Skip to main content
SpringerLink
Log in

Esophageal squamous cell carcinoma: Pathology and prognosis

  • Published:
World Journal of Surgery Aims and scope Submit manuscript

Abstract

Between 1985 and 1992 a total of 403 patients with resected thoracic esophageal squamous cell carcinoma were evaluated histopathologically, and various pathologic findings related to survival were examined. Concerning depth of tumor invasion, 8 (2%) cases were pTis, 110 (27%) were pT1, 48 (12%) were pT2, 202 (50%) were pT3, and 35 (9%) were pT4. Lymphatic invasion was detected in 299 cases (74%), blood vessel invasion in 200 cases (49%), intramural metastasis in 45 (11%), and lymph node metastasis in 232 (58%). In pT1 carcinoma cases, 4% of mucosal carcinomas and 30% of submucosal carcinomas had lymph node metastasis. Tumors with deeper invasion had a higher incidence of lymph node metastasis: 74% of pT3 carcinomas and 83% of pT4 carcinomas. The sites of lymph node metastasis were divided into mediastinal, cervical, and abdominal fields; and rates of lymph node metastasis were 49%, 14%, and 41%, respectively. In all resected cases, the operative mortality rate was 3.2%, and the overall 5-year survival rate was 44.8%. The 5-year survival rate of patients with curative resection (R0 and R1) was 49.5%, whereas patients with palliative resection (R2) did not survive more than 3 years. There was no significant difference in survival relative to tumor location. In curatively resected cases, the significant prognostic factors by multivariate analysis were pT category, vascular invasion, lymph node metastasis, and intramural metastasis. Prognosis of lymph node-positive cases did not depend on the positive node site. Patients with only one positive node had a better prognosis, and those with six or more positive nodes had a poor prognosis. Concerning lymph node metastasis, other factors that worsened prognosis were a positive node larger than 1 cm, two- to three-field metastasis, and positive cervical nodes in cases of lower-third esophageal carcinoma.

Résumé

Entre 1985 et 1992, 403 patients ayant eu une résection de leur cancer épidermoïde de l'oesophage thoracique ont eu une évaluation histopathologique corrélée avec la survie. En ce qui concerne la profondeur de l'invasion, huit cas (2%) étaient des pTis, 110 (38%) étaient des pT1, 48 (12%) étaient des pT2, 202 (50%) étaient des pT3, et 35 (8%) étaient des pT4. L'atteinte lymphatique a été détectée chez 299 (74%) patients, une invasion vasculaire dans 200 (49%) des cas, une résurgence intramurale dans 45 (11%) des cas et une atteìnte ganglionnaire chez 232 (58%) des cas. Dans le cas des tumeurs pT1, 4% des cancers de la muqueuse, et 30% des cancers de la sous-muqueuse étaient accompagnées de métastases ganglionnaires. Des tumeurs ayant une invasion plus profonde, les pT3 et les pT4 étaient associées à des métastases ganglionnaires dans 74% et 83% des cas. Les sites des métastases ganglionnaires étaient le médiastin, les chaînes cervicales, et l'abdomen chez, respectivement, 49%, 14% et 41% des cas. Parmi les cas de résection, la mortalité opératoire était de 3.2% et la survie globale à 5 ans étaient de 44.8%. La survie à 5 ans des patients ayant eu une résection à visée curative (R0 et R1) était de 49.5% alors qu'aucun des patients ayant eu une résection palliative (R2) n'étaient en vie à 3 ans. Il n'y avait aucune différence de survie selon la localisation tumorale. Chez les patients réséqués de façon curative, les facteurs pronostiques significatifs étaient la classe pT, l'invasion vasculaire, la métastase lymphatique, et l'invasion intramurale. Le pronostic des patients ayant une métastase ganglionnaire était indépendant de la localisation. Le pronostic des patients ayant un seul ganglion envahi était meilleur que le pronostic des patients ayant six ou plus de ganglions envahis. Le pronostic était moins bon lorsque la métastase ganglionnaire était plus grande que 1 cm, intéressait plus de 2–3 champs différents et lorsqu'elle intéressait la chaîne cervicale en cas de cancer du tiers inférieur de l'oesophage.

Resumen

Se analizaron desde el punto de vista histopatológico 403 pacientes, 348 hombres y 55 mujeres, sometidos a resección de carcinoma escamocelular del esófago torácico en el período 1985 a 1992, y se examinaron diversos hallazgos patológicos en relación a sobrevida. En cuanto a profundidad de invasión tumoral, 8(2%) casos fueron Tis, 110(38%) p T1, 48(12%) p T2, 202(50%) p T3 y 35(8%) p T4. Se detectó invasión linfática en 299 casos (74%), invasión de vasos sanguíneos en 200 (49%), metástasis intramurales en 45(11%) y metástasis ganglionares en 232 (58%). Entre los casos en estado p T1, 4% de los carcinomas mucosos y 30% de los submucosos tenían metástasis ganglionares.

Los tumores con invasión más profunda exhibieron una mayor incidencia de metástasis ganglionares, 74% en los pacientes en estado pT3 y 83% en los estados pT4. La ubicación de las metástasis ganglionares fue dividida en tres campos: mediastinal, cervical y abdominal, y las ratas de metástasis ganglionares correspondientes fueron 49%, 14%, y 41%. La tasa de mortalidad operatoria fue 3.2% y la tasa global de sobrevida a 5 años fue 44.8%; para los casos con resección curativa (R0 y R1) ésta fue de 49.5%, en tanto que ninguno de los pacientes con resección paliative (R2) sobrevivió más allá de 3 años no se hallaron diferencias significativas en lo relativo a ubicación del cáncer.

En los pacientes con resección curativa, los factores pronóstico de importancia significativa determinados por análisis multivariado fueron el estado pT, la invasión vascular, las metástasis ganglionares y las metástasis intramurales. El pronóstico en los pacientes con ganglios positivos no dependió de la ubicación de los ganglios afectados, y los pacientes con sólo un ganglio afectado tuvieron un mejor pronóstico, en tanto que aquellos con 6 o más ganglios afectados tuvieron un pronóstico pobre.

En lo relativo a las metástasis ganglionares, otros factores que ensombrecieron el pronóstico fueron los ganglios mayores de 1 cm, metástasis a 2–3 campos y ganglios cervicales positivos cuando el carcinoma primario era del tercio inferior del esófago.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Li, R., Lu, Y., Chen, H., Gu, Y., Yang, J., Hu, J.: Late results of surgical treatment in esophageal carcinoma and factors influencing prognosis. Chin. Med. J. 94:729, 1981

    Google Scholar 

  2. Dark, J.F., Mousalli, H., Vaughan, R.: Surgical treatment of the esophagus. Thorax 36:891, 1981

    Google Scholar 

  3. Endo, M., Kinoshita, Y., Yamada, A., Ide, H., Nakayama, K.: Surgical treatment of esophageal cancer including clinical evaluation of early esophageal cancer. In Cancer of the esophagus (Vol. 2), C.J. Pfeiffer, editor. Boca Raton, FL, CRC Press, 1982, pp. 57–69

    Google Scholar 

  4. Launois, B., Paul, J.L., Lygidakis, N.J., et al.: Results of surgical treatment of carcinoma of the esophagus. Surg. Gynecol. Obstet. 156:753, 1983

    Google Scholar 

  5. Ellis, F.H., Gibb, S.P., Watkins, E.: Esophagectomy, a safe, widely applicable, and expeditious form of palliation for patients with carcinoma of the esophagus and cardia. Ann. Surg. 198:531, 1983

    Google Scholar 

  6. Wang, P., Chein, K.: Surgical treatment of carcinoma of the esophagus and cardia among the Chinese. Ann. Thorac. Surg. 35:143, 1983

    Google Scholar 

  7. Iizuka, T., Isono, K., Kakegawa, T., Watanabe, H.: Parameter linked to ten-year survival in Japan of resected esophageal carcinoma. Chest 96:1005, 1989

    Google Scholar 

  8. Fekete, F., Gayet, F., Langonnet, F., Lemee, J.: Radicality in esophageal cancer surgery. Ital. J. Surg. Sci. 17:15, 1987

    Google Scholar 

  9. Malliet, P., Baulieux, J., Boulez, J., Benheim, R.: Carcinoma of the thoracic esophagus, results of one-stage surgery (271 cases). Am. J. Surg. 143:629, 1982

    Google Scholar 

  10. Pasterino, U., Varente, M., Alloisio, M., et al.: Current results of esophageal cancer surgery time survival. Tumori 73:139, 1987

    Google Scholar 

  11. Akiyama, H., Turumaru, M., Kawamura, T., Ono, Y.: Principles of surgical treatment for carcinoma of the esophagus, analysis of lymph node involvement. Ann. Surg. 194:438, 1981

    Google Scholar 

  12. Ishida, K., Mori, S., Okamoto, K., et al.: Results of extended dissection of lymph nodes in operation for thoracic esophageal cancer. In Disease of the Esophagus, J.R. Siewert, A.H. Holscher, editors. New York, Springer, 1987, pp. 694–696

    Google Scholar 

  13. Turumaru, M., Akiyama, H., Udagawa, H., Ono, Y., Suzuki, M., Watanabe, G.: Cervical-thoracic-abdominal lymph node dissection for intrathoracic esophageal carcinoma. In Diseases of the Esophagus. Vol. I. Malignant Disease. M.K. Ferguson, A.G. Little, D.B. Skinner, editors. Mount Kisco, N.Y., Futura, 1990, pp. 187–186

    Google Scholar 

  14. Akiyama, H., Turumaru, M., Ono, Y., Udagawa, H., Kajiyama, Y.: Background of lymph node dissection for squamous cell carcinoma of the esophagus. In Color Atlas of Surgical Anatomy for Esophageal Cancer, T. Sato, T. Iizuka, editors. Tokyo, Springer, 1991, pp. 9–23

    Google Scholar 

  15. Kato, H., Tachimori, Y., Watanabe, H., et al.: Lymph node metastasis in thoracic esophageal carcinoma. J. Surg. Oncol. 48: 106, 1991

    Google Scholar 

  16. Kato, H., Watanabe, H., Tachimori, Y., Iizuka, T.: Evaluation of neck lymph node dissection for thoracic esophageal carcinoma. Ann. Thorac. Surg. 51:931, 1991

    Google Scholar 

  17. Sugimachi, K., Kitamura, K., Masuda, H., Mori, M., Kuwano, H., Ide, H.: Proposed new criteria for early carcinoma of the esophagus. Surg. Gynecol. Obstet. 173:303, 1991

    Google Scholar 

  18. Ide, H., Nogami, A., Hanashi, T., et al.: A clinical study on prognosis of submucosal esophageal cancer. Stomach Intestine 25:1067, 1990 [in Japanese]

    Google Scholar 

  19. Murata, Y., Yoshida, M., Ide, H., Suzuki, S., Yamada, A.: Preoperative staging of thoracic esophageal cancer by ultrasonography according to the new TNM classification. In Diseases of the Esophagus, J.R. Siewert, A.H. Holscher, editors. New York, Springer, 1987, pp. 135–144

    Google Scholar 

  20. Ide, H., Hanyu, F., Murata, Y., Kobayashi, A., Yamada, A., Kobayashi, S.: Extended dissection for thoracic esophageal cancer based on preoperative staging. In Diseases of the Esophagus. Vol. I. Malignant Disease. M.K. Ferguson, A.G. Little, D.B. Skinner, editors. Mount Kisco, N.Y., Futura, 1990, pp. 177–179

    Google Scholar 

  21. UICC International Union Against Cancer: TNM Classification of Malignant Tumours (4th ed.). Berlin, Springer-Verlag, 1987, pp. 40–42

    Google Scholar 

  22. Kaplan, E.L., Meier, P.: Nonparametric estimation for incomplete observations. J. Am. Stat. Assoc. 53:457, 1958

    Google Scholar 

  23. Cox, D.R.: Regression models and life tables. J.R. Stat. Soc. 34:187, 1972

    Google Scholar 

  24. Wong, J.: Esophageal resection for cancer: the rationale of current practice. Am. J. Surg. 53:18, 1987

    Google Scholar 

  25. Huang, J., Lin, S.K.: Prognostic significance of lymph node metastasis in surgical resection of esophageal carcinoma. In Diseases of the Esophagus. Vol. I. Malignant Disease. M.K. Ferguson, A.G. Little, D.B. Skinner, editors. Mount Kisco, N.Y., Futura, 1990, pp. 213–218

    Google Scholar 

  26. Bardini, R., Castro, C., Sorrentino, P., et al.: Prognostic factors for squamous cell carcinoma of the thoracic esophagus after curative resection. In Diseases of the Esophagus. Vol. I. Malignant Disease. M.K. Ferguson, A.G. Little, D.B. Skinner, editors. Mount Kisco, N.Y., Futura, 1990, pp. 219–228

    Google Scholar 

  27. Edwards, J.M., Hiller, V.F., Lawson, R.A.M., Moussalli, H., Hasleton, P.S.: Squamous carcinoma of the esophagus, histological criteria and their prognostic significance. Cancer 59:429, 1989

    Google Scholar 

  28. Theunissen, P.H.M.H., Borchard, E., Poortviliet, D.C.J.: Histopathological evaluation of oesophageal carcinoma, the significance of venous invasion. Br. J. Surg. 78:930, 1991

    Google Scholar 

  29. Yoshinaka, H., Shimazu, H., Fukumoto, T., Baba, M.: Superficial esophageal carcinoma, a clinicopathological review of 59 cases. Am. J. Gastroenterol. 86:1413, 1991

    Google Scholar 

  30. Bogomoletz, W.V., Molas, G., Gayet, B., Potet, F.: Superficial squamous cell carcinoma of the esophagus, a report of 76 cases and review of literature. Am. J. Surg. Pathol. 13:535, 1989

    Google Scholar 

  31. Goseki, N., Koike, M., Yoshida, M.: Histologic characteristics of early stage esophageal carcinoma, a comparative study with gastric carcinoma. Cancer 69:1088, 1992

    Google Scholar 

  32. Kato, H., Tachimori, Y., Watanabe, H., Yamaguchi, H., Ishikawa, T., Itabashi, M.: Superficial esophageal carcinoma, surgical treatment and the results. Cancer 66:2319, 1990

    Google Scholar 

  33. Kato, H., Tachimori, Y., Watanabe, H., et al.: Intramural metastasis of thoracic esophageal carcinoma. Int. J. Cancer 50:49, 1992

    Google Scholar 

  34. Skinner, D.B., Furgason, M.K., Little, A.G.: Selection of operation for esophageal cancer based on staging. Ann. Surg. 204:391, 1986

    Google Scholar 

  35. Sugimachi, K., Ide, H., Okamura, T., Matsuura, H., Endo, M., Inokuchi, K.: Cytophotometric DNA analysis of mucosal and submucosal carcinoma of the esophagus. Cancer 53:2683, 1984

    Google Scholar 

  36. Matsuura, H., Sugimachi, K., Ueo, H., Kuwano, H., Koga, Y., Okamua, T.: Malignant potentiality of squamous cell carcinoma of the esophagus predictable by DNA analysis. Cancer 57:1801, 1986

    Google Scholar 

  37. Nakamura, T.: Analysis of the malignant potentiality in superficial esophageal carcinoma by cytofluorometry of nuclear DNA and cellular protein contents. Nihon Kyobu Geka Gakkai Zasshi 40: 242, 1992 [in Japanese]

    Google Scholar 

  38. Roul, A., Segalin, A., Panozzo, M., et al.: Flow cytometric DNA analysis of squamous cell carcinoma of the esophagus. Cancer 65:1185, 1990

    Google Scholar 

  39. Kaketani, K., Saito, T., Kobayashi, M.: Flow cytometric analysis of nuclear DNA content in esophageal cancer. Cancer 64:887, 1989

    Google Scholar 

  40. Rikitake, H.: Studies on DNA content in ploidy patterns of esophageal cancer. Nihon Geka Gakkai Zasshi 91:564, 1989 [in Japanese]

    Google Scholar 

  41. Hasegawa, M.: Cytodynamic evaluation on the relationship between the mode of intracellular DNA content and the prognosis of esophageal cancer patients. Nihon Geka Gakkai Zasshi 91:191, 1990 [in Japanese]

    Google Scholar 

  42. Edwards, S.M., Jones, D.J., Wilkes, S.J.L., Hillier, V.F., Hasleton, P.S.: Ploidy as a prognostic indicator in esophageal squamous carcinoma and its relationship to various histological criteria. J. Pathol. 159:35, 1989

    Google Scholar 

  43. Robey-Caffetry, S.S., El-Naggar, A.K., Sahin, A.A., Bruner, J.M., Ro, J.Y., Cleary, K.R.: Prognostic factors in esophageal squamous carcinoma. Am. J. Clin. Pathol. 95:844, 1991

    Google Scholar 

  44. Partil, P., Redkar, A., Patel, S.G., et al.: Prognosis of operable squamous cell carcinoma of the esophagus. Cancer 72:20, 1993

    Google Scholar 

  45. Sasaki, K., Murakami, T., Murakami, T., Nakamura, M.: Intratumoral heterogeneity in DNA ploidy squamous cell carcinoma. Cancer 68:2403, 1991

    Google Scholar 

  46. Hall, P.A., Levision, D.A., Woods, A.L., et al.: Proliferating nuclear antigen (PCNA) immunolocalization in paraffin sections: an index of cell proliferation with evidence of deregulated expression in some neoplasms. J. Pathol. 162:285, 1990

    Google Scholar 

  47. Morita, M., Kuwano, H., Matsuda, H., Moriguchi, S., Sugimachi, K.: Prognostic significance of argyrophilic nuclear organizer regions in esophageal carcinoma. Cancer Res. 51:5339, 1991

    Google Scholar 

  48. Mori, M., Shimono, R., Kido, A., Kuwano, H., Akazawa, K., Sugimachi, K.: Distribution of basement membrane antigens in human esophageal lesions: a immunochemical study. Int. J. Cancer 47:839, 1991

    Google Scholar 

  49. Shima, I., Sasaguri, Y., Kusukawa, J., et al.: Production of matrix metalloproteinase-2 and metalloproteinase-3 related to malignant behavior of esophageal carcinoma. Cancer 70:2747, 1992

    Google Scholar 

  50. Shiozaki, H., Tahara, H., Oka, H., et al.: Expression of immunoreactive E-cadherin adhesion molecules in human cancers. Am. J. Pathol. 139:17, 1991

    Google Scholar 

  51. Kitagawa, Y., Ueda, M., Ando, N., Shinozawa, Y., Shimizu, N., Abe, O.: Significance of int-2/hst-1 coamplification as a prognostic factor in patients with esophageal squamous carcinoma. Cancer Res. 51:1504, 1991

    Google Scholar 

  52. Jiang, W., Kahn, S.M., Tomita, N., Zhang, Y.J., Lu, S.H., Weinstein, I.B.: Amplification and expression of the human cyclin D gene in esophageal cancer. Cancer Res. 52:2980, 1992

    Google Scholar 

  53. Mukaida, H., Toi, M., Hirai, T., Yamashita, Y., Toge, T.: Clinical significance of the expression of epidermal growth factor and its receptor in esophageal cancer. Cancer 68:142, 1991

    Google Scholar 

  54. Hollstein, M.C., Smits, A.M., Galiana, C., et al.: Amplication of epidermal growth factor receptor gene but no evidence of ras mutations in primary human esophageal cancer. Cancer Res. 48: 5119, 1988

    Google Scholar 

  55. Miyazaki, S., Sasano, H., Shiga, K., et al.: Analysis of c-myc oncogene in human esophageal carcinoma: immunohistochemistry, in situ hybridization and northern and southern blot studies. Anticancer Res. 12:1747, 1992

    Google Scholar 

  56. Meltzer, S.J., Yin, J., Huang, Y., et al.: Reduction to homozygosity involving p53 in esophageal cancers demonstrated by the polymerase chain reaction. Proc. Natl. Acad. Sci. U.S.A. 88:4976, 1991

    Google Scholar 

  57. Hollstein, M.C., Metcalf, R.A., Welsh, J.A., Montesano, R., Harris, C.C.: Frequent mutation of the p53 gene in human esophageal cancer. Proc. Natl. Acad. Sci. U.S.A. 87:9958, 1990

    Google Scholar 

  58. Ssano, H., Goukon, Y., Nishihira, T., Nagura, H.: In situ hybridization and immunohistochemistry of p53 tumor suppressor gene in human esophageal carcinoma. Am. J. Pathol. 141:545, 1992

    Google Scholar 

  59. Boynton, R.F., Blount, P.L., Yin, J., et al.: Loss of heterozygosity involving the APC and MCC genetic loci occurs in the majority of human esophageal cancers. Proc. Natl. Acad. Sci. U.S.A. 89:3385, 1992

    Google Scholar 

  60. Inoue, H., Endo, M., Takeshita, K., Yoshino, K., Muraoka, Y., Yoneshima, H.: A new simplified technique of endoscopic esophageal mucosal resection using a cap-fitted panendoscope (EMRC). Surg. Endosc. 6:264, 1992

    Google Scholar 

  61. Makuuchi, H., Matimura, K., Mizutani, K., et al.: Endoscopic mucosal resection for early esophageal cancer by EEMR-tube method. Stomach Intestine 28:153, 1993 [in Japanese]

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Surgery, Institute of Gastroenterology, Tokyo Women's Medical College, 8-1 Kawada-cho, Shinjuku-ku, 162, Tokyo, Japan

    Hiroko Ide M.D., Ph.D., Tsutomu Nakamura M.D., Ph.D., Kazuhiko Hayashi M.D., Takeshi Endo M.D., Ph.D., Ataru Kobayashi M.D., Reiki Eguchi M.D., Ph.D. & Fujio Hanyu M.D., Ph.D.

Authors
  1. Hiroko Ide M.D., Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tsutomu Nakamura M.D., Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kazuhiko Hayashi M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Takeshi Endo M.D., Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ataru Kobayashi M.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Reiki Eguchi M.D., Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Fujio Hanyu M.D., Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ide, H., Nakamura, T., Hayashi, K. et al. Esophageal squamous cell carcinoma: Pathology and prognosis. World J. Surg. 18, 321–330 (1994). https://doi.org/10.1007/BF00316810

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00316810

Keywords

Search

Navigation