Surgical Anatomy of the Hypoglossal Nerve for Facial Nerve Reconstruction Research in Swine

The hypoglossal-facial nerve interpositional nerve graft is a strategy for the treatment of facial paralysis.[1] [2] However, the mechanisms of double/dual innervation[2] and end-to-side neurorrhaphy[1] and the neural supercharge concept[2] remain unclear. To investigate these mechanisms, large animal models are necessary. Miniature swine are used as an experimental or preclinical model for facial surgery, including mandibular reconstruction,[3] distraction osteogenesis,[4] and face transplantation,[5] because the anatomical structure and size of miniature swine are similar to those in humans[6] [7] and because it is a suitable model for surgical training and the teaching of novel transplantation methods.[6]

We reported the surgical anatomy of the miniature swine face, including the buccal branch and the marginal mandibular branch of the facial nerve, in our previous study.[7] Miniature pigs are a suitable experimental model for facial surgery.[7] However, no description of the surgical anatomy of the swine hypoglossal nerve has been published to date. Therefore, this study investigated the surgical anatomy of the hypoglossal nerve in miniature pigs. This study included 10- to 11-month-old male NIBS miniature pigs (Nisseiken Co. Ltd, Tokyo, Japan) (24–33 kg, n = 5). The pigs were anesthetized under sevoflurane-induced general anesthesia. Animal care and handling procedures were performed in accordance with the “Principles of Laboratory Animal Care” of the Tokyo Women's Medical University Animal Experimentation Committee.

A retromandibular to submandibular incision was made in the swine face. The platysma muscle was exposed by undermining the skin and subcutaneous tissue. The platysma muscle was dissected to expose the superficial layer of deep cervical fascia (SLDCF). The marginal mandibular branch of the facial nerve, as well as the facial artery and vein, run through the SLDCF, and the marginal mandibular branch runs parallel to the facial artery and vein on the medial margin of the masseter muscle.[7] The SLDCF was dissected at the margin of the mandible from the posterior of margin of the masseter muscle, causing the medial pterygoid muscle to be exposed. The tissue immediately below the medial pterygoid muscle was dissected toward the condyle. A whitish posterior belly of the digastric muscle was observed ([Fig. 1A]). The hypoglossal nerve was observed to run parallel to the back side of the posterior belly of the digastric muscle ([Fig. 1B]). The dissected tissue immediately below the medial pterygoid muscle contained the marginal mandibular branch.

Fig. 1 Retromandibular view of the miniature swine face after dissection from above of the medial pterygoid muscle and the superficial layer of deep cervical fascia. (A) Arrows indicate the posterior belly of the digastric muscle. (B) The hypoglossal nerve (indicated by blue vessel tape) runs parallel to immediately below the. MM, masseter muscle. MP, medial pterygoid muscle; PBDM, posterior belly of the digastric muscle.

The hypoglossal nerve was isolated and then stimulated using a nerve stimulator (Vari-Stim III, Medtronic, Jacksonville, FL). The nerve stimulation results indicated that the hypoglossal nerve innervated muscles and tissues in the tongue ([Fig. 2]). The human hypoglossal nerve runs beneath the posterior belly of the digastric muscle onto the hypoglossus muscle.[8] The location of the hypoglossal nerve in miniature swine was similar to that observed in humans. The whitish posterior belly of the digastric muscle was characteristic of the hypoglossal nerve. The swine hypoglossal nerve diameter was approximately 3 to 4 mm.

Fig. 2 Schematic diagram of the surgical anatomy of the miniature swine face and hypoglossal nerve, buccal branch, and marginal mandibular branch of the facial nerve innervation. PG, parotid gland, SG, submandibular gland, MM, masseter muscle, ZA, zygomatic arch, BB, buccal branch of the facial nerve, MMB, marginal mandibular branch of the facial nerve, (U), upper division of MMB, (L), lower division of MMB, DM, digastric muscle, HG, hypoglossal nerve.

Toluidine blue staining of the dissected hypoglossal nerve indicated that there were 8,889 ± 211 (n = 3) myelinated fibers in miniature swine ([Fig. 3]). Asaoka et al reported that there were 9,778 ± 1,516 myelinated fibers in a normal human hypoglossal nerve.[9] Mackinnon and Dellon also reported that there were 9,202 ± 2,182 myelinated fibers in humans.[10] It has been indicated that the myelinated fibers of the hypoglossal nerve are similar to those of humans. In conclusion, miniature swine offer a suitable experimental model for the hypoglossal-facial nerve interpositional nerve graft, as the anatomical location and number of myelinated fibers of the hypoglossal nerve in miniature swine are similar to those in humans.

Fig. 3 Toluidine blue staining of the hypoglossal nerve in miniature swine.

• References

• 1 May M, Sobol SM, Mester SJ. Hypoglossal-facial nerve interpositional-jump graft for facial reanimation without tongue atrophy. Otolaryngol Head Neck Surg 1991; 104 (6) 818-825
• 2 Yamamoto Y, Sekido M, Furukawa H, Oyama A, Tsutsumida A, Sasaki S. Surgical rehabilitation of reversible facial palsy: facial—hypoglossal network system based on neural signal augmentation/neural supercharge concept. J Plast Reconstr Aesthet Surg 2007; 60 (3) 223-231
• 3 Terheyden H, Jepsen S, Rueger DR. Mandibular reconstruction in miniature pigs with prefabricated vascularized bone grafts using recombinant human osteogenic protein-1: a preliminary study. Int J Oral Maxillofac Surg 1999; 28 (6) 461-463
• 4 Goldwaser BR, Magill J, Papadaki ME , et al. Continuous mandibular distraction osteogenesis: novel device and preliminary results in minipigs. J Oral Maxillofac Surg 2013; 71 (4) e168-e177
• 5 Kuo YR, Chen CC, Goto S , et al. Immunomodulatory effects of bone marrow-derived mesenchymal stem cells in a swine hemi-facial allotransplantation model. PLoS ONE 2012; 7 (4) e35459
• 6 Swindle MM, Smith AC, Laber-Laird K, Dungan L. Swine in biomedical research: management and models. ILAR J 1994; 36: 1-5
• 7 Sasaki R, Watanabe Y, Yamato M, Aoki S, Okano T, Ando T. Surgical anatomy of the swine face. Lab Anim 2010; 44 (4) 359-363
• 8 Polayes I. M's Surgical treatment of disease of the salivary glands. In: McCarthy JG, , eds. Plastic Surgery, Vol 5 Tumors of the Head & Neck and Skin. Philadelphia, PA: WB Saunders; 1990: 3280
• 9 Asaoka K, Sawamura Y, Nagashima M, Fukushima T. Surgical anatomy for direct hypoglossal-facial nerve side-to-end “anastomosis”. J Neurosurg 1999; 91 (2) 268-275
• 10 Mackinnon SE, Dellon AL. Fascicular patterns of the hypoglossal nerve. J Reconstr Microsurg 1995; 11 (3) 195-198