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Home / Equine Research Bank / J Anat / Allometry of left ventricular myocardial innervation.
Journal of anatomy2013; 224(4); 518-526; doi: 10.1111/joa.12151

Allometry of left ventricular myocardial innervation.

Abstract: Body mass (BM) of terrestrial mammalian species ranges from a few grams in the case of the Etruscan shrew to a few tonnes for an elephant. The mass-specific metabolic rate, as well as heart rate, decrease with increasing BM, whereas heart mass is proportional to BM. In the present study, we investigated the scaling behaviour of several compartments of the left ventricular myocardium, notably its innervation, capillaries and cardiomyocytes. Myocardial samples were taken from 10 mammalian species with BM between approximately 2 g and 900 kg. Samples were analysed by design-based stereology and electron microscopy and the resulting data were subjected to linear regression and correlation analyses. The total length of nerve fibres (axons) in the left ventricle increased from 0.017 km (0.020 km) in the shrew to 7237 km (13,938 km) in the horse. The innervation density was similar among species but the mean number of axons per nerve fibre profile increased with rising BM. The total length of capillaries increased from 0.119 km (shrew) to 10,897 km (horse). The volume of cardiomyocytes was 0.017 cm(3) in the shrew and 1818 cm(3) in the horse. Scaling of the data against BM indicated a higher degree of complexity of the axon tree in larger animals and an allometric relationship between total length of nerve fibres/axons and BM. In contrast, the density of nerve fibres is independent of BM. It seems that the structural components of the autonomic nervous system in the heart are related to BM and heart mass rather than to functional parameters such as metabolic rate.
© 2013 Anatomical Society.
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Publication Date: 2013-12-10 PubMed ID: 24325466PubMed Central: PMC4098685DOI: 10.1111/joa.12151Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research paper postulates that the size of the heart and its components including nerve fibers, capillaries, and cardiac muscle cells (cardiomyocytes) vary proportionately with the body mass (BM) of different mammalian species. Further, the complexity of the nerve fibers increases with size, implying a direct relationship between the total length of nerve fibers and BM.

Body Mass and Heart Scaling

  • The research involved 10 mammalian species with varying body mass, spanning from 2g to approximately 900kg. The authors examined the scaling behavior of different compartments of the left ventricular myocardium.
  • While metabolic rate and heart rate decrease with an increase in BM, the heart mass was found to match the BM. This signifies that the heart evolves in proportion to the size of the mammal, ensuring adequate blood circulation across an incrementally large body size.

Analysis of Myocardial Samples

  • The samples from the species were analyzed using stereology (a method to derive 3-D information from 2-D images) and electron microscopy.
  • The study also performed linear regression (a statistical analysis technique) and correlation analyses to understand the dependencies and relationships between the various variables involved.

Nerve Fibers and their Complexities

  • It was found that the total length of nerve fibers in the left ventricle increased significantly with the body mass – from around 0.017 km in the shrew to 7237 km in the horse, indicating a strong correlation.
  • The authors speculate a higher degree of complexity in the axon tree (nerve fiber structure) for larger animals. However, the density of the nerve fibers remained consistent across the species, implying it is independent of the body mass.

Capillaries and Cardiomyocytes

  • Just like nerve fibers, capillaries’ total length was also observed to increase with BM – from 0.119 km in the shrew to 10,897 km in the horse.
  • The volume of cardiomyocytes showed a similar trend – from 0.017 cm(3) in the shrew to 1818 cm(3) in the horse, thereby establishing an allometric relationship.

Conclusion

  • In conclusion, this study suggests that key structural components of the autonomic nervous system – responsible for unconscious regulation of organs – in the heart, change in harmony with body mass and heart mass rather than metabolic or functional parameters.

Cite This Article

APA
Schipke J, Mayhew TM, Mühlfeld C. (2013). Allometry of left ventricular myocardial innervation. J Anat, 224(4), 518-526. https://doi.org/10.1111/joa.12151

Publication

Journal of anatomy
ISSN: 1469-7580
NlmUniqueID: 0137162
Country: England
Language: English
Volume: 224
Issue: 4
Pages: 518-526

Researcher Affiliations

Schipke, Julia
  • Institute of Functional and Applied Anatomy, Hannover Medical School, Biomedical Research in Endstage and Obstructive Lung Disease Hannover (BREATH), Member of the German Center for Lung Research (DZL), Hannover, Germany.
Mayhew, Terry M
    Mühlfeld, Christian

      MeSH Terms

      • Animals
      • Axons / ultrastructure
      • Cats
      • Cattle
      • Heart Ventricles / innervation
      • Horses
      • Mice
      • Myocardium / ultrastructure
      • Nerve Fibers / ultrastructure
      • Rats
      • Regression Analysis
      • Shrews

      References

      This article includes 63 references
      1. Anderson RH. The disposition, morphology and innervation of cardiac specialized tissue in the guinea-pig.. J Anat 1972 Apr;111(Pt 3):453-68.
        pmc: PMC1271134pubmed: 4560935
      2. Andreassen AK. Point: Cardiac denervation does/does not play a major role in exercise limitation after heart transplantation.. J Appl Physiol (1985) 2008 Feb;104(2):559-60.
        pubmed: 17615275doi: 10.1152/japplphysiol.00694.2007google scholar: lookup
      3. Armour JA, Hopkins DA. Localization of sympathetic postganglionic neurons of physiologically identified cardiac nerves in the dog.. J Comp Neurol 1981 Oct 20;202(2):169-84.
        pubmed: 6271849doi: 10.1002/cne.902020204google scholar: lookup
      4. Barth E, Stämmler G, Speiser B, Schaper J. Ultrastructural quantitation of mitochondria and myofilaments in cardiac muscle from 10 different animal species including man.. J Mol Cell Cardiol 1992 Jul;24(7):669-81.
        pubmed: 1404407doi: 10.1016/0022-2828(92)93381-sgoogle scholar: lookup
      5. Bengel FM. Imaging targets of the sympathetic nervous system of the heart: translational considerations.. J Nucl Med 2011 Aug;52(8):1167-70.
        pubmed: 21764793doi: 10.2967/jnumed.110.084228google scholar: lookup
      6. Burnstock G. Evolution of the autonomic innervation of visceral and cardiovascular systems in vertebrates.. Pharmacol Rev 1969 Dec;21(4):247-324.
        pubmed: 4311664
      7. Cao JM, Fishbein MC, Han JB, Lai WW, Lai AC, Wu TJ, Czer L, Wolf PL, Denton TA, Shintaku IP, Chen PS, Chen LS. Relationship between regional cardiac hyperinnervation and ventricular arrhythmia.. Circulation 2000 Apr 25;101(16):1960-9.
        pubmed: 10779463doi: 10.1161/01.cir.101.16.1960google scholar: lookup
      8. Cavalcanti RA, da Pureza DY, de Melo MP, de Souza RR, Bergamaschi CT, do Amaral SL, Tang H, Loesch A, Ribeiro AA. Low-intensity treadmill exercise-related changes in the rat stellate ganglion neurons.. J Neurosci Res 2009 May 1;87(6):1334-42.
        pubmed: 19115406doi: 10.1002/jnr.21961google scholar: lookup
      9. Conley KE, Kayar SR, Rösler K. Adaptive variation in the mammalian respiratory system in relation to energetic demand: IV. Capillaries and their relationship to oxidative capacity.. Respir Physiol 1987;69:47–64.
      10. Corr LA, Aberdeen JA, Milner P, Lincoln J, Burnstock G. Sympathetic and nonsympathetic neuropeptide Y-containing nerves in the rat myocardium and coronary arteries.. Circ Res 1990 Jun;66(6):1602-9.
        pubmed: 1693104doi: 10.1161/01.res.66.6.1602google scholar: lookup
      11. Crick SJ, Wharton J, Sheppard MN, Royston D, Yacoub MH, Anderson RH, Polak JM. Innervation of the human cardiac conduction system. A quantitative immunohistochemical and histochemical study.. Circulation 1994 Apr;89(4):1697-708.
        pubmed: 7908612doi: 10.1161/01.cir.89.4.1697google scholar: lookup
      12. Crick SJ, Sheppard MN, Anderson RH, Polak JM, Wharton J. A quantitative assessment of innervation in the conduction system of the calf heart.. Anat Rec 1996 Aug;245(4):685-98.
        pubmed: 8837727doi: 10.1002/(sici)1097-0185(199608)245:4<685::aid-ar9>3.0.co;2-ngoogle scholar: lookup
      13. Crick SJ, Sheppard MN, Anderson RH, Polak JM, Wharton J. A quantitative study of nerve distribution in the conduction system of the guinea pig heart.. J Anat 1996 Apr;188 ( Pt 2)(Pt 2):403-16.
        pmc: PMC1167577pubmed: 8621340
      14. Crick SJ, Anderson RH, Ho SY, Sheppard MN. Localisation and quantitation of autonomic innervation in the porcine heart II: endocardium, myocardium and epicardium.. J Anat 1999 Oct;195 ( Pt 3)(Pt 3):359-73.
        pmc: PMC1468005pubmed: 10580851doi: 10.1046/j.1469-7580.1999.19530359.xgoogle scholar: lookup
      15. Forehand CJ. Density of somatic innervation on mammalian autonomic ganglion cells is inversely related to dendritic complexity and preganglionic convergence.. J Neurosci 1985 Dec;5(12):3403-8.
        pmc: PMC6565234pubmed: 4078634doi: 10.1523/jneurosci.05-12-03403.1985google scholar: lookup
      16. Gerstheimer FP, Metz J. Distribution of calcitonin gene-related peptide-like immunoreactivity in the guinea pig heart.. Anat Embryol (Berl) 1986;175(2):255-60.
        pubmed: 3548482doi: 10.1007/bf00389603google scholar: lookup
      17. Gruber C, Kohlstedt K, Loot AE, Fleming I, Kummer W, Mühlfeld C. Stereological characterization of left ventricular cardiomyocytes, capillaries, and innervation in the nondiabetic, obese mouse.. Cardiovasc Pathol 2012 Jul-Aug;21(4):346-54.
        pubmed: 22197049doi: 10.1016/j.carpath.2011.11.003google scholar: lookup
      18. Gruber C, Nink N, Nikam S, Magdowski G, Kripp G, Voswinckel R, Mühlfeld C. Myocardial remodelling in left ventricular atrophy induced by caloric restriction.. J Anat 2012 Feb;220(2):179-85.
        pmc: PMC3275773pubmed: 22077432doi: 10.1111/j.1469-7580.2011.01453.xgoogle scholar: lookup
      19. Gundersen HJG. Notes on the estimation of the numerical density of arbitrary profiles: the edge effect.. J Microsc 1977;111:219–223.
      20. Hassankhani A, Steinhelper ME, Soonpaa MH, Katz EB, Taylor DA, Andrade-Rozental A, Factor SM, Steinberg JJ, Field LJ, Federoff HJ. Overexpression of NGF within the heart of transgenic mice causes hyperinnervation, cardiac enlargement, and hyperplasia of ectopic cells.. Dev Biol 1995 May;169(1):309-21.
        pubmed: 7750647doi: 10.1006/dbio.1995.1146google scholar: lookup
      21. Heusner AA. Energy metabolism and body size. I. Is the 0.75 mass exponent of Kleiber's equation a statistical artifact?. Respir Physiol 1982 Apr;48(1):1-12.
        pubmed: 7111915doi: 10.1016/0034-5687(82)90046-9google scholar: lookup
      22. Hillman SS, Hancock TV, Hedrick MS. A comparative meta-analysis of maximal aerobic metabolism of vertebrates: implications for respiratory and cardiovascular limits to gas exchange.. J Comp Physiol B 2013 Feb;183(2):167-79.
        pubmed: 22776908doi: 10.1007/s00360-012-0688-1google scholar: lookup
      23. Himura Y, Felten SY, Kashiki M, Lewandowski TJ, Delehanty JM, Liang CS. Cardiac noradrenergic nerve terminal abnormalities in dogs with experimental congestive heart failure.. Circulation 1993 Sep;88(3):1299-309.
        pubmed: 8102598doi: 10.1161/01.cir.88.3.1299google scholar: lookup
      24. Holt JP, Rhode EA, Kines H. Ventricular volumes and body weight in mammals.. Am J Physiol 1968 Sep;215(3):704-15.
        pubmed: 5671010doi: 10.1152/ajplegacy.1968.215.3.704google scholar: lookup
      25. Hoppeler H, Lindstedt SL, Claassen H, Taylor CR, Mathieu O, Weibel ER. Scaling mitochondrial volume in heart to body mass.. Respir Physiol 1984 Feb;55(2):131-7.
        pubmed: 6729269doi: 10.1016/0034-5687(84)90018-5google scholar: lookup
      26. Kass DA, Hare JM, Georgakopoulos D. Murine cardiac function: a cautionary tail.. Circ Res 1998 Mar 9;82(4):519-22.
        pubmed: 9506713doi: 10.1161/01.res.82.4.519google scholar: lookup
      27. Kaye DM, Vaddadi G, Gruskin SL, Du XJ, Esler MD. Reduced myocardial nerve growth factor expression in human and experimental heart failure.. Circ Res 2000 Apr 14;86(7):E80-4.
        pubmed: 10764418doi: 10.1161/01.res.86.7.e80google scholar: lookup
      28. Kimura K, Ieda M, Kanazawa H, Yagi T, Tsunoda M, Ninomiya S, Kurosawa H, Yoshimi K, Mochizuki H, Yamazaki K, Ogawa S, Fukuda K. Cardiac sympathetic rejuvenation: a link between nerve function and cardiac hypertrophy.. Circ Res 2007 Jun 22;100(12):1755-64.
        pubmed: 17495227doi: 10.1161/01.res.0000269828.62250.abgoogle scholar: lookup
      29. Kimura K, Kanazawa H, Ieda M, Kawaguchi-Manabe H, Miyake Y, Yagi T, Arai T, Sano M, Fukuda K. Norepinephrine-induced nerve growth factor depletion causes cardiac sympathetic denervation in severe heart failure.. Auton Neurosci 2010 Aug 25;156(1-2):27-35.
        pubmed: 20335077doi: 10.1016/j.autneu.2010.02.005google scholar: lookup
      30. Kleiber M. The Fire of Life: An Introduction to Animal Energetics.. New York: Wiley; 1961.
      31. Lee JC, Taylor FN, Downing SE. A comparison of ventricular weights and geometry in newborn, young, and adult mammals.. J Appl Physiol 1975 Jan;38(1):147-50.
        pubmed: 1110231doi: 10.1152/jappl.1975.38.1.147google scholar: lookup
      32. Lindstedt SL. Pulmonary transit time and diffusing capacity in mammals.. Am J Physiol 1984 Mar;246(3 Pt 2):R384-8.
        pubmed: 6703093doi: 10.1152/ajpregu.1984.246.3.r384google scholar: lookup
      33. Lindstedt SL, Calder WA. Body size, physiological time, and longevity of homeothermic animals.. Q Rev Biol 1981;56:1–16.
      34. Lindstedt SL, Schaeffer PJ. Use of allometry in predicting anatomical and physiological parameters of mammals.. Lab Anim 2002 Jan;36(1):1-19.
        pubmed: 11833526doi: 10.1258/0023677021911731google scholar: lookup
      35. Loesch A, Mayhew TM, Tang H, Ladd FV, Ladd AA, de Melo MP, da Silva AA, Coppi AA. Stereological and allometric studies on neurons and axo-dendritic synapses in the superior cervical ganglia of rats, capybaras and horses.. Cell Tissue Res 2010 Aug;341(2):223-37.
        pubmed: 20596877doi: 10.1007/s00441-010-1002-8google scholar: lookup
      36. Mattfeldt T, Mall G, Gharehbaghi H, Möller P. Estimation of surface area and length with the orientator.. J Microsc 1990 Sep;159(Pt 3):301-17.
        pubmed: 2243364doi: 10.1111/j.1365-2818.1990.tb03036.xgoogle scholar: lookup
      37. Mayhew TM. Taking tissue samples from the placenta: an illustration of principles and strategies.. Placenta 2008 Jan;29(1):1-14.
        pubmed: 17658596doi: 10.1016/j.placenta.2007.05.010google scholar: lookup
      38. Meerson FZ, Krokhina EM, Pshennikova MG, Saponicova VI. Dynamics of the rate of protein synthesis in sympathetic neurons as a factor determining the hyperfunction and hypertrophy of the heart.. J Mol Cell Cardiol 1970 Dec;1(4):411-23.
        pubmed: 4255341doi: 10.1016/0022-2828(70)90038-6google scholar: lookup
      39. Mendez J, Keys A. Density and composition of mammalian muscle.. Metabolism 1961;9:184–188.
      40. Momose M, Tyndale-Hines L, Bengel FM, Schwaiger M. How heterogeneous is the cardiac autonomic innervation?. Basic Res Cardiol 2001 Nov;96(6):539-46.
        pubmed: 11770071doi: 10.1007/s003950170004google scholar: lookup
      41. Mühlfeld C, Nyengaard JR, Mayhew TM. A review of state-of-the-art stereology for better quantitative 3D morphology in cardiac research.. Cardiovasc Pathol 2010 Mar-Apr;19(2):65-82.
        pubmed: 19144544doi: 10.1016/j.carpath.2008.10.015google scholar: lookup
      42. Mühlfeld C, Papadakis T, Krasteva G, Nyengaard JR, Hahn U, Kummer W. An unbiased stereological method for efficiently quantifying the innervation of the heart and other organs based on total length estimations.. J Appl Physiol (1985) 2010 May;108(5):1402-9.
        pubmed: 20150568doi: 10.1152/japplphysiol.01013.2009google scholar: lookup
      43. Mühlfeld C, Das SK, Heinzel FR, Schmidt A, Post H, Schauer S, Papadakis T, Kummer W, Hoefler G. Cancer induces cardiomyocyte remodeling and hypoinnervation in the left ventricle of the mouse heart.. PLoS One 2011;6(5):e20424.
        pmc: PMC3102720pubmed: 21637823doi: 10.1371/journal.pone.0020424google scholar: lookup
      44. Mühlfeld C, Schipke J, Schmidt A, Post H, Pieske B, Sedej S. Hypoinnervation is an early event in experimental myocardial remodelling induced by pressure overload.. J Anat 2013 Jun;222(6):634-44.
        pmc: PMC3666243pubmed: 23565587doi: 10.1111/joa.12044google scholar: lookup
      45. Nyengaard JR, Gundersen HJG. The isector: a simple and direct method for generating isotropic, uniform random sections from small specimens.. J Microsc 1992;165:427–431.
      46. Nyengaard JR, Bendtsen TF, Bjugn R. A stereological approach to capillary networks.. In: Sharma AK, Abdulrazzaq Y, Bedi KS, Dunn EV, James NT, Sima AAF, Yagihashi S, et al., editors. Morphometry: Applications to Medical Sciences. New Delhi: Macmillan India Ltd; 1996. pp. 265–275.
      47. Patterson JL Jr, Goetz RH, Doyle JT, Warren JV, Gauer OH, Detweiler DK, Said SI, Hoernicke H, McGregor M, Keen EN, Smith MH Jr, Hardie EL, Reynolds M, Flatt WP, Waldo DR. Cardiorespiratory dynamics in the ox and giraffe, with comparative observations on man and other mammals.. Ann N Y Acad Sci 1965 Sep 8;127(1):393-413.
        pubmed: 5217272doi: 10.1111/j.1749-6632.1965.tb49416.xgoogle scholar: lookup
      48. Peruzzi D, Hendley ED, Forehand CJ. Hypertrophy of stellate ganglion cells in hypertensive, but not hyperactive, rats.. Am J Physiol 1991 Oct;261(4 Pt 2):R979-84.
        pubmed: 1928445doi: 10.1152/ajpregu.1991.261.4.r979google scholar: lookup
      49. Peyronnet J, Poncet L, Denoroy L, Pequignot JM, Lagercrantz H, Dalmaz Y. Plasticity in the phenotypic expression of catecholamines and vasoactive intestinal peptide in adult rat superior cervical and stellate ganglia after long-term hypoxia in vivo.. Neuroscience 1999;91(3):1183-94.
        pubmed: 10391493doi: 10.1016/s0306-4522(98)00607-1google scholar: lookup
      50. Purves D, Lichtman JW. Geometrical differences among homologous neurons in mammals.. Science 1985 Apr 19;228(4697):298-302.
        pubmed: 3983631doi: 10.1126/science.3983631google scholar: lookup
      51. Qayyum MA. Innervation of the heart of the Indian cat Felis catus.. Acta Anat (Basel) 1973;85(3):395-406.
        pubmed: 4723386
      52. Ribeiro AA, Davis C, Gabella G. Estimate of size and total number of neurons in superior cervical ganglion of rat, capybara and horse.. Anat Embryol (Berl) 2004 Aug;208(5):367-80.
        pubmed: 15235907doi: 10.1007/s00429-004-0407-0google scholar: lookup
      53. Rubner M. Über den Einfluss der Körpergröße auf Stoff-und Kraftwechsel.. Z Biol 1883;19:535–562.
      54. Schaper J, Meiser E, Stämmler G. Ultrastructural morphometric analysis of myocardium from dogs, rats, hamsters, mice, and from human hearts.. Circ Res 1985 Mar;56(3):377-91.
        pubmed: 3882260doi: 10.1161/01.res.56.3.377google scholar: lookup
      55. SCHMIDT-NIELSEN K, PENNYCUIK P. Capillary density in mammals in relation to body size and oxygen consumption.. Am J Physiol 1961 Apr;200:746-50.
        pubmed: 13748094doi: 10.1152/ajplegacy.1961.200.4.746google scholar: lookup
      56. Smeyne RJ, Klein R, Schnapp A, Long LK, Bryant S, Lewin A, Lira SA, Barbacid M. Severe sensory and sympathetic neuropathies in mice carrying a disrupted Trk/NGF receptor gene.. Nature 1994 Mar 17;368(6468):246-9.
        pubmed: 8145823doi: 10.1038/368246a0google scholar: lookup
      57. Sosunov AA, Hassall CJ, Loesch A, Turmaine M, Burnstock G. Ultrastructural investigation of nitric oxide synthase-immunoreactive nerves associated with coronary blood vessels of rat and guinea-pig.. Cell Tissue Res 1995 Jun;280(3):575-82.
        pubmed: 7541718doi: 10.1007/bf00318361google scholar: lookup
      58. Stahl WR. Scaling of respiratory variables in mammals.. J Appl Physiol 1967 Mar;22(3):453-60.
        pubmed: 6020227doi: 10.1152/jappl.1967.22.3.453google scholar: lookup
      59. Stringer BM, Wynford-Thomas D, Williams ED. Physical randomization of tissue architecture: an alternative to systemic sampling.. J Microsc 1982 May;126(Pt 2):179-82.
        pubmed: 7045376doi: 10.1111/j.1365-2818.1982.tb00369.xgoogle scholar: lookup
      60. Wallis D, Watson AH, Mo N. Cardiac neurones of autonomic ganglia.. Microsc Res Tech 1996 Sep 1;35(1):69-79.
        pubmed: 8873060doi: 10.1002/(sici)1097-0029(19960901)35:1<69::aid-jemt6>3.0.co;2-ngoogle scholar: lookup
      61. Weibel ER. Stereological Methods. Practical Methods for Biological Morphometry.. London: Academic Press; 1979.
      62. Weibel ER. The Pathway for Oxygen. Structure and Function in the Mammalian Respiratory System.. Cambridge, MA: Harvard University Press; 1984.
      63. White CR, Blackburn TM, Seymour RS. Phylogenetically informed analysis of the allometry of Mammalian Basal metabolic rate supports neither geometric nor quarter-power scaling.. Evolution 2009 Oct;63(10):2658-67.
        pubmed: 19519636doi: 10.1111/j.1558-5646.2009.00747.xgoogle scholar: lookup

      Citations

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