2015; ••: 16: ••–•• 501–512 Pain Medicine 2014; Wiley Periodicals, Inc.
Evaluation of the Treatment Modalities for Neurosensory Disturbances of the Inferior Alveolar Nerve Following Retromolar Bone Harvesting for Bone Augmentation
Shinnosuke Nogami, DDS, PhD,* Kensuke Yamauchi, DDS, PhD,* Shunji Shiiba, DDS, PhD,† Yoshihiro Kataoka, DDS, PhD,* Bunichi Hirayama, DDS,* and Tetsu Takahashi, DDS, PhD* *Division of Oral and Maxillofacial Surgery, Department of Oral Medicine and Surgery, Tohoku University Graduate School of Dentistry, Miyagi and † Division of Dental Anesthesiology, Department of Control of Physical Function, Kyushu Dental University, Fukuoka, Japan Reprint requests to: Shinnosuke Nogami, DDS, PhD, Department of Oral Medicine and Surgery, Division of Oral and Maxillofacial Surgery, Tohoku University Graduate School of Dentistry, Miyagi 980-8575, Japan. Tel: 81-22-717-8350; 81-90-7454-7584; Fax: 81-22-717-8359; E-mail: [email protected]; [email protected].
Methods. One hundred four patients, of which 49 and 55 exhibited vertical or horizontal alveolar ridge defects in the mandible and maxilla, respectively, were enrolled. Nineteen patients underwent block bone grafting, 38 underwent guided bone generation or autogenous bone grafting combined with titanium mesh reconstruction, and 47 underwent sinus floor augmentation. Using a visual analog scale, we examined subjective symptoms and discomfort related to sensory alteration within the area of the NSDs in these patients. NSDs were clinically investigated using a two-point discrimination test with blunt-tipped calipers. In addition, neurometry was used for evaluation of trigeminal nerve injury. We tested three treatment modalities for NSDs: follow-up observation (no treatment), medication, and stellate ganglion block (SGB).
Funding sources: We performed this research without receiving any financial support or incentive from any third party.
Results. A week after surgery, 26 patients (25.0%) experienced NSDs. Five patients received no treatment, 10 patients received medication, and 11 patients received SGB. Three months after surgery, patients in the medication and SGB group achieved complete recovery. Current perception threshold values recovered to near-baseline values at 3 months: recovery was much earlier in this group than in the other two groups. SGB can accelerate recovery from NSDs.
Acknowledgment: This study was approved by the Ethics Committee of Kyushu Dental University (Approval No. 02-12).
Conclusions. Our results justify SGB as a reasonable treatment modality for NSDs occurring after the harvesting of retromolar bone grafts.
Abstract
Key Words. Stellate Ganglion Block; Neurosensory Disturbances; Inferior Alveolar Nerve
Conflict of interest: The authors declare that they have no conflict of interest.
Subjects. The purpose of this study was to evaluate the treatment modalities for neurosensory disturbances (NSDs) of the inferior alveolar nerve occurring after retromolar bone harvesting for bone augmentation procedures before implant placement.
Introduction The increased use of bone augmentation surgery as part of implant treatment has led to an increase in the variety of
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Nogami et al. complications including infection, bone resorption, and neurosensory disturbances (NSDs). NSDs can cause permanent or transient sensory impairment of the inferior alveolar nerve (IAN), which travels within the inferior alveolar canal in the mandible and is supported by the alveolus and the neurovascular bundle. Nerve damage can be classified as paresthesia, dysesthesia, or anesthesia, and its primary iatrogenic causes include the removal of impacted mandibular third molars [1,2], endodontic treatment [3], alveolar nerve blocks [4], and autogenous bone grafting [5]. The use of autogenous bone grafts for the augmentation of resorbed alveolar ridges is still considered the gold standard in implantology. Various extraoral donor sites such as the calvarium, tibia, rib, and iliac crest have been used. Obtaining grafts from these areas usually involves the use of general anesthesia. However, localized bone defects of the alveolar ridge require only a limited amount of bone, and donor sites for these grafts can be found within the oral cavity. A major advantage of an intraoral donor site is that the bone can be harvested under local anesthesia. Several reports on the harvesting of bone grafts from the retromolar region are available [6–13]; however, the complications reported in these studies vary widely, ranging from the absence of complications over impairment of the sensory function of the IAN to mandibular fractures [10,11]. Nkenke et al. reported the rate of complications after retromolar bone graft harvesting and the measurement of changes in the sensory function of the inferior alveolar and lingual nerves; however, they did not report on the treatment for NSDs [5]. Because the goal of implant treatment is to improve the patient’s quality of life, the positive feelings associated with implant treatment, including autogenous bone grafting, cannot be disregarded either. It is therefore essential to discuss the treatment options for NSDs. This prospective study aimed to evaluate the treatment modalities for NSDs of the IAN occurring after retromolar bone harvesting for bone augmentation procedures before implant placement. Patients and Methods Patients The study sample for the present prospective, randomized clinical trial was derived from patients who came to Kyushu Dental University Hospital between October 2002 and November 2011 for evaluation, then conducted detailed evaluations of 104 (54 women, 50 men; mean age 49.9 years; range 20–72 years), of whom 49 had vertical and 55 horizontal alveolar ridge defects. The local ethics committee approved this study, and informed consent was obtained from all patients after they received an explanation of the advantages and disadvantages of treatment. Randomization was done by lot using closed envelopes. All patients were postoperatively evaluated by a single assessor who was blinded to the treatment pro-
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tocol. Nineteen patients (10 women, 9 men) underwent block bone grafting (BG), 38 (20 women, 18 men) underwent guided bone generation (GBR) or autogenous bone grafting combined with stabilization using a titanium mesh, and 47 (25 women, 22 men) underwent sinus floor augmentation (sinus lift; Table 1). In all patients, autologous bone was harvested from the external oblique ridge of the mandibular ramus by an experienced surgeon (last author). All patients provided written informed consent prior to study initiation. Surgical Techniques BG A full-thickness mucoperiosteal flap was elevated and the bone defect was exposed. The cancellous block graft was harvested from the external oblique ridge of the mandibular ramus using a reciprocating bone saw and an oscillating saw and was refined to fit into the defect. In all patients, the recipient site was perforated with a 1-mm diameter round bur to increase blood supply from endosseous vessels to the transplanted bone. Once the graft was placed and stabilized, it was fixed with 1.6 × 10-mm bone screws (Jeil Medical Corp., Seoul, South Korea). The BG was covered with an absorbable collagen membrane (Biomend®; Zimmer Dental Inc., Carlsbad, CA, USA). GBR and Titanium Mesh Reconstruction Augmentations was performed by GBR wherein an autogenous particulate bone graft was harvested from the external oblique ridge of the mandibular ramus using a bone scraper (MX-Grafter®; Maxilon Laboratories, Inc., Hollis, NH, USA) or a reciprocating bone saw and an oscillating saw. The graft materials (Osferion®; Olympus Terumo Biomaterials Corp., Tokyo, Japan) were covered with an absorbable collagen membrane (Biomend®; Zimmer Dental Inc.) or an expanded polytetrafluoroethylene membrane (Gore-Tex®; W. L. Gore Associates, Inc., Flagstaff, AZ, USA) in GBR. In titanium mesh reconstruction, titanium meshes (0.1- or 0.2-mm thickness; M-TAM, Stryker Leibinger GmbH & Co. KG, Freiburg, Germany or ASTM F-67, Jeil Medical Corp.) were used according to the shape of each defect and fixed with small
Table 1 Summary of surgical procedures and mean patient ages Surgical Procedure
Patients
Age
BG GBR, titanium mesh reconstruction Sinus lift
19 38 47
41.9 53.2 54.6
BG = block bone graft; GBR = guided bone generation; sinus lift = sinus floor augmentation procedure.
Neurosensory Neurosensory Disturbances Disturbances of of Inferior Inferior Alveolar Alveolar Nerve titanium screws. In both procedures, decortication of the drill holes was performed using a round bur to ensure vascular nutrition of the grafted bone. Sinus Lift The sinus lift technique was performed according to procedures reported previously [14]. The sinus space was then filled with a mixture of graft materials (Osferion®; Olympus Terumo Biomaterials Corp.) and autologous bone that was harvested from the external oblique ridge of the mandibular ramus using a bone scraper (MX-Grafter®; Maxilon Laboratories, Inc.). Treatment for NSDs We tested three treatment modalities for NSDs: follow-up observation (no treatment), medication, and stellate ganglion block (SGB). The medication used was mecobalamin (Methycobal®, Eisai Co. Ltd, Tokyo, Japan: 1500 μg/day). Patients who experienced NSDs were administered with this at 1 week after surgery, as an NSD appearing soon after surgical intervention might have been due to swelling, surgery in proximity of nerves, or retraction of the soft tissue. SGB was also administered at 1 week after surgery by the dental anesthesiology department of our hospital after receiving patient consent. Patients who did not consent to SGB received no treatment or continued medication, and were observed (no treatment). The SGB technique followed methods described previously [15]. Briefly, each patient was placed supine with the neck slightly hyperextended. The lower jaw was loosely opened to relax the platysma and facilitate palpation of the deep structures of the neck. The tip of the index finger was used to identify the cricothyroid notch and then moved laterally, retracting the carotid sheath and sternocleidomastoid muscle. The C6 anterior transverse process (carotid or Chassaignac’s tubercle-tuberculum caroticum vertebrae cervicalis VI) was then identified and fixed with the palpating finger. A 2.5-cm, 22- or 23-gauge needle was introduced immediately medial to the palpating finger. Contact with the C6 transverse process was made just medial to the tubercle at a depth of approximately 1 cm and a 3-mL quality of 1% lidocaine without epinephrine was injected after negative aspiration. Successful block was ascertained by the development of Claude Bernard-Horner syndrome (Horner’s ptosis) and loss of galvanic skin response and thermography, an increase in skin temperature, and plethysmography. Evaluation of NSDs and Observation Period Visual Analog Scale Using a visual analog scale (VAS), we examined subjective symptoms and discomfort related to sensory alterations within the area of the NSDs. The patients rated their discomfort from 0 (no sensation) to 10 (completely normal sensation).
Two-Point Discrimination Test NSDs were also clinically investigated using a two-point discrimination test with blunt-tipped calipers that were calibrated and applied (by the third author) to provoke a static stimulus. Testing began with application of the caliper points that were placed 20 mm apart. The interprobe distance was then decreased in 2-mm increments, and patients were asked whether they sensed one or two points. Self-Evaluation In addition, patients also provided self-evaluation of spontaneous pain and abnormal sensation 1 week, 1 month, 3 months, 6 months, and 1 year after surgery (Table 2). We used these self-evaluations to determine whether complete recovery had occurred. Neurometry Furthermore, neurometry was performed by an experienced dental anesthesiologist (third author) and also utilized a NeurometerTM® (Neurotron, Baltimore, MD, USA; Figure 1A and B) equipped with a platinum electrode that was placed on the oral mucosa but not the skin. The current perception threshold (CPT) was defined by the intensity of the alignment mode that applies stimulation in both an ascending and a descending manner. The regions tested were mental skin right or mental skin left (Figure 2). Affected sites received three stimulus frequencies that are
Table 2 Self-evaluation of spontaneous pain and abnormal sensation after surgery Relief from spontaneous pain Good Pain was absent 1 year later. Activities of daily living (ADL) were not limited. Fair Pain was reduced and ADL improved, but the patient was still uncomfortable. Poor Pain and ADL did not improve sufficiently. Recovery of sensation Good Complete recovery of sensation. Patients felt normal sensation both at rest and when stimuli were applied. Fair Sufficient, but not complete recovery. Patients were a little irritable because of abnormal sensations. Poor Poor recovery. Patients were still irritable because of abnormal sensations.
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Figure 1A A neurometer as an evaluation tool for trigeminal nerve injury. known to stimulate the A-beta (2,000 Hz), A-delta (250 Hz), and C-fibers (5 Hz). The electrical stimuli were delivered through two 1-cm diameter, disposable, goldplated electrodes placed in close proximity within the affected area. The patient was given a remote device to control delivery of the electrical stimuli. They depressed a button until the threshold of the first sensation around the site of the electrodes was detected; at this point, they released the button to terminate the delivery of electrical current. The instrument began current delivery for each specific frequency at the lowest output intensity, i.e., 0.001 mA, and increased the current until the patient released the remote control button or until the maximum stimulus of 9.99 mA was reached. The neurometer automatically repeated a minimum of three sets of testing for each frequency until the software determined a threshold. During testing, neither the operator nor the patient was aware of the output current intensity. The observation periods were 1 week, 1 month, 3 months, 6 months, and 1 year after surgery.
Figure 1B A platinum electrode connected to the neurometer is placed on the oral mucosa but not the skin. The current perception threshold (CPT) was defined by the intensity of the alignment mode that applied stimulation in both an ascending and a descending manner. 504 4
Statistical Analysis Statistical differences were calculated and analyzed using repeated-measures analysis of variance. Data are presented as means ± standard deviations. Differences were considered statistically significant when the P value was less than 0.05.
Neurosensory Neurosensory Disturbances Disturbances of of Inferior Inferior Alveolar Alveolar Nerve
Table 4 Summary of the surgical procedure and type of harvested bone Surgical Procedure BG GBR, titanium mesh reconstruction Sinus lift
Figure 2 Diagram illustrating the regions tested. MR = mental skin right; ML = mental skin left.
Particulate Bone (%)
Block Bone (%)
0 (0) 27 (71.1)
19 (100) 11 (28.9)
47 (100)
0 (0)
BG = block bone graft; GBR = guided bone generation; sinus lift = sinus floor augmentation.
and abnormal sensation on self-evaluation 1 year after surgery (Table 3).
Results Immediate postoperative infection did not occur in any patient. One week after surgery, 26 patients (25.0%) experienced NSDs of the IAN (Table 3). Five patients received no treatment (19.2%), 10 received medication (38.5%), and 11 received SGB (42.3%). Patient #1 and #2 reported abnormal sensations in the two-point discrimination test as well as spontaneous pain
Table 3
Bone was harvested as particulate bone in 74 patients and block bone in 30. Eleven patients with block bone harvesting underwent GBR and titanium mesh reconstruction (Table 4). Thirteen (20.3%) patients with particulate bone harvesting and 13 (43.3%) with block bone harvesting exhibited NSDs of the IAN (Table 5). Sixteen patients (15.4 %) experienced NSDs of the IAN 1 month after surgery, 11 (10.6%) experienced IAN
Summary of NSDs of the IAN
No.
Surgical procedure
Donor site
Host region
Harvested bone
Treatment
Complete recovery
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26
GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME BG BG BG BG BG BG BG BG BG BG
Right ramus Right ramus Right ramus Right ramus Left ramus Left ramus Right ramus Right ramus Right ramus Left ramus Left ramus Left ramus Right ramus Left ramus Right ramus Right ramus Left ramus Right ramus Left ramus Left ramus Left ramus Left ramus Right ramus Right ramus Left ramus Right ramus
29–31 29–31 29–31 29–31 19–20 18–19 30–31 20–24 19–20 19–21 19–21 30–31 21–24 18–20 29–31 29–31 30 18 31 30–31 30 30 18–19 19 30 19
Particulated Particulated Particulated Particulated Particulated Particulated Particulated Particulated Particulated Particulated Particulated Particulated Particulated Block Block Block Block Block Block Block Block Block Block Block Block Block
No treatment No treatment Medication Medication No treatment No treatment Medication Medication Medication Medication SGB SGB SGB No treatment Medication Medication Medication Medication SGB SGB SGB SGB SGB SGB SGB SGB
○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○
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Table 5 Summary of type of harvested bone and incidence of NSDs
Particulate bone Block bone
NSD (%)
No NSD (%)
13 (20.3) 13 (43.3)
51 (79.7) 17 (56.7)
NSD = neurosensory disturbance.
paresthesia 3 months after surgery, 4 (3.8%) experienced NSDs of the IAN 6 months after surgery, and 2 (2.0%) patients experienced NSD of the IAN 1 year after surgery (Figure 3). One month after NSD onset, the no treatment group comprised four patients, the medication group comprised seven patients, and the SGB group comprised five patients. Three months after NSD onset, the no treatment group comprised four patients while seven patients in the medication group received treatment. One year after NSD onset, NSD of the IAN persisted in two patients in the no treatment group (Figure 4). The VAS score gradually increased in all groups after surgery (Figure 5). In the SGB groups, that score reached 10 (completely normal sensation) earlier than in the other groups. Two-point discrimination values decreased gradually in all groups after surgery. The values in the medication group were lower than those in the no treatment group at every time point after surgery (Figure 6). Significantly higher CPT values were observed after surgery in all groups (Figure 7A–C), and the values in the
Figure 4 Treatment methods for neurosensory disturbances (NSDs) of the inferior alveolar nerve (IAN) (N) at various time points after surgery. SGB = stellate ganglion block.
SGB group were markedly lower than those in the no treatment and medication groups. CPT values before surgery (baseline) were 30.4 ± 1.14, 19.4 ± 1.51, and 20.4 ± 1.67 at 2,000, 250, 5 Hz, respectively, in the SGB group. These values increased to 85.6 ± 3.20, 49.2 ± 1.92, and 54.8 ± 5.06, respectively, 1 week after surgery and decreased gradually thereafter to nearbaseline values of 33.6 ± 1.51, 23.8 ± 2.38, and
Figure 3 Incidence of neurosensory disturbances (NSDs) of the inferior alveolar nerve (IAN) (%). 506 6
Neurosensory Neurosensory Disturbances Disturbances of of Inferior Inferior Alveolar Alveolar Nerve Discussion
Figure 5 Change in visual analog scale (VAS) after surgery. SGB = stellate ganglion block.
24.8 ± 3.83 at 2,000, 250, and 5 Hz, respectively, 3 months after surgery. On the other hand, CPT values remained significantly higher than preoperative values even at 1 year after surgery in the no treatment group.
Figure 6 Changes in two-point discrimination (mm) values after surgery. All data are presented as mean ± standard deviation. One-factor repeatedmeasures analysis of variance was used for comparison with data obtained 1 week after surgery. SGB = stellate ganglion block.
Bone augmentation surgery has become common with an increase in the popularity of implant surgery. The forms of surgery are both numerous and, like implant surgery, invasive, with many reports of complications. NSD of the IAN is one such complication. The incidence of permanent IAN sensory disturbance reportedly ranges from 0.4% to 13.4% [16,17]. In cases where the IAN bundle is exposed during third molar surgery, the incidence of IAN paresthesia after 1 week is reported to be approximately 20% [18]. Chaushu et al. reported NSDs after mandibular molar implant surgery in 12% of patients [19]. The present prospective study was conducted as a clinical investigation of NSDs occurring following retromolar bone harvesting for bone augmentation procedures in a total of 104 patients, in whom autologous bone was harvested from the external oblique ridge of the mandibular ramus and used for bone augmentation of a highly atrophied maxilla or mandible. NSDs persisted in 26 (25.0%) patients for 1 week after surgery and in 2 (2.0%) for at least 1 year after surgery. In those two patients, we discovered that a surgical instrument had made direct contact with the mental foramen during surgical site exposure. Bone harvesting using an MX grafter® (Implatex, Tokyo, Japan) was limited to cortical bone obtained from the external oblique ridge of the mandibular ramus, which was thought to be a contributing factor to the lower NSD incidence (20.3%) compared with that (43.3%) when block bone was harvested using a reciprocating bone saw and an oscillating saw. In one patient (#26), the mandibular canal was exposed during the procedure. When the buccal cortex of the mandible is used as a bone graft material, exposure of the IAN cannot be safely avoided. The average distance of the IAN from the buccal aspect of the mandible in the retromolar region is 2.835 mm [20]. However, a cortical graft thickness of as much as 4 mm has been described [21]. Therefore, exposure of the IAN occurs frequently, sometimes accompanied by massive bleeding because of injury to the inferior alveolar artery [10]. Apparently, modification of retromolar bone harvesting with the trephine bur helps in decreasing sequelae and complications. Lakshmiganthan et al. reported that piezoelectric surgery is a minimally invasive technique that lessens the risk of damage to surrounding soft tissues and important structures such as nerves, vessels, and mucosa [22]. It also decreases damage to osteocytes and permits good survival of bony cells during bone harvesting. However, we used a reciprocating bone saw and an oscillating saw to harvest block bone. Major drawbacks of these techniques are mechanical pressure and vibrations on the bone. When block bone is harvested, not just cortical bone but also cancellous bone is involved, which is thought to increase the risk of NSDs. Alling reported spontaneous recovery to a degree of 96% in the IAN in the first 4–8 weeks after third molar surgery [21]. In this study, we used medication and SGB to decrease the duration of treatment for NSDs of the IAN. The medication used was mecobalamin (Methycobal®), a
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Figure 7 (A–C) Changes in current perception threshold (CPT) values after trigeminal nerve injury. All data are presented as mean ± standard deviation. CPT values at three different frequencies of stimulation (2,000, 250, 5 Hz) increased significantly after surgery. One-factor repeated-measures analysis of variance was used for comparison with preoperative data. Ͻ = P < 0.05. SGB = stellate ganglion block. ◀
B12 vitamin. B12 vitamins are generally used for the treatment of pernicious anemia following gastrectomy. However, in recent years, they are being used for the treatment of peripheral nerve damage, irrespective of the presence or absence of B12 deficiency. In our department, the maximum period of medication was 6 months. Medication was continued for 1 week, and if there was no amelioration of symptoms, SGB was administered to patients after they provided consent. SGB is used for the treatment of idiopathic facial paralysis, migraine, hyperhidrosis, cervico-omo-brachial syndrome, stiff shoulder, Meniere’s disease, and depression [23,24]. The usefulness of SGB as a treatment modality has been widely recognized. However, a certain level of skill and familiarity is necessary for administration. SGB increases tissue blood flow in the head, face, neck, and upper limbs because of its sympatholytic effects [25], and it has been used for the treatment of several types of disorders, including traumatic trigeminal neuropathy [26], post-herpetic neuralgia [27], facial nerve paralysis [28], and progressive facial hemiatrophy [29,30]. The stellate ganglion is composed of cell bodies of the inferior cervical and first thoracic sympathetic ganglia. The associated cerebral vasculature receives noradrenergic sympathetic input mainly through the fibers that originate in the cervical ganglion, accompanies the carotid artery, and projects into the ipsilateral cerebral hemisphere [31,32]. Intracerebral vessels constrict in response to cervical sympathetic stimulation and dilate when these fibers are interrupted [31]. A blockage of the stellate ganglion induces a definite ipsilateral increase in cerebral blood flow, as determined by cerebral scintigraphy [32]. The mechanism underlying the physiological consequences of blockage of sympathetic nerve activity or reversal of overactivity, irrespective of whether the sympathetic disorder causes a critical reduction in cerebral blood flow, may be explained by the subsequent dilation of intracerebral vessels and improvement of cerebral blood flow. Studies have shown that SGB can induce a significant decrease in zero flow pressure, a surrogate marker of cerebral vascular tone, thus improving cerebral perfusion pressure [33]. Quan et al. reported that cervical sympathetic block can significantly dilate cerebral vessels, increase cerebral blood velocity, regulate the imbalance with endothim and calcitonin gene-related protein and excessive expression of neurons’ heat shock 8508
Neurosensory Neurosensory Disturbances Disturbances of of Inferior Inferior Alveolar Alveolar Nerve Nerve protein 70 after global cerebral ischemia-reperfusion injury in rabbits, improve the immune function of erythrocyte of patients with cerebral infarction, regulate the content of substance causing systolic and diastolic vessels in serum such like NO and NOS, and promote neural functional recovery [34]. Some studies have reported that increased tissue blood flow on the ipsilateral side is attributable to the redistribution of tissue blood flow from the contralateral side [35,36]. Recently, Terakawa et al. showed that SGB increases mandibular bone marrow and masseter muscle blood flow on the ipsilateral side and decreases it on the contralateral side through redistribution mechanisms [37]. It is therefore suggested that tissue blood flow in the mental nerve on the contralateral side also decreases after SGB. The IAN passes through the mandibular canal, which is surrounded by hard bone. Damage to the IAN during surgery can be direct mechanical damage or caused by pressure within the mandibular canal from the bony wall, and it includes not only damage to the nerve fibers but also ischemia in the feeding vessels, congestion of veins, and lymph flow blockage. The IAN, surrounded by hard bone, closely resembles the facial nerve, which passes through the facial canal in the temporal bone. It is thought that idiopathic facial paralysis and Ramsay Hunt syndrome occur when ischemia and inflammation in the facial nerve cause localized edema, which, together with compression by the bony wall, leads to secondary ischemia. Constriction caused by the edema and compression leads to the occurrence of facial paralysis [38]. Consequently, because the same symptoms are manifested when the mandibular nerve is damaged, SGB treatment is used in our department to treat IAN paresthesia occurring after bone augmentation surgery. Furthermore, in patients with facial paralysis, SGB increases blood flow in the vessels and tissues and is effective in treating nerve disturbances due to ischemia in the feeding vessels and secondary damage caused by constriction and in regenerating facial nerve fibers that have been subject to Wallerian degeneration. Therefore, it can be inferred from the results of the present study that, in patients with mandibular NSDs, SGB will demonstrate its effectiveness through an expected increase in blood flow in the tissues of the mandibular nerve. The general principle of sensory testing is the evaluation of responses to varied stimuli such as temperature, directional sense, pain, and fine touch to allow for comparisons at different times to determine whether spontaneous changes have occurred. These techniques allow for a subjective quantification of the degree of sensory deficit. Neurosensory testing can be divided into mechanoceptive and nociceptive testing according to the specific receptors stimulated. Mechanoceptive testing includes twopoint discrimination, static fine touch, brush directional sense, and vibration. Nociception includes thermal discrimination and pain (pinprick). The sensory modalities that should be minimally included in neurosensory testing are touch or proprioception for the assessment of A-beta fibers, cold detection or pinprick for the assessment of
A-delta fibers, and heat/pain detection for the assessment of unmyelinated C-fibers. The techniques of clinical sensory testing have been well described in the literature [39,40]. Moving two-point discrimination has also been described as a method of assessing lingual nerve injuries, with some predictive capacity for injuries not likely to resolve spontaneously [41]. These traditional neurosensory testing techniques, however, have some limitations. Two-point discrimination generally records the distance perceived without consideration for the cutaneous pressure threshold. Pressurespecified sensory devices measure the forces applied by the surface area of the instrument at the pressure at which the patient perceives the stimuli. The cutaneous pressure two-point threshold is defined by both pressure and distance measurements [42,43]. Conventional clinical sensory tests have been reported to demonstrate poor reproducibility, low sensitivity, and moderate specificity. There is a need for objective documentation and grading to decrease patient complaints and potential litigation resulting from trigeminal nerve injuries [44]. CPT has been described as an adjunctive diagnostic tool for the assessment of various orofacial pathological disorders such as temporomandibular joint disorders, burning mouth syndrome, oral malignancies, and trigeminal nerve injuries [45]. Modality-specific assessments can differentiate between large-diameter thickly myelinated A-beta fibers, thinly myelinated A-beta fibers, and unmyelinated C-fibers [46]. Heat and very low-frequency electrical stimulation (5 Hz) activate thin unmyelinated C-fibers that comprise up to 90% of the cutaneous nerve fibers. A-delta fibers have a thin myelinated sheath and are activated primarily by cold, fast-onset contact and mediumfrequency electrical stimulus (200 Hz). Beta fibers have a thicker myelin sheath, mediate touch and vibratory sensation, and respond to greater frequency electrical stimulation (2,000 Hz) [47–49]. CPT and clinical neurosensory testing are useful modalities for the assessment of lingual nerve injuries [50]. In the present study, we also used CPT as a quantitative sense test in addition to the VAS and two-point discrimination to evaluate the effectiveness of treatments and found that CPT values gradually decreased in all groups. These values were significantly elevated immediately after injury, followed by a gradual fall at all frequencies in all groups. In particular, recovery from NSDs was the earliest in the medication and SGB group, in which the CPT values at 3 months after surgery were similar to those at baseline. Our results may support SGB as a reasonable treatment modality for NSDs occurring after retromolar bone graft harvesting. Anti-inflammatory medications and steroids were prescribed during the immediate postoperative period. This could have had an effect on inflammation and edema around the injured nerves. Since it was not unified about these postoperative given doses or dosing periods, a
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Nogami et al. detailed examination is required from now on. Because of the small number of patients examined in the present study, it is premature to conclude that a combination of medication and SGB can decrease the duration of treatment for NSDs. In addition, we did not perform a Semmes-Weinstein monofilament test for any of the patients, which is a well-known objective evaluation that can provide important information.
10 Von Arx T, Kurt B. Endoral donor bone removal for autografts: A comparative clinical study of donor sites in the chin area and the retromolar region. Schweiz Monatsschr Zahnmed 1998;108:446–59. 11 Khoury F. Augmentation of the sinus floor with mandibular bone block and simultaneous implantation: A 6-year clinical investigation. Int J Oral Maxillofac Implants 1999;14:557–64.
Conclusion The present results suggest that SGB may be a potent treatment modality for patients with NSDs of the IAN. To obtain additional evidence, further studies concerning the long-term clinical course of SGB treatment for NSDs occurring after retromolar bone graft harvesting are necessary. References 1 Kipp DP, Goldstein BH, Weiss WW. Dysesthesia after mandibular third molar surgery: A retrospective study and analysis of 1377 surgical procedures. J Am Dent Assoc 1980;100:185–92. 2 Gulicher D, Gerlach KL. Sensory impairment of the lingual and inferior alveolar nerves following removal of impacted mandibular third molars. Int J Oral Maxillofac Surg 2001;30:306–12. 3 Giuliani M, Lajoro C, Deli G, Silveri C. Inferior alveolar paresthesia caused by endodontic pathosis: A case report and review of the literature. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2001;92:670– 4. 4 Pogrel MA. The results of microneurosurgery of the inferior alveolar and lingual nerve. J Oral Maxillofac Surg 2002;60:485–9. 5 Nkenke E, Radespiel TM, Wiltfang J, et al. Morbidity of harvesting of retromolar bone grafts: A prospective study. Clin Oral Implants Res 2002;13:514–21. 6 Laskin JL, Edwards DM. Immediate reconstruction of an orbital complex fracture with autogenous mandibular bone. J Oral Surg 1977;35:749–51. 7 Girdler NM, Hosseini M. Orbital floor reconstruction with autogenous bone harvested from the mandibular lingual cortex. Br J Oral Maxillofac Surg 1992; 30:36–8.
12 Misch CM. The harvest of ramus bone in conjunction with third molar removal for onlay grafting before placement of dental implants. J Oral Maxillofac Surg 1999;57:1376–9. 13 Pikos MA. Alveolar ridge augmentation with ramus buccal shelf autografts and impacted third molar removal. Dent Implantol Update 1999;10:27–31. 14 Miyamoto S, Shinmyouzu K, Miyamoto I, et al. Histomorphometric and immunohistochemical analysis of human maxillary sinus-floor augmentation using porous β-tricalcium phosphate for dental implant treatment. Clin Oral Implants Res 2013;24:134–8. 15 Carron H, Litwiller R. Stellate ganglion block. Anesth Analg 1975;54:567–70. 16 Cheung LK, Leung YY, Chow LK, et al. Incidence of neurosensory deficits and recovery after lower third molar surgery: A prospective clinical study of 4338 cases. Int J Oral Maxillofac Surg 2010;38:320– 6. 17 Townend JV. Third molar surgery: An audit of the indications for surgery, post-operative complaints and patient satisfaction. Br J Oral Maxillofac Surg 1995;33:265–8. 18 Tay AB, Go WS. Effect of exposed inferior alveolar neurovascular bundle during surgical removal of impacted lower third molars. J Oral Maxillofac Surg 2004;62:592–600. 19 Chaushu G, Taicher S, Halamish ST, Givol N. Medicolegal aspects of altered sensation following implant placement in the mandible. Int J Oral Maxillofac Implants 2002;17:413–5. 20 Reich RH. Anatomical trials on the course of the mandibular canal. Dtsch Zahnarztl Z 1980;35:972– 5.
8 Raghoebar GM, Batenburg RH, Vissink A, Reintsema H. Augmentation of localized defects of the anterior maxillary ridge with autogenous bone before insertion of implants. J Oral Maxillofac Surg 1996;54:1180–5.
21 Alling CC. Dysesthesia of the lingual and inferior alveolar nerves following third molar surgery. J Oral Maxillofac Surg 1986;44:454–7.
9 Von Arx T, Hardt N, Wallkamm B. The TIME technique: A new method for localized alveolar ridge augmentation prior to placement of dental implants. Int J Oral Maxillofac Implants 1996;11:387–94.
22 Lakshmiganthan M, Gokulanathan S, Shanmugasundaram N, Daniel R, Ramesh SB. Piezosurgical osteotomy for harvesting intraoral block bone graft. J Pharm Bioallied Sci 2012;4:165–8.
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Neurosensory Neurosensory Disturbances Disturbances of of Inferior Inferior Alveolar Alveolar Nerve Nerve 23 Elias M. Cervical sympathetic and stellate ganglion blocks. Pain Physician 2000;3:294–304. 24 Kashiwagi M, Ikeda N, Tsuji A, Kudo K. Sudden unexpected death following stellate ganglion block. Legal Med 1999;1:262–5. 25 Melis M, Zawawi K, Badawi E, Lobo LS, Mehta N. Complex regional pain syndrome in the head and neck: A review of the literature. J Orofac Pain 2002;16:93–104. 26 Hanamatsu N, Yamashiro M, Sumitomo M, Furuya H. Effectiveness of cervical sympathetic ganglia block on regeneration of the trigeminal nerve following transaction in rats. Reg Anesth Pain Med 2002;27:268– 76. 27 Milligan NN, Nash TP. Treatment of post-herpetic neuralgia. A review of 77 consecutive cases. Pain 1985;23:381–6. 28 Murakawa K, Ishimoto E, Noma K, et al. Stellate ganglion block for facial palsy. Eur Arch Otorhinolaryngol 1994;12:S532. 29 Mizuguchi M, Komiya K. Stellate ganglion block therapy against progressive facial hemiatrophy. No to Hattatsu 1989;21:574–8. 30 Kawano Y, Araki E, Arakawa K, et al. A case of progressive hemifacial atrophy with Pourfour de Petit syndrome which was successfully treated by stellate ganglion block. Rinsyo Shinkeigaku 1999;39:731– 4. 31 Thor UI. Local distribution of the effects of sympathetic stimulation on cerebral blood flow in the rat. Brain Res 1990;529:224–31. 32 Umeyama T, Kugimya T, Ogata T, et al. Changes in cerebral blood flow estimated after stellate ganglion block by single photo emission. J Auton Nerv Syst 1995;50:339–46. 33 Gupta MM, Bitha PK, Dash HH, Chaturvedi A, Mahajan RP. Effects of stellate ganglion block on cerebral haemodynamics as assessed by transcranial Doppler ultrasonography. Br J Anaesth 2005;95:660– 73. 34 Quan SB, Liu JY, Wang QX, Yang GA, Fu NA. Effect of stellate ganglion block on the genes of endothelin and calcitonin related peptides in rabbits with global cerebral ischemia-reperfusion injury. J Clin Anesthesiol 2005;4:260–2. 35 Yamazaki Y, Mimura M, Iwasaki F, Namiki A. Regional cerebral blood flow and oxygenation following cervicothoracic sympathetic block. Masui 1998;47: 1233–6.
36 Okuda Y, Kitajima T. Influence of stellate ganglion block on bilateral cervicobrachial arterial and venous blood flow. Masui 1994;43:1201–6. 37 Terakawa Y, Ichinohe T, Kaneko Y. Redistribution of tissue blood flow after stellate ganglion block in the rabbit. Reg Anesth Pain Med 2009;34:553– 6. 38 Devriese PP. Compression and ischemia of the facial nerve. Acta Otolaryngol 1974;77:108– 18. 39 Poort LJ, Neck JW, Wal KG. Sensory testing of inferior alveolar nerve injuries: A review of methods used in prospective studies. J Oral Maxillofac Surg 2009;67:292–300. 40 Zuniga JR, Meyer RA, Gregg JM, Miloro M, Davis LF. The accuracy of clinical neurosensory testing for nerve injury diagnosis. J Oral Maxillofac Surg 1998;56:2– 8. 41 Blackburn CW. A method of assessment in cases of lingual nerve injury. Br J Oral Maxillofac Surg 1990;28:238–45. 42 Dellon AL, Andonian E, Dejesus RA. Measuring sensibility of the trigeminal nerve. Plast Reconstr Surg 2007;120:1546–50. 43 Rutner TW, Ziccardi VB, Janal MN. Long term outcome assessment for lingual nerve microsurgery. J Oral Maxillofac Surg 2005;63:1145– 9. 44 Jaaskelainen SK, Teerijoki T, Forssell H. Neurophysiologic and quantitative sensory testing in the diagnosis of trigeminal neuropathy and neuropathic pain. Pain 2005;117:349–57. 45 Ziccardi VB, Hullett JS, Gomes J. Physical neurosensory testing versus current perception threshold assessment in trigeminal nerve injuries related to dental treatment: A retrospective study. Quintessence Int 2009;40:603–9. 46 Kemler MA, Schouten HJ, Gracely RH. Diagnosing sensory abnormalities with either normal values or values from contralateral skin: Comparison of two approaches in complex regional pain syndrome I. Anesthesiology 2000;93:718–27. 47 Benoliel R, Biron A, Quek SY, Nahlieli O, Eliav E. Trigeminal neurosensory changes following acute and chronic paranasal sinusitis. Quintessence Int 2006;37:437–43. 48 Eliav E, Gracely RH, Nahlieli O, Benoliel R. Quantitative sensory testing in trigeminal nerve damage assessment. J Orofac Pain 2004;18:339–44.
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Evaluation of the Treatment Modalities for Neurosensory Disturbances of the Inferior Alveolar Nerve Following Retromolar Bone Harvesting for Bone Augmentation
Shinnosuke Nogami, DDS, PhD,* Kensuke Yamauchi, DDS, PhD,* Shunji Shiiba, DDS, PhD,† Yoshihiro Kataoka, DDS, PhD,* Bunichi Hirayama, DDS,* and Tetsu Takahashi, DDS, PhD* *Division of Oral and Maxillofacial Surgery, Department of Oral Medicine and Surgery, Tohoku University Graduate School of Dentistry, Miyagi and † Division of Dental Anesthesiology, Department of Control of Physical Function, Kyushu Dental University, Fukuoka, Japan Reprint requests to: Shinnosuke Nogami, DDS, PhD, Department of Oral Medicine and Surgery, Division of Oral and Maxillofacial Surgery, Tohoku University Graduate School of Dentistry, Miyagi 980-8575, Japan. Tel: 81-22-717-8350; 81-90-7454-7584; Fax: 81-22-717-8359; E-mail: [email protected]; [email protected].
Methods. One hundred four patients, of which 49 and 55 exhibited vertical or horizontal alveolar ridge defects in the mandible and maxilla, respectively, were enrolled. Nineteen patients underwent block bone grafting, 38 underwent guided bone generation or autogenous bone grafting combined with titanium mesh reconstruction, and 47 underwent sinus floor augmentation. Using a visual analog scale, we examined subjective symptoms and discomfort related to sensory alteration within the area of the NSDs in these patients. NSDs were clinically investigated using a two-point discrimination test with blunt-tipped calipers. In addition, neurometry was used for evaluation of trigeminal nerve injury. We tested three treatment modalities for NSDs: follow-up observation (no treatment), medication, and stellate ganglion block (SGB).
Funding sources: We performed this research without receiving any financial support or incentive from any third party.
Results. A week after surgery, 26 patients (25.0%) experienced NSDs. Five patients received no treatment, 10 patients received medication, and 11 patients received SGB. Three months after surgery, patients in the medication and SGB group achieved complete recovery. Current perception threshold values recovered to near-baseline values at 3 months: recovery was much earlier in this group than in the other two groups. SGB can accelerate recovery from NSDs.
Acknowledgment: This study was approved by the Ethics Committee of Kyushu Dental University (Approval No. 02-12).
Conclusions. Our results justify SGB as a reasonable treatment modality for NSDs occurring after the harvesting of retromolar bone grafts.
Abstract
Key Words. Stellate Ganglion Block; Neurosensory Disturbances; Inferior Alveolar Nerve
Conflict of interest: The authors declare that they have no conflict of interest.
Subjects. The purpose of this study was to evaluate the treatment modalities for neurosensory disturbances (NSDs) of the inferior alveolar nerve occurring after retromolar bone harvesting for bone augmentation procedures before implant placement.
Introduction The increased use of bone augmentation surgery as part of implant treatment has led to an increase in the variety of
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Nogami et al. complications including infection, bone resorption, and neurosensory disturbances (NSDs). NSDs can cause permanent or transient sensory impairment of the inferior alveolar nerve (IAN), which travels within the inferior alveolar canal in the mandible and is supported by the alveolus and the neurovascular bundle. Nerve damage can be classified as paresthesia, dysesthesia, or anesthesia, and its primary iatrogenic causes include the removal of impacted mandibular third molars [1,2], endodontic treatment [3], alveolar nerve blocks [4], and autogenous bone grafting [5]. The use of autogenous bone grafts for the augmentation of resorbed alveolar ridges is still considered the gold standard in implantology. Various extraoral donor sites such as the calvarium, tibia, rib, and iliac crest have been used. Obtaining grafts from these areas usually involves the use of general anesthesia. However, localized bone defects of the alveolar ridge require only a limited amount of bone, and donor sites for these grafts can be found within the oral cavity. A major advantage of an intraoral donor site is that the bone can be harvested under local anesthesia. Several reports on the harvesting of bone grafts from the retromolar region are available [6–13]; however, the complications reported in these studies vary widely, ranging from the absence of complications over impairment of the sensory function of the IAN to mandibular fractures [10,11]. Nkenke et al. reported the rate of complications after retromolar bone graft harvesting and the measurement of changes in the sensory function of the inferior alveolar and lingual nerves; however, they did not report on the treatment for NSDs [5]. Because the goal of implant treatment is to improve the patient’s quality of life, the positive feelings associated with implant treatment, including autogenous bone grafting, cannot be disregarded either. It is therefore essential to discuss the treatment options for NSDs. This prospective study aimed to evaluate the treatment modalities for NSDs of the IAN occurring after retromolar bone harvesting for bone augmentation procedures before implant placement. Patients and Methods Patients The study sample for the present prospective, randomized clinical trial was derived from patients who came to Kyushu Dental University Hospital between October 2002 and November 2011 for evaluation, then conducted detailed evaluations of 104 (54 women, 50 men; mean age 49.9 years; range 20–72 years), of whom 49 had vertical and 55 horizontal alveolar ridge defects. The local ethics committee approved this study, and informed consent was obtained from all patients after they received an explanation of the advantages and disadvantages of treatment. Randomization was done by lot using closed envelopes. All patients were postoperatively evaluated by a single assessor who was blinded to the treatment pro-
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tocol. Nineteen patients (10 women, 9 men) underwent block bone grafting (BG), 38 (20 women, 18 men) underwent guided bone generation (GBR) or autogenous bone grafting combined with stabilization using a titanium mesh, and 47 (25 women, 22 men) underwent sinus floor augmentation (sinus lift; Table 1). In all patients, autologous bone was harvested from the external oblique ridge of the mandibular ramus by an experienced surgeon (last author). All patients provided written informed consent prior to study initiation. Surgical Techniques BG A full-thickness mucoperiosteal flap was elevated and the bone defect was exposed. The cancellous block graft was harvested from the external oblique ridge of the mandibular ramus using a reciprocating bone saw and an oscillating saw and was refined to fit into the defect. In all patients, the recipient site was perforated with a 1-mm diameter round bur to increase blood supply from endosseous vessels to the transplanted bone. Once the graft was placed and stabilized, it was fixed with 1.6 × 10-mm bone screws (Jeil Medical Corp., Seoul, South Korea). The BG was covered with an absorbable collagen membrane (Biomend®; Zimmer Dental Inc., Carlsbad, CA, USA). GBR and Titanium Mesh Reconstruction Augmentations was performed by GBR wherein an autogenous particulate bone graft was harvested from the external oblique ridge of the mandibular ramus using a bone scraper (MX-Grafter®; Maxilon Laboratories, Inc., Hollis, NH, USA) or a reciprocating bone saw and an oscillating saw. The graft materials (Osferion®; Olympus Terumo Biomaterials Corp., Tokyo, Japan) were covered with an absorbable collagen membrane (Biomend®; Zimmer Dental Inc.) or an expanded polytetrafluoroethylene membrane (Gore-Tex®; W. L. Gore Associates, Inc., Flagstaff, AZ, USA) in GBR. In titanium mesh reconstruction, titanium meshes (0.1- or 0.2-mm thickness; M-TAM, Stryker Leibinger GmbH & Co. KG, Freiburg, Germany or ASTM F-67, Jeil Medical Corp.) were used according to the shape of each defect and fixed with small
Table 1 Summary of surgical procedures and mean patient ages Surgical Procedure
Patients
Age
BG GBR, titanium mesh reconstruction Sinus lift
19 38 47
41.9 53.2 54.6
BG = block bone graft; GBR = guided bone generation; sinus lift = sinus floor augmentation procedure.
Neurosensory Neurosensory Disturbances Disturbances of of Inferior Inferior Alveolar Alveolar Nerve titanium screws. In both procedures, decortication of the drill holes was performed using a round bur to ensure vascular nutrition of the grafted bone. Sinus Lift The sinus lift technique was performed according to procedures reported previously [14]. The sinus space was then filled with a mixture of graft materials (Osferion®; Olympus Terumo Biomaterials Corp.) and autologous bone that was harvested from the external oblique ridge of the mandibular ramus using a bone scraper (MX-Grafter®; Maxilon Laboratories, Inc.). Treatment for NSDs We tested three treatment modalities for NSDs: follow-up observation (no treatment), medication, and stellate ganglion block (SGB). The medication used was mecobalamin (Methycobal®, Eisai Co. Ltd, Tokyo, Japan: 1500 μg/day). Patients who experienced NSDs were administered with this at 1 week after surgery, as an NSD appearing soon after surgical intervention might have been due to swelling, surgery in proximity of nerves, or retraction of the soft tissue. SGB was also administered at 1 week after surgery by the dental anesthesiology department of our hospital after receiving patient consent. Patients who did not consent to SGB received no treatment or continued medication, and were observed (no treatment). The SGB technique followed methods described previously [15]. Briefly, each patient was placed supine with the neck slightly hyperextended. The lower jaw was loosely opened to relax the platysma and facilitate palpation of the deep structures of the neck. The tip of the index finger was used to identify the cricothyroid notch and then moved laterally, retracting the carotid sheath and sternocleidomastoid muscle. The C6 anterior transverse process (carotid or Chassaignac’s tubercle-tuberculum caroticum vertebrae cervicalis VI) was then identified and fixed with the palpating finger. A 2.5-cm, 22- or 23-gauge needle was introduced immediately medial to the palpating finger. Contact with the C6 transverse process was made just medial to the tubercle at a depth of approximately 1 cm and a 3-mL quality of 1% lidocaine without epinephrine was injected after negative aspiration. Successful block was ascertained by the development of Claude Bernard-Horner syndrome (Horner’s ptosis) and loss of galvanic skin response and thermography, an increase in skin temperature, and plethysmography. Evaluation of NSDs and Observation Period Visual Analog Scale Using a visual analog scale (VAS), we examined subjective symptoms and discomfort related to sensory alterations within the area of the NSDs. The patients rated their discomfort from 0 (no sensation) to 10 (completely normal sensation).
Two-Point Discrimination Test NSDs were also clinically investigated using a two-point discrimination test with blunt-tipped calipers that were calibrated and applied (by the third author) to provoke a static stimulus. Testing began with application of the caliper points that were placed 20 mm apart. The interprobe distance was then decreased in 2-mm increments, and patients were asked whether they sensed one or two points. Self-Evaluation In addition, patients also provided self-evaluation of spontaneous pain and abnormal sensation 1 week, 1 month, 3 months, 6 months, and 1 year after surgery (Table 2). We used these self-evaluations to determine whether complete recovery had occurred. Neurometry Furthermore, neurometry was performed by an experienced dental anesthesiologist (third author) and also utilized a NeurometerTM® (Neurotron, Baltimore, MD, USA; Figure 1A and B) equipped with a platinum electrode that was placed on the oral mucosa but not the skin. The current perception threshold (CPT) was defined by the intensity of the alignment mode that applies stimulation in both an ascending and a descending manner. The regions tested were mental skin right or mental skin left (Figure 2). Affected sites received three stimulus frequencies that are
Table 2 Self-evaluation of spontaneous pain and abnormal sensation after surgery Relief from spontaneous pain Good Pain was absent 1 year later. Activities of daily living (ADL) were not limited. Fair Pain was reduced and ADL improved, but the patient was still uncomfortable. Poor Pain and ADL did not improve sufficiently. Recovery of sensation Good Complete recovery of sensation. Patients felt normal sensation both at rest and when stimuli were applied. Fair Sufficient, but not complete recovery. Patients were a little irritable because of abnormal sensations. Poor Poor recovery. Patients were still irritable because of abnormal sensations.
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Figure 1A A neurometer as an evaluation tool for trigeminal nerve injury. known to stimulate the A-beta (2,000 Hz), A-delta (250 Hz), and C-fibers (5 Hz). The electrical stimuli were delivered through two 1-cm diameter, disposable, goldplated electrodes placed in close proximity within the affected area. The patient was given a remote device to control delivery of the electrical stimuli. They depressed a button until the threshold of the first sensation around the site of the electrodes was detected; at this point, they released the button to terminate the delivery of electrical current. The instrument began current delivery for each specific frequency at the lowest output intensity, i.e., 0.001 mA, and increased the current until the patient released the remote control button or until the maximum stimulus of 9.99 mA was reached. The neurometer automatically repeated a minimum of three sets of testing for each frequency until the software determined a threshold. During testing, neither the operator nor the patient was aware of the output current intensity. The observation periods were 1 week, 1 month, 3 months, 6 months, and 1 year after surgery.
Figure 1B A platinum electrode connected to the neurometer is placed on the oral mucosa but not the skin. The current perception threshold (CPT) was defined by the intensity of the alignment mode that applied stimulation in both an ascending and a descending manner. 504 4
Statistical Analysis Statistical differences were calculated and analyzed using repeated-measures analysis of variance. Data are presented as means ± standard deviations. Differences were considered statistically significant when the P value was less than 0.05.
Neurosensory Neurosensory Disturbances Disturbances of of Inferior Inferior Alveolar Alveolar Nerve
Table 4 Summary of the surgical procedure and type of harvested bone Surgical Procedure BG GBR, titanium mesh reconstruction Sinus lift
Figure 2 Diagram illustrating the regions tested. MR = mental skin right; ML = mental skin left.
Particulate Bone (%)
Block Bone (%)
0 (0) 27 (71.1)
19 (100) 11 (28.9)
47 (100)
0 (0)
BG = block bone graft; GBR = guided bone generation; sinus lift = sinus floor augmentation.
and abnormal sensation on self-evaluation 1 year after surgery (Table 3).
Results Immediate postoperative infection did not occur in any patient. One week after surgery, 26 patients (25.0%) experienced NSDs of the IAN (Table 3). Five patients received no treatment (19.2%), 10 received medication (38.5%), and 11 received SGB (42.3%). Patient #1 and #2 reported abnormal sensations in the two-point discrimination test as well as spontaneous pain
Table 3
Bone was harvested as particulate bone in 74 patients and block bone in 30. Eleven patients with block bone harvesting underwent GBR and titanium mesh reconstruction (Table 4). Thirteen (20.3%) patients with particulate bone harvesting and 13 (43.3%) with block bone harvesting exhibited NSDs of the IAN (Table 5). Sixteen patients (15.4 %) experienced NSDs of the IAN 1 month after surgery, 11 (10.6%) experienced IAN
Summary of NSDs of the IAN
No.
Surgical procedure
Donor site
Host region
Harvested bone
Treatment
Complete recovery
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26
GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME GBR,TIME BG BG BG BG BG BG BG BG BG BG
Right ramus Right ramus Right ramus Right ramus Left ramus Left ramus Right ramus Right ramus Right ramus Left ramus Left ramus Left ramus Right ramus Left ramus Right ramus Right ramus Left ramus Right ramus Left ramus Left ramus Left ramus Left ramus Right ramus Right ramus Left ramus Right ramus
29–31 29–31 29–31 29–31 19–20 18–19 30–31 20–24 19–20 19–21 19–21 30–31 21–24 18–20 29–31 29–31 30 18 31 30–31 30 30 18–19 19 30 19
Particulated Particulated Particulated Particulated Particulated Particulated Particulated Particulated Particulated Particulated Particulated Particulated Particulated Block Block Block Block Block Block Block Block Block Block Block Block Block
No treatment No treatment Medication Medication No treatment No treatment Medication Medication Medication Medication SGB SGB SGB No treatment Medication Medication Medication Medication SGB SGB SGB SGB SGB SGB SGB SGB
○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○ ○
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Table 5 Summary of type of harvested bone and incidence of NSDs
Particulate bone Block bone
NSD (%)
No NSD (%)
13 (20.3) 13 (43.3)
51 (79.7) 17 (56.7)
NSD = neurosensory disturbance.
paresthesia 3 months after surgery, 4 (3.8%) experienced NSDs of the IAN 6 months after surgery, and 2 (2.0%) patients experienced NSD of the IAN 1 year after surgery (Figure 3). One month after NSD onset, the no treatment group comprised four patients, the medication group comprised seven patients, and the SGB group comprised five patients. Three months after NSD onset, the no treatment group comprised four patients while seven patients in the medication group received treatment. One year after NSD onset, NSD of the IAN persisted in two patients in the no treatment group (Figure 4). The VAS score gradually increased in all groups after surgery (Figure 5). In the SGB groups, that score reached 10 (completely normal sensation) earlier than in the other groups. Two-point discrimination values decreased gradually in all groups after surgery. The values in the medication group were lower than those in the no treatment group at every time point after surgery (Figure 6). Significantly higher CPT values were observed after surgery in all groups (Figure 7A–C), and the values in the
Figure 4 Treatment methods for neurosensory disturbances (NSDs) of the inferior alveolar nerve (IAN) (N) at various time points after surgery. SGB = stellate ganglion block.
SGB group were markedly lower than those in the no treatment and medication groups. CPT values before surgery (baseline) were 30.4 ± 1.14, 19.4 ± 1.51, and 20.4 ± 1.67 at 2,000, 250, 5 Hz, respectively, in the SGB group. These values increased to 85.6 ± 3.20, 49.2 ± 1.92, and 54.8 ± 5.06, respectively, 1 week after surgery and decreased gradually thereafter to nearbaseline values of 33.6 ± 1.51, 23.8 ± 2.38, and
Figure 3 Incidence of neurosensory disturbances (NSDs) of the inferior alveolar nerve (IAN) (%). 506 6
Neurosensory Neurosensory Disturbances Disturbances of of Inferior Inferior Alveolar Alveolar Nerve Discussion
Figure 5 Change in visual analog scale (VAS) after surgery. SGB = stellate ganglion block.
24.8 ± 3.83 at 2,000, 250, and 5 Hz, respectively, 3 months after surgery. On the other hand, CPT values remained significantly higher than preoperative values even at 1 year after surgery in the no treatment group.
Figure 6 Changes in two-point discrimination (mm) values after surgery. All data are presented as mean ± standard deviation. One-factor repeatedmeasures analysis of variance was used for comparison with data obtained 1 week after surgery. SGB = stellate ganglion block.
Bone augmentation surgery has become common with an increase in the popularity of implant surgery. The forms of surgery are both numerous and, like implant surgery, invasive, with many reports of complications. NSD of the IAN is one such complication. The incidence of permanent IAN sensory disturbance reportedly ranges from 0.4% to 13.4% [16,17]. In cases where the IAN bundle is exposed during third molar surgery, the incidence of IAN paresthesia after 1 week is reported to be approximately 20% [18]. Chaushu et al. reported NSDs after mandibular molar implant surgery in 12% of patients [19]. The present prospective study was conducted as a clinical investigation of NSDs occurring following retromolar bone harvesting for bone augmentation procedures in a total of 104 patients, in whom autologous bone was harvested from the external oblique ridge of the mandibular ramus and used for bone augmentation of a highly atrophied maxilla or mandible. NSDs persisted in 26 (25.0%) patients for 1 week after surgery and in 2 (2.0%) for at least 1 year after surgery. In those two patients, we discovered that a surgical instrument had made direct contact with the mental foramen during surgical site exposure. Bone harvesting using an MX grafter® (Implatex, Tokyo, Japan) was limited to cortical bone obtained from the external oblique ridge of the mandibular ramus, which was thought to be a contributing factor to the lower NSD incidence (20.3%) compared with that (43.3%) when block bone was harvested using a reciprocating bone saw and an oscillating saw. In one patient (#26), the mandibular canal was exposed during the procedure. When the buccal cortex of the mandible is used as a bone graft material, exposure of the IAN cannot be safely avoided. The average distance of the IAN from the buccal aspect of the mandible in the retromolar region is 2.835 mm [20]. However, a cortical graft thickness of as much as 4 mm has been described [21]. Therefore, exposure of the IAN occurs frequently, sometimes accompanied by massive bleeding because of injury to the inferior alveolar artery [10]. Apparently, modification of retromolar bone harvesting with the trephine bur helps in decreasing sequelae and complications. Lakshmiganthan et al. reported that piezoelectric surgery is a minimally invasive technique that lessens the risk of damage to surrounding soft tissues and important structures such as nerves, vessels, and mucosa [22]. It also decreases damage to osteocytes and permits good survival of bony cells during bone harvesting. However, we used a reciprocating bone saw and an oscillating saw to harvest block bone. Major drawbacks of these techniques are mechanical pressure and vibrations on the bone. When block bone is harvested, not just cortical bone but also cancellous bone is involved, which is thought to increase the risk of NSDs. Alling reported spontaneous recovery to a degree of 96% in the IAN in the first 4–8 weeks after third molar surgery [21]. In this study, we used medication and SGB to decrease the duration of treatment for NSDs of the IAN. The medication used was mecobalamin (Methycobal®), a
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Figure 7 (A–C) Changes in current perception threshold (CPT) values after trigeminal nerve injury. All data are presented as mean ± standard deviation. CPT values at three different frequencies of stimulation (2,000, 250, 5 Hz) increased significantly after surgery. One-factor repeated-measures analysis of variance was used for comparison with preoperative data. Ͻ = P < 0.05. SGB = stellate ganglion block. ◀
B12 vitamin. B12 vitamins are generally used for the treatment of pernicious anemia following gastrectomy. However, in recent years, they are being used for the treatment of peripheral nerve damage, irrespective of the presence or absence of B12 deficiency. In our department, the maximum period of medication was 6 months. Medication was continued for 1 week, and if there was no amelioration of symptoms, SGB was administered to patients after they provided consent. SGB is used for the treatment of idiopathic facial paralysis, migraine, hyperhidrosis, cervico-omo-brachial syndrome, stiff shoulder, Meniere’s disease, and depression [23,24]. The usefulness of SGB as a treatment modality has been widely recognized. However, a certain level of skill and familiarity is necessary for administration. SGB increases tissue blood flow in the head, face, neck, and upper limbs because of its sympatholytic effects [25], and it has been used for the treatment of several types of disorders, including traumatic trigeminal neuropathy [26], post-herpetic neuralgia [27], facial nerve paralysis [28], and progressive facial hemiatrophy [29,30]. The stellate ganglion is composed of cell bodies of the inferior cervical and first thoracic sympathetic ganglia. The associated cerebral vasculature receives noradrenergic sympathetic input mainly through the fibers that originate in the cervical ganglion, accompanies the carotid artery, and projects into the ipsilateral cerebral hemisphere [31,32]. Intracerebral vessels constrict in response to cervical sympathetic stimulation and dilate when these fibers are interrupted [31]. A blockage of the stellate ganglion induces a definite ipsilateral increase in cerebral blood flow, as determined by cerebral scintigraphy [32]. The mechanism underlying the physiological consequences of blockage of sympathetic nerve activity or reversal of overactivity, irrespective of whether the sympathetic disorder causes a critical reduction in cerebral blood flow, may be explained by the subsequent dilation of intracerebral vessels and improvement of cerebral blood flow. Studies have shown that SGB can induce a significant decrease in zero flow pressure, a surrogate marker of cerebral vascular tone, thus improving cerebral perfusion pressure [33]. Quan et al. reported that cervical sympathetic block can significantly dilate cerebral vessels, increase cerebral blood velocity, regulate the imbalance with endothim and calcitonin gene-related protein and excessive expression of neurons’ heat shock 8508
Neurosensory Neurosensory Disturbances Disturbances of of Inferior Inferior Alveolar Alveolar Nerve Nerve protein 70 after global cerebral ischemia-reperfusion injury in rabbits, improve the immune function of erythrocyte of patients with cerebral infarction, regulate the content of substance causing systolic and diastolic vessels in serum such like NO and NOS, and promote neural functional recovery [34]. Some studies have reported that increased tissue blood flow on the ipsilateral side is attributable to the redistribution of tissue blood flow from the contralateral side [35,36]. Recently, Terakawa et al. showed that SGB increases mandibular bone marrow and masseter muscle blood flow on the ipsilateral side and decreases it on the contralateral side through redistribution mechanisms [37]. It is therefore suggested that tissue blood flow in the mental nerve on the contralateral side also decreases after SGB. The IAN passes through the mandibular canal, which is surrounded by hard bone. Damage to the IAN during surgery can be direct mechanical damage or caused by pressure within the mandibular canal from the bony wall, and it includes not only damage to the nerve fibers but also ischemia in the feeding vessels, congestion of veins, and lymph flow blockage. The IAN, surrounded by hard bone, closely resembles the facial nerve, which passes through the facial canal in the temporal bone. It is thought that idiopathic facial paralysis and Ramsay Hunt syndrome occur when ischemia and inflammation in the facial nerve cause localized edema, which, together with compression by the bony wall, leads to secondary ischemia. Constriction caused by the edema and compression leads to the occurrence of facial paralysis [38]. Consequently, because the same symptoms are manifested when the mandibular nerve is damaged, SGB treatment is used in our department to treat IAN paresthesia occurring after bone augmentation surgery. Furthermore, in patients with facial paralysis, SGB increases blood flow in the vessels and tissues and is effective in treating nerve disturbances due to ischemia in the feeding vessels and secondary damage caused by constriction and in regenerating facial nerve fibers that have been subject to Wallerian degeneration. Therefore, it can be inferred from the results of the present study that, in patients with mandibular NSDs, SGB will demonstrate its effectiveness through an expected increase in blood flow in the tissues of the mandibular nerve. The general principle of sensory testing is the evaluation of responses to varied stimuli such as temperature, directional sense, pain, and fine touch to allow for comparisons at different times to determine whether spontaneous changes have occurred. These techniques allow for a subjective quantification of the degree of sensory deficit. Neurosensory testing can be divided into mechanoceptive and nociceptive testing according to the specific receptors stimulated. Mechanoceptive testing includes twopoint discrimination, static fine touch, brush directional sense, and vibration. Nociception includes thermal discrimination and pain (pinprick). The sensory modalities that should be minimally included in neurosensory testing are touch or proprioception for the assessment of A-beta fibers, cold detection or pinprick for the assessment of
A-delta fibers, and heat/pain detection for the assessment of unmyelinated C-fibers. The techniques of clinical sensory testing have been well described in the literature [39,40]. Moving two-point discrimination has also been described as a method of assessing lingual nerve injuries, with some predictive capacity for injuries not likely to resolve spontaneously [41]. These traditional neurosensory testing techniques, however, have some limitations. Two-point discrimination generally records the distance perceived without consideration for the cutaneous pressure threshold. Pressurespecified sensory devices measure the forces applied by the surface area of the instrument at the pressure at which the patient perceives the stimuli. The cutaneous pressure two-point threshold is defined by both pressure and distance measurements [42,43]. Conventional clinical sensory tests have been reported to demonstrate poor reproducibility, low sensitivity, and moderate specificity. There is a need for objective documentation and grading to decrease patient complaints and potential litigation resulting from trigeminal nerve injuries [44]. CPT has been described as an adjunctive diagnostic tool for the assessment of various orofacial pathological disorders such as temporomandibular joint disorders, burning mouth syndrome, oral malignancies, and trigeminal nerve injuries [45]. Modality-specific assessments can differentiate between large-diameter thickly myelinated A-beta fibers, thinly myelinated A-beta fibers, and unmyelinated C-fibers [46]. Heat and very low-frequency electrical stimulation (5 Hz) activate thin unmyelinated C-fibers that comprise up to 90% of the cutaneous nerve fibers. A-delta fibers have a thin myelinated sheath and are activated primarily by cold, fast-onset contact and mediumfrequency electrical stimulus (200 Hz). Beta fibers have a thicker myelin sheath, mediate touch and vibratory sensation, and respond to greater frequency electrical stimulation (2,000 Hz) [47–49]. CPT and clinical neurosensory testing are useful modalities for the assessment of lingual nerve injuries [50]. In the present study, we also used CPT as a quantitative sense test in addition to the VAS and two-point discrimination to evaluate the effectiveness of treatments and found that CPT values gradually decreased in all groups. These values were significantly elevated immediately after injury, followed by a gradual fall at all frequencies in all groups. In particular, recovery from NSDs was the earliest in the medication and SGB group, in which the CPT values at 3 months after surgery were similar to those at baseline. Our results may support SGB as a reasonable treatment modality for NSDs occurring after retromolar bone graft harvesting. Anti-inflammatory medications and steroids were prescribed during the immediate postoperative period. This could have had an effect on inflammation and edema around the injured nerves. Since it was not unified about these postoperative given doses or dosing periods, a
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Nogami et al. detailed examination is required from now on. Because of the small number of patients examined in the present study, it is premature to conclude that a combination of medication and SGB can decrease the duration of treatment for NSDs. In addition, we did not perform a Semmes-Weinstein monofilament test for any of the patients, which is a well-known objective evaluation that can provide important information.
10 Von Arx T, Kurt B. Endoral donor bone removal for autografts: A comparative clinical study of donor sites in the chin area and the retromolar region. Schweiz Monatsschr Zahnmed 1998;108:446–59. 11 Khoury F. Augmentation of the sinus floor with mandibular bone block and simultaneous implantation: A 6-year clinical investigation. Int J Oral Maxillofac Implants 1999;14:557–64.
Conclusion The present results suggest that SGB may be a potent treatment modality for patients with NSDs of the IAN. To obtain additional evidence, further studies concerning the long-term clinical course of SGB treatment for NSDs occurring after retromolar bone graft harvesting are necessary. References 1 Kipp DP, Goldstein BH, Weiss WW. Dysesthesia after mandibular third molar surgery: A retrospective study and analysis of 1377 surgical procedures. J Am Dent Assoc 1980;100:185–92. 2 Gulicher D, Gerlach KL. Sensory impairment of the lingual and inferior alveolar nerves following removal of impacted mandibular third molars. Int J Oral Maxillofac Surg 2001;30:306–12. 3 Giuliani M, Lajoro C, Deli G, Silveri C. Inferior alveolar paresthesia caused by endodontic pathosis: A case report and review of the literature. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2001;92:670– 4. 4 Pogrel MA. The results of microneurosurgery of the inferior alveolar and lingual nerve. J Oral Maxillofac Surg 2002;60:485–9. 5 Nkenke E, Radespiel TM, Wiltfang J, et al. Morbidity of harvesting of retromolar bone grafts: A prospective study. Clin Oral Implants Res 2002;13:514–21. 6 Laskin JL, Edwards DM. Immediate reconstruction of an orbital complex fracture with autogenous mandibular bone. J Oral Surg 1977;35:749–51. 7 Girdler NM, Hosseini M. Orbital floor reconstruction with autogenous bone harvested from the mandibular lingual cortex. Br J Oral Maxillofac Surg 1992; 30:36–8.
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