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DOI: 10.1055/s-0045-1809047
Comparative Analysis of Bite Force after Cranioplasty with and without Temporalis Dissection in Large Skull Defects Caused by Decompressive Craniectomy
Abstract
Introduction
Cranioplasty involves repairing the skull defect using an autologous bone flap or synthetic molds. The temporalis muscle, detached during decompressive craniectomy (DC), may be reattached to the bone flap for better cosmetic reconstruction. Along with the masseter and pterygoid muscles, the temporalis muscle significantly contributes to the human bite force. In this study, we analyze patients' bite force in which the temporalis muscle was either dissected and reattached or left undisturbed during cranioplasty.
Materials and Methods
All patients who previously underwent DC for traumatic brain injury or stroke were grouped into two, depending on the method of cranioplasty. In group 1, patients underwent temporalis muscle dissection and reattachment to the bone flap or prosthesis. In group 2, the temporalis muscle was left undisturbed. The bite force of the subjects was measured bilaterally in both groups by a gnathodynamometer before cranioplasty and 3 months after the surgery. We compared the difference in bite force of the subjects individually on both sides, preoperatively and postoperatively, as well as between the groups.
Results
This study included 36 patients over 18 years of age, with 18 patients in each group. Preoperatively, the bite force of all the subjects was decreased on the side of the DC compared with the normal side. After cranioplasty, the bite force significantly improved compared with preoperative values in both groups.
Conclusion
Temporalis dissection can be safely done during cranioplasty. There is improvement in bite force after cranioplasty with or without temporalis dissection.
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Introduction
Decompressive craniectomy (DC) is a common life-saving operation performed to decrease raised intracranial pressure in patients with traumatic brain injury (TBI)[1] [2] [3] and stroke.[4] [5] It most commonly involves removing a large part of the skull, namely fronto-temporo-parietal regions of the skull of least 12 × 15 cm in diameter.[1] The temporalis muscle is dissected off its attachment during this procedure. The exposed dura is then opened and augmented by a dural substitute or a fascia lata graft to accommodate the brain swelling. The dissected temporalis muscle is then placed over the dural substitute. The excised bone flap is stored in the anterior abdominal wall or bone bank.
Cranioplasty (CP) is the surgery performed to repair this skull defect following recovery. It involves replacing the bone flap or a prefashioned synthetic mold into the skull defect. The temporalis muscle can either be dissected off and resuspended or left undisturbed during this procedure. Electromyogram studies in the past have provided sufficient evidence of the role of the temporalis muscle and the masseter to the bite force in humans.[6] In this study, we analyze the effect of temporalis dissection and reattachment during CP on the bite force and compare it to subjects in whom the temporalis was left undisturbed over the dura.
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Materials and Methods
This study was a prospective study done at Government Medical College, Trivandrum, from October 2020 to October 2021. The study was done after obtaining the institution's ethics committee clearance (HEC No-03/03/2021/MCT). The study subjects consisted of patients who underwent DC for TBI or stroke. The inclusion criteria involved fully conscious, oriented, and cooperative patients in the 18 to 65 year age group without any neurobehavioral sequelae of TBI or stroke. Patients with traumatic craniofacial fractures, loss of teeth, artificial dentures, or musculoskeletal disorders were excluded from the study. All patients who underwent surgery of CP were grouped into two. Group 1 had CP with temporalis muscle dissection and reattachment, and group 2 without it. The details of the procedure in each group are described below.
Group 1—Cranioplasty with Temporalis Dissection and Reattachment
The procedure was done under general anesthesia in supine position with the head rotated to the opposite side of the craniectomy defect. A small linearly folded sheet was kept under the shoulder to get some head extension. After that, the cranial and abdominal incision site was cleansed and draped. The skin incision was made over the initial DC incision, and the flap was raised. The flap was dissected from all sides exposing all the bony edges of the craniectomy defect. After placing retraction sutures over the skin flap, attention was focused on the dissection of the temporalis muscle. The superior edge of the temporalis was initially palpated with a dissector and slowly incised at the superior part, where it blended closely with the underlying dura. This incision was dissected anteriorly and posteriorly to release the entire muscle from the synthetic dura ([Fig. 1A]). The muscle was dissected inferiorly, where the inferior end of the craniectomy was then exposed near the zygomatic arch. While this procedure was done at the cranial end, the second surgeon at the abdominal end harvested the bone flap from the anterior abdominal wall where it was placed during the initial DC. This bone flap was then cleaned thoroughly with betadine and saline. The bone flap was then temporarily placed over the craniectomy site, and the previous site of attachment of the temporalis muscle was marked. A linear array of small holes was created with the electric drill. The temporalis muscle was then anchored over the bone flap by passing several interrupted sutures through these newly created linear arrays of holes ([Fig. 1B]). The edges of the bone flap are then fixed to the cranium with the help of titanium plates and screws. The final construct with the anchored bone flap with the temporalis is depicted in [Fig. 1C]. A suction drain was kept over the bone, and then the skin wound was then closed in layers.


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Group 2—Cranioplasty without Temporalis Muscle Dissection
This method of CP is done in the same steps as mentioned above until the temporalis dissection part. In this method, after raising the skin flap, all the margins of the craniectomy are well-defined except for the inferior part, which is hidden by the overlying temporalis muscle. The temporalis muscle overlying the dural substitute (kept during the initial DC) is left undisturbed. The bone flap is harvested from the abdominal wall and thoroughly cleaned with betadine and saline. This is then anchored to the craniectomy defect by titanium plates and screws. In the case of a customized implant, it is placed directly over the defect without dissection of the temporalis muscle ([Fig. 1D]). A suction drain is kept, and the wound is closed in layers.
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Gnathodynamometery
The measurement of human bite force is done using a gnathodynamometer. In our case, this was done by a gnathodynamometer obtained from Safal Enteprise Inc. ([Fig. 2]) The measurements were conducted in the area of the left and right first permanent molars or the adjacent teeth (second primary molars). The participant was asked to bite on the segment of the gnathodynamometer with maximal occlusal strength. The measurement was repeated three times with an interval of 10 seconds. The mean was taken as the final value, which was determined in kilograms. The patients were then taken up for CP by any one of the methods described above, depending upon the preference of the surgeon. After the procedure, the patients were followed up in the outpatient department. Three months later, the measurements of the bite force were repeated on both sides. The difference in the bite force over both sides was compared. This procedure was followed in patients who undergo CP without temporalis dissection too. The difference in bite force was compared between the two groups.


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Statistical Analysis
All data were entered into an Excel sheet and analyzed using the statistical software SPSS version 26. The continuous variables were expressed in means and standard deviation. The qualitative variables were expressed in proportions. The mean difference in bite force before and after CP was measured in the group with and without CP using a paired sample t-test. The difference in means between the two groups was compared using the independent sample t-test.
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Results
There were 36 subjects enrolled in the study. There were 29 males (80.56%) and 7 females (19.45%). The mean age of the male participants was 33.76 years, whereas the females had a mean age of 39 years. Thirty patients underwent DC for TBI and six for ischemic stroke. Seventeen patients underwent CP on the left and 19 on the right. There were 18 patients in each group. No patients had any ventriculomegaly or post-DC hydrocephalus. In total, 13.89% of the population were hypertensive, 8.33% of the population were diabetic, and 2.78% of the population had history of seizures. 69.44% of people had no comorbidities. There were no postoperative complications in any group. The baseline demography of the subjects in each group is depicted in [Tables 1] and [2]. No randomization was done to select the type of CP in each subject as this was subject to surgeons' preference.
Abbreviations: CVA, cerebrovascular accident; DM, diabetes mellitus; F, female; HTN, hypertension; L, left; M, male; Post-op, postoperative; Pre-op, Preoperative; R. right.
Abbreviations: CVA, cerebrovascular accident; DM, diabetes mellitus; F, female; HTN, hypertension; L, left; M, male; Post-op, postoperative; Pre-op, preoperative; R, right.
Group 1
There were 18 patients in this group. Among them, there were 14 males and 4 females. The mean age of the participants in this group was 33.72 years (standard deviation [SD]: 11.8 years). The mean duration from DC to CP in this group was 9 ± 7.22 months. Seven patients underwent CP on the left side, and 11 patients underwent CP on the right side. The preoperative mean bite force in this group was 21.17 (SD: 9.37) on the operated side and 25.25 (SD: 13.85) on the nonoperated side. The mean bite force improved to 25.55 (SD: 11.6) on the operated side and 27.43 (SD: 14.1) on the nonoperated side. The difference is depicted in the box plot in [Fig. 3]. The improvement was analyzed statistically using paired sample t-test and was found to be statistically significant for both the operated side (p = 0.023) as well as the nonoperated side (p = 0.001; [Table 3]).


Abbreviation: SD, standard deviation.
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Group 2
There were 18 patients in this group. Among them, there were 15 males and 3 females. The mean age of the participants in this group was 35.83 years (SD: 9.85 years; p = 0.56). The mean time duration for CP after DC was 12 ± 7.7 months in this group. Ten patients underwent CP on the left side, and eight patients underwent CP on the right side. The preoperative mean bite force in this group on the operated side was 20.17 (SD: 10.19) and 32.4 (SD: 15.83) on the nonoperated side. The mean bite force improved to 23.92 (SD: 11) on the operated side and 32 (SD: 15.36) on the nonoperated side. The difference is depicted in the box plot in [Fig. 4]. The improvement in bite force after CP within the group was statistically significant on paired sample t-test for the operative side (p = 0.001) but not on the nonoperative side (p = 0.829; [Table 3]). There were no postoperative complications in this group.


The mean difference in preoperative and postoperative bite force in group 1 was 4.38 (SD: 7.45) and 3.75 (SD: 6.83) in group 2. This difference was compared using an independent sample t-test and was not statistically significant (p = 0.794).
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Discussion
Methods of CP after DC described in the literature have been diverse. Several types of CP materials have been described ranging from autologous bone grafts to prosthetic materials like titanium, PEEK, ceramic molds, etc. The essential surgical steps of the procedure are more or less the same except for the part which deals with the temporalis muscle is concerned.[7] Some surgeons prefer to meticulously dissect the plain between the muscle and the underlying dura and reattach the muscle to the autologous bone or newly paced cranial prosthesis during CP,[8] [9] [10] while others may not try this maneuver in fear of causing damage to the underlying brain resulting in an intracerebral hematoma.[7] Temporalis muscle resuspension during CP has been shown to have a better cosmetic outcome,[11] but the value of this procedure in the improvement of bite force has not been studied well in adults. Jin et al studied the effect of temporalis reflection on cerebral blood flow, symmetry, and functional independence after CP.[12] They found no difference in the cranial symmetry between individuals in whom the temporalis muscle was reflected or not. However, they noted a significant improvement in cerebral blood flow and functional independence scale in patients in whom the temporalis was reflected and reattached during CP. Martini et al evaluated the role of temporalis osteosynthetic fixation upon bite force in children who underwent correction of craniosynostosis.[13] Their study included children with craniosynostosis in whom only a fronto-basal advancement was necessary to correct the cranial deformity. In their cohort, only the anterior belly of the temporalis was detached and reattached. In our study, we examine the effect of entire temporalis muscle detachment and refixation performed during CP on the stomatognathic system, a study that has not been performed so far.
The maximal voluntary bite force is a vital determinant of masticatory function.[14] It is defined as the forces exercised by the muscles of mastication in normal occlusion.[15] The bite force is used to evaluate oral function in relation to occlusal factors,[16] [17] dentition,[18] [19] dental prostheses,[20] [21] implant treatment,[22] [23] orthognathic surgery,[24] [25] oral surgery,[26] temporomandibular disorders,[27] [28] and neuromuscular disease.[29] It has considerable influence on the masticatory performance of the individuals.[30] There is a significant correlation between bite force and muscle activity, and the amount of muscle contraction is an indication of how forcefully an individual can bite[14] and a superior masticatory system leads to a stronger bite force.[31] The temporalis muscle is one of the vital muscles of mastication.[32] [33] The anterior and the middle fibers act to elevate the mandible, whereas the posterior fibers retract the mandible. Balance activity occurs in all three parts of the temporalis muscle (anterior, middle, and posterior) at rest and during habitual clenching, and the posterior part of the muscle plays a dominant role during clenching with the mandible in the retruded position.[34] The temporalis resuspension, hence, seems logically essential in restoring the normal bite force after CP.
Several techniques of temporalis muscle fixation have been proposed during craniotomy closure. The most commonly employed method worldwide was described by Spetzler and Lee, which proposed the fixation of temporalis muscle and fascia to a superior cuff of the leftover rim of temporalis muscle and fascia during initial craniotomy.[35] Other techniques described involve suturing the temporalis fascia to microscrews inserted above[36] or below[37] the superior temporal line, suturing the muscle to contourable titanium strut plate[38] [39] and trans-osseous reconstruction of temporalis muscle by suturing it to the newly drilled holes.[40] In our series, the anchoring was done similar to the method described by Brunori et al, which is by drilling holes through the bone and suturing the muscle to it.[40] Our technique described in group 1 is very similar to the one described earlier by Spetzler and Lee. In group 2, we placed the bone flap in a “pericranial on lay” fashion described earlier by Gordon et al.[41]
There are several authors who do not agree with the idea of temporalis resuspension. They would abstain from dissecting the intensely adherent temporalis muscle from the synthetic dura. In our study, this was not a problem as we used a double layer of synthetic dura (G Patch, Surgiwear Inc.) during the initial DC. This method, which was described earlier by our institution as well as by other researchers, was found to facilitate CP with ease as the plain between the two dural prostheses is easy to dissect.[42] [43]
The normal occlusive bite force in adults depends on age,[44] dentition,[45] and gender.[46] Females have lower bite forces compared with males due to lower jaw surfaces and a decrease in muscle mass. There is generally not much difference between the two sides in an individual, as determined by the previous authors.[46] In our cohort, the occlusive force determined by gnathodynamometery on the nonoperated side was normal.
There was a significant difference in bite force between the operated and nonoperated sides. This difference in bite force is presumed to be due to the temporalis muscle dysfunction precipitated by the temporalis dissection performed during the initial DC. Oikawa et al described the retrograde temporalis dissection method, which preserves the deep temporal nerves and arteries during the procedure, thereby reducing the atrophy in the postoperative period.[47] In our institution, we usually perform DC as a life-saving procedure in an emergency. The temporalis is usually reflected down along with the scalp as a myocutaneous flap with an electrocautery. This might have added to the temporalis muscle dysfunction and the consequent low bite force on the operated side.
There was an improvement in bite force on both the operated and nonoperated sides in both the groups with and without temporalis dissection. The difference in the means between groups was not statistically significant. The improvement in the side of the temporalis resuspension (group 1) might be due to remodeling of the original structure of the stomatognathic system.
Limitations of the Study
This was a study with a small sample size that examined the role of temporalis dissection and reattachment and its influence on the bite force of individuals. No proper randomization technique was employed in this study as it involved several neurosurgeons who preferred their own technique of CP. A larger sample size and proper randomization would have been more appropriate to reveal a statistical difference in bite force between the two methods.
The patients enrolled in this study were diverse in age and gender. It is not appropriate to have a blanket value of bite force as a standard, as considerable variability exists between groups and within each group. However, we give a rough estimate of the fact that there is some improvement in bite force, comparing it with the preoperative values. The cosmetological factor, which is considered to be the main factor while evaluating the outcome of CP, was not analyzed. However, earlier studies have shown that no significant difference in cranial symmetry occurs between the two choices of temporalis dissection.[12] Although we have not evaluated it scientifically, based on our wide experience in managing TBI and performing CP, we concur with the findings of this study.
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Conclusion
The temporalis reflection and reattachment during CP is safe. There is a trend toward improvement in bite force in patients either with or without temporalis resuspension following CP. A larger number of patients is required in each group to quantify a meaningful difference in bite force between either of the methods of CP.
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Conflict of Interest
None declared.
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- 7 Honeybul S. Management of the temporal muscle during cranioplasty: technical note. J Neurosurg Pediatr 2016; 17 (06) 701-704
- 8 Hönig JF. V-tunnel drill system in craniofacial surgery: a new technique for anchoring the detached temporalis muscle. J Craniofac Surg 1996; 7 (02) 168-169
- 9 Barone CM, Jimenez DF, Boschert MT. Temporalis muscle resuspension using titanium miniplates and screws: technical note. Neurosurgery 2001; 48 (02) 450-451
- 10 Van Kouwenberg E, Kotamarti V, Reinhardt M, Adetayo OA. Cranial suture anchor temporalis resuspension: a new technique to reconstruct temporal hollowing after craniotomy. J Craniofac Surg 2019; 30 (06) 1696-1699
- 11 Yang J, Yang X, Wang J. et al. Surgical technique of temporal muscle resuspension during cranioplasty for minimizing temporal hollowing: a case series. Front Surg 2022; 9: 996484
- 12 Jin Y, Jiang J, Zhang X. Effect of reflection of temporalis muscle during cranioplasty with titanium mesh after standard trauma craniectomy. J Craniofac Surg 2016; 27 (01) 145-149
- 13 Martini M, Wiedemeyer V, Heim N, Messing-Jünger M, Linsen S. Bite force and electromyography evaluation after cranioplasty in patients with craniosynostosis. Oral Surg Oral Med Oral Pathol Oral Radiol 2017; 124 (06) e267-e275
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References
- 1 Hawryluk GWJ, Rubiano AM, Totten AM. et al. Guidelines for the management of severe traumatic brain injury: 2020 update of the decompressive craniectomy recommendations. Neurosurgery 2020; 87 (03) 427-434
- 2 Sahuquillo J, Dennis JA. Decompressive craniectomy for the treatment of high intracranial pressure in closed traumatic brain injury. Cochrane Database Syst Rev 2019; 12 (12) CD003983
- 3 Hutchinson PJ, Kolias AG, Tajsic T. et al. Consensus statement from the International Consensus Meeting on the Role of Decompressive Craniectomy in the Management of Traumatic Brain Injury: Consensus statement. Acta Neurochir (Wien) 2019; 161 (07) 1261-1274
- 4 Lin J, Frontera JA. Decompressive hemicraniectomy for large hemispheric strokes. Stroke 2021; 52 (04) 1500-1510
- 5 van der Worp HB, Hofmeijer J, Jüttler E. et al. European Stroke Organisation (ESO) guidelines on the management of space-occupying brain infarction. Eur Stroke J 2021; 6 (02) XC-CX
- 6 Gonzalez Y, Iwasaki LR, McCall Jr WD, Ohrbach R, Lozier E, Nickel JC. Reliability of electromyographic activity vs. bite-force from human masticatory muscles. Eur J Oral Sci 2011; 119 (03) 219-224
- 7 Honeybul S. Management of the temporal muscle during cranioplasty: technical note. J Neurosurg Pediatr 2016; 17 (06) 701-704
- 8 Hönig JF. V-tunnel drill system in craniofacial surgery: a new technique for anchoring the detached temporalis muscle. J Craniofac Surg 1996; 7 (02) 168-169
- 9 Barone CM, Jimenez DF, Boschert MT. Temporalis muscle resuspension using titanium miniplates and screws: technical note. Neurosurgery 2001; 48 (02) 450-451
- 10 Van Kouwenberg E, Kotamarti V, Reinhardt M, Adetayo OA. Cranial suture anchor temporalis resuspension: a new technique to reconstruct temporal hollowing after craniotomy. J Craniofac Surg 2019; 30 (06) 1696-1699
- 11 Yang J, Yang X, Wang J. et al. Surgical technique of temporal muscle resuspension during cranioplasty for minimizing temporal hollowing: a case series. Front Surg 2022; 9: 996484
- 12 Jin Y, Jiang J, Zhang X. Effect of reflection of temporalis muscle during cranioplasty with titanium mesh after standard trauma craniectomy. J Craniofac Surg 2016; 27 (01) 145-149
- 13 Martini M, Wiedemeyer V, Heim N, Messing-Jünger M, Linsen S. Bite force and electromyography evaluation after cranioplasty in patients with craniosynostosis. Oral Surg Oral Med Oral Pathol Oral Radiol 2017; 124 (06) e267-e275
- 14 van der Bilt A, Tekamp A, van der Glas H, Abbink J. Bite force and electromyograpy during maximum unilateral and bilateral clenching. Eur J Oral Sci 2008; 116 (03) 217-222
- 15 Subramaniam P, Girish Babu KL. Ifzah, Evaluation of occlusal forces in different stages of children - an exploratory study. Saudi Journal of Oral Sciences 2018; 5 (01) 11
- 16 Tsuga K, Carlsson GE, Osterberg T, Karlsson S. Self-assessed masticatory ability in relation to maximal bite force and dental state in 80-year-old subjects. J Oral Rehabil 1998; 25 (02) 117-124
- 17 Bakke M, Holm B, Jensen BL, Michler L, Möller E. Unilateral, isometric bite force in 8-68-year-old women and men related to occlusal factors. Scand J Dent Res 1990; 98 (02) 149-158
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