Free Access
Issue
Math. Model. Nat. Phenom.
Volume 4, Number 3, 2009
Cancer modelling (Part 2)
Page(s) 68 - 96
DOI https://doi.org/10.1051/mmnp/20094303
Published online 05 June 2009
  1. C.A. Klein, D. Hoelzel. Systemic cancer progression and tumor dormancy: mathematical models meet single cell genomics. Cell Cycle, 5 (2006), No. 16, 1788–1798. [CrossRef] [PubMed] [Google Scholar]
  2. R.A. Willis. The Spread of Tumors in the Human Body. Butterworth and Co. Ltd., London, 1952. [Google Scholar]
  3. J.A. Aguirre-Ghiso. Models, mechanisms and clinical evidence for cancer dormancy. Nature Rev. Cancer, 7 (2007), No. 11, 834–846. [CrossRef] [PubMed] [Google Scholar]
  4. T.G. Karrison, D.J. Ferguson, P. Meier. Dormancy of Mammary Carcinoma after Mastectomy. J. Natl. Cancer Inst., 91 (1999), No. 1, 80–85. [CrossRef] [PubMed] [Google Scholar]
  5. D. Weckermann, P. Mueller, F. Wawroschek, R. Harzmann, G. Riethmueller, G. Schlimok. Disseminated Cytokeratin Positive Tumour Cells in the Bone Marrow of Patients with Prostate Cancer: Detection and Prognostic value. J. Urol., 166 (2001), No. 2, 699–703. [CrossRef] [PubMed] [Google Scholar]
  6. Early Breast Cancer Trialists' Collaborative Group (EBCTCG). Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet, 365 (2005), No. 9472, 1687–1717. [Google Scholar]
  7. T. Saphner, D.C. Tormey, R. Gray. Annual hazard rates of recurrence for breast cancer after primary therapy. J. Clin. Oncol., 14 (1996), No. 10, 2738–2746. [PubMed] [Google Scholar]
  8. L.E. Rutqvist, A. Wallgren, B. Nilsson. Is breast cancer a curable disease? A study of 14,731 women with breast cancer from the cancer registry of Norway. Cancer, 53 (1984), No. 8, 1793–1800. [CrossRef] [PubMed] [Google Scholar]
  9. S. Meng, D. Tripathy, E.P. Frenkel, S. Shete, E.Z. Naftalis, J.F. Huth, P.D. Beitsch, M. Leitch, S. Hoover, D. Euhus, B. Haley, L. Morrison, T.P. Fleming, D. Herlyn, L.W.M.M. Terstappen, T. Fehm, T.F. Tucker, N. Lane, J. Wang, J.W. Uhr. Circulating tumour cells in patients with breast cancer dormancy. Clin. Cancer Res., 10, (2004), No. 24, 8152–8162. [Google Scholar]
  10. L. Norton, R. Simon, H.D. Brereton, A.E. Bogden. Predicting the course of Gompertzian growth. Nature, 264 (1976), No. 5586, 542–545. [CrossRef] [PubMed] [Google Scholar]
  11. M.W. Retsky, R. Demicheli, D.E. Swartzendruber, P.D. Bame, R.H. Wardwell, G. Bonadonna, J.F. Speer, P. Valagussa. Computer Simulation of a breast cancer metastasis model. Breast Cancer Res. and Treat., 45 (1997), No. 2, 193–202. [CrossRef] [Google Scholar]
  12. H.J.G. Bloom, W.W. Richardson and E.J. Harries. Natural history of untreated breast cancer (1805-1933). Br. Med. J., 2 (1962), No. 5299, 213–221. [CrossRef] [PubMed] [Google Scholar]
  13. S.E. Clare, F. Nakhlis, J.C. Panetta. Molecular biology of breast cancer metastasis: the use of mathematical models to determine relapse and to predict response to chemotherapy in breast cancer. Breast Cancer Res., 2 (2000), No. 6, 430–435. [CrossRef] [PubMed] [Google Scholar]
  14. R. Demicheli, A. Abbatista, R. Micheli, P. Valagussa, G. Bonadonna. Time distribution of the recurrence risk for breast cancer patients undergoing mastectomy: further support about the concept of tumor dormancy. Breast Cancer Res. Treat., 41 (1996), No. 2, 177–185. [Google Scholar]
  15. R. Demicheli, R. Micheli, P. Valagussa, G. Bonadonna. re: Dormancy of mammary carcinoma after mastectomy. J. Natl. Cancer Inst., 92 (1999), No. 4, 347–348. [CrossRef] [Google Scholar]
  16. R. Demicheli. Tumour dormancy: findings and hypotheses from clinical research on breast cancer. Semin. Cancer Biol., 11 (2001), No. 4, 297–305. [CrossRef] [PubMed] [Google Scholar]
  17. T.G. Karrison, D.J. Ferguson, P. Meier. RESPONSE: re: Dormancy of mammary carcinoma after mastectomy., J. Natl. Cancer Inst., 92 (1999), No. 4, 348. [Google Scholar]
  18. M. Brackstone, J.L. Townson, A.F. Chambers. Tumour dormancy in breast cancer: an update. Breast Cancer Res., 9 (2007), No. 3, 208. [CrossRef] [PubMed] [Google Scholar]
  19. R.P. Araujo and D.L.S. McElwain. A history of the study of solid tumour growth: the contribution of mathematical modelling. Bull. Math. Biol., 66 (2004), No. 5, 1039–1091. [CrossRef] [MathSciNet] [PubMed] [Google Scholar]
  20. N. Bellomo, N.K. Li, P.K. Maini. On the foundations of cancer modelling: selected topics, speculations and perspectives. Math. Models Methods Appl. Sci., 18 (2008), No. 4, 593–646. [NASA ADS] [CrossRef] [EDP Sciences] [MathSciNet] [PubMed] [Google Scholar]
  21. J. Folkman. Tumor angiogenesis: therapeutic implications. N. Eng J. Med., 285 (1971), No. 21, 1182–1186. [CrossRef] [PubMed] [Google Scholar]
  22. J. Folkman. Angiogenesis in cancer, vascular, rheumatoid and other diseases. Nature Med., 1 (1995), No. 1, 27–31. [CrossRef] [Google Scholar]
  23. L. Holmgren, M.S. O'Reilly, J. Folkman. Dormancy of micrometastases: Balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nature Med., 1 (1995), No. 2, 149–153. [CrossRef] [Google Scholar]
  24. M.S. O'Reilly, L. Holmgren, Y. Shing, C. Chen, R.A. Rosenthal, M. Moses, W.S. Lane, Y. Cao, E.H. Sage, J. Folkman. Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79 (1994), No. 2, 315–328. [Google Scholar]
  25. D. Hanahan, J. Folkman. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell, 86 (1996), No. 3, 353–364. [CrossRef] [PubMed] [Google Scholar]
  26. W. Risau, H. Sariola, H.-G. Zerwes, J. Sasse, P. Ekblom, R. Kemler, T. Doetschmann. Vasculogenesis and angiogenesis in embryonic-stem-cell-derived embryoid bodies. Development, 102 (1988), No. 3, 471–478. [PubMed] [Google Scholar]
  27. W. Risau. Mechansims of angiogenesis. Nature, 386 (1997), No. 6626, 671–674. [CrossRef] [PubMed] [Google Scholar]
  28. M.F. Bolontrade, R.R. Zhou, E.S. Kleinerman. Vasculogenesis plays a role in the growth of Ewing's sarcoma in vivo. Clin. Cancer Res., 8 (2002), No. 11, 3622–3627. [PubMed] [Google Scholar]
  29. D. Ribatti, A. Vacca, F. Dammacco. New non-angiogenesis dependent pathways of tumour growth. Eur. J. Cancer, 39 (2003), No. 13, 1835–1841. [CrossRef] [PubMed] [Google Scholar]
  30. N.V. Mantzaris, S. Webb, H.G. Othmer. Mathematical modeling of tumor-induced angiogenesis. J. Math. Biol., 49 (2004), No. 2, 111–187. [MathSciNet] [PubMed] [Google Scholar]
  31. M.A.J. Chaplain, S.R. McDougall, A.R.A. Anderson. Mathematical modeling of tumor-induced angiogenesis. Annu. Rev. Biomed. Eng., 8 (2006), 233–257. [CrossRef] [PubMed] [Google Scholar]
  32. M. Baum, M.A.J. Chaplain, A.R.A. Anderson, M. Douek, J.S. Vaidya. Does breast cancer exist in a state of chaos?, Europ. J. Cancer, 35 (1999), No. 6, 886–891. [Google Scholar]
  33. A.R.A Anderson, M.A.J. Chaplain. Continuous and discrete models mathematical models of tumor-induced angiogenesis. Bull. Math. Biol., 60 (1998), No. 5, 857–899. [CrossRef] [PubMed] [Google Scholar]
  34. V.R. Muthukkaruppan, L. Kubai, R. Auerbach. Tumor-induced neovascularization in the mouse eye. J. Natl. Cancer Inst., 69 (1982), No. 3, 699–705. [PubMed] [Google Scholar]
  35. T. Alarcon, H.M. Byrne, P.K. Maini. A cellular automaton model for tumour growth in inhomogeneous environment. J. Theor. Biol., 225 (2003), No. 2, 257–274. [CrossRef] [PubMed] [Google Scholar]
  36. M.R. Owen, T. Alarcon, P.K. Maini, H.M. Byrne. Angiogenesis and vascular remodelling in normal and cancerous tissues. J. Math. Biol., 58 (2009), No.s 4-5, 689–721. [Google Scholar]
  37. S.R. McDougall, A.R.A. Anderson, M.A.J. Chaplain, J.A. Sherratt. Mathematical modelling of flow through vascular networks: implications for tumour-induced angiogenesis and chemotherapy strategies. Bull. Math. Biol., 64 (2002), No. 4, 673–702. [CrossRef] [PubMed] [Google Scholar]
  38. M. Welter, K. Bartha, H. Rieger. Emergent vascular network inhomogeneities and resulting blood flow patterns in a growing tumor. J. Theor. Biol., 250 (2008), No. 2, 257–280. [CrossRef] [PubMed] [Google Scholar]
  39. A.R. Pries, T.W. Secomb, P. Gaehtgens. Biophysical aspects of blood flow in the microvasculature. Cardiovsacular Research, 32 (1996), No. 4, 654–667. [Google Scholar]
  40. A.R. Pries, T.W. Secomb, P. Gaehtgens. Structural adaptation and stability of microvascular networks: theory and simulations. Am. J. Physiol. Heart Circ. Physiol., 275 (1998), No. 2, H349–H360. [Google Scholar]
  41. A.R. Pries, B. Reglin, T.W. Secomb. Structural adaptation of microvascular networks: functional roles of adaptive responses. Am. J. Physiol. Heart Circ. Physiol., 281 (2001), No. 3, H1015–H1025. [PubMed] [Google Scholar]
  42. H.V. Jain, J.E. Noer, T.L. Jackson. Modeling the VEGF-Bcl-2-CXCL8 pathway in intratumoral angiogenesis. Bull. Math. Biol., 70 (2008), No. 1, 89–117. [Google Scholar]
  43. D. Wodarz, Y. Iwasa, N.L. Komarova. On the emergence of multifocal cancers. J. Carcinogenesis, 3 (2004), 13. [CrossRef] [Google Scholar]
  44. D. Wodarz, N.L. Komarova. Computational biology of cancer: lecture notes and mathematical modeling. World Scientific Publishing, Singapore, 2005. [Google Scholar]
  45. S. Ramanujan, G.C. Koenig, T.P. Padera, B.R. Stoll, R.K. Jain. Local imbalance of proangiogenic and antiangiogenic factors: a potential mechanism of focal necrosis and dormancy in tumors. Cancer Research, 60 (2000), No. 5, 1442–1448. [PubMed] [Google Scholar]
  46. D. Wodarz, D.C. Krakauer. Genetic instability and the evolution of angiogenic tumor cell lines. Oncology Reports, 8 (2001), No. 6, 1195–1201. [PubMed] [Google Scholar]
  47. M.J. Plank, B.D. Sleeman, P.F. Jones. A Mathematical Model of Tumour Angiogenesis, Regulated by Vascular Endothelial Growth Factor and the Angiopoietins. J. Theor. Biol., 229 (2004), No. 4, 435–454. [CrossRef] [PubMed] [Google Scholar]
  48. H.G. Othmer, A. Stevens. Aggregation, blowup, and collapse: the ABC's of taxis in reinforced random walks. SIAM J. Appl. Math., 57 (1997), No. 4, 1044–1081. [CrossRef] [MathSciNet] [Google Scholar]
  49. G.N. Naumov, E. Bender, D. Zurakowski, S.-Y. Kand, D. Sampson, E. Flynn, R.S. Watnick, O. Straume, L.A. Akslen, J. Folkman, N. Almog. A model of human tumor dormancy: an angiogenic switch from the nonangiogenic phenotype. J. Natl. Cancer Inst., 98 (2006), No. 5, 316–325. [CrossRef] [PubMed] [Google Scholar]
  50. G. Bergers, L.E. Benjamin. Tumorigenesis and the angiogenic switch. Nature Rev. Cancer, 3 (2002), No. 6, 401–410. [CrossRef] [PubMed] [Google Scholar]
  51. A. Abdollahi, C. Schwager, J. Kleeff, I. Esposito, S. Domhan, P. Peschke, K. Hauser, P. Hahnfelt, L. Hlatky, J. Debus, J.M. Peters, H. Friess, J. Folkman, P.E. Huber. Transcriptional network governing the angiogenic switch in human pancreatic cancer. PNAS, 104 (2007), No. 21, 12890–12895. [CrossRef] [Google Scholar]
  52. P.T. Logan, B.F. Fernandes, S. Di Cesare, J.-C.A. Marshall, S.C. Maloney, M.N. Burnier. Single-cell tumor dormancy model of uveal melanoma. Clin. Exp. Metastasis, 25 (2008), No. 5, 509–516. [CrossRef] [PubMed] [Google Scholar]
  53. J.L. Townson, A.F. Chambers. Dormancy of solitary metastatic cells. Cell Cycle, 5 (2006), No. 16, 1744–1750. [CrossRef] [PubMed] [Google Scholar]
  54. G.N. Naumov, I.C. MacDonald, P.M. Weinmeister, N. Kerkvliet, K.V. Nadkarni, S.M. Wilson, V.L. Morris, A.C. Groom, A.F. Chambers. Persistence of solitary mammary carcinoma cells in a secondary site: a possible contributor to dormancy. Cancer Res., 62 (2002), No. 7, 2162–2168. [PubMed] [Google Scholar]
  55. J.A. Aguirre-Ghiso, D. Liu, A. Mignatti, K. Kovalski, L. Ossowaki. Urokinase receptor and fibronectin regulate the ERK(MAPK) to p38(MAPK) activity ratios that determine carcinoma cell proliferation or dormancy in vivo. Mol. Biol. Cell, 12 (2001), No. 4, 863–879. [PubMed] [Google Scholar]
  56. C.M. Shachaf, A.M. Kopelman, C. Arvanitis, Å. Karlsson, S. Beer, S. Mandl, M.H. Bachmann, A.D. Borowsky, B. Ruebner, R.D. Cardiff, Q. Yang, J.M. Bishop, C.H. Contag, D.W. Felsher. MYC inactivation uncovers pluripotent differentiation and tumour dormancy in hepatocellular carcinoma. Nature, 431 (2004), No. 7012, 1112–1117. [CrossRef] [PubMed] [Google Scholar]
  57. M. Guba, G. Cernaianu, G. Koehl, E.K. Geissler, K.-W. Jauch, M. Anthuber, W. Falk, M. Steinbauer. A primary tumor promotes dormancy of solitary tumor cells before inhibiting angiogenesis. Cancer Res., 61 (2001), No. 14, 5575–5579. [PubMed] [Google Scholar]
  58. A.L. Allan, S.A. Vantyghem, A.B. Tuck, A.F. Chambers. Tumor dormancy and cancer stem cells: implications for the biology and treatment of breast cancer metastasis. Breast Disease, 26 (2006, 2007), No. 1, 87–98. [Google Scholar]
  59. M. Balic, H. Lin, L. Young, D. Hawes, A. Giuliano, G. McNamara, R.H. Datar, R.J. Cote. Most early disseminated cancer cells detected in bone marrow of breast cancer patients have a putative stem cell phenotype. Clin. Cancer Res., 12 (2006), No. 19, 5615–5621. [CrossRef] [PubMed] [Google Scholar]
  60. T. Alarcon, R. Marches, K.M. Page. Mathematical models of the fate of lymphoma B cells after antigen receptor ligation with specific antibodies. J. Theor. Biol., 240 (2006), No. 1, 54–71. [CrossRef] [PubMed] [Google Scholar]
  61. T. Alarcon, H.M. Byrne, P.K. Maini. Towards whole organ modelling of tumour growth. Prog. Biophys. Mol. Biol. 85 (2004), No.s 2–3, 451–472. [Google Scholar]
  62. T. Alarcon, H.M. Byrne, P.K. Maini. A multiple scale model for tumor growth. Multiscale Model. Simul., 3 (2005), No. 2, 440–475. [NASA ADS] [CrossRef] [EDP Sciences] [MathSciNet] [PubMed] [Google Scholar]
  63. H.M. Byrne, M.R. Owen, T. Alarcon, J. Murphy, P.K. Maini. Modelling the response of vascular tumours to chemotherapy. Math. Mod. Meth. Appl. Sci., 16 (2006), No. 7S, 1219–1241. [CrossRef] [Google Scholar]
  64. B. Ribba, T. Colin, S. Schnell. A mathematical model of cancer and its use in analyzing irradiation therapies. Theor. Biol. Med. Model., 3 (2006), 7. [CrossRef] [PubMed] [Google Scholar]
  65. V. Hatzimanikatis, K.H. Lee, J.E. Bailey. A mathematical description of refulation of the G1-S transition of the mammalian cell cycle. Biotechnol. bioeng., 65 (1999), No. 6, 631–637. [CrossRef] [PubMed] [Google Scholar]
  66. M. Gyllenberg. G.F. Webb. Quiescence as an explanation of Gompertzian tumor growth. Growth, dev. aging, 86 (1987), No.s 1-2, 67–95. [Google Scholar]
  67. N.L. Komarova, D. Wodarz. Effect of cellular quiescence on the success of targeted CML therapy. PLoS ONE, 2 (2007), No. 10, e990. [Google Scholar]
  68. J.W. Uhr, R.H. Scheuermann, N.E. Street, E.S. Vitetta. Cancer dormancy: opportunities for new therapeutic approaches. Nature Med., 3 (1997), No. 5, 505–509. [CrossRef] [Google Scholar]
  69. B. Quesnel. Dormant tumor cells as a therapeutic target? Cancer Lett., 267 (2008), No. 1, 10–17. [Google Scholar]
  70. G.P. Dunn, A.T. Bruce, H. Ikeda, L.J. Old, R.D. Schreiber. Cancer immunoediting: from immunosurveillance to tumor escape. Nature Immunology, 3 (2002), No. 11, 991–999. [CrossRef] [PubMed] [Google Scholar]
  71. K.J. Weinhold, L.T. Goldstein, E.F. Wheelock. Tumour-dormant states established with L5178Y lymphoma cells in immunised syngeneic murine hosts. Nature, 270 (1977), No. 5632, 59–61. [CrossRef] [PubMed] [Google Scholar]
  72. H. Siu, E.S. Vitetta, R.D. May, J.W. Uhr. Tumor dormancy. I. Regression of BCL1 tumor and induction of a dormant tumor state in mice chimeric at the major histocompatibility complex. J. Immunol., 137 (1986), No. 4, 1376–1382. [PubMed] [Google Scholar]
  73. C.G. Clemente, M.C. Mihm Jr., R. Bufalino, S. Zurrida, P. Collini, N. Cascinelli. Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma. Cancer, 77 (1996), No. 7, 1303–1310. [CrossRef] [PubMed] [Google Scholar]
  74. J. Galon, A. Costes, F. Sanchez-Cabo, A. Kirilovsky, B. Mlecnik, C. Lagorce-Pagès, M. Tosolini, M. Camus, A. Berger, P. Wind, F. Zinzindohoué, P. Bruneval, P.-H. Cugnenc, Z. Trajanoski, W.-H. Fridman, F. Pagès. Type, density and location of immune cells within human colorectal tumors predict clinical outcome. Science, 313 (2006), No. 5795, 1960–1964. [CrossRef] [PubMed] [Google Scholar]
  75. E. Sato, S. H. Olson, J. Ahn, B. Bundy, H. Nishikawa, F. Qian, A.A. Jungbluth, D. Frosina, S. Gnjatic, C. Ambrosone, J. Kepner, T. Odunsi, G. Ritter, S. Lele, Y.-T. Chen, H. Ohtani, L.J. Old, K. Odunsi. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc. Natl. Acad. Sci., 102 (2005), No. 51, 18538–18543. [CrossRef] [Google Scholar]
  76. C.M. Koebel, W. Vermi, J.B. Swann, N. Zerafa, S.J. Rodig, L.J. Old, M.J. Smyth, R.D. Schreiber. Adaptive immunity maintains occult cancer in an equilibrium state. Nature, 450 (2007), No. 7171, 903–907. [CrossRef] [PubMed] [Google Scholar]
  77. K.M. Page, J.W. Uhr. Mathematical models of cancer dormancy. Leukemia and Lymphoma, 46 (2005), No. 3, 313–327. [CrossRef] [Google Scholar]
  78. V.A. Kuznetsov, I.A. Makalkin, M.A. Taylor, S. Perelson. Nonlinear dynamics of immunogenic tumors: parameter estimation and global bifurcation analysis. Bull. Math. Biol., 56 (1994), No. 2, 295–321. [CrossRef] [PubMed] [Google Scholar]
  79. V.A. Kuznetsov, G.D. Knott. Modeling tumor regrowth and immunotherapy. Math. Comp. Modelling, 33 (2001), No.s 12–13, 1275–1287. [Google Scholar]
  80. J.A. Adam, N. Bellomo. A survey of tumor-immune system dynamics (modeling and simulation in science, engineering and technology). Birkhaeuser, Boston, 1996. [Google Scholar]
  81. N. Bellomo, L. Preziosi. Modelling and mathematical problems related to tumor evolution and its interaction with the immune system. Math. Comp. Model., 32 (2000), No.s 3–4, 413–452. [Google Scholar]
  82. D. Kirschner, J.C. Panetta. Modeling immunotherapy of the tumor-immune interaction. J. Math. Biol., 37 (1998), No. 3, 235–252. [CrossRef] [PubMed] [Google Scholar]
  83. L.G. De Pillis, W. Gu, A.E. Radunskaya. Mixed immunotherapy and chemotherapy of tumors: modeling, applications and biological interpretations. J. Theor. Biol., 238 (2006), No. 4, 841–862. [CrossRef] [PubMed] [Google Scholar]
  84. A. Diefenbach, E.R. Jensen, A.M. Jamison, D. Raulet. Rae1 and H60 ligands of the NKG2D receptor stimulate tumor immunity. Nature, 413 (2001), No. 6852, 165–171. [CrossRef] [PubMed] [Google Scholar]
  85. D. Wodarz. Use of oncolytic viruses for the eradication of drug-resistant cancer cells. J. R. Soc. Interface, 6 (2009), No. 31, 179–186. [CrossRef] [PubMed] [Google Scholar]
  86. D. Wodarz, N. Komarova. Towards predictive computational models of oncolytic virus therapy: basis for experimental validation and model selection. PLoS One, 4 (2009) , No. 1, e4271. [Google Scholar]
  87. A. Matzavinos, M.A.J. Chaplain, V.A. Kuznetsov. Mathematical modelling of the spatio-temporal response of cytotoxic T-lymphocytes to a solid tumour. Math. Medicine and Biology: A Journal of the IMA, 21 (2004), No. 1, 1–34. [CrossRef] [PubMed] [Google Scholar]
  88. A. Matzavinos. Dynamic irregular patterns and invasive wavefronts: the control of tumour growth by cytotoxic T-lymphcytes. In: Selected topics in cancer modeling (modeling and simulation in science engineering and technology), Birkhauser, Boston, 2008. [Google Scholar]
  89. A.W. Le Serve, K. Hellman. Metastases and the normalization of tumour blood vessels by ICRF 159: a new type of drug action. Br. Med. J., 1 (1972), No. 5800, 597–601. [CrossRef] [PubMed] [Google Scholar]

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