Morphology and Fracture of Enamel Sangwon Myoung

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Spring 5-8-2009 Morphology and fracture of enamel Sangwon Myoung

James Lee

Paul J. Constantino Biological Sciences, [email protected]

Peter Lucas

Herzl Chai

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Recommended Citation Myoung S, Lee J, Constantino P, Lucas P, Chai H, Lawn B. Morphology and fracture of enamel. Journal of Biomechanics 42: 1947-1951.

This Article is brought to you for free and open access by the Biological Sciences at Marshall Digital Scholar. It has been accepted for inclusion in Biological Sciences Faculty Research by an authorized administrator of Marshall Digital Scholar. For more information, please contact [email protected], [email protected]. Authors Sangwon Myoung, James Lee, Paul J. Constantino, Peter Lucas, Herzl Chai, and Brian Law

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Journal of Biomechanics 42 (2009) 1947–1951

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Journal of Biomechanics

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Morphology and fracture of enamel

Sangwon Myoung a,b, James Lee a,c,Ã, Paul Constantino c, Peter Lucas c, Herzl Chai d, Brian Lawn a a Ceramics Division, National Institute of Standards and Technology, 100 Bureau Drive, MS 8520, Gaithersburg, MD 20899, USA b School of Nano and Advanced Materials Engineering, Changwon National University, Changwon, Kyung-Nam, Korea c Department of Anthropology, George Washington University, Washington, DC, USA d School of Mechanical Engineering, Tel Aviv University, Tel Aviv, Israel article info abstract

Article history: This study examines the inter-relation between enamel morphology and crack resistance by sectioning Accepted 8 May 2009 extracted human molars after loading to fracture. Cracks appear to initiate from tufts, hypocalcified defects at the enamel–dentin junction, and grow longitudinally around the enamel coat to produce Keywords: failure. Microindentation corner cracks placed next to the tufts in the sections deflect along the tuft Enamel interfaces and occasionally penetrate into the adjacent enamel. Although they constitute weak Dentistry interfaces, the tufts are nevertheless filled with organic matter, and appear to be stabilized against easy Fracture extension by self-healing, as well as by mutual stress-shielding and decussation, accounting at least in Tufts part for the capacity of tooth enamel to survive high functional forces. Evolutionary biology & 2009 Elsevier Ltd. All rights reserved. Microindentation

1. Introduction failure (Lawn and Lee, 2009). The importance of these failure loads extends well beyond dental biomechanics into evolutionary Teeth are remarkably resilient and damage tolerant—‘‘built to biology, particularly as it relates to diets of primates and other last’’ (Maas and Dumont, 1999). The hard enamel provides animal species (Lucas et al., 2008). protection to the soft dentin interior, yet is highly brittle with a The question that arises is, if enamel is so brittle, why are teeth toughness comparable to glass (Xu et al., 1998; Bajaj et al., 2008). so durable? Part of the reason lies in the tooth geometry—the Recent studies of simulated functional loading on extracted capacity to support and sustain an essentially compressive human molars have identiﬁed the crack systems depicted in vertical load, rather like the dome of a cathedral (Lawn and Lee, Fig. 1 as principal modes of tooth failure, with critical loads 2009). But what is the role of the dental microstructure? Tooth 400–600 N for any one crack to span a side wall (Chai et al., 2009; enamel has a complex hierarchical composite structure consisting Lawn and Lee, 2009; Lee et al., 2009). These include ‘‘radial/ of mineralized prisms encased in protein sheaths (Osborn, 1981; median’’ cracks driven downward by local stress concentrations at Janis and Fortelius, 1988). Weak pathways between the prisms occlusal contacts or by channel-like margin cracks driven upward account for the susceptibility to fracture and deformation (He and by tensile ‘‘hoop’’ stresses at the enamel shell margins. Both these Swain, 2007, 2008). Enamel contains arrays of internal defects crack systems grow longitudinally as ribbons contained within which emanate from the enamel–dentin junction (EDJ) with a the enamel walls, in planes containing the load axis, although tuft-like appearance, closed cracks ﬁlled with organic matter in human teeth margin cracks tend to dominate. They tend to (Sognnaes, 1949; Osborn, 1969, 1981; Palamara et al., 1989). It propagate stably, and require a considerable overload or extensive appears that these ‘‘tufts’’ act as effective sources for the fractures cycling to grow to completion. At higher loads, approaching depicted in Fig. 1. One factor mitigating the implied intrinsic 1000 N, adjacent cracks can link up and spall fragments of enamel weakness of tufts and like defects is the existence of ‘‘decussation’’ from the dentin, and ultimately penetrate into the dentin itself in which adjacent bundles of prisms periodically change direction (Xu et al., 1998; Popowics et al., 2004). Cusp radius and enamel relative to their neighbors and cross each other, like a basket thickness emerge as important geometric variables—the larger weave (Sognnaes, 1949; Osborn, 1969, 1981; Koenigswald et al., these dimensions the higher the critical loads required to cause 1987; Maas and Dumont, 1999). Another factor is the apparent propensity for the tufts to ‘‘self-heal’’ (Sognnaes, 1949). However, the underlying nature of these microstructural elements in

Ã relation to damage containment has yet to be fully elucidated. Corresponding author at: Ceramics Division, National Institute of Standards In the present study we address the issue of damage tolerance and Technology, 100 Bureau Drive, MS 8520, Gaithersburg, MD 20899, USA. Tel./fax: +1301975 5774. by examining the microstructural responses to externally applied E-mail address: [email protected] (B. Lawn). loadings. We do this by sectioning the fractured teeth and

1948 S. Myoung et al. / Journal of Biomechanics 42 (2009) 1947–1951

An advantage of this technique is that many indents can be placed on a single specimen surface, at preselected locations. It is also a useful means of introducing secondary cracks that can be driven across the natural ﬁssures, in order to probe interface properties. Some 100 test indents were made adjacent to tufts and 150 adjacent to margin cracks. Corner cracks from control indents placed in apparently defect-free regions of the transverse sections were largely symmetrical and extended a distance 100720 mm away from the indent center, so those from the actual test indents invariably intersected the tuft or margin crack interfaces. The indented surfaces were gold coated for examination by optical microscopy and scanning electron microscopy (SEM).

3. Results

3.1. Observations of microstructure in sectioned specimens

Selected teeth were sectioned to reveal the internal microstructure. Fig. 2 is a transverse section of a non-indented third molar, cut 2.0 mm below the top of the most prominent cusp. The amount of enamel removed is just sufficient in this case to expose the dentin. The contrast fringes in the enamel coat are ‘‘Hunter–Schreger’’ bands, regions of differentiating light reflection where the orientation of prisms changes direction (Osborn, 1981; Koenigswald et al., 1987). Fig. 1. Schematic of enamel cracks formed by occlusal contact. Grey areas Also faintly visible in Fig. 2 are tufts, as crack-like intrusions represent cracks. Black area below contact is plastic zone from which median cracks initiate, white region at lower surface of coat is newly initiated radial crack. into the enamel from the EDJ. These are seen more clearly in Fig. 3, a higher magnification view of the EDJ region of another third molar tooth, sequentially sectioned after loading to 400 N. Transverse sections were cut at depths (a) 2.0 mm, (b) 2.5 mm correlating the fractures with pre-existing tuft patterns. Explora- and (c) 3.0 mm beneath the most prominent, loaded cusp. Three tory indentation cracks in the vicinity of the tufts and ensuing particularly large tufts are designated by T. The tufts have a wavy cracks enable us to probe the nature of the internal interfaces, appearance, reflecting the underlying undulations in prism with particular attention to the role of organic filler and prism orientation. Note the disjointed nature of some of these defects, decussation. We demonstrate that cracks in enamel may be with deflections and bridging along the weak inter-prism inhibited by various elements of the microstructure, notably pathways. It is pertinent that the tuft patterns are more or less by intrinsic self-healing as well as by stress-shielding and maintained in successive sections, notwithstanding the above- decussation. mentioned deflections, although some coalescence has occurred in (c). This sequence indicates a certain degree of continuity

2. Materials and methods (albeit disjointed) along longitudinal planes containing the tooth axis. Third-molar teeth for study were provided by the American Dental Association Fig. 4 is a segment of yet another third molar tooth, sectioned (ADA) laboratories at the National Institute of Standards and Technology (NIST), to depth 4.4 mm, after loading to 450 N. In this case the tooth taken from a pool of human male and female patients 18–25 years old. These teeth fractured along the side wall by margin cracking, traces of which were screened for visible pre-existing damage, and 25 relatively undamaged ones were selected for testing. The average tooth width was 10 mm and crown height 7.5 mm. Approval to test these specimens was granted by the NIST Internal Review Board. The teeth were rinsed and kept stored in water prior to testing. These specimens were dried and mounted into epoxy blocks, with roots embedded and cusps uppermost. Each mounted tooth was then loaded in a mechanical testing machine until cracking occurred around a side wall. The teeth were loaded normally at their most prominent cusps with a metal disk or spherical indenter, similar to earlier studies on model glass/epoxy dome structures simulating all-ceramic dental crowns (Qasim et al., 2006, 2007). In those earlier studies, it was found that the nature of the indenter and the axis of loading were of secondary importance to the essential margin crack geometry. Thus, although a somewhat simplistic representation of actual occlusal loading, our test configuration introduced well-defined cracks for investigating morphological influences with minimal geometrical complication. Water from a squirt bottle was used to keep the specimens moist throughout the mechanical testing. Load was applied until crack patterns of the type depicted in Fig. 1 developed on the enamel surface. Both median and margin cracks were observed, but the latter tended to be the first to run along the full length of the side wall of the enamel adjacent to the loaded cusp, generally at 400–600 N, and so constituted the dominant fracture mode (Lee et al., 2009). At this stage, the specimens remained fully intact without any signs of spalling. Most specimens were set aside for immediate sectioning, while others were stored in water for later examination. Sectioning was performed by conventional grinding and polishing protocols. Longitudinal and transverse sections were made parallel and perpendicular to the tooth axis, respectively. Final polishing was made with diamond paste to 1 mm Fig. 2. Stitched optical microscope image of transverse section through non- finish. indented human molar, depth 2.2 mm below cusp, exposing dentin (dark central Vickers indentations were placed into some of the sections at a load of 10 N, at region). Note faint Hunter–Schreger bands, indicating decussation of prisms. Note distances 60715 mm between impression center and tuft or margin crack traces. also the tufts emerging into the enamel from the enamel–dentin junction (EDJ). ARTICLE IN PRESS

S. Myoung et al. / Journal of Biomechanics 42 (2009) 1947–1951 1949

Fig. 4. Section of tooth loaded to 450 N and sectioned to depth 4.4 mm below cusp, showing tufts emerging from EDJ plus margin cracks M.

3.2. Microindentation experiments

Fig. 5 shows an indentation placed immediately adjacent to a large tuft, in a transverse section 2.2 mm below the cusp. We chose this particular indentation for illustration because it demonstrates both delamination and penetration of the tuft interface. The corner cracks in the optical micrograph in Fig. 5a are still well formed but not symmetrical, indicating some interaction with the tuft interface. The upper and lower crack arms have bent toward the tuft, reminiscent of chipping cracks near free surfaces or low-modulus interfaces (Lardner et al., 1990; Chai and Lawn, 2007). The crack at left has bifurcated into two main arms, one of which has penetrated through the tuft wall, indicating that there must be some solid material within the interface providing crack-wall adhesion. This bifurcation of the crack pattern occurred in 20% of the tests, apparently indicative of some interaction with the low-modulus tuft interface. In Fig. 5a, traces of the prism boundaries are evident, and the cracks have largely followed inter-prism paths. The higher magnification SEM view of portion of the field in Fig. 5b reveals crucial details of the crack–tuft intersection. The divergent corner cracks at left of the indentation have intersected the tuft at an angle. The uppermost of these cracks has arrested at the tuft, while the lowermost one has propagated through the tuft into the adjacent enamel. Most importantly, the tuft has delaminated between these two crack intersections. Hence the tuft must contain enough adhesive material to allow transfer of stress across the interface, but be sufficiently weak as to allow for delamination and associated crack penetration. Fig. 6 shows an SEM image of an indentation-generated corner crack entering a tuft at lower right, running along the tuft interface in a series of serrated S-cracks, and finally emerging at upper left in the adjacent enamel. This kind of alternating interfacial crack pattern is reminiscent of the fracture of a brittle adhesive between two stiffer layers, and can be explained in terms of mixed-mode crack instabilities (Chai, 1988). Again, this is evidence for a weak but intact tuft interface. Fig. 3. Series of transverse sections, at depths (a) 2.0 mm, (b) 2.5 mm and (c) Fig. 7 shows optical micrographs of Vickers indentations placed 3.0 mm beneath tooth cusp, loaded to 400 N. Showing tufts as continuous crack- adjacent to remnant margin cracks MM in an aged tooth section. like defects in longitudinal direction. Those marked T appear to have extended This specimen was kept in water for one week after loading to under load. fracture, then allowed to dry out in air for another week, prior to sectioning. SEM observations revealed the presence of matter, are designated by M. These cracks appear to be connected to presumably organic (Sognnaes, 1949; Palamara et al., 1989), within specific tufts at the EDJ. Note that some of the other tufts have the margin crack walls (but not within the Vickers cracks). The extended almost half way across the enamel thickness, suggesting uppermost corner crack in Fig. 7a arrested at the margin crack, some stable extension during the loading. whereas that in Fig. 7b penetrated the interface into the adjacent ARTICLE IN PRESS

1950 S. Myoung et al. / Journal of Biomechanics 42 (2009) 1947–1951

Fig. 6. SEM image of intersection of oblique Vickers corner crack CC (propagating bottom to top) with tuft TT, showing segmented delamination and ultimate penetration of crack into adjacent enamel.

Fig. 7. Optical micrographs of vickers indentations placed adjacent to margin crack MM in transverse section, optical micrograph, showing (a) crack arrest and (b) penetration. Specimen aged in water for one week after fracture, followed by drying in air for another week.

Fig. 5. Vickers indentations placed adjacent to tuft TT in transverse section: (a) optical image and (b) enlarged SEM image. Outline of indent enhanced by white lines in (b). Note delamination at one wall of tuft in (b). EDJ is below lower edge of fractured along their side walls by loading with a flat indenter field of view in this figure. at the most prominent cusp have been sectioned to reveal correlations between the cracks and tufts at the EDJ. It is enamel. This is again consistent with a weak but intact interface, concluded that the tufts act as sources for the cracks that lead analogous to the tuft in Fig. 5. The incidence of corner-crack to failure of the enamel along weak inter-prism pathways under penetration versus arrest or delamination for specimens left for one stress. There are indications from sections such as those in Figs. 3 week in air was 12% (5/41) and for 5 weeks was 36% (29/81). By and 4 that crack extension from the tufts is a progressive process, contrast, in non-aged specimens (0/15) the corner cracks always most likely stabilized by inhibition from decussation bands (Bajaj arrested at margin crack interfaces without penetration. These et al., 2008). Further stabilization may arise from ‘‘stress- results indicate progressive hardening of the filler matter. shielding’’, whereby next-neighbors in crack arrays representative of the tuft ‘‘forests’’ (Fig. 4) screen out the tensile stresses acting on any given member, hence increasing the compliance in the 4. Discussion region of the EDJ and diminishing the crack driving force (Fett and Munz, 1997). This study has explored the relationship between microstruc- The response of corner cracks from Vickers microindentations ture and mechanical response. Molar teeth that have been placed adjacent to tufts is consistent with an interface filled with ARTICLE IN PRESS

S. Myoung et al. / Journal of Biomechanics 42 (2009) 1947–1951 1951 organic matter (Sognnaes, 1949; Palamara et al., 1989). The Bodecker, C.F., 1953. Enamel lamellae and their origin. Journal of Dental Research Vickers corner cracks tend to arrest at the tufts, but if placed 32, 239–245. Chai, H., 1988. Shear fracture. International Journal of Fracture 37, 137–159. close enough can delaminate the tuft boundary or penetrate into Chai, H., Lawn, B.R., 2007. A universal relation for edge chipping from sharp the adjacent enamel. Such competition between delamination and contacts in brittle materials: a simple means of toughness evaluation. Acta penetration for cracks intersecting interfaces is well documented Materialia 55, 2555–2561. Chai, H., Lee, J.J.-W., Kwon, J.-Y., Lucas, P., Lawn, B.R., 2009. A simple model for in the literature, and indicates a weak interface, with toughness enamel fracture from margin cracks. 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