Topography and Spatial Fascicular Arrangement of the Human Inferior Alveolar Nerve

ABSTRACT

Background: Topography and fascicular arrangement of the inferior alveolar nerve (IAN) can provide critical information for the estimation of damage to IAN based on patient symptoms, or conversely to evaluate the symptoms resulting from injury to the IAN.

Purpose: The fascicular composition and organization of the IAN were determined to confirm the microarchitecture of the IAN bundles into each of the mandibular teeth, including the composition of the mental nerve.

Materials and Methods: The IAN within the mandibular canal (MC) was examined in 30 hemifaces of embalmed Korean cadavers.

Results: The most common patterns of nerve fascicle innervation to the mandibular teeth could be grossly classified into three: (1) the superior buccal portion of the IAN innervating the molars, (2) the superior portion innervating the premolars, and (3) the superior lingual or the superior lingual and inferior lingual portions in the posterior MC and the lingual portions in the anterior MC, innervating the incisors and canine. The buccal two-thirds portion of the IAN was composed of the mental nerve.

Conclusion: The IAN had distinctive fascicular organizations, which make it possible to forecast the degree, location, and extent of nerve damage according to presenting symptoms.

INTRODUCTION

The inferior alveolar nerve (IAN) is a sensory nerve that innervates the mandibular teeth, periodontium, buccal mucosa, and lower lip. It runs downward and forward within the mandibular canal (MC), generally below the apex of the teeth.¹ The complete division of the IAN into the dental nerve and the mental nerve (MN) is easily distinguished.²

There are several ways in which the IAN can be damaged during dental surgery; it might be affected by perforation of the MC during drilling, positioning of an implant fixture too close to the canal, with subsequent formation of an adjacent hematoma that presses against the nerve, or by damage to a double or supplementary dental canal.³ Retromolar surgical procedures such as third-molar extraction are also a common cause of IAN damage,⁴ as is osteotomy near the mental foramen.⁵

Injury to the IAN during implant placement is a serious complication.⁶ The results of nerve damage range from mild paresthesia to complete anesthesia or disabling dysesthesia.⁷ The result of injury to either the IAN or the MN may produce sensory disturbances following implant placement in the mandible.⁸

Little attention has been paid to the detailed fascicular anatomy of the IAN, although observations made during various clinical procedures have revealed that there is considerable variation in the fascicular arrangement of this nerve. Rather than plexiform, the fascicles of peripheral nerves are arranged mainly in a cable-like fashion, indicating a high degree of somatic organization. Each fascicle of the peripheral nerve contains motor or sensory fibers that innervate very specific areas of the skin or specific muscles.⁹ Indeed, partial focal nerve lesions can produce restricted clinical deficits. This fascicular pattern is also one of the most important components of a nerve that is responsible for the achievement of a successful functional result during a microsurgical reconstruction.¹⁰

The inferior alveolar artery (IAA), one of three arteries that supply the mandible, is also important in dental implant surgery. The loss of neural blood supply or the development of an intraneural hematoma might cause IAN neuropathy.¹¹ It is thus important to understand this relationship and the topography of the neurovascular bundle within the MC to provide references for this procedure.

The aim of this study was to clarify the patterns and variations in the course of the IAN by topographic examination followed by detailed dissection and micro-computed tomography (micro-CT) analysis. The fascicular composition and organization of the IAN were also determined to confirm the microarchitecture of the IAN bundles into each of the mandibular teeth, including the composition of the MN. The findings of this study will provide critical information for the estimation of damage to portions of the IAN based on patient symptoms, or conversely to evaluate the symptoms resulting from injury to a known part of the IAN.

MATERIALS AND METHODS

The IAN within the MC was examined in 30 hemifaces (19 males, 11 females) of embalmed Korean cadavers (mean age 66.8 years, range 48–87 years). Latex (Neoprene, Lot no. 307L146; DuPont, France) with a red coloring agent (Colorant Universal, Castorama, France) was injected into all of the specimens through the common carotid artery to enable clear observation of the topography between the IAN and IAA within the MC.

Prior to 17 of the dissections, the specimens were decalcified in 40 L of decalcification solution for 2 weeks. The decalcification solution was prepared with 7 g of aluminum chloride hexahydrate (Al₂Cl₃6H₂O), 8.5 mL of 30% hydrochloric acid, and 8.5 mL of 100% formic acid, which was then diluted to 100 mL with distilled water. After decalcification, the specimens were neutralized for 2 to 3 days in a neutralization solution prepared from 5 g of sodium sulfate in 100 mL of distilled water. A detailed dissection on the lingual side of the mandible was performed in these 17 decalcified specimens, with the aid of a surgical microscope (OPMI-FC, Carl Zeiss, Oberkochen, Germany). Extreme care was taken not to damage the dental branches of IAN after opening the MC. After exposing the IAN and its branches, the specimens were immersed in guanidine HCl (0.2 M) for 2 weeks, and then treated with ultrasonic cleaner for 1 hour to soften the connective tissue around the nerve bundles. The processed IAN and its branches were dissected, again with the aid of a surgical microscope, carefully removing the connective tissue to trace the nerve fascicles innervating each tooth and to confirm the composition and organization of the IAN.

Specimens of 13 mandibles were scanned using a micro-CT system (Skyscan 1072, Skyscan, Antwerp, Belgium). The specimens were placed on the holder between the x-ray source and the charge-coupled device (CCD) camera, and were rotated around the vertical axis at intervals of 0.9° for 180°, while keeping it in the field of view, thereby producing 200 projections. The beam was projected onto a phosphorus screen, which converted the x-rays into visible light that was detected by a CCD camera. The data were then digitized by a frame grabber and transmitted to a computer with tomographic reconstruction software. Cross-sectional 1968 × 1968-pixel images were created. A three-dimensional structural image with voxels 35 × 35 × 35 µm in size was created from the two-dimensional images using a three-dimensional reconstruction program (Lucion, Cybermed, Seoul, Korea). After reconstructing the images, the mandible wassectioned arbitrarily to observe the presence and configuration of accessory MC and retromolar canal. Measurements were also made of the diameters of the MC before it divides into the accessory canals or retromolar canals, the accessory and retromolar canals themselves, and the MC at the mandibular first, second, and third molar regions, using the three-dimensional reconstruction program. All photographs and diagrams in this article are of structures viewed from the left and lingual side of the face, and all mean data are presented with the standard deviation (±SD).

RESULTS

The course of the IAN was classified into three types (Figure 1):

Figure 1. Patterns of the course of the inferior alveolar nerve (IAN) from the posterior view of the mandible. (A) IAN of a single mandibular canal (MC) (dissection). (B) Sectional image of a reconstruction of the mandible to show the IAN of a single MC (micro-computed tomography [micro-CT] image; thickness 35 µm). (C) IAN of a single MC with an accessory canal (arrowhead) innervating the retromolar area, and the second and third molars (dissection). (D) Sectional image of a reconstruction of the mandible to show the IAN of a single MC with an accessory canal (arrowhead) (micro-CT image; thickness 35 µm). (E) IAN of bifid MCs. Upper canal (arrow) was thinner than the lower major MC (dissection).

• •
  Type I: IAN in a single MC. This type was the most frequently observed, being seen in 21 out of 30 specimens (70.0%): 11 out of 17 dissections (64.7%) and 10 out of 13 micro-CT images (76.9%).
• •
  Type II: IAN in a single MC with an accessory canal. This type was found in 7 out of 30 specimens (23.3%): 4 out of 17 dissections (23.5%) and 3 out of 13 micro-CT images (23.1%).
• •
  Type III: IANs in a bifid MC. This type was found in only 2 out of 30 specimens (6.7%), and both were from dissected specimens.

The accessory canals were divided below the mandibular foramen, running close to the root apices of the mandibular molars. The bifid MCs ran parallel to each other, and the dental branches innervating molars arose from the upper canal, which was thinner than the lower major MC.

Retromolar branches were observed in 13 out of the 30 specimens (43.3%): 10 out of 17 dissections (58.8%) and 3 out of 13 micro-CT images (23.1%). These branches, which were observed more than twice as often in dissections as in micro-CT images, usually ascended lingually, and finally innervated the internal oblique ridge (Figure 2).

Figure 2. The nerve branch innervating the retromolar area. (A) The retromolar branch (arrowhead) ascending a little lingually to innervate the retromolar area (dissection). (B) Sectional image of a reconstruction of the mandible to show the retromolar canal (arrowhead).

On micro-CT image, the mean diameter of the MC before it divides into the accessory and retromolar canals was 4.1 ± 0.9 mm (range 3.5–5.1 mm) and 4.1 ± 0.7 mm (range 3.7–4.9 mm), respectively. The mean diameter of the accessory and retromolar canals on micro-CT image was 1.0 ± 0.5 mm (range 0.6–1.6 mm) and 1.1 ± 0.3 mm (range 0.8–1.3 mm), respectively. The mean diameters of the MC in the mandibular first, second, and third molar regions were 3.3 ± 0.8 mm (range 2.1–4.9 mm), 3.1 ± 0.6 mm (range 2.4–4.3 mm), and 3.3 ± 0.8 mm (range 2.2–5.0 mm), respectively. The MC thus showed a tendency to maintain its diameter in the molar regions.

The relationship between the IAN and the IAA was classified into three types according to the location of the IAA relative to the IAN within the mandibular foramen and MC (Figure 3):

Figure 3. Spatial relationships between inferior alveolar nerve (IAN) and inferior alveolar artery (IAA). IAA located (A) inferobuccally, (B) superobuccally, and (C) lingually in the mandibular foramen, and traveling toward the superior and lingual to IAN throughout the canal. Insets (A–C): diagrammatic representation of the path of the IAN (yellow) and IAA (red) are seen in the main picture.

• •
  Type A: The IAA is located inferobuccally against the IAN in the mandibular foramen, travels to the lingual aspect, and is then located superior and lingual to the IAN within the MC. This pattern was the most frequently observed, being seen in 10 out of 17 dissections (58.8%).
• •
  Type B: The IAA is located superobuccally in the mandibular foramen and travels toward the superior and lingual aspect to the IAN. This pattern was observed in 6 out of 17 dissections (35.3%).
• •
  Type C: The IAA is located lingually to the IAN within the MC throughout the canal. This pattern was observed in only one case, and that was one of the cases of a bifid MC.

In all specimens, one arterial branch left the IAA after entering the mandibular foramen. In cases where the IAA was located inferobuccally within the mandibular foramen (type A), the arterial branch ascended superobuccally against the IAN, usually to supply the mandibular molars. In cases where the IAA ran superobuccally within the mandibular foramen (type B), the arterial branch traveled parallel to the main IAA; the IAA and its branch then ran lingually to those IAN nerve fascicles that usually innervate the mandibular molars (Figure 4). Where there was an accessory canal and a bifid MC, the nerve fascicles comprising the superior buccal aspect of the IAN were located within these canals (types II and III) instead of the single MC (type I).

Figure 4. The arterial branch (arrowhead) of the inferior alveolar artery (IAA) traveling parallel to the main IAA. The IAA and its branch then run along the lingual aspect to some of the inferior alveolar nerve (IAN) fascicles, usually those innervating the mandibular molars (the IAA and the IAN are pulled inferiorly to show the arterial branch of IAA).

The spatial fascicular arrangement of the IAN took various forms. The somatotopic arrangement of the IAN was categorized according to the nerve fascicles innervating each tooth. In all of 15 cases of nerve fascicle separation, the nerve fascicles located at the superior buccal portion of the IAN within the MC innervated the mandibular second and third molars (Figure 5). In case of presenting the retromolar branch, this branch also arose from the superior buccal nerve fascicles of the IAN. The nerve fascicles innervating the first molar were classified into two categories: (1) those running in the superior buccal portion of IAN (10 out of 15 specimens, 66.7%) and (2) those running in the superior portion of the IAN (5 out of 15 specimens, 33.3%). A nerve branch innervating the second premolar was observed for two categories of nerve fascicles running in (1) the superior portion of the IAN (13 cases, 86.7%) and (2) the superior buccal portion of the IAN (two cases, 13.3%). The nerve fascicles innervating the first premolar were classified into four types, with the nerve fascicles running in (1) the superior lingual portion (nine cases, 60.0%), (2) the superior buccal portion (three cases, 20.0%), (3) inferior lingual portion (two cases, 13.3%), and (4) the superior portion of the IAN (one case, 6.7%).

Figure 5. The superior buccal portion (SB) of the inferior alveolar nerve (IAN) innervating the second and third molars (the other fascicles of the IAN are pulled inferiorly to show the SB fascicles of the IAN).

The courses of the nerve fascicles innervating the mandibular anterior teeth (central, lateral incisors, and canine) could be divided into six categories, with nerve fascicles running in:

• 1
  the superior lingual portion of the IAN within the posterior MC and the lingual portion within the anterior MC (five cases, 33.3%, Figure 6);
• 2
  the superior and inferior lingual portions of the IAN within the posterior MC, and then in the lingual portion within the anterior MC after merging (five cases, 33.3%);
• 3
  the superior lingual portion of the IAN throughout the MC (two cases, 13.3%, Figure 7);
• 4
  the inferior lingual portion of the IAN throughout the MC (one case, 6.7%);
• 5
  the inferior portion of the IAN, receiving the nerve fascicles from the inferior lingual and inferior buccal portions within the posterior MC, and then in the inferior lingual portion of the IAN within the anterior MC (one case, 6.7%); and
• 6
  the lingual and buccal portions of the IAN within the posterior MC, and then in the lingual portion of the IAN within the anterior MC (one case, 6.7%).

Figure 6. The superior lingual portion (SL) of the inferior alveolar nerve (IAN) within the posterior mandibular canal and the lingual (L) portion within the anterior mandibular canal, innervating anterior teeth (the inferior alveolar artery is pulled superiorly to show the IAN).

Figure 7. The superior lingual portion (SL) of the inferior alveolar nerve (IAN) throughout the mandibular canal, innervating anterior teeth.

The MN traveled mainly within the IAN and contained nerve fascicles running in the buccal portion throughout the MC.

DISCUSSION

Knowledge of the anatomy of the MC and its related structures can provide information regarding the degree and extent of damage to the IAN resulting from both direct and indirect injuries. With regard to direct injury, MC configuration and variations could be risk factors in surgical procedures involving the mandible, such as extraction of an impacted third molar, dental implant treatment, and ramus osteotomy.¹²

The intraosseous course of the IAN has been described in several studies of the configuration of the MC and the branching patterns of the IAN.^13–16 The presence of a bifid canal has been reported to occur less than 1%.^17–19 In the present study, accessory and bifid canals were found in 30.0% of cases by dissection and micro-CT observation, a much higher frequency of occurrence than observed in those previous studies. We found that an accessory canal and bifid MCs usually run below the roots of the mandibular molars, and give off nerve branches to the first and second molars. Hence, the possibility of the presence of an accessory canal and a bifid MC should be recognized during implant surgical procedures performed prior to implant fixture placement in the molar region.

Indirect damage following surgical procedures can cause altered sensation. Placement of an implant fixture too close to the MC can impose a mechanical stress on the structures of the MC, resulting in impairments in nerve function.^20,21 It has been suggested that 1.5 to 2.0-mm distance between the implant fixture and the MC is needed to avoid such nerve damage.^22,23

Damage to the inferior alveolar vessels within the MC by either direct or indirect injury results in hemorrhage, which can in turn compress the underlying IAN and MN.²⁴ There are discrepancies between previous studies of the relationship between the IAN and IAA. Li and colleagues²⁵ reported that the blood vessel is located superiorly to the IAN within the MC; Zoud and Doran²⁶ reported that the IAN and IAA form an intertwined plexus throughout the MC; Wadu and colleagues²⁷ stated that the nerve lies between the blood vessels and the bone, and that the vein is anterior to the artery at the mandibular foramen. However, to our knowledge, there has been no study on the classification of the topography of the relationship between the IAN and IAA.

In the present study, we classified the topography of the IAN and IAA into three types, and found that in most cases, the arterial branch is located at the superior buccal aspect of the MC in the mandibular molar and retromolar regions. The anatomical relationship between the IAN and IAA found in the present study is similar to that described in other studies of the anterior MC. The IAA is thus more vulnerable to instrument-induced damage than the IAN during implant surgery.

If the sensory loss resulting from the damage to the IAN reveals the extent of the paresthetic lesion, similar to the case in spinal cord segmental lesions, detailed knowledge of the topography of the IAN could provide a useful basic map with which to interpret the symptoms of a nerve injury, and will aid in repair of the injured nerve. In the present study, the fascicular somatotopic arrangement of IAN and its branches exhibited an array of patterns and variations. However, there was some degree of consistency. The most common patterns of nerve fascicle innervation to the mandibular teeth could be grossly classified into three: (1) the superior buccal portion of the IAN innervating the molars, (2) the superior portion innervating the premolars, and (3) the superior lingual or the superior lingual and inferior lingual portions in the posterior MC and the lingual portions in the anterior MC, innervating the incisors and canine. The buccal two-thirds portion of the IAN was composed of the MN innervating the lower lip, the skin of the chin, and the vestibular gingiva (Figure 8). The innervating patterns of nerve fascicles described in the present study are similar to those detailed previously for the prenatal MC and innervation to the deciduous dentition by Cávez-Lomeli and colleagues.²⁸ These authors stated that the IAN presumably exists in the mandible as three individual nerve paths that arise at different stages of development. The prenatal nerve paths of the IAN with three MCs might still be considerably preserved, thus affecting the organization of the IAN nerve fascicles and its branches in the adult.

Figure 8. The most common spatial fascicular arrangements of the inferior alveolar nerve (IAN). Superior buccal portion (SB) of the IAN innervating the first molar (1st M), second molar (2nd M), third molar (3rd M), and the retromolar area (RM); the superior portion (S) innervating the first premolar (1st PM) and second premolar (2nd PM); the superior lingual portion (SL) or superior lingual and inferior lingual (IL) portions in the posterior mandibular canal, and the lingual portions in the anterior mandibular canal, innervating the central incisor (CI), lateral incisor (LI), and canine (C). The buccal (B) two-thirds portion of the IAN comprised the mental nerve.

In conclusion, by using our results, we can forecast the degree, location, and extent of nerve damage within the MC according to presenting symptoms:

• •
  Sensory loss of the mandibular incisors and canine can result from injury to the superior lingual fascicles and inferior lingual fascicles of the IAN in the molar and retromolar areas, or from the injury to the lingual fascicles of the IAN within the anterior MC.
• •
  Sensory loss of the molars can result from injury to the superior buccal fascicles of the IAN in the molar and retromolar areas.
• •
  Sensory loss of the premolars can result from injury to the superior fascicles of the IAN throughout the MC.
• •
  Sensory loss of the lower lip and chin region can result from damage to the buccal two-thirds of the fascicles of the IAN throughout the MC.

Conversely, it is possible to evaluate nerve symptoms from the injured portion of the MC during implant surgery, genioplasty, and other surgical procedures of the mandible.