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Value of Contrast-Enhanced Ultrasonography in the Differential Diagnosis of Enlarged Lymph Nodes: a Meta-Analysis of Diagnostic Accuracy Studies

  • Jin, Ya (Department of Ultrasound in West China Hospital) ;
  • He, Yu-Shuang (Department of Ultrasound in West China Hospital) ;
  • Zhang, Ming-Ming (The Center of Evidence-Based Medicine in West China Hospital, University of Sichuan) ;
  • Parajuly, Shyam Sundar (Department of Ultrasound, Paropakar Maternity and Children Hospital) ;
  • Chen, Shuang (Department of Ultrasound in West China Hospital) ;
  • Zhao, Hai-Na (Department of Ultrasound in West China Hospital) ;
  • Peng, Yu-Lan (Department of Ultrasound in West China Hospital)
  • Published : 2015.04.03

Abstract

Objective: To evaluate the diagnostic accuracy of contrast-enhanced ultrasonography (CEUS) in differentiating between benign and malignant enlarged lymph nodes using meta-analysis. Materials and Methods: Pubmed, Embase, SCI and Cochrane databases were searched for studies (up to September 1, 2014) reporting the diagnostic performance of CEUS in discriminating between benign and malignant lymph nodes. Inclusion criteria were: prospective study; histopathology as the reference standard; and sufficient data to construct $2{\times}2$ contingency tables. Methodological quality was assessed using Quality Assessment of Diagnostic Accuracy Studies-2 (QUADAS-2). Patient clinical characteristics, sensitivity and specificity were extracted. The summary receiver operating characteristic curve was used to examine the accuracy of CEUS. A meta-analysis was performed to evaluate the clinical utility in identification of benign and malignant lymph nodes. Sensitivity analysis was performed after omitting outliers identified in a bivariate boxplot and publication bias was assessed with Egger testing. Results: The pooled sensitivity, specificity and AUROC were 0.92 (95%CI, 0.85-0.96), 0.91 (95%CI, 0.82-0.95) and 0.97 (95%CI, 0.95-0.98), respectively. After omitting 3 outlier studies, heterogeneity decreased. Sensitivity analysis demonstrated no disproportionate influences of individual studies. Publication bias was not significant. Conclusions: CEUS is a promising diagnostic modality in differentiating between benign and malignant lymph nodes and can potentially reduce unnecessary fine-needle aspiration biopsies of benign nodes.

Keywords

References

  1. Ahuja A, Ying M (2002). An overview of neck node sonography. Invest Radiol, 37, 333-42. https://doi.org/10.1097/00004424-200206000-00005
  2. Deeks JJ, Macaskill P, Irwig L (2005). The performance of tests of publication bias and other sample size effects in systematic reviews of diagnostic test accuracy was assessed. J Clin Epidemiol, 58, 882-93. https://doi.org/10.1016/j.jclinepi.2005.01.016
  3. Deeks JJ, Bossuyt PM, Gatsonis C (2010). Cochrane Handbook for Systematic Reviews of Diagnostic Test Accuracy Version 1.0. Cochrane Collaborat, http://srdta.cochrane.org/handbook-dta-reviews.
  4. De Giorgi V, Gori A, Grazzini M, et al (2010). Contrast-enhanced ultrasound: A filter role in AJCC stage I/II melanoma patients. Oncol, 79, 370-5. https://doi.org/10.1159/000323494
  5. Deng J, Zhang R, Pan Y, et al (2014). Comparison of the staging of regional lymph nodes using the sixth and seventh editions of the tumor-node-metastasis (TNM) classification system for the evaluation of overall survival in gastric cancer patients: Findings of a case-control analysis involving a single institution in China. Surgery, 156, 64-74. https://doi.org/10.1016/j.surg.2014.03.020
  6. Esen G (2006). Ultrasound of superficial lymph nodes. Eur J Radiol, 58, 345-59. https://doi.org/10.1016/j.ejrad.2005.12.039
  7. Fatima S, Arshad S, Ahmed Z, Hasan SH (2011). Spectrum of cytological findings in patients with neck lymphadenopathy--experience in a tertiary care hospital in Pakistan. APJCP, 12, 1873-5.
  8. Fayaz MS, El-Sherify MS, El-Basmy A, et al (2014). Clinicopathological features and prognosis of triple negative breast cancer in Kuwait: A comparative/perspective analysis. Rep Pract Oncol Radiother, 19, 173-81. https://doi.org/10.1016/j.rpor.2013.08.007
  9. Gasparri ML, Bellati F, Pernice M, et al (2014). Surgical treatment of an isolated omental cervical cancer recurrence: report of a case and review of the literature. Tumori, 100, 52-4.
  10. Higgins JP, Thompson SG (2002). Quantifying heterogeneity in a meta-analysis. Stat Med, 21, 1539-58. https://doi.org/10.1002/sim.1186
  11. Hocke M, Menges M, Topalidis T, Dietrich CF, Stallmach A (2008). Contrast-enhanced endoscopic ultrasound in discrimination between benign and malignant mediastinal and abdominal lymph nodes. J Cancer Res Clin Oncol, 134, 473-80. https://doi.org/10.1007/s00432-007-0309-7
  12. Iannace C, Di Libero L, Lepore M, et al (2010). Prognostic and curative value of sentinel node in breast cancer. A 377 patients experience. Ann Ital Chir, 81, 103-13.
  13. Kanamori A, Hirooka Y, Itoh A, et al (2006). Usefulness of contrast-enhanced endoscopic ultrasonography in the differentiation between malignant and benign lymphadenopathy. Am J Gastroenterol, 101, 45-51. https://doi.org/10.1111/j.1572-0241.2006.00394.x
  14. Karina C, Ali S, Pippa M, et al (2013). Validation of a technique using microbubbles and contrast enhanced ultrasound to identify and biopsy sentinel lymph nodes in pre-operative breast cancer patients. Eur J Surg Oncol, 39, 760-5. https://doi.org/10.1016/j.ejso.2013.03.026
  15. Kawada H, Kurita N, Nakamura F, et al (2014). Incorporation of apical lymph node status into the seventh edition of the TNM classification improves prediction of prognosis in stage III colonic cancer. Br J Surg, 101, 1143-52. https://doi.org/10.1002/bjs.9548
  16. Lijmer JG, Bossuyt PM, Heisterkamp SH (2002). Exploring sources of heterogeneity in systematic reviews of diagnostic tests. Stat Med, 21,1525-37. https://doi.org/10.1002/sim.1185
  17. Moritz JD, Ludwig A, Oestmann JW (2000). Contrast-enhanced color Doppler sonography for evaluation of enlarged cervical lymph nodes in head and neck tumors. Am J Roentgenol, 174, 1279-84. https://doi.org/10.2214/ajr.174.5.1741279
  18. Podkrajsek M, Hocevar M (2011). The role of contrast enhanced axillary ultrasonography in early breast cancer patients. CollAntropol, 35, 33-7.
  19. Poanta L, Serban O, Pascu I, et al (2014). The place of CEUS in distinguishing benign from malignant cervical lymph nodes: a prospective study. Medical Ultrasonography, 16, 7-14. https://doi.org/10.11152/mu.2014.2066.161.lp1os2
  20. Rubaltelli L, Khadivi Y, Tregnaghi A, et al (2004). Evaluation of lymph node perfusion using continuous mode harmonic ultrasonography with a second-generation contrast agent. J Ultrasound Med, 23, 829-36.
  21. Reitsma JB, Glas AS, Rutjes AW, et al (2005). Bivariate analysis of sensitivity and specificity produces informative summary measures in diagnostic reviews. J Clin Epidemiol, 58, 982-90. https://doi.org/10.1016/j.jclinepi.2005.02.022
  22. Rubaltelli L, Corradin S, Dorigo A, et al (2007). Automated quantitative evaluation of lymph node perfusion on contrast-enhanced sonography. Am J Roentgenol, 188, 977-83. https://doi.org/10.2214/AJR.06.0562
  23. Rubaltelli L, Beltrame V, Tregnaghi A, et al (2011). Contrast-enhanced ultrasound for characterizing lymph nodes with focal cortical thickening in patients with cutaneous melanoma. Am J Roentgenol, 196, 8-12. https://doi.org/10.2214/AJR.10.4711
  24. Riegger C, Koeninger A, Hartung V, et al (2012). Comparison of the diagnostic value of FDG-PET/CT and axillary ultrasound for the detection of lymph node metastases in breast cancer patients. Acta Radiol, 53, 1092-8. https://doi.org/10.1258/ar.2012.110635
  25. Rubaltelli L, Beltrame V, Scagliori E, et al (2014). Potential use of contrast-enhanced ultrasound (CEUS) in the detection of metastatic superficial lymph nodes in melanoma patients. Ultraschall in der Medizin, 35, 67-71.
  26. Schmid-Wendtner MH, Partscht K, Korting HC, Volkenandt M (2002). Improved differentiation of benign and malignant lymphadenopathy in patients with cutaneous melanoma by contrast-enhanced color Doppler sonography. Arch Dermatol, 138, 491-7. https://doi.org/10.1001/archderm.138.4.491
  27. Schroder RJ, Rost B, Hidajat N, et al (2002). Value of contrast-enhanced ultrasound vs. CT and MRI in palpable enlarged lymph nodes of the head and neck. Ro Fo, 174, 1099-106.
  28. Stramare R, Tregnaghi A, Fitta C, et al (2004). High-sensitivity power Doppler of normal superficial lymph nodes. J Clin Ultrasound, 32, 273-6. https://doi.org/10.1002/jcu.20036
  29. Smidt N, Deeks J, Moore T (2008). Guide to the contents of a Cochrane review and protocol for Diagnostic Test Accuracy version 1.0.1. Cochrane Collaborat. http://www.cochrane.org/resources/handbook.
  30. Steppan I, Reimer D, Muller-Holzner E, et al (2010). Breast cancer in women: evaluation of benign and malignant axillary lymph nodes with contrast-enhanced ultrasound. Ultraschall Med, 31, 63-7. https://doi.org/10.1055/s-0028-1109847
  31. Sun DS, Chen Y, Zhong JY, Hu ZM, Hu HY (2012). Application of CEUS-guided needle biopsy for superficial lymphadenopathy.. CJIIT, 9, 229-32 (in Chinese).
  32. Slaisova R, Benda K, Jarkovsky J, et al (2013). Contrast-enhanced ultrasonography compared to gray-scale and power doppler in the diagnosis of peripheral lymphadenopathy. EurJ Radiol, 82, 693-8. https://doi.org/10.1016/j.ejrad.2012.12.008
  33. Wang CL, Yang YM, Cui J, et al (2009). Diagnostic value of double contrast-enhanced ultrasonography in preoperative staging of gastric cancer. Zhonghua Zhong Liu Za Zhi, 31, 701-4.
  34. Whiting PF, Rutjes AW, Westwood ME, et al (2011). QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med, 155, 529-36. https://doi.org/10.7326/0003-4819-155-8-201110180-00009
  35. Xue N, Huang P, Aronow WS, et al (2011). Predicting lymph node status in patients with early gastric carcinoma using double contrast-enhanced ultrasonography. Arch Med Sci, 7, 457-64.
  36. Yu M, Liu Q, Song HP, et al (2010). Clinical application of contrast-enhanced ultrasonography in diagnosis of superficial lymphadenopathy. J Ultrasound Med, 29, 735-40.
  37. Zheng Z, Yu Y, Lu M, et al (2011). Double contrast-enhanced ultrasonography for the preoperative evaluation of gastric cancer: a comparison to endoscopic ultrasonography with respect to histopathology. Am J Surg, 202, 605-11. https://doi.org/10.1016/j.amjsurg.2010.09.033

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