Diagnostic Approach Lympnode Metastase With Usg and Fna

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    38 AJR:194 , January 2010

    larity on color Doppler images [3, 6, 8, 9, 14].

    Recent studies have shown excellent diag-

    nostic performance using a combination of

    various ultrasound characteristics [3, 710].

    However, loss of fatty hilum as a diagnostic

    ultrasound criterion of metastatic lymph

    nodes has been the subject of debate [1619].

    The cytology results of metastatic thyroid

    cancer in cervical lymph nodes displayed

    a higher frequency of foamy macrophages

    (38.5%) and cystic degeneration (44.7%),even though no malignant cells were found

    on cytology [20]. However, to the best of

    our knowledge, the frequency of metastasis

    according to each cytology result of lymph

    nodes has not been reported. Therefore, in

    this study we investigated the most accurate

    criteria to differentiate metastatic from be-

    nign lymph nodes on ultrasound and evalu-

    ated the frequency of metastasis according to

    the cytology results.

    Diagnostic Approach for Evaluation

    of Lymph Node Metastasis FromThyroid Cancer Using Ultrasoundand Fine-Needle Aspiration Biopsy

    Yu-Mee Sohn1,2

    Jin Young Kwak1

    Eun-Kyung Kim1

    Hee Jung Moon1

    Soo Jin Kim1

    Min Jung Kim1

    Sohn YM, Kwak JY, Kim EK, Moon HJ, Kim SJ,

    Kim MJ

    1Department of Radiology, Research Institute of

    Radiological Science, Yonsei University College ofMedicine, 250 Seongsanno, Seodaemun-gu, Seoul

    120-752, South Korea. Address correspondence to

    J. Y. Kwak ([email protected]).

    2Department of Radiology, Kyung Hee University Medical

    Center, Seoul, South Korea.

    Neuroradiology/Head and Neck Imaging Original Research

    AJR2010; 194:384 3

    0361803X/10/194138

    American Roentgen Ray Society

    Thyroid cancer often metastasizes

    to cervical lymph nodes, and ear-

    ly detection of metastasis is im-

    portant for planning surgery and

    management of patients [1]. Ultrasound is the

    imaging method of choice for detecting and

    characterizing cervical lymph nodes in thy-

    roid cancer and providing guidance for fine-

    needle aspiration biopsy (FNAB) [1]. Ultra-

    sound and ultrasound-guided FNAB are the

    main diagnostic tools for detecting cervicalmetastasis of thyroid cancer by preoperative

    cytologic analysis and recurrence after thy-

    roid surgery [25]. Numerous previous re-

    ports have described the ultrasound character-

    istics of metastatic lymph nodes of papillary

    thyroid cancer, such as the presence of calcifi-

    cation [1, 3, 510], cystic change [1, 3, 512],

    loss of an echogenic fatty hilum [3, 510, 13

    15], hyperechogenicity [3, 6, 810], round

    shape [3, 510, 13, 14], and abnormal vascu-

    Keywords:fine-needle aspiration biopsy, lymph node

    metastasis, ultrasound

    DOI:10.2214/AJR.09.3128

    Received June 3, 2009; accepted after revision

    July 2, 2009.

    FOCUSON:

    OBJECTIVE.The purpose of our study was to investigate ultrasound criteria to deter-

    mine the most accurate criterion to differentiate metastatic from benign lymph nodes on ul-

    trasound and to evaluate the frequency of metastasis according to the cytology results.

    MATERIALS AND METHODS.One hundred eighteen consecutive patients with thy-

    roid malignancy underwent fine-needle biopsy of suspicious lymph nodes. We investigated

    the diagnostic performance of each ultrasound feature (loss of fatty hilum, presence of cystic

    change or calcification, hyperechogenicity, and round shape) and ultrasound criteria 1 and 2.We considered criterion 1 to be if one of the aforementioned malignant ultrasound findings

    was present and criterion 2 to be if one of the aforementioned malignant ultrasound findings,

    excluding the loss of fatty hilum, was present. Cytology results were divided into metastasis,

    macrophages without malignant cells, cell paucity, and negative for malignancy, and we eval-

    uated the frequency of metastasis.

    RESULTS.There were 91 metastatic and 27 benign nodes. The area under the receiver

    operating characteristic curve value of criterion 2 was significantly higher than that of crite-

    rion 1. The frequency of metastasis was highest with a cytologic result of metastasis (95.8%),

    followed by macrophages without malignant cells (87.5%), cell paucity (71.4%), and negative

    for malignancy (34.4%).

    CONCLUSION.The most accurate ultrasound criterion to differentiate metastatic from

    benign lymph nodes was ultrasound criterion 2 (any suspicious ultrasound features except for

    loss of fatty hilum), and we should not neglect lymph nodes with suspicious ultrasound fea-

    tures, even if they do not contain malignant cells on cytology.

    Sohn et al.Ultrasound and FNAB of Lymph Node Metastasis

    Neuroradiology/Head and Neck ImagingOriginal Research

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    AJR:19 4, January 2010 39

    Ultrasound and FNAB of Lymph Node Metastasis

    Materials and Methods

    Patients

    The institutional review board approved this

    retrospective observational study and required nei-

    ther patient approval nor patient informed consent

    for the review of images and records. Informed

    consent was obtained from all patients before

    FNAB. From January 2003 to December 2005,

    135 consecutive patients at our institution under-

    went FNAB due to suspicious metastatic cervical

    lymph nodes of papillary thyroid carcinoma. Dur-

    ing the study period, we considered a lymph node

    to be suspicious when it had one of following fea-

    tures: loss of fatty hilum, cystic change, calcifica-

    tion, hyperechogenicity (higher echogenicity than

    the surrounding muscles), and round shape (long

    to transverse diameter ratio < 1.5). Doppler ultra-

    sound was not routinely performed. Eight lymph

    nodes in eight patients were excluded because

    there was no subsequent surgical excision or long-

    term imaging follow-up for at least 2 years. Nine

    patients also were excluded because ultrasound

    examinations were unavailable. Ultimately, 118lymph nodes in 118 patients were included in this

    analysis. Forty-eight patients had already under-

    gone surgery for thyroid papillary carcinoma, and

    the remaining 70 had no pr ior surgery for cytologi-

    cally confirmed papillary carcinoma (Table 1).

    Imaging and Image Analyses

    Ultrasound evaluation of cervical lymph nodes

    was undertaken using a 7-15MHz linear-array

    transducer (HDI 5000, Philips Healthcare) and

    8-15MHz linear-array transducer (Acuson Se-

    quoia, Siemens Healthcare). Compound imaging

    was performed in all cases using the HDI 5000

    machine, and lymph node sizes were measured

    along the longest diameter on transverse scans.

    Two radiologists with 2 and 8 years of expe-

    rience with thyroid imaging retrospectively re-

    viewed the thyroid ultrasound examinations in

    consensus. They had no knowledge of the clini-

    cal history or cytopathologic results of the patients

    while performing the consensus reading. Suspi-

    cious ultrasound features of lymph nodes were

    the following: loss of fatty hilum, cystic change,

    calcification, hyperechogenicity (higher echoge-

    nicity than the surrounding muscles), and round

    shape (long to transverse diameter ratio < 1.5)

    (Figs. 13). The ultrasound results were grouped

    as positive (suspicious) and negative (benign),

    and lymph nodes were considered positive if one

    of the malignant sonographic findings was pres-

    ent on ultrasound (cr iterion 1) [1, 3, 510]. Lymph

    nodes were also considered positive if one of the

    malignant sonographic findings was present, ex-

    cluding loss of fatty hilum (criterion 2), on ultra-

    sound [1619].

    Preoperative Evaluation of Lymph Nodes

    At our institution, we performed ultrasound-

    guided FNAB on lymph nodes with suspicious ul-

    trasound features. However, we did not perform

    ultrasound-guided FNAB on central lymph nodes

    with suspicious ultrasound features in patients

    who were scheduled for thyroidectomy because

    routine central lymph node dissections were per-

    formed at the time of thyroidectomy. Lymph nodes

    were considered suspicious during the study peri-od when one of the suspicious ultrasound findings

    (loss of fatty hilum, calcifications, cystic change,

    hyperechogenicity, and round shape) was present.

    Ultrasound-guided FNAB was performed by

    one of three radiologists who had 4, 6, and 10

    years of experience with thyroid imaging. They

    were aware of the patients clinical histories. Ul-

    trasound-guided FNAB was performed with a

    23-gauge needle attached to a 20-mL disposable

    plastic syringe and aspirator. Materials obtained

    from FNAB were smeared on glass slides. All

    smears were placed in 95% alcohol for Papanico-

    lau staining, and the remaining material was rinsed

    in saline to be processed as a cell block. The cyto-

    pathologist was not on site during the biopsy.

    Cytopathologic Evaluation

    One of five cytopathologists interpreted the ul-

    trasound-guided FNAB according to their sched-

    ules. They were blinded with respect to the ul-

    trasound diagnosis. At our institution, cytology

    results were divided into one of the following four

    categories: metastasis, macrophages without ma-

    lignant cells, cell paucity, and negative for ma-

    lignancy. Metastasis was defined as positive for

    metastatic thyroid carcinoma [3], macrophages

    without malignant cells were reported when cy-

    tology showed foamy macrophages with no malig-

    nant cells [20], cell paucity was assigned in cases

    with insufficient material [3], and negative for ma-

    lignancy included reactive lymph nodes or other

    benign lymphadenitis [3]. We used the initial cy-

    tologic report for the cytopathologic evaluations.

    Surgical Protocol and Histopathologic Analyses

    When cytology results revealed malignant cells

    in lymph nodes, unilateral modified neck dissec-

    tion was performed as the initial thyroid surgery.

    However, selective frozen sectioning was per-

    formed as the initial thyroid surgery in patients

    with lymph nodes with suspicious ultrasound fea-tures but no definite malignant cells on cytology.

    Selective dissection was performed in patients

    who had already undergone thyroid surgery.

    We evaluated the final results of aspirated

    lymph nodes in level-by-level analyses and com-

    pared them to pathology reports.

    TABLE 1: Aspirated Lymph Nodes in 118 Patients

    Levels of Aspirated LymphNodes

    No. of Patients

    Initial Surgery (n= 70) Postsurgery (n= 48)

    I 1

    II 4 8

    III 31 14

    IV 28 19

    V 7 4

    VI 2

    Fig. 137-year-oldwoman with level IVmetastatic lymph nodein left neck. Ultrasoundimage shows loss of fattyhilum, microcalcification,and hyperechogenicityin lymph node (arrows).Cytology resultsconfirmed lymph nodemetastasis.

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    Sohn et al.

    Statistical AnalysesA reference standard was set by pathology re-

    sults from lymph node dissections or long-term

    imaging follow-up for at least 2 years with no sub-

    sequent surgical excision. Categorical data were

    summarized using frequencies and percentages.

    The Students t test was used to determine dif-

    ferences between metastatic and benign lymph

    nodes according to age and lymph node size on

    ultrasound. The chi-square test was performed to

    evaluate the differences between benign and ma-

    lignant groups by sex.

    Diagnostic performance, including sensitiv-

    ity, specificity, accuracy, positive predictive val-

    ue (PPV), and negative predictive value (NPV),

    was calculated according to the ultrasound find-

    ings. We also examined diagnostic performance

    by ultrasound grouping (criteria 1 and 2). The chi-

    square test or Fishers exact test was used to com-

    pare each ultrasound finding to standard results.

    Receiver operating characteristic (ROC) curve

    analysis was performed to compare the two ul-

    trasound criteria to differentiate metastatic from

    benign lymph nodes. We evaluated the frequency

    of metastasis according to cytology results. Statis-

    tical significance was assumed when the pvalue

    was less than 0.05.

    Results

    This study included 23 men and 95 women

    with a mean age of 51 13.4 years. The mean

    size of lymph nodes was 13.8 8.5 mm.

    Pathologic confirmations were obtained from

    115 patients. There were 91 malignant and

    24 benign results on pathology. Three pa-

    tients who did not undergo surgery had nodes

    that decreased in size during the long-term

    imaging follow-up duration of at least 2

    years. Therefore, this study consisted of 91

    malignant and 27 benign lymph nodes. There

    was no significant difference between meta-

    static and benign lymph nodes according to

    age (p = 0.765) and sex (p = 0.071). The

    mean longest diameter of metastatic lymph

    nodes (14.5 mm 9 mm) was significantly

    larger than that of benign nodes (11.4 mm

    5.8 mm) (p= 0.042).

    The diagnostic performance of each ultra-

    sound finding in this study is shown in Table 2.

    Ultrasound criteria 1 and 2 as well as each

    suspicious ultrasound feature had statistical

    significance with metastasis. Most ultrasound

    features had high specificity and PPV but low

    sensitivity and NPV. However, loss of fatty hi-

    lum had the highest sensitivity and NPV but

    showed lower specificity than other ultrasound

    features. When each ultrasound feature and

    ultrasound criteria 1 and 2 were compared,

    criterion 2 had the highest accuracy. The area

    under the ROC curve value (0.83; 95% CI,

    0.7390.920] of criterion 2 was significantly

    higher than that (0.704; 95% CI, 0.6090.798)

    of criterion 1 (p= 0.006) (Fig. 4).

    Fig. 256-year-old woman with level IV metastatic lymph nodes in right neck.Ultrasound image shows microcalcification (arrow), loss of fatty hilum, and roundshape in lymph nodes (arrowheads). Cytology results confirmed lymph nodemetastasis.

    Fig. 332-year-old woman with level II metastatic lymph nodes in left neck.Ultrasound image shows loss of fatty hilum and cystic change. Cytology resultsconfirmed macrophages without malignant cells.

    TABLE 2: Diagnostic Accuracy of Each Ultrasound Feature

    Ultrasound Feature TP TN FP FNSensitivity

    (%)Specificity

    (%) Accuracy (%) PPV (%) NPV (%)

    Loss of fatty hilum 91 13 14 0 100 (91/91) 48 (13/27) 88 (104/118) 87 (91/105) 100 (13/13)

    Cystic change 31 26 1 60 34 (31/91) 96 (26/27) 48 (57/118) 97 (31/32) 30 (26/86)Presence of calcification 41 25 2 50 45 (41/91) 93 (25/27) 56 (66/118) 95 (41/43) 33 (25/75)

    Hyperechogenicity 54 23 4 37 59 (54/91) 85 (23/27) 65 (77/118) 93 (54/58) 38 (23/60)

    Round shape 50 24 3 41 55 (50/91) 89 (24/27) 63 (74/118) 94 (50/58) 37 (24/65)

    Any suspicious ultrasound feature (criterion 1) 91 11 16 0 100 (91/91) 41 (11/27) 86 (102 /118) 85 (91/107) 100 (11/11)

    Any suspicious ultrasound feature, excludingloss of fatty hilum (criterion 2)

    87 19 8 4 96 (87/91) 70 (19/27) 89 (106/118) 92 (87/95) 83 (19/23)

    NoteData in parentheses are number of cases. TP = true-positive, TN = true-negative, FP = false-positive, FN = false-negative, PPV = positive predictive value,NPV = negative predictive value.

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    AJR:19 4, January 2010 41

    Ultrasound and FNAB of Lymph Node Metastasis

    The frequency of metastasis was highest

    with a cytology reading of metastasis (68/71,

    95.8%), followed by macrophages without

    malignant cells (7/8, 87.5%), cell paucity

    (5/7, 71.4%), and negative for malignancy

    (11/32, 34.4%).

    Discussion

    Ultrasound characteristics of metastatic

    lymph nodes of thyroid cancer have been re-

    ported by several investigators [1, 5, 6, 11].

    Major ultrasound characteristics suggest-

    ing metastasis of thyroid cancer included the

    presence of calcification [1, 3, 510], cystic

    change [1, 3, 512], loss of echogenic fatty

    hilum [3, 510, 1315], hyperechogenicity

    [3, 6, 810], round shape [3, 510, 13, 14],

    and abnormal vascularity [3, 6, 8, 9, 14]. The

    results of previous studies [5, 711] that ex-

    amined diagnostic performance of each ul-

    trasound characteristic are shown in Table 3.

    The frequency of metastasis was 62.0100%

    in lymph nodes with absent hilum [5, 710],19.080.0% in those with round shapes [7

    10], 58.086.0% in those with hyperechoge-

    nicity [810], 3.049.5% in those with calci-

    fication [5, 711], 13.270.0% in those with

    cystic change [5, 7, 911], and 47.047.6% in

    those with abnormal vascularity [8, 9].

    Of these ultrasound characteristics, sever-

    al studies have shown that calcification and

    cystic change have 100% specificity and PPV

    [10, 11] and that they are not observed in nor-

    mal or reactive lymph nodes [10]. Calcifica-

    tions in metastatic lymph nodes are shown in

    punctate microcalcifications on ultrasound,

    and these calcifications are laminated, cal-cified, spherical bodies on cytology that are

    called psammoma bodies [21]. Psammoma

    bodies were reported to be formed by calci-

    fication of intravascular tumor thrombi or in-

    farcted tips of malignant papillae, and their

    presence is considered to be diagnostic of

    malignancy [22]. Some investigators have

    reported that cystic degeneration of lymph

    nodes was highly suggestive of metastasis in

    thyroid cancer [1, 11, 23] and squamous cell

    carcinoma of the head and neck [23]. Thy-

    roid papillary carcinoma most commonly

    showed cystic formation in lymph node me-

    tastasis, and the incidence of cystic change of

    lymph nodes in thyroid cancer was reported

    in 1025% of cases [23]. This cystic change

    is the result of liquefaction necrosis [12] or

    spontaneous or postradiotherapeutic central

    breakdown of keratin, which gives the node a

    pseudocystic appearance [24]. Cystic chang-

    es are shown on ultrasound as small solitary

    cystic areas, multiple peripheral cystic areas,

    or almost complete replacement of the node

    by cystic formation [11]. Another study [12]

    reported that pure cystic change was most-

    ly found in young adults. These ultrasound

    findings were explained by the increased ag-

    gressiveness of tumors at a young age, which

    caused extensive necrosis [24]. In the current

    study, cystic change also had high specificity

    and PPV as diagnostic ultrasound features.

    Several investigators revealed good re-sults on preoperative staging when the cri-

    terion involving one suspicious finding was

    present on ultrasound [9, 17, 25, 26]. In this

    study, we evaluated diagnostic performance

    in the diagnosis of metastasis with combined

    ultrasound criteria (1 and 2) as well as sus-

    picious ultrasound findings, such as loss of

    fatty hilum, calcification, cystic change, hy-

    perechogenicity, and round shape. Most ul-

    trasound features had high specificity and

    PPV but low sensitivity and NPV. However,

    loss of fatty hilum had the highest sensitiv-

    ity and NPV but lower specificity than oth-

    er ultrasound features. This result is consis-tent with previous reports [1619] that loss

    of fatty hilum is not a definite criterion for

    differentiation between malignant and be-

    nign lymph nodes. When each ultrasound

    feature and ultrasound criteria 1 and 2 were

    compared, criterion 2 had the highest accu-

    racy, with a significantly higher area under

    the curve value than criterion 1. The results

    correspond to those of previous studies that

    loss of fatty hilum is not a specific ultrasound

    feature for malignancy [1619].

    Until now, malignant cells on cytology

    have been considered suggestive of metasta-

    sis, prompting surgical management. How-

    ever, the frequency of metastasis has been

    reported rarely on other cytologic results of

    suspicious lymph nodes on ultrasound, to thebest of our knowledge. Cytology results of

    metastatic thyroid cancer in cervical lymph

    nodes displayed a higher frequency of foamy

    macrophages (38.5%), even if no malignant

    cells were found on cytology [20, 23]. In this

    study, we categorized cytologic results as

    metastasis, presence of macrophages with-

    out malignant cells, cell paucity, and nega-

    tive for malignancy. The inclusion of mac-

    rophages in this criterion was supported by

    a previous report [20]. The frequency of me-

    tastasis was the highest in lymph nodes with

    suspicious ultrasound features having malig-

    nant cells (95.8%), followed by macrophag-

    es without malignant cells (87.5%), cell pau-

    city (71.4%), and negative for malignancy

    (34.4%).

    When metastatic lymph nodes were diag-

    nosed on cytology, functional compartment

    en bloc dissection was preferred over selec-

    tive dissection (berry picking) because of

    improved mortality [2730]. However, we

    cannot neglect a lymph node with a suspi-

    cious ultrasound feature, even when it does

    not have malignant cells on cytology. A re-

    cent study [31] reported an effective meth-

    od of preoperative ultrasound-guided tattoo-ing using charcoal suspension for localizing

    nonpalpable cervical recurrent lymph nodes

    after thyroidectomy. This method can be ap-

    plied to suspicious lymph nodes on ultra-

    sound as a preoperative ultrasound marking

    for sampling with frozen sectioning and de-

    termining further surgical treatment. There-

    fore, we suggest that frozen sampling with

    preoperative ultrasound marking should be

    performed for pathologic confirmation of a

    lymph node with a suspicious ultrasound fea-

    ture to prevent undertreatment of patients.

    In addition to FNAB, several studies [3,

    4, 17, 3234] have reported the detection ofthyroglobulin (Tg) in FNAB washout fluid.

    FNAB-Tg identified metastasis and recur-

    rence of the neck with excellent sensitivity

    and specificity, especially cystic metastatic

    lymph nodes, which can show a higher inci-

    dence of false-negative findings on cytology

    than metastatic lymph nodes without cystic

    change [3, 23, 32, 33]. Moreover, the FNAB-

    Tg test and the combination of FNAB-Tg and

    1.0

    Sensitivity

    1 Specificity

    0.8

    0.6

    0.4

    0.2

    00 1.00.80.60.40.2

    Fig. 4Graph showsreceiver operatingcharacteristic curveof two ultrasoundcriteria to differentiatemetastatic from benignlymph nodes. Areaunder ROC curve value(0.83) of criterion 2

    (dashed line) wassignificantly higher than

    that of criterion 1 (0.704)(solid line).

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    FNAB cytology have been shown to be more

    sensitive and accurate than FNAB cytology

    alone [3, 32, 34]. However, the current study

    was a retrospective study, and additional Tg

    data could not be obtained.

    The first limitation of the current study

    is that it is retrospective and included only

    patients who underwent ultrasound-guidedFNAB and thyroid surgery or imaging fol-

    low-up for at least 2 years. Therefore, selec-

    tion bias does exist. Second, the high percent-

    age of included lymph nodes with metastasis

    with suspicious features on initial ultrasound

    resulted in incomplete examination of the

    most accurate criterion to differentiate ma-

    lignant from benign lymph nodes. This was

    another form of selection bias. Third, abnor-

    mal vascularity of lymph nodes was not in-

    cluded, and inclusion was not possible be-

    cause of the retrospective design. Fourth, we

    used the initial cytologic results of the lymph

    nodes. In the study period, five cytopatholo-

    gists interpreted the FNAB slides at our in-

    stitution. This was a limitation of the study

    because of the possibility of interobserver

    variability in cytologic interpretations. Fifth,

    we could not perform a node-by-node analy-

    sis of all lymph nodes and instead, a level-

    by-level analysis was performed. Lastly, the

    study included a relatively small number of

    patients. Further prospective study will be

    necessary to resolve these issues.

    In conclusion, the most accurate ultra-

    sound criterion to differentiate metastatic

    from benign lymph nodes was ultrasoundcriterion 2 (any suspicious ultrasound fea-

    tures except loss of fatty hilum), and we

    should not neglect lymph nodes with suspi-

    cious ultrasound features, even if they do not

    contain malignant cells on cytology.

    Acknowledgments

    The authors are grateful to Kyung Hwa

    Han, biostatistician, Department of Research

    Affairs, Yonsei University College of Medi-

    cine, Seoul, Korea, for her help with the sta-

    tistics in this study.

    References 1. Miseikyte-Kaubriene E, Trakymas M, Ulys A. Cys-

    tic lymph node metastasis in papillary thyroid carci-

    noma.Medicina (Kaunas)2008; 44:455459

    2. Boland GW, Lee MJ, Mueller PR, Mayo-Smith W,

    Dawson SL, Simeone JF. Efficacy of sonographi-

    cally guided biopsy of thyroid masses and cervi-

    cal lymph nodes.AJR1993; 161:10531056

    3. Jeon SJ, Kim E, Park JS, et al. Diagnostic benefit

    of thyroglobulin measurement in fine-needle aspi-

    ration for diagnosing metastatic cervical lymph

    nodes from papillary thyroid cancer: correlations

    with US features. Korean J Radiol2009; 10:106

    111

    4. Kim MJ, Kim EK, Kim BM, et al. Thyroglobulin

    measurement in fine-needle aspirate washouts:

    the criteria for neck node dissection for patients

    with thyroid cancer. Clin Endocrinol (Oxf)2009;

    70:145151

    5. Takashima S, Sone S, Nomura N, Tomiyama N,

    Kobayashi T, Nakamura H. Nonpalpable lymph

    nodes of the neck: assessment with US and US-

    guided fine-needle aspiration biopsy. J Clin Ul-

    trasound1997; 25:283292

    6. Fish SA, Langer JE, Mandel SJ. Sonographic im-

    aging of thyroid nodules and cervical lymph

    nodes. Endocrinol Metab Clin North Am 2008;

    37:401417, ix

    7. Kuna SK, Bracic I, Tesic V, Kuna K, Herceg GH,

    Dodig D. Ultrasonographic differentiation of be-

    nign from malignant neck lymphadenopathy in

    thyroid cancer.J Ultrasound Med2006; 25:1531

    1537; quiz 15381540

    8. Lyshchik A, Higashi T, Asato R, et al. Cervical

    lymph node metastases: diagnosis at sonoelastog-

    raphyinitial experience. Radiology 2007; 243:

    258267

    9. Park JS, Son KR, Na DG, Kim E, Kim S. Perfor-

    mance of preoperative sonographic staging of

    papillary thyroid carcinoma based on the sixth

    edition of the AJCC/UICC TNM classification

    system.AJR2009; 192:6672

    10. Rosario PW, de Faria S, Bicalho L, et al. Ultra-

    sonographic differentiation between metastatic

    and benign lymph nodes in patients with papillarythyroid carcinoma. J Ultrasound Med2005; 24:

    13851389

    11. Kessler A, Rappaport Y, Blank A, Marmor S,

    Weiss J, Graif M. Cystic appearance of cervical

    lymph nodes is characteristic of metastatic papil-

    lary thyroid carcinoma.J Clin Ultrasound2003;

    31:2125

    12. Wunderbaldinger P, Harisinghani MG, Ha hn PF,

    et al. Cystic lymph node metastases in papillary

    thyroid carcinoma.AJR2002; 178:693697

    13. Ahuja A, Ying M, King A, Yuen HY. Lymph node

    hilus: gray scale and power Doppler sonography

    of cervical nodes. J Ultrasound Med 2001; 20:

    987992; quiz 994

    14. Na DG, Lim HK, Byun HS, Kim HD, Ko YH,

    Baek JH. Differential diagnosis of cervical lymph-

    adenopathy: usefulness of color Doppler sonogra-

    phy.AJR1997; 168:13111316

    15. Ying M, Ahuja A, Metreweli C. Diagnostic accu-

    racy of sonographic criteria for evaluation of cer-

    vical lymphadenopathy.J Ultrasound Med1998;

    17:437445

    16. Ahuja A, Ying M. Sonography of neck lymph

    T

    ABLE3:PreviousReportsofDiagnosticValuesAccordingtoUltrasoundCriteriatoDifferentiateMetastaticFromB

    enignLymphNodes

    Study

    [ReferenceNo.]

    Total

    No.o

    f

    Lymph

    Nodes

    No.o

    f

    Metastatic

    Lymph

    Nodes

    Short-to-LongAxis

    DiameterRatio>0.5

    AbnormalEchogenicity

    Calcification

    CysticChange

    AbsentHilum

    PeripheralVascularity

    Sensitivity

    (%)

    Specificity

    (%)

    PPV

    (%)

    Sensitivity

    (%)

    Specific

    ity

    (%)

    PPV

    (%)

    Sensitivity

    (%)

    Specificity

    (%)

    PPV

    (%)

    Sensitivity

    (%)

    Specificity

    (%)

    PPV

    (%)

    Sensitivity

    (%)

    Specificity

    (%)

    PPV

    (%)

    Sensitivity

    (%)

    Specificity

    (%)

    PPV

    (%)

    Lyshchiketal.[8]

    141

    60

    75

    81

    75

    58

    91

    83

    3

    100

    100

    NA

    NA

    NA

    72

    54

    54

    47

    99

    97

    Kessleretal.[11]

    63

    20

    NA

    NA

    NA

    NA

    NA

    NA

    30

    NA

    NA

    70

    NA

    NA

    NA

    NA

    NA

    NA

    NA

    NA

    Takashimaetal.[5]

    91

    53

    NA

    NA

    NA

    NA

    NA

    NA

    92

    63

    78

    92

    61

    77

    100

    21

    64

    NA

    NA

    NA

    Parketal.[9]

    45

    21

    23.8

    80.2

    66.7

    78.9

    42.9

    78.9

    31.6

    100

    100

    26.3

    100

    100

    31.6

    71.4

    75.0

    52.6

    57.1

    76.9

    Kunaetal.[7]

    517

    221

    65.6

    NA

    NA

    NA

    NA

    NA

    5.4

    NA

    NA

    21.3

    NA

    NA

    99.5

    NA

    NA

    NA

    NA

    NA

    Rosarioetal.[10]

    350

    198

    80

    70.5

    78

    86

    95.5

    96

    49.5

    100

    100

    20

    100

    100

    88

    90

    92

    NA

    NA

    NA

    Thisstudy

    118

    91

    55

    89

    94

    59

    85

    93

    45

    93

    95

    34

    96

    97

    100

    48

    87

    NA

    NA

    NA

    NotePPV=positivepredictivevalue,NA=notapplicable.

  • 8/10/2019 Diagnostic Approach Lympnode Metastase With Usg and Fna

    6/6

    AJR:19 4, January 2010 43

    Ultrasound and FNAB of Lymph Node Metastasis

    nodes. Part II. Abnormal lymph nodes. Clin Ra-

    diol2003; 58:359366

    17. Kim E, Park JS, Son KR, Kim JH, Jeon SJ, Na

    DG. Preoperative diagnosis of cervical metastatic

    lymph nodes in papillary thyroid carcinoma:

    comparison of ultrasound, computed tomography,

    and combined ultrasound with computed tomog-

    raphy. Thyroid2008; 18:411418

    18. Tsunodo-Shimizu H, Saida Y. Ultrasonographic

    visibility of supraclavicular lymph nodes in normal

    subjects.J Ultrasound Med1997; 16:481483

    19. Vassallo P, Wernecke K, Roos N, Peters PE. Dif-

    ferentiation of benign from malignant superficial

    lymphadenopathy: the role of high-resolution US.

    Radiology1992; 183:215220

    20. Tseng FY, Hsiao YL, Chang TC. Cytologic fea-

    tures of metastatic papillary thyroid carcinoma in

    cervical lymph nodes.Acta Cytol2002; 46:1043

    1048

    21. Ahuja AT, Chow L, Chick W, King W, Metreweli

    C. Metastatic cervical nodes in papillary carcino-

    ma of the thyroid: ultrasound and histological cor-

    relation. Clin Radiol1995; 50:229231

    22. Ellison E, Lapuer ta P, Mart in SE. Psammoma

    bodies in fine-needle aspirates of the thyroid: pre-

    dictive value for papillary carcinoma. Cancer

    1998; 84:169175

    23. Ustun M, Risberg B, Davidson B, Berner A. Cys-

    tic change in metastatic lymph nodes: a common

    diagnostic pitfall in fine-needle aspiration cytolo-

    gy.Diagn Cytopathol2002; 27:387392

    24. Verge J, Guixa J, Alejo M, et al. Cervical cystic

    lymph node metastasis as first manifestation of

    occult papillary thyroid carcinoma: report of sev-

    en cases.Head Neck1999; 21:370374

    25. Gonzalez HE, Cruz F, OBrien A, et al. Impact of

    preoperative ultrasonographic staging of the neck

    in papillary thyroid carcinoma.Arch Otolaryngol

    Head Neck Surg2007; 133:12581262

    26. Shimamoto K, Satake H, Sawaki A, Ish igaki T,

    Funahashi H, Imai T. Preoperative staging of thy-

    roid papillary carcinoma with ultrasonography.

    Eur J Radiol1998; 29:410

    27. Cooper DS, Doherty GM, Haugen BR, et al. Man-

    agement guidelines for patients with thyroid nod-

    ules and differentiated thyroid cancer. Thyroid

    2006; 16:109142

    28. Goropoulos A, Karamoshos K, Christodoulou A,

    et al. Value of the cervical compartments in the

    surgical treatment of papillary thyroid carcinoma.

    World J Surg2004; 28:12751281

    29. Kupferman ME, Patterson M, Mandel SJ, LiVolsi

    V, Weber RS. Patterns of lateral neck metastasis

    in papillary thyroid carcinoma.Arch Otolaryngol

    Head Neck Surg2004; 130:857860

    30. Wang TS, Dubner S, Sznyter LA, Heller KS. Inci-

    dence of metastatic well-differentiated thyroid

    cancer in cervical lymph nodes.Arch Otolaryngol

    Head Neck Surg2004; 130:110113

    31. Kang TW, Shin JH, Han BK, et al. Preoperative

    ultrasound-guided tattooing localization of recur-

    rences after thyroidectomy: safety and effective-

    ness.Ann Surg Oncol 2009; 16:16551659

    32. Cignarelli M, Ambrosi A, Marino A, et al. Diag-

    nostic utility of thyroglobulin detection in fine-

    needle aspiration of cervical cystic metastatic

    lymph nodes from papillary thyroid cancer with

    negative cytology. Thyroid2003; 13:11631167

    33. Cunha N, Rodrigues F, Curado F, et al. Thyro-

    globulin detection in fine-needle aspirates of cer-

    vical lymph nodes: a technique for the diagnosis

    of metastatic differentiated thyroid cancer. Eur J

    Endocrinol2007; 157:101107

    34. Frasoldati A , Toschi E, Zini M, et al. Role of thy-

    roglobulin measurement in fine-needle aspiration

    biopsies of cervical lymph nodes in patients with

    differentiated thyroid cancer. Thyroid 1999; 9:

    105111