Abstract
Purposes
The purpose of our meta-analysis was to assess the overall diagnostic value of diffusion-weighted magnetic resonance imaging (DW-MRI) in detecting node metastases and investigate whether the apparent diffusion coefficient (ADC) value could be used to discriminate between metastatic and non-metastatic lymph nodes in patients with primary tumors.
Materials and methods
The meta-analysis included a total of 1,748 metastatic and 6,547 non-metastatic lymph nodes from 39 studies, including 8 different tumor types with lymph node metastases.
Results
The pooled sensitivity and specificity of DW-MRI were 0.82 (95 % CI 0.76–0.87) and 0.92 (95 % CI 0.88–0.94), respectively. The positive likelihood ratio (PLR), negative likelihood ratio (NLR), and the area under the curve were 9.8 (95 % CI 6.9–14.0), 0.20 (95 % CI 0.15–0.26) and 0.93 (95 % CI 0.91–0.95), respectively. The probability of 42 % can be viewed as the cutoff pretest probability for DW-MRI to diagnosis lymph node metastases; when the more chance of metastatic increased from 42 % that the pretest probability was estimated, it was more suitable to emphasize on “ruling in,” on the contrary, and when the more chance of metastatic decreased from 42 %, it was more suitable to emphasize on “ruling out.” Furthermore, the mean ADC value of metastatic lymph nodes was significantly lower than that of non-metastatic (P = 0.001).
Conclusions
DW-MRI is useful for differentiation between metastatic and non-metastatic lymph nodes. However, DW-MRI has a moderate diagnostic value for physician’s decision making when PLR and NLR took into consideration, while a superior ability for nodal metastases confirmation, but an inferior ability for ruling out. In the future, large-scale, high-quality trials are necessary to evaluate, respectively, their clinical value in different tumor types with nodal metastases.
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References
Abdel Razek AA et al (2006) Role of diffusion-weighted MR imaging in cervical lymphadenopathy. Eur Radiol 16(7):1468–1477
Akobeng AK (2007) Understanding diagnostic tests 2: likelihood ratios, pre- and post-test probabilities and their use in clinical practice. Acta Paediatr 6(4):487–491
Budiharto T, Joniau S, Lerut E, Van den Bergh L, Mottaghy F et al (2011) Prospective evaluation of 11C-choline positron emission tomography/computed tomography and diffusion-weighted magnetic resonance imaging for the nodal staging of rostate cancer with a high risk of lymph nodemetastases. Eur Urol 60(1):125–130
Chae BJ, Bae JS, Kang BJ, Kim SH, Jung SS, Song BJ (2009) Positron emission tomography-computed tomography in the detection of axillary lymph node metastasis in patients with early stage breast cancer. Jpn J Clin Oncol 39:284–289
Charles-Edwards EM, deSouza NM (2006) Diffusion-weighted magnetic resonance imaging and its application to cancer. Cancer Imaging 6:135–143
Chen W, Jian W, Li HT, Li C, Zhang YK, Xie B, Zhou DQ et al (2010) Whole-body diffusion-weighted imaging vs. FDG-PET for the detection of non-small-cell lung cancer. How do they measure up? Magn Reson Imaging 28(5):613–620
Chen YB, Hu CM, Chen GL, Hu D, Liao J (2011a) Staging of uterine cervical carcinoma: whole-body diffusion-weighted magnetic resonance imaging. Abdom Imaging 36(5):619–626
Chen YB, Liao J, Xie R, Chen GL, Chen G (2011b) Discrimination of metastatic from hyperplastic pelvic lymph nodes in patients with cervical cancer by diffusion-weighted magnetic resonance imaging. Abdom Imaging 36(1):102–109
Cho EY, Kim SH, Yoon JH, Lee Y, Lim YJ, Kim SJ, Baek HJ, Eun CK (2013) Apparent diffusion coefficient for discriminating metastatic from non-metastatic lymph nodes in primary rectal cancer. Eur J Radiol 82(11):e662–e668
Choi EK, Kim JK, Choi HJ, Park SH, Park BW, Kim N, Kim JS, Im KC, Cho G, Cho KS (2009) Node-by-node correlation between MR and PET/CT in patients with uterine cervical cancer: diffusion-weighted imaging versus size-based criteria on T2WI. Eur Radiol 19(8):2024–2032
Chung J, Youk JH, Kim JA, Gweon HM, Kim EK, Ryu YH, Son EJ (2014) Role of diffusion-weighted MRI: predicting axillary lymph node metastases in breast cancer. Acta Radiol 55(8):909–916
de Bondt RB, Hoeberigs MC, Nelemans PJ, Deserno WM, Peutz-Kootstra C, Kremer B, Beets-Tan RG (2009) Diagnostic accuracy and additional value of diffusion-weighted imaging for discrimination of malignant cervical lymph nodes in head and neck squamous cell carcinoma. Neuroradiology 51(3):183–192
Deeks JJ (2001) Systematic reviews in health care: systematic reviews of evaluations of diagnostic and screening tests. BMJ 323:157–162
Dirix P, Vandecaveye V, De Keyzer F, Op de Beeck K et al (2010) Diffusion-weighted MRI for nodal staging of head and neck squamous cell carcinoma: impact on radiotherapy planning. Int J Radiat Oncol Biol Phys 76(3):761–766
Eiber M, Beer AJ, Holzapfel K, Tauber R, Ganter C, Weirich G et al (2010) Preliminary results for characterization of pelvic lymph nodes in patients with prostate cancer by diffusion-weighted MR-imaging. Invest Radiol 45(1):15–23
Fagan TJ (1975) Nomogram for Bayes theorem. N Engl J Med 293:257
Fornasa F, Nesoti MV, Bovo C, Bonavina MG (2012) Diffusion-weighted magnetic resonance imaging in the characterization of axillary lymph nodes in patients with breast cancer. J Magn Reson Imaging 36(4):858–864
Hardie AD, Rieter WJ, Bradshaw ML, Gordon LL, Young MA, Keane TE et al (2013) Improved performance of SPECT-CT In-111 capromab pendetide by correlation with diffusion-weighted magnetic resonance imaging for identifying metastatic pelvic lymphadenopathy in prostate cancer. World J Urol 31(6):1327–1332
Hasegawa I, Boiselle PM, Kuwabara K, Sawafuji M, Sugiura H (2008) Mediastinal lymph nodes in patients with non-small cell lung cancer: preliminary experience with diffusion-weighted MR imaging. J Thorac Imaging 23(3):157–161
Heusch P, Sproll C, Buchbender C, Rieser E, Terjung J, Antke C et al (2014) Diagnostic accuracy of ultrasound, 18F-FDG-PET/CT, and fused 18F-FDG-PET-MR images with DWI for the detection of cervical lymph node metastases of HNSCC. Clin Oral Investig 18(3):969–978
Heusner TA, Kuemmel S, Hahn S et al (2009) Diagnostic value of full-dose FDG PET/CT for axillary lymph node staging in breast cancer patients. Eur J Nucl Med Mol Imaging 36:1543–1550
Hovels AM, Heesakkers RA, Adang EM et al (2008) The diagnostic accuracy of CT and MRI in the staging of pelvic lymph nodes in patients with prostate cancer: a meta-analysis. Clin Radiol 63(4):387–395
Jaeschke R, Guyatt G, Sackett DL (1994) Users’ guides to the medical literature. III. How to use an article about a diagnostic test. A. Are the results of the study alid? Evidence-based medicine Working Group. JAMA 271(5):389–391
Kamitani T, Hatakenaka M, Yabuuchi H, Matsuo Y et al (2013) Detection of axillary node metastasis using diffusion-weighted MRI in breast cancer. Clin Imaging 37(1):56–61
Kim JK, Kim KA, Park BW, Kim N, Cho KS (2008) Feasibility of diffusion-weighted imaging in the differentiation of metastatic from nonmetastatic lymph nodes: early experience. J Magn Reson Imaging 28(3):714–719
Kim EJ, Kim SH, Kang BJ, Choi BG, Song BJ, Choi JJ (2014) Diagnostic value of breast MRI for predicting metastatic axillary lymph nodes in breast cancer patients: diffusion-weighted MRI and conventional MRI. Magn Reson Imaging. doi:10.1016/j.mri.2014.07.001
Kitajima K, Yamasaki E, Kaji Y, Murakami K, Sugimura K (2012) Comparison of DWI and PET/CT in evaluation of lymph node metastasis in uterine cancer. World J Radiol 28;4(5):207–214
Koplay M, Dogan NU, Erdogan H, Sivri M, Erol C, Nayman A, Karabagli P, Paksoy Y, Celik C (2014) Diagnostic efficacy of diffusion-weighted MRI for re-operative assessment of myometrial and cervical invasion and pelvic lymph node metastasis in endometrial carcinoma. J Med Imaging Radiat Oncol 58(5):538–546
Lin G, Ho KC, Wang JJ, Ng KK, Wai YY, Chen YT, Chang CJ, Ng SH, Lai CH, Yen TC (2008) Detection of lymph node metastasis in cervical and uterine cancers by diffusion-weighted magnetic resonance imaging at 3T. J Magn Reson Imaging 28(1):128–135
Luo N, Su D, Jin G, Liu L, Zhu X, Xie D, Liu Y (2013) Apparent diffusion coefficient ratio between axillary lymph node with primary tumor to detect nodal metastasis in breast cancer patients. J Magn Reson Imaging 38(4):824–828
Matoba M et al (2007) Lung carcinoma: diffusion-weighted mr imaging preliminary evaluation with apparent diffusion coefficient. Radiology 243(2):570–577
Mizukami Y, Ueda S, Mizumoto A, Sasada T, Okumura R, Kohno S, Takabayashi A (2011) Diffusion-weighted magnetic resonance imaging for detecting lymph node metastasis of rectal cancer. World J Surg 35(4):895–899
Moses LE, Shapiro D, Littenberg B (1993) Combining independent studies of a diagnostic test into a summary ROC curve: data-analytic approaches and some additional considerations. Stat Med 12:1293–1316
Nakai G, Matsuki M, Harada T, Tanigawa N, Yamada T, Barentsz J, Narumi Y (2011) Evaluation of axillary lymph nodes by diffusion-weighted MRI using ultrasmall super paramagnetic iron oxide in patients with breast cancer: initial clinical experience. J Magn Reson Imaging 34(3):557–562
Nakayama J, Miyasaka K, Omatsu T, Onodera Y, Terae S, Matsuno Y, Cho Y, Hida Y, Kaga K, Shirato H (2010) Metastases in mediastinal and hilar lymph nodes in patients with non-small cell lung cancer: quantitative assessment with diffusion-weighted magnetic resonance imaging and apparent diffusion coefficient. J Comput Assist Tomogr 34(1):1–8
Ono K, Ochiai R, Yoshida T, Kitagawa M, Omagari J, Kobayashi H, Yamashita Y (2009) Comparision of diffusion-weighted MRI and 2-[fluorine-18]-fluoro-2-deoxy-d-glucose positron emission tomography (FDG-PET) for detecting primary colorectal cancer and regional lymph node metastases. J Magn Reson Imaging 29(2):336–340
Papalia R, Simone G, Grasso R, Augelli R, Faiella E et al (2012) Diffusion-weighted magnetic resonance imaging in patients selected for radical cystectomy: detection rate of pelvic lymph node metastases. BJU Int 109(7):1031–1036
Park SO, Kim JK, Kim KA, Park BW, Kim N, Cho G, Choi HJ, Cho KS (2009) Relative apparent diffusion coefficient: determination of reference site and validation of benefit for detecting metastatic lymph nodes in uterine cervical cancer. J Magn Reson Imaging 29(2):383–390
Perrone A, Guerrisi P, Izzo L, D’Angeli I, Sassi S, Mele LL, Marini M, Mazza D, Marini M (2011) Diffusion-weighted MRI in cervical lymph nodes: differentiation between benign and malignant lesions. Eur J Radiol 77(2):281–286
Rieter WJ, Keane TE, Ahlman MA, Ellis CT, Spicer KM, Gordon LL (2011) Diagnostic performance of In-111 capromab pendetide SPECT/CT in localized and metastatic prostate cancer. Clin Nucl Med 36(10):872–878
Rockall AG, Sohaib SA, Harisinghani MG, Babar SA, Singh N, Jeyarajah AR, Oram DH, Jacobs IJ, Shepherd JH, Reznek RH (2005) Diagnostic performance of nanoparticle-enhanced magnetic resonance imaging in the diagnosis of lymph node metastases in patients with endometrial and cervical cancer. J Clin Oncol 23:2813–2821
Rockall AG, Meroni R, Sohaib SA, Reynolds K, Alexander-Sefre F, Shepherd JH, Jacobs I, Reznek RH (2007) Evaluation of endometrial carcinoma on magnetic resonance imaging. Int J Gynecol Cancer 17:188–196
Roy C, Bierry G, Matau A et al (2010) Value of diffusion-weighted imaging to detect small malignant pelvic lymph nodes at 3 T. Eur Radiol 20(8):1803–1811
Sakurada A, Takahara T, Kwee TC, Yamashita T, Nasu S, Horie T, Van Cauteren M, Imai Y (2009) Diagnostic performance of diffusion-weighted magnetic resonance imaging in esophageal cancer. Eur Radiol 19(6):1461–1469
Si J, Huang S, Shi H, Liu Z, Hu Q, Wang G, Shen G, Zhang D (2014) Usefulness of 3T diffusion-weighted MRI for discrimination of reactive and metastatic cervical lymph nodes in patients with oral squamous cell carcinoma: a pilot study. Dentomaxillofac Radiol 43(3):20130202. doi:10.1259/dmfr.20130202
Sumi M, Sakihama N, Sumi T, Morikawa M, Uetani M, Kabasawa H, Shigeno K, Hayashi K, Takahashi H, Nakamura T (2003) Discrimination of metastatic cervical lymph nodes with diffusion-weighted MR imaging in patients with head and neck cancer. AJNR Am J Neuroradiol 24(8):1627–1634
Thoeny HC, Triantafyllou M, Birkhaeuser FD, Froehlich JM et al (2009) Combined ultrasmall superparamagnetic particles of iron oxide-enhanced and diffusion-weighted magnetic resonance imaging reliably detect pelvic lymph node metastases in normal-sized nodes of bladder and prostate cancer patients. Eur Urol 55(4):761–769
Usuda K, Sagawa M, Motono N, Patterson DM, Padhani AR, Collins DJ (2008) Technology insight: water diffusion MRI—a potential new biomarker of response to cancer therapy. Nat Clin Pract Oncol 5(4):220–233
Usuda K, Zhao XT, Sagawa M, Matoba M, Kuginuki Y, Taniguchi M, Ueda Y, Sakuma T (2011) Diffusion-weighted imaging is superior to positron emission tomography in the detection and nodal assessment of lung cancers. Ann Thorac Surg 91(6):1689–1695
Vandecaveye V, De Keyzer F, Vander Poorten V, Dirix P, Verbeken E, Nuyts S, Hermans R (2009) Head and neck squamous cell carcinoma: value of diffusion-weighted MR imaging for nodal staging. Radiology 251(1):134–146
Xue HD, Li S, Sun F, Sun HY, Jin ZY, Yang JX, Yu M (2008) Clinical application of body diffusion weighted MR imaging in the diagnosis and preoperative N staging of cervical cancer. Chin Med Sci J 23(3):133–137
Yabuuchi H, Matsuo Y, Okafuji T, Kamitani T, Soeda H, Setoguchi T, Sakai S, Hatakenaka M, Kubo M, Sadanaga N, Yamamoto H, Honda H (2008) Enhanced mass on contrast-enhanced breast MR imaging: lesion characterization using combination of dynamic contrast-enhanced and diffusion-weighted MR images. J Magn Reson Imaging 28:1157–1165
Yasui O, Sato M, Kamada A (2009) Diffusion-weighted imaging in the detection of lymph node metastasis in colorectal cancer. Tohoku J Exp Med 218(3):177–183
Zamora J, Abraira V, Muriel A, Khan K, Coomarasamy A (2006) Meta-DiSc: a software for meta-analysis of test accuracy data. BMC Med Res Methodol 6:31
Zhang Y, Chen J, Shen J, Zhong J, Ye R, Liang B (2013) Apparent diffusion coefficient values of necrotic and solid portion of lymph nodes: differential diagnostic value in cervical lymphadenopathy. Clin Radiol 68(3):224–231
Zhong J, Lu Z, Xu L, Dong L, Qiao H, Hua R et al (2014) The diagnostic value of cervical lymph node metastasis in head and neck squamous carcinoma by using diffusion-weighted magnetic resonance imaging and computed tomography perfusion. Biomed Res Int. doi:10.1155/2014/260859
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Min Zhou and Bin Lu have contributed equally to this work.
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Zhou, M., Lu, B., Lv, G. et al. Differential diagnosis between metastatic and non-metastatic lymph nodes using DW-MRI: a meta-analysis of diagnostic accuracy studies. J Cancer Res Clin Oncol 141, 1119–1130 (2015). https://doi.org/10.1007/s00432-014-1895-9
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DOI: https://doi.org/10.1007/s00432-014-1895-9