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Intraneural Hematoma: A Proposed Anatomic Classification with Potential Treatment Implications
Original Article
Intraneural Hematoma: A Proposed Anatomic Classification with Potential Treatment Implications Godard C. W. de Ruiter1, Nikhil K. Prasad2, Robert J. Spinner2, Allen H. Maniker3
Intraneural hematoma is a rare entity with fewer than 20 cases reported in the literature. There is no consensus on surgical treatment due to its rarity. We present a novel classification for intraneural hematomas based on a review of the literature and illustrated by 4 cases that were treated in our 3 centers. This classification system localizes the hematoma to the different connective tissue layers that compose the nerve: the paraneurium, epineurium, and perineurium. We believe that this classification has consequences for surgical treatment and can form the foundation for future research into the natural history of these types of lesions.
and torsional forces. From outside to inside these layers are called the paraneurium, epineurium, perineurium, and endoneurium (Figure 1). The paraneurium (sometimes referred to as the mesoneurium) comprises thin films of adipose and connective tissue that surround the relatively thicker epineurium.6 The epineurium consists of 2 parts: 1) the dense extrafascicular (or outer) epineurium, which is made largely of collagen to contain and protect the nerve fascicles; and 2) the interfascicular (or inner) epineurium, which has more adipose and is similar in consistency to the paraneurium.6 The perineurium, which forms the blood-nerve barrier, is a dense multilaminar sheath composed of alternating mesothelial cell and collagen layers surrounding individual fascicles.7 Finally, the endoneurium (also called the basal lamina tube) is the layer through which the individual axon runs. MATERIALS AND METHODS
INTRODUCTION
T
he extrinsic compression of peripheral nerves due to a collection of blood (extraneural hematoma) within osteofibrous tunnels or intermuscular compartments is well recognized.1e5 Occasionally hematomas may form within the nerve (intraneural hematoma) as a consequence of trauma or spontaneously due to a derangement in the patient’s clotting function. Although these lesions may resorb spontaneously, many surgeons opt for timely decompression to prevent irreversible damage to the nerve. Case reports of this condition have been sporadic, and no consensus exists on the best surgical management. We introduce a novel anatomic classification system for intraneural hematomas to guide surgical planning on the basis of a thorough review of the literature and 4 cases from our own experience. ANATOMIC FRAMEWORK Peripheral nerves are composed of connective tissue layers that isolate and protect individual nerve fascicles from compressive
All cases of intraneural hematoma encountered in the past 5 years at our 3 centers were reviewed. The hematomas were classified according to the connective tissue layers mentioned earlier: subparaneurial, subepineurial, and intrafascicular. We chose the term intrafascicular instead of subperineurial because of potential confusion with the subparaneurial layer. Hematoma that occupied several different layers was classified as multicompartmental. LITERATURE REVIEW A thorough review of 3 databases—PubMed, Medline, and Google Scholar—was performed, using the search terms “intraneural,” “epineural,” “intrafascicular,” “hematoma,” and “peripheral nerve.” Results obtained after this first pass were cross referenced to obtain missing data. The details of each case report were reviewed looking for demographic information, affected nerve, mechanism of injury, associated coagulopathy/anticoagulant use, and surgical management. Each case was then classified according
To whom correspondence should be addressed: Godard C. W. de Ruiter, M.D. Ph.D. [E-mail: [email protected]]
Key words Hematoma - Interfascicular - Intrafascicular - Subepineurial - Subparaneurial -
Citation: World Neurosurg. (2015) 84, 6:1977-1984. http://dx.doi.org/10.1016/j.wneu.2015.08.063 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1
From the Departments of Neurosurgery, Medical Center Haaglanden, The Hague, The Netherlands; 2Neurosurgery, Mayo Clinic Rochester, Minnesota, USA; 3Neurosurgery, Mount Sinai Beth Israel Medical Center, New York, New York, USA
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ORIGINAL ARTICLE GODARD C. W. DE RUITER ET AL.
CLASSIFICATION OF INTRANEURAL HEMATOMA
Table 1. Four Cases of Intraneural Hematoma Type of Intraneural Hematoma Based on Location in the Nerve
Figure 1. Normal anatomy of the peripheral nerve illustrating the different layers, from outside to inside: paraneurium, epineurium, perineurium, and endoneurium.
to the anatomic framework, using descriptions provided and imaging (when available). RESULTS Cases Illustrations We identified 4 cases of intraneural hematoma and classified them according to the anatomic framework (Table 1): 1 subparaneurial hematoma (Figure 2, Case 1); 2 subepineurial hematomas, 1
Surgical Treatment
Subparaneurial
Paraneuriotomy and evacuation of hematoma
Subepineurial
Epineuriotomy and evacuation hematoma
Intrafascicular
Epineuriotomy and interfascicular neurolysis
Multicompartmental
Combination of the above or in severe cases, resection of the affected nerve segment with reconstruction
being eccentric (Figure 3, Case 2) and the other being interfascicular (Figure 4, Case 3); and 1, multicompartmental hematoma (Figure 5, Case 4). We did not encounter any cases of intrafascicular hematomas but have reproduced an image by Wolfrum et al.8 (Figure 6) to illustrate their appearance. Three of the 4 cases presented with a history of trauma, and none had evidence of deranged clotting. Compressive neuropathy was relieved in all 4 cases with surgical decompression of the nerve and evacuation of the hematoma. The multicompartmental hematoma required sural nerve grafting for tension-free apposition of nonhemorrhagic nerve segments. All but 1 patient achieved
Figure 2. Case 1. A 40-year-old man tore his hamstring tendon after falling on an outstretched leg. This was associated with neuropathic pain that radiated down his leg. Axial T2-weighted image of the left leg with fat saturation (A) shows circumferential hematoma (arrows) around the peroneal division (P) of the sciatic nerve; there appears to be an increased signal intensity on the dependent side of the nerve. Coronal T2-weighted image with fat saturation (B) shows hematoma tracking along the course of the common peroneal nerve (arrows) toward the sciatic bifurcation. There was extensive scarring of the nerve noted intraoperatively with some blood collecting around the surface of the nerve. The nerve was decompressed with careful circumferential dissection of scar tissue. Tendon repair was also performed, and the patient experienced complete resolution of neuropathic pain. Ant, anterior; Inf, inferior; Lat, lateral; Post, posterior; Med, medial; Sup, superior; T, tibial nerve.
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ORIGINAL ARTICLE GODARD C. W. DE RUITER ET AL.
CLASSIFICATION OF INTRANEURAL HEMATOMA
Figure 3. Case 2. A 15-year-old man was struck by an automobile while riding a moped. The patient sustained a left femoral shaft fracture that was reduced and fixed with an intramedullary nail. Shortly thereafter he developed a complete left footdrop with electromyography evidence of a sciatic neuropathy. The patient underwent surgical exploration due to persistent peroneal neuropathy at 3 months postoperative. Intraoperative images show a subepineurial hematoma in the sciatic nerve. The patient is in the prone position. Rostral is to the left, caudal is to the right. Hemorrhagic aspect of the nerve (A) was opened up to reveal dark “crank-case oil”elike fluid (B).The epineurium is held up with forceps (C). The dissector points at a bone spicule that had pierced the nerve (D). Postoperatively, the patient was pain free. The weakness of the peroneal nerveeinnervated muscles was initially unchanged but recovered slowly in time to normal strength 8 months after the surgery.
complete resolution of symptoms in the postoperative period (Case 4 required nerve reconstruction). Literature Review There were 17 previously reported cases of intraneural hematoma (Table 2). Five were classified as subparaneurial; 6, subepineurial; 5, intrafascicular; and 1 could not be subcategorized on the basis of information provided. The most commonly affected nerve was the median nerve in 10 cases. Six patients had a coagulopathy; of these, 4 were associated with intrafascicular hemorrhage. Three patients were on anticoagulant or antiplatelet agents at the time of presentation. Two reports were supported with magnetic resonance imaging, 1 with a subparaneurial pattern and 1 with a subepineurial pattern. DISCUSSION On the basis of our experience and review of the literature (see Table 2), we feel that the anatomic classification of these lesions is justified (Figure 7). The exact mechanism by which compressive neuropathy causes neurologic deficit is not fully understood but involves axonal demyelination, edema of the nerve, and obstruction of blood supply and drainage.23 As the connective tissue layers of the nerve vary in their composition and compliance, it stands to reason that the localization of the
WORLD NEUROSURGERY 84 [6]: 1977-1984, DECEMBER 2015
lesion can influence the presentation, imaging findings, and surgical management. Implications of the Anatomic Framework Mechanism of Hematoma Formation. According to our anatomic framework we identified that traumatic injury to the nerve was most associated with subparaneurial and subepineurial hematomas (7 of 8 cases). Our fourth case (a gunshot injury to the knee with multicompartmental hematoma of the peroneal nerve) shows that damage to the nerve might be more severe than one would suspect macroscopically. In this case the continuity of the nerve during surgery seemed intact, but after opening of the epineurium the fascicles turned out to be completely lacerated (Figure 5C). A similar case has been presented previously.24 The explanation for the seemingly intact neural continuity is that this type of injury (grade 4 Sunderland) is not caused by direct transection (e.g., as in knife injury) but by distribution of energy (as in Case 4) to the peroneal nerve after direct impact of the bullet on the fibular bone, causing a multifragmented bone fracture. We acknowledge that neuropathy may also result from direct injury to the nerve, for example puncture22,25 or compression injury.12,13 Another mechanism of hematoma formation that has been reported in the literature (and was observed in case 1) is stretch injury to the nerve.11 We believe that the extensive scarring
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ORIGINAL ARTICLE GODARD C. W. DE RUITER ET AL.
CLASSIFICATION OF INTRANEURAL HEMATOMA
Figure 4. Case 3. A 34-year-old woman developed a lesion in the left forearm after she had given birth to twins. Midway through her pregnancy she first noted numbness on the dorsum of her left hand in the area supplied by the superficial branch of the radial nerve. After the delivery she noticed a small swelling on the radial site of her left forearm. She experienced dysesthesias radiating from the site of the swelling to the area of the numbness in her left hand. Ultrasonography revealed an anechoic cystic structure in the radial superficial nerve. Upon dissection an interfascicular hematoma in the superficial branch of the radial nerve (A) was noted. After opening of the epineurium, the clot is clearly visible between the fascicles of the nerve (B). (The patient was in supine position; rostral to the right, caudal to the left). Microscopic image of section stained with hematoxylin and eosin (C) was suggestive of an organized hematoma. Microscopic image of section stained with Prussian blue (D) showed hemosiderin deposits. The patient had complete resolution of neuropathy at 6-week follow-up.
of the sciatic nerve in Case 1 may have been associated with subparaneurial hematoma; this is supported by experimental models.26 Intrafascicular hematoma is most prevalent in patients with deranged clotting function.8,9,15e17,21 Finally, intraneural hematoma may also occur spontaneously, causing onset of motor weakness or dysesthesia as in our third case and the case presented by Richardson et al.27; both of these cases were located in subepineurial compartments. Yet in these cases minor injury cannot be completely eliminated, and a coagulopathy should be ruled out by performing the appropriate hematologic investigations. Surgical Management. The first step in the management of these lesions is to identify the nerve affected and compartment in which the hematoma is contained. Possible reasons for the prevalence of intraneural hematoma in specific nerves may include proximity to bony structures and extent of “cushioning” by surrounding soft tissue. Lesions affecting nerves that travel through narrow osteofibrous tunnels (such as the median nerve at the carpal tunnel8,10,19,20) may be more vulnerable to changes in intraneural
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pressure and are therefore more likely to be symptomatic. We observed a relatively even distribution in the literature of intraneural hematomas in the different compartments of the nerve according to our classification. In the case of subparaneurial or subepineurial hematoma, we believe that the hematoma can best be removed through a paraneuriotomy or epineuriotomy, respectively. As illustrated by our first 3 cases, this evacuation may lead to complete relief of symptoms (Cases 1 and 3) and even recovery of nerve function (Case 2). In severe traumatic cases (such as Case 4), decompression and evacuation of the hematoma alone might not be sufficient to maximize neurologic recovery and nerve grafting might be necessary. We do not recommend ultrasoundguided aspiration, employed in 1 case18 due to the risk of iatrogenic nerve injury and the inability to visualize the full extent of the lesion. In the case of intrafascicular hematoma we advise external decompression of the nerve (e.g., opening of the transverse carpal ligament in the case of intraneural hematoma of the median nerve at the wrist).19,20 In severe cases, epineuriotomy can further relieve pressure with the nerve. Given that and the potential risk of neurologic deficit, as well as the association of
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2015.08.063
ORIGINAL ARTICLE GODARD C. W. DE RUITER ET AL.
CLASSIFICATION OF INTRANEURAL HEMATOMA
Figure 5. Case 4. A 37-year-old man presented to the emergency department after he had been shot in the right upper leg while in a sitting position with his knee flexed. The bullet had exited his right upper leg and again entered the right lower leg near the fibula. There was complete weakness of all his peroneal nerveeinnervated muscles (peronei, anterior tibialis, and extensor hallucis longus) of the right leg, and he had no sensation on the dorsum of the foot and the lateral aspect of the right lower leg. Plain radiograph demonstrated a round defect in the lateral side of the right femur and a comminuted fracture of the proximal fibula (A). Surgery was performed within 6 hours after the injury. During exploration the continuity of the peroneal nerve seemed intact, but stimulation proximal to the hemorrhagic nerve segment could not elicit dorsiflexion. The epineurium was opened (B), after which there was spontaneous release of hematoma (as in our first case) revealing fascicles with a lacerated, hemorrhagic appearance. Microscopic image of section stained with hematoxylin and eosin (H&E, 4 magnification) demonstrated subepineurial, interfascicular, and intrafascicular hematoma (C) (the disrupted nerve ends are lined). Microscopic image of section stained with H&E (10 magnification) demonstrated intrafascicular hematoma (D). As it was not possible to reconnect the nerve ends without tension, subsequently sural nerve cable grafts were used for reconstruction of the nerve defect. One year after the surgery his dorsiflexion function had partially recovered (strength tibialis anterior muscle MRC 3).
intrafascicular hematomas with coagulopathies, we do not advocate perineuriotomy for these lesions. The bleeding in these cases is often more diffuse, making it difficult to identify all of the affected fascicles.8,9,17
Figure 6. Intraoperative image of median nerve after epineurotomy showing intrafascicular hematomas in multiple fascicles. (obtained with permission from Wolfrum et al.8).
WORLD NEUROSURGERY 84 [6]: 1977-1984, DECEMBER 2015
Limitations of This Study. We acknowledge that surgical management is not necessary for all cases of intraneural hematoma. A meaningful comparison between surgical and conservative management cannot be made due to the rarity of this condition and the bias toward reporting surgically treated cases. The entity probably occurs more frequently than is reported in the literature (as can be concluded from the relatively high incidence of accidental nerve punctures for local nerve blocks.28,29 We are aware that magnetic resonance imaging was not available in most cases (1 of our own and only 2 in the literature), making it difficult to accurately classify lesions. Even when imaging was available, localization of the lesion was not always straightforward, as evidenced by a previous report that was reclassified according to our new framework.12 Lastly, it is difficult to make comparisons about
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ORIGINAL ARTICLE GODARD C. W. DE RUITER ET AL.
CLASSIFICATION OF INTRANEURAL HEMATOMA
Table 2. Literature Review on Intraneural Hematoma Study
Affected Nerve
Age/ Sex
Localization*
Bigelow, 19529
Femoral
80/M Intrafascicular, multiple fascicles
Hayden, 196410
Median
70/F
Nobel, 196611
Peroneal, 2 16/F cases 42/F
Proposed Mechanism of Trauma
Hematologic Disorder or Anticoagulation
Surgical Treatment
Thrombocytopenia in reaction to penicillin
Subparaneurial
Opening of the paraneurium and evacuation hematoma
Subparaneurial, both Stretch injury due to ankle sprain cases
Opening of the paraneurium and evacuation hematoma
Polis, 197712 Median
23/M Subepineurial
Compression of forearm by case of potatoes for 30 min
Epineuriotomy and evacuation hematoma
Richardson, Sciatic 197813
57/M Subepineurial
Fall on buttocks
Epineuriotomy and evacuation hematoma
Cordingley, 198414
Ulnar
McLeod, 198415,*
Sciatic
Moneim, 198416
Median, 2 20/M Intrafascicular cases
Hemophilia
One case epineuriotomy and interfascicular neurolysis
Poppi, 199117
Ulnar
34/M Intrafascicular, multiple fascicles
Thrombocytopenia in patient with AIDS
Epineuriotomy and fascicular biopsy
Chuang, 200218
Median
73/M Subparaneurial
Warfarin and aspirin
Sonographic guided needle aspiration
Mandal, 200419
Median
71/M No distinctiony
Multiple myeloma
Opening transverse carpal ligament only
Wolfrum, 20078
Median
66/M Intrafascicular, multiple fascicles
Phenprocoumon
Epineuriotomy and interfascicular neurolysis
Kheirelseid, Median 200820
9/M
Subepineurial
Hemophilia
—
Intrafascicular
Acute leukemia
63/F
Subepineurial
Epineuriotomy and evacuation hematoma
Distal radius fracture (12 weeks before Normal bleeding profile onset of symptoms)
Opening transverse carpal ligament only Epineuriotomy and evacuation hematoma
Kokkinakis, 200921
Median
71/M Interfascicular
Spontaneous
Spinner, 201222
Median
54/F
Venepuncture
Epineuriotomy and evacuation hematoma
Spontaneous
Epineuriotomy and evacuation of hematoma
Richardson, Sural 201527
Subparaneurial
57/M Subepineurial
Low dose of aspirin
Localization was obtained from case description and/or images provided in these articles. *Demographic information not provided. yInsufficient data provided.
outcomes given the variability in the detail with which they are reported. Despite these limitations we believe that our anatomic framework provides a useful foundation to guide future research and raise awareness about these rare lesions.
Although it may not always be necessary to operate on intraneural hematoma, our framework enables surgical planning. In the future, with improvement of radiologic techniques, intraneural hematomas may be more frequently visualized and better distinction between the different subtypes might be possible.
CONCLUSIONS We apply a novel classification for intraneural hematomas illustrated by 4 cases of our own and a review of the literature.
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ACKNOWLEDGEMENT The authors thank Mrs. M. Kunen for her wonderful illustrations.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2015.08.063
ORIGINAL ARTICLE GODARD C. W. DE RUITER ET AL.
CLASSIFICATION OF INTRANEURAL HEMATOMA
Figure 7. Classification of intraneural hematomas based on our 4 cases and a review of the literature.
REFERENCES 1. Ahmed K, Yavari A, Walker DM, Buchanan JA. Haematoma of the hand as a complication of thrombolysis for myocardial infarction. J Hand Surg Eur Vol. 2007;32:720e721.
2. Brantigan JW, Owens ML, Moody FG. Femoral neuropathy complicating anticoagulant therapy. Am J Surg. 1976;132:108e109.
thrombosis: to stop or not to stop (the anticoagulation)? BMJ Case Rep. 2015;6:2015.
3. Fernandes C, Pereira P, Rodrigues M. Spontaneous iliopsoas muscle haematoma as a complication of anticoagulation in acute cerebral venous
4. Jamjoom ZA, al-Bakry A, al-Momen A, Malabary T, Tahan AR, Yacub B. Bilateral femoral nerve compression by iliacus hematomas
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complicating anticoagulant therapy. Surg Today. 1993;23:535e540. 5. Mastroianni PP, Roberts MP. Femoral neuropathy and retroperitoneal hemorrhage. Neurosurgery. 1983;13:44e47.
CLASSIFICATION OF INTRANEURAL HEMATOMA
14. Cordingley F, Crawford G. Ulnar nerve palsy in a haemophiliac due to intraneural haemorrhage. BMJ. 1984;289:18e19. 15. McLeod J, Walsh J. Peripheral neuropathy associated with lymphomas and other reticuloses. Peripheral Neuropathy. 1975;2:2192e2203.
6. Reina MA, Sala-Blanch X, Arriazu R, Machés F. Microscopic Morphology and Ultrastructure of Human Peripheral Nerves. San Diego, CA: Elsevier; 2015.
16. Moneim MS, Gribble TJ. Carpal tunnel syndrome in hemophilia. J Hand Surg. 1984;9:580e583.
7. Ortiz-Hidalgo C, Weller R. Histology for Pathologists. Philadelphia, PA: Lippincott Williams & Wilkins; 2007.
17. Poppi M, Staffa G, Martinelli P, Fabrizi AP, Giuliani G. Neuropathy caused by spontaneous intraneural hemorrhage: case report. Neurosurgery. 1991;28:292e295.
8. Wolfrum F, Voellinger M, Rudolf K, Partecke B. [Neuropathy of the median nerve caused by intraneural haematoma after carpal tunnel release in an anticoagulated patient]. Hand Chir Mikrochir Plast Chir. 2007;39:427e429.
18. Chuang Y-M, Luo C-B, Chou Y-H, Cheng Y-C, Chang C-Y, Chiou H-J. Sonographic diagnosis and treatment of a median nerve epineural hematoma caused by brachial artery catheterization. J Ultrasound Med. 2002;21:705e708.
9. Bigelow NH, Graves RW. Peripheral-nerve lesions in hemorrhagic diseases. AMA Arch Neurol Psych. 1952;68:819e830.
19. Mandal A, Colville J, Jones M, Erdmann MW. An unusual case of haemorrhagic median neuropathy. Ann R Coll Surg Engl. 2004;86:258e259.
10. Hayden JW. Median neuropathy in the carpal tunnel caused by spontaneous intraneural hemorrhage. J Bone Joint Surg Am. 1964;46:1242e1244.
20. Kheirelseid E, Murphy M, Devitt A. Spontaneous subperineural haemorrhage causing acute carpal tunnel syndrome. J Hand Surg Eur. 2008;33:91e92.
11. Nobel W. Peroneal palsy due to hematoma in the common peroneal nerve sheath after distal torsional fractures and inversion ankle sprains. J Bone Joint Surg Am. 1966;48:1484e1495.
21. Kokkinakis M, Hinsche A, Rajeev A. Spontaneous intraneural haematoma causing acute neuropathy of the median nerve. J Hand Surg Eur. 2009;34:280e281.
12. Polis L, Brzezinski J. Posttraumatic hematoma beneath the epineurium of a branch of the median nerve. Case report. J Neurosurg. 1977;46:542e543.
22. Spinner RJ, Edwards WD, Amrami KK. Hemorrhagic cystic lesion of the median nerve: an unusual complication of venipuncture. Clin Anat. 2013;26:540e543.
13. Richardson RR, Hahn YS, Siqueira EB. Intraneural hematoma of the sciatic nerve. Case report. J Neurosurg. 1978;49:298e300.
23. Thawait SK, Wang K, Subhawong TK, et al. Peripheral nerve surgery: the role of high-resolution MR neurography. AJNR. 2012;33:203e210.
24. Oberlin C, Rantissi M. Gunshot injuries to the nerves. Chir Main. 2011;30:176e182. 25. Kanei Y, Kwan T, Nakra NC, et al. Transradial cardiac catheterization: a review of access site complications. Catheter Cardiovasc Interv. 2011;78: 840e846. 26. Scopel GP, Faria JCM, Busnardo FF, Alves H, Orpheu SC, Ferreira MC. Experimental intraneural hematoma model in rats: evaluation of functional recovery and neural histomorphometry. Acta Orthop Bras. 2007;15:222e226. 27. Richardson SS, McLawhorn AS, Mintz DN, DiCarlo EF, Weiland AJ. Spontaneous intraneural hematoma of the sural nerve. Skeletal Radiol. 2015; 44:605e608. 28. Jeng C, Rosenblatt M. Intraneural injections and regional anesthesia: the known and the unknown. Minerva Anesthesiol. 2011;77:54e58. 29. Moore AE, Stringer MD. Iatrogenic femoral nerve injury: a systematic review. Surg Radiol Anat. 2011; 33:649e658.
Conflict of interest statement: The authors have no conflicts of interest to declare. Received 25 June 2015; accepted 27 August 2015 Citation: World Neurosurg. (2015) 84, 6:1977-1984. http://dx.doi.org/10.1016/j.wneu.2015.08.063 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com
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1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2015.08.063
Intraneural Hematoma: A Proposed Anatomic Classification with Potential Treatment Implications Godard C. W. de Ruiter1, Nikhil K. Prasad2, Robert J. Spinner2, Allen H. Maniker3
Intraneural hematoma is a rare entity with fewer than 20 cases reported in the literature. There is no consensus on surgical treatment due to its rarity. We present a novel classification for intraneural hematomas based on a review of the literature and illustrated by 4 cases that were treated in our 3 centers. This classification system localizes the hematoma to the different connective tissue layers that compose the nerve: the paraneurium, epineurium, and perineurium. We believe that this classification has consequences for surgical treatment and can form the foundation for future research into the natural history of these types of lesions.
and torsional forces. From outside to inside these layers are called the paraneurium, epineurium, perineurium, and endoneurium (Figure 1). The paraneurium (sometimes referred to as the mesoneurium) comprises thin films of adipose and connective tissue that surround the relatively thicker epineurium.6 The epineurium consists of 2 parts: 1) the dense extrafascicular (or outer) epineurium, which is made largely of collagen to contain and protect the nerve fascicles; and 2) the interfascicular (or inner) epineurium, which has more adipose and is similar in consistency to the paraneurium.6 The perineurium, which forms the blood-nerve barrier, is a dense multilaminar sheath composed of alternating mesothelial cell and collagen layers surrounding individual fascicles.7 Finally, the endoneurium (also called the basal lamina tube) is the layer through which the individual axon runs. MATERIALS AND METHODS
INTRODUCTION
T
he extrinsic compression of peripheral nerves due to a collection of blood (extraneural hematoma) within osteofibrous tunnels or intermuscular compartments is well recognized.1e5 Occasionally hematomas may form within the nerve (intraneural hematoma) as a consequence of trauma or spontaneously due to a derangement in the patient’s clotting function. Although these lesions may resorb spontaneously, many surgeons opt for timely decompression to prevent irreversible damage to the nerve. Case reports of this condition have been sporadic, and no consensus exists on the best surgical management. We introduce a novel anatomic classification system for intraneural hematomas to guide surgical planning on the basis of a thorough review of the literature and 4 cases from our own experience. ANATOMIC FRAMEWORK Peripheral nerves are composed of connective tissue layers that isolate and protect individual nerve fascicles from compressive
All cases of intraneural hematoma encountered in the past 5 years at our 3 centers were reviewed. The hematomas were classified according to the connective tissue layers mentioned earlier: subparaneurial, subepineurial, and intrafascicular. We chose the term intrafascicular instead of subperineurial because of potential confusion with the subparaneurial layer. Hematoma that occupied several different layers was classified as multicompartmental. LITERATURE REVIEW A thorough review of 3 databases—PubMed, Medline, and Google Scholar—was performed, using the search terms “intraneural,” “epineural,” “intrafascicular,” “hematoma,” and “peripheral nerve.” Results obtained after this first pass were cross referenced to obtain missing data. The details of each case report were reviewed looking for demographic information, affected nerve, mechanism of injury, associated coagulopathy/anticoagulant use, and surgical management. Each case was then classified according
To whom correspondence should be addressed: Godard C. W. de Ruiter, M.D. Ph.D. [E-mail: [email protected]]
Key words Hematoma - Interfascicular - Intrafascicular - Subepineurial - Subparaneurial -
Citation: World Neurosurg. (2015) 84, 6:1977-1984. http://dx.doi.org/10.1016/j.wneu.2015.08.063 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1
From the Departments of Neurosurgery, Medical Center Haaglanden, The Hague, The Netherlands; 2Neurosurgery, Mayo Clinic Rochester, Minnesota, USA; 3Neurosurgery, Mount Sinai Beth Israel Medical Center, New York, New York, USA
WORLD NEUROSURGERY 84 [6]: 1977-1984, DECEMBER 2015
1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
www.WORLDNEUROSURGERY.org
1977
ORIGINAL ARTICLE GODARD C. W. DE RUITER ET AL.
CLASSIFICATION OF INTRANEURAL HEMATOMA
Table 1. Four Cases of Intraneural Hematoma Type of Intraneural Hematoma Based on Location in the Nerve
Figure 1. Normal anatomy of the peripheral nerve illustrating the different layers, from outside to inside: paraneurium, epineurium, perineurium, and endoneurium.
to the anatomic framework, using descriptions provided and imaging (when available). RESULTS Cases Illustrations We identified 4 cases of intraneural hematoma and classified them according to the anatomic framework (Table 1): 1 subparaneurial hematoma (Figure 2, Case 1); 2 subepineurial hematomas, 1
Surgical Treatment
Subparaneurial
Paraneuriotomy and evacuation of hematoma
Subepineurial
Epineuriotomy and evacuation hematoma
Intrafascicular
Epineuriotomy and interfascicular neurolysis
Multicompartmental
Combination of the above or in severe cases, resection of the affected nerve segment with reconstruction
being eccentric (Figure 3, Case 2) and the other being interfascicular (Figure 4, Case 3); and 1, multicompartmental hematoma (Figure 5, Case 4). We did not encounter any cases of intrafascicular hematomas but have reproduced an image by Wolfrum et al.8 (Figure 6) to illustrate their appearance. Three of the 4 cases presented with a history of trauma, and none had evidence of deranged clotting. Compressive neuropathy was relieved in all 4 cases with surgical decompression of the nerve and evacuation of the hematoma. The multicompartmental hematoma required sural nerve grafting for tension-free apposition of nonhemorrhagic nerve segments. All but 1 patient achieved
Figure 2. Case 1. A 40-year-old man tore his hamstring tendon after falling on an outstretched leg. This was associated with neuropathic pain that radiated down his leg. Axial T2-weighted image of the left leg with fat saturation (A) shows circumferential hematoma (arrows) around the peroneal division (P) of the sciatic nerve; there appears to be an increased signal intensity on the dependent side of the nerve. Coronal T2-weighted image with fat saturation (B) shows hematoma tracking along the course of the common peroneal nerve (arrows) toward the sciatic bifurcation. There was extensive scarring of the nerve noted intraoperatively with some blood collecting around the surface of the nerve. The nerve was decompressed with careful circumferential dissection of scar tissue. Tendon repair was also performed, and the patient experienced complete resolution of neuropathic pain. Ant, anterior; Inf, inferior; Lat, lateral; Post, posterior; Med, medial; Sup, superior; T, tibial nerve.
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ORIGINAL ARTICLE GODARD C. W. DE RUITER ET AL.
CLASSIFICATION OF INTRANEURAL HEMATOMA
Figure 3. Case 2. A 15-year-old man was struck by an automobile while riding a moped. The patient sustained a left femoral shaft fracture that was reduced and fixed with an intramedullary nail. Shortly thereafter he developed a complete left footdrop with electromyography evidence of a sciatic neuropathy. The patient underwent surgical exploration due to persistent peroneal neuropathy at 3 months postoperative. Intraoperative images show a subepineurial hematoma in the sciatic nerve. The patient is in the prone position. Rostral is to the left, caudal is to the right. Hemorrhagic aspect of the nerve (A) was opened up to reveal dark “crank-case oil”elike fluid (B).The epineurium is held up with forceps (C). The dissector points at a bone spicule that had pierced the nerve (D). Postoperatively, the patient was pain free. The weakness of the peroneal nerveeinnervated muscles was initially unchanged but recovered slowly in time to normal strength 8 months after the surgery.
complete resolution of symptoms in the postoperative period (Case 4 required nerve reconstruction). Literature Review There were 17 previously reported cases of intraneural hematoma (Table 2). Five were classified as subparaneurial; 6, subepineurial; 5, intrafascicular; and 1 could not be subcategorized on the basis of information provided. The most commonly affected nerve was the median nerve in 10 cases. Six patients had a coagulopathy; of these, 4 were associated with intrafascicular hemorrhage. Three patients were on anticoagulant or antiplatelet agents at the time of presentation. Two reports were supported with magnetic resonance imaging, 1 with a subparaneurial pattern and 1 with a subepineurial pattern. DISCUSSION On the basis of our experience and review of the literature (see Table 2), we feel that the anatomic classification of these lesions is justified (Figure 7). The exact mechanism by which compressive neuropathy causes neurologic deficit is not fully understood but involves axonal demyelination, edema of the nerve, and obstruction of blood supply and drainage.23 As the connective tissue layers of the nerve vary in their composition and compliance, it stands to reason that the localization of the
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lesion can influence the presentation, imaging findings, and surgical management. Implications of the Anatomic Framework Mechanism of Hematoma Formation. According to our anatomic framework we identified that traumatic injury to the nerve was most associated with subparaneurial and subepineurial hematomas (7 of 8 cases). Our fourth case (a gunshot injury to the knee with multicompartmental hematoma of the peroneal nerve) shows that damage to the nerve might be more severe than one would suspect macroscopically. In this case the continuity of the nerve during surgery seemed intact, but after opening of the epineurium the fascicles turned out to be completely lacerated (Figure 5C). A similar case has been presented previously.24 The explanation for the seemingly intact neural continuity is that this type of injury (grade 4 Sunderland) is not caused by direct transection (e.g., as in knife injury) but by distribution of energy (as in Case 4) to the peroneal nerve after direct impact of the bullet on the fibular bone, causing a multifragmented bone fracture. We acknowledge that neuropathy may also result from direct injury to the nerve, for example puncture22,25 or compression injury.12,13 Another mechanism of hematoma formation that has been reported in the literature (and was observed in case 1) is stretch injury to the nerve.11 We believe that the extensive scarring
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ORIGINAL ARTICLE GODARD C. W. DE RUITER ET AL.
CLASSIFICATION OF INTRANEURAL HEMATOMA
Figure 4. Case 3. A 34-year-old woman developed a lesion in the left forearm after she had given birth to twins. Midway through her pregnancy she first noted numbness on the dorsum of her left hand in the area supplied by the superficial branch of the radial nerve. After the delivery she noticed a small swelling on the radial site of her left forearm. She experienced dysesthesias radiating from the site of the swelling to the area of the numbness in her left hand. Ultrasonography revealed an anechoic cystic structure in the radial superficial nerve. Upon dissection an interfascicular hematoma in the superficial branch of the radial nerve (A) was noted. After opening of the epineurium, the clot is clearly visible between the fascicles of the nerve (B). (The patient was in supine position; rostral to the right, caudal to the left). Microscopic image of section stained with hematoxylin and eosin (C) was suggestive of an organized hematoma. Microscopic image of section stained with Prussian blue (D) showed hemosiderin deposits. The patient had complete resolution of neuropathy at 6-week follow-up.
of the sciatic nerve in Case 1 may have been associated with subparaneurial hematoma; this is supported by experimental models.26 Intrafascicular hematoma is most prevalent in patients with deranged clotting function.8,9,15e17,21 Finally, intraneural hematoma may also occur spontaneously, causing onset of motor weakness or dysesthesia as in our third case and the case presented by Richardson et al.27; both of these cases were located in subepineurial compartments. Yet in these cases minor injury cannot be completely eliminated, and a coagulopathy should be ruled out by performing the appropriate hematologic investigations. Surgical Management. The first step in the management of these lesions is to identify the nerve affected and compartment in which the hematoma is contained. Possible reasons for the prevalence of intraneural hematoma in specific nerves may include proximity to bony structures and extent of “cushioning” by surrounding soft tissue. Lesions affecting nerves that travel through narrow osteofibrous tunnels (such as the median nerve at the carpal tunnel8,10,19,20) may be more vulnerable to changes in intraneural
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pressure and are therefore more likely to be symptomatic. We observed a relatively even distribution in the literature of intraneural hematomas in the different compartments of the nerve according to our classification. In the case of subparaneurial or subepineurial hematoma, we believe that the hematoma can best be removed through a paraneuriotomy or epineuriotomy, respectively. As illustrated by our first 3 cases, this evacuation may lead to complete relief of symptoms (Cases 1 and 3) and even recovery of nerve function (Case 2). In severe traumatic cases (such as Case 4), decompression and evacuation of the hematoma alone might not be sufficient to maximize neurologic recovery and nerve grafting might be necessary. We do not recommend ultrasoundguided aspiration, employed in 1 case18 due to the risk of iatrogenic nerve injury and the inability to visualize the full extent of the lesion. In the case of intrafascicular hematoma we advise external decompression of the nerve (e.g., opening of the transverse carpal ligament in the case of intraneural hematoma of the median nerve at the wrist).19,20 In severe cases, epineuriotomy can further relieve pressure with the nerve. Given that and the potential risk of neurologic deficit, as well as the association of
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ORIGINAL ARTICLE GODARD C. W. DE RUITER ET AL.
CLASSIFICATION OF INTRANEURAL HEMATOMA
Figure 5. Case 4. A 37-year-old man presented to the emergency department after he had been shot in the right upper leg while in a sitting position with his knee flexed. The bullet had exited his right upper leg and again entered the right lower leg near the fibula. There was complete weakness of all his peroneal nerveeinnervated muscles (peronei, anterior tibialis, and extensor hallucis longus) of the right leg, and he had no sensation on the dorsum of the foot and the lateral aspect of the right lower leg. Plain radiograph demonstrated a round defect in the lateral side of the right femur and a comminuted fracture of the proximal fibula (A). Surgery was performed within 6 hours after the injury. During exploration the continuity of the peroneal nerve seemed intact, but stimulation proximal to the hemorrhagic nerve segment could not elicit dorsiflexion. The epineurium was opened (B), after which there was spontaneous release of hematoma (as in our first case) revealing fascicles with a lacerated, hemorrhagic appearance. Microscopic image of section stained with hematoxylin and eosin (H&E, 4 magnification) demonstrated subepineurial, interfascicular, and intrafascicular hematoma (C) (the disrupted nerve ends are lined). Microscopic image of section stained with H&E (10 magnification) demonstrated intrafascicular hematoma (D). As it was not possible to reconnect the nerve ends without tension, subsequently sural nerve cable grafts were used for reconstruction of the nerve defect. One year after the surgery his dorsiflexion function had partially recovered (strength tibialis anterior muscle MRC 3).
intrafascicular hematomas with coagulopathies, we do not advocate perineuriotomy for these lesions. The bleeding in these cases is often more diffuse, making it difficult to identify all of the affected fascicles.8,9,17
Figure 6. Intraoperative image of median nerve after epineurotomy showing intrafascicular hematomas in multiple fascicles. (obtained with permission from Wolfrum et al.8).
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Limitations of This Study. We acknowledge that surgical management is not necessary for all cases of intraneural hematoma. A meaningful comparison between surgical and conservative management cannot be made due to the rarity of this condition and the bias toward reporting surgically treated cases. The entity probably occurs more frequently than is reported in the literature (as can be concluded from the relatively high incidence of accidental nerve punctures for local nerve blocks.28,29 We are aware that magnetic resonance imaging was not available in most cases (1 of our own and only 2 in the literature), making it difficult to accurately classify lesions. Even when imaging was available, localization of the lesion was not always straightforward, as evidenced by a previous report that was reclassified according to our new framework.12 Lastly, it is difficult to make comparisons about
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CLASSIFICATION OF INTRANEURAL HEMATOMA
Table 2. Literature Review on Intraneural Hematoma Study
Affected Nerve
Age/ Sex
Localization*
Bigelow, 19529
Femoral
80/M Intrafascicular, multiple fascicles
Hayden, 196410
Median
70/F
Nobel, 196611
Peroneal, 2 16/F cases 42/F
Proposed Mechanism of Trauma
Hematologic Disorder or Anticoagulation
Surgical Treatment
Thrombocytopenia in reaction to penicillin
Subparaneurial
Opening of the paraneurium and evacuation hematoma
Subparaneurial, both Stretch injury due to ankle sprain cases
Opening of the paraneurium and evacuation hematoma
Polis, 197712 Median
23/M Subepineurial
Compression of forearm by case of potatoes for 30 min
Epineuriotomy and evacuation hematoma
Richardson, Sciatic 197813
57/M Subepineurial
Fall on buttocks
Epineuriotomy and evacuation hematoma
Cordingley, 198414
Ulnar
McLeod, 198415,*
Sciatic
Moneim, 198416
Median, 2 20/M Intrafascicular cases
Hemophilia
One case epineuriotomy and interfascicular neurolysis
Poppi, 199117
Ulnar
34/M Intrafascicular, multiple fascicles
Thrombocytopenia in patient with AIDS
Epineuriotomy and fascicular biopsy
Chuang, 200218
Median
73/M Subparaneurial
Warfarin and aspirin
Sonographic guided needle aspiration
Mandal, 200419
Median
71/M No distinctiony
Multiple myeloma
Opening transverse carpal ligament only
Wolfrum, 20078
Median
66/M Intrafascicular, multiple fascicles
Phenprocoumon
Epineuriotomy and interfascicular neurolysis
Kheirelseid, Median 200820
9/M
Subepineurial
Hemophilia
—
Intrafascicular
Acute leukemia
63/F
Subepineurial
Epineuriotomy and evacuation hematoma
Distal radius fracture (12 weeks before Normal bleeding profile onset of symptoms)
Opening transverse carpal ligament only Epineuriotomy and evacuation hematoma
Kokkinakis, 200921
Median
71/M Interfascicular
Spontaneous
Spinner, 201222
Median
54/F
Venepuncture
Epineuriotomy and evacuation hematoma
Spontaneous
Epineuriotomy and evacuation of hematoma
Richardson, Sural 201527
Subparaneurial
57/M Subepineurial
Low dose of aspirin
Localization was obtained from case description and/or images provided in these articles. *Demographic information not provided. yInsufficient data provided.
outcomes given the variability in the detail with which they are reported. Despite these limitations we believe that our anatomic framework provides a useful foundation to guide future research and raise awareness about these rare lesions.
Although it may not always be necessary to operate on intraneural hematoma, our framework enables surgical planning. In the future, with improvement of radiologic techniques, intraneural hematomas may be more frequently visualized and better distinction between the different subtypes might be possible.
CONCLUSIONS We apply a novel classification for intraneural hematomas illustrated by 4 cases of our own and a review of the literature.
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ACKNOWLEDGEMENT The authors thank Mrs. M. Kunen for her wonderful illustrations.
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ORIGINAL ARTICLE GODARD C. W. DE RUITER ET AL.
CLASSIFICATION OF INTRANEURAL HEMATOMA
Figure 7. Classification of intraneural hematomas based on our 4 cases and a review of the literature.
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14. Cordingley F, Crawford G. Ulnar nerve palsy in a haemophiliac due to intraneural haemorrhage. BMJ. 1984;289:18e19. 15. McLeod J, Walsh J. Peripheral neuropathy associated with lymphomas and other reticuloses. Peripheral Neuropathy. 1975;2:2192e2203.
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18. Chuang Y-M, Luo C-B, Chou Y-H, Cheng Y-C, Chang C-Y, Chiou H-J. Sonographic diagnosis and treatment of a median nerve epineural hematoma caused by brachial artery catheterization. J Ultrasound Med. 2002;21:705e708.
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19. Mandal A, Colville J, Jones M, Erdmann MW. An unusual case of haemorrhagic median neuropathy. Ann R Coll Surg Engl. 2004;86:258e259.
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20. Kheirelseid E, Murphy M, Devitt A. Spontaneous subperineural haemorrhage causing acute carpal tunnel syndrome. J Hand Surg Eur. 2008;33:91e92.
11. Nobel W. Peroneal palsy due to hematoma in the common peroneal nerve sheath after distal torsional fractures and inversion ankle sprains. J Bone Joint Surg Am. 1966;48:1484e1495.
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22. Spinner RJ, Edwards WD, Amrami KK. Hemorrhagic cystic lesion of the median nerve: an unusual complication of venipuncture. Clin Anat. 2013;26:540e543.
13. Richardson RR, Hahn YS, Siqueira EB. Intraneural hematoma of the sciatic nerve. Case report. J Neurosurg. 1978;49:298e300.
23. Thawait SK, Wang K, Subhawong TK, et al. Peripheral nerve surgery: the role of high-resolution MR neurography. AJNR. 2012;33:203e210.
24. Oberlin C, Rantissi M. Gunshot injuries to the nerves. Chir Main. 2011;30:176e182. 25. Kanei Y, Kwan T, Nakra NC, et al. Transradial cardiac catheterization: a review of access site complications. Catheter Cardiovasc Interv. 2011;78: 840e846. 26. Scopel GP, Faria JCM, Busnardo FF, Alves H, Orpheu SC, Ferreira MC. Experimental intraneural hematoma model in rats: evaluation of functional recovery and neural histomorphometry. Acta Orthop Bras. 2007;15:222e226. 27. Richardson SS, McLawhorn AS, Mintz DN, DiCarlo EF, Weiland AJ. Spontaneous intraneural hematoma of the sural nerve. Skeletal Radiol. 2015; 44:605e608. 28. Jeng C, Rosenblatt M. Intraneural injections and regional anesthesia: the known and the unknown. Minerva Anesthesiol. 2011;77:54e58. 29. Moore AE, Stringer MD. Iatrogenic femoral nerve injury: a systematic review. Surg Radiol Anat. 2011; 33:649e658.
Conflict of interest statement: The authors have no conflicts of interest to declare. Received 25 June 2015; accepted 27 August 2015 Citation: World Neurosurg. (2015) 84, 6:1977-1984. http://dx.doi.org/10.1016/j.wneu.2015.08.063 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com
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1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.
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