Clinical Orthopaedics and Related Research

, Volume 466, Issue 10, pp 2527–2532 | Cite as

Differences in Innervation and Innervated Neurons between Hip and Inguinal Skin

  • Takayuki Nakajima
  • Seiji Ohtori
  • Shinji Yamamoto
  • Kazuhisa Takahashi
  • Yoshitada Harada
Original Article


Pain originating from the hip may be referred to the groin and anterior thigh. We investigated sensory dorsal root ganglion neurons innervating the hip and the inguinal skin in rats using retrograde neurotransport and immunohistochemistry. A retrograde neurotracer Fluoro-Gold™ was injected into the left hip or inguinal skin of rats. Seven days later, we harvested bilateral dorsal root ganglions and counted the number of Fluoro-Gold™-labeled neurons positive for calcitonin gene-related peptide, a marker of nerve growth factor-dependent neurons, or isolectin B4, a marker of glial cell line-derived neurotrophic factor-dependent neurons. In the hip group, Fluoro-Gold™-labeled neurons were distributed throughout the left dorsal root ganglions from T13 to L5, primarily at L1, L2, L3, and L4, and the percentage of calcitonin gene-related peptide-positive neurons was higher than that of isolectin B4-binding neurons. In the inguinal skin group, Fluoro-Gold™-labeled neurons were distributed throughout the left dorsal root ganglions from T13 to L3, primarily at L1, L2, and L3, and the percentage of isolectin B4-binding neurons was higher than that of calcitonin gene-related peptide-positive neurons. These data suggest the sensory innervation pattern and characteristics of the sensory nerve of the rat hip are different from those of inguinal skin.


  1. 1.
    Ambalavanar R, Moritani M, Haines A, Hilton T, Dessem D. Chemical phenotypes of muscle and cutaneous afferent neurons in the rat trigeminal ganglion. J Comp Neurol. 2003;460:167–179.PubMedCrossRefGoogle Scholar
  2. 2.
    Averill S, McMahon SB, Clary DO, Reichardt LF, Priestley JV. Immunocytochemical localization of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur J Neurosci. 1995;7:1484–1494.PubMedCrossRefGoogle Scholar
  3. 3.
    Bennett DL, Dmietrieva N, Priestley JV, Clary D, McMahon SB. trkA, CGRP and IB4 expression in retrogradely labelled cutaneous and visceral primary sensory neurones in the rat. Neurosci Lett. 1996;206:33–36.PubMedCrossRefGoogle Scholar
  4. 4.
    Bennett DL, Koltzenburg M, Priestley JV, Shelton DL, McMahon SB. Endogenous nerve growth factor regulates the sensitivity of nociceptors in the adult rat. Eur J Neurosci. 1998;10:1282–1291.PubMedCrossRefGoogle Scholar
  5. 5.
    Birnbaum K, Prescher A, Hessler S, Heller KD. The sensory innervation of the hip joint: an anatomical study. Surg Radiol Anat. 1997;19:371–375.PubMedCrossRefGoogle Scholar
  6. 6.
    Boucher TJ, Okuse K, Bennett DL, Munson JB, Wood JN, McMahon SB. Potent analgesic effects of GDNF in neuropathic pain states. Science. 2000;290:124–127.PubMedCrossRefGoogle Scholar
  7. 7.
    Greene WB. Hip and thigh—an overview. In: Essential of Musculoskeletal Care. 2nd Ed. Rosemont, IL: Academy of Orthopaedic Surgeons; 2001:292–293.Google Scholar
  8. 8.
    Ivanavicius SP, Blake DR, Chessell IP, Mapp PI. Isolectin B4 binding neurons are not present in the rat knee joint. Neuroscience. 2004;128:555–560.PubMedCrossRefGoogle Scholar
  9. 9.
    Koltzenburg M, Bennett DL, Shelton DL, McMahon SB. Neutralization of endogenous NGF prevents the sensitization of nociceptors supplying inflamed skin. Eur J Neurosci. 1999;11:1698–1704.PubMedCrossRefGoogle Scholar
  10. 10.
    Lesher JM, Dreyfuss P, Hager N, Kaplan M, Furman M. Hip joint pain referral patterns: a descriptive study. Pain Med. 2008;9:22–25.PubMedCrossRefGoogle Scholar
  11. 11.
    McMahon SB, Bennett DL, Priestley JV, Shelton DL. The biological effects of endogenous nerve growth factor on adult sensory neurons revealed by a trkA-IgG fusion molecule. Nat Med. 1995;1:774–780.PubMedCrossRefGoogle Scholar
  12. 12.
    Molliver DC, Wright DE, Leitner ML, Parsadanian AS, Doster K, Wen D, Yan Q, Snider WD. IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron. 1997;19:849–861.PubMedCrossRefGoogle Scholar
  13. 13.
    Nakajima T, Ohtori S, Inoue G, Koshi T, Yamamoto S, Nakamura J, Takahashi K, Harada Y. The characteristics of dorsal-root ganglia and sensory innervation of the hip in rats. J Bone Joint Surg Br. 2008;90:254–257.PubMedCrossRefGoogle Scholar
  14. 14.
    Priestley JV, Michael GJ, Averill S, Liu M, Willmott N. Regulation of nociceptive neurons by nerve growth factor and glial cell line derived neurotrophic factor. Can J Physiol Pharmacol. 2002;80:495–505.PubMedCrossRefGoogle Scholar
  15. 15.
    Ramer MS, Bradbury EJ, McMahon SB. Nerve growth factor induces P2X(3) expression in sensory neurons. J Neurochem. 2001;77:864–875.PubMedCrossRefGoogle Scholar
  16. 16.
    Ro LS, Chen ST, Tang LM, Jacobs JM. Effect of NGF and anti-NGF on neuropathic pain in rats following chronic constriction injury of the sciatic nerve. Pain. 1999;79:265–274.PubMedCrossRefGoogle Scholar
  17. 17.
    Rucker HK, Holloway JA. Viscerosomatic convergence onto spinothalamic tract neurons in the cat. Brain Res. 1982;243:155–157.PubMedCrossRefGoogle Scholar
  18. 18.
    Safieh-Garabedian B, Poole S, Allchorne A, Winter J, Woolf CJ. Contribution of interleukin–1 beta to the inflammation-induced increase in nerve growth factor levels and inflammatory hyperalgesia. Br J Pharmacol. 1995;115:1265–1275.PubMedGoogle Scholar
  19. 19.
    Silverman JD, Kruger L. Selective neuronal glycoconjugate expression in sensory and autonomic ganglia: relation of lectin reactivity to peptide and enzyme markers. J Neurocytol. 1990;19:789–801.PubMedCrossRefGoogle Scholar
  20. 20.
    Snider WD, McMahon SB. Tackling pain at the source: new ideas about nociceptors. Neuron. 1998;20:629–632.PubMedCrossRefGoogle Scholar
  21. 21.
    Woolf CJ, Safieh-Garabedian B, Ma QP, Crilly P, Winter J. Nerve growth factor contributes to the generation of inflammatory sensory hypersensitivity. Neuroscience. 1994;62:327–331.PubMedCrossRefGoogle Scholar

Copyright information

© The Association of Bone and Joint Surgeons 2008

Authors and Affiliations

  • Takayuki Nakajima
    • 1
  • Seiji Ohtori
    • 1
  • Shinji Yamamoto
    • 1
  • Kazuhisa Takahashi
    • 1
  • Yoshitada Harada
    • 1
  1. 1.Department of Orthopaedic Surgery, Graduate School of MedicineChiba UniversityChuo-kuJapan

Personalised recommendations