Abstract
Objective
Sutures are fibrous joints connecting the bones of the head. Despite the fundamental role played by sutures in dentofacial orthopaedics, their biomechanical properties are not completely understood. This study evaluated anatomy, biomechanics, and acoustic emission (AE) during distraction of the sutural ligament (SL).
Methods
Seventy-two suture samples were removed from a twelve-months-old swine ( Sus scrofa ) head. Each volume was acquired using micro-computed tomography (μCT), and the linear interdigitation index was calculated on both planes ( LII COR and LII SAG ). Mechanical testing till failure was carried at 1 mm/min, and four piezoelectric sensors were used for recording of amplitude ( A ), duration ( D ), and energy ( E ) of AE. The relationships between interdigitation, fracture types, tensile stress ( σ 0 ), and AE were statistically analysed with non-parametric tests ( α = 0.05).
Results
σ 0 of the SL had median values of 4.0 MPa, and AE were characterised by A of 49.3 dB (IQR = 2.2), D of 826.3 μs (IQR = 533.4), and E of 57,715.8 eu (IQR = 439,613.5). Most of the fractures happened in the SL (46%), some within the bone (34%), and fewer were combined (19%). LII COR had correlation with A (0.383, p = 0.028), D (0.348, p = 0.048), and E (0.437, p = 0.011) of the AE, and σ 0 had similar relationship with A (0.500, p = 0.003), D (0.495, p = 0.003), and E (0.579, p < 0.001). Maximum energy values were different between fractures within the bone and within the SL (p = 0.021).
Significance
Biomechanical properties under tension of most of the sutures of the craniofacial skeleton were reported. AE provided information about the sequence of events during SL distraction, and had significant relationship with its mechanical properties. Further studies are necessary to confirm these preliminary findings, and to identify their relationship with biological processes and dentofacial treatments.
1
Introduction
Cranial sutures are articulations joining bones of the head through a sutural ligament (SL). Two main approaches may exist to the biomechanics of the sutures: the first one considering their function in the sutural system of the craniofacial skeleton as a whole e.g. , suture system biomechanics, the second one isolating them as single entity e.g. , suture biomechanics. Studies in both humans and mammalian animals have evaluated the suture system biomechanics mainly in shock absorption during impacts , in presence of pathologies affecting sutural growth , during rapid maxillary expansion (RME) or during mastication . In this context, the suture is not interpreted as a single functional unit, and thus its extraction from the suture is required to test the mechanical properties of its SL per se .
The morbidity of suture alterations include severe function impairment and even mortality , and SL mechanical characterisation is of primary importance to optimise treatments such as sutural distraction osteogenesis (SDO) , which relies on the application of tensile stress on the SL to promote bone generation. Despite the first report of SDO through RME could be traced back to 1860 , and it has become a routinely treatment since the 60s , performing distraction of suture other than the maxillo-maxillary one only came in a rather late stage and has been less frequently applied . However, mechanical studies on single suture samples in humans were focused on impacts , nano-indentation , or bending , whereas all domains sparsely oriented to SDO. In animals, interest was primary towards impact or bending as well, and the few studies on tension at low velocities involved only the parieto-parietal , fronto-parietal , and fronto-frontal suture . However, SDO is based on tensional forces, and each suture may have specific requirements for optimal mechanically-induced osteogenesis . As a consequence, a comprehensive mechanical assessment of all the sutures is probably the first move towards a more calibrated application of forces in clinical treatments.
Nevertheless, classical mechanical investigations or even sub-cutaneous strain gages , traction callipers , X-rays , magnetic resonance and ultrasounds , may have limitations in providing stress-related information. The acoustic emission (AE) technique is a non-destructive test (NDT) based on the detection of energy release in the form of sound waves during deformation of materials ( Fig. 1 ). One of the first report in the literature of AE applied on bone is attributed to Hanagud et al. in the 70s . Then, AE has also demonstrated to find useful application in joints and tendons , providing additional information beyond the load-displacement evaluation. Later, Cormier et al. extended the application of AE analysis to facial bones , but neglected to consider any relationship with the sutures. Very recently, Savoldi et al. attempted the use of AE sensors to detect the stress distribution in the craniofacial skeleton of a swine model during RME . However, no prior art seems to be available in the published literature relatively to AE technique application to evaluate mechanical properties of a single suture unit.
2
Materials and methods
2.1
Specimen preparation and experimental setup
One swine head of a just-suppressed twelve-months-old domestic pig ( Sus scrofa ) was studied in agreement with the local regulation concerning the use of animals for research purposes. Mandible and soft tissues were removed with scalpel blade. Two specimens (A and B) were removed from each suture either on the rostral and caudal region of single sutures, or on the left and right side for sutures present on both sides of the skull. Seventy-two testing specimens were extracted using a hand-piece air-turbine (PrestoAcqua © II, Nakanishi Inc., Japan) with saline water supply. The orientation of the long side of the specimen was almost perpendicular to the suture main axis, the thickness was determined by the natural anatomy of each region, the width was ≈5 mm, and the length was subsequently standardised at ≈20 mm. The extremities of the specimens were embedded into acrylic resin (Orthoresin © , Dentsply, US) using a custom-made mould, giving to the non-embedded central part a fixed length of 10 mm, and providing connections for mechanical testing ( Fig. 2 ). Specimens were stored at −20 °C and defrosted at room temperature (25 °C) for 8 h in saline solution before the experiment.
2.2
Acquisition of anatomical data
Each specimen’s volume was acquired with micro-computed tomography (μCT) (SkyScan © 1172, Bruker, US). The length of the suture ( l , mm) and the width of the specimen ( w , mm) were measured on the coronal plane parallel to the external surface (COR, l COR and w COR, ), and on the sagittal plane perpendicular to the external surface and to the suture main axis (SAG, l SAG and w SAG ). For measurements, both planes were centred in the middle of the specimen and images were captured using a graphical software (ImageJ ) calibrated on the scale of the μCT acquisition. Respective linear interdigitation index ( LII COR and LII SAG , mm/mm) was calculated, expressed as the ratio between the length of the suture line and the width of the specimen ( LII = l / w ). Interdigitation measurements were used in a further study on the same samples, focused on the anatomical details. After mechanical testing, μCT scanning of the specimens was repeated and the fracture type ( F t ) was determined as internal to the SL (S), internal to the bone (B), or combined (C).
2.3
Acquisition of mechanical data
Tensile tests till failure were carried using a mechanical testing machine (ElectroPuls ® 3000, Instron, US), at constant velocity (1 mm/min) and temperature (25 °C). During tests, specimens were kept moisturised using saline solution spray. Data were acquired at sampling rate of 0.1 kHz, with displacement ( δ , mm) and force ( F , N) recording. Ultimate stress ( σ , MPa), based on the maximum force, was calculated relatively to both geometrical ( S G , mm 2 , w COR × w SAG ) and actual cross-sectional areas from μCT images ( S 0 , mm 2 ). Necking or drawing of the gage section of the specimens during loading were assumed to be negligible and stress ( σ ) was defined as σ G = F/S G and σ 0 = F/S 0 respectively.
2.4
Acquisition of AE data
Four piezoelectric sensors (CH1, CH2, CH3, and CH4) with frequency range 20–450 kHz and frequency peak at 275 kHz (VS45-H, Vallen Systeme © , Germany) were stabilised with tape on the jigs, and contact was enhanced by means of AE coupling gel. Four screws were used to hold the extremity of the specimen, acting on the acrylic resin block ( Fig. 2 ). Sensors were connected to the AE system (AMSY-6, Vallen Systeme © , Germany), with 32 dB amplification gained with four external pre-amplifiers (AEP5, Vallen Systeme © , Germany). Background noise threshold was fixed at 32 dB according to the maximum noise during a simulated test without specimen, and a layer of anti-shock rubber was placed in between both the upper and lower connections of the jig with the testing machine. The data were collected with continuous recording at sampling rate of 10 MHz. The mechanical testing machine was connected to the AE system with a BNC analogue cable. AE amplitudes ( A , dB), duration ( D , μs) and energy ( E , eu, where 1 eu = 1 nVs ) were analysed with dedicated software (VisualAE © , Vallen Systeme, Germany).
2.5
Statistical analysis
Variables ( Table 1 ) were analysed using statistical software (SPSS © , IBM, USA) with significance set at α = 0.05. Normality of the distribution was verified with the Shapiro–Wilk test. The Wilcoxon signed rank test for related samples was used to study differences between A and B samples. The Kruskal–Wallis test was used to compare F t with median values of LII COR , LII SAG , σ G , σ 0 , A , D, E , and the Mann–Whitney test was used in the respective post hoc evaluation with the Bonferroni correction of significance ( α = 0.05/ n = 0.017, where n = number of categories), AE maximum values ( A max , D max , E max ) between fracture internal to the bone and internal to the SL were compared with independent samples Student’s T-test. Correlation between continuous variables was analysed with the Spearman-Rho test.
| Variable | Abbreviation | Unit | Formula a | Categories b | ||
|---|---|---|---|---|---|---|
| Independent | Anatomical | Suture | N/A | N/A | ||
| Linear interdigitation index (coronal) | LII COR | mm/mm | l COR / w COR | |||
| Linear interdigitation index (sagittal) | LII SAG | mm/mm | l SAG / w SAG | |||
| Dependent | Mechanical | Ultimate stress (geometrical) | σ | MPa | F / SG | |
| Ultimate stress (cross-section) | σ 0 | MPa | F / S 0 | |||
| Fracture type | F | N/A | S, B, C d | |||
| AE | Amplitude | A | dB | |||
| Duration | D | μs | ||||
| Energy | E | eu c |
d S = internal to the suture; B = internal to the bone; C = combined.
2
Materials and methods
2.1
Specimen preparation and experimental setup
One swine head of a just-suppressed twelve-months-old domestic pig ( Sus scrofa ) was studied in agreement with the local regulation concerning the use of animals for research purposes. Mandible and soft tissues were removed with scalpel blade. Two specimens (A and B) were removed from each suture either on the rostral and caudal region of single sutures, or on the left and right side for sutures present on both sides of the skull. Seventy-two testing specimens were extracted using a hand-piece air-turbine (PrestoAcqua © II, Nakanishi Inc., Japan) with saline water supply. The orientation of the long side of the specimen was almost perpendicular to the suture main axis, the thickness was determined by the natural anatomy of each region, the width was ≈5 mm, and the length was subsequently standardised at ≈20 mm. The extremities of the specimens were embedded into acrylic resin (Orthoresin © , Dentsply, US) using a custom-made mould, giving to the non-embedded central part a fixed length of 10 mm, and providing connections for mechanical testing ( Fig. 2 ). Specimens were stored at −20 °C and defrosted at room temperature (25 °C) for 8 h in saline solution before the experiment.
2.2
Acquisition of anatomical data
Each specimen’s volume was acquired with micro-computed tomography (μCT) (SkyScan © 1172, Bruker, US). The length of the suture ( l , mm) and the width of the specimen ( w , mm) were measured on the coronal plane parallel to the external surface (COR, l COR and w COR, ), and on the sagittal plane perpendicular to the external surface and to the suture main axis (SAG, l SAG and w SAG ). For measurements, both planes were centred in the middle of the specimen and images were captured using a graphical software (ImageJ ) calibrated on the scale of the μCT acquisition. Respective linear interdigitation index ( LII COR and LII SAG , mm/mm) was calculated, expressed as the ratio between the length of the suture line and the width of the specimen ( LII = l / w ). Interdigitation measurements were used in a further study on the same samples, focused on the anatomical details. After mechanical testing, μCT scanning of the specimens was repeated and the fracture type ( F t ) was determined as internal to the SL (S), internal to the bone (B), or combined (C).
2.3
Acquisition of mechanical data
Tensile tests till failure were carried using a mechanical testing machine (ElectroPuls ® 3000, Instron, US), at constant velocity (1 mm/min) and temperature (25 °C). During tests, specimens were kept moisturised using saline solution spray. Data were acquired at sampling rate of 0.1 kHz, with displacement ( δ , mm) and force ( F , N) recording. Ultimate stress ( σ , MPa), based on the maximum force, was calculated relatively to both geometrical ( S G , mm 2 , w COR × w SAG ) and actual cross-sectional areas from μCT images ( S 0 , mm 2 ). Necking or drawing of the gage section of the specimens during loading were assumed to be negligible and stress ( σ ) was defined as σ G = F/S G and σ 0 = F/S 0 respectively.
2.4
Acquisition of AE data
Four piezoelectric sensors (CH1, CH2, CH3, and CH4) with frequency range 20–450 kHz and frequency peak at 275 kHz (VS45-H, Vallen Systeme © , Germany) were stabilised with tape on the jigs, and contact was enhanced by means of AE coupling gel. Four screws were used to hold the extremity of the specimen, acting on the acrylic resin block ( Fig. 2 ). Sensors were connected to the AE system (AMSY-6, Vallen Systeme © , Germany), with 32 dB amplification gained with four external pre-amplifiers (AEP5, Vallen Systeme © , Germany). Background noise threshold was fixed at 32 dB according to the maximum noise during a simulated test without specimen, and a layer of anti-shock rubber was placed in between both the upper and lower connections of the jig with the testing machine. The data were collected with continuous recording at sampling rate of 10 MHz. The mechanical testing machine was connected to the AE system with a BNC analogue cable. AE amplitudes ( A , dB), duration ( D , μs) and energy ( E , eu, where 1 eu = 1 nVs ) were analysed with dedicated software (VisualAE © , Vallen Systeme, Germany).
2.5
Statistical analysis
Variables ( Table 1 ) were analysed using statistical software (SPSS © , IBM, USA) with significance set at α = 0.05. Normality of the distribution was verified with the Shapiro–Wilk test. The Wilcoxon signed rank test for related samples was used to study differences between A and B samples. The Kruskal–Wallis test was used to compare F t with median values of LII COR , LII SAG , σ G , σ 0 , A , D, E , and the Mann–Whitney test was used in the respective post hoc evaluation with the Bonferroni correction of significance ( α = 0.05/ n = 0.017, where n = number of categories), AE maximum values ( A max , D max , E max ) between fracture internal to the bone and internal to the SL were compared with independent samples Student’s T-test. Correlation between continuous variables was analysed with the Spearman-Rho test.
| Variable | Abbreviation | Unit | Formula a | Categories b | ||
|---|---|---|---|---|---|---|
| Independent | Anatomical | Suture | N/A | N/A | ||
| Linear interdigitation index (coronal) | LII COR | mm/mm | l COR / w COR | |||
| Linear interdigitation index (sagittal) | LII SAG | mm/mm | l SAG / w SAG | |||
| Dependent | Mechanical | Ultimate stress (geometrical) | σ | MPa | F / SG | |
| Ultimate stress (cross-section) | σ 0 | MPa | F / S 0 | |||
| Fracture type | F | N/A | S, B, C d | |||
| AE | Amplitude | A | dB | |||
| Duration | D | μs | ||||
| Energy | E | eu c |
d S = internal to the suture; B = internal to the bone; C = combined.
3
Results
Seventy-two specimens belonging to thirty-six different sutures were analysed. Data sets resulted to be not normally distributed (p < 0.05), non-parametric tests were performed, and results were represented by median values and interquartile range (IQR). Since no significant differences were found between specimens A and B for LII COR (p = 0.934), LII SAG (p = 0.642), σ G (p = 0.406), σ 0 (p = 0.499) , A (p = 0.652), D (p = 0.694), and E (p = 0.947), average values were used to represent each suture ( Table 2 ).
| F t | LII COR | LII SAG | σ G | σ 0 | A | D | E | A max | D max | E max | ||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| (mm/mm) | (mm/mm) | (MPa) | (MPa) | (dB) | (μs) | (eu) b | (dB) | (μs) | (eu) b | |||||
| Suture | General | Median | 2.3 | 3.5 | 3.7 | 3.8 | 50.3 | 855 | 139,835 | 82.6 | 8,442 | 6,435,028 | ||
| IQR a | 2.0 | 3.5 | 3.0 | 2.6 | 4.1 | 661 | 600,553 | 21.4 | 11,024 | 18,170,498 | ||||
| Sutural ligament fracture | Median | 1.3 | 2.8 | 3.9 | 4.0 | 49.3 | 826 | 57,716 | 77.4 | 7,445 | 1,085,317 | |||
| ( F t = S) | IQR a | 1.6 | 3.5 | 2.4 | 2.2 | 3.1 | 533 | 439,614 | 23.6 | 11,572 | 31,713,442 | |||
| Bone fracture | Median | 3.5 | 2.8 | 3.8 | 4.2 | 48.8 | 628 | 94,869 | 83.7 | 10,454 | 7,497,763 | |||
| ( F t = B) | IQR a | 5.6 | 3.7 | 3.9 | 4.8 | 4.8 | 576 | 460,866 | 20.9 | 8,456 | 11,634,627 | |||
| 1 | Anterior maxillo-maxillary | S | 1.1 | 1.5 | 3.7 | 6.0 | 48.1 | 711 | 28,037 | 72.0 | 5,454 | 1,085,317 | ||
| 2 | Anterior maxillo-nasal | S | 1.0 | 1.3 | 2.7 | 3.1 | 45.2 | 218 | 362 | 53.1 | 1,036 | 3,714 | ||
| 3 | Inferior nasal conchae-maxillary | B&C | 1.2 | 4.6 | 11.3 | 8.6 | 50.9 | 1,512 | 2,353,665 | 96.6 | 28,439 | 108,650,000 | ||
| 4 | Palato-palatal | S | 10.8 | 5.1 | 5.7 | 4.6 | 54.6 | 1,614 | 2,715,416 | 98.4 | 17,324 | 53,700,000 | ||
| 5 | Maxillo-lacrimal | B&S | 2.4 | 8.3 | 3.8 | 4.6 | 50.9 | 1,107 | 1,037,000 | 83.6 | 7,211 | 11,590,500 | ||
| 6 | Maxillo-maxillary | S | 2.5 | 4.9 | 1.3 | 1.2 | 51.1 | 1,290 | 908,739 | 83.7 | 17,178 | 11,813,200 | ||
| 7 | Maxillo-nasal | B&C | 2.3 | 4.5 | 4.0 | 3.3 | 51.3 | 965 | 168,926 | 92.7 | 8,548 | 6,470,000 | ||
| 8 | Maxillo-palatal | B | 1.9 | 3.7 | 39.9 | 33.0 | 52.2 | 1,350 | 3,883,959 | 98.7 | 15,013 | 97,600,000 | ||
| 9 | Maxillo-vomeral | S | 2.5 | 4.9 | 0.6 | 0.6 | 46.3 | 425 | 10,719 | 64.7 | 3,038 | 162,940 | ||
| 10 | Maxillo-zygomatic | B | 8.9 | 6.0 | 9.3 | 9.7 | 52.1 | 573 | 656,235 | 100.0 | 39,759 | 202,000,000 | ||
| 11 | Naso-nasal | S | 1.1 | 3.3 | 4.1 | 4.0 | 49.3 | 652 | 39,390 | 71.5 | 4,459 | 426,200 | ||
| 12 | Palato-vomeral | B | 1.1 | 1.0 | 5.5 | 6.2 | 46.9 | 440 | 35,503 | 73.3 | 5,896 | 4,155,525 | ||
| 13 | Zygomatico-lacrimal | B | 7.1 | 5.7 | 4.3 | 4.5 | 50.2 | 906 | 154,236 | 94.1 | 16,538 | 10,840,000 | ||
| 14 | Ethmoido-inferior nasal conchae | B&S | 1.8 | 3.7 | 0.5 | 0.6 | 49.1 | 758 | 595,907 | 70.8 | 5,118 | 6,400,056 | ||
| 15 | Ethmoido-maxillary | S | 1.8 | 4.6 | 4.6 | 4.4 | 51.3 | 1,232 | 70,299 | 82.7 | 7,445 | 1,001,000 | ||
| 16 | Ethmoido-nasal | B | 10.5 | 1.2 | 3.3 | 2.9 | 47.4 | 441 | 1,931 | 58.1 | 1,882 | 13,515 | ||
| 17 | Ethmoido-palatal | B&S | 2.3 | 6.2 | 1.8 | 2.1 | 52.7 | 1,363 | 60,681 | 82.7 | 8,651 | 1,025,000 | ||
| 18 | Ethmoido-vomeral | B | 2.0 | 1.8 | 0.4 | 0.3 | 43.2 | 5 | 10 | 44.1 | 55 | 13 | ||
| 19 | Fronto-lacrimal | C | 4.7 | 4.9 | 6.9 | 8.2 | 56.8 | 1,283 | 1,172,999 | 98.8 | 14,147 | 50,050,000 | ||
| 20 | Fronto-maxillary | C | 3.3 | 3.9 | 2.8 | 3.7 | 48.1 | 320 | 4,462 | 91.8 | 51,962 | 3,680,000 | ||
| 21 | Fronto-nasal | S | 10.3 | 6.7 | 4.4 | 4.5 | 50.3 | 826 | 173,464 | 77.4 | 6,209 | 18,252,850 | ||
| 22 | Lacrimo-ethmoidal | B&C | 3.2 | 2.4 | 0.0 | 0.0 | 43.0 | 2 | 7 | 47.6 | 13 | 16 | ||
| 23 | Palato-sphenoidal | B&C | 1.2 | 3.7 | 2.3 | 2.2 | 53.3 | 1,236 | 125,434 | 92.0 | 10,841 | 8,335,000 | ||
| 24 | Spheno-vomeral | B&C | 3.2 | 3.9 | 3.6 | 3.5 | 53.6 | 884 | 926,295 | 80.1 | 5,865 | 20,921,700 | ||
| 25 | Temporo-zygomatic | S | 1.0 | 1.3 | 3.9 | 3.9 | 51.2 | 1,104 | 9,587 | 82.6 | 8,335 | 165,500 | ||
| 26 | Ethmoido-frontal | S | 1.1 | 1.8 | 0.0 | 0.0 | 44.6 | 499 | 3,580 | 72.4 | 53,969 | 6,101,370 | ||
| 27 | Ethmoido-sphenoidal | B | 4.6 | 5.2 | 0.5 | 0.5 | 47.4 | 682 | 931 | 55.2 | 1,670 | 2,960 | ||
| 28 | Fronto-frontal | C | 1.0 | 1.1 | 0.5 | 0.4 | 43.4 | 58 | 55 | 47.0 | 310 | 328 | ||
| 29 | Fronto-parietal | S | 1.3 | 1.0 | 5.7 | 6.1 | 51.7 | 1,109 | 410,856 | 93.0 | 15,130 | 13,375,000 | ||
| 30 | Fronto-sphenoidal | S | 2.8 | 2.8 | 5.2 | 4.5 | 48.9 | 726 | 57,716 | 72.6 | 4,458 | 1,041,650 | ||
| 31 | Occipito-parietal | B&C | 1.2 | 1.1 | 2.7 | 2.8 | 48.8 | 616 | 289,010 | 72.2 | 8,700 | 19,400,052 | ||
| 32 | Occipito-sphenoidal | S | 1.1 | 1.1 | 2.7 | 3.7 | 48.4 | 1,209 | 504,773 | 92.4 | 21,662 | 12,635,000 | ||
| 33 | Occipito-temporal | C | 3.1 | 3.4 | 5.3 | 5.4 | 53.6 | 1,160 | 217,825 | 92.2 | 11,559 | 12,625,000 | ||
| 34 | Parieto-parietal | S | 1.2 | 1.0 | 1.6 | 1.6 | 48.3 | 686 | 25,683 | 63.3 | 2,557 | 198,010 | ||
| 35 | Parieto-temporal | S | 3.0 | 3.3 | 4.5 | 4.6 | 52.0 | 1,195 | 1,473,070 | 95.7 | 14,279 | 29,075,000 | ||
| 36 | Spheno-temporal | B | 2.3 | 1.9 | 3.3 | 3.8 | 54.6 | 1,582 | 397,985 | 94.8 | 18,989 | 27,255,000 | ||
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