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Retrograde degeneration of the facial nerve after acute traction on parotid gland: An experimental investigation
Retrograde degeneration of the facial nerve after acute traction on parotid gland: An experimental investigation ZHENGMIN WANG,
MD, PHD,
CHUN-FU DAI,
MD, PHD,
and FANGLU CHI,
The parotid gland of the cat underwent traction for 2 hours (group A) or until the facial nerve was broken (group B). The cats survived postoperatively for 1 day, 2 weeks, 1 month, and 3 months, respectively. Each cat underwent an electroneurography session before they were killed. The facial nerve was harvested and underwent histologic examination. The present study demonstrated that, in group A, the degree of facial nerve degeneration indicated with evoked electroneurography was 100% at 1 day and 2 weeks and 85% and 35%, respectively, at 1 and 3 months after damage. In group B, no electric response was recorded, epineurium of extratemporal segment was broken. This study also showed that the pronounced alteration of the facial nerve following acute traction on the parotid gland was retrograde degeneration; it involved up to its internal acoustic meatus segment. Furthermore, pronounced damage was noted in its stylomastoid foramen and extratemporal segment. (Otolaryngol Head Neck Surg 2002;127:55-59.)
T he facial nerve of the intratemporal segment is within the fallopian canal, greater superficial petrosal nerve, tympanic chorda, and stapedial muscle nerve stem from this segment. The facial nerve of extratemporal segment is embedded in the parotid gland. On the basis of anatomy of the facial nerve, acute stretch of the facial nerve occurred with removal of a parotid gland tumor, lateral skull surgery, and fracture of the skull base. Acute stretch of the facial nerve frequently resulted in facial paralysis. Although many studies have been conducted on facial nerve stretching, most focused on chronic From the Department of Otolaryngology, Eye Ear Nose and Throat Hospital, Medical Center of Fudan University. Reprint requests: Chun-Fu Dai, MD, Department of Otolaryngology, Eye, Ear, Nose, and Throat Hospital, Medical Center of Fudan University. Shanghai 200031, Peoples Republic of China; e-mail, [email protected]. Copyright © 2002 by the American Academy of Otolaryngology–Head and Neck Surgery Foundation, Inc. 0194-5998/2002/$35.00 ⫹ 0 23/77/126720 doi:10.1067/mhn.2002.126720
MD, PHD,
Shanghai, China
expansion of the facial nerve. Growth of tumor in internal acoustic meatus and parotid gland results in chronic expansion of the facial nerve. The nerve has a high degree of plasticity, often retaining its function despite being inordinately stretched by a larger tumor. Studies have reported elongation of the peripheral nerve trunk from 4% to 100% with no impact on neuronal function.1 Many believed that the nerves were highly resistant to expansion. The nerves tolerate a greater degree of expansion when the rate of expansion is slow. In fact, nerves have been observed to expand up to 100% when stretched by slowly growing tumors with minimal impact on the function.2 Recent findings suggested that the extracranial facial nerve could tolerate significant stretching without demonstrating impaired function.3-5 When the facial nerve was expanded by stages in 7 sessions over a period of 40 days, the length of the nerve increased an average of 95% without significantly impairing nerve function.3 Our previous study showed the facial nerve underwent retrograde degeneration after the facial nerve was stretched for 2 hours. However, in that study the traction force was applied directly on the facial nerve and compressed the nerve stylomastoid foramen. This made contribution to pronounced fibrosis in mastoid and extratemporal segment.6 Histologic and functional changes after acute stretching of the facial nerve are poorly understood. In the present study, we mimicked lateral skull base surgery; the facial nerve underwent stretching through stretching of parotid gland for 2 hours or until the facial nerve became broken as a result of the parotid gland being displaced far away. Electroneurography and histologic examination were performed postoperatively to clarify the pathologic processes. MATERIALS AND METHODS Animals Thirty-four cats weighing from 1.6 to 3.3 kg were used in this study. Anesthesia was achieved by through inhalation of 0.5% to 1% isoflurane, 55
Otolaryngology– Head and Neck Surgery July 2002
56 WANG et al
1:1 N2O/O2 with intubation. An incision was made in the preauricular area, and the parotid gland was exposed and wrapped with terylend mash work (10-mm width, 0.2-mm thickness), and stretched with a weight. As a result, its traction force was increased. The animals were divided into 2 groups. In group A (18 cats), the parotid gland was shifted 15mm away laterally for 2 hours maintain the parotid gland in displacement traction force of 460 to 920g. In group B (16 cats), Traction force increased until the facial nerve broke at the stylomastoid foramen; traction force ranged from 800 to 1780g. All surgery was performed on the left side; the right facial nerve served as the normal control. Each cat was given intramuscular antibiotics to minimize the possibility of infectious complication. The methods and protocol of the study were reviewed and approved by the Institutional Animal Care and Use Committee of Medical Center of Fudan University.
were immersed in 3% glutaraldehyde for 2 hours, 1% osmium tetroxide for 1 hour, and then dehydration in grade alcohol; then they were embedded in Epon 812. Semithin sections were made and stained with toluidine blue for microscopic examination, and thin sections were stained with uranyl acetate and lead citrate for electron microscopic examination (JEM-2000CX; Japan).
Test of Facial Nerve Function
In group A, the degree of facial nerve degeneration was 100% at 1 day postoperatively, and it remained 100% at 2 weeks postoperatively, 85% at 1 month postoperatively, and 35% at 3 months postoperatively. In group B, there was no electric response in the proximal and distal stump of the facial nerve after injury.
The Nicolet Compact Model 4 (Nicolet Instrument Corporation, Madison, WI) was used for the electroneurography study. Each cat underwent an electroneurographic session before being killed. The method used for lead placement was described by Fisch.7 The facial nerve was stimulated with bipolar stimulating electrodes, and the amplitude of evoked CAP was recorded. The degree of facial nerve degeneration was calculated with the formula: Degree of Facial Nerve Degeneration ⫽ (1-amplitude of left facial nerve/amplitude of right facial nerve) ⫻ 100. Histologic Examination After the electrodiagnostic test was completed, each animal was killed with deep anesthesia. The animals were killed at 1 day (4 in group A, 4 in group B), at 2 weeks (4 in group A, 4 in group B), at 1 month (6 in group A, 4 in group B), and at 3 months (4 in group A, 4 in group B), postoperatively. The facial nerve was exposed from the internal acoustic meatus to the parotid gland and removed and then divided into extratemporal, mastoid, tympanic, labyrinthine, and internal acoustic meatus portions. The nerves were examined macroscopically and prepared for histologic and electron microscopic study. All segments
RESULTS Length of Facial Nerve The length of the extratemporal segment increased to an average of 350% of normal control in group B, and in group A, the facial nerve was elongated to an average of 150% of normal control. All stretched nerves appeared to be thinned out, but the thickness of the nerve was not calibrated. Electroneurography
Histologic Examination Macroappearance. Obvious pathologic processes appeared in the animals that developed facial palsy regardless of whether the facial nerve was continued or broken. Even if considerable variation in degree was noted, the characteristics and extension were similar. In group A, only elongation of facial nerve was observed. In group B, epineurium of extratemporal segment was broken; however, epineurium of fallopian canal segment remained intact, and there was no necrosis and hernia of the facial nerve. Microappearance. In both groups A and B, acute nerve degeneration (axonal swelling or disintegrates), vein congestion, and interstitial edema were noted in extratemporal and stylomastoid segments 1 day postoperatively, These changes were most pronounced around the stylomastoid foramen (Fig 1). Retrograde axonal degeneration extended to the tympanic segment 1 day postoperatively. Two weeks postoperatively, proliferation
Otolaryngology– Head and Neck Surgery Volume 127 Number 1
WANG et al 57
Fig 1. Axonal degeneration with fiber deformation exhibited in mastoid segment of facial nerve 1 day postoperatively (toluidine blue stain, original magnification ⫻480).
Fig 3. Regenerative axons arranged in cluster with fibroblast (arrowhead) proliferation in genicular ganglion of facial nerve 1 month postoperatively (toluidine blue stain, original magnification ⫻960).
Fig 2. Schwann cell (arrowhead) proliferation with macrophagocyte (star) distributed along the vessel of endoneurium in the internal acoustic meatus segment of facial nerve 2 weeks postoperatively (toluidine blue stain, original magnification ⫻768).
Fig 4. Connective tissue proliferation was identified with a few regenerative axons (arrowhead) at the mastoid segment 3 months postoperatively (toluidine blue stain, original magnification ⫻480).
of Schwann cells at extratemporal segment was identified. Macrophages with cytorhyctes were arranged around the blood vessels of endoneurium. Labyrinthine and internal acoustic meatus segment also exhibited significant histologic changes; axon degeneration and proliferation of Schwann cell were observed. The results indicated that degeneration of proximal segment resulting from parotid gland stretching could involve the internal acoustic meatus segment (Fig 2). One month postoperatively, proliferation of connective tissue
from epineurium and endoneurium was observed in extratemporal and mastoid segments; a few regenerated axons reached the distal segment. A number of regeneration axons were identified in tympanic, labyrinthine, and internal acoustic meatus segment (Fig 3), depending on the strength of the traction force applied to the nerve. Three months postoperatively, more connective tissue proliferation was noted at extratemporal and mastoid segments with a few regenerative axons reaching distal stumps (Fig 4). The histologic
58 WANG et al
study indicated that facial nerve of extratemporal and mastoid segments were partly damaged after parotid gland stretching. Moreover, there was retrograde degeneration that could reach the internal acoustic meatus. In group A, the incidence of retrograde degeneration of the tympanic, labyrinthine, and internal acoustic meatus segments was 77.8% (14 cats), 55.6% (10 cats), and 27.8% (5 cats), respectively. In group B, the retrograde degeneration extended to the segment of internal acoustic meatus of all animals. DISCUSSION Functional and morphologic changes after peripheral nerve stretching were related to the severity of the force; the length of time during which a force is applied, the internal arrangement of the fascicles, their number and size of axons, and the amount of epineurium present also influence the impact of a traction injury.2 In any case, increasing traction first blocked conduction without significantly altering the morphology of the nerve. The effects of such an injury narrow the fascicles, increasing the intrafascicular pressure and reducing neural blood flow, thereby adversely affecting nerve conduction.8-10 Complete ischemia of nerve causes their function to deteriorate within 30 to 90 minutes.11 The histologic and chemical responses of neuronal degeneration and regeneration after injury and various pathologic processes of the human facial nerve have been well described.12 One study of traction injury suggests that the amount of traction needed to produce facial nerve palsy varies greatly. Intermittent traction has less effect on facial nerve function than does continuous traction.13 To sustain a mechanical injury, the longitudinal stretch applied to a nerve must exceed the inherent limits of elasticity of the nerve. In this study, facial nerve elongated to 150% of normal control after parotid gland stretching for 2 hours. It also resulted in 100% degeneration of facial nerve, which partly recovered from the injury. The degree of degeneration of facial nerve was 35% at 3 months postoperatively. When the facial nerve was bluntly stretched and extended to 115% to 120% of its original length, the stretching injury had no electric reflection after injury, with the recovery starting on the 30th day and approaching normal on the
Otolaryngology– Head and Neck Surgery July 2002
60th day. Histologic studies revealed that the myelin lesion was more severe than the axonal lesion. The myelin lesion was stable by the 30th day, and recovery started on the 60th day. The axonal lesion began to recover on the 15th day and was fully recovered on the 90th day.14 Dakin et al5 reported elongation of up to 95% of facial nerve trunk over a period of 40 days without an impact on function; histologic study revealed that expanded nerve showed increased polymorphonuclear leukocyte and macrophages predominantly in the subperineural zone and a reduction in the number of axons compared with control. Nerves tolerate a greater degree of expansion when the rate of expansion is slow. In fact, nerve has been observed to expand up to 100% when stretched by a slowly growing tumor with minimal impact on the function.2 It is reasonable to conclude that acute stretching does more damage to expanded nerve. The present study indicated that the pronounced alteration of the facial nerve after acute traction on parotid gland was retrograde degeneration; it even involved the internal acoustic meatus segment depending on the strength of the traction force on parotid gland or the displacement of the parotid gland. We must be cognizant of the fact that the injury is not isolated to one segment of the nerve but affects its entire length. The most clinically relevant injury may be far from the site of actual trauma. It was also found that the perineurium and epineurium were almost intact. Thus, it was reasonable to speculate that retrograde degeneration resulted from direct stretching of the nerve fibers. Nerve traction injury is also compression injury with an ischemic component, which can cause impairment of both the intrinsic and extrinsic nutrient vasculature and lead to extensive intraneural edema. The retrograde effect is most probably due to damming of the blocked axoplasmatic flow after intraneural edema. It is well known that the facial nerve occupies more than 80% of the crosssectional area of the surrounding facial canal between the meatal foramen and geniculate ganglion. In contrast, the nerve occupies less than 75% of the facial canal lumen as it courses peripherally through the distal tympanic and vertical segment of the canal, and these levels maintains a
Otolaryngology– Head and Neck Surgery Volume 127 Number 1
buffering space that likely reduces the risk of significant axonal injury.15,16 Grovman et al17 presented findings from a patient who died of intracranial injuries soon after the injury. Partial left facial nerve paralysis developed 5 days after the trauma. The facial palsy progressed to paralysis. The patient died 12 days after the trauma and 7 days after the onset of facial paralysis. The fracture line went through the horizontal segment but, interestingly, the intraneural edema and demyelinization extended proximally to the meatal foramen. Injury of the facial nerve at the horizontal segment resulted in retrograde degeneration; the findings supported our results. CONCLUSIONS The present results indicate that pronounced alteration of the facial nerve after acute traction on parotid gland was retrograde degeneration; it even involved the internal acoustic meatus segment. In this case, once the facial nerve underwent decompression surgery, total surgical exploration of the facial nerve should be performed from the meatal foramen to the styloid foramen. The fibrosis in mastoid segment would interfere with axonal regeneration. In case facial palsy does not recover 3 months postoperatively, we recommend that the mastoid segment should be removed and that nerve grafting should be performed. The authors are grateful to Dr Renee Cohen and Assoc Prof Yuezhen Dai for their helpful comments on the manuscript. REFERENCES
1. Hoen TI, Brackett CE. Peripheral nerve lengthening. J Neurosurg 1956;13:43-62.
WANG et al 59
2. Sunderland S. Nerve and Nerve Injuries. Edinburgh/London/New York: Churchill Livingstone; 1978. p. 4-13. 3. Anand VK. Plasticity of the extracranial facial nerve. Laryngscope 1997;107:1393-404. 4. Malis DS, MacMillian JG, Kelley JL. Tissue expansion of the facial nerve in an animal model. Ear Nose Throat J 1995;74:261-70. 5. Dakin K, Sanders T, Harrison S, et al. Electroneurography during facial nerve expansion. Otolaryngol Head Neck Surg 1998;119:603-8. 6. Wang ZM, Kishimoto S, Felix H, et al. Experimentell erzeugte Dehnung des Nervus facialis bei Katzen. Akt Probl Otorhinolaryngol 1983;6:95-100. 7. Fisch U. Maximal nerve excitability testing vs EnoG. Arch Otolaryngol 1980;106:352-7. 8. Lundberg G, Rydevck B, Gothenburg. Effects of stretching the tibia nerve of the rabbit. J Bone Joint Surg 1973;55:390-8. 9. Vander Wey LP, Gabreels-Festen, Merks MH. Peripheral nerve elongation by laser Doppler flowmeter controlled expansion: morphological aspects. Acta Neuropathol 1995;89:166-9. 10. Vander Wey LP, Polder TW, Merks MH. Peripheral nerve elongation by laser Doppler flowmeter controlled expansion: functional and neurophysiological aspects. J Neural Sci 1994;12:149-56. 11. Tzadink A, Babin RW, Ryu JH. Hypotension induced neuropraxia in the cat facial nerve. Otolaryngol Head Neck Surg 1982;90:163-7. 12. May M. The Facial Nerve. New York: Thieme; 1986. p. 78-80. 13. Hart PF. Traction injury of the facial nerve in rabbit. Aust N Z J Surg 1971;41:75-80. 14. Cai ZG, Yu GG, Ma DQ, et al. Experimental studies on traumatic facial nerve injury. J Laryngol Otol 1998;112: 243-7. 15. Brodie HA, Thompson TC. Management of complications from 820 temporal bone fractures. Am J Otol 1997; 18:188-97. 16. McKennan KX, Chole RA. Facial paralysis in temporal bone trauma. Am J Otol 1992;13:167-72. 17. Grovman LR, Pollak A, Fisch U. Entrapment injury of the facial nerve resulting from longitudinal fracture of the temporal bone. Otolaryngol Head Neck Surg 1989;101: 404-8.
MD, PHD,
CHUN-FU DAI,
MD, PHD,
and FANGLU CHI,
The parotid gland of the cat underwent traction for 2 hours (group A) or until the facial nerve was broken (group B). The cats survived postoperatively for 1 day, 2 weeks, 1 month, and 3 months, respectively. Each cat underwent an electroneurography session before they were killed. The facial nerve was harvested and underwent histologic examination. The present study demonstrated that, in group A, the degree of facial nerve degeneration indicated with evoked electroneurography was 100% at 1 day and 2 weeks and 85% and 35%, respectively, at 1 and 3 months after damage. In group B, no electric response was recorded, epineurium of extratemporal segment was broken. This study also showed that the pronounced alteration of the facial nerve following acute traction on the parotid gland was retrograde degeneration; it involved up to its internal acoustic meatus segment. Furthermore, pronounced damage was noted in its stylomastoid foramen and extratemporal segment. (Otolaryngol Head Neck Surg 2002;127:55-59.)
T he facial nerve of the intratemporal segment is within the fallopian canal, greater superficial petrosal nerve, tympanic chorda, and stapedial muscle nerve stem from this segment. The facial nerve of extratemporal segment is embedded in the parotid gland. On the basis of anatomy of the facial nerve, acute stretch of the facial nerve occurred with removal of a parotid gland tumor, lateral skull surgery, and fracture of the skull base. Acute stretch of the facial nerve frequently resulted in facial paralysis. Although many studies have been conducted on facial nerve stretching, most focused on chronic From the Department of Otolaryngology, Eye Ear Nose and Throat Hospital, Medical Center of Fudan University. Reprint requests: Chun-Fu Dai, MD, Department of Otolaryngology, Eye, Ear, Nose, and Throat Hospital, Medical Center of Fudan University. Shanghai 200031, Peoples Republic of China; e-mail, [email protected]. Copyright © 2002 by the American Academy of Otolaryngology–Head and Neck Surgery Foundation, Inc. 0194-5998/2002/$35.00 ⫹ 0 23/77/126720 doi:10.1067/mhn.2002.126720
MD, PHD,
Shanghai, China
expansion of the facial nerve. Growth of tumor in internal acoustic meatus and parotid gland results in chronic expansion of the facial nerve. The nerve has a high degree of plasticity, often retaining its function despite being inordinately stretched by a larger tumor. Studies have reported elongation of the peripheral nerve trunk from 4% to 100% with no impact on neuronal function.1 Many believed that the nerves were highly resistant to expansion. The nerves tolerate a greater degree of expansion when the rate of expansion is slow. In fact, nerves have been observed to expand up to 100% when stretched by slowly growing tumors with minimal impact on the function.2 Recent findings suggested that the extracranial facial nerve could tolerate significant stretching without demonstrating impaired function.3-5 When the facial nerve was expanded by stages in 7 sessions over a period of 40 days, the length of the nerve increased an average of 95% without significantly impairing nerve function.3 Our previous study showed the facial nerve underwent retrograde degeneration after the facial nerve was stretched for 2 hours. However, in that study the traction force was applied directly on the facial nerve and compressed the nerve stylomastoid foramen. This made contribution to pronounced fibrosis in mastoid and extratemporal segment.6 Histologic and functional changes after acute stretching of the facial nerve are poorly understood. In the present study, we mimicked lateral skull base surgery; the facial nerve underwent stretching through stretching of parotid gland for 2 hours or until the facial nerve became broken as a result of the parotid gland being displaced far away. Electroneurography and histologic examination were performed postoperatively to clarify the pathologic processes. MATERIALS AND METHODS Animals Thirty-four cats weighing from 1.6 to 3.3 kg were used in this study. Anesthesia was achieved by through inhalation of 0.5% to 1% isoflurane, 55
Otolaryngology– Head and Neck Surgery July 2002
56 WANG et al
1:1 N2O/O2 with intubation. An incision was made in the preauricular area, and the parotid gland was exposed and wrapped with terylend mash work (10-mm width, 0.2-mm thickness), and stretched with a weight. As a result, its traction force was increased. The animals were divided into 2 groups. In group A (18 cats), the parotid gland was shifted 15mm away laterally for 2 hours maintain the parotid gland in displacement traction force of 460 to 920g. In group B (16 cats), Traction force increased until the facial nerve broke at the stylomastoid foramen; traction force ranged from 800 to 1780g. All surgery was performed on the left side; the right facial nerve served as the normal control. Each cat was given intramuscular antibiotics to minimize the possibility of infectious complication. The methods and protocol of the study were reviewed and approved by the Institutional Animal Care and Use Committee of Medical Center of Fudan University.
were immersed in 3% glutaraldehyde for 2 hours, 1% osmium tetroxide for 1 hour, and then dehydration in grade alcohol; then they were embedded in Epon 812. Semithin sections were made and stained with toluidine blue for microscopic examination, and thin sections were stained with uranyl acetate and lead citrate for electron microscopic examination (JEM-2000CX; Japan).
Test of Facial Nerve Function
In group A, the degree of facial nerve degeneration was 100% at 1 day postoperatively, and it remained 100% at 2 weeks postoperatively, 85% at 1 month postoperatively, and 35% at 3 months postoperatively. In group B, there was no electric response in the proximal and distal stump of the facial nerve after injury.
The Nicolet Compact Model 4 (Nicolet Instrument Corporation, Madison, WI) was used for the electroneurography study. Each cat underwent an electroneurographic session before being killed. The method used for lead placement was described by Fisch.7 The facial nerve was stimulated with bipolar stimulating electrodes, and the amplitude of evoked CAP was recorded. The degree of facial nerve degeneration was calculated with the formula: Degree of Facial Nerve Degeneration ⫽ (1-amplitude of left facial nerve/amplitude of right facial nerve) ⫻ 100. Histologic Examination After the electrodiagnostic test was completed, each animal was killed with deep anesthesia. The animals were killed at 1 day (4 in group A, 4 in group B), at 2 weeks (4 in group A, 4 in group B), at 1 month (6 in group A, 4 in group B), and at 3 months (4 in group A, 4 in group B), postoperatively. The facial nerve was exposed from the internal acoustic meatus to the parotid gland and removed and then divided into extratemporal, mastoid, tympanic, labyrinthine, and internal acoustic meatus portions. The nerves were examined macroscopically and prepared for histologic and electron microscopic study. All segments
RESULTS Length of Facial Nerve The length of the extratemporal segment increased to an average of 350% of normal control in group B, and in group A, the facial nerve was elongated to an average of 150% of normal control. All stretched nerves appeared to be thinned out, but the thickness of the nerve was not calibrated. Electroneurography
Histologic Examination Macroappearance. Obvious pathologic processes appeared in the animals that developed facial palsy regardless of whether the facial nerve was continued or broken. Even if considerable variation in degree was noted, the characteristics and extension were similar. In group A, only elongation of facial nerve was observed. In group B, epineurium of extratemporal segment was broken; however, epineurium of fallopian canal segment remained intact, and there was no necrosis and hernia of the facial nerve. Microappearance. In both groups A and B, acute nerve degeneration (axonal swelling or disintegrates), vein congestion, and interstitial edema were noted in extratemporal and stylomastoid segments 1 day postoperatively, These changes were most pronounced around the stylomastoid foramen (Fig 1). Retrograde axonal degeneration extended to the tympanic segment 1 day postoperatively. Two weeks postoperatively, proliferation
Otolaryngology– Head and Neck Surgery Volume 127 Number 1
WANG et al 57
Fig 1. Axonal degeneration with fiber deformation exhibited in mastoid segment of facial nerve 1 day postoperatively (toluidine blue stain, original magnification ⫻480).
Fig 3. Regenerative axons arranged in cluster with fibroblast (arrowhead) proliferation in genicular ganglion of facial nerve 1 month postoperatively (toluidine blue stain, original magnification ⫻960).
Fig 2. Schwann cell (arrowhead) proliferation with macrophagocyte (star) distributed along the vessel of endoneurium in the internal acoustic meatus segment of facial nerve 2 weeks postoperatively (toluidine blue stain, original magnification ⫻768).
Fig 4. Connective tissue proliferation was identified with a few regenerative axons (arrowhead) at the mastoid segment 3 months postoperatively (toluidine blue stain, original magnification ⫻480).
of Schwann cells at extratemporal segment was identified. Macrophages with cytorhyctes were arranged around the blood vessels of endoneurium. Labyrinthine and internal acoustic meatus segment also exhibited significant histologic changes; axon degeneration and proliferation of Schwann cell were observed. The results indicated that degeneration of proximal segment resulting from parotid gland stretching could involve the internal acoustic meatus segment (Fig 2). One month postoperatively, proliferation of connective tissue
from epineurium and endoneurium was observed in extratemporal and mastoid segments; a few regenerated axons reached the distal segment. A number of regeneration axons were identified in tympanic, labyrinthine, and internal acoustic meatus segment (Fig 3), depending on the strength of the traction force applied to the nerve. Three months postoperatively, more connective tissue proliferation was noted at extratemporal and mastoid segments with a few regenerative axons reaching distal stumps (Fig 4). The histologic
58 WANG et al
study indicated that facial nerve of extratemporal and mastoid segments were partly damaged after parotid gland stretching. Moreover, there was retrograde degeneration that could reach the internal acoustic meatus. In group A, the incidence of retrograde degeneration of the tympanic, labyrinthine, and internal acoustic meatus segments was 77.8% (14 cats), 55.6% (10 cats), and 27.8% (5 cats), respectively. In group B, the retrograde degeneration extended to the segment of internal acoustic meatus of all animals. DISCUSSION Functional and morphologic changes after peripheral nerve stretching were related to the severity of the force; the length of time during which a force is applied, the internal arrangement of the fascicles, their number and size of axons, and the amount of epineurium present also influence the impact of a traction injury.2 In any case, increasing traction first blocked conduction without significantly altering the morphology of the nerve. The effects of such an injury narrow the fascicles, increasing the intrafascicular pressure and reducing neural blood flow, thereby adversely affecting nerve conduction.8-10 Complete ischemia of nerve causes their function to deteriorate within 30 to 90 minutes.11 The histologic and chemical responses of neuronal degeneration and regeneration after injury and various pathologic processes of the human facial nerve have been well described.12 One study of traction injury suggests that the amount of traction needed to produce facial nerve palsy varies greatly. Intermittent traction has less effect on facial nerve function than does continuous traction.13 To sustain a mechanical injury, the longitudinal stretch applied to a nerve must exceed the inherent limits of elasticity of the nerve. In this study, facial nerve elongated to 150% of normal control after parotid gland stretching for 2 hours. It also resulted in 100% degeneration of facial nerve, which partly recovered from the injury. The degree of degeneration of facial nerve was 35% at 3 months postoperatively. When the facial nerve was bluntly stretched and extended to 115% to 120% of its original length, the stretching injury had no electric reflection after injury, with the recovery starting on the 30th day and approaching normal on the
Otolaryngology– Head and Neck Surgery July 2002
60th day. Histologic studies revealed that the myelin lesion was more severe than the axonal lesion. The myelin lesion was stable by the 30th day, and recovery started on the 60th day. The axonal lesion began to recover on the 15th day and was fully recovered on the 90th day.14 Dakin et al5 reported elongation of up to 95% of facial nerve trunk over a period of 40 days without an impact on function; histologic study revealed that expanded nerve showed increased polymorphonuclear leukocyte and macrophages predominantly in the subperineural zone and a reduction in the number of axons compared with control. Nerves tolerate a greater degree of expansion when the rate of expansion is slow. In fact, nerve has been observed to expand up to 100% when stretched by a slowly growing tumor with minimal impact on the function.2 It is reasonable to conclude that acute stretching does more damage to expanded nerve. The present study indicated that the pronounced alteration of the facial nerve after acute traction on parotid gland was retrograde degeneration; it even involved the internal acoustic meatus segment depending on the strength of the traction force on parotid gland or the displacement of the parotid gland. We must be cognizant of the fact that the injury is not isolated to one segment of the nerve but affects its entire length. The most clinically relevant injury may be far from the site of actual trauma. It was also found that the perineurium and epineurium were almost intact. Thus, it was reasonable to speculate that retrograde degeneration resulted from direct stretching of the nerve fibers. Nerve traction injury is also compression injury with an ischemic component, which can cause impairment of both the intrinsic and extrinsic nutrient vasculature and lead to extensive intraneural edema. The retrograde effect is most probably due to damming of the blocked axoplasmatic flow after intraneural edema. It is well known that the facial nerve occupies more than 80% of the crosssectional area of the surrounding facial canal between the meatal foramen and geniculate ganglion. In contrast, the nerve occupies less than 75% of the facial canal lumen as it courses peripherally through the distal tympanic and vertical segment of the canal, and these levels maintains a
Otolaryngology– Head and Neck Surgery Volume 127 Number 1
buffering space that likely reduces the risk of significant axonal injury.15,16 Grovman et al17 presented findings from a patient who died of intracranial injuries soon after the injury. Partial left facial nerve paralysis developed 5 days after the trauma. The facial palsy progressed to paralysis. The patient died 12 days after the trauma and 7 days after the onset of facial paralysis. The fracture line went through the horizontal segment but, interestingly, the intraneural edema and demyelinization extended proximally to the meatal foramen. Injury of the facial nerve at the horizontal segment resulted in retrograde degeneration; the findings supported our results. CONCLUSIONS The present results indicate that pronounced alteration of the facial nerve after acute traction on parotid gland was retrograde degeneration; it even involved the internal acoustic meatus segment. In this case, once the facial nerve underwent decompression surgery, total surgical exploration of the facial nerve should be performed from the meatal foramen to the styloid foramen. The fibrosis in mastoid segment would interfere with axonal regeneration. In case facial palsy does not recover 3 months postoperatively, we recommend that the mastoid segment should be removed and that nerve grafting should be performed. The authors are grateful to Dr Renee Cohen and Assoc Prof Yuezhen Dai for their helpful comments on the manuscript. REFERENCES
1. Hoen TI, Brackett CE. Peripheral nerve lengthening. J Neurosurg 1956;13:43-62.
WANG et al 59
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