Review Article
Technologies supporting analytical cytology: clinical, research and drug discovery applications
Ivana K. Cecic,
Gerald Li,
Calum MacAulay,
Ivana K. Cecic
Integrative Oncology Department, BC Cancer Research Centre, 675 West 10 th Ave, Vancouver, BC, Canada
Search for more papers by this authorGerald Li
Integrative Oncology Department, BC Cancer Research Centre, 675 West 10 th Ave, Vancouver, BC, Canada
Search for more papers by this authorCorresponding Author
Calum MacAulay
Integrative Oncology Department, BC Cancer Research Centre, 675 West 10 th Ave, Vancouver, BC, Canada
Integrative Oncology Department, BC Cancer Research Centre, 675 West 10th Ave, Vancouver, BC, CanadaSearch for more papers by this authorIvana K. Cecic,
Gerald Li,
Calum MacAulay,
Ivana K. Cecic
Integrative Oncology Department, BC Cancer Research Centre, 675 West 10 th Ave, Vancouver, BC, Canada
Search for more papers by this authorGerald Li
Integrative Oncology Department, BC Cancer Research Centre, 675 West 10 th Ave, Vancouver, BC, Canada
Search for more papers by this authorCorresponding Author
Calum MacAulay
Integrative Oncology Department, BC Cancer Research Centre, 675 West 10 th Ave, Vancouver, BC, Canada
Integrative Oncology Department, BC Cancer Research Centre, 675 West 10th Ave, Vancouver, BC, CanadaSearch for more papers by this authorAbstract
The tools and techniques developed for analytical cytology have become invaluable in expanding the development of cancer screening programs and biomarker discovery for personalized medicine. Detecting cellular, molecular, and functional changes of diseased tissue as defined by quantitative analytical methodologies has enhanced the field of medical diagnostics and prognostics. The focus of this review is to outline applications and recent technical advances in flow cytometry, laser scanning cytometry, image cytometry, and quantitative image analysis, as they pertain to clinical, research, and drug discovery applications. (© 2012 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim)
References
- [1] L. A. Herzenberg and R. G. Sweet, Sci. Am. 234, 108–117 (1976).
- [2] H. R. Hulett, W. A. Bonner, J. Barrett, and L. A. Herzenberg, Science 166, 747–749 (1969).
- [3] J. Brind'Amour and P. M. Lansdorp, Nat. Methods 8, 484–486 (2011).
- [4] S. P. Perfetto, P. K. Chattopadhyay, and M. Roederer, Nat. Rev. Immunol. 4, 648–655 (2004).
- [5] F. Preffer and D. Dombkowski, Cytometry B Clin. Cytom. 76, 295–314 (2009).
- [6]
M. Roederer and R. R. Hardy, Cytometry 45, 56–64 (2001).
10.1002/1097-0320(20010901)45:1<56::AID-CYTO1144>3.0.CO;2-9 CAS PubMed Web of Science® Google Scholar
- [7]
M. Roederer, W. Moore, A. Treister, R. R. Hardy, and L. A. Herzenberg, Cytometry 45, 47–55 (2001).
10.1002/1097-0320(20010901)45:1<47::AID-CYTO1143>3.0.CO;2-A CAS PubMed Web of Science® Google Scholar
- [8]
M. Roederer, A. Treister, W. Moore, and L. A. Herzenberg, Cytometry 45, 37–46 (2001).
10.1002/1097-0320(20010901)45:1<37::AID-CYTO1142>3.0.CO;2-E CAS PubMed Web of Science® Google Scholar
- [9] W. H. Coulter, United States Patent No. 2656508 (1953).
- [10] M. R. Melamed, Methods Cell Biol. 63, 3–17 (2001).
- [11] J. C. Parker and W. R. Horst, United States Patent No. 2875666 (1953).
- [12] L. A. Kamentsky, M. R. Melamed, and H. Derman, Science 150, 630–631 (1965).
- [13] W. Dittrich and W. Gohde, Z. Naturforsch. B 24, 360–361 (1969).
- [14] C. D. Jennings and K. A. Foon, Blood 90, 2863–2892 (1997).
- [15] K. A. Foon and R. F. Todd, 3rd, Blood 68, 1–31 (1986).
- [16] M. A. Van Dilla, T. T. Trujillo, P. F. Mullaney, and J. R. Coulter, Science 163, 1213–1214 (1969).
- [17] G. Goddard, J. C. Martin, S. W. Graves, and G. Kaduchak, Cytometry A 69, 66–74 (2006).
- [18] A. Anderson and J. Bradford, J. Immunol. 184, 144.4 (2010).
- [19] N. H. Terry and R. A. White, Nat. Protoc. 1, 859–869 (2006).
- [20] G. M. Baerlocher, I. Vulto, G. de Jong, and P. M. Lansdorp, Nat. Protoc. 1, 2365–2376 (2006).
- [21] A. C. Rawstron, N. Villamor, M. Ritgen, S. Bottcher, P. Ghia, J. L. Zehnder, G. Lozanski, D. Colomer, C. Moreno, M. Geuna, P. A. Evans, Y. Natkunam, S. E. Coutre, E. D. Avery, L. Z. Rassenti, T. J. Kipps, F. Caligaris-Cappio, M. Kneba, J. C. Byrd, M. J. Hallek, E. Montserrat, and P. Hillmen, Leukemia 21, 956–964 (2007).
- [22] A. C. Rawstron, B. Kennedy, P. A. Evans, F. E. Davies, S. J. Richards, A. P. Haynes, N. H. Russell, G. Hale, G. J. Morgan, A. S. Jack, and P. Hillmen, Blood 98, 29–35 (2001).
- [23] J. E. Sausville, R. G. Salloum, L. Sorbara, D. W. Kingma, M. Raffeld, R. J. Kreitman, P. D. Imus, D. Venzon, and M. Stetler-Stevenson, Am. J. Clin. Pathol. 119, 213–217 (2003).
- [24] E. G. Weir, K. Cowan, P. LeBeau, and M. J. Borowitz, Leukemia 13, 558–567 (1999).
- [25] N. G. Haycocks, L. Lawrence, J. W. Cain, and X. F. Zhao, Cytometry B Clin. Cytom. 80, 221–229 (2011).
- [26] B. J. Bain, D. Barnett, D. Linch, E. Matutes, and J. T. Reilly, Clin. Lab. Haematol. 24, 1–13 (2002).
- [27] G. E. Marti, A. C. Rawstron, P. Ghia, P. Hillmen, R. S. Houlston, N. Kay, T. A. Schleinitz, and N. Caporaso, Br. J. Haematol. 130, 325–332 (2005).
- [28]
C. C. Stewart, F. G. Behm, J. L. Carey, J. Cornbleet, R. E. Duque, S. D. Hudnall, P. E. Hurtubise, M. Loken, R. R. Tubbs, and S. Wormsley, Cytometry 30, 231–235 (1997).
10.1002/(SICI)1097-0320(19971015)30:5<231::AID-CYTO3>3.0.CO;2-K CAS PubMed Web of Science® Google Scholar
- [29] C. R. Friese, C. C. Earle, L. S. Magazu, J. R. Brown, B. A. Neville, N. D. Hevelone, L. C. Richardson, and G. A. Abel, Cancer 117, 1470–1477 (2011).
- [30] W. G. Nieto, J. Almeida, C. Teodosio, F. Abbasi, S. D. Allgood, F. Connors, J. M. Rachel, P. Ghia, M. C. Lanasa, A. C. Rawstron, A. Orfao, N. E. Caporaso, C. A. Hanson, Y. K. Shim, R. F. Vogt, and G. E. Marti, Cytometry B Clin. Cytom. 78(Suppl. 1), S4–S9 (2010).
- [31] O. Landgren, M. Albitar, W. Ma, F. Abbasi, R. B. Hayes, P. Ghia, G. E. Marti, and N. E. Caporaso, N. Engl. J. Med. 360, 659–667 (2009).
- [32] G. Marti, F. Abbasi, E. Raveche, A. C. Rawstron, P. Ghia, T. Aurran, N. Caporaso, Y. K. Shim, and R. F. Vogt, Br. J. Haematol. 139, 701–708 (2007).
- [33] A. C. Rawstron, F. L. Bennett, S. J. M. O'Connor, M. Kwok, J. A. L. Fenton, M. Plummer, R. de Tute, R. G. Owen, S. J. Richards, A. S. Jack, and P. Hillmen, N. Engl. J. Med. 359, 575–583 (2008).
- [34] T. D. Shanafelt, N. E. Kay, T. G. Call, C. S. Zent, D. F. Jelinek, B. LaPlant, W. G. Morice, and C. A. Hanson, Leuk. Res. 32, 1458–1461 (2008).
- [35] J. R. Fromm, A. Thomas, and B. L. Wood, Am. J. Clin. Pathol. 131, 322–332 (2009).
- [36] A. Demurtas, G. Accinelli, D. Pacchioni, L. Godio, D. Novero, G. Bussolati, G. Palestro, M. Papotti, and A. Stacchini, Appl. Immunohistochem. Mol. Morphol. 18, 311–322 (2010).
- [37] M. Bangerter, O. Brudler, B. Heinrich, and M. Griesshamnuer, Acta Cytol. 51, 390–398 (2007).
- [38] S. Schmid, M. Tinguely, P. Cione, H. Moch, and B. Bode, Cytopathology 22, 397–406 (2011).
- [39] W. Zhang, Y. C. Yang, B. N. Zhang, Q. J. Pan, S. D. Hart, K. Duvall, Z. F. Zhang, and J. Y. Rao, Int. J. Cancer 119, 359–364 (2006).
- [40]
K. Truong, P. Vielh, B. Malfoy, J. Klijanienko, B. Dutrillaux, and C. A. Bourgeois, Cancer 84, 309–316 (1998).
10.1002/(SICI)1097-0142(19981025)84:5<309::AID-CNCR7>3.0.CO;2-Z CAS PubMed Web of Science® Google Scholar
- [41] R. Nunez, Curr. Issues Mol. Biol. 3, 67–70 (2001).
- [42] M. Hayashi, S. Kawauchi, K. Ueda, Y. Kaneda, A. Oga, T. Furuya, K. Hamano, and K. Sasaki, Oncol. Rep. 14, 1429–1435 (2005).
- [43] X. P. Liu, T. Sato, A. Oga, K. Ikemoto, S. Kawauchi, E. Ikeda, and K. Sasaki, Int. J. Oncol. 25, 615–621 (2004).
- [44] U. De Giorgi, V. Valero, E. Rohren, S. Dawood, N. T. Ueno, M. C. Miller, G. V. Doyle, S. Jackson, E. Andreopoulou, B. C. Handy, J. M. Reuben, H. A. Fritsche, H. A. Macapinlac, G. N. Hortobagyi, and M. Cristofanilli, J. Clin. Oncol. 27, 3303–3311 (2009).
- [45] D. F. Hayes, M. Cristofanilli, G. T. Budd, M. J. Ellis, A. Stopeck, M. C. Miller, J. Matera, W. J. Allard, G. V. Doyle, and L. W. Terstappen, Clin. Cancer Res. 12, 4218–4224 (2006).
- [46] Y. Hu, L. Fan, J. Zheng, R. Cui, W. Liu, Y. He, X. Li, and S. Huang, Cytometry A 77, 213–219 (2010).
- [47] L. De Mattos-Arruda, I. Elattar, and H. A. Azim, Jr., Ann. Oncol. 22, 234 (2011).
- [48] E. Ortolan, R. Arisio, S. Morone, P. Bovino, N. Lo-Buono, G. Nacci, R. Parrotta, D. Katsaros, I. Rapa, G. Migliaretti, E. Ferrero, M. Volante, and A. Funaro, J. Natl. Cancer Inst. 102, 1160–1177 (2010).
- [49] D. C. Douek, J. M. Brenchley, M. R. Betts, D. R. Ambrozak, B. J. Hill, Y. Okamoto, J. P. Casazza, J. Kuruppu, K. Kunstman, S. Wolinsky, Z. Grossman, M. Dybul, A. Oxenius, D. A. Price, M. Connors, and R. A. Koup, Nature 417, 95–98 (2002).
- [50] O. P. Arewa, Afr. J. Med. Med. Sci. 39, 5–12 (2010).
- [51] F. Mandy, G. Janossy, M. Bergeron, R. Pilon, and S. Faucher, Cytometry B Clin. Cytom. 74(Suppl. 1), S27–S39 (2008).
- [52] R. A. Bray, Methods Cell Biol. 41, 103–119 (1994).
- [53] N. Goulden, P. Bader, V. Van Der Velden, J. Moppett, M. Schilham, H. O. Masden, O. Krejci, H. Kreyenberg, A. Lankester, T. Revesz, T. Klingebiel, and J. Van Dongen, Br. J. Haematol. 122, 24–29 (2003).
- [54] M. G. Ormerod, F. Paul, M. Cheetham, and X. M. Sun, Cytometry 21, 300–304 (1995).
- [55] W. G. Telford, A. Komoriya, and B. Z. Packard, Methods Mol. Biol. 263, 141–160 (2004).
- [56] J. M. Irish, R. Hovland, P. O. Krutzik, O. D. Perez, O. Bruserud, B. T. Gjertsen, and G. P. Nolan, Cell 118, 217–228 (2004).
- [57] N. Kotecha, N. J. Flores, J. M. Irish, E. F. Simonds, D. S. Sakai, S. Archambeault, E. Diaz-Flores, M. Coram, K. M. Shannon, G. P. Nolan, and M. L. Loh, Cancer Cell 14, 335–343 (2008).
- [58] P. O. Krutzik and G. P. Nolan, Cytometry A 55, 61–70 (2003).
- [59] O. D. Perez and G. P. Nolan, Nat. Biotechnol. 20, 155–162 (2002).
- [60] G. Noppe, P. Dekker, C. de Koning-Treurniet, J. Blom, D. van Heemst, R. W. Dirks, H. J. Tanke, R. G. Westendorp, and A. B. Maier, Cytometry A 75, 910–916 (2009).
- [61] S. Pyne, X. Hu, K. Wang, E. Rossin, T. I. Lin, L. M. Maier, C. Baecher-Allan, G. J. McLachlan, P. Tamayo, D. A. Hafler, P. L. De Jager, and J. P. Mesirov, Proc. Natl. Acad. Sci. U.S.A. 106, 8519–8524 (2009).
- [62] E. S. Costa, M. E. Arroyo, C. E. Pedreira, M. A. Garcia-Marcos, M. D. Tabernero, J. Almeida, and A. Orfao, Leukemia 20, 1221–1230 (2006).
- [63] A. Bashashati and R. R. Brinkman, Adv. Bioinformatics, 584603 (2009).
- [64] V. Kapoor, F. V. Subach, V. G. Kozlov, A. Grudinin, V. V. Verkhusha, and W. G. Telford, Nat. Methods 4, 678–679 (2007).
- [65] W. Telford, M. Murga, T. Hawley, R. Hawley, B. Packard, A. Komoriya, F. Haas, and C. Hubert, Cytometry A 68, 36–44 (2005).
- [66] L. A. Kamentsky and L. D. Kamentsky, Cytometry 12, 381–387 (1991).
- [67] R. Shack, R. Baker, R. Buchroeder, D. Hillman, R. Shoemaker, and P. H. Bartels, J. Histochem. Cytochem. 27, 153–159 (1979).
- [68] Z. Darzynkiewicz, E. Bedner, X. Li, W. Gorczyca, and M. R. Melamed, Exp. Cell Res. 249, 1–12 (1999).
- [69] M. M. Harnett, Nat. Rev. Immunol. 7, 897–904 (2007).
- [70] R. J. Clatch and J. L. Walloch, Acta Cytol. 41, 109–122 (1997).
- [71] L. A. Kamentsky, D. E. Burger, R. J. Gershman, L. D. Kamentsky, and E. Luther, Acta Cytol. 41, 123–143 (1997).
- [72] J. Inglese, D. S. Auld, and T. P. Begley, Wiley Encyclopedia of Chemical Biology (John Wiley & Sons, Inc., 2007), pp. 1–15.
- [73] N. Thomas, J. Biomol. Screen 15, 1–9 (2010).
- [74] W. Gorczyca, M. R. Melamed, and Z. Darzynkiewicz, Cell Prolif. 29, 539–547 (1996).
- [75]
S. Kakino, K. Sasaki, A. Kurose, and H. Ito, Cytometry 24, 49–54 (1996).
10.1002/(SICI)1097-0320(19960501)24:1<49::AID-CYTO6>3.0.CO;2-D CAS PubMed Web of Science® Google Scholar
- [76] X. Li, M. R. Melamed, and Z. Darzynkiewicz, Exp. Cell Res. 222, 28–37 (1996).
- [77] X. Li, F. Traganos, M. R. Melamed, and Z. Darzynkiewicz, Cytometry 20, 172–180 (1995).
- [78] D. Basiji, in: Proceedings of the 2007 4th IEEE International Symposium on Biomedical Imaging: From Nano to Macro, Arlington, VA, USA, 12–15 April 2007, pp. 1100–1103.
- [79] D. A. Basiji, W. E. Ortyn, L. Liang, V. Venkatachalam, and P. Morrissey, Clin. Lab. Med. 27, 653–670 (2007).
- [80] E. Luther, L. A. Kamentsky, and E. S. Cibas, Anal. Quant. Cytol. Histol. 18, 76–77 (1996).
- [81]
E. Bedner, X. Li, W. Gorczyca, M. R. Melamed, and Z. Darzynkiewicz, Cytometry 35, 181–195 (1999).
10.1002/(SICI)1097-0320(19990301)35:3<181::AID-CYTO1>3.0.CO;2-5 CAS PubMed Web of Science® Google Scholar
- [82] T. Tsujioka and K. Tohyama, in: C.-C. Wang (ed.) Laser Scanning, Theory and Applications (InTech, 2011).
- [83] D. Roman and P. G. Germann, Exp. Toxicol. Pathol. 54, 169–170 (2002).
- [84]
L. Suter, E. Koch, R. Bechter, and M. Bobadilla, Cytometry 27, 161–168 (1997).
10.1002/(SICI)1097-0320(19970201)27:2<161::AID-CYTO8>3.0.CO;2-J CAS PubMed Web of Science® Google Scholar
- [85] J. Medina, D. Roman, G. E. Garcia, M. Bobadilla, W. Sutter, and A. deFraisinette, J. Invest. Dermatol. 110, 552 (1998).
- [86]
D. Roman and M. Bobadilla, Toxicol. Lett. 95(Suppl. 1), 198 (1998).
10.1016/S0378-4274(98)80790-X Google Scholar
- [87]
D. Roman, F. Locher, W. Suter, A. Cordier, and M. Bobadilla, Environ. Mol. Mutagen 32, 387–396 (1998).
10.1002/(SICI)1098-2280(1998)32:4<387::AID-EM13>3.0.CO;2-Y CAS PubMed Web of Science® Google Scholar
- [88] D. Roman, A. deBrugerolle-deFraissinette, B. Greiner, J. Marty, B. Vogel, M. Kolopp, A. Cordier, H. Van Cauteren, and M. Bobadilla, Toxicol. Lett. 109(Suppl. 1), 110 (1999).
- [89] D. Roman, A. deBrugerolle-deFraissinette, B. Greiner, and M. Bobadilla, Cytometry 10(Suppl.), 96 (2000).
- [90] V. Espina, J. D. Wulfkuhle, V. S. Calvert, A. VanMeter, W. Zhou, G. Coukos, D. H. Geho, E. F. Petricoin, 3rd, and L. A. Liotta, Nat. Protoc. 1, 586–603 (2006).
- [91] M. R. Emmert-Buck, R. F. Bonner, P. D. Smith, R. F. Chuaqui, Z. Zhuang, S. R. Goldstein, R. A. Weiss, and L. A. Liotta, Science 274, 998–1001 (1996).
- [92] B. Domazet, G. T. Maclennan, A. Lopez-Beltran, R. Montironi, and L. Cheng, Int. J. Clin. Exp. Pathol. 1, 475–488 (2008).
- [93] A. Pierzchalski, A. Mittag, and A. Tarnok, Methods Cell Biol. 102, 1–21 (2011).
- [94] E. K. Zuba-Surma, M. Kucia, A. Abdel-Latif, J. W. Lillard, Jr., and M. Z. Ratajczak, Folia Histochem. Cytobiol. 45, 279–290 (2007).
- [95] K. E. McGrath, T. P. Bushnell, and J. Palis, J. Immunol. Methods 336, 91–97 (2008).
- [96] X. Li and Z. Darzynkiewicz, Exp. Cell Res. 249, 404–412 (1999).
- [97] T. W. Remmerbach, D. Meyer-Ebrecht, T. Aach, T. Würflinger, A. A. Bell, T. E. Schneider, N. Nietzke, B. Frerich, and A. Böcking, Cancer Cytopathol. 117, 228–235 (2009).
- [98] T. Würflinger, J. Stockhausen, D. Meyer-Ebrecht, and A. Böcking, Comput. Med. Imaging Graph. 28, 87–98 (2004).
- [99] W. Laffers, A. Mittag, D. Lenz, A. Tárnok, and A. O. H. Gerstner, Cytometry A 69A, 127–130 (2006).
- [100] T. Gaiser, L. Berroa-Garcia, R. Kemmerling, A. Dutta, T. Ried, and K. Heselmeyer-Haddad, Cell. Oncol. 34, 337–342 (2011).
- [101] K. Preston, Jr., J. Histochem. Cytochem. 34, 67–74 (1986).
- [102] M. Ingram and K. Preston, Jr., Sci. Am. 223, 72–82 (1970).
- [103] P. H. Bartels, G. B. Olson, J. M. Layton, R. E. Anderson, and G. L. Wied, Acta Cytol. 19, 53–57 (1975).
- [104] J. M. Prewitt and M. L. Mendelsohn, Ann. N. Y. Acad. Sci. 128, 1035–1053 (1966).
- [105] D. K. Green, Exp. Cell Res. 86, 170–174 (1974).
- [106] D. K. Green and P. W. Neurath, J. Histochem. Cytochem. 22, 531–535 (1974).
- [107] A. P. Verhest, in: G. L. Wied, P. H. Bartels, P. H. Rosenthal, and U. Schenck (eds.), Compendium on the Computerized Cytology and Histology Laboratory (Tutorials of Cytology, Chicago, 1994), pp. 278–283.
- [108] G. P. Vooijs, B. E. van't Hof Grootenboer, A. J. M. van Aspert van Erp, F. A. de Schipper, M. M. M. Pahlplatz, and T. G. J. M. Hanselaar, in: G. L. Wied, P. H. Bartels, P. H. Rosenthal, and U. Schenck (eds.), Compendium on the Computerized Cytology and Histology Laboratory (Tutorials of Cytology, Chicago, 1994), pp. 32–42.
- [109] G. F. Bahr, P. H. Bartels, M. Bibbo, M. De Nicolas, and G. L. Wied, Acta Cytol. 17, 106–112 (1973).
- [110] P. H. Bartels, M. Bibbo, G. F. Bahr, J. Taylor, and G. L. Wied, Acta Cytol. 17, 449–453 (1973).
- [111] P. H. Bartels and G. L. Wied, J. Histochem. Cytochem. 22, 660–662 (1974).
- [112] M. Bibbo, P. H. Bartels, G. F. Bahr, J. Taylor, and G. L. Wied, Acta Cytol. 17, 340–350 (1973).
- [113] G. G. Birdsong, Hum. Pathol. 27, 468–481 (1996).
- [114] J. Blomster and B. Stenkvist, Virchows Arch. B Cell Pathol. 20, 205–216 (1976).
- [115] G. Burger, U. Jutting, and K. Rodenacker, Anal. Quant. Cytol. 3, 261–271 (1981).
- [116] I. M. Dawson, C. P. Heanley, A. C. Heber-Percy, and J. K. Tylko, J. Clin. Pathol. 20, 724–730 (1967).
- [117] E. G. Diacumakos, E. Day, and M. J. Kopac, Ann. N. Y. Acad. Sci. 97, 498–513 (1962).
- [118] J. Holmquist, E. Bengtsson, O. Eriksson, B. Nordin, and B. Stenkvist, J. Histochem. Cytochem. 26, 1000–1017 (1978).
- [119] J. Holmquist, E. Bengtsson, B. Olsen, B. Stenkvist, and Y. Noguchi, Comput. Biol. Med. 6, 213–223 (1976).
- [120] G. W. McMaster, Acta Cytol. 12, 9–14 (1968).
- [121] R. C. Mellors and R. Silver, Science 114, 356–360 (1951).
- [122] L. H. Oliver, R. S. Poulsen, G. T. Toussaint, and C. Louis, Pattern Recognit. 11, 205–212 (1979).
- [123] S. A. Rosenberg, K. S. Ledeen, and T. Kline, Science 163, 1065–1067 (1969).
- [124] B. Stenkvist, R. Bergstrom, U. Brinne, I. Hesselius, A. Kiviranta, H. Nordgren, L. Schnurer, U. Stendahl, S. Stenson, J. Soderstrom, and C. S. Sorensen, Gynecol. Oncol. 27, 1–14 (1987).
- [125] N. Tanaka, H. Ikeda, T. Ueno, A. Mukawa, S. Watanabe, K. Okamoto, S. Hosoi, and S. Tsunekawa, Appl. Opt. 26, 3301–3307 (1987).
- [126] N. Tanaka, H. Ikeda, T. Ueno, S. Watanabe, and Y. Imasato, Acta Cytol. 21, 85–89 (1977).
- [127]
W. E. Tolles, W. J. Horvath, and R. C. Bostrom, Cancer 14, 455–468 (1961).
10.1002/1097-0142(199005/06)14:3<455::AID-CNCR2820140303>3.0.CO;2-5 CAS PubMed Web of Science® Google Scholar
- [128]
W. E. Tolles, W. J. Horvath, and R. C. Bostrom, Cancer 14, 437–454 (1961).
10.1002/1097-0142(199005/06)14:3<437::AID-CNCR2820140302>3.0.CO;2-4 CAS PubMed Web of Science® Google Scholar
- [129] J. H. Tucker, Comput. Biomed. Res. 9, 93–107 (1976).
- [130] J. Taylor, G. F. Bahr, P. H. Bartels, M. Bibbo, D. L. Richards, and G. L. Wied, Acta Cytol. 19, 289–298 (1975).
- [131] E. Bengtsson, O. Eriksson, J. Holmquist, and B. Stenkvist, Comput. Programs Biomed. 7, 233–246 (1977).
- [132] E. Bengtsson, J. Holmquist, B. Olsen, and B. Stenkvist, Comput. Programs Biomed. 6, 39–49 (1976).
- [133] J. V. Bacus, in: G. L. Wied, P. H. Bartels, P. H. Rosenthal, and U. Schenck (eds.), Compendium on the Computerized Cytology and Histology Laboratory (Tutorials of Cytology, Chicago, 1994), pp. 360–367.
- [134] L. G. Koss, P. H. Bartels, J. J. Sychra, and G. L. Wied, Acta Cytol. 22, 392–397 (1978).
- [135] L. G. Koss, P. H. Bartels, M. Bibbo, S. Z. Freed, J. Taylor, and G. L. Wied, Acta Cytol. 19, 378–391 (1975).
- [136] L. G. Koss, P. H. Bartels, and G. L. Wied, J. Urol. 123, 846–849 (1980).
- [137] L. J. Mango, Cancer Lett. 77, 155–162 (1994).
- [138] R. Ashfaq, F. Saliger, B. Solares, S. Thomas, G. Liu, Y. Liang, and M. H. Saboorian, Acta Cytol. 41, 1058–1064 (1997).
- [139] C. Bergeron, M. Masseroli, A. Ghezi, A. Lemarie, L. Mango, and L. G. Koss, Acta Cytol. 44, 151–157 (2000).
- [140] D. C. Wilbur and M. K. Norton, Epidemiology 13, S30–S33 (2002).
- [141] M. Schiffman and D. Solomon, JAMA 302, 1809–1810 (2009).
- [142] D. J. Zahniser, in: G. L. Wied, P. H. Bartels, P. H. Rosenthal, and U. Schenck (eds.), Compendium on the Computerized Cytology and Histology Laboratory (Tutorials of Cytology, Chicago, 1994), pp. 389–398.
- [143] A. G. Siebers, P. J. J. M. Klinkhamer, J. M. M. Grefte, L. F. A. G. Massuger, J. E. M. Vedder, A. Beijers-Broos, J. Bulten, and M. Arbyn, JAMA 302, 1757–1764 (2009).
- [144] M. Arbyn, C. Bergeron, P. Klinkhamer, P. Martin-Hirsch, A. G. Siebers, and J. Bulten, Obstet. Gynecol. 111, 167–177 (2008).
- [145] F. S. Miller, L. E. Nagel, and M. B. Kenny-Moynihan, Diagn. Cytopathol. 35, 213–217 (2007).
- [146] R. Lozano, Gynecol. Oncol. 104, 134–138 (2007).
- [147] C. V. Biscotti, A. E. Dawson, B. Dziura, L. Galup, T. Darragh, A. Rahemtulla, and L. Wills-Frank, Am. J. Clin. Pathol. 123, 281–287 (2005).
- [148] P. Kjellstrand, J. Microsc. 119, 391–396 (1980).
- [149] E. K. Schulte and D. H. Wittekind, Anal. Cell. Pathol. 2, 149–157 (1990).
- [150] A. Reith and H. Danielsen, in: G. L. Wied, P. H. Bartels, P. H. Rosenthal, and U. Schenck (eds.), Compendium on the Computerized Cytology and Histology Laboratory (Tutorials of Cytology, Chicago, 1994), pp. 185–193.
- [151] S. Biesterfeld, S. Beckers, M. Del Carmen Villa Cadenas, and M. Schramm, Anticancer Res. 31, 53–58 (2011).
- [152] G. Haroske, J. P. Baak, H. Danielsen, F. Giroud, A. Gschwendtner, M. Oberholzer, A. Reith, P. Spieler, and A. Bocking, Anal. Cell. Pathol. 23, 89–95 (2001).
- [153] C. Cohen, Hum. Pathol. 27, 482–493 (1996).
- [154] A. Böcking, C. P. Adler, H. H. Common, M. Hilgarth, B. Granzen, and W. Auffermann, Anal. Quant. Cytol. 6, 1–8 (1984).
- [155] A. Böcking, E. Striepecke, H. Auer, and L. Füzesi, in: G. L. Wied, P. H. Bartels, P. H. Rosenthal, and U. Schenck (eds.), Compendium on the Computerized Cytology and Histology Laboratory (Tutorials of Cytology, Chicago, 1994), pp. 107–128.
- [156] G. U. Auer, T. O. Caspersson, and A. S. Wallgren, Anal. Quant. Cytol. 2, 161–165 (1980).
- [157] H. Tong, R. Shen, Z. Wang, Y. Kan, Y. Wang, F. Li, F. Wang, J. Yang, X. Guo, and the Mass Cervical Cancer Screening Regimen Group, Clin. Cancer Res. 15, 6438–6445 (2009).
- [158] M. Guillaud, J. L. Benedet, S. B. Cantor, G. Staerkel, M. Follen, and C. MacAulay, Cancer 107, 309–318 (2006).
- [159] X. R. Sun, J. Wang, D. Garner, and B. Palcic, Cell. Oncol. 27, 33–41 (2005).
- [160] M. Lorenzato, S. Caudroy, J. M. Nou, V. Dalstein, K. Joseph, S. Bellefqih, A. Durlach, C. Thil, F. Dez, D. Bouttens, C. Clavel, and P. Birembaut, Cancer 114, 263–269 (2008).
- [161]
A. G. Hanselaar, G. P. Vooijs, P. S. Oud, M. M. Pahlplatz, and J. L. Beck, Cancer 62, 2537–2545 (1988).
10.1002/1097-0142(19881215)62:12<2537::AID-CNCR2820621215>3.0.CO;2-W CAS PubMed Web of Science® Google Scholar
- [162] A. G. Hanselaar, G. P. Vooijs, A. E. Van't Hof-Grootenboer, J. H. Gemmink, H. De Leeuw, and M. M. Pahlplatz, Cytometry 12, 1–9 (1991).
- [163] A. G. Hanselaar, G. P. Vooijs, A. E. Van't Hof-Grootenboer, and M. M. Pahlplatz, Cytometry 11, 901–906 (1990).
- [164] G. Mariuzzi, A. Santinelli, M. Valli, S. Sisti, R. Montironi, L. Mariuzzi, R. Alberti, and E. Pisani, Anal. Quant. Cytol. Histol. 14, 137–147 (1992).
- [165] A. Böcking, M. Hilgarth, W. Auffermann, C. Hack-Werdier, D. Fischer-Becker, and G. von Kalkreuth, Acta Cytol. 30, 608–615 (1986).
- [166] M. C. Tammemagi, S. C. Lam, A. M. McWilliams, and D. D. Sin, Cancer Prev. Res. (Phila) 4, 552–561 (2011).
- [167] S. Xing, B. Khanavkar, J. A. Nakhosteen, Z. Atay, K.-H. Jöckel, W. Marek, and the Research Institute for Diagnosis Treatment of Early Lung Cancer (RIDTELC) Lung Study Group, Eur. Respir. J. 25, 956–963 (2005).
- [168] M. Schramm, C. Wrobel, I. Born, M. Kazimirek, N. Pomjanski, M. William, R. Kappes, C. D. Gerharz, S. Biesterfeld, and A. Böcking, Cancer Cytopathol 119, 177–192 (2011).
- [169] W. Auffermann and A. Böcking, Anal. Quant. Cytol. Histol. 7, 218–226 (1985).
- [170] A. R. Santos-Silva, A. C. P. Ribeiro, A. M. P. Soubhia, G. I. Miyahara, R. Carlos, P. M. Speight, K. D. Hunter, A. Torres-Rendon, P. A. Vargas, and M. A. Lopes, Histopathology 58, 1127–1135 (2011).
- [171] J. F. Bremmer, R. H. Brakenhoff, M. A. Broeckaert, J. A. Beliën, C. R. Leemans, E. Bloemena, I. van der Waal, and B. J. Braakhuis, Oral Oncol. 47, 956–960 (2011).
- [172] T. W. Remmerbach, H. Weidenbach, N. Pomjanski, K. Knops, S. Mathes, A. Hemprich, and A. Böcking, Anal. Cell. Pathol. 22, 211–221 (2001).
- [173] B. Stenkvist and E. Olding-Stenkvist, Eur. J. Cancer 26, 261–267 (1990).
- [174] A. Zetterberg and G. Forsslund, Acta Oncol. 30, 193–199 (1991).
- [175] D. W. Hedley, M. L. Friedlander, I. W. Taylor, C. A. Rugg, and E. A. Musgrove, J. Histochem. Cytochem. 31, 1333–1335 (1983).
- [176] L. A. Boardman, R. A. Johnson, G. M. Petersen, A. L. Oberg, B. F. Kabat, J. P. Slusser, L. Wang, B. W. Morlan, A. J. French, T. C. Smyrk, N. M. Lindor, and S. N. Thibodeau, Clin. Cancer Res. 13, 2323–2328 (2007).
- [177] M. Iwaizumi, K. Shinmura, H. Mori, H. Yamada, M. Suzuki, Y. Kitayama, H. Igarashi, T. Nakamura, H. Suzuki, Y. Watanabe, A. Hishida, M. Ikuma, and H. Sugimura, Gut 58, 249–260 (2009).
- [178] M. M. Moura, B. M. Cavaco, A. E. Pinto, and V. Leite, J. Clin. Endocrinol. Metab. 96, E863–E868 (2011).
- [179] D. W. Hedley, Cytometry 10, 229–241 (1989).
- [180] D. W. Hedley, M. L. Friedlander, and I. W. Taylor, Cytometry 6, 327–333 (1985).
- [181] C. J. Cornelisse, C. J. van de Velde, R. J. Caspers, A. J. Moolenaar, and J. Hermans, Cytometry 8, 225–234 (1987).
- [182] P. V. Zimmerman, G. A. Hawson, M. H. Bint, and P. G. Parsons, Lancet 2, 530–533 (1987).
- [183] O. C. Gruner, Brit. J. Surg. 3, 506–525 (1916).
- [184] H. E. Nieburgs, Acta Cytol. 12, 445–453 (1968).
- [185] B. Palcic, D. M. Garner, J. Beveridge, X. R. Sun, A. Doudkine, C. MacAulay, S. Lam, and P. W. Payne, Cytometry 50, 168–176 (2002).
- [186] H. Klawe and J. Rowinski, Acta Cytol. 18, 30–33 (1974).
- [187] M. Us-Krasovec, J. Erzen, M. Zganec, M. Strojan-Flezar, J. Lavrencak, D. Garner, A. Doudkine, and B. Palcic, Anal. Quant. Cytol. Histol. 27, 254–262 (2005).
- [188] E. C. M. Mommers, N. Poulin, J. Sangulin, C. J. L. M. Meijer, J. P. A. Baak, and P. J. van Diest, J. Pathol. 193, 33–39 (2001).
- [189] G. Anderson, C. MacAulay, J. Matisic, D. Garner, and B. Palcic, Cytopathology 8, 298–312 (1997).
- [190] M. Guillaud, D. Cox, K. Adler-Storthz, A. Malpica, G. Staerkel, J. Matisic, D. Van Niekerk, N. Poulin, M. Follen, and C. MacAulay, Cytometry A 60A, 81–89 (2004).
- [191] D. M. Garner, A. Harrison, C. MacAulay, and B. Palcic, in: G. L. Wied, P. H. Bartels, P. H. Rosenthal, and U. Schenck (eds.), Compendium on the Computerized Cytology and Histology Laboratory (Tutorials of Cytology, Chicago, 1994), pp. 346–352.
- [192] B. Palcic and C. MacAulay, in: G. L. Wied, P. H. Bartels, P. H. Rosenthal, and U. Schenck (eds.), Compendium on the Computerized Cytology and Histology Laboratory (Tutorials of Cytology, Chicago, 1994), pp. 157–165.
- [193] N. K. Shirata, A. Longatto Filho, C. Roteli-Martins, L. M. Espoladore, J. E. Pittoli, and K. Syrjanen, Anal. Quant. Cytol. Histol. 25, 210–214 (2003).
- [194] M. Bibbo, F. Michelassi, P. H. Bartels, H. Dytch, C. Bania, E. Lerma, and A. G. Montag, Cancer Res. 50, 147–151 (1990).
- [195] A. G. Montag, P. H. Bartels, H. E. Dytch, E. Lerma-Puertas, F. Michelassi, and M. Bibbo, Anal. Quant. Cytol. Histol. 13, 159–167 (1991).
- [196] R. A. Kemp, D. M. Reinders, and B. Turic, J. Thorac. Oncol. 2, 993–1000 (2007).
- [197] P. W. Payne, T. J. Sebo, A. Doudkine, D. Garner, C. MacAulay, S. Lam, J. C. LeRiche, and B. Palcic, Mayo Clin. Proc. 72, 697–704 (1997).
- [198] C. F. Poh, C. E. MacAulay, D. M. Laronde, P. M. Williams, L. Zhang, and M. P. Rosin, Periodontol. 2000 57, 73–88 (2011).
- [199] M. Guillaud, K. Adler-Storthz, A. Malpica, G. Staerkel, J. Matisic, D. Van Niekirk, D. Cox, N. Poulin, M. Follen, and C. MacAulay, Gynecol. Oncol. 99, S16–S23 (2005).
- [200] M. E. Scheurer, M. Guillaud, G. Tortolero-Luna, C. McAulay, M. Follen, and K. Adler-Storthz, Cytometry B Clin. Cytom. 72, 324–331 (2007).
- [201] S. Lam, T. Kennedy, M. Unger, Y. E. Miller, D. Gelmont, V. Rusch, B. Gipe, D. Howard, J. C. LeRiche, A. Coldman, and A. F. Gazdar, Chest 113, 696–702 (1998).
- [202] M. Guillaud, J. C. le Riche, C. Dawe, J. Korbelik, A. Coldman, I. I. Wistuba, I.-W. Park, A. Gazdar, S. Lam, and C. E. MacAulay, Cytometry A 63, 34–40 (2005).
- [203] R. C. Winterhalder, F. R. Hirsch, G. K. Kotantoulas, W. A. Franklin, and P. A. Bunn, Jr., Ann. Oncol. 15, 185–196 (2004).
- [204] S. Lam, C. MacAulay, J. C. Le Riche, Y. Dyachkova, A. Coldman, M. Guillaud, E. Hawk, M. O. Christen, and A. F. Gazdar, J. Natl. Cancer Inst. 94, 1001–1009 (2002).
- [205] S. Lam, J. C. leRiche, A. McWilliams, C. MacAulay, Y. Dyachkova, E. Szabo, J. Mayo, R. Schellenberg, A. Coldman, E. Hawk, and A. Gazdar, Clin. Cancer Res. 10, 6502–6511 (2004).
- [206] T. Smitha, P. Sharada, and H. C. Girish, J. Oral Maxillofac. Pathol. 15, 26–33 (2011).
- [207] J. Song and C. R. Shea, Mod. Pathol. 23, 799–803 (2010).
- [208] S. S. Priya and S. Sundaram, J. Cytol. 28, 98–102 (2011).
- [209] H. G. Gratzner, I. T. Young, and S. E. Sher, J. Histochem. Cytochem. 27, 496–499 (1979).
- [210] P. Schätzle, R. Wuttke, U. Ziegler, and P. Sonderegger, J. Neurosci. Methods 204, 144–149 (2011).
- [211] D. S. Gross and J. M. Rothfeld, J. Histochem. Cytochem. 33, 11–20 (1985).
- [212] S. Natarajan, S. Mahajan, K. Boaz, and T. George, Indian J. Cancer 47, 406–411 (2010).
