Intercostal, ilioinguinal, and iliohypogastric nerve transfers for lower limb reinnervation after spinal cord injury: an anatomical feasibility and experimental study

Restricted access


Spinal cord injury (SCI) has been investigated in various animal studies. One promising therapeutic approach involves the transfer of peripheral nerves originating above the level of injury into those originating below the level of injury. The purpose of the present study was to evaluate the feasibility of nerve transfers for reinnervation of lower limbs in patients suffering SCI to restore some hip and knee functions, enabling them to independently stand or even step forward with assistive devices and thus improve their quality of life.


The feasibility of transferring intercostal to gluteal nerves and the ilioinguinal and iliohypogastric nerves to femoral nerves was assessed in 5 cadavers. Then, lumbar cord hemitransection was performed below L1 in 20 dogs, followed by transfer of the 10th, 11th, and 12th intercostal and subcostal nerves to gluteal nerves and the ilioinguinal and iliohypogastric nerves to the femoral nerve in only 10 dogs (NT group). At 6 months, clinical and electrophysiological evaluations of the recipient nerves and their motor targets were performed.


The donor nerves had sufficient length to reach the recipient nerves in a tension-free manner. At 6 months postoperatively, the mean conduction velocity of gluteal and femoral nerves, respectively, increased to 96.1% and 92.8% of the velocity in controls, and there was significant motor recovery of the quadriceps femoris and glutei.


Intercostal, ilioinguinal, and iliohypogastric nerves are suitable donors to transfer to the gluteal and femoral nerves after SCI to restore some hip and knee motor functions.

ABBREVIATIONS ASIS = anterosuperior iliac spine; EMG = electromyography; MAP = motor action potential; NT = nerve transfer; SCI = spinal cord injury.

Article Information

Correspondence Asser A. Sallam: Suez Canal University Hospitals, Ismailia, Egypt.

INCLUDE WHEN CITING Published online November 23, 2018; DOI: 10.3171/2018.8.SPINE181.

A.A.T. and A.A.S. contributed equally to this article.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.



  • View in gallery

    Illustrations depicting the surgical incisions used in the cadaver study. Left: The ilioinguinal incision for ilioinguinal and iliohypogastric to femoral nerve bypass surgery. Right: The surgical incisions and the subcutaneous tunnel for intercostal to gluteal nerve bypass surgery.

  • View in gallery

    Transfer of the ilioinguinal and iliohypogastric to the femoral nerve in a dog. A: The incision was made just distal to the inguinal ligament. B: Identification of ilioinguinal (II), iliohypogastric (IH), and femoral (F) nerves. C: The ilioinguinal and iliohypogastric nerves were divided as distally as possible and transferred to the femoral nerve, which was divided as proximally as possible to allow for a tension-free repair. D: The completed anastomosis.

  • View in gallery

    Intercostal nerve transfer to the gluteal nerves in a dog. The dog was placed in a lateral position. A: The lateral thoracic incision and another 2 transgluteal incisions for superior gluteal nerve (SGN) and inferior gluteal nerve (IGN). B: Exploration of 10th (T-10), 11th (T-11), and 12th (T-12) intercostal nerves, and the subcostal nerve (T-13) C: Identification of SGN. D: Identification of IGN. E: The completed anastomosis after transfer of T-10 and T-11 to the SGN. F: The completed anastomosis after transfer of the 12th and 13th intercostal nerves to the IGN.

  • View in gallery

    Mean thigh circumference before and after surgery in NT and control groups. The y-axis shows thigh circumference in centimeters.

  • View in gallery

    The amplitude of the MAPs in the study and control groups at baseline and the 6-week, 12-week, and 6-month follow-up assessments of the femoral nerve (left) and gluteal nerves (right).



Augutis MLevi R: Pediatric spinal cord injury in Sweden: incidence, etiology and outcome. Spinal Cord 41:3283362003


Bickenbach JOfficer AShakespeare Tvon Groote P (eds): International Perspectives on Spinal Cord Injury. Geneva: World Health Organization2013


Bos JCStoeckart RKlooswijk AIvan Linge BBahadoer R: The surgical anatomy of the superior gluteal nerve and anatomical radiologic bases of the direct lateral approach to the hip. Surg Radiol Anat 16:2532581994


Brown JMBarbe MFAlbo MELai HHRuggieri MR Sr: Anatomical feasibility of performing intercostal and ilioinguinal nerve to pelvic nerve transfer: a possible technique to restore lower urinary tract innervation. J Neurosurg Spine 17:3573622012


Brown JMMackinnon SE: Nerve transfers in the forearm and hand. Hand Clin 24:319340 v 2008


Brown JMShah MNMackinnon SE: Distal nerve transfers: a biology-based rationale. Neurosurg Focus 26(2):E122009


Brown WFBolton CF: Clinical Electromyography. Boston: Butterworths1987


Carlsson CASundin T: Reconstruction of afferent and efferent nervous pathways to the urinary bladder in two paraplegic patients. Spine (Phila Pa 1976) 5:37411980


Court CVialle RLepeintre JFTadié M: The thoracoabdominal intercostal nerves: an anatomical study for their use in neurotization. Surg Radiol Anat 27:8142005


Dai KRYu CTWu RSZhang XFYuan JXSun YH: Intercostal-lumbar-spinal nerve anastomoses for cord transection. A preliminary investigation. J Reconstr Microsurg 1:2232261985


Daube JR: AAEM minimonograph #11: Needle examination in clinical electromyography. Muscle Nerve 14:6857001991


Deletis VKiprovski KMorota N: The influence of halothane, enflurane, and isoflurane on motor evoked potentials. Neurosurgery 33:1731741993


Epstein FSpielholz NBattista AMcCarthy J: Delayed cauda equina reconstruction in meningomyelocele: preliminary report. Neurosurgery 6:5405411980


Gustafson KJPinault GCNeville JJSyed IDavis JA JrJean-Claude J: Fascicular anatomy of human femoral nerve: implications for neural prostheses using nerve cuff electrodes. J Rehabil Res Dev 46:9739842009


Haque RMMalone HRBauknight MWKellner MAOgden ATMartin JH: Spinal cord bypass surgery with intercostal and spinal accessory nerves: an anatomical feasibility study in human cadavers. J Neurosurg Spine 16:1781862012


Järvelä TKannus PLatvala KJärvinen M: Simple measurements in assessing muscle performance after an ACL reconstruction. Int J Sports Med 23:1962012002


Kalkman CJBeen HDOngerboer de Visser BW: Intraoperative monitoring of spinal cord function. A review. Acta Orthop Scand 64:1141231993


Klaassen ZMarshall ETubbs RSLouis RG JrWartmann CTLoukas M: Anatomy of the ilioinguinal and iliohypogastric nerves with observations of their spinal nerve contributions. Clin Anat 24:4544612011


Liu SPeulve PJin OBoisset NTiollier JSaid G: Axonal regrowth through collagen tubes bridging the spinal cord to nerve roots. J Neurosci Res 49:4254321997


Malik HGBuhr AJ: Intercostal nerve transfer to lumbar nerve roots. Part I: development of an animal model and cadaver studies. Spine (Phila Pa 1976) 4:4104151979


Marsolais GSMcLean SDerrick TConzemius MG: Kinematic analysis of the hind limb during swimming and walking in healthy dogs and dogs with surgically corrected cranial cruciate ligament rupture. J Am Vet Med Assoc 222:7397432003


Monk MLPreston CAMcGowan CM: Effects of early intensive postoperative physiotherapy on limb function after tibial plateau leveling osteotomy in dogs with deficiency of the cranial cruciate ligament. Am J Vet Res 67:5295362006


Mostafa AAGriffon DJThomas MWConstable PD: Morphometric characteristics of the pelvic limbs of Labrador Retrievers with and without cranial cruciate ligament deficiency. Am J Vet Res 70:4985072009


Oppenheim JSSpitzer DEWinfree CJ: Spinal cord bypass surgery using peripheral nerve transfers: review of translational studies and a case report on its use following complete spinal cord injury in a human. Experimental article. Neurosurg Focus 26(2):E62009


Patil A: Intercostal nerves to spinal nerve roots anastomosis (spinal cord bypass) and Harrington rod fusion in traumatic paraplegia—technical note. Acta Neurochir (Wien) 57:2993031981


Pieber KHerceg MPaternostro-Sluga TSchuhfried O: Optimizing stimulation parameters in functional electrical stimulation of denervated muscles: a cross-sectional study. J Neuroeng Rehabil 12:512015


Puisto VKääriäinen SImpinen AParkkila TVartiainen EJalanko T: Incidence of spinal and spinal cord injuries and their surgical treatment in children and adolescents: a population-based study. Spine (Phila Pa 1976) 35:1041072010


Scelsi RMarchetti CPoggi PLotta SLommi G: Muscle fiber type morphology and distribution in paraplegic patients with traumatic cord lesion. Histochemical and ultrastructural aspects of rectus femoris muscle. Acta Neuropathol 57:2432481982


Schneider CARasband WSEliceiri KW: NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:6716752012


Tyler TFMcHugh MPGleim GWNicholas SJ: The effect of immediate weightbearing after anterior cruciate ligament reconstruction. Clin Orthop Relat Res (357):1411481998


Vialle RCourt CHarding ILepeintre JFKhouri NTadié M: Multiple lumbar plexus neurotizations of the ninth, tenth, and eleventh intercostal nerves. Clin Anat 19:51582006


Vialle RCourt CHarding ILepeintre JFKhouri NTadié M: Retraction for “Multiple lumbar plexus neurotizations of the ninth, tenth, and eleventh intercostal nerves,” Clinical Anatomy 19:51–58, 2006. Clin Anat 21:7542008


Vialle RLacroix CHarding ILoureiro MCTadié M: Motor and sensitive axonal regrowth after multiple intercosto-lumbar neurotizations in a sheep model. Spinal Cord 48:3673742010


Vialle RLepeintre JFCourt CLoureiro MCLacroix CTadié M: Anatomical feasibility of using the ninth, 10th, and 11th intercostal nerves for the treatment of neurological deficits after damage to the spinal cord. J Neurosurg Spine 4:2252322006


Vialle RLozeron PLoureiro MCTadié M: Multiple lumbar roots neurotizations with the lower intercostal nerves. Preliminary clinical and electrophysiological results in a sheep model. J Surg Res 149:1992052008


Vorstman BSchlossberg SLandy HKass L: Nerve crossover techniques for urinary bladder reinnervation: animal and human cadaver studies. J Urol 137:104310471987


Weiss LWConey HDClark FC: Gross measures of exercise-induced muscular hypertrophy. J Orthop Sports Phys Ther 30:1431482000


Zentner JAlbrecht THeuser D: Influence of halothane, enflurane, and isoflurane on motor evoked potentials. Neurosurgery 31:2983051992


Zhang SJohnston LZhang ZMa YHu YWang J: Restoration of stepping-forward and ambulatory function in patients with paraplegia: rerouting of vascularized intercostal nerves to lumbar nerve roots using selected interfascicular anastomosis. Surg Technol Int 11:2442482003


Zhao SBeuerman RWKline DG: Neurotization of motor nerves innervating the lower extremity by utilizing the lower intercostal nerves. J Reconstr Microsurg 13:39451997




All Time Past Year Past 30 Days
Abstract Views 88 88 88
Full Text Views 30 30 30
PDF Downloads 46 46 46
EPUB Downloads 0 0 0


Google Scholar