Staging investigations for oesophageal cancer: a meta-analysis

E P M van Vliet, M H Heijenbrok-Kal, M G M Hunink, E J Kuipers, P D Siersema, E P M van Vliet, M H Heijenbrok-Kal, M G M Hunink, E J Kuipers, P D Siersema

Abstract

The aim of the study was to compare the diagnostic performance of endoscopic ultrasonography (EUS), computed tomography (CT), and 18F-fluoro-2-deoxy-D-glucose positron emission tomography (FDG-PET) in staging of oesophageal cancer. PubMed was searched to identify English-language articles published before January 2006 and reporting on diagnostic performance of EUS, CT, and/or FDG-PET in oesophageal cancer patients. Articles were included if absolute numbers of true-positive, false-negative, false-positive, and true-negative test results were available or derivable for regional, celiac, and abdominal lymph node metastases and/or distant metastases. Sensitivities and specificities were pooled using a random effects model. Summary receiver operating characteristic analysis was performed to study potential effects of study and patient characteristics. Random effects pooled sensitivities of EUS, CT, and FDG-PET for regional lymph node metastases were 0.80 (95% confidence interval 0.75-0.84), 0.50 (0.41-0.60), and 0.57 (0.43-0.70), respectively, and specificities were 0.70 (0.65-0.75), 0.83 (0.77-0.89), and 0.85 (0.76-0.95), respectively. Diagnostic performance did not differ significantly across these tests. For detection of celiac lymph node metastases by EUS, sensitivity and specificity were 0.85 (0.72-0.99) and 0.96 (0.92-1.00), respectively. For abdominal lymph node metastases by CT, these values were 0.42 (0.29-0.54) and 0.93 (0.86-1.00), respectively. For distant metastases, sensitivity and specificity were 0.71 (0.62-0.79) and 0.93 (0.89-0.97) for FDG-PET and 0.52 (0.33-0.71) and 0.91 (0.86-0.96) for CT, respectively. Diagnostic performance of FDG-PET for distant metastases was significantly higher than that of CT, which was not significantly affected by study and patient characteristics. The results suggest that EUS, CT, and FDG-PET each play a distinctive role in the detection of metastases in oesophageal cancer patients. For the detection of regional lymph node metastases, EUS is most sensitive, whereas CT and FDG-PET are more specific tests. For the evaluation of distant metastases, FDG-PET has probably a higher sensitivity than CT. Its combined use could however be of clinical value, with FDG-PET detecting possible metastases and CT confirming or excluding their presence and precisely determining the location(s).

Figures

Figure 1
Figure 1
Funnel plot in which the number of patients included in studies on the use of EUS for the detection of regional lymph node metastases was plotted against the log of the diagnostic odds ratio (D).
Figure 2
Figure 2
Funnel plot in which the number of patients included in studies on the use of CT for the detection of regional lymph node metastases was plotted against the log of the diagnostic odds ratio (D).
Figure 3
Figure 3
Summary receiver operating characteristic curves for EUS, FDG-PET, and CT for detection of regional lymph node metastases. P=not significant.
Figure 4
Figure 4
Summary receiver operating characteristic curves for FDG-PET and CT for detection of distant metastases. P<0.03.

References

    1. Becker CD, Barbier P, Porcellini B (1986) CT evaluation of patients undergoing transhiatal esophagectomy for cancer. J Comput Assist Tomogr 10: 607–611
    1. Binmoeller KF, Seifert H, Seitz U, Izbicki JR, Kida M, Soehendra N (1995) Ultrasonic esophagoprobe for TNM staging of highly stenosing esophageal carcinoma. Gastrointest Endosc 41: 547–552
    1. Block MI, Patterson GA, Sundaresan RS, Bailey MS, Flanagan FL, Dehdashti F, Siegel BA, Cooper JD (1997) Improvement in staging of esophageal cancer with the addition of positron emission tomography. Ann Thorac Surg 64: 770–776; discussion 776, 777
    1. Bossuyt PM, Reitsma JB, Bruns DE, Gatsonis CA, Glasziou PP, Irwig LM, Lijmer JG, Moher D, Rennie D, de Vet HC (2003) Towards complete and accurate reporting of studies of diagnostic accuracy: The STARD Initiative. Radiology 226: 24–28
    1. Botet JF, Lightdale CJ, Zauber AG, Gerdes H, Winawer SJ, Urmacher C, Brennan MF (1991) Preoperative staging of esophageal cancer: comparison of endoscopic US and dynamic CT. Radiology 181: 419–425
    1. Bowrey DJ, Clark GW, Roberts SA, Maughan TS, Hawthorne AB, Williams GT, Carey PD (1999) Endosonographic staging of 100 consecutive patients with esophageal carcinoma: introduction of the 8-mm esophagoprobe. Dis Esophagus 12: 258–263
    1. Catalano MF, Alcocer E, Chak A, Nguyen CC, Raijman I, Geenen JE, Lahoti S, Sivak Jr MV (1999) Evaluation of metastatic celiac axis lymph nodes in patients with esophageal carcinoma: accuracy of EUS. Gastrointest Endosc 50: 352–356
    1. Choi JY, Lee KH, Shim YM, Lee KS, Kim JJ, Kim SE, Kim BT (2000) Improved detection of individual nodal involvement in squamous cell carcinoma of the esophagus by FDG PET. J Nucl Med 41: 808–815
    1. DeWitt J, Kesler K, Brooks JA, LeBlanc J, McHenry L, McGreevy K, Sherman S (2005) Endoscopic ultrasound for esophageal and gastroesophageal junction cancer: impact of increased use of primary neoadjuvant therapy on preoperative locoregional staging accuracy. Dis Esophagus 18: 21–27
    1. Dittler HJ, Siewert JR (1993) Role of endoscopic ultrasonography in esophageal carcinoma. Endoscopy 25: 156–161
    1. Eloubeidi MA, Wallace MB, Reed CE, Hadzijahic N, Lewin DN, Van Velse A, Leveen MB, Etemad B, Matsuda K, Patel RS, Hawes RH, Hoffman BJ (2001) The utility of EUS and EUS-guided fine needle aspiration in detecting celiac lymph node metastasis in patients with esophageal cancer: a single-center experience. Gastrointest Endosc 54: 714–719
    1. Finch MD, John TG, Garden OJ, Allan PL, Paterson-Brown S (1997) Laparoscopic ultrasonography for staging gastroesophageal cancer. Surgery 121: 10–17
    1. Flamen P, Lerut A, Van Cutsem E, De Wever W, Peeters M, Stroobants S, Dupont P, Bormans G, Hiele M, De Leyn P, Van Raemdonck D, Coosemans W, Ectors N, Haustermans K, Mortelmans L (2000) Utility of positron emission tomography for the staging of patients with potentially operable esophageal carcinoma. J Clin Oncol 18: 3202–3210
    1. Flanagan FL, Dehdashti F, Siegel BA, Trask DD, Sundaresan SR, Patterson GA, Cooper JD (1997) Staging of esophageal cancer with 18F-fluorodeoxyglucose positron emission tomography. AJR Am J Roentgenol 168: 417–424
    1. Fleming ID, Cooper JS, Henson DE (1997) AJCC Cancer Staging Manual. Philadelphia: Lippincott-Raven Publishers
    1. Greenberg J, Durkin M, Van Drunen M, Aranha GV (1994) Computed tomography or endoscopic ultrasonography in preoperative staging of gastric and esophageal tumors. Surgery 116: 696–701; discussion 701, 702
    1. Grimm H, Binmoeller KF, Hamper K, Koch J, Henne-Bruns D, Soehendra N (1993) Endosonography for preoperative locoregional staging of esophageal and gastric cancer. Endoscopy 25: 224–230
    1. Halvorsen RA, Thompson WM (1984) Computed tomographic evaluation of esophageal carcinoma. Semin Oncol 11: 113–126
    1. Hasegawa N, Niwa Y, Arisawa T, Hase S, Goto H, Hayakawa T (1996) Preoperative staging of superficial esophageal carcinoma: comparison of an ultrasound probe and standard endoscopic ultrasonography. Gastrointest Endosc 44: 388–393
    1. Heeren PA, Jager PL, Bongaerts F, van Dullemen H, Sluiter W, Plukker JT (2004) Detection of distant metastases in esophageal cancer with (18)F-FDG PET. J Nucl Med 45: 980–987
    1. Hunerbein M, Dohmoto M, Rau B, Schlag PM (1996) Endosonography and endosonography-guided biopsy of upper-GI-tract tumors using a curved-array echoendoscope. Surg Endosc 10: 1205–1209
    1. Imdahl A, Hentschel M, Kleimaier M, Hopt UT, Brink I (2004) Impact of FDG-PET for staging of oesophageal cancer. Langenbecks Arch Surg 389: 283–288
    1. Kienle P, Buhl K, Kuntz C, Dux M, Hartmann C, Axel B, Herfarth C, Lehnert T (2002) Prospective comparison of endoscopy, endosonography and computed tomography for staging of tumours of the oesophagus and gastric cardia. Digestion 66: 230–236
    1. Kneist W, Schreckenberger M, Bartenstein P, Grunwald F, Oberholzer K, Junginger T (2003) Positron emission tomography for staging esophageal cancer: does it lead to a different therapeutic approach? World J Surg 27: 1105–1112
    1. Kneist W, Schreckenberger M, Bartenstein P, Menzel C, Oberholzer K, Junginger T (2004) Prospective evaluation of positron emission tomography in the preoperative staging of esophageal carcinoma. Arch Surg 139: 1043–1049
    1. Kole AC, Plukker JT, Nieweg OE, Vaalburg W (1998) Positron emission tomography for staging of oesophageal and gastroesophageal malignancy. Br J Cancer 78: 521–527
    1. Lerut T, Flamen P, Ectors N, Van Cutsem E, Peeters M, Hiele M, De Wever W, Coosemans W, Decker G, De Leyn P, Deneffe G, Van Raemdonck D, Mortelmans L (2000) Histopathologic validation of lymph node staging with FDG-PET scan in cancer of the esophagus and gastroesophageal junction: a prospective study based on primary surgery with extensive lymphadenectomy. Ann Surg 232: 743–752
    1. Lowe VJ, Booya F, Fletcher JG, Nathan M, Jensen E, Mullan B, Rohren E, Wiersema MJ, Vazquez-Sequeiros E, Murray JA, Allen MS, Levy MJ, Clain JE (2005) Comparison of positron emission tomography, computed tomography, and endoscopic ultrasound in the initial staging of patients with esophageal cancer. Mol Imaging Biol 7: 422–430
    1. Luketich JD, Friedman DM, Weigel TL, Meehan MA, Keenan RJ, Townsend DW, Meltzer CC (1999) Evaluation of distant metastases in esophageal cancer: 100 consecutive positron emission tomography scans. Ann Thorac Surg 68: 1133–1136; discussion 1136, 1137
    1. Luketich JD, Schauer PR, Meltzer CC, Landreneau RJ, Urso GK, Townsend DW, Ferson PF, Keenan RJ, Belani CP (1997) Role of positron emission tomography in staging esophageal cancer. Ann Thorac Surg 64: 765–769
    1. McAteer D, Wallis F, Couper G, Norton M, Welch A, Bruce D, Park K, Nicolson M, Gilbert FJ, Sharp P (1999) Evaluation of 18F-FDG positron emission tomography in gastric and oesophageal carcinoma. Br J Radiol 72: 525–529
    1. Natsugoe S, Yoshinaka H, Morinaga T, Shimada M, Baba M, Fukumoto T, Stein HJ, Aikou T (1996) Ultrasonographic detection of lymph-node metastases in superficial carcinoma of the esophagus. Endoscopy 28: 674–679
    1. Nesje LB, Svanes K, Viste A, Laerum OD, Odegaard S (2000) Comparison of a linear miniature ultrasound probe and a radial-scanning echoendoscope in TN staging of esophageal cancer. Scand J Gastroenterol 35: 997–1002
    1. Nishimaki T, Tanaka O, Ando N, Ide H, Watanabe H, Shinoda M, Takiyama W, Yamana H, Ishida K, Isono K, Endo M, Ikeuchi T, Mitomi T, Koizumi H, Imamura M, Iizuka T (1999) Evaluation of the accuracy of preoperative staging in thoracic esophageal cancer. Ann Thorac Surg 68: 2059–2064
    1. Parmar KS, Zwischenberger JB, Reeves AL, Waxman I (2002) Clinical impact of endoscopic ultrasound-guided fine needle aspiration of celiac axis lymph nodes (M1a disease) in esophageal cancer. Ann Thorac Surg 73: 916–920; discussion 920, 921
    1. Pedrazzani C, Bernini M, Giacopuzzi S, Pugliese R, Catalano F, Festini M, Rodella L, de Manzoni G (2005) Evaluation of Siewert classification in gastro-esophageal junction adenocarcinoma: what is the role of endoscopic ultrasonography? J Surg Oncol 91: 226–231
    1. Pham T, Roach E, Falk GL, Chu J, Ngu MC, Jones DB (1998) Staging of oesophageal carcinoma by endoscopic ultrasound: preliminary experience. Aust NZ J Surg 68: 209–212
    1. Quint LE, Glazer GM, Orringer MB, Gross BH (1985) Esophageal carcinoma: CT findings. Radiology 155: 171–175
    1. Quint LE, Hepburn LM, Francis IR, Whyte RI, Orringer MB (1995) Incidence and distribution of distant metastases from newly diagnosed esophageal carcinoma. Cancer 76: 1120–1125
    1. Rankin SC, Taylor H, Cook GJ, Mason R (1998) Computed tomography and positron emission tomography in the pre-operative staging of oesophageal carcinoma. Clin Radiol 53: 659–665
    1. Rasanen JV, Sihvo EI, Knuuti MJ, Minn HR, Luostarinen ME, Laippala P, Viljanen T, Salo JA (2003) Prospective analysis of accuracy of positron emission tomography, computed tomography, and endoscopic ultrasonography in staging of adenocarcinoma of the esophagus and the esophagogastric junction. Ann Surg Oncol 10: 954–960
    1. Rice TW, Boyce GA, Sivak MV (1991) Esophageal ultrasound and the preoperative staging of carcinoma of the esophagus. J Thorac Cardiovasc Surg 101: 536–543
    1. Richards DG, Brown TH, Manson JM (2000) Endoscopic ultrasound in the staging of tumours of the oesophagus and gastro-oesophageal junction. Ann R Coll Surg Engl 82: 311–317
    1. Salminen JT, Farkkila MA, Ramo OJ, Toikkanen V, Simpanen J, Nuutinen H, Salo JA (1999) Endoscopic ultrasonography in the preoperative staging of adenocarcinoma of the distal oesophagus and oesophagogastric junction. Scand J Gastroenterol 34: 1178–1182
    1. Shinkai M, Niwa Y, Arisawa T, Ohmiya N, Goto H, Hayakawa T (2000) Evaluation of prognosis of squamous cell carcinoma of the oesophagus by endoscopic ultrasonography. Gut 47: 120–125
    1. Sihvo EI, Rasanen JV, Knuuti MJ, Minn HR, Luostarinen ME, Viljanen T, Farkkila MA, Salo JA (2004) Adenocarcinoma of the esophagus and the esophagogastric junction: positron emission tomography improves staging and prediction of survival in distant but not in locoregional disease. J Gastrointest Surg 8: 988–996
    1. Sondenaa K, Skaane P, Nygaard K, Skjennald A (1992) Value of computed tomography in preoperative evaluation of resectability and staging in oesophageal carcinoma. Eur J Surg 158: 537–540
    1. Terrin N, Schmid CH, Lau J (2005) In an empirical evaluation of the funnel plot, researchers could not visually identify publication bias. J Clin Epidemiol 58: 894–901
    1. Thompson WM (1997) Esophageal carcinoma. Abdom Imaging 22: 138–142
    1. Tio TL, Coene PP, den Hartog Jager FC, Tytgat GN (1990) Preoperative TNM classification of esophageal carcinoma by endosonography. Hepatogastroenterology 37: 376–381
    1. Van Overhagen H, Lameris JS, Berger MY, Tilanus HW, Van Pel R, Klooswijk AI, Schutte HE (1993) Improved assessment of supraclavicular and abdominal metastases in oesophageal and gastro-oesophageal junction carcinoma with the combination of ultrasound and computed tomography. Br J Radiol 66: 203–208
    1. van Vliet EP, Eijkemans MJ, Poley JW, Steyerberg EW, Kuipers EJ, Siersema PD (2006) Staging of esophageal carcinoma in a low-volume EUS center compared with reported results from high-volume centers. Gastrointest Endosc 63: 938–947
    1. van Westreenen HL, Heeren PA, van Dullemen HM, van der Jagt EJ, Jager PL, Groen H, Plukker JT (2005) Positron emission tomography with F-18-fluorodeoxyglucose in a combined staging strategy of esophageal cancer prevents unnecessary surgical explorations. J Gastrointest Surg 9: 54–61
    1. van Westreenen HL, Westerterp M, Bossuyt PM, Pruim J, Sloof GW, van Lanschot JJ, Groen H, Plukker JT (2004) Systematic review of the staging performance of 18F-fluorodeoxyglucose positron emission tomography in esophageal cancer. J Clin Oncol 22: 3805–3812
    1. Vazquez-Sequeiros E, Norton ID, Clain JE, Wang KK, Affi A, Allen M, Deschamps C, Miller D, Salomao D, Wiersema MJ (2001) Impact of EUS-guided fine-needle aspiration on lymph node staging in patients with esophageal carcinoma. Gastrointest Endosc 53: 751–757
    1. Vazquez-Sequeiros E, Wiersema MJ, Clain JE, Norton ID, Levy MJ, Romero Y, Salomao D, Dierkhising R, Zinsmeister AR (2003) Impact of lymph node staging on therapy of esophageal carcinoma. Gastroenterology 125: 1626–1635
    1. Vickers J (1998) Role of endoscopic ultrasound in the preoperative assessment of patients with oesophageal cancer. Ann R Coll Surg Engl 80: 233–239
    1. Watt I, Stewart I, Anderson D, Bell G, Anderson JR (1989) Laparoscopy, ultrasound and computed tomography in cancer of the oesophagus and gastric cardia: a prospective comparison for detecting intra-abdominal metastases. Br J Surg 76: 1036–1039
    1. Wren SM, Stijns P, Srinivas S (2002) Positron emission tomography in the initial staging of esophageal cancer. Arch Surg 137: 1001–1006; discussion 1006, 1007
    1. Wu LF, Wang BZ, Feng JL, Cheng WR, Liu GR, Xu XH, Zheng ZC (2003) Preoperative TN staging of esophageal cancer: comparison of miniprobe ultrasonography, spiral CT and MRI. World J Gastroenterol 9: 219–224
    1. Yoon YC, Lee KS, Shim YM, Kim BT, Kim K, Kim TS (2003) Metastasis to regional lymph nodes in patients with esophageal squamous cell carcinoma: CT vs FDG PET for presurgical detection prospective study. Radiology 227: 764–770
    1. Yoshikane H, Tsukamoto Y, Niwa Y, Goto H, Hase S, Shimodaira M, Maruta S, Miyata A, Yoshida M (1994) Superficial esophageal carcinoma: evaluation by endoscopic ultrasonography. Am J Gastroenterol 89: 702–707
    1. Ziegler K, Sanft C, Zeitz M, Friedrich M, Stein H, Haring R, Riecken EO (1991) Evaluation of endosonography in TN staging of oesophageal cancer. Gut 32: 16–20

Source: PubMed

3
Subscribe