Quantitative pathology of cutaneous nerve terminal degeneration in the human skin

Hsiung-Fei Chien, T.-J. Tseng, W.-M. Lin, C.-C. Yang, Y.-C. Chang, R.-C. Chen, S.-T. Hsieh

Research output: Contribution to journalArticle

73 Citations (Scopus)

Abstract

Pathological diagnosis of neuropathy has traditionally depended on ultrastructural examinations of nerve biopsy specimens, particularly for sensory neuropathies affecting unmyelinated and small-myelinated nociceptive nerves. These sensory nerves terminate in the epidermis of the skin, and the pathology of neuropathy usually begins from nerve terminals. We investigated the feasibility of diagnosing small-fiber sensory neuropathy by evaluating cutaneous innervation. Skin biopsy specimens of 3-mm in diameter were obtained from the distal leg and the distal forearm of 55 healthy controls and 35 patients with sensory neuropathy. In the healthy controls, conventional intraepidermal nerve fiber densities (IENF densities) as measured using the image analysis system in the distal forearm and in the distal leg were correlated (r=0.55, P
Original languageEnglish
Pages (from-to)455-461
Number of pages7
JournalActa Neuropathologica
Volume102
Issue number5
Publication statusPublished - 2001
Externally publishedYes

Fingerprint

Nerve Degeneration
Pathology
Forearm
Skin
Leg
Biopsy
Nerve Fibers
Epidermis

Keywords

  • Epidermal nerve fibers
  • Nerve degeneration
  • Neuropathy
  • Skin biopsy
  • Skin innervation
  • adult
  • aged
  • article
  • clinical article
  • controlled study
  • correlation function
  • density
  • epidermis
  • evaluation
  • eye
  • feasibility study
  • female
  • forearm
  • histopathology
  • human
  • human tissue
  • image analysis
  • leg
  • male
  • measurement
  • myelinated nerve
  • nerve biopsy
  • nerve degeneration
  • nerve ending
  • nerve fiber
  • neuropathy
  • nociceptive receptor
  • nonmyelinated nerve
  • prediction
  • priority journal
  • quantitative assay
  • sensory neuropathy
  • skin biopsy
  • skin nerve
  • tissue section
  • ultrastructure
  • Adult
  • Aged
  • Biopsy
  • Cell Count
  • Epidermis
  • Female
  • Humans
  • Male
  • Middle Aged
  • Nerve Degeneration
  • Peripheral Nervous System Diseases
  • Receptors, Sensory

Cite this

Chien, H-F., Tseng, T-J., Lin, W-M., Yang, C-C., Chang, Y-C., Chen, R-C., & Hsieh, S-T. (2001). Quantitative pathology of cutaneous nerve terminal degeneration in the human skin. Acta Neuropathologica, 102(5), 455-461.

Quantitative pathology of cutaneous nerve terminal degeneration in the human skin. / Chien, Hsiung-Fei; Tseng, T.-J.; Lin, W.-M.; Yang, C.-C.; Chang, Y.-C.; Chen, R.-C.; Hsieh, S.-T.

In: Acta Neuropathologica, Vol. 102, No. 5, 2001, p. 455-461.

Research output: Contribution to journalArticle

Chien, H-F, Tseng, T-J, Lin, W-M, Yang, C-C, Chang, Y-C, Chen, R-C & Hsieh, S-T 2001, 'Quantitative pathology of cutaneous nerve terminal degeneration in the human skin', Acta Neuropathologica, vol. 102, no. 5, pp. 455-461.
Chien H-F, Tseng T-J, Lin W-M, Yang C-C, Chang Y-C, Chen R-C et al. Quantitative pathology of cutaneous nerve terminal degeneration in the human skin. Acta Neuropathologica. 2001;102(5):455-461.
Chien, Hsiung-Fei ; Tseng, T.-J. ; Lin, W.-M. ; Yang, C.-C. ; Chang, Y.-C. ; Chen, R.-C. ; Hsieh, S.-T. / Quantitative pathology of cutaneous nerve terminal degeneration in the human skin. In: Acta Neuropathologica. 2001 ; Vol. 102, No. 5. pp. 455-461.
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abstract = "Pathological diagnosis of neuropathy has traditionally depended on ultrastructural examinations of nerve biopsy specimens, particularly for sensory neuropathies affecting unmyelinated and small-myelinated nociceptive nerves. These sensory nerves terminate in the epidermis of the skin, and the pathology of neuropathy usually begins from nerve terminals. We investigated the feasibility of diagnosing small-fiber sensory neuropathy by evaluating cutaneous innervation. Skin biopsy specimens of 3-mm in diameter were obtained from the distal leg and the distal forearm of 55 healthy controls and 35 patients with sensory neuropathy. In the healthy controls, conventional intraepidermal nerve fiber densities (IENF densities) as measured using the image analysis system in the distal forearm and in the distal leg were correlated (r=0.55, P",
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author = "Hsiung-Fei Chien and T.-J. Tseng and W.-M. Lin and C.-C. Yang and Y.-C. Chang and R.-C. Chen and S.-T. Hsieh",
note = "被引用次數:63 Export Date: 16 March 2016 CODEN: ANPTA 通訊地址: Hsieh, S.-T.; Department of Anatomy/Cell Biology, Natl. Taiwan Univ. College Medicine, 1 Jen-Ai Road, Taipei 10018, Taiwan; 電子郵件: sthsieh@ha.mc.ntu.edu.tw 參考文獻: Barohn, R.J., Intraepidermal nerve fiber assessment: A new window on peripheral neuropathy (1998) Arch Neurol, 55, pp. 1505-1506; Chiang, H.Y., Huang, I.T., Chen, W.P., Chien, H.-F., Shun, C.T., Chang, Y.C., Hsieh, S.T., Regional difference in epidermal thinning after skin denervation (1998) Exp Neurol, 154, pp. 137-145; Dyck, P.J., Chalk, C.H., The 10 P's: A mnemonic helpful in characterization and differential diagnosis of peripheral neuropathy (1992) Neurology, 42, pp. 14-18; Dyck, P.J., Giannini, C., Lais, A., Pathologic alterations of nerves (1993) Peripheral Neuropathy., pp. 514-596. , Dyck PJ, Thomas PK, Griffin JW, Low PA, Poduslo JF (eds) Saunders, Philadelphia; Hedge, A.N., Inokuchi, K., Pei, W., Casadio, A., Ghirardi, M., Chain, D.G., Martin, K.C., Schwartz, J.H., Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia (1997) Cell, 89, pp. 115-126; Herrmann, D.N., Griffin, J.W., Hauer, P., Cornblath, D.R., McArthur, J.C., Epidermal nerve fiber density and sural nerve morphometry in peripheral neuropathies (1999) Neurology, 53, pp. 1634-1640; Hilliges, M., Wang, L., Johansson, O., Ultrastructural evidence for nerve fibers within all vital layers of the human epidermis (1995) J Invest Dermatol, 104, pp. 134-137; Holland, N.R., Stocks, A., Hauer, P., Cornblath, D.R., Griffin, J.W., McArthur, J.C., Intraepidermal nerve fiber density in patients with painful sensory neuropathy (1997) Neurology, 48, pp. 708-711; Holland, N.R., Crawford, T.O., Hauer, P., Cornblath, D.R., Griffin, J.W., McArthur, J.C., Small-fiber sensory neuropathies: Clinical course and neuropathology of idiopathic cases (1998) Ann Neurol, 44, pp. 47-59; Hsieh, S.T., Lin, W.M., Modulation of keratinocyte proliferation by skin innervation (1999) J Invest Dermatol, 113, pp. 579-586; Hsieh, S.T., Chiang, H.Y., Lin, W.M., Pathology of nerve terminal degeneration in the skin (2000) J Neuropathol Exp Neurol, 59, pp. 297-307; Johansson, O., Wang, L., Hilliges, M., Liang, Y., Intraepidermal nerves in human skin: PGP 9.5 immunohistochemistry with special reference to the nerve density in skin from different body regions (1999) J Periph Nerv Syst, 4, pp. 43-52; Karanth, S.S., Springall, D.R., Kuhn, D.M., Levene, M.M., Polak, J.M., An immunocytochemical study of cutaneous innervation and the distribution of neuropeptides and protein gene product 9.5 in man and commonly employed laboratory animals (1991) Am J Anat, 191, pp. 369-383; Kennedy, W.R., Said, G., Sensory nerves in skin: Answers about painful feet? (1999) Neurology, 53, pp. 1614-1615; Kennedy, W.R., Wendelschafer-Crabb, G., The innervation of human epidermis (1993) J Neurol Sci, 115, pp. 184-190; Kennedy, W.R., Wendelschafer-Crabb, G., Johnson, T., Quantitation of epidermal nerves in diabetic neuropathy (1996) Neurology, 47, pp. 1042-1048; Kennedy, W.R., Nolano, M., Wendelschafer-Crabb, G., Johnson, T.L., Tamura, E., A skin blister method to study epidermal nerves in peripheral nerve disease (1999) Muscle Nerve, 22, pp. 360-371; Lauria, G., Holland, N., Hauer, P., Cornblath, D.R., Griffin, J.W., McArthur, J.C., Epidermal innervation: Changes with aging, topographic location, and in sensory neuropathy (1999) J Neurol Sci, 164, pp. 172-178; Liang, Y., Johansson, O., Light and electron microscopic demonstration of the p75 nerve growth factor receptor in normal human cutaneous nerve fibers: New vistas (1998) J Invest Dermatol, 111, pp. 114-118; Lin, Y.H., Huang, M.H., Chang, Y.C., Tai, T.Y., Chen, W.H., Yang, C.C., Chen, R.C., Hsieh, S.T., Quantitative sensory testing: Normative values and its application in diabetic neuropathy (1998) Acta Neurol Taiwan, 7, pp. 176-184; McArthur, J.C., Stocks, E.A., Hauer, P., Cornblath, D.R., Griffin, J.W., Epidermal nerve fiber density: Normative reference range and diagnostic efficiency (1998) Arch Neurol, 55, pp. 1513-1520; McCarthy, B., Hsieh, S.T., Stocks, E.A., Hauer, P., Macko, C., Cornblath, D.R., Griffin, J.W., McArthur, J.C., Cutaneous innervation in sensory neuropathies: Evaulation by skin biopsy (1995) Neurology, 45, pp. 1848-1855; Pan, C.L., Lin, Y.H., Lin, W.M., Tai, T.Y., Hsieh, S.T., Degeneration of nociceptive nerve terminals in human peripheral neuropathy (2001) Neuro Report, 12, pp. 1-6; Periquet, M.I., Novak, V., Collins, M.P., Nagaraja, H.N., Erdem, S., Nash, S.M., Freimer, M.L., Mendell, J.R., Painful sensory neuropathy: Prospective evaluation using skin biopsy (1999) Neurology, 53, pp. 1641-1647; Scott, L.J., Griffin, J.W., Luciano, C., Barton, N.W., Banerjee, T., Crawford, T., McArthur, J.C., Schiffmann, R., Quantitative analysis of epidermal innervation in Fabry disease (1999) Neurology, 52, pp. 1249-1254; Stocks, E.A., McArthur, J.C., Griffin, J.W., Mouton, P.R., Griffin, J.W., An unbiased method for estimation of total epidermal nerve fiber length (1996) J Neurocytol, 25, pp. 637-644; Verze, L., Viglietti-Panzica, C., Plumari, L., Calcagni, M., Stella, M., Schrama, L.H., Panzica, G.C., Cutaneous innervation in hereditary sensory and autonomic neuropathy type IV (2000) Neurology, 55, pp. 126-128; Wang, L., Hilliges, M., Jernberg, T., Wiegleb-Edstronom, D., Johansson, O., Protein gene product 9.5-immunoreactive nerve fibers and cells in human skin (1990) Cell Tissue Res, 261, pp. 25-33; Wilkinson, K.D., Lee, K., Deshpande, S., Duerksen-Hughes, P., Boss, J.M., Pohl, J., The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase (1989) Science, 246, pp. 670-673",
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pages = "455--461",
journal = "Acta Neuropathologica",
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}

TY - JOUR

T1 - Quantitative pathology of cutaneous nerve terminal degeneration in the human skin

AU - Chien, Hsiung-Fei

AU - Tseng, T.-J.

AU - Lin, W.-M.

AU - Yang, C.-C.

AU - Chang, Y.-C.

AU - Chen, R.-C.

AU - Hsieh, S.-T.

N1 - 被引用次數:63 Export Date: 16 March 2016 CODEN: ANPTA 通訊地址: Hsieh, S.-T.; Department of Anatomy/Cell Biology, Natl. Taiwan Univ. College Medicine, 1 Jen-Ai Road, Taipei 10018, Taiwan; 電子郵件: sthsieh@ha.mc.ntu.edu.tw 參考文獻: Barohn, R.J., Intraepidermal nerve fiber assessment: A new window on peripheral neuropathy (1998) Arch Neurol, 55, pp. 1505-1506; Chiang, H.Y., Huang, I.T., Chen, W.P., Chien, H.-F., Shun, C.T., Chang, Y.C., Hsieh, S.T., Regional difference in epidermal thinning after skin denervation (1998) Exp Neurol, 154, pp. 137-145; Dyck, P.J., Chalk, C.H., The 10 P's: A mnemonic helpful in characterization and differential diagnosis of peripheral neuropathy (1992) Neurology, 42, pp. 14-18; Dyck, P.J., Giannini, C., Lais, A., Pathologic alterations of nerves (1993) Peripheral Neuropathy., pp. 514-596. , Dyck PJ, Thomas PK, Griffin JW, Low PA, Poduslo JF (eds) Saunders, Philadelphia; Hedge, A.N., Inokuchi, K., Pei, W., Casadio, A., Ghirardi, M., Chain, D.G., Martin, K.C., Schwartz, J.H., Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia (1997) Cell, 89, pp. 115-126; Herrmann, D.N., Griffin, J.W., Hauer, P., Cornblath, D.R., McArthur, J.C., Epidermal nerve fiber density and sural nerve morphometry in peripheral neuropathies (1999) Neurology, 53, pp. 1634-1640; Hilliges, M., Wang, L., Johansson, O., Ultrastructural evidence for nerve fibers within all vital layers of the human epidermis (1995) J Invest Dermatol, 104, pp. 134-137; Holland, N.R., Stocks, A., Hauer, P., Cornblath, D.R., Griffin, J.W., McArthur, J.C., Intraepidermal nerve fiber density in patients with painful sensory neuropathy (1997) Neurology, 48, pp. 708-711; Holland, N.R., Crawford, T.O., Hauer, P., Cornblath, D.R., Griffin, J.W., McArthur, J.C., Small-fiber sensory neuropathies: Clinical course and neuropathology of idiopathic cases (1998) Ann Neurol, 44, pp. 47-59; Hsieh, S.T., Lin, W.M., Modulation of keratinocyte proliferation by skin innervation (1999) J Invest Dermatol, 113, pp. 579-586; Hsieh, S.T., Chiang, H.Y., Lin, W.M., Pathology of nerve terminal degeneration in the skin (2000) J Neuropathol Exp Neurol, 59, pp. 297-307; Johansson, O., Wang, L., Hilliges, M., Liang, Y., Intraepidermal nerves in human skin: PGP 9.5 immunohistochemistry with special reference to the nerve density in skin from different body regions (1999) J Periph Nerv Syst, 4, pp. 43-52; Karanth, S.S., Springall, D.R., Kuhn, D.M., Levene, M.M., Polak, J.M., An immunocytochemical study of cutaneous innervation and the distribution of neuropeptides and protein gene product 9.5 in man and commonly employed laboratory animals (1991) Am J Anat, 191, pp. 369-383; Kennedy, W.R., Said, G., Sensory nerves in skin: Answers about painful feet? (1999) Neurology, 53, pp. 1614-1615; Kennedy, W.R., Wendelschafer-Crabb, G., The innervation of human epidermis (1993) J Neurol Sci, 115, pp. 184-190; Kennedy, W.R., Wendelschafer-Crabb, G., Johnson, T., Quantitation of epidermal nerves in diabetic neuropathy (1996) Neurology, 47, pp. 1042-1048; Kennedy, W.R., Nolano, M., Wendelschafer-Crabb, G., Johnson, T.L., Tamura, E., A skin blister method to study epidermal nerves in peripheral nerve disease (1999) Muscle Nerve, 22, pp. 360-371; Lauria, G., Holland, N., Hauer, P., Cornblath, D.R., Griffin, J.W., McArthur, J.C., Epidermal innervation: Changes with aging, topographic location, and in sensory neuropathy (1999) J Neurol Sci, 164, pp. 172-178; Liang, Y., Johansson, O., Light and electron microscopic demonstration of the p75 nerve growth factor receptor in normal human cutaneous nerve fibers: New vistas (1998) J Invest Dermatol, 111, pp. 114-118; Lin, Y.H., Huang, M.H., Chang, Y.C., Tai, T.Y., Chen, W.H., Yang, C.C., Chen, R.C., Hsieh, S.T., Quantitative sensory testing: Normative values and its application in diabetic neuropathy (1998) Acta Neurol Taiwan, 7, pp. 176-184; McArthur, J.C., Stocks, E.A., Hauer, P., Cornblath, D.R., Griffin, J.W., Epidermal nerve fiber density: Normative reference range and diagnostic efficiency (1998) Arch Neurol, 55, pp. 1513-1520; McCarthy, B., Hsieh, S.T., Stocks, E.A., Hauer, P., Macko, C., Cornblath, D.R., Griffin, J.W., McArthur, J.C., Cutaneous innervation in sensory neuropathies: Evaulation by skin biopsy (1995) Neurology, 45, pp. 1848-1855; Pan, C.L., Lin, Y.H., Lin, W.M., Tai, T.Y., Hsieh, S.T., Degeneration of nociceptive nerve terminals in human peripheral neuropathy (2001) Neuro Report, 12, pp. 1-6; Periquet, M.I., Novak, V., Collins, M.P., Nagaraja, H.N., Erdem, S., Nash, S.M., Freimer, M.L., Mendell, J.R., Painful sensory neuropathy: Prospective evaluation using skin biopsy (1999) Neurology, 53, pp. 1641-1647; Scott, L.J., Griffin, J.W., Luciano, C., Barton, N.W., Banerjee, T., Crawford, T., McArthur, J.C., Schiffmann, R., Quantitative analysis of epidermal innervation in Fabry disease (1999) Neurology, 52, pp. 1249-1254; Stocks, E.A., McArthur, J.C., Griffin, J.W., Mouton, P.R., Griffin, J.W., An unbiased method for estimation of total epidermal nerve fiber length (1996) J Neurocytol, 25, pp. 637-644; Verze, L., Viglietti-Panzica, C., Plumari, L., Calcagni, M., Stella, M., Schrama, L.H., Panzica, G.C., Cutaneous innervation in hereditary sensory and autonomic neuropathy type IV (2000) Neurology, 55, pp. 126-128; Wang, L., Hilliges, M., Jernberg, T., Wiegleb-Edstronom, D., Johansson, O., Protein gene product 9.5-immunoreactive nerve fibers and cells in human skin (1990) Cell Tissue Res, 261, pp. 25-33; Wilkinson, K.D., Lee, K., Deshpande, S., Duerksen-Hughes, P., Boss, J.M., Pohl, J., The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase (1989) Science, 246, pp. 670-673

PY - 2001

Y1 - 2001

N2 - Pathological diagnosis of neuropathy has traditionally depended on ultrastructural examinations of nerve biopsy specimens, particularly for sensory neuropathies affecting unmyelinated and small-myelinated nociceptive nerves. These sensory nerves terminate in the epidermis of the skin, and the pathology of neuropathy usually begins from nerve terminals. We investigated the feasibility of diagnosing small-fiber sensory neuropathy by evaluating cutaneous innervation. Skin biopsy specimens of 3-mm in diameter were obtained from the distal leg and the distal forearm of 55 healthy controls and 35 patients with sensory neuropathy. In the healthy controls, conventional intraepidermal nerve fiber densities (IENF densities) as measured using the image analysis system in the distal forearm and in the distal leg were correlated (r=0.55, P

AB - Pathological diagnosis of neuropathy has traditionally depended on ultrastructural examinations of nerve biopsy specimens, particularly for sensory neuropathies affecting unmyelinated and small-myelinated nociceptive nerves. These sensory nerves terminate in the epidermis of the skin, and the pathology of neuropathy usually begins from nerve terminals. We investigated the feasibility of diagnosing small-fiber sensory neuropathy by evaluating cutaneous innervation. Skin biopsy specimens of 3-mm in diameter were obtained from the distal leg and the distal forearm of 55 healthy controls and 35 patients with sensory neuropathy. In the healthy controls, conventional intraepidermal nerve fiber densities (IENF densities) as measured using the image analysis system in the distal forearm and in the distal leg were correlated (r=0.55, P

KW - Epidermal nerve fibers

KW - Nerve degeneration

KW - Neuropathy

KW - Skin biopsy

KW - Skin innervation

KW - adult

KW - aged

KW - article

KW - clinical article

KW - controlled study

KW - correlation function

KW - density

KW - epidermis

KW - evaluation

KW - eye

KW - feasibility study

KW - female

KW - forearm

KW - histopathology

KW - human

KW - human tissue

KW - image analysis

KW - leg

KW - male

KW - measurement

KW - myelinated nerve

KW - nerve biopsy

KW - nerve degeneration

KW - nerve ending

KW - nerve fiber

KW - neuropathy

KW - nociceptive receptor

KW - nonmyelinated nerve

KW - prediction

KW - priority journal

KW - quantitative assay

KW - sensory neuropathy

KW - skin biopsy

KW - skin nerve

KW - tissue section

KW - ultrastructure

KW - Adult

KW - Aged

KW - Biopsy

KW - Cell Count

KW - Epidermis

KW - Female

KW - Humans

KW - Male

KW - Middle Aged

KW - Nerve Degeneration

KW - Peripheral Nervous System Diseases

KW - Receptors, Sensory

M3 - Article

VL - 102

SP - 455

EP - 461

JO - Acta Neuropathologica

JF - Acta Neuropathologica

SN - 0001-6322

IS - 5

ER -