Int. J. Oral Maxillofac. Surg. 2007; 36: 884–889 doi:10.1016/j.ijom.2007.06.004, available online at http://www.sciencedirect.com Leading Clinical Paper Oral Surgery Lingual nerve injury in third molar surgery I. Observations on recovery of sensation with spontaneous healing S. Hillerup1,2, K. Stoltze1,2 1 Department of Oral and Maxillofacial Surgery, Rigshospitalet, Blegdamsvej 9, DK2100 Copenhagen Ø, Denmark; 2Department of Periodontology, Dental School, Faculty of Health Sciences, University of Copenhagen, Denmark S. Hillerup, K. Stoltze: Lingual nerve injury in third molar surgery. Int. J. Oral Maxillofac. Surg. 2007; 36: 884–889. # 2007 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. Abstract. The aim of this study was to investigate the healing potential of damaged lingual nerves with some remaining function at least 3 months post injury. Fortysix patients were monitored at different time intervals after injury. A simple neurosensory examination included the perception of tactile, thermal stimuli and location of stimulus, as well as two-point discrimination, pain and the presence of a neuroma at the lesion site. Neurogenic signs and symptoms related to the injury and their variation over time were registered. Females were more often referred than males. Most lingual nerve injuries exhibited a significant potential for recovery, but only a few patients made a full recovery with absence of neurogenic symptoms. The recovery rate was highest during the first 6 months. Recovery was not influenced by gender, and only slightly by age. The presence of a neuroma was associated with a more severe injury. Patients should be monitored repeatedly for at least 3 months, and not operated on until neurosensory function no longer improves, and is less than what might be rendered by microsurgical repair. Through proper training and mastery of the surgical approach, every effort should be focused on sparing the lingual nerve, considering its proximity to the field of surgery. The tongue is an important and sensitive anatomical structure that serves a range of vital functions. Unintended iatrogenic injury to the lingual nerve (LN) may happen during third molar surgery due to its 0901-5027/100884 + 06 $30.00/0 anatomical proximity, separated from the cortex of the third molar region only by the periosteum15,16. Some LN injuries cause temporary sensory disturbances but a fraction of cases fail to resolve and result in Key words: lingual nerve; nerve injury; recovery; third molar surgery. Accepted for publication 28 June 2007 Available online 4 September 2007 permanent neurosensory disability, loss of sensory function and neurogenic symptoms7. The incidence of LN injury varies and depends on a number of factors: the # 2007 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. Lingual nerve injury in third molar surgery experience of the surgeon21, difficulty of the case, depth of impaction, presence of overhanging ramus bone, lingual flap elevation, and operating time14, surgical approach19 (lingual split bone technique) and the mere focus on registration and documentation of such injury1,20,26. Rates of temporary effects on the LN after third molar surgery have been reported in the surprisingly high order of magnitude of 15%, and permanent damage may occur in 0.3–0.6%3,4,14. MASON14 demonstrated anatomical factors (depth of impaction, distal overhanging bone, state of eruption and angulation of tooth) and surgical factors (lingual flap elevation, bone removal, lingual plate splitting and operation time), all associated with a significantly increased incidence of disturbance of the LN. Management of LN injury is a challenge to the oral and maxillofacial surgeon, and decision making in terms of therapeutic action, micro-neurosurgical repair versus wait and see, must be based on evidence-based criteria6. These include considerations related to the outcome of neurosensory examination and timing, since an injured nerve may recover with some regained function within a certain time limit. The aims of the present study were to: demonstrate the potential for spontaneous neurosensory recovery in patients that exhibited some nerve function within the first 3 months after the injury or later; describe neurosensory malfunctions associated with the injury and their change over time; investigate the possible influence of age, gender and the presence of a neuroma on neurosensory recovery. Patients and methods Patients with LN injury meeting the criteria given below were drawn from a database of 449 injuries to oral branches of the trigeminal nerve collected consecutively during the period 1987–2005. Of these, 261 were lingual nerve injuries of various etiologies10. Criterion for inclusion: patients with iatrogenic injury to the LN nerve caused by third molar surgery and with some remaining sensory function at 3 months after injury or later, depending on time of referral. Patients seen less than 12 months after the injury were offered one or more reexaminations. Only patients with a course of follow up were included, n = 46. Criterion for exclusion: neurological disease, known alcoholism, patients with bilateral injuries and patients who had received reconstructive micro-neurosurgery. Follow-up examinations were intended at 3, 6 and 12 months post injury or later. The course of follow up was on average 7.4 months (SD = 4.0, range 2–17 months). Neurosensory evaluation Patient records included date and mode of injury, an interview addressing the patients’ subjective assessment of reduced sensory function of the injured LN, and neurogenic malfunctions (paraesthesia, etc.). A simple neurosensory examination was carried out as described previously11,12. Details of the examination protocol have been presented in a recent article10. Follow-up examinations were performed with the examiner blinded to the results of preceding examination(s). Tactile perception of the following stimuli was assessed: (1) feather light touch (by extruded filaments of a cotton stick), (2) pin prick (point of dental probe), (3) point/dull discrimination (point of dental probe versus blunt touch with the tip of the probe handle), (4) warmth (touch of blunt instrument heated to 45–50 8C), (5) cold (touch of blunt instrument cooled to 0– 20 8C), (6) point location (touch of blunt instrument), (7) brush stroke direction (blunt instrument moved over area to be examined). The perception of stimuli 1–7 was rated according to a simple scale ranging from 0 to 3: 0 = no perception of touch, 1 = perception of touch with no ability to differentiate (pointed/blunt, warm/cold, localization of touch, direction of moving touch), 2 = perception with ability to differentiate less clear than normal, and 3 = normal perception10,12. The level of overall neurosensory function was characterized through the sum of perception ratings (1–7) that might range from 0 to 21: sum score 0 signifying a total loss of nerve conductivity and sum score 21 denoting normal neurosensory function of the nerve in question. Two-point discrimination thresholds (2PD) were set to 5, 10, 15, 20 mm (8). Pain perception on pinching with a tissue forceps was rated as present or absent (9). An unpleasant, irradiating sensation in the injured side of the tongue, evoked by digital pressure to the region of suspected injury at the medial aspect of the mandibular ramus, was interpreted as being caused by a traumatic neuroma. The pattern and distribution of fungiform papillae were assessed with the uninjured side as control. 885 Patients with impaired LN function were informed on the potential of improvement of perception rendered by ‘sensory re-education’. They were urged to practice targeted exercises in order to obtain a central adaptation to a changed pattern of afferent neurosensory input22, thus utilizing the plasticity of the central nervous system. Nerve injuries causing signs and symptoms, reduced function or neurogenic malfunction more than 12 months after the injury were considered permanent. Statistics Differences between categorical scores were tested with a ‘sign test’. When appropriate, variables were described through mean, standard deviation (SD), range or median values. Chi-square or Kruskal– Wallis tests were applied to test differences between distributions. Level of significance: 5%. The software used were the EPI6 program for DOS and SPSS for Windows version 13, and graphics were produced with the help of the SPSS and Microsoft Office program packages. Results Demography A significant over-representation of referred female patients was found, F/M ratio among the 46 patients being 33/13 (72%/28%), P < 0.001. The patients’ mean age at time of initial examination was 29 years (SD = 8.9, range 15–53 years) with no difference between gender or side of nerve injury. The average time course from injury to initial examination was 4.5 months (range 0–10 months). Median time between injury and final examination was 12 months (range 3–24 months). The course of healing from initial to final follow-up examination was monitored in all 46 patients. Of these, 19 patients were also examined between the initial and final examinations. Subjective signs and symptoms The patients’ subjective rating of sensory function in the injured side of the tongue at the initial examination was classified as anaesthesia (n = 9), hypoaesthesia (n = 36) and subjective normal sensory function in spite of objective deficit (n = 1). At the final examination the ratings were anaesthesia (n = 1), hypoaesthesia (n = 25) and normal sensation (n = 14). Data for comparison were missing in six patients. 886 Hillerup and Stoltze The patients’ initial ratings of their subjective sensory status averaged score 1.2 according to the rating scale, range 0–3. The sum score rating at the final examination was 1.9. Twenty-seven patients’ scores indicated an improvement in subjective sensory scores (recovery), 11 were unchanged, and eight patients reported a worsening. The recovery, felt and rated by the patients, is statistically significant (P < 0.01). Paraesthesia (n = 29) was the most prevalent neurogenic symptom followed by dysaesthesia (n = 5, unpleasant, painful, burning sensation). Eight patients with initial paraesthesia recovered to normal. Other neurogenic disturbances at the final examination included taste abnormality (n = 15) that might be an inability to recognize taste, typically salt with incapability to adjust while cooking, thermal hypersensitivity (n = 7), speech difficulty (n = 5), pain on tooth brushing (n = 2), and tongue bite (n = 1). Nine out of 11 patients (82%) with full sensory recovery (sum score 21) still had paraesthesia. Neurosensory ratings Pain perception, as an extreme of neurosensory perception, was initially absent in four patients and finally in only one individual. Two-point discrimination thresholds improved considerably during follow up. Initially 12 patients exhibited a 2PD >20 mm. The average threshold value in the remaining patients was 9.7 mm (SD 3.6). For comparison, the 2PD in the uninjured side was 6.3 mm (SD 2.3). At the final examination six patients scored a 2PD threshold >20 mm, and the mean threshold value of the remaining patients was 8.5 (SD 4.3). An average 1.4 mm improvement in 2PD thresholds over time was found (P < 0.05). All tested tactile and thermal qualities (1–7) showed a significant reduction of function compared to the uninjured side at the initial examination. A significant recovery took place over time in terms of improved ratings of the sensory qualities tested (Fig. 1). Improvement was registered in 40 patients, two were unchanged, and in four patients a worsening in sensory perception was recorded (Fig. 2). Recovery was registered mainly during the first 12 months after injury, with the highest rate of sensory regain during the first 6 months, and less improvement beyond 12 months (Fig. 3). Eleven patients (24%) reached normal levels of sensory perception (sum score 21). In the remaining group of patients, 29 Fig. 1. Sensory recovery of tactile and thermal perception, location, and overall subjective perception in patients with LN injury after third molar surgery. Average follow up = 8 months. Paired observations, n = 46. (63%) showed an increase in sum score ranging from 1 to 19, two patients (4%) remained unchanged and four (9%) got worse during follow up. No difference in severity of injury or recovery was found related to gender. The final ratings of neurosensory function showed a negative correlation with age (P < 0.01; Pearson, r = 0.42) (Fig. 4). In terms of recovery, expressed as the difference between final and initial sum score, there was no statistically significant association with age within the range given. Digital pressure to the region of suspected injury at the medial aspect of the mandibular ramus at the initial examination evoked an irradiating abnormal sensation towards the tip of the tongue in 19 patients (53%), a reaction that was interpreted as produced by a traumatic neuroma. No data were obtained in 10 patients, and no such Fig. 2. Sensory recovery of LN after injury caused by third molar surgery in 46 patients. Recovery is expressed in terms of difference between initial and final score ratings of tactile, thermal and locational perception (sum score difference). Average follow up = 8 months. Lingual nerve injury in third molar surgery Fig. 3. Sensory recovery of LN after injury caused by third molar surgery in 46 patients. Sum scores denote the added ratings of perception of seven qualities of stimulus. Rate of recovery is fastest during first 6 months, thereafter fading. reaction was experienced in the healthy side. This feature remained essentially unchanged, since 20 patients (53%) exhibited a similar reaction at the final examination (no data in eight patients). The neurosensory function was more severely affected in patients displaying a traumatic neuroma than in patients without clinical signs of a neuroma at the final examination (P < 0.01; Table 1). The recovery in terms of sensory improvement expressed as the difference in sum scores between final and initial examinations in 18 patients without a neuroma averaged a median value of 5.5 (range 1–21) versus 3.5 (range 8 to 15) in 20 patients with a neuroma. This difference was not statistically significant. The distribution of fungiform papillae was registered at both initial and final examination in 35 patients. In 14 patients, ratings were identical at the two examinations (9 with fewer fungiform papillae in the injured side, 5 without difference between sides), and 16 patients with a reduced number of fungiform papillae ‘normalized’ during follow up. In five patients with evenly distributed fungiform papillae, the number of fungiform papillae reduced in the injured side during the course of follow up. No association was found between the distribution of fungiform papillae and the presence of a neuroma or sensory recovery. Discussion Previous studies have focused on LN injuries and their occasional potential for recovery3,8,14. As shown in the present study, based on history and neurosensory examination of each patient followed over time, injured LNs have a considerable potential for spontaneous recovery. A nerve that appears anaesthetised shortly Fig. 4. LN function after injury caused by third molar surgery correlated with age of patient. Negative influence of age on final nerve function, r = 0.42, P < 0.01 (Pearson correlation). Sum score stands for added ratings of perception of seven qualities of stimulus. 887 after injury may recover to full function depending on the nature of injury and probably the age of the patient. Conversely, follow-up examinations may show a nerve to be injured to a degree that can only be improved by micro-neurosurgical repair. Almost all LN injuries associated with third molar surgery are ‘closed injuries’. This means that the surgeon is not aware of the lesion at the time of surgery, and is unable to diagnose its true nature of origin (compression, traction, partial or total severance) or to classify the lesion according to SUNDERLAND23 at the first postoperative examination. The only way to acquire a clue to the nature of a LN lesion, and to make an evidence-based decision on how to handle the injury, is follow up with repeated and standardised neurosensory examinations6,18. As a general rule, injured LNs in a process of recovery, subjective or objective (sum score improvement or similar), should be monitored according to a follow-up protocol. Micro-neurosurgical repair must be considered in nerves with a persistent, total or near total loss of function beyond 3–6 months, and where the potential benefit of repair will justify microsurgery. The recovery observed in the present study is characteristic for Sunderland grade 2 and 3 lesions, and it may be that the few injuries with poor recovery belonged to grade 423. The rate of recovery proved fastest during the initial 6 months after injury. Later recovery was slower but still possible, and the distinction between recovery of function rendered by healing and improvement due to sensory re-education is difficult. The mode of recovery was in contrast to nerve lesions associated with the injection of local analgesia, where no systematic trend for improvement of sensory functions was found12. This may explain the difference between mechanical nerve injury and the probable neurotoxic damage rendered by certain local analgesics that may mirror Sunderland grade 4 lesions5. Whereas injury to the inferior alveolar nerve may be unavoidable and constitute a calculated risk to be accepted, injuries to the LN can and should be prevented by adaptation of the surgical procedure to the regional anatomy. Surgeons have nothing to do ‘on the wrong side of the periosteum’. As stated by BLACKBURN2: ‘The lesson to be learnt is quite simple, never let the bur enter the tissues on the lingual side of the mandible, whether there is a lingual flap retractor/guard in position or not’. 888 Hillerup and Stoltze Table 1. Association of the presence of a neuroma and neurosensory function (sum score) in patients with LN lesions after third molar surgery Traumatic neuroma Median of sum score (min–max) P* 14.5 (3–21) 20.0 (14–21) <0.001 Present (n = 20) Absent (n = 18) At final examination after an average course of follow up of 7.4 months (SD = 4.0, range 2–17 months). * Kruskal–Wallis test for two groups (equivalent to Chi square). If the unhappy event of an LN injury should occur, the surgeon must deal with the situation in a correct manner. It is almost impossible to establish a prognosis based on only one examination of a nerve injury patient shortly after the damage. The prognosis of a LN lesion may be assessed at 3–6 months after the injury, but still with some uncertainty. If the patient has at least pain perception at this stage, there is hope for further recovery. As seen in Fig. 3, even patients seen for initial examination more than 6 months after the injury showed some regeneration of function. One patient scheduled for surgery on the admission day, 7 months post injury, reported a recent improvement of sensation, and surgery was cancelled. She recovered to a level comparable to that which may be obtained with reasonably successful microsurgical repair. Generally, a patient with persistent total or near total loss of sensation in the affected LN well beyond 6 months will have a lesser chance of spontaneous recovery to a function as good as or better than can be obtained through reconstructive micro-neurosurgery17. Nerve injuries, including LN injuries, are frequent objects of litigation or malpractice suits9,13,24, and the importance of written informed consent to the risk has been emphasized13. Court decisions have varied. HANDSCHEL et al.9 stated: ‘In some former decisions only the fact of the damage was equivalent to a lack of care, while recently other courts had the opinion that an injury of the lingual nerve could also be caused in spite of careful treatment’. Considering the fact that LN injuries in third molar surgery are avoidable, informed consent to such a complication is of questionable ethical value, and focus has to be directed towards adequacy of training in mastering the correct atraumatic surgical approach. The presence of a neuroma indicates fascicular severance with subsequent axonal outgrowth and Schwann cell proliferation, and may be conceived as a feature of the more severe lesions. Cases with a traumatic neuroma are apparently associated with a poorer prognosis than cases with absence of a clinically recognizable neuroma (Table 1). Notably, some patients got worse during the course of follow up. Apart from minor fluctuations ascribable to inaccuracies in the rating of sensory functions, a neuroma in continuity in Sunderland grade 3 lesions23 might constrict intact nerve fibres, establish an intra-fascicular compartment syndrome, or otherwise present an obstacle for nerve conductivity22. LN injury may severely compromise the well-being and quality of life of patients in a number of aspects, including communication, chewing ability and enjoyment of food and drinks. LN injury should be avoided, and merely focussing on the problem is helpful25. References 1. Blackburn CW. A method of assessment in cases of lingual nerve injury. Br J Oral Maxillofac Surg 1990: 28: 238– 245. 2. Blackburn CW. Experiences in lingual nerve repair. Br J Oral Maxillofac Surg 1992: 30: 72–77. 3. Blackburn CW, Bramley PA. Lingual nerve damage associated with the removal of lower third molars. Br Dent J 1989: 167: 103–107. 4. Carmichael FA, McGowan DA. Incidence of nerve damage following third molar removal: a West of Scotland Oral Surgery Research Group Study. Br J Oral Maxillofac Surg 1992: 30: 78–82. 5. Cornelius CP, Roser M, Wiethölter H, Wolburg H. Nerve injection injuries due to local anaesthetics. Experimental work. J Craniomaxillofac Surg 2000: 28(Suppl. 3):134–135. 6. Dodson TB, Kaban LB. Recommendations for management of trigeminal nerve defects based on a critical appraisal of the literature. J Oral Maxillofac Surg 1997: 55: 1380–1386. 7. Fielding AF, Rachiele DP, Frazier G. Lingual nerve paresthesia following third molar surgery. A retrospective clinical study. Oral Surg 1997: 84: 345–348. 8. 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: 306–312. 9. Handschel J, Figgener L, Joos U. Die forensische Bewertung von Verletzungen der Nerven und des Kieferknochens nach Weisheitszahnentfernungen im Blickwinkel der aktuellen Rechtsprechung. Mund Kiefer Gesichtschir 2001: 5: 44–48. 10. Hillerup S. Iatrogenic injury to oral branches of the trigeminal nerve: records of 449 cases. Clin Oral Investig 2007: 11: 133–142. 11. Hillerup S, Hjørting-Hansen E, Reumert T. Repair of the lingual nerve after iatrogenic injury. A follow-up study of return of sensation and taste. J Oral Maxillofac Surg 1994: 52: 1028–1031. 12. Hillerup S, Jensen R. Nerve injury caused by mandibular block analgesia. Int J Oral Maxillofac Surg 2006: 35: 437–443. 13. Lydiatt DD. Litigation and the lingual nerve. J Oral Maxillofac Surg 2003: 61: 197–200. 14. Mason DA. Lingual nerve damage following lower third molar surgery. Int J Oral Maxillofac Surg 1988: 17: 290– 294. 15. Miloro M, Halkias LE, Slone WH, Chakeres DW. Assessment of the lingual nerve in the third molar region using magnetic resonance imaging. J Oral Maxillofac Surg 1997: 55: 134–137. 16. Pogrel MA, Renaut A, Schmidt B, Ammar A. The relationship of the lingual nerve to the mandibular third molar region: an anatomic study. J Oral Maxillofac Surg 1995: 53: 1178–1181. 17. Robinson PP, Loescher AR, Smith KG. A prospective, quantitative study on the clinical outcome of lingual nerve repair. Br J Oral Maxillofac Surg 2000: 38: 255– 263. 18. Robinson PP, Loescher AR, Yates JM, Smith KG. Current management of damage to the inferior alveolar and lingual nerves as a result of removal of third molars. Br J Oral Maxillofac Surg 2004: 42: 285–292. 19. Robinson PP, Smith KG. Lingual nerve damage during lower third molar removal: a comparison of two surgical methods. Br Dent J 1996: 180: 456–461. 20. Robinson PP, Smith KG, Johnson FP, Coppins DA. Equipment and methods for simple sensory testing. Br J Oral Maxillofac Surg 1992: 30: 387–389. 21. Sisk AL, Hammer WB, Shelton DW, Joy ED. Complications following removal of impacted third molars. J Oral Maxillofac Surg 1986: 44: 855–859. 22. Sunderland S. Nerve Injuries and their Repair. A Critical Appraisal. Edinburgh: Churchill Livingstone 1991. 23. Sunderland S. A classification of peripheral nerve injuries producing loss of function. Brain 1951: 74: 491–516. 24. Venta I, Lindqvist C, Ylipaavalniemi P. Malpractice claims for permanent nerve injuries related to third molar removals. Acta Odont Scand 1998: 56: 193–196. Lingual nerve injury in third molar surgery 25. Walters H. Reducing lingual nerve damage in third molar surgery: a clinical audit of 1350 cases. Br Dent J 1995: 25: 140–144. 26. 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. Address: Søren Hillerup Department of Oral and Maxillofacial Surgery Rigshospitalet Blegdamsvej 9 DK-2100 Copenhagen Ø Denmark Tel: +45 35458399 Fax: +45 35452364 E-mail: sohi@rh.dk 889