J Gastric Cancer.  2013 Dec;13(4):214-225.

Test Execution Variation in Peritoneal Lavage Cytology Could Be Related to Poor Diagnostic Accuracy and Stage Migration in Patients with Gastric Cancer

Affiliations
  • 1Department of Surgery, Korea Cancer Center Hospital, Korea Institute of Radiological & Medical Sciences, Seoul, Korea. shjin@kcch.re.kr
  • 2Department of Surgery, Dongnam Institute of Radiological & Medical Sciences, Busan, Korea.
  • 3Department of Pathology, Korea Cancer Center Hospital, Korea Institute of Radiological & Medical Sciences, Seoul, Korea.
  • 4Department of Surgery, Konkuk University School of Medicine, Seoul, Korea.

Abstract

PURPOSE
Peritoneal lavage cytology is part of the routine staging workup for patients with advanced gastric cancer. However, no quality assurance study has been conducted to show variations or biases in peritoneal lavage cytology results. The aim of this study was to demonstrate a test execution variation in peritoneal lavage cytology between investigating surgeons.
MATERIALS AND METHODS
A prospective cohort study was designed for determination of the positive rate of peritoneal lavage cytology using a liquid-based preparation method in patients with potentially curable advanced gastric cancer (cT2~4/N0~2/M0). One hundred thirty patients were enrolled and underwent laparotomy, peritoneal lavage cytology, and standard gastrectomy, which were performed by 3 investigating surgeons. Data were analyzed using the chi-square test and a logistic regression model.
RESULTS
The overall positive peritoneal cytology rate was 10.0%. Subgroup positive rates were 5.3% in pT1 cancer, 2.0% in pT2/3 cancer, 11.1% in pT4a cancer, and 71.4% in pT4b cancer. In univariate analysis, positive peritoneal cytology showed significant correlation with pT stage, lymphatic invasion, vascular invasion, ascites, and the investigating surgeon. We found the positive rate to be 2.1% for surgeon A, 10.2% for surgeon B, and 20.6% for surgeon C (P=0.024). Multivariate analysis identified pT stage, ascites, and the investigating surgeon to be significant risk factors for positive peritoneal cytology.
CONCLUSIONS
The peritoneal lavage cytology results were significantly affected by the investigating surgeon, providing strong evidence of test execution variation that could be related to poor diagnostic accuracy and stage migration in patients with advanced gastric cancer.

Keyword

Cytology; Peritoneal lavage; Stomach neoplasms; Variation; Cytology

MeSH Terms

Ascites
Bias (Epidemiology)
Cohort Studies
Gastrectomy
Humans
Laparotomy
Logistic Models
Methods
Multivariate Analysis
Peritoneal Lavage*
Prospective Studies
Risk Factors
Stomach Neoplasms*

Figure

  • Fig. 1 A remarkable difference in positive cytology rates according to T stage in patients with advanced gastric cancer was noted between surgeon groups (P=0.024). The difference suggests a variation in sample collection between investigating surgeons and it can be related to poor diagnostic accuracy and stage migration in patients with advanced gastric cancer.


Reference

1. Ikeguchi M, Oka A, Tsujitani S, Maeta M, Kaibara N. Relationship between area of serosal invasion and intraperitoneal free cancer cells in patients with gastric cancer. Anticancer Res. 1994; 14:2131–2134.
2. Bando E, Yonemura Y, Takeshita Y, Taniguchi K, Yasui T, Yoshimitsu Y, et al. Intraoperative lavage for cytological examination in 1,297 patients with gastric carcinoma. Am J Surg. 1999; 178:256–262.
Article
3. Suzuki T, Ochiai T, Hayashi H, Hori S, Shimada H, Isono K. Peritoneal lavage cytology findings as prognostic factor for gastric cancer. Semin Surg Oncol. 1999; 17:103–107.
Article
4. Nakajima T, Harashima S, Hirata M, Kajitani T. Prognostic and therapeutic values of peritoneal cytology in gastric cancer. Acta Cytol. 1978; 22:225–229.
5. Iitsuka Y, Kaneshima S, Tanida O, Takeuchi T, Koga S. Intraperitoneal free cancer cells and their viability in gastric cancer. Cancer. 1979; 44:1476–1480.
Article
6. Funami Y, Tokumoto N, Miyauchi H, Ochiai T, Kuga K. Prognostic value of peritoneal lavage cytology and chemotherapy during surgery for advanced gastric cancer. Int Surg. 1999; 84:220–224.
7. Japanese Gastric Cancer Association. Japanese classification of gastric carcinoma - 2nd English edition -. Gastric Cancer. 1998; 1:10–24.
8. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A. AJCC cancer staging manual. 7th ed. New York: Springer;2010.
9. Shimada S, Tanaka E, Marutsuka T, Honmyo U, Tokunaga H, Yagi Y, et al. Extensive intraoperative peritoneal lavage and chemotherapy for gastric cancer patients with peritoneal free cancer cells. Gastric Cancer. 2002; 5:168–172.
Article
10. Yonemura Y, Bandou E, Sawa T, Yoshimitsu Y, Endou Y, Sasaki T, et al. Neoadjuvant treatment of gastric cancer with peritoneal dissemination. Eur J Surg Oncol. 2006; 32:661–665.
Article
11. Nakagawa S, Nashimoto A, Yabusaki H. Role of staging laparoscopy with peritoneal lavage cytology in the treatment of locally advanced gastric cancer. Gastric Cancer. 2007; 10:29–34.
Article
12. Kuramoto M, Shimada S, Ikeshima S, Matsuo A, Yagi Y, Matsuda M, et al. Extensive intraoperative peritoneal lavage as a standard prophylactic strategy for peritoneal recurrence in patients with gastric carcinoma. Ann Surg. 2009; 250:242–246.
Article
13. Fujiwara Y, Nishida T, Takiguchi S, Nakajima K, Miyata H, Yamasaki M, et al. Feasibility study of S-1 and intraperitoneal docetaxel combination chemotherapy for gastric cancer with peritoneal dissemination. Anticancer Res. 2010; 30:1335–1339.
14. Ishigami H, Kitayama J, Kaisaki S, Hidemura A, Kato M, Otani K, et al. Phase II study of weekly intravenous and intraperitoneal paclitaxel combined with S-1 for advanced gastric cancer with peritoneal metastasis. Ann Oncol. 2010; 21:67–70.
Article
15. Lorenzen S, Panzram B, Rosenberg R, Nekarda H, Becker K, Schenk U, et al. Prognostic significance of free peritoneal tumor cells in the peritoneal cavity before and after neoadjuvant chemotherapy in patients with gastric carcinoma undergoing potentially curative resection. Ann Surg Oncol. 2010; 17:2733–2739.
Article
16. Mezhir JJ, Shah MA, Jacks LM, Brennan MF, Coit DG, Strong VE. Positive peritoneal cytology in patients with gastric cancer: natural history and outcome of 291 patients. Ann Surg Oncol. 2010; 17:3173–3180.
Article
17. Greenhalgh T. How to read a paper. Papers that report diagnostic or screening tests. BMJ. 1997; 315:540–543.
Article
18. Hutchinson ML, Zahniser DJ, Sherman ME, Herrero R, Alfaro M, Bratti MC, et al. Utility of liquid-based cytology for cervical carcinoma screening: results of a population-based study conducted in a region of Costa Rica with a high incidence of cervical carcinoma. Cancer. 1999; 87:48–55.
Article
19. Abulafia O, Pezzullo JC, Sherer DM. Performance of ThinPrep liquid-based cervical cytology in comparison with conventionally prepared Papanicolaou smears: a quantitative survey. Gynecol Oncol. 2003; 90:137–144.
Article
20. Davey E, Barratt A, Irwig L, Chan SF, Macaskill P, Mannes P, et al. Effect of study design and quality on unsatisfactory rates, cytology classifications, and accuracy in liquid-based versus conventional cervical cytology: a systematic review. Lancet. 2006; 367:122–132.
Article
21. Hawkins DM, Garrett JA, Stephenson B. Some issues in resolution of diagnostic tests using an imperfect gold standard. Stat Med. 2001; 20:1987–2001.
Article
22. Whiting P, Rutjes AW, Reitsma JB, Glas AS, Bossuyt PM, Kleijnen J. Sources of variation and bias in studies of diagnostic accuracy: a systematic review. Ann Intern Med. 2004; 140:189–202.
Article
23. Viera AJ, Garrett JM. Understanding interobserver agreement: the kappa statistic. Fam Med. 2005; 37:360–363.
24. Dodd LG, Sneige N, Villarreal Y, Fanning CV, Staerkel GA, Caraway NP, et al. Quality-assurance study of simultaneously sampled, non-correlating cervical cytology and biopsies. Diagn Cytopathol. 1993; 9:138–144.
Article
25. Tritz DM, Weeks JA, Spires SE, Sattich M, Banks H, Cibull ML, et al. Etiologies for non-correlating cervical cytologies and biopsies. Am J Clin Pathol. 1995; 103:594–597.
Article
26. Regev A, Berho M, Jeffers LJ, Milikowski C, Molina EG, Pyrsopoulos NT, et al. Sampling error and intraobserver variation in liver biopsy in patients with chronic HCV infection. Am J Gastroenterol. 2002; 97:2614–2618.
Article
27. Cholongitas E, Senzolo M, Standish R, Marelli L, Quaglia A, Patch D, et al. A systematic review of the quality of liver biopsy specimens. Am J Clin Pathol. 2006; 125:710–721.
Article
28. Corkill M, Knapp D, Martin J, Hutchinson ML. Specimen adequacy of ThinPrep sample preparations in a direct-to-vial study. Acta Cytol. 1997; 41:39–44.
Article
29. Papanicolaou GN. Cytologic diagnosis of uterine cancer by examination of vaginal and uterine secretions. Am J Clin Pathol. 1949; 19:301–308.
Article
30. Marshall PN. Papanicolaou staining--a review. Microsc Acta. 1983; 87:233–243.
31. Jass JR, Smith M. Sialic acid and epithelial differentiation in colorectal polyps and cancer--a morphological, mucin and lectin histochemical study. Pathology. 1992; 24:233–242.
Article
32. Chuwa EW, Khin LW, Chan WH, Ong HS, Wong WK. Prognostic significance of peritoneal lavage cytology in gastric cancer in Singapore. Gastric Cancer. 2005; 8:228–237.
Article
33. Yamamoto M, Matsuyama A, Kameyama T, Okamoto M, Okazaki J, Utsunomiya T, et al. Prognostic re-evaluation of peritoneal lavage cytology in Japanese patients with gastric carcinoma. Hepatogastroenterology. 2009; 56:261–265.
34. Bando E, Yonemura Y, Taniguchi K, Fushida S, Fujimura T, Miwa K. Outcome of ratio of lymph node metastasis in gastric carcinoma. Ann Surg Oncol. 2002; 9:775–784.
Article
35. Ryu CK, Park JI, Min JS, Jin SH, Park SH, Bang HY, et al. The clinical significance and detection of intraperitoneal micrometastases by ThinPrep(R) cytology with peritoneal lavage fluid in patients with advanced gastric cancer. J Korean Gastric Cancer Assoc. 2008; 8:189–197.
Article
36. Nemes S, Jonasson JM, Genell A, Steineck G. Bias in odds ratios by logistic regression modelling and sample size. BMC Med Res Methodol. 2009; 9:56.
Article
37. Sobin LH, Wittekind C, editors. TNM: classification of malignant tumours. 6th ed. New York: Wiley-Liss;2002.
38. Wong JH, Johnson DS, Hemmings D, Hsu A, Imai T, Tominaga GT. Assessing the quality of colorectal cancer staging: documenting the process in improving the staging of node-negative colorectal cancer. Arch Surg. 2005; 140:881–886.
39. Jha MK, Corbett WA, Wilson RG, Koreli A, Papagrigoriadis S. Variance of surgeons versus pathologists in staging of colorectal cancer. Minerva Chir. 2006; 61:385–391.
40. Yoshikawa T, Sasako M, Sano T, Nashimoto A, Kurita A, Tsujinaka T, et al. Stage migration caused by D2 dissection with para-aortic lymphadenectomy for gastric cancer from the results of a prospective randomized controlled trial. Br J Surg. 2006; 93:1526–1529.
Article
41. Ayantunde AA, Parsons SL. Pattern and prognostic factors in patients with malignant ascites: a retrospective study. Ann Oncol. 2007; 18:945–949.
Article
42. Marutsuka T, Shimada S, Shiomori K, Hayashi N, Yagi Y, Yamane T, et al. Mechanisms of peritoneal metastasis after operation for non-serosa-invasive gastric carcinoma: an ultrarapid detection system for intraperitoneal free cancer cells and a prophylactic strategy for peritoneal metastasis. Clin Cancer Res. 2003; 9:678–685.
43. Nanda K, McCrory DC, Myers ER, Bastian LA, Hasselblad V, Hickey JD, et al. Accuracy of the Papanicolaou test in screening for and follow-up of cervical cytologic abnormalities: a systematic review. Ann Intern Med. 2000; 132:810–819.
Article
44. Burke EC, Karpeh MS Jr, Conlon KC, Brennan MF. Peritoneal lavage cytology in gastric cancer: an independent predictor of outcome. Ann Surg Oncol. 1998; 5:411–415.
Article
45. Kodera Y, Nakanishi H, Ito S, Yamamura Y, Kanemitsu Y, Shimizu Y, et al. Quantitative detection of disseminated free cancer cells in peritoneal washes with real-time reverse transcriptase-polymerase chain reaction: a sensitive predictor of outcome for patients with gastric carcinoma. Ann Surg. 2002; 235:499–506.
Article
46. Weiss L. Metastatic inefficiency. Adv Cancer Res. 1990; 54:159–211.
Article
47. Yonemura Y, Kawamura T, Bandou E, Tsukiyama G, Endou Y, Miura M. The natural history of free cancer cells in the peritoneal cavity. Recent Results Cancer Res. 2007; 169:11–23.
Article
48. Makino T, Fujiwara Y, Takiguchi S, Miyata H, Yamasaki M, Nakajima K, et al. The utility of pre-operative peritoneal lavage examination in serosa-invading gastric cancer patients. Surgery. 2010; 148:96–102.
Article
49. Kodera Y, Yamamura Y, Shimizu Y, Torii A, Hirai T, Yasui K, et al. Peritoneal washing cytology: prognostic value of positive findings in patients with gastric carcinoma undergoing a potentially curative resection. J Surg Oncol. 1999; 72:60–64.
Article
50. Bonenkamp JJ, Songun I, Hermans J, van de Velde CJ. Prognostic value of positive cytology findings from abdominal washings in patients with gastric cancer. Br J Surg. 1996; 83:672–674.
Article
51. Majima T, Ichikura T, Mochizuki H. Prognostic significance of the cytologic features of free cancer cells in the peritoneal cavity of patients with gastric cancer. Surg Today. 2002; 32:35–39.
Article
52. Miyashiro I, Takachi K, Doki Y, Ishikawa O, Ohigashi H, Murata K, et al. When is curative gastrectomy justified for gastric cancer with positive peritoneal lavage cytology but negative macroscopic peritoneal implant? World J Surg. 2005; 29:1131–1134.
Article
53. Inoue M, Tsugane S. Epidemiology of gastric cancer in Japan. Postgrad Med J. 2005; 81:419–424.
Article
54. Ahn HS, Lee HJ, Yoo MW, Jeong SH, Park DJ, Kim HH, et al. Changes in clinicopathological features and survival after gastrectomy for gastric cancer over a 20-year period. Br J Surg. 2011; 98:255–260.
Article
55. Mulherin SA, Miller WC. Spectrum bias or spectrum effect? Subgroup variation in diagnostic test evaluation. Ann Intern Med. 2002; 137:598–602.
Article
56. Strander B, Andersson-Ellström A, Milsom I, Rådberg T, Ryd W. Liquid-based cytology versus conventional Papanicolaou smear in an organized screening program: a prospective randomized study. Cancer. 2007; 111:285–291.
Article
57. Siebers AG, Klinkhamer PJ, Grefte JM, Massuger LF, Vedder JE, Beijers-Broos A, et al. Comparison of liquid-based cytology with conventional cytology for detection of cervical cancer precursors: a randomized controlled trial. JAMA. 2009; 302:1757–1764.
Article
58. Schiffman M, Solomon D. Screening and prevention methods for cervical cancer. JAMA. 2009; 302:1809–1810.
Article
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