Magnetic resonance imaging evidence for perineural spread of endometriosis to the lumbosacral plexus: report of 2 cases

We propose that perineural spread from the organ to the LSP , demonstrated in pelvic cancer1,11,22 including cer- vical cancer,25 applies to EM as well and represents an alternate mechanism in selected cases. The possibility of EM tracking along the nerves as a form of spread was de- scribed by Possover et al.;37 however, such an anatomical, mechanistic explanation as the one described in the pres- ent report has not yet been postulated. We provide compel- ling evidence by presenting our 2 cases and the previously published case18 that showed signs of perineural spread. We hypothesize that endometrial glands and stroma in- filtrate the uterine plexus, part of the inferior hypogastric plexus (IHP). From the IHP , EM continues to grow toward the sacral plexus along the sacral and pelvic splanchnic nerves and toward the lumbar plexus along the hypogastric nerves (Fig. 6). Within the plexus, EM can spread proxi- mally to the spinal nerves (Figs. 1C and D and 5C and D) or distally to the arborizing nerves. We were surprised by the presence of EM in the pelvic muscles (Figs. 2D and E and 4A and B) and pelvic bone (Fig. 4A and B) in a pat - tern similar to that which has been described for perineu- FIg. 2. Case 1. 2013 MRI. An axial spoiled gradient recall (SPGR) Gd-enhanced image (A) demonstrates an area of enhancing  abnormality (dashed arrow) extending from the body of the uterus to the left LSP and left sciatic nerve, which is markedly enlarged  and appears to be infiltrated by the abnormality (arrowhead) . The gluteal musculature is atrophic (asterisks) . A coronal oblique  T2-weighted image (b) shows increased signal of the L-4 and L-5 spinal nerves (arrowheads)  proximal to an area of spiculated hy - perintense soft-tissue mass (arrow) . Increased signal on a T2-weighted image (C) is also demonstrated by the left S-1 spinal nerve  (arrowhead). A coronal oblique SPGR image ( d) demonstrates enhancing lesion with center area of decreased signal in the upper  portion of the left obturator internus muscle (arrowhead)  and an abnormally enhancing and heterogeneous left uterosacral liga - ment, possibly representing extension of endometrial tissue from the cervix to the inferior hypogastric plexus (dashed arrow) . The  same lesions were hyperintense on a T2-weighted coronal image ( e: arrowhead and dashed arrow), the central area presumably  representing hemosiderin collection. A CT-navigated biopsy (F)  of the soft-tissue mass in close vicinity of the LSP was performed  and revealed endometriosis. Neurosurg Focus  Volume 39 • September 2015 3 Unauthenticated | Downloaded 06/11/26 03:40 AM UTC A. C. siquara de sousa et al. ral spread of malignant cancer to muscle 8 and bone.9 We theorize that these deposits could result from perineural spread of EM along the motor and bone branches from t h e L SP. How EM invades the uterine plexus is not clear. Up to 90% of women with EM 6 have adenomyosis, and deep ad- enomyotic nodules have been demonstrated to be closely associated with nerves. 5 We theorize that endometriotic cells and stroma can propagate from deep adenomyotic nodules along the fine uterine nerves toward the IHP in the uterosacral ligament (Fig. 2D and E) and then as de - scribed above. The perineural spread as a possible expla- nation is supported by reciprocal interactions between EM and nerves. 5,6,12,37 Not only does EM promote neurogen - esis,5 but in turn the nerves promote angiogenesis and EM growth.6,39 EM can be classified into several subtypes, of which deep infiltrating endometriosis (DIE) seems to be the most aggressive and most challenging to treat due to its invasive nature. 5 DIE is more painful than other forms of EM, which can be explained by its propensity to invade and extend along the pelvic nerves. 2–4 DIE can cause ure- teral or rectosigmoid strictures and sacral plexus entrap - ment requiring demanding reconstructive surgeries. 3,48 Intraneural invasion of major somatic nerves such as the sciatic or obturator nerve prevents complete resection. DIE can also be more challenging to diagnose as it may have no peritoneal manifestation at all 36 or may present only with peritoneal “pockets,”6 probably caused by sub- peritoneal scarring and retraction. Possover et al.37 were the first to propose a “neural hy- pothesis,” describing a major role of the pelvic nervous system in EM. To support the theory, they correlated common locations of DIE with major components of the pelvic sympathetic system. Although the parasympathetic system might be implicated as well, 27 other authors have observed a similar distribution of DIE.14,15,52 EM is heterogeneously hyperintense on T1-weighted MRI due to blood collections and hypointense from hemo- siderin depositions. On T2-weighted MRI, it has a similar heterogeneous appearance. Typical, but very nonspecific, is retraction of surrounding tissue due to scarring. The perineural spread can be visualized as an abnormality ex- tending from the uterus toward the LSP (Figs. 2A and 5A and B), which is hyperintense on T2-weighted MRI and avidly enhancing on post-Gd scans. The LSP and branch- ing nerves infiltrated with EM are enlarged, hyperintense FIg. 3. Case 1. Pathology.  A: A single benign-appearing gland is present with minimal underlying stroma. H & E, original magnifi - cation ×200.  b: The gland and scant underlying stroma are positive for estrogen receptors. Estrogen receptor immunohistochem - istry, original magnification × 200.  C: The stroma is also positive for CD10. Original magnification × 200. These staining patterns in  conjunction with the morphology support the diagnosis of endometriosis. Neurosurg Focus  Volume 39 • September 20154 Unauthenticated | Downloaded 06/11/26 03:40 AM UTC Perineural spread of endometriosis on T2-weighted MR images, and heterogeneously enhanc- ing on contrast-enhanced images. We understand that intraperitoneal seeding with sub - sequent nerve compression is the most probable explana- tion for most cases with neural symptoms. A review of the literature revealed several other cases of interest. These can be divided into 2 subgroups: 1) cases with nerve in - volvement and no peritoneal disease; and 2) cases with in- traneural (e.g., intrasciatic) EM with either unspecified or some peritoneal disease. Possover and Chiantera 36 report- ed 3 cases of sciatic nerve EM, one of which was intraneu- ral. None of these cases had any peritoneal disease. Pham et al.35 reported a case in a patient presenting with sciatic nerve weakness. At the time of presentation, the patient had no peritoneal disease, and on biopsy EM was found in the epineurium. Interestingly, gluteal and pelvic muscles demonstrated denervation, pointing to a more widespread process. Torkelson et al. 46 reported 2 cases, one of which had no peritoneal disease and intraneural EM of the sci - atic nerve. Ceccaroni et al.13 reported another case of sci- atic nerve EM and no peritoneal disease. Several authors, however, reported cases of intraneural sciatic nerve EM, which could be explained by perineural spread. 24,30,31,43,56 Waer et al.51 reported a case of EM with perineural spread along the obturator nerve. We wonder if cases of EM with nerve and bone or muscle involvement could be explained by perineural spread along the periosteal and muscle branches. Redwine and Sharpe 40 reported a case of obtu - rator nerve EM extending to the ilium. A case of sciatic nerve EM that spread to the femur was described by Oei et al.33 Also, the second case of sciatic nerve EM reported by Torkelson et al.46 had EM in the ischial tuberosity in a pat- tern that was reminiscent of that described in perineural spread of cancer and in Case 2. 9 In their series, Possover and Chiantera36 reported a case of sciatic nerve EM with extension to the obturator internus muscle—again, a simi- lar pattern to that seen in our case and to that described in perineural cancer spread.8 We further hypothesize that cases of conus medullaris EM could be explained as an extension of the same process intradurally along the sacral and lumbar nerve roots, 20,44 possibly with subsequent in- tradural seeding 19 as proposed in perineural spread of prostate cancer.10

We understand that our article has several limitations. It is based on 2 individual cases, and further research is needed to confirm perineural spread of EM as an alter - native explanation for sciatic nerve EM. We acknowledge that the theory of retrograde menstruation with intraperi- toneal seeding first proposed by Sampson7,41 is the likely explanation for most cases of sacral plexus EM. We pro- FIg. 4. Case 2. MRI. An axial T2-weighted MR image (A) demonstrates  heterogeneously increased signal in the enlarged right sciatic nerve (el - lipse). The obturator internus muscle is infiltrated with a heterogeneous  hyperintense soft-tissue mass with hemosiderin depositions (thin arrow) .  The muscle itself and the piriformis muscle (arrowheads)  show diffusely  increased signal suggestive of denervation. Another nodulus of similar  characteristics is observed in the right ischium (thick arrow) . The same  structures demonstrate prominent heterogeneous enhancement on  axial T1-weighted Gd-enhanced MR imaging ( b) (thin arrow: obturator  internus muscle; thick arrow : ischium; arrowheads: piriformis muscle;  ellipse: sciatic nerve). An axial T2-weighted image (C)  demonstrates a  massively enlarged and infiltrated right sciatic nerve at the sciatic notch  (arrowhead). An axial follow-up T1-weighted image ( d) obtained 6 years  later shows marked improvement of the sciatic nerve enlargement (ar - rowhead). FIg. 5. Outside case. MRI. An axial T1-weighted Gd-enhanced image  (A) demonstrates an enhancing abnormality extending from the cervix  (asterisk) to the sciatic notch and the sciatic nerve (dashed arrow) . A  coronal T2-weighted fat-saturated image ( b) demonstrates the same  hyperintense and heterogeneous abnormality (dashed arrow)  extending  from the cervix (asterisk) . Coronal fat-saturated fast spin echo images  (C and d) from an MRI examination performed 3 years later show the  hyperintense and enlarged right S-1 and L-4 spinal nerves demonstrat - ing signs of perineural spread (C, dashed arrow, the S-1 spinal nerve; D,  dashed arrow, the L-4 spinal nerve). Neurosurg Focus  Volume 39 • September 2015 5 Unauthenticated | Downloaded 06/11/26 03:40 AM UTC A. C. siquara de sousa et al. vide a secondary explanation applicable to selected cas - es supported by compelling evidence based on imaging studies and review of the literature. Vercellini et al. 47 re- viewed the reported cases of sciatic nerve EM published until 2002 and found that the right sciatic nerve was sig - nificantly more involved than the left sciatic nerve. They proposed that this could be explained anatomically as the sigmoid “protects” the left sacral plexus. However, when we used the same methodology, reviewed all cases they referenced, and added all cases published until the time of writing (47 new cases), 13,16,21,23,26,28,29,31,32,34,35,38,42,43,45,49,50,53–55 we could not confirm their finding—there was no statisti- cally significant difference between the left and right side. We acknowledge other possible explanations such as lym- phatic or hematogenous spread, but none of these theories would explain a continuous band of EM extending from the uterus to the LSP as seen in the imaging evidence pre- sented here. Separated, individual lesions (e.g., EM focus in lungs) would be expected with hematogenous or lym - phogenous spread. None of our patients had evidence sug- gestive of such lesions; in addition, this has been excluded in our Case 1 by whole-body PET/CT scanning.

We described the cases of 2 patients with sciatic nerve EM. We demonstrated that our theory is applicable to oth- er cases reported in the literature. We theorize that both can be explained by perineural spread of EM from the uterus to the sacral plexus along the visceral autonomic nerves. From the plexus, EM can spread proximally to the spinal nerves or distally to the sciatic nerve or pelvic bone and musculature using bone and muscle nerve branches. Such a complete, mechanistic explanation for selected cas- es of EM presenting with nerve symptoms has not, to our knowledge, been presented until now. Acknowledgments We are very thankful for the contribution of Dr. Caterina Giannini, who initially evaluated the specimen in Case 1. We are very grateful to Drs. Domínguez-Páez and Socolovsky, who provided us with imaging material of the case they previously reported on. Dr. Capek is supported by European Regional Development Fund–Project FNUSA-ICRC (CZ.1.05/1.1.00/02.0123).

1. Aghion DM, Capek S, Howe BM, Hepel JT, Sambandam S, Oyelese AA, et al: Perineural tumor spread of bladder cancer causing lumbosacral plexopathy: an anatomic explanation. Acta Neurochir (Wien) 156:2331–2336, 2014 [Erratum in Acta Neurochir (Wien) 157:153, 2015] 2. Anaf V , El Nakadi I, De Moor V , Chapron C, Pistofidis G, Noel JC: Increased nerve density in deep infiltrating endome - triotic nodules. Gynecol Obstet Invest 71:112–117, 2011 3. Anaf V , El Nakadi I, Simon P, Van de Stadt J, Fayt I, Simon- art T, et al: Preferential infiltration of large bowel endome- FIg. 6. Illustration of perineural spread of endometriosis. An artistic rendition of perineural spread of endometriosis along the  pelvic autonomic nerves to the sacral plexus and further distally to the sciatic nerve or proximally to the spinal nerves. A possible  intradural extension along the nerve roots is depicted. Used with permission of the Mayo Foundation for Medical Education and  Research. All rights reserved. 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J Spinal Disord Tech 22:328–333, 2009 56. Zager EL, Pfeifer SM, Brown MJ, Torosian MH, Hackney DB: Catamenial mononeuropathy and radiculopathy: a treat - able neuropathic disorder. J Neurosurg 88:827–830, 1998 disclosure The authors report no conflict of interest concerning the materi - als or methods used in this study or the findings specified in this paper. Author Contributions Conception and design: all authors. Acquisition of data: all authors. Analysis and interpretation of data: all authors. Drafting the article: all authors. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Spinner. Administrative/technical/material support: Capek, Howe, Jentoft. Study supervision: Spinner, Siquara de Sousa, Amrami. Correspondence Robert J. Spinner, Mayo Clinic, Gonda 8-214, 200 First St. SW, Rochester, MN 55905. email: [email protected]. 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