Vet Med - Czech, 2018, 63(6):261-270 | DOI: 10.17221/61/2017-VETMED

Distribution and immunohistochemical properties of autonomic neurons supplying the ovine hip joint capsuleOriginal Paper

W. Sienkiewicz*,1, A. Dudek1, A. Chroszcz2, M. Janeczek2, J. Kaleczyc1
1 Faculty of Veterinary Medicine, University of Warmia and Mazury, Olsztyn, Poland
2 Faculty of Veterinary Medicine, Wroclaw University of Environmental and Life Sciences, Wroclaw, Poland

Combined retrograde tracing and double labelling immunohistochemistry were applied to study the distribution and chemical coding of autonomic neurons projecting to the ovine hip joint capsule. As revealed by retrograde tracing, fast blue-positive autonomic neurons supplying the lateral side of the hip joint capsule and the medial side of the hip joint capsule were located within the lumbar and sacral of the ipsilateral sympathetic chain ganglia and within the caudal mesenteric ganglion. Immunohistochemistry revealed that nearly all (sympathetic chain ganglia: 96% and caudal mesenteric ganglion: 98.8%) the neurons were adrenergic in nature (positive for dopamine β-hydroxylase). Many retrogradely labelled neurons also displayed immunoreactivity to neuropeptide Y (approximately 34% of fast blue-positive neurons within caudal mesenteric ganglion and sympathetic chain ganglia). Populations of Met-Enk+ (20%) and Leu-Enk+ (6%) neurons were present only in the sympathetic chain ganglia while within caudal mesenteric ganglion no enkephalinergic-labelled neurons were noted. Only a small population (2.2%) of hip joint capsule-projecting neurons were Gal-IR and they were observed only within the caudal mesenteric ganglion. No cholinergic neurons involved in the innervation of the hip joint capsule were found. However, fast blue-positive nerve cell bodies were surrounded by numerous cholinergic nerve fibres often forming basket-like formations. Single Gal+ nerve fibres were found in the intraganglionic connective tissue. Substance P-positive or calcitonin gene-related peptide-positive intraganglionic nerve terminals were very numerous and formed "baskets" surrounding fast blue-positive perikarya within sympathetic chain ganglias and caudal mesenteric ganglion.

Keywords: sheep; hip joint capsule; tracing; autonomic neurons; immunohistochemistry

Published: June 30, 2018  Show citation

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Sienkiewicz W, Dudek A, Chroszcz A, Janeczek M, Kaleczyc J. Distribution and immunohistochemical properties of autonomic neurons supplying the ovine hip joint capsule. Vet Med-Czech. 2018;63(6):261-270. doi: 10.17221/61/2017-VETMED.
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References

  1. Ackermann PW, Li J, Finn A, Ahmed M, Kreicbergs A (2001): Autonomic innervation of tendons, ligaments and joint capsules. A morphologic and quantitative study in the rat. Journal of Orthopaedic Research 19, 372-378. Go to original source... Go to PubMed...
  2. Ahmed M, Bjurholm A, Kreicbergs A, Schultzberg M (1993): Sensory and autonomic innervation of the facet joint in the rat lumbar spine. Spine 18, 2121-2126. Go to original source... Go to PubMed...
  3. Ahmed M, Bjurholm A, Srinivasan GR, Theodorsson E, Kreicbergs A (1994): Extraction of neuropeptides from joint tissue for quantitation by radioimmunoassay. A study in the rat. Peptides 15, 317-322. Go to original source... Go to PubMed...
  4. Ahmed M, Bjurholm A, Theodorsson E, Schultzberg M, Kreicbergs A (1995): Neuropeptide Y- and vasoactive intestinal polypeptide-like immunoreactivity in adjuvant arthritis, effects of capsaicin treatment. Neuropeptides 29, 33-43. Go to original source... Go to PubMed...
  5. Bergmann G, Siraky J, Rohlmann A, Koelbel R (1984): A comparison of hip joint forces in sheep, dog and man. Journal of Biomechanics 17, 907-921. Go to original source... Go to PubMed...
  6. Bergmann G, Graichen F, Rohlmann A (1999): Hip joint forces in sheep. Journal of Biomechanics 32, 769-777. Go to original source... Go to PubMed...
  7. Bialecki J, Majchrzycki M, Szymczak A, Klimowicz-Bodys MD, Wierzchos E, Kolomecki K (2014): Hip joint replacement using monofilament polypropylene surgical mesh, an animal model. BioMed Research International 2014, doi: 10.1155/2014/187320. Go to original source... Go to PubMed...
  8. Buma P (1994): Innervation of the patella. An immunohistochemical study in mice. Acta Orthopaedica Scandinavica 65, 80-86. Go to original source... Go to PubMed...
  9. Casatti CA, Frigo L, Bauer JA (1999): Origin of sensory and autonomic innervation of the rat temporomandibular joint: a retrograde axonal tracing study with the fluorescent dye fast blue. Journal of Dental Research 78, 776-783. Go to original source... Go to PubMed...
  10. Catre MG, Salo PT (1999): Quantitative analysis of the sympathetic innervation of the rat knee joint. Journal of Anatomy 194, 233-239. Go to original source... Go to PubMed...
  11. Dudek A, Sienkiewicz W, Marczak M, Kaleczyc J (2011): Immunohistochemical properties of motoneurons supplying the trapezius muscle in the rat. Polish Journal of Veterinary Sciences 14, 199-205. Go to original source... Go to PubMed...
  12. Dudek A, Sienkiewicz W, Pidsudko Z, Franke-Radowiecka A, Tomaszewska O, Kaleczyc J (2014): The distribution of trapezius muscle-projecting autonomic neurons in the pig. International Conference Current Approaches to Health and Diseases in Animals and Humas. Lublin, Poland. 55 pp.
  13. Heppelmann B, Shahbazian Z, Hanesch U (1997): Quantitative examination of calcitonin gene-related peptide immunoreactive nerve fibres in the cat knee joint capsule. Anatomy and Embryology 195, 525-530. Go to original source... Go to PubMed...
  14. Janig W (ed.) (2006): The Integrative Action of the Autonomic Nervous System: Neurobiology of Homeostasis. Cambridge University Press, Cambridge. 620 pp. Go to original source...
  15. Janig W, Green PG (2014): Acute inflammation in the joint: its control by the sympathetic nervous system and by neuroendocrine systems. Autonomic Neuroscience 182, 42-54. Go to original source... Go to PubMed...
  16. Lee SH, Wang SC, Shen CL (1991): Innervation of the knee joint in the rabbit and the Formosan rock-monkey (Macaca cyclopis): a retrograde HRP study. Proceedings of the National Science Council, Republic of China. Part B, Life Sciences 15, 171-177.
  17. Lundberg JM, Rudehill A, Sollevi A (1989a): Pharmacological characterization of neuropeptide Y and noradrenaline mechanisms in sympathetic control of pig spleen. European Journal of Pharmacology 163, 103-113. Go to original source... Go to PubMed...
  18. Lundberg JM, Rudehill A, Sollevi A, Fried G, Wallin G (1989b): Co-release of neuropeptide Y and noradrenaline from pig spleen in vivo: importance of subcellular storage, nerve impulse frequency and pattern, feedback regulation and resupply by axonal transport. Neuroscience 28, 475- 486. Go to original source... Go to PubMed...
  19. Marshall KW, Theriault E, Homonko DA (1994): Distribution of substance P and calcitonin gene related peptide immunoreactivity in the normal feline knee. The Journal of Rheumatology 21, 883-889.
  20. Miozzari HH, Clark JM, Jacob HA, von RB, Notzli HP (2004): Effects of removal of the acetabular labrum in a sheep hip model. Osteoarthritis and Cartilage 12, 419-430. Go to original source... Go to PubMed...
  21. Muhr G, Stockhusen H, Scartazini R (1974): Biological stabilization of plastic implants in the sheep hip joint. Langenbecks Archiv fur Chirurgie, 221-223. Go to original source...
  22. Preston E, McManus CD, Jonsson AC, Courtice GP (1995): Vasoconstrictor effects of galanin and distribution of galanin containing fibres in three species of elasmobranch fish. Regulatory Peptides 58, 123-134. Go to original source... Go to PubMed...
  23. Ruth JA, Doerr AL, Eiden LE (1984): [Leu5]enkephalin inhibits norepinephrine-induced contraction of rat aorta. European Journal of Pharmacology 105, 189-191. Go to original source... Go to PubMed...
  24. Saxler G, Loer F, Skumavc M, Pfortner J, Hanesch U (2007): Localization of SP- and CGRP-immunopositive nerve fibers in the hip joint of patients with painful osteoarthritis and of patients with painless failed total hip arthroplasties. European Journal of Pain 11, 67-74. Go to original source... Go to PubMed...
  25. Schaible HG, Straub RH (2014): Function of the sympathetic supply in acute and chronic experimental joint inflammation. Autonomic Neuroscience 182, 55-64. Go to original source... Go to PubMed...
  26. Sienkiewicz W, Majewski M, Kaleczyc J, Lakomy M (1995): Immunohistochemical study of the existence and coexistence of catecholamine synthesizing enzymes and some neuropeptides in perivascular nerve fibres of the main thoraco-cranial arteries in the pig. Folia Histochemica et Cytobiologica 33, 59-67.
  27. Sienkiewicz W, Chroszcz A, Dudek A, Janeczek M, Kaleczyc J (2015): Caudal mesenteric ganglion in the sheep - macroanatomical and immunohistochemical study. Polish Journal of Veterinary Sciences 18, 379-389. Go to original source... Go to PubMed...
  28. Tamura R, Hanesch U, Schmidt RF, Kumazawa T, Mizumura K (1998): Examination of colocalization of calcitonin gene-related peptide- and substance P-like immunoreactivity in the knee joint of the dog. Neuroscience Letters 254, 53-56. Go to original source... Go to PubMed...
  29. Uddman R, Grunditz T, Kato J, Sundler F (1998): Distribution and origin of nerve fibers in the rat temporomandibular joint capsule. Anatomy and Embryology 197, 273-282. Go to original source... Go to PubMed...
  30. Wiberg M, Widenfalk B (1991): An anatomical study of the origin of sympathetic and sensory innervation of the elbow and knee joint in the monkey. Neuroscience Letters 127, 185-188. Go to original source... Go to PubMed...
  31. Widenfalk B, Wiberg M (1989): Origin of sympathetic and sensory innervation of the knee joint. A retrograde axonal tracing study in the rat. Anatomy and Embryology 180, 317-323. Go to original source... Go to PubMed...
  32. Widenfalk B, Wiberg M (1990): Origin of sympathetic and sensory innervation of the temporo-mandibular joint. A retrograde axonal tracing study in the rat. Neuroscience Letters 109, 30-35. Go to original source... Go to PubMed...
  33. Widenfalk B, Elfvin LG, Wiberg M (1988): Origin of sympathetic and sensory innervation of the elbow joint in the rat: a retrograde axonal tracing study with wheat germ agglutinin conjugated horseradish peroxidase. Journal of Comparative Neurology 271, 313-318. Go to original source... Go to PubMed...
  34. Witonski D, Wagrowska-Danielewicz M (1999): Distribution of substance-P nerve fibers in the knee joint in patients with anterior knee pain syndrome. A preliminary report. Knee Surgery, Sports Traumatology, Arthroscopy 7, 177-183. Go to original source... Go to PubMed...
  35. Wojtys EM, Beaman DN, Glover RA, Janda D (1990): Innervation of the human knee joint by substance-P fibers. Arthroscopy: The Journal of Arthroscopic and Related Surgery 6, 254-263. Go to original source... Go to PubMed...
  36. Yoshida N, Nishiyama K, Tonosaki Y, Kikuchi S, Sugiura Y (1995): Sympathetic and sensory innervation of the rat shoulder joint: a WGA-HRP tracing and CGRP immunohistochemical study. Anatomy and Embryology 191, 465-469. Go to original source... Go to PubMed...
  37. Yoshida H, Fujita S, Nishida M, Iizuka T (1999): The expression of substance P in human temporomandibular joint samples: an immunohistochemical study. Journal of Oral Rehabilitation 26, 338-344. Go to original source... Go to PubMed...
  38. Yuan XP, Lin SX, Yuan SL, Qin BZ, Ma D (1994): Distribution, content and action site of leucine-enkephalin in pulmonary artery wall of rat and rabbit. Sheng Li Xue Bao 46, 381-389.

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