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Looking for the Word “Angiogenesis” in the History of Health Sciences: From Ancient Times to the First Decades of the Twentieth Century

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Abstract

This review deals with the origin of the term “angiogenesis”, with an attention to John Hunter who is credited with this neologism. A part of the literature refers to a Hunter’s work dating 1787, and the other part claims the first use of the term “angiogenesis” in the Hunter’s masterpiece published in 1794. Since we were unable to find the term “angiogenesis” in Hunter’s works, this review attempts to bring a new contribution to the historical research of this important concept, moving from ancient times to the first decades of the twentieth century, when “angiogenesis” begun to appear on titles of scientific articles. The development of the knowledge on the cardiocirculatory system and the principal steps of this fascinating subject were examined, with particular regard to microvascular bed and vessel sprouting, and to the intriguing observations on blood vessel neoformation that have been also made in the premicroscopic era. In Hunter’s works, the concept of angiogenesis indeed emerges, but not the term “angiogenesis”. The scientific language occurring during Hunter’s time was still old-fashioned, and the term “angiogenesis” was not one of those he used, rather a much later neologism that sounds too modern to appear in that context. Would the first appearance of the term “angiogenesis” occur in late nineteenth century in studies dealing with embryogenesis and organ vascularization? The present study aims to explore the scientific literature and to open a debate to better define this matter.

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References

  1. Ausprunk DH, Folkman J (1977) Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. Microvasc Res 14:53–65

    Article  CAS  PubMed  Google Scholar 

  2. Patan S (2000) Vasculogenesis and angiogenesis as mechanisms of vascular network formation, growth and remodeling. J Neurooncol 50:1–15

    Article  CAS  PubMed  Google Scholar 

  3. Cimpean AM, Ribatti D, Raica M (2011) A brief history of angiogenesis assay. Int J Dev Boil 55:377–382

    Article  Google Scholar 

  4. Patan S (2004) Vasculogenesis and angiogenesis. Cancer Treat Res 117:3–32

    Article  CAS  PubMed  Google Scholar 

  5. Ribatti D, Crivellato E (2012) “Sprouting angiogenesis”, a reappraisal. Dev Biol 372:157–165

    Article  CAS  PubMed  Google Scholar 

  6. Lenzi P, Bocci G, Natale G (2016) John Hunter and the origin of the term “angiogenesis”. Angiogenesis 19:255–256

    Article  PubMed  Google Scholar 

  7. Singer C (1957) A short history of anatomy and physiology from the Greeks to Harvey. Dover Publication, New York

    Google Scholar 

  8. Willerson JT, Teaff R (1996) Egyptian contributions to cardiovascular medicine. Tex Heart Inst J 23:191–200

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Boisaubin EV (1988) Cardiology in ancient Egypt. Tex Heart Inst J 15:80–85

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Ziskind B, Halioua B (2004) Contribution of ancient Egypt to cardiovascular medicine. Arch Mal Coeur Vaiss 97:70–374

    Google Scholar 

  11. Wong KC, Wu LT (1932) History of Chinese Medicine: Being a Chronicle of Medicine Happenings in China from Ancient Time to the Present. National Quarantine Services, Shanghai

    Google Scholar 

  12. Maoshing M (1995) The Yellow Emperor’s Classic of Medicine: A New Translation of the Neijing Suwen With Commentary. Shambhala Publication Inc, Boston

    Google Scholar 

  13. Dzitkowiak AJ (2006) Outlined history of the development of the world and polish cardiac surgery. J Physiol Pharm 57:43–105

    Google Scholar 

  14. Loukas M, Tubbs RS, Louis RGJ et al (2007) The cardiovascular system in the pre-Hippocratic era. Int J Cardiol 120:145–149

    Article  PubMed  Google Scholar 

  15. Sprengel C (1824) Storia prammatica della medicina. Tomo I, Da’ Torchi di Raffaele Miranda, Napoli

  16. Renouard PV (2013) History of medicine, from its origin to the nineteenth century, with an appendix, containing a philosophical and historical review of medicine to the present time, (Original work published 1856). Forgotten books, London

    Google Scholar 

  17. Khan IA, Daya SK, Gowda RM (2005) Evolution of the theory of circulation. Int J Cardiol 98:519–521

    Article  PubMed  Google Scholar 

  18. Crivellato E, Ribatti D (2006) Aristotle: the first student of angiogenesis. Leukemia 20:1209–1210

    Article  CAS  PubMed  Google Scholar 

  19. Weiss L (2000) Early concepts of cancer. Cancer Metastasis Rev 19:205–217

    Article  Google Scholar 

  20. Fancher TT, Muto A, Fitzgerald TN et al (2008) Control of blood vessel identity: from embryo to adult. Ann Vasc Dis 1:28–34

    Article  PubMed  PubMed Central  Google Scholar 

  21. Dobson JF (1927) Erasistratus. Proc R Soc Med 20:825–832

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Leith D (2015) Erasistratus’ triplokia of Arteries, veins and nerves. Apeiron 48:251–262

    Article  Google Scholar 

  23. Kühn CG (1826) Claudii Galeni Opera Omnia. Tomus XI, Officina Libraria Car. Knoblochii, Lipsiae

  24. ElMaghawry M, Zanatta A, Zampieri F (2014) The discovery of pulmonary circulation: from Imhotep to William Harvey. Global Cardiol Sci Pract. doi:10.5339/gcsp.2014.31

    Google Scholar 

  25. Abdel-Halim RE (2008) Contributions of Ibn Al-Nafis (1210-1288 AD) to the progress of medicine and urology. A study and translations from his medical works. Saudi Med J 29:13–22

    PubMed  Google Scholar 

  26. Zarshenas MM, Zargaran A (2015) A review on the Avicenna’s contribution to the field of cardiology. Int J Cardiol 182:237–241

    Article  PubMed  Google Scholar 

  27. Karimi A, Zargaran A, Borhani-Haghighi A (2013) Avicenna’s description of Willis circle. Int J Cardiol 168:30–41

    Article  Google Scholar 

  28. Dalfardi B, Yarmohammadi H (2014) The heart under the lens of Avicenna. Int J Cardiol 173:1–2

    Article  Google Scholar 

  29. Daneshfard B, Yarmohammadi H, Dalfardi B (2014) The origins of the theory of capillary circulation. Int J Cardiol 172:491–492

    Article  PubMed  Google Scholar 

  30. Gruner OC, Shah Mazar H (1930) The canon of medicine of Avicenna. AMS Press, New York

    Google Scholar 

  31. Ashtiyani SC, Shamsi M (2013) The Discoverer of Pulmonary Blood Circulation: Ibn Nafis or William Harvey? Middle East J Sci Res 18:562–568

    Google Scholar 

  32. Yarmohammadi H, Dalfardi B, Kalantari Meibodi M et al (2013) Ibn al-Quff (1233-1286 AD), genius theorist of the existence of capillaries. Int J Cardiol 168:e165

    Article  PubMed  Google Scholar 

  33. Pearce JM (2007) Malpighi and the discovery of capillaries. Eur Neurol 58:253–255

    Article  CAS  PubMed  Google Scholar 

  34. Prioreschi P (2004) Andrea Cesalpino and systemic circulation. Ann Pharm Fr 62:382–400

    Article  CAS  PubMed  Google Scholar 

  35. Harvey W (1628) Exercitatio anatomica de motu cordis et sanguinis in animalibus. Sumptibus Guilielmi Fitzeri, Frankfürt

    Google Scholar 

  36. Malpighi M (1686) Opera Omnia. R. Scot, London

    Google Scholar 

  37. Needham W (1667) Disquisitio anatomica de formato foetu, Typis Gulielmi Godbid, Prostantq; venales apud Radulphum Needham, ad Insigne Campanae in vico vulgo vocato. Little-St. Bartholomews, Londini

  38. Androutsos G, Vladimiros L, Diamantis A (2007) John Hunter (1728-1793): founder of scientific surgery and precursor of oncology. J Buon 12:421–427

    CAS  PubMed  Google Scholar 

  39. Hall AP (2005) The role of angiogenesis in cancer. Comp Clin Path 13:95–99

    Article  Google Scholar 

  40. Folkman J (2008) History of angiogenesis. In: Figg WD, Folkman J (eds) Angiogenesis. An Integrative Approach From Science To Medicine, Spinger, New York, pp 1–14

    Chapter  Google Scholar 

  41. Stephenson JA, Goddard JC, Al-Taan O et al (2013) Angiogenesis: a growth area—from John Hunter to Judah Folkman and beyond. J Cancer Res. doi:10.1155/2013/895019

    Google Scholar 

  42. Ghosh S (2013) Angiogenesis Inhibition—a promising approach to combat cancer. IOSR J Pharm Biol Sci (IOSR-JPBS) 7:52–54

    Article  Google Scholar 

  43. Vandekeere S, Dewerchin M, Carmeliet P (2015) Angiogenesis revisited: an overlooked role of endothelial cell metabolism in vessel sprouting. Microcirculation 22:509–517

    Article  PubMed  Google Scholar 

  44. Hunter J (1787) An experiment to determine the effect of extirpating one ovarium upon the number of young produced. Philos Trans R Soc Lond. doi:10.1098/rstl.1787.0021

    Google Scholar 

  45. Hunter J (1787) Observations tending to shew that the wolf, jackal, and dog, are all of the same species. Philos Trans R Soc Lond. doi:10.1098/rstl.1787.0024

    Google Scholar 

  46. Hunter J (1787) Observations on the structure and oeconomy of whales. Philosophical transactions of the royal society of london, communicated by Sir Joseph Banks. doi:10.1098/rstl.1787.0038

  47. Mariotti M, Maier JAM (2006) Angiogenesis: an overview. In: Forough R (ed) New frontiers in angiogenesis. Springer, Netherland, pp 1–29

    Chapter  Google Scholar 

  48. Ribatti D (2009) History of research on tumor angiogenesis. Springer, United Kingdom

    Google Scholar 

  49. Pathak A, Penet M, Bhuiwalla ZM (2010) MR molecular imaging of tumor vasculature and vascular targets. In: Friedmann T, Dunlap JC, Goodwin SF (eds) Advances in genetics. Elsevier, USA

    Google Scholar 

  50. Pories SE, Wulf GM (2010) Evidence for the role of bevacizumab in the treatment of advanced metastatic breast cancer: a review. Breast Cancer 2:37–44

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Kobler J (1960) The reluctant surgeon. A biography of John Hunter. Doubleday & Company, New York

    Google Scholar 

  52. Hunter J (1794) A treatise on the blood, inflammation, and gun-shot wounds. John Richardson, London

    Google Scholar 

  53. Chaplin SDJ (2009) John Hunter and the ‘museum oeconomy’, 1750–1800. Thesis submitted for the degree of Doctor of Philosophy of the University of London

  54. Skalak TC (2005) Angiogenesis and microvascular remodeling: a brief history and future roadmap. Microcirculation 12:47–58

    Article  PubMed  Google Scholar 

  55. Stapleton S (2009) The history of tumour angiogenesis as a therapeutic target. Univ Toronto Med J 87:45–49

    Google Scholar 

  56. Adair TH, Montani JP (2010) Angiogenesis. In: Granger DN, Granger JP (eds) Colloquium series on integrated systems physiology: from molecule to function. San Rafael (CA) p, Morgan & Claypool Life Sciences, pp 1–84

    Google Scholar 

  57. Hunter J (1835–1837) The works of John Hunter, F.R.S. with notes. In: Palmer JF (ed). Longman, Rees, Orme, Brown, Green, and Longman, London

  58. Hunter J (1840) A treatise on the blood, inflammation and gunshot wounds. In: Palmer JF (ed). Raswell, Barrington, and Haswell, Philadelphia

  59. Ogle W (1882) Aristotle on the parts of animals. Kegan Paul, Trench & Co, London

    Google Scholar 

  60. Hunter J (1861) Essays and Observations on Natural History, Anatomy, Physiology, Psychology and Geology. In: Owen R (ed). John van Voorst, London

  61. Rogers W, Edlich RF, Aust JB (1969) Tumor blood flow. II. Distribution of blood flow in experimental tumors. Angiology 20:374–387

    Article  CAS  PubMed  Google Scholar 

  62. Platner EA (1844) Einige Beobachtungen über die Entwicklung der Kapillargefäße (Some observations on the development of capillaries). Müller’s Archiv für Anat, Physiol und wissensch Medicin, pp 525–526

  63. Meyer J, Über die Neubildung von Blutgefässen (1853) In: Plastischen Exsudaten seröser Membranen und in Hautwunden, Ann Charité, Berlin, pp 41–140

  64. Billroth T (1856) Untersuchungen über die Entwicklung der Blutgefäße [studies on the development of blood vessels]. Druck und Verlag von Georg Reimer, Berlin

    Google Scholar 

  65. Flint JM (1900) The blood supply, angiogenesis, organogenesis, reticulum and histology of the adrenal. Johns Hopkins Hosp Rep 4:154–229

    Google Scholar 

  66. Flint JM (1903) The angiology, angiogenesis, and organogenesis of the submaxillary gland. Am J Anat 2:417–444

    Article  Google Scholar 

  67. Thoma R (1893) Untersuchungen über die Histogenese und Histomechanik des Gefässsystems. Verlag Von Ferdinander Enke, Stuttgart

    Google Scholar 

  68. Goldmann E (1908) The growth of malignant disease in man and the lower animals, with special reference to the vascular system. Proc R Soc Med (Surg Sect) 1:1–13

    CAS  Google Scholar 

  69. Sabin FR (1917) Origin and development of the primitive vessels of the chick and of the pig. Contr Embryol Carnegie Inst 6:61–124

    Google Scholar 

  70. Hertig A (1935) Angiogenesis in the early human chorion and in the primary placenta of the macaque monkey. Contr Embryol Carnegie Inst 25:37–81

    Google Scholar 

  71. His W (1868) Untersuchungen über die erste anlage des Wirbelthierleibes. Die erste Entwicklung des Hühnchens im Ei. Verlag von FCW Vogel, Leipzig

    Book  Google Scholar 

  72. Reagan FP (1917) Experimental studies on the origin of vascular endothelium and of erythrocytes. Am J Anat 21:39–175

    Article  Google Scholar 

  73. McClure CFW (1921) The endothelial problem. Anat Rec 22:219–237

    Article  Google Scholar 

  74. Lewis W (1927) The vascular patterns of tumors. Bull. Johns Hopkins Hosp 41:156–162

    Google Scholar 

  75. Rondoni P (1946) Il cancro. Istituzioni di patologia generale dei tumori. Ambrosiana, Milano

    Google Scholar 

  76. Noback CR (1946) Placentation and angiogenesis in the amnion of a baboon (Papio papio). Anat Rec 94:553–567

    Article  CAS  PubMed  Google Scholar 

  77. Greenblatt M, Shubi P (1968) Tumor angiogenesis: transfilter diffusion studies in the hamster by the transparent chamber technique. J Natl Cancer Inst 41:111–124

    CAS  PubMed  Google Scholar 

  78. Folkman J (1971) Tumor angiogenesis: therapeutic implication. N Engl J Med 285:1182–1186

    Article  CAS  PubMed  Google Scholar 

  79. Folkman J, Cole P, Zimmerman S (1966) Tumor behavior in isolated perfused organs: in vitro growth and metastases of biopsy material in rabbit thyroid and canine intestinal segment. Ann Surg 164:491–502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Gimbrone MA Jr, Aster RH, Cotran RS, Corkery J, Jandl JH, Folkman J (1969) Preservation of vascular integrity in organs perfused in vitro with a platelet-rich medium. Nature 222:33–36

    Article  PubMed  Google Scholar 

  81. Jayson GC, Kerbel R, Ellis LM, Harris AL (2016) Antiangiogenic therapy in oncology: current status and future directions. Lancet pii S0140–6736(15):01088. doi:10.1016/S0140-6736(15)01088-0

    Google Scholar 

  82. Ferrara N, Hillan KJ, Gerber HP, Novotny W (2004) Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat Rev Drug Discov 3:391–400

    Article  CAS  PubMed  Google Scholar 

  83. Gimbrone MA Jr, Leapman SB, Cotran RS, Folkman J (1972) Tumor dormancy in vivo by prevention of neovascularization. J Exp Med 136:261–276

    Article  PubMed  PubMed Central  Google Scholar 

  84. Gimbrone MA Jr, Cotran RS, Folkman J (1973) Endothelial regeneration: studies with human endothelial cells in culture. Ser Haematol 6:453–455

    PubMed  Google Scholar 

  85. Folkman J, Haudenschild C (1980) Angiogenesis in vitro. Nature 288:551–556

    Article  CAS  PubMed  Google Scholar 

  86. Taylor S, Folkman J (1982) Protamine is an inhibitor of angiogenesis. Nature 297:307–312

    Article  CAS  PubMed  Google Scholar 

  87. Crum R, Szabo S, Folkman J (1985) A new class of steroids inhibits angiogenesis in the presence of heparin or a heparin fragment. Science 230:1375–1378

    Article  CAS  PubMed  Google Scholar 

  88. Carmeliet P (2005) Angiogenesis in life, disease and medicine. Nature 438:932–936

    Article  CAS  PubMed  Google Scholar 

  89. Gensicka M, Głowacka A, Dzierzbicka K et al (2015) Inhibitors of angiogenesis in cancer therapy—synthesis and biological activity. Curr Med Chem 22:3830–3847

    Article  CAS  PubMed  Google Scholar 

  90. Huang D, Lan H, Liu F (2015) Anti-angiogenesis or pro-angiogenesis for cancer treatment: focus on drug distribution. Int J Clin Exp Med 8:8369–8376

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Rao N, Lee YF, Ge R (2015) Novel endogenous angiogenesis inhibitors and their therapeutic potential. Acta Pharmacol Sin 36:1177–1190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Zhang M, Ye G, Li J et al (2015) Recent advance in molecular angiogenesis in glioblastoma: the challenge and hope for anti-angiogenic therapy. Brain Tumor Pathol 32:229–236

    Article  CAS  PubMed  Google Scholar 

  93. Pezzella F, Gatter K (2015) Non-angiogenic tumours unveil a new chapter in cancer biology. J Pathol 235:381–383

    Article  PubMed  Google Scholar 

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Acknowledgments

The present historical research has been funded by the Museum of Human Anatomy “Filippo Civinini” of the University of Pisa.

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All the authors contributed to the writing of this review.

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Authors and Affiliations

  1. Department of Translational Research and New Technologies in Medicine and Surgery, Medical School, University of Pisa, Via Roma 55, 56126, Pisa, Italy

    Gianfranco Natale & Paola Lenzi

  2. Museum of Human Anatomy “Filippo Civinini”, Department of Translational Research and New Technologies in Medicine and Surgery, Medical School, University of Pisa, Via Roma 55, 56126, Pisa, Italy

    Gianfranco Natale & Paola Lenzi

  3. Department of Clinical and Experimental Medicine, Medical School, University of Pisa, Via Roma 55, 56126, Pisa, Italy

    Guido Bocci

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  1. Gianfranco Natale
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Correspondence to Guido Bocci.

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Natale, G., Bocci, G. & Lenzi, P. Looking for the Word “Angiogenesis” in the History of Health Sciences: From Ancient Times to the First Decades of the Twentieth Century. World J Surg 41, 1625–1634 (2017). https://doi.org/10.1007/s00268-016-3680-1

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