Literature DB >> 26089682

Computed tomography versus magnetic resonance imaging for diagnosing cervical lymph node metastasis of head and neck cancer: a systematic review and meta-analysis.

J Sun1, B Li2, C J Li1, Y Li1, F Su3, Q H Gao4, F L Wu4, T Yu5, L Wu6, L J Li1.   

Abstract

Computed tomography (CT) and magnetic resonance imaging (MRI) are common imaging methods to detect cervical lymph node metastasis of head and neck cancer. We aimed to assess the diagnostic efficacy of CT and MRI in detecting cervical lymph node metastasis, and to establish unified diagnostic criteria via systematic review and meta-analysis. A systematic literature search in five databases until January 2014 was carried out. All retrieved studies were reviewed and eligible studies were qualitatively summarized. Besides pooling the sensitivity (SEN) and specificity (SPE) data of CT and MRI, summary receiver operating characteristic curves were generated. A total of 63 studies including 3,029 participants were involved. The pooled results of meta-analysis showed that CT had a higher SEN (0.77 [95% confidence interval {CI} 0.73-0.87]) than MRI (0.72 [95% CI 0.70-0.74]) when node was considered as unit of analysis (P<0.05); MRI had a higher SPE (0.81 [95% CI 0.80-0.82]) than CT (0.72 [95% CI 0.69-0.74]) when neck level was considered as unit of analysis (P<0.05) and MRI had a higher area under concentration-time curve than CT when the patient was considered as unit of analysis (P<0.05). With regards to diagnostic criteria, for MRI, the results showed that the minimal axial diameter of 10 mm could be considered as the best size criterion, compared to 12 mm for CT. Overall, MRI conferred significantly higher SPE while CT demonstrated higher SEN. The diagnostic criteria for MRI and CT on size of metastatic lymph nodes were suggested as 10 and 12 mm, respectively.

Entities:  

Keywords:  computed tomography; head and neck cancer; magnetic resonance imaging; meta-analysis; metastasis

Year:  2015        PMID: 26089682      PMCID: PMC4467645          DOI: 10.2147/OTT.S73924

Source DB:  PubMed          Journal:  Onco Targets Ther        ISSN: 1178-6930            Impact factor:   4.147


Introduction

The occurrence of cervical lymph node metastasis in patients with head and neck cancers are very common.1 The presence of cervical lymph node metastasis may affect the optimal treatment choice as well as prognosis in patients.2 Management of patients presenting with cervical lymph node metastasis includes selective or radical neck dissection, followed by radiotherapy and/or chemotherapy depending on the pathological findings of the nodes.3–5 Besides, the detection of cervical lymph node metastasis is very important for predicting prognosis in patients with head and neck cancers.6–8 Many imaging techniques exist for identifying cervical lymph node metastasis in patients with head and neck cancers.9–12 Among them, computed tomography (CT) and magnetic resonance imaging (MRI) are the most widely used tools.13 Both of them have improved accuracy of nodal staging over clinical palpation and the nodes which are clinically occulted can be visualized through these techniques.14 Usually the cervical lymph nodes demonstrate similar density as muscle on pre-contrast images of CT examination, and they can be separated from adjacent vessels by their differential enhancement after contrast administration.15 On the other hand, MRI is considered to have similar accuracy for identifying the cervical lymph node metastasis of head and neck cancer.16,17 Because of the intrinsic high soft-tissue discrimination, MRI has become the preferred method for evaluating the soft tissues of the head and neck recently.18 Under current health care settings, the routine practice for evaluating patients with head and neck cancer is to perform either CT or MRI, but not both.19 Thus, to determine whether one of the two techniques is superior to the other is critical for providing guidance for clinical practice. Besides, since relevant studies utilized very different diagnostic criteria, it is warranted to determine the unified criteria that are most appropriate. A systematic review to assess all available evidence is thus needed for providing a comprehensive evaluation for these aims. The aim of this study was thus to compare CT and MRI for detecting cervical lymph node metastasis in patients with head and neck cancer and to establish the unified diagnostic criteria by performing a systematic review and meta-analysis.

Methods

Inclusion criteria

The inclusion criteria were as follows: a) types of study: diagnostic accuracy test studies designed as cohort studies; b) participants: patients with biopsy proven head and neck cancers who would undergo neck dissection; c) index tests: CT and/or MRI; d) target condition: cervical lymph node metastasis; e) reference standard: histopathology examination; f) outcome: rates of true positive, false positive, false negative, and true negative or related data that could be used to calculate them.

Literature search

With no language restriction, the following databases were searched for retrieving studies: MEDLINE (1948 to 25 January 2014), EMBASE (1980 to 25 January 2014), China National Knowledge Infrastructure (1994 to 25 January 2014), VIP Chinese Journal Database (1989 to 25 January 2014), and Chinainfo (1998 to 25 January 2014). The search strategy was optimized for all consulted databases, taking into account the differences in the various controlled vocabularies as well as the differences of database-specific technical variations.20 Once relevant articles were identified, their reference lists were searched for additional articles. Both Medical Subject Headings (MeSH) and free text words were used in the search strategy with the following MeSH terms: “head and neck neoplasm”, “neoplasm metastases”, “SEN and SPE”, “Tomography, Spiral Computed” and “Magnetic Resonance Imaging”.

Study selection

Two reviewers independently examined the titles and abstracts of each search record to remove obviously irrelevant ones, and then retrieved the full text articles for potentially eligible articles. The full-texts were further examined according to the inclusion criteria. Discrepancies were resolved by consensus.

Data extraction

A standardized data extraction form was used by two authors independently for data extraction from included studies. Discrepancies were resolved by discussion, with input from a third author. The contents of the form included: name of first author, publication year, country, participants’ age, sex, number of included patients, tumor location, unit, details of CT and/or MRI, study design (prospective or retrospective).

Quality assessment

The methodological quality of included studies was assessed by The Quality Assessment Diagnostic Accuracy Studies statement-2 (QUADAS-2),21 which included four domains: patient selection, index test, reference standard, and flow and timing. Each domain was assessed in terms of risk of bias and the first three were assessed in terms of concerns regarding applicability. Signaling questions were included to assist judgments on risk of bias. The signaling questions in the QUADAS-2 were presented as shown in Table 1. The result for each item was categorized as yes (Y), unclear (U), or no (N). The summary risk of bias for each study was categorized as low (A), unclear (B), or high (C).
Table 1

Signaling questions in the QUADAS-2

DomainPatient selectionIndex testReference standardFlow and timing
Signaling questions (yes/no/unclear)1 Was a consecutive or random sample of patients enrolled?4 Were the index test results inter preted without knowledge of the results of the reference standard?5 Is the reference standard likely to correctly classify the target condition?7 Was there an appropriate interval between index test(s) and reference standard?
2 Was a case-control design avoided?6 Were the reference standard results interpreted without know ledge of the results of the index test?8 Did all patients receive a reference standard?
3 Did the study avoid inappropriate exclusions?9 Were all patients included in the analysis?

Abbreviation: QUADAS-2, The Quality Assessment Diagnostic Accuracy Studies statement-2.

Meta-analysis

Measures of diagnostic efficacy of CT and/or MRI included sensitivity (SEN), specificity (SPE), positive likelihood ratio (+LR), negative likelihood ratio (−LR), accuracy (ACC), and diagnostic odds ratios (DOR) with 95% confidence intervals (CIs). Summary receiver operating characteristic (SROC) curves were then drawn. The area under the curve (AUC) and Q* (the point where SEN is equal to SPE on the SROC curve) were calculated. To detect any differences for SEN, SPE, AUC, and Q* between CT and MRI, a Z-test was conducted (Z= (VAL1–VAL2)/SQRT (SE12+SE22). The test standard was set at α=0.05. VAL indicates the mean of SEN, SPE, AUC or Q* of the CT or MRI and SE indicates the standard error of the corresponding variable.

Heterogeneity analysis

Heterogeneity between studies was evaluated by I2 statistic.22,23 If I2≤50% and P≥0.10, the heterogeneity was considered not significant and in such case the fixed-effects model would be used in meta-analysis. Otherwise, the random-effects model would be used.24,25

Meta-regression

Meta-regression was used to determine any potential source of heterogeneity that might influence the overall assessment. The test standard for meta-regression was set at α=0.10. Relevant variables which might cause heterogeneities were tested, and any suggested sources of heterogeneity were considered as proof for a subgroup analysis. Variables detected by meta-regression included publication year (0= published before 2000; 1= published in or after 2000), race (0= Mongolia; 1= Caucasian), study type (0= retrospective; 1= prospective), risk of bias (0= high; 1= unclear; 2= low), blinding of the radiologists (0= no or unclear; 1= yes) and blinding of the pathologists (0= no or unclear; 1= yes). Meta-disc 1.4 and STATA 11.0 (StataCorp LP, College Station, TX, USA) were used to perform the statistical analyses.26,27

Results

Selection of literature

The computerized and manual search retrieved a total of 306 articles. After assessing the titles and abstracts, 144 articles were found to be potentially relevant. After the full text assessment, 63 studies met the inclusion criteria and were included in this meta-analysis (Figure 1).28–90
Figure 1

Flow chart of the literature search and selection.

Abbreviations: CT, computed tomography; MRI, magnetic resonance imaging.

Study characteristics

Of the 63 included studies, 24 were retrospective and 39 were prospective. A total of 3,029 participants were involved in these studies. Among those patients, 1,044 underwent both CT and MRI examination, 2,395 underwent MRI examination, and 1,678 underwent CT examination. Three kinds of unit of analysis were used, including node, neck level (the neck was classified as five levels according to anatomical landmarks), and patients. When node was considered as the unit of analysis, available studies involved 22 with CT and 30 with MRI. When neck level was considered as the unit of analysis, eight studies with CT and 16 with MRI were available. When patient was considered as the unit of analysis, available studies included eight with CT and eleven with MRI. The tumor locations included floor of mouth, nasopharynx, retromolar trigonum, mandibule, maxilla, supra-glottic larynx, oropharynx, laryngopharynx, hypopharynx, parotid gland, submandibular gland, tonsil, thyroid gland, cervical esophageal, paranasal sinuses et al. The characteristics of included studies are listed in Table 2.
Table 2

Study characteristics and included data sets for CT and MRI of the included articles

Study IDCountryStudy typePatients (M/F)Age (yr), mean (range)Tumor locationImaging modalityUnit
Adams et al28 1998GermanyP60 (16/44)58.3 (38–76)Tongue, FOM, Palate, MAN, MAXMRI, CTnode
Akoglu et al29 2005TurkeyP23 (19/4)58.3 (40–78)Head and neckMRI, CTnode
Anzai et al30 1994USAP12 (7/5)39–78EAC, MAN, BCC, RMT, Lip, Oral cavity, LarynxMRInode
Ao et al31 1998JapanR42 (9/33)60 (39–78)LarynxMRI, CTnode
Bondt et al32 2009The NetherlandsP16 (9/7)40–77Tongue, NP, RMT, SMG, Cheek, RMT, SP, NoseMRI, CTneck level
Braams et al33 1996The NetherlandsP11 (7/4)62.3 (46–73)FOM, RMT, Cheek, GingivaMRI, CTnode
Braams et al34 1995The NetherlandsP12 (8/4)65.3 (48–85)Tongue, Lip, Gingiva, RMT, FOMMRInode
Bruschini et al35 2003ItalyP22 (19/3)62.3 (46–79)Larynx, OP, Oral cavity, SkinCTnode
Curtin et al36 1997CanadaR213 (150/63)59.6 (18–84)Oral cavity, OP, HP, LarynxMRI, CTneck level
Dammann et al37 2005GermanyP64 (43/21)56 (26–83)Oral cavity, OPMRI, CTneck level
Ding et al38 2005People’s Republic of ChinaP92 (58/34)53 (24–81)TongueMRIneck level
Dirix et al39 2010SwedenP22 (13/9)60 (41–83)Oral cavity, Larynx, HPMRInode
Eida et al40 2003JapanP111 (74/37)FOM, Tongue, Palate, Gingiva, CheekCTnode
Fan et al41 2006People’s Republic of ChinaR42 (37/5)53.6 (45–70)OP, HP, Cervical esophagealCTpatient
Fukunari et al42 2010JapanR2058 (23–81)Tongue, Gingiva, Buccal, MAN, FOMMRInode
Gross et al43 2001USAR26 (8/18)40 (10–80)ThyroidMRInode
Gu et al44 2000People’s Republic of ChinaP6258 (44–77)Head and neckMRInode
Guenzel et al45 2013GermanyP120 (95/25)41–85OP, LarynxMRInode
Guo et al46 2006People’s Republic of ChinaR48 (28/20)56 (21–66)Tongue, Buccal, Gingiva, FOM, PalateMRInode
Hannah et al47 2002AustraliaP48 (34/14)61 (26–92)Oral cavity, OP, SGL, HPCTneck level
Hao et al48 2000People’s Republic of ChinaP60Tongue, Gingiva, FOM, Palate, RMT, Buccal, Larynx, HPMRInode
Hafidh et al49 2006IrelandR48 (42/6)56 (32–80)Oral cavity, OP, HP, Paranasal sinuses, Ear(skin)MRI, CTnode
Hlawitschka et al50 2002GermanyP38 (28/10)59 (41–89)Tongue, Buccal, Palate, MAXMRI, CTnode
Hoffman et al51 2000USAP9 (6/3)43–76Oral cavity, OP, LipMRInode, neck level
Jeong et al52 2007GreeceR47 (41/6)56.3Oral cavity, Larynx, OP, HP, PGCTneck level
Kau et al53 1999GermanyP111 (95/16)29–78Larynx, OP, LP, Lip, EarMRI, CTnode, neck level
Kawai et al54 2005JapanP29 (23/6)60 (28–81)Tongue, OP, NP, Larynx, Buccal, Palate, PG, GingivaMRIneck level
Ke et al55 2006People’s Republic of ChinaR20 (15/5)54.5 (31–69)Tongue, Larynx, Thyroid glandCTnode
Krabbe et al56 2008The NetherlandsP38 (21/17)59 (53–680)Tongue, Gingiva, FOM, Tonsillar fossaMRI, CTnode
Laubenbacher et al57 1994GermanyP22 (20/2)54.4 (38–70)OP, HPMRInode, neck level
Lee et al58 2013People’s Republic of ChinaP22 (21/1)49.8 (26–66)Tongue, Buccal, OP, FOM, HP, Palate, RMT, epiglottis, Pyriform sinusMRIpatient
Lu et al59 2007People’s Republic of ChinaP13 (11/2)58 (47–71)Oral cavity, HP, OP, LarynxCTnode
Lwin et al60 2012UKR102 (68/34)59 (23–89)Tongue, FOM, Palate, Buccal, RMT, Tonsil, GingivaMRIpatient
Mcguirt et al61 1995UKP49Oral cavity, OP, HPCTnode
Nakamoto et al62 2009JapanR65 (50/15)62 (27–81)Larynx, HP, MAX, Tongue, OP, PG, Gingiva, FOM, NP, Ethmoid, EAM, ThyoidMRIpatient
Nishimura et al63 2006JapanP16 (13/3)65.8 (37–76)Cervical EsophagealMRInode
Olmos et al64 1999The NetherlandsP12 (6/6)61.8 (44–73)OP, Larynx, HP, Tongue, MAXMRIneck level
Ou et al65 2007People’s Republic of ChinaR24 (19/5)50 (23–80)Tongue, OP, Palate, Cheek, Maxillary sinus, Branchial cleftMRInode
Paulus et al66 1998BelgiumR25 (21/4)48–74SGL, Tongue, Glottis, Palate, RMT, FOM, HP, Vocal cord, Vestibule, Pyriform sinusCTnode
Perrone et al67 2011ItalyR17 (10/7)63 (15–85)Head and neckMRIpatient
Peters et al68 2013The NetherlandsR149 (120/29)62 (40–78)SGL, Glottis, NP, Cervical EsophagealMRI, CTpatient
Pohar et al69 2006USAR25 (17/8)63.4Oral cavity, OP, HP, Larynx, Nasal cavityCTnode, neck level
Ren et al70 2000People’s Republic of ChinaP20 (18/2)45–68SGLCTnode
Schwartz et al71 2004USAP20 (20/0)61 (42–78)Oral cavity, OPCTnode
Semedo et al72 2006PortugalP20 (20/0)57.3 (36–78)HP, Larynx, OPMRInode
Seitz et al73 2009GermanyR66 (39/27)63 (25–89)Oral cavity, OPMRInode, patient
Stokkel et al74 2000The NetherlandsP54 (31/23)60 (34–81)Tongue, FOM, Gingiva, RMT, OPCTnode
Stuckensen et al75 2000GermanyP106 (89/17)59.6 (33–87)FOM, Tongue, RMT, MAN, MAX, BuccalMRI, CTneck level
Sumi et al76 2007JapanR38 (32/6)65HP, Gingiva, OP, Tongue, Larynx, FOMMRI, CTnode
Sumi et al77 2006JapanP26OP, Gingiva, Larynx, TongueMRInode
Sumi et al78 2003JapanP3224–80OP, Gingiva, FOM, Tongue, Buccal, EACMRInode
Sun et al79 2013People’s Republic of ChinaR114 (60/54)51.2 (34–70)Thyroid gland, Larynx, NP, HP, Tongue, PG, Cervical Esophageal, Maxillary sinus, EarCTnode
Sun et al79 2013People’s Republic of ChinaR86 (45/41)52.7 (35–75)Thyroid gland, Larynx, NP, HP, Tongue, PG, Cervical Esophageal, Maxillary sinus, EarMRInode
Tai et al80 2002People’s Republic of ChinaP40 (24/16)25–65NPMRIpatient
Takashima et al81 1997JapanR50 (13/37)57 (24–81)ThyroidMRInode
Tuli et al82 2008IndiaP20 (12/8)54.75 (30–85)TongueMRI, CTpatient
Van den Brekel et al83 1991The NetherlandsP10063±12.8Tongue, FOM, SP, Lip, Tonsil, Pharyngeal wall, Ear, Tonsil, PS, SGL, GingivaMRIpatient
Vandecaveye et al84 2008BelgiumP3641–81Nasal cavity, SGL, FOM, OP, Glottis, Tongue, HPMRInode, neck level, patient
Wang et al85 1999JapanP14 (10/4)46 (26–71)ThyroidMRInode
WIDE et al86 1999UKR5858.1 (32–82)Tongue, FOM, Buccal, RMT, OP, GingivaMRIneck level
Wilson et al87 1994UKP12FOM, Tongue, Tonsillar, Skin, Pinna, PG, ThyroidMRIneck level
Wu et al88 2010People’s Republic of ChinaR24 (23/1)53.6 (45–85)Larynx, HPCTnode
Yoon et al89 2008KoreaR67 (58/9)60 (24–85)Larynx, Pharynx, Tonsil, Tongue, Oral cavity, Skin, MAXMRI, CTneck level
Yuan et al90 2000People’s Republic of ChinaR19 (12/7)42–66LarynxMRIneck level

Abbreviations: M, male; F, female; R, Retrospective; P, Prospective; EAC, external auditory canal; BCC, branchial cleft cyst; PS, piriform sinus; SGL, supra-glottic larynx; TGL, trans-glottic larynx; CT, computed tomography; MRI, magnetic resonance imaging; FOM, floor of mouth; MAN, mandibule; MAX, maxilla; RMT, retro-molar trigonum; NP, nasopharynx; SMG, submandibular gland; OP, oropharynx; HP, hypopharynx; LP, laryngopharynx; PG, parotid gland; SP, supropharynx; yr, years.

Quality of included studies

All included studies had fairly good applicability. For the risk of bias assessment, only two studies had a low risk of bias, five had a high risk, and 56 had an unclear risk (Table 3).
Table 3

Risk of bias of included studies

Study IDPatient selection
Index test
Reference standard
Flow and timing
Summary risk of biasApplicability
123456789
Adams et al28 1998UYYYYUYYYBH
Akoglu et al29 2005YYYUYUUYYBH
Anzai et al30 1994UYYUYUYYYBH
Ao et al31 1998UYYUYUUYYBH
Bondt et al32 2009YYYYYUUYYBH
Braams et al33 1996UYYYYUYYYBH
Braams et al34 1995UYYYYUUYYBH
Bruschini et al35 2003UYYYYYUYYBH
Curtin et al36 1997YYYUYUUYYBH
Dammann et al37 2005UYYYYUYYYBH
Ding et al38 2005UYYYYUYYYBH
Dirix et al39 2010UYYUYUYYYBH
Eida et al40 2003UYYYYUUYYBH
Fan et al41 2006UYYYYUUYNAH
Fukunari et al42 2010UYYUYUUYYBH
Gross et al43 2001UYYYYUYYYBH
Gu et al44 2000UYYYYUUYYBH
Guenzel et al45 2013UYYUYUUYYBH
Guo et al46 2006UYYUYUUYNAH
Hannah et al47 2002UYYUYUUYYBH
Hao et al48 2000UYYYYYUYYBH
Hafidh et al49 2006UYYYYUUYYBH
Hlawitschka et al50 2002YYYUYUUYNAH
Hoffman et al51 2000UYYUYUUYYBH
Jeong et al52 2007UYYYYUUYYBH
Kau et al53 1999YYYYYUYYYBH
Kawai et al54 2005YYYYYUYYYBH
Ke et al55 2006YYYYYUYYYBH
Krabbe et al56 2008UYYUYUUYYBH
Laubenbacher et al57 1994UYYUYUUYYBH
Lee et al58 2013YYYUYUYYYBH
Lu et al59 2007YYYYYUUYYBH
Lwin et al60 2012UYYYYUUYYBH
Mcguirt et al61 1995YYYUYYUYYBH
Nakamoto et al62 2009UYYUYUUYYBH
Nishimura et al63 2006YYYUYUYYYBH
Olmos et al64 1999UYYUYUYYNAH
Ou et al65 2007UYYUYUUYYBH
Paulus et al66 1998UYYUYUUYYBH
Perrone et al67 2011UYYUYUUYYBH
Peters et al68 2013UYYYYUUYYBH
Pohar et al69 2006YYYYYUUYYBH
Ren et al70 2000UYYYYUUYYBH
Schwartz et al71 2004UYYYYUUYYBH
Semedo et al72 2006YYYYYUUYYBH
Seitz et al73 2009YYYYYYYYYCH
Stokkel et al74 2000UYYUYUYYYBH
Stuckensen et al75 2000YYYUYUYYYBH
Sumi et al76 2007UYYUYUYYYBH
Sumi et al77 2006YYYYYUYYYBH
Sumi et al78 2003YYYUYUUYYBH
Sun et al79 2013YYYYYUUYYBH
Tai et al80 2002UYYYYUUYNAH
Takashima et al81 1997UYYYYUYYYBH
Tuli et al82 2008YYYYYUYYYBH
Van den Brekel et al83 1991UYYYYUYYYBH
Vandecaveye et al84 2008YYYYYYUYYBH
Wang et al85 1999UYYYYYYYYCH
WIDE et al86 1999UYYYYUUYYBH
Wilson et al87 1994YYYYYUUYYBH
Wu et al88 2010UYYUYUUYYBH
Yoon et al89 2008UYYUYUYYYBH
Yuan et al90 2000UYYUYUYYYBH

Abbreviations: Y, yes; U, unclear; N, no; A, high risk of bias; B, unclear risk of bias; C, low risk of bias; H, high applicability.

Comparison of CT and MRI in detecting cervical lymph node metastasis with node as unit of analysis

For CT, meta-regression analysis showed that the diagnostic efficacy was not affected by any of the tested variables. These variables thus did not account for heterogeneity between studies. After pooling 22 studies, we detected that CT had a mean (CI) SEN of 0.77 (95% CI 0.73–0.80), SPE of 0.85 (0.84–0.87), +LR of 3.84 (2.51–5.87), −LR of 0.34 (0.24–0.27), ACC of 0.8357, and DOR of 13.57 (6.99–26.33). The SROC was demonstrated in Figure 2 and the AUC was 0.8429 and Q* was 0.7745. For MRI, meta-regression analysis also showed that the diagnostic efficacy was not affected by any of the tested variables. After pooling 30 studies, we identified that MRI had a mean (CI) SEN of 0.72 (0.70–0.74), SPE of 0.84 (0.83–0.85), +LR of 5.06 (3.72–6.88), −LR of 0.27 (0.21–0.34), ACC of 0.8126, and DOR of 25.21 (15.97–39.80). The SROC is shown in Figure 2 and the AUC was 0.9054 and Q* was 0.8371.
Figure 2

Summary receiver operator characteristic curves of CT and MRI (node as unit of analysis).

Abbreviations: CT, computed tomography; MRI, magnetic resonance imaging.

By comparing the diagnostic efficacy between CT and MRI when node was treated as the unit of analysis, the results indicated that CT had a higher SEN, although the SPE and summarized diagnostic efficacy were comparable. The details are listed in Table 4.
Table 4

Comparison of meta-analysis results on diagnostic efficacy between CT and MRI

UnitVariableNumber detectedSEN (95% CI)SPE (95% CI)AUC (SE)Q* (SE)
NodeCT2,4830.77 (0.73–0.87)0.85 (0.84–0.87)0.8429 (0.0341)0.7745 (0.0318)
MRI7,1000.72 (0.70–0.74)0.84 (0.83–0.85)0.9054 (0.0198)0.8371 (0.0215)
P0.01760.27390.10980.1262
Neck levelCT1,6650.84 (0.75–0.84)0.72 (0.69–0.74)0.8787 (0.0268)0.8091 (0.0270)
MRI4,0220.80 (0.77–0.82)0.81 (0.80–0.82)0.8860 (0.0262)0.8165 (0.0269)
P1.00000.00000.86890.8702
PatientCT2300.67 (0.52–0.80)0.74 (0.68–0.81)0.6860 (0.0815)0.6418 (0.0643)
MRI7160.78 (0.70–0.81)0.76 (0.72–0.80)0.8631 (0.0437)0.7937 (0.0424)
P0.19920.61610.04910.0683

Abbreviations: AUC, area under the curve; CI, confidence interval; SE, standard error; CT, computed tomography; MRI, magnetic resonance imaging; SEN, sensitivity; SPE, specificity.

Comparison of CT and MRI in detecting cervical lymph node metastasis with neck level as unit of analysis

For MRI, meta-regression analysis detected that none of the tested variables accounted for heterogeneity between studies. After pooling 16 studies, it was detected that MRI had a mean (CI) SEN of 0.80 (0.77–0.82), SPE of 0.81 (0.80–0.82), +LR of 5.34 (3.24–8.82), −LR of 0.27 (0.20–0.37), ACC of 0.5257, DOR of 24.61 (12.21–49.61) and the AUC was 0.8860 and Q* was 0.8165 (Figure 3). For CT, similarly none of the tested variables accounted for heterogeneity. The pooling of available studies identified that CT had a mean (CI) SEN of 0.80 (0.75–0.84), SPE of 0.72 (0.69–0.74), +LR of 5.60 (2.13–14.73), −LR of 0.26 (0.19–0.36), ACC of 0.6888, DOR of 23.76 (7.87–71.79) and the AUC was 0.8787 and Q* was 0.8091 (Figure 3).
Figure 3

Summary receiver operator characteristic curves of CT and MRI (neck level as unit of analysis).

Abbreviations: CT, computed tomography; MRI, magnetic resonance imaging.

The comparison between CT and MRI showed that MRI had significantly higher SPE than CT while the other variables were comparable between these two techniques (Table 4).

Comparison of CT and MRI in detecting cervical lymph node metastasis with patient as unit of analysis

For the two studies, the pooled results showed that CT had a mean (CI): SEN, 0.81 (0.65–0.92); SPE, 0.35 (0.24–0.42); +LR, 1.14 (0.87–1.50); −LR, 0.70 (0.32–1.52); DOR, 1.66 (0.57–4.82) (Figure S1). For MRI, which included ten studies, meta-regression analysis showed that study type significantly affected the assessment of diagnostic efficacy (P=0.04) (Table 5). Based on the subgroup analysis according to study types, for the four retrospective studies, the pooled results indicated that MRI had a mean (CI) SEN, 0.77 (0.69–0.85); SPE, 0.48 (0.42–0.55); +CR, 2.42 (0.99–5.91); −CR, 0.54 (0.27–1.06); DOR, 5.24 (0.96–28.55) (Figure S2). For the five prospective studies, the pooled results showed that MRI had a mean (CI) SEN, 0.80 (0.72–0.86); SPE, 0.35 (0.67–0.86); +LR, 2.79 (1.44–5.40); −LR, 0.25 (0.08–0.76); DOR, 14.63 (3.64–58.70) (Figure S3). Pooling of the overall nine studies indicated the mean (CI) values for the following parameters to be: SEN, 0.79 (0.73–0.84); SPE, 0.56 (0.51–0.62); +LR, 2.64 (1.30–5.34); −LR, 0.37(0.20–0.71); DOR, 8.87 (2.42–32.55); AUC (0.8158); Q* (0.7498) (Figure S4).
Table 5

Results of meta-regression (MRI patient)

VariableCoefficientSEP-valueRDOR95% CI
Cte−0.5112.54930.8539
S−0.3300.18960.1798
Publication year0.8811.51560.60202.41(0.02–300.01)
Race1.7861.18840.22985.97(0.14–262.04)
Study type3.2880.97420.043226.80(1.21–595.04)
Blinding of radiologists−0.7741.19520.56360.46(0.01–20.70)
Blinding of pathologists−0.2901.52780.86150.75(0.01–96.74)
Risk of bias−0.2270.92250.82170.80(0.04–15.02)

Abbreviations: MRI, magnetic resonance imaging; CI, confidence interval; SE, standard error; RDOR, relative diagnostic odds ratio.

The comparison between CT and MRI showed that MRI had significantly higher AUC than CT while the other variables demonstrated no statistical significance between them. The details are listed in Table 4.

Lymph node size criteria

The size of metastatic lymph nodes used as diagnostic criteria of MRI and CT varied considerably among studies and among different neck levels (Table S1). To determine the best diagnostic criteria, a meta-analysis was conducted for different neck levels with lymph node unit data. For each neck level, the SROC curve was drawn to show the diagnostic efficacy of MRI for different node sizes (Figure 4). The results revealed that the minimal axial diameter of 10 mm in lymph node-bearing regions could be considered as the best size criterion for assessing cervical lymph node metastasis in patients with head and neck cancer (Table S2). For CT, the suggested criterion was 12 mm (Table S3). Considering the limited number of studies for CT, SROC curves were not drawn.
Figure 4

Summary receiver operator characteristic curves of CT and MRI (lymph node size criteria).

Abbreviations: CT, computed tomography; MRI, magnetic resonance imaging; SROC, summary receiver operating characteristic.

Discussion

Head and neck cancer is a common malignant neoplasm worldwide.1 One of the most important factors that influences treatment approaches and therapeutic outcomes for patients with head and neck cancer is the presence of metastatic cervical lymph node. The accurate detection of the cervical lymph node metastasis is thus very important.91,92 Clinical palpation used to be the method to detect cervical nodal metastasis before the development of imaging technologies. However, studies have shown that both the SEN and the SPE of this technique were unsatisfactory, with a high false positive rate of 25%–51%. The improvements in imaging technologies may make it possible for cervical lymph nodes metastasis in head and neck cancer patients can be effectively diagnosed, especially with CT and MRI.11,12,93–96 However, under current health care settings usually only one imaging technique will be performed. Thus a systematic evaluation regarding whether one of the two imaging techniques (CT and MRI) can have a better efficacy than the other will be critical to better guide the clinical practice. In our systematic review and meta-analysis, we comprehensively evaluated all available evidence from 63 studies for evaluating this question whether one of the two imaging techniques (CT and MRI) can have a better efficacy. Besides pooling results from available studies, we assessed potential sources of heterogeneities via meta-regression and conducted sub-group analyses for significant heterogeneity sources detected. Our meta-analyses suggested that CT had a higher SEN than MRI when node was used as unit of analysis; MRI had a higher SPE when neck level was used as unit of analysis; and MRI had a higher AUC when patient was used as unit of analysis. Our findings showed that CT and MRI are effective tools for detecting the cervical lymph node metastasis in patients with head and neck cancer. Since the diagnostic criteria presented in relevant studies varied significantly, we also summarized available evidence to reveal the most appropriate ones for these two techniques, respectively. Usually, the diagnosis of metastatic cervical lymph nodes consisted of two parts, namely, structural and size changes. The structural changes included central necrosis or cystic degeneration, spherical (rather than flat or bean) shape, or abnormal grouping of nodes (a cluster of three or more lymph nodes of borderline size). In different studies, the description of the structural changes differed only mildly. However, the criteria for sizes differed considerably. Most authors recommended using the minimal axial diameter to assess metastasis. The criterion for minimal axial diameter varied between 5 to 15 mm. Our meta-analysis showed that the minimal axial diameter of 10 mm in lymph node-bearing regions could be considered as the best criterion for assessing cervical lymph node metastasis in patients with head and neck cancer for MRI, compared to 12 mm for CT. Several limitations should be acknowledged for the interpretation of our findings. Firstly, although we conducted meta-regression analyses and showed that the assessed variables largely did not account for heterogeneities between studies, additional undetected variables may account for heterogeneities which warrants further research. Secondly, in some of our analyses, only a very limited number of studies were available. For example, when focusing on the 12 mm size criterion, there was only one study available for evaluating CT with node unit, and future studies for evaluating relevant topics are warranted. In conclusion, through this comprehensive systematic review and meta-analysis, we identified that CT and MRI had acceptable diagnostic efficacy in detecting cervical lymph node metastasis in patients with head and neck cancer. When node was used as unit of analysis, CT had a higher SEN. When neck level was used as unit of analysis, MRI had a higher SPE. Out findings suggest that MRI is superior to CT in the diagnosis of cervical lymph node metastasis, especially in diagnosis confirmation. While CT had a better efficacy in diagnosis exclusion. The diagnostic criteria for MRI and CT for size of metastatic lymph nodes were established. Further high-quality studies are warranted to confirm our findings. Meta-analysis of CT for detecting cervical lymph node metastasis in head and neck cancer patients (patient as unit of analysis). Abbreviations: CT, computed tomography; CI, confidence interval; LR, likelihood ratio; df, degrees of freedom; SROC, summary receiver operating characteristic; AUC, area under the curve; SE, standard error. Meta-analysis of MRI for detecting cervical lymph node metastasis in head and neck cancer patients (patient as unit of analysis) (retrospective studies). Abbreviations: MRI, magnetic resonance imaging; CI, confidence interval; df, degrees of freedom; LR, likelihood ratio; OR, odds ratio. Meta-analysis of MRI for detecting cervical lymph node metastasis in head and neck cancer patients (patient as unit of analysis) (prospective studies). Abbreviations: MRI, magnetic resonance imaging; CI, confidence interval; df, degrees of freedom; LR, likelihood ratio; OR, odds ratio. Meta-analysis of MRI for detecting cervical lymph node metastasis in head and neck cancer patients (patient as unit of analysis). Abbreviations: MRI, magnetic resonance imaging; CI, confidence interval; df, degrees of freedom; LR, likelihood ratio; OR, odds ratio; SROC, summary receiver operating characteristic; AUC, area under the curve; SE, standard error. Study characteristics of lymph node size per neck level Abbreviations: MRI, magnetic resonance imaging; CT, computed tomography; MR-TSE,; MR-DW,; MRSTIR,; MRSPIR,; TP, true positive; FP, false positive; TN, true negative. Meta-analysis results on diagnostic efficacy of MRI on size of metastatic lymph nodes Abbreviations: MRI, magnetic resonance imaging; SEN, sensitivity; CI, confidence interval; SPE, specificity; AUC, area under the curve; SE, standard error. Meta-analysis results on diagnostic efficacy of CT on size of metastatic lymph nodes Abbreviations: CT, computed tomography; SEN, sensitivity; CI, confidence interval; SPE, specificity; AUC, area under the curve; SE, standard error.
Table S1

Study characteristics of lymph node size per neck level

Study IDMethodUnitIIIIIIIVRetroOthersTPFPFNTN
Adams et al1 1998CTnode1212121212129617521992
Adams et al1 1998MRInode1212121212129425023917
Akoglu et al2 2005CTnode151515151515212612
Akoglu et al2 2005MRInode1515151515151611113
Anzai et al4 1994MRInode101010101010387234
Braams et al7 1995CTnode111010101010510413
Braams et al7 1995MRInode1011101010105610134
Braams et al7 1995MRInode11101010101081014167
Curtin et al9 1997CTneck level55555557415162
Curtin et al9 1997CTneck level77777756396281
Curtin et al9 1997CTneck level888888553723105
Curtin et al9 1997CTneck level999999533295148
Curtin et al9 1997CTneck level101010101010512917186
Curtin et al9 1997CTneck level1111111111114621012267
Curtin et al9 1997CTneck level1212121212124315715320
Curtin et al9 1997CTneck level151515151515327626401
Curtin et al9 1997MRIneck level55555553382595
Curtin et al9 1997MRIneck level777777523676110
Curtin et al9 1997MRIneck level888888503298148
Curtin et al9 1997MRIneck level9999994828110196
Curtin et al9 1997MRIneck level1010101010104724811229
Curtin et al9 1997MRIneck level1111111111114116717310
Curtin et al9 1997MRIneck level1212121212123813420343
Curtin et al9 1997MRIneck level151515151515306728410
Dammann et al10 2005CTneck level10101010101032178236
Dammann et al10 2005MRIneck level10101010101037143239
Ding et al12 2005MRIneck level8888881322734255
Dirix et al12 2010MR-DWneck level101010101010303293
Dirix et al12 2010MR-DWnode1010101010104045149
Dirix et al12 2010MR-DWpatient10101010101013206
Eida et al13 2003CTnode8967353162
Fan et al14 2006CTpatient101110101010231144
Fukunari et al15 2010MRnode1010101010101913066
Gross et al16 2001MRnode11101010101014322639
Gu et al17 2000MRInode10111010101083150
Guenzel et al18 2013MRnode101010101010232628
Guenzel et al18 2013MRnode151515151515206228
Guo et al19 2006MRInode10101010101083136
Hafidh et al22 2006CTnode101010101010810122
Hafidh et al22 2006MRInode101010101010111092
Hao et al21 2000MRInode1515101010103021138
Kau et al26 1999CTneck level151515151515617117
Kau et al26 1999MRIneck level151515151515217115
Kau et al26 1999CTnode1515151515151320718
Kau et al26 1999MRInode1515151515152322315
Kawai et al27 2005MRSPIRneck level I5828022
Kawai et al27 2005MRSPIRneck level I6818032
Kawai et al27 2005MRSPIRneck level I7810139
Kawai et al27 2005MRSPIRneck level I885144
Kawai et al27 2005MRSPIRneck level I981148
Kawai et al27 2005MRSPIRneck level I1050251
Kawai et al27 2005MRSTIRneck level I5824026
Kawai et al27 2005MRSTIRneck level I6816034
Kawai et al27 2005MRSTIRneck level I787043
Kawai et al27 2005MRSTIRneck level I886044
Kawai et al27 2005MRSTIRneck level I981148
Kawai et al27 2005MRSTIRneck level I1060448
Kawai et al27 2005MRSPIRneck level II52521012
Kawai et al27 2005MRSPIRneck level II62519014
Kawai et al27 2005MRSPIRneck level II72516116
Kawai et al27 2005MRSPIRneck level II82510221
Kawai et al27 2005MRSPIRneck level II9251626
Kawai et al27 2005MRSPIRneck level II10240628
Kawai et al27 2005MRSTIRneck level II52522011
Kawai et al27 2005MRSTIRneck level II62519113
Kawai et al27 2005MRSTIRneck level II72519113
Kawai et al27 2005MRSTIRneck level II82511121
Kawai et al27 2005MRSTIRneck level II9256225
Kawai et al27 2005MRSTIRneck level II10254227
Kawai et al27 2005MRSPIRneck level III55157036
Kawai et al27 2005MRSPIRneck level III66154237
Kawai et al27 2005MRSPIRneck level III77152239
Kawai et al27 2005MRSPIRneck level III88152239
Kawai et al27 2005MRSPIRneck level III99130342
Kawai et al27 2005MRSPIRneck level III1010120343
Kawai et al27 2005MRSTIRneck level III551510033
Kawai et al27 2005MRSTIRneck level III66158134
Kawai et al27 2005MRSTIRneck level III77153436
Kawai et al27 2005MRSTIRneck level III88152437
Kawai et al27 2005MRSTIRneck level III99110443
Kawai et al27 2005MRSTIRneck level III101080743
Ke et al28 2006CTnode15101010101010334
Laubenbacher et al30 1994MRIneck level15151515151513759
Laubenbacher et al30 1994MRInode1515151515156512618312
Lee et al31 2013MR-DWpatient22222273111
Lee et al31 2013MR-TSEpatient2222227618
Lu et al32 2007CTnode15101019101011136
Lwin et al33 2012MRpatient1015101051063821524
Mcguirt et al34 1995CTnode151510101010183119
Nakamoto et al35 2009MRIpatient101010101010162430
Olmos et al37 1999MRIneck level1010101010102211227
Paulus et al39 1998CTnode1515101010108104
Peters et al41 2013CTpatient333333105601
Peters et al41 2013CTpatient44444484829
Peters et al41 2013CTpatient555555629428
Peters et al41 2013CTpatient666666518539
Peters et al41 2013CTpatient77777756551
Peters et al41 2013CTpatient88888845652
Peters et al41 2013CTpatient99999931756
Peters et al41 2013CTpatient10101010101031756
Ren et al43 2000CTnode555555369211
Schwartz et al44 2004CTnode101510101010211668
Semedo et al45 2006MRnode101010101010248130
Seitz et al46 2009MRnode101010105109261218
Tai et al53 2002MRIpatient11101010101031102
Van den Brekel et al56 1991MRIneck level101010101010871342415
Van den Brekel et al56 1991MRIpatient1010101010106361546
Vandecaveye et al57 2008MR-TSEneck level101010101010271020208
Vandecaveye et al57 2008MR-TSEnode101010101010341040217
Vandecaveye et al57 2008MR-TSEpatient10101010101020517
Wang et al58 1999MRInode10101010101023015130
WIDE et al59 1999MRIneck level1015101010101811934
Wilson et al60 1994MRIneck level5555551716018
Wu et al61 2010CTnode888888101211
Yoon et al62 2008CTneck level15151010101057217326
Yoon et al62 2008MRIneck level151510101057217326
Yuan et al63 2000MRIneck level12121010101012129

Abbreviations: MRI, magnetic resonance imaging; CT, computed tomography; MR-TSE,; MR-DW,; MRSTIR,; MRSPIR,; TP, true positive; FP, false positive; TN, true negative.

Table S2

Meta-analysis results on diagnostic efficacy of MRI on size of metastatic lymph nodes

UnitNode size (mm)SEN (95% CI)SPE (95% CI)AUC (SE)Q* (SE)
Level I100.768 (0.725–0.808)0.901 (0.880–0.919)0.9159 (0.0348)0.8487 (0.0394)
110.8830.866
120.8030.786
150.774 (0.709–0.830)0.721 (0.682–0.758)0.8653 (0.0295)0.7959 (0.0287)
Level II100.812 (0.778–0.844)0.883 (0.861–0.902)0.9151 (0.0341)0.8477 (0.0385)
110.5420.953
120.8030.786
150.774 (0.709–0.830)0.721 (0.682–0.758)0.8653 (0.0295)0.7959 (0.0287)
Level III100.801 (0.767–0.833)0.894 (0.875–0.911)0.9121 (0.0314)0.8444 (0.0350)
120.8030.786
150.785 (0.712–0.846)0.704 (0.662–0.742)0.8385 (0.0274)0.7705 (0.0253)
Level IV100.801 (0.767–0.833)0.894 (0.875–0.911)0.9121 (0.0314)0.8444 (0.0350)
120.8030.786
150.785 (0.712–0.846)0.704 (0.662–0.742)0.8385 (0.0274)0.7705 (0.0253)
Retro50.8850.750
100.780 (0.742–0.814)0.899 (0.880–0.915)0.9138 (0.0315)0.8464 (0.0354)
120.8030.786
150.785 (0.712–0.846)0.704 (0.662–0.742)0.8385 (0.0274)0.7705 (0.0253)
Others100.801 (0.767–0.833)0.894 (0.875–0.911)0.9121 (0.0314)0.8444 (0.0350)
120.8030.786
150.785 (0.712–0.846)0.704 (0.662–0.742)0.8385 (0.0274)0.7705 (0.0253)

Abbreviations: MRI, magnetic resonance imaging; SEN, sensitivity; CI, confidence interval; SPE, specificity; AUC, area under the curve; SE, standard error.

Table S3

Meta-analysis results on diagnostic efficacy of CT on size of metastatic lymph nodes

UnitNode size (mm)SEN (95% CI)SPE (95% CI)AUC (SE)Q* (SE)
Level I50.9470.550
80.722 (0.465–0.903)0.966 (0.928–0.988)
100.617 (0.464–0.755)0.864 (0.770–0.930)
110.5560.565
120.8210.850
150.802 (0.711–0.875)0.677 (0.573–0.771)0.8519 (0.0818)0.7830 (0.0776)
Level II50.9470.550
80.7690.917
90.5000.970
100.607 (0.468–0.735)0.510 (0.363–0.656)0.7272 (0.1426)0.6747 (0.1157)
110.5560.565
120.8210.850
150.802 (0.711–0.875)0.818 (0.746–0.876)0.9083 (0.0599)0.8402 (0.0658)
Level III50.9470.550
60.5000.970
80.5000.970
100.746 (0.659–0.820)0.809 (0.739–0.867)0.8499 (0.0783)0.7811 (0.0740)
120.8210.850
150.723 (0.574–0.844)0.577 (0.432–0.713)
Level IV50.9470.550
70.5000.970
80.5000.970
100.746 (0.659–0.820)0.809 (0.739–0.867)0.8499 (0.0783)0.7811 (0.0740)
120.8210.850
150.723 (0.574–0.844)0.577 (0.432–0.713)
Retro50.9470.550
80.5000.970
100.746 (0.659–0.820)0.809 (0.739–0.867)0.8499 (0.0783)0.7811 (0.0740)
120.8210.850
150.723 (0.574–0.844)0.577 (0.432–0.713)
Others50.9470.550
80.5000.970
100.746 (0.659–0.820)0.809 (0.739–0.867)0.8499 (0.0783)0.7811 (0.0740)
120.8210.850
150.723 (0.574–0.844)0.577 (0.432–0.713)

Abbreviations: CT, computed tomography; SEN, sensitivity; CI, confidence interval; SPE, specificity; AUC, area under the curve; SE, standard error.

  84 in total

Review 1.  Magnetic resonance imaging vs palpation of cervical lymph node metastasis.

Authors:  M W van den Brekel; J A Castelijns; G A Croll; H V Stel; J Valk; I van der Waal; R P Golding; C J Meyer; G B Snow
Journal:  Arch Otolaryngol Head Neck Surg       Date:  1991-06

2.  Turbo short tau inversion recovery imaging for metastatic node screening in patients with head and neck cancer.

Authors:  Y Kawai; M Sumi; T Nakamura
Journal:  AJNR Am J Neuroradiol       Date:  2006 Jun-Jul       Impact factor: 3.825

3.  Comparative analysis of imaging modalities in the preoperative assessment of nodal metastasis in esophageal cancer.

Authors:  R Y Chandawarkar; T Kakegawa; H Fujita; H Yamana; N Hayabuthi
Journal:  J Surg Oncol       Date:  1996-03       Impact factor: 3.454

4.  18F-FDG PET/CT for detecting nodal metastases in patients with oral cancer staged N0 by clinical examination and CT/MRI.

Authors:  Heiko Schöder; Diane L Carlson; Dennis H Kraus; Hilda E Stambuk; Mithat Gönen; Yusuf E Erdi; Henry W D Yeung; Andrew G Huvos; Jatin P Shah; Steven M Larson; Richard J Wong
Journal:  J Nucl Med       Date:  2006-05       Impact factor: 10.057

5.  Detection of medullary thyroid carcinoma and regional lymph node metastases by magnetic resonance imaging.

Authors:  Q Wang; S Takashima; H Fukuda; F Takayama; S Kobayashi; S Sone
Journal:  Arch Otolaryngol Head Neck Surg       Date:  1999-08

6.  Preoperative evaluation of patients with primary head and neck cancer using dual-head 18fluorodeoxyglucose positron emission tomography.

Authors:  M P Stokkel; F W ten Broek; G J Hordijk; R Koole; P P van Rijk
Journal:  Ann Surg       Date:  2000-02       Impact factor: 12.969

7.  Diagnostic accuracy of 99mTc-MIBI-SPECT in the detection of lymph node metastases in patients with carcinoma of the tongue: comparison with computed tomography and MRI.

Authors:  Harsimran S Tuli; Baljinder Singh; Vikas Prasad; Asim Das; Ashok K Gupta; Bhagwant R Mittal
Journal:  Nucl Med Commun       Date:  2008-09       Impact factor: 1.690

8.  Diffusion-weighted MRI in cervical lymph nodes: differentiation between benign and malignant lesions.

Authors:  Anna Perrone; Pietro Guerrisi; Luciano Izzo; Ilaria D'Angeli; Simona Sassi; Luigi Lo Mele; Marina Marini; Dario Mazza; Mario Marini
Journal:  Eur J Radiol       Date:  2009-08-28       Impact factor: 3.528

9.  Nodal spread of squamous cell carcinoma of the oral cavity detected with PET-tyrosine, MRI and CT.

Authors:  J W Braams; J Pruim; P G Nikkels; J L Roodenburg; W Vaalburg; A Vermey
Journal:  J Nucl Med       Date:  1996-06       Impact factor: 10.057

10.  [The evaluation of cervical lymph node metastasis of laryngeal cancer using magnetic resonance imaging (MRI)].

Authors:  Y G Yuan; D M Han; E Z Fan; Y Li; F Yan; J F Xian
Journal:  Lin Chuang Er Bi Yan Hou Ke Za Zhi       Date:  2000-10
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  16 in total

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Authors:  Lars Morawietz
Journal:  Clin Orthop Relat Res       Date:  2017-06-27       Impact factor: 4.176

Review 2.  [Molecular imaging of head and neck cancers : Perspectives of PET/MRI].

Authors:  P Stumpp; S Purz; O Sabri; T Kahn
Journal:  Radiologe       Date:  2016-07       Impact factor: 0.635

3.  Elective neck dissection in T1/T2 oral squamous cell carcinoma with N0 neck: essential or not? A systematic review and meta-analysis.

Authors:  Samer Ahmed Ibrahim; Ahmed Nabil Abdelhamid Ahmed; Hisham Abdelaty Elsersy; Islam Mohammed Hussein Darahem
Journal:  Eur Arch Otorhinolaryngol       Date:  2020-02-25       Impact factor: 2.503

4.  Radiomics analysis of CT imaging improves preoperative prediction of cervical lymph node metastasis in laryngeal squamous cell carcinoma.

Authors:  Xingguo Zhao; Wenming Li; Jiulou Zhang; Shui Tian; Yang Zhou; Xiaoquan Xu; Hao Hu; Dapeng Lei; Feiyun Wu
Journal:  Eur Radiol       Date:  2022-08-19       Impact factor: 7.034

5.  Ultrasound evaluation of cervical lymphadenopathy: Can it reduce the need of histopathology/cytopathology?

Authors:  Somali Pattanayak; Samar Chatterjee; R Ravikumar; V S Nijhawan; Jyotindu Debnath
Journal:  Med J Armed Forces India       Date:  2017-05-31

6.  Real-Time Ultrasound Image Fusion with FDG-PET/CT to Perform Fused Image-Guided Fine-Needle Aspiration in Neck Nodes: Feasibility and Diagnostic Value.

Authors:  P K de Koekkoek-Doll; M Maas; W Vogel; J Castelijns; L Smit; I Zavrakidis; R Beets-Tan; M van den Brekel
Journal:  AJNR Am J Neuroradiol       Date:  2021-01-28       Impact factor: 3.825

7.  Can preoperative computed tomography predict tissue origin of primary maxillary cancer?

Authors:  Ying Yuan; Jingbo Wang; Yingwei Wu; Guojun Li; Xiaofeng Tao
Journal:  Medicine (Baltimore)       Date:  2016-10       Impact factor: 1.889

8.  Photoacoustic Molecular Imaging for the Identification of Lymph Node Metastasis in Head and Neck Cancer Using an Anti-EGFR Antibody-Dye Conjugate.

Authors:  Naoki Nishio; Nynke S van den Berg; Brock A Martin; Stan van Keulen; Shayan Fakurnejad; Eben L Rosenthal; Katheryne E Wilson
Journal:  J Nucl Med       Date:  2020-10-02       Impact factor: 10.057

9.  Tomoelastography for non-invasive detection of ameloblastoma and metastatic neck lymph nodes.

Authors:  Marie Beier; Ingolf Sack; Benedicta Beck-Broichsitter; Bernd Hamm; Stephan Rodrigo Marticorena Garcia
Journal:  BMJ Case Rep       Date:  2020-09-09

10.  The diagnostic value of 1.5-T diffusion-weighted MR imaging in detecting 5 to 10 mm metastatic cervical lymph nodes of nasopharyngeal carcinoma.

Authors:  Guan Qiao Jin; Jun Yang; Li Dong Liu; Dan Ke Su; Duo Ping Wang; Sheng Fa Zhao; Zhi Ling Liao
Journal:  Medicine (Baltimore)       Date:  2016-08       Impact factor: 1.889

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