 2.0% chlorhexidine gluconate and 5.25% sodium hypochlorite as antimicrobial endodontic irrigants. J Endod 1994;20:276-8.

role of smear layer in the outcome of root canal therapy.

REFERENCES
1. McComb D, Smith DC. A preliminary scanning electron microscopic study of root canals after endodontic procedures. J Endod 1975;1:238-42. 2. Moodnik RM, Dorn SO, Feldman MJ, Levey M, Borden BG. Efcacy of biomechanical instrumentation: a scanning electron microscopic study. J Endod 1976;2:261-6. 3. Mader CL, Baumgartner JC, Peters DD. Scanning electron microscopic investigation of the smeared layer on root canal walls. J Endod 1984;10:477-83. 4. Cengiz T, Aktener BO, Pikin B. The effect of dentinal tubule orientation on the removal of smear layer by root canal irrigants. A scanning electron microscopic study. Int Endod J 1990; 23:163-171 5. Pashley DH. Smear layer: overview of structure and function. Proc Finn Dent Soc 1992; 88(Suppl l):215-24. 6. Kakehashi S, Stanley HR, Fitzgerald RJ. The effects of surgical exposures of dental pulps in germ-free and conventional laboratory rats. Oral Surg Oral Med Oral Pathol 1965;20:340-9. 7. Bergenholtz G. Micro-organisms from necrotic pulp of traumatized teeth. Odontol Revy 1974;25:347-58. 8. Sundqvist G. Bacteriological studies of necrotic dental pulps [dissertation]. Ume University Odontology Dissertation, No 7. University of Ume, Sweden, 1976. hman AE, Heyden G. 9. Mo ller JR, Fabricius L, Dahle n G, O Inuence on periapical tissues of indigenous oral bacteria and necrotic pulp tissue in monkeys. Scand J Dent Res 1981;89: 475-84. hman AE, Mo 10. Fabricius L, Dahle n G, O ller JR. Predominant indigenous oral bacteria isolated from infected root canals after varied times of closure. Scand J Dent Res 1982;90:134-44. 11. Kantz WE, Henry CA. Isolation and classication of anaerobic bacteria from intact pulp chambers of non-vital teeth in man. Arch Oral Biol 1974;19:91-96. 12. Swanson K, Madison S. An evaluation of coronal microleakage in endodontically treated teeth. Part I. Time periods. J Endod 1987;13:56-9. 13. Madison S, Swanson K, Chiles S. An evaluation of coronal microleakage in endodontically treated teeth. Part II. Sealer types. J Endod 1987;13:109-12. 14. Madison S, Wilcox LR. An evaluation of coronal microleakage in endodontically treated teeth. Part III. In vivo study. J Endod 1988;14:455-8. 15. Torabinejad M, Ung B, Kettering JD. In vitro bacterial penetration of coronally unsealed endodontically treated teeth. J Endod 1990;16:566-9. 16. Magura ME, Kafrawy AH, Brown CE Jr, Newton CW. Human saliva coronal microleakage in obturated root canals: an in vitro study. J Endod 1991;17:324-31. 17. Davis SR, Brayton S, Goldman M. The morphology of the prepared root canal: a study utilizing injectable silicone. Oral Surg Oral Med Oral Pathol 1972;34:642-8. 18. Ando N, Hoshino E. Predominant obligate anaerobes invading the deep layers of root canal dentine. Int Endod J 1990;23:20-7. 19. Armitage GC, Ryder MI, Wilcox SE. Cemental changes in teeth with heavily infected root canals. J Endod 1983;9:127-30. 20. Sen BH, Pikin B, Demirci T. Observation of bacteria and fungi in infected root canals and dentinal tubules by SEM. Endod Dent Traumatol 1995;11:6-9. 21. Mjo r IA, Nordahl I. The density and branching of dentinal tubules in human teeth. Arch Oral Biol 1996;41:401-12. 22. Garberoglio R, Bra nnstro m M. Scanning electron microscopic investigation of human dentinal tubules. Arch Oral Biol 1976; 21:355-62. 23. Horiba N, Maekawa Y, Matsumoto T, Nakamura H. A study of the distribution of endotoxin in the dentinal wall of infected root canals. J Endod 1990;16:331-4.

ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY Volume 94, Number 6

49. Kuruvilla JR, Kamath MP. Antimicrobial activity of 2.5% sodium hypochlorite and 0.2% chlorhexidine gluconate separately and combined, as endodontic irrigants. J Endod 1998;24:472-6. 50. Katebzadeh N, Hupp J, Trope M. Histological periapical repair after obturation of infected root canals in dogs. J Endod 1999; 25:364-8. 51. Sjo gren U, Figdor D, Persson S, Sundqvist G. Inuence of infection at the time of root lling on the outcome of endodontic treatment of teeth with apical periodontitis. Int Endod J 1997; 30:297-306. 52. Bystro m A, Happonen R-P, Sjo gren U, Sundqvist G. Healing of periapical lesions of pulpless teeth after endodontic treatment with controlled asepsis. Endod Dent Traumatol 1987;3:58-63. 53. Bystro m A, Sundqvist G. The antibacterial action of sodium hypochlorite and EDTA in 60 cases of endodontic therapy. Int Endod J 1985;18:35-40. 54. Abramovich A, Goldberg F. The relationship of the root canal sealer to the dentine wall. An in vitro study using scanning electron microscope. J Br Endod Soc 1976;9:81 6. 55. Tidmarsh BG. Acid-cleansed and resin-sealed root canals. J Endod 1978;4:117-21. 56. White R, Goldman M, Peck S-L. The inuence of the smeared layer upon dentinal tubule penetration by plastic lling materials. J Endod 1984;10:558-62. 57. Pitt Ford TR, Roberts GJ. Tissue response to glass ionomer retrograde root llings. Int Endod J 1990;23:233-8. 58. Loel DA. Use of acid cleanser in endodontic therapy. J Am Dent Assoc 1975;90:148-51. 59. Gutie rrez JH, Herrera VR, Berg EH, Villena F, Jofre A. The risk of intentional dissolution of the smear layer after mechanical preparation of root canals. Oral Surg Oral Med Oral Pathol 1990;70:96-108. 60. Pallare s A, Faus V, Glickman GN. The adaptation of mechanically softened gutta-percha to the canal walls in the presence or absence of smear layer: a scanning electron microscopic study. Int Endod J 1995;28:266-9. 61. Kouvas V, Liolios E, Vassiliadis L, Parissis-Messimeris S, Boutsioukis A. Inuence of smear layer depth of penetration of three endodontic sealers: an SEM study. Endod Dent Traumatol 1998;14:191-5. 62. Genc og lu N, Samani S, Gu nday M. Dentinal wall adaptation of thermoplasticized gutta-percha in the absence or presence of smear layer: a scanning electron microscopic study. J Endod 1993;19:558-62. 63. Gettleman BH, Messer HH, ElDeeb ME. Adhesion of sealer cements to dentin with and without the smear layer. J Endod 1991;17:15-20. 64. Economides N, Liolios E, Kolokuris I, Beltes P. Long-term evaluation of the inuence of smear layer removal on the sealing ability of different sealers. J Endod 1999;25:123-5. 65. Kennedy WA, Walker WA, Gough RW. Smear layer removal effects on apical leakage. J Endod 1986;12:21-7. 66. Cergneux M, Ciucchi B, Dietschi JM, Holz J. The inuence of the smear layer on the sealing ability of canal obturation. Int Endod J 1987;20:228-32. 67. Vassiliadis L, Liolios E, Kouvas V, Economides N. Effect of smear layer on coronal microleakage. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1996;82:315-20. 68. Taylor JK, Jeansonne BG, Lemon RR. Coronal leakage: effects of smear layer, obturation technique, and sealer. J Endod 1997; 23:508-12. 69. Karago z-Ku c u kay I, Bayirli G. An apical leakage study in the presence and absence of the smear layer. Int Endod J 1994;27: 87-93. 70. Saunders WP, Saunders EM. The effect of smear layer upon the coronal leakage of gutta percha root lling and a glass ionomer sealer. Int Endod J 1992;25:245-9. 71. Evans JT, Simon JHS. Evaluation of the apical seal produced by injected thermoplasticized gutta-percha in the absence of smear layer and root canal sealer. J Endod 1986;12:101-7. 72. Chailertvanitkul P, Saunders WP, Mackenzie D. The effect of

Torabinejad et al 665

73.

74. 75. 76. 77. 78. 79. 80. 81. 82. 83. 84. 85. 86. 87. 88.

89. 90. 91. 92. 93. 94. 95. 96.

smear layer on microbial coronal leakage of gutta-percha root llings. Int Endod J 1996;29:242-8. Saunders WP, Saunders EM. Inuence of smear layer and the coronal leakage of thermal and laterally condensed guttapercha root llings with a glass ionomer sealer. J Endod 1994; 20:155-8. Madison S, Krell KV. Comparison of ethylenediamine tetraacetic acid and sodium hypochlorite on the apical seal of endodontically treated teeth. J Endod 1984;10:499-503. Timpawat S, Sripanaratanakul S. Apical sealing ability of glass ionomer sealer with and without smear layer. J Endod 1998;24: 343-5. Timpawat S, Vongsavan N, Messer HH. Effect of removal of the smear layer on apical microleakage. J Endod 2001;27: 351-3. Brannstro m M. Smear layer: pathologic and treatment considerations. Oper Dent 1984;suppl 3:35-42. Pashley DH. Smear layer: physiological considerations. Oper Dent 1984;suppl 3:13-29. Goldman M, Goldman LB, Cavaleri R, Bogis J, Peck S-L. The efcacy of several endodontic irrigating solutions: a scanning electron microscopic study: part 2. J Endod 1982;8:487-92. Yamada RS, Armas A, Goldman M, Peck S-L. A scanning electron microscopic comparison of a high volume nal ush with several irrigating solutions: part 3. J Endod 1983;9:137-42. Baumgartner JC, Mader CL. A scanning electron microscopic evaluation of four root canal irrigation regimens. J Endod 1987;13:147-57. OConnell MS, Morgan LA, Beeler WJ, Baumgartner JC. A comparative study of smear layer removal using different salts of EDTA. J Endod 2000;26:739-43. Aktener BO, Bilkay U. Smear layer removal with different concentrations of EDTA-ethylenediamine mixtures. J Endod 1993;19:228-31. Goldberg F, Abramovich A. Analysis of the effect of EDTAC on the dentinal walls on the root canal. J Endod 1977;3:101-5. Goldberg F, Spielberg C. The effect of EDTAC and the variation of its working time analyzed with scanning electron microscopy. Oral Surg Oral Med Oral Pathol 1982;53:74-7. C alt S, Serper A. Smear layer removal by EGTA. J Endod 2000;8:459-61. Morgan LA, Baumgartner JC. Demineralization of resected root-ends with methylene blue dye. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1997;84:74-8. Baumgartner JC, Brown CM, Mader CL, Peters DD, Shulman JD. A scanning electron microscopic evaluation of root canal debridement using saline, sodium hypochlorite and citric acid. J Endod 1984;10:525-31. Wayman BE, Kopp WM, Pinero GJ, Lazzari EP. Citric and lactic acids as root canal irrigants in vitro. J Endod 1979;5:25865. Bitter NC. A 25% tannic acid solution as a root canal irrigant cleanser: A scanning electron microscope study. Oral Surg Oral Med Oral Pathol 1989;67:333-7. Sabbak SA, Hassanin MB. A scanning electron microscopic study of tooth surface changes induced by tannic acid. J Prosthet Dent 1998;79:169-74. Berry EA, von der Lehr WN, Herrin HK. Dentin surface treatments for the removal of the smear layer: an SEM study. J Am Dent Assoc 1987;115:65-7. Albert A, Margrath D. The choice of a chelating agent for inactivating trace metals. J Biochem 1947;41:534-43. Kaufman AY, Binderman I, Tal M, Gedalia I, Peretz G. New chemotherapeutic agent for root canal treatment. Oral Surg Oral Med Oral Pathol 1978;46:283-95. Kaufman AY. The use of dequalinium acetate as a disinfectant and chemotherapeutic agent in endodontics. Oral Surg Oral Med Oral Pathol 1981;51:434-41. Kaufman AY, Greenberg I. Comparative study of the conguration and the cleanliness level of root canals prepared with the aid of sodium hypochlorite and bis-dequalinium-acetate solutions. Oral Surg Oral Med Oral Pathol 1986;62:191-7.

666 Torabinejad et al

ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY December 2002

113. Guerisoli DMZ, Marchesan MA, Walmsley AD, Lumley PJ, Pecora JD. Evaluation of smear layer removal by EDTAC and sodium hypochlorite with ultrasonic agitation. Int Endod J 2002;35:418-21. 114. Takeda FH, Harashima T, Kimura Y, Matsumoto K. Efcacy of Er:YAG laser irradiation in removing debris and smear layer on root canal walls. J Endod 1998;24:548-51. 115. Takeda FH, Harashima T, Kimura Y, Matsumoto K. A comparative study of the removal of smear layer by three endodontic irrigants and two types of laser. Int Endod J 1999;32:32-9. 116. Dederich DN, Zakariasen KL, Tulip J. Scanning electron microscopic analysis of canal wall dentin following neodymiumyttrium-aluminum-garnet laser irradiation. J Endod 1984;10: 428-31. nal B, Ertl T, Siebert G, Mu 117. O ller G. Preliminary report on the application of pulsed CO2 laser radiation on root canals with AgCl bers: a scanning and transmission electron microscopic study. J Endod 1993;19:272-6. 118. Moshonov J, Sion A, Kasirer J, Rotstein I, Stabholz A. Effect of argon laser irradiation in removing intracanal debris. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1995;79:221-5. 119. Tewk HM, Pashley DH, Horner JA, Sharawy MM. Structural and functional changes in root dentin following exposure to KTP/532 laser. J Endod 1993;19:492-7. 120. Stabholz A, Neev J, Liaw L-HL, Stabholz A, Khayat A, Torabinejad M. Effect of ArF-193 nm excimer laser on human dentinal tubules. A scanning electron microscopic study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1993;75:90-4. 121. Harashima T, Takeda FH, Zhang C, Kimura Y, Matsumoto K. Effect of argon laser irradiation on instrumented root canal walls. Endod Dent Traumatol 1998;14:26-30. 122. Takeda FH, Harashima T, Kimura Y, Matsumoto K. Comparative study about the removal of smear layer by three types of laser devices. J Clin Laser Med Surg 1998;16:117-22. 123. Kimura Y, Yonaga K, Yokoyama K, Kinoshita J, Ogata Y, Matsumoto K. Root surface temperature increase during Er: YAG laser irradiation of root canals. J Endod 2002;28:76-8. Reprint requests: Mahmoud Torabinejad, DMD, MSD, PhD Department of Endodontics School of Dentistry Loma Linda University Loma Linda, CA 92350

97. Berg MS, Jacobsen EL, BeGole EA, Remeikis NA. A comparison of ve irrigating solutions: A scanning electron microscopic study. J Endod 1986;12:192-7. 98. Genco R, Singh S, Krygier G, Levine M. Use of tetracycline in the treatment of adult periodontitis. I. Clinical studies [abstract]. J Dent Res 1978;57(A):266;768. 99. Bjo rvatn K. Antibiotic compounds and enamel demineralization. An in vitro study. Acta Odontol Scand 1982;40:341-52. 100. Wikesjo UME, Baker PJ, Christersson LA, Genco RJ, Lyall RM, Hic S, et al. A biochemical approach to periodontal regeneration: tetracycline treatment conditions dentin surfaces. J Periodontal Res 1986;21:322-9. 101. Baker PJ, Evans RT, Coburn RA, Genco RJ. Tetracycline and its derivatives strongly bind to and are released from the tooth surface in active form. J Periodontol 1983;54:580-5. 102. Bjo rvatn K, Skaug N, Selvig KA. Tetracycline-impregnated enamel and dentin: duration of antimicrobial capacity. Scand J Dent Res 1985;93:192-7. 103. Barkhordar RA, Watanabe LG, Marshall GW, Hussain MZ. Removal of intracanal smear by doxycycline in vitro. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1997;84:420-3. 104. Haznedaroglu F, Ersev H. Tetracycline HCl solution as a root canal irrigant. J Endod 2001;27:738-40. 105. Cameron JA. The use of ultrasonics in the removal of the smear layer: a scanning electron microscope study. J Endod 1983; 9:289-92. 106. Ahmad M, Pitt Ford TR, Crum LA. Ultrasonic debridement of root canals: acoustic streaming and its possible role. J Endod 1987;13:490-9. 107. Lumley PJ, Walmsley AD, Walton RE, Rippin JW. Effect of precurving endosonic les on the amount of debris and smear layer remaining in curved root canals. J Endod 1992;18:616-9. 108. Cameron JA. The use of ultrasound for the removal of the smear layer. The effect of sodium hypochlorite concentration: SEM study. Aust Dent J 1988;33:193-200. 109. Prati C, Selighini M, Ferrieri P, Mongiorgi R. Scanning electron microscopic evaluation of different endodontic procedures on dentin morphology of human teeth. J Endod 1994;20:174-9. 110. Walker TL, del Rio CE. Histological evaluation of ultrasonic and sonic instrumentation of curved root canals. J Endod 1989; 15:49-59. 111. Walker TL, del Rio CE. Histological evaluation of ultrasonic debridement comparing sodium hypochlorite and water. J Endod 1991;17:66-71. 112. Baumgartner JC, Cuenin PR. Efcacy of several concentrations of sodium hypochlorite for root canal irrigation. J Endod 1992; 18:605-12.