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Research ArticleHead and Neck Imaging

CT Texture Analysis of Cervical Lymph Nodes on Contrast-Enhanced [18F] FDG-PET/CT Images to Differentiate Nodal Metastases from Reactive Lymphadenopathy in HIV-Positive Patients with Head and Neck Squamous Cell Carcinoma

H. Kuno, N. Garg, M.M. Qureshi, M.N. Chapman, B. Li, S.K. Meibom, M.T. Truong, K. Takumi and O. Sakai
American Journal of Neuroradiology March 2019, 40 (3) 543-550; DOI: https://doi.org/10.3174/ajnr.A5974
H. Kuno
aFrom the Departments of Radiology (H.K., N.G., M.M.Q., M.N.C., B.L., S.K.M., M.T.T., K.T., O.S.)
dDepartment of Diagnostic Radiology (H.K.), National Cancer Center Hospital East, Kashiwa, Chiba, Japan
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  • ORCID record for H. Kuno
N. Garg
aFrom the Departments of Radiology (H.K., N.G., M.M.Q., M.N.C., B.L., S.K.M., M.T.T., K.T., O.S.)
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M.M. Qureshi
aFrom the Departments of Radiology (H.K., N.G., M.M.Q., M.N.C., B.L., S.K.M., M.T.T., K.T., O.S.)
bRadiation Oncology (M.M.Q., M.T.T., O.S.)
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M.N. Chapman
aFrom the Departments of Radiology (H.K., N.G., M.M.Q., M.N.C., B.L., S.K.M., M.T.T., K.T., O.S.)
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B. Li
aFrom the Departments of Radiology (H.K., N.G., M.M.Q., M.N.C., B.L., S.K.M., M.T.T., K.T., O.S.)
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S.K. Meibom
aFrom the Departments of Radiology (H.K., N.G., M.M.Q., M.N.C., B.L., S.K.M., M.T.T., K.T., O.S.)
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M.T. Truong
aFrom the Departments of Radiology (H.K., N.G., M.M.Q., M.N.C., B.L., S.K.M., M.T.T., K.T., O.S.)
bRadiation Oncology (M.M.Q., M.T.T., O.S.)
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K. Takumi
aFrom the Departments of Radiology (H.K., N.G., M.M.Q., M.N.C., B.L., S.K.M., M.T.T., K.T., O.S.)
eDepartment of Radiology (K.T.), Kagoshima University Graduate School of Medical and Dental Sciences, Kagoshima, Japan.
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O. Sakai
aFrom the Departments of Radiology (H.K., N.G., M.M.Q., M.N.C., B.L., S.K.M., M.T.T., K.T., O.S.)
bRadiation Oncology (M.M.Q., M.T.T., O.S.)
cOtolaryngology–Head and Neck Surgery (O.S.), Boston Medical Center, Boston University School of Medicine, Boston, Massachusetts
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    Fig 1.

    Flowchart shows patient selection for the study.

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    Fig 2.

    Representative case of false-positive findings on FDG-PET for benign nodes in a 74-year-old woman with unknown primary squamous cell carcinoma who had both benign and malignant nodes (HIV-positive; absolute CD4 = 473). Axial contrast-enhanced CT images (A and D), [18F] FDG-PET/CT fusion images (B and E), and corresponding axial section ROI mask-segmented lymph nodes (C and F) for pathologically benign (A–C) and malignant (D–F) lymph nodes. [18F] FDG-PET/CT shows abnormal uptake (cutoff = >5.5) for both lymph nodes with SUVmax = 8.1 (benign, B) and 9.5 (malignant, E). However, texture features with SRE (cutoff = <0.164) of both lymph nodes were correctly diagnosed as follows: 0.188 (benign, C) and 0.151 (malignant, F).

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    Table 1:

    Patient demographics and tumor characteristics of patients with head and neck cancera

    CharacteristicHIV-Positive Group (n = 9)HIV-Negative Group (n = 26)P Value
    Age (yr).034b
        Median (range)48 (29–62)59 (30–86)
    Sex.490
        Male7 (78)17 (65)
        Female2 (22)9 (35)
    HPV status (protein 16).283
        Positive312
        Negative114
        Unknown50
    Primary site.169
        Oropharynx3 (33)10 (38)
        Hypopharynx0 (0)1 (4)
        Larynx1 (11)3 (12)
        Oral cavity3 (33)12 (46)
        Primary unknown1 (11)0 (0)
        Maxilla1 (11)0 (0)
    T-Stage.444
        T01 (11)0 (0)
        T11 (11)7 (27)
        T23 (33)9 (35)
        T31 (11)2 (8)
        T43 (33)8 (30)
    • Note:—HPV indicates human papillomavirus.

    • ↵a Data are presented as number of patients with percentages in parentheses unless otherwise noted.

    • ↵b Indicates a significant difference by the Pearson χ2 or Mann-Whitney U test (P < .05).

    • View popup
    Table 2:

    [18F] FDG-PET/CT characteristics and selected texture parameters differentiating lymph node characterization in patients with HIV infection (group 1 vs 2)

    Texture ParameterBenign Nodes (n = 9)Malignant Nodes (n = 13)P ValueaCutoffAUCb (GLIMMROC)
    MeanSDMeanSD
    Node characteristics
        Size (cm)1.4000.3001.8920.690.024<2.00.752
        Volume (cm3)0.5470.3632.5352.218.007>0.760.889
        SUVmax5.1111.6108.5623.886.042>5.50.803
    Histogram
        Mean624.474.6735.375.2.017>683.30.872
        Median774.0217.91013.171.2.018>877.80.872
        Second SD93.7628.7059.8519.19.017<76.30.872
        Range273.782.9175.454.5.017<232.70.863
    Geometric mean199.644.7272.863.8.032>237.30.829
        SD 581.929.416.819.2.018<62.890.872
        SD 999.749.319.517.3.017<63.160.889
    GLCM
        Contrast113.120.284.116.9.009<97.70.889
        Energy0.0360.0190.0810.047.025>0.0470.812
        Homogeneity0.4510.0650.5420.069.020>0.4980.821
    GLRL
        SRE0.1770.0070.1570.009<.001<0.1640.966c
        LRE0.1970.0100.1730.012.001<0.1860.957
        GLN0.1830.0090.1600.011.001<0.1720.949
        RLN0.1960.0100.1730.012.002<0.1840.932
        LRHGE224.651.8300.068.7.035>261.80.863
    • Note:—GLIMMROC indicates generalized linear mixed model receiver operating characteristic.

    • ↵a Indicates a significant difference by the mixed linear regression model (Proc MIXED) to adjust the variance-covariance matrix among multiple values recorded for each patient (P < .05).

    • ↵b Using the generalized linear mixed model (GLIMMROC).

    • ↵c The highest AUC among 41 texture features.

    • View popup
    Table 3:

    [18F] FDG-PET/CT characteristics and selected texture parameters differentiating lymph node characterization in patients with head and neck squamous cell carcinoma without HIV infection (group 3 vs 4)

    Texture ParameterBenign Nodes (n = 39)Malignant Nodes (n = 22)P ValueaCutoffAUCb (GLIMMROC)
    MeanSDMeanSD
    Node characteristics
        Size (cm)1.4390.0481.6870.831.079DNC0.643
        Volume (cm3)1.1220.1473.4684.718.001c>2.5990.702
        SUVmax3.2280.3156.4384.811.007c>3.9800.731
    Histogram
        Mean670.668.4751.8137.3.022c>738.10.705
        Geometric mean225.950.6297.6124.5.020c>257.50.667
        Harmonic mean24.124.2129.579.42.020c>25.50.678
    IQR1064.363.9865.0360.2.022c<1017.00.723
    Fourth moment8.71E+105.74E+099.41E+101.00E+10.018c>9.38E+100.698
    GLCM
        Contrast102.518.281.828.3.015c<75.70.754
        Energy0.0410.0220.0720.055.034c>0.0580.712
        Homogeneity0.4750.0560.5410.104.029c>0.5280.735
    GLRL
        SRE0.1640.0110.1540.019.036c<0.1530.695
        RLN0.1830.0140.1700.023.034c<0.1720.698
        RHGE254.277.2367.0193.6.016c>305.40.739
        LRLGE322.691.4469.8231.9.006c>397.10.759
        LRHGE246.260.5352.7168.8.003c>340.90.760d
    Laws features
        L11,130,272.9280,670.9876,676.6413,942.2.024c<911,080.50.722
    • Note:—DNC indicates did not converge; IQR, interquartile range; GLIMMROC, generalized linear mixed model receiver operating characteristic.

    • ↵a Indicates a significant difference by the mixed linear regression model (Proc MIXED) to adjust the variance-covariance matrix among multiple values recorded for each patient (P < .05).

    • ↵b Using the generalized linear mixed model (GLIMMROC).

    • ↵c Significant.

    • ↵d The highest AUC among 41 texture features.

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American Journal of Neuroradiology: 40 (3)
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H. Kuno, N. Garg, M.M. Qureshi, M.N. Chapman, B. Li, S.K. Meibom, M.T. Truong, K. Takumi, O. Sakai
CT Texture Analysis of Cervical Lymph Nodes on Contrast-Enhanced [18F] FDG-PET/CT Images to Differentiate Nodal Metastases from Reactive Lymphadenopathy in HIV-Positive Patients with Head and Neck Squamous Cell Carcinoma
American Journal of Neuroradiology Mar 2019, 40 (3) 543-550; DOI: 10.3174/ajnr.A5974

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CT Texture Analysis of Cervical Lymph Nodes on Contrast-Enhanced [18F] FDG-PET/CT Images to Differentiate Nodal Metastases from Reactive Lymphadenopathy in HIV-Positive Patients with Head and Neck Squamous Cell Carcinoma
H. Kuno, N. Garg, M.M. Qureshi, M.N. Chapman, B. Li, S.K. Meibom, M.T. Truong, K. Takumi, O. Sakai
American Journal of Neuroradiology Mar 2019, 40 (3) 543-550; DOI: 10.3174/ajnr.A5974
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