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104 JAYPEE Grayscale Ultrasonography in the Assessment of Regional Lymph Nodes in Oral Cancer and its Correlation with TNM Staging and FNAC 1 Ankur Aggarwal, 2 M Jonathan Daniel, 3 SV Srinivasan, 4 Charles P Sargouname 1 Junior Resident, Department of Oral Medicine and Radiology, Mahatma Gandhi Postgraduate Institute of Dental Sciences, Puducherry, India 2 Professor and Head, Department of Oral Medicine and Radiology, Mahatma Gandhi Postgraduate Institute of Dental Sciences, Puducherry, India 3 Associate Professor, Department of Oral Medicine and Radiology, Mahatma Gandhi Postgraduate Institute of Dental Sciences, Puducherry, India 4 Specialist Grade II Radiologist, Mahatma Gandhi Postgraduate Institute of Dental Sciences, Puducherry, India Correspondence: Ankur Aggarwal, Junior Resident, Department of Oral Medicine and Radiology, Mahatma Gandhi Postgraduate Institute of Dental Sciences, Puducherry-605006, India, e-mail: [email protected] ABSTRACT Objectives: The purpose of the study was to evaluate the role of grayscale ultrasound (US) in differentiation of benign from malignant lymph nodes in oral cancer patients and to correlate the ultrasonographic features with TNM staging and FNAC findings of cervicofacial lymph nodes. Methods: In the study, 34 patients with histopathologically proved oral cancer presenting with enlarged superficial cervicofacial lymphadenopathy were included. The clinical, ultrasonographic and fine needle aspiration cytology (FNAC) findings were compared in these patients. Patients were assessed for presence of nodes, their size, ratio of maximum longitudinal diameter to maximum transverse diameter (L/T) and echogenicity. All patients then underwent fine needle aspiration cytology of the lymph nodes and the slides were examined for the presence of malignant cells. Results: It was found that ultrasonography had assessed the status of 28 nodes positively out of 34 nodes for metastasis when compared with results of FNAC. Thus, ultrasonography had a sensitivity of 75% and specificity of 86% in detecting the metastatic nodes when compared with FNAC taken as standard in the detection of metastatic nodes. Conclusion: The lymph node status can be assessed successfully by ultrasonography preoperatively for the presence of metastasis in majority of cases. Therefore, ultrasonography was found to be efficient and cost-effective preoperatively, in planning appropriate management in oral cancer patients. Keywords: Ultrasonography, Lymph node, Fine needle aspiration cytology. ORIGINAL ARTICLE INTRODUCTION Regional lymph node status in oral cancer patients is of paramount prognostic significance. Patients who present with tumors localized at the primary site without dissemination to regional lymph nodes have excellent prognosis. On the other hand, once dissemination to regional lymph nodes takes place, the probability of 5-year survivorship, regardless of the treatment rendered, reduces to nearly half of that seen in early staged patients. 1,5,6 The inadequacy of physical palpation in examination of regional lymph nodes is well-documented and other investigations, like computed tomography, magnetic resonance imaging and newer positron emission tomography are expensive for the average income patient in our country. Ultrasonography being a noninvasive and radiation free modality can be used as a powerful tool in assessment of regional lymph nodes in oral cancer. 4,7 Hence, the study was undertaken with the following aim and objective: (1) To evaluate the role of grayscale ultrasonography in differentiation of benign from malignant lymph nodes in oral cancer patients. (2) To correlate the ultrasonographic features with TNM staging and FNAC findings of cervicofacial lymph nodes. MATERIALS AND METHODS A total of 34 patients were included in the study. Patients with histopathologically proved oral cancer and oral cancer presenting with enlarged cervicofacial lymph nodes were included in the study. Other known causes for cervicofacial lymphadenopathy like oral infection, tuberculosis, sarcoidosis etc. were excluded. Patients presenting with enlarged palpable cervicofacial lymph node were subjected to clinical examination and TNM staging was done. Clinical criteria used for differentiating malignant nodes were: (i) Lymph node with approximate size larger than 1 cm in diameter; (ii) a hard, stony hard or indurated consistency; (iii) fixation to underlying structures, implying that the tumor cells had invaded through the capsule of the lymph node. The patients were subjected to 10.5005/jp-journals-10011-1105

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  • Ankur Aggarwal et al

    104JAYPEE

    Grayscale Ultrasonography in the Assessmentof Regional Lymph Nodes in Oral Cancer andits Correlation with TNM Staging and FNAC

    1Ankur Aggarwal, 2M Jonathan Daniel, 3SV Srinivasan, 4Charles P Sargouname1Junior Resident, Department of Oral Medicine and Radiology, Mahatma Gandhi Postgraduate Institute of

    Dental Sciences, Puducherry, India2Professor and Head, Department of Oral Medicine and Radiology, Mahatma Gandhi Postgraduate Institute of

    Dental Sciences, Puducherry, India3Associate Professor, Department of Oral Medicine and Radiology, Mahatma Gandhi Postgraduate Institute of

    Dental Sciences, Puducherry, India4Specialist Grade II Radiologist, Mahatma Gandhi Postgraduate Institute of Dental Sciences, Puducherry, India

    Correspondence: Ankur Aggarwal, Junior Resident, Department of Oral Medicine and Radiology, Mahatma Gandhi PostgraduateInstitute of Dental Sciences, Puducherry-605006, India, e-mail: [email protected]

    ABSTRACT

    Objectives: The purpose of the study was to evaluate the role of grayscale ultrasound (US) in differentiation of benign from malignant lymphnodes in oral cancer patients and to correlate the ultrasonographic features with TNM staging and FNAC findings of cervicofacial lymphnodes.Methods: In the study, 34 patients with histopathologically proved oral cancer presenting with enlarged superficial cervicofaciallymphadenopathy were included. The clinical, ultrasonographic and fine needle aspiration cytology (FNAC) findings were compared inthese patients. Patients were assessed for presence of nodes, their size, ratio of maximum longitudinal diameter to maximum transversediameter (L/T) and echogenicity. All patients then underwent fine needle aspiration cytology of the lymph nodes and the slides wereexamined for the presence of malignant cells.Results: It was found that ultrasonography had assessed the status of 28 nodes positively out of 34 nodes for metastasis when comparedwith results of FNAC. Thus, ultrasonography had a sensitivity of 75% and specificity of 86% in detecting the metastatic nodes whencompared with FNAC taken as standard in the detection of metastatic nodes.Conclusion: The lymph node status can be assessed successfully by ultrasonography preoperatively for the presence of metastasis inmajority of cases. Therefore, ultrasonography was found to be efficient and cost-effective preoperatively, in planning appropriate managementin oral cancer patients.Keywords: Ultrasonography, Lymph node, Fine needle aspiration cytology.

    ORIGINAL ARTICLE

    INTRODUCTION

    Regional lymph node status in oral cancer patients is ofparamount prognostic significance. Patients who present withtumors localized at the primary site without dissemination toregional lymph nodes have excellent prognosis. On the otherhand, once dissemination to regional lymph nodes takes place,the probability of 5-year survivorship, regardless of thetreatment rendered, reduces to nearly half of that seen in earlystaged patients.1,5,6 The inadequacy of physical palpation inexamination of regional lymph nodes is well-documented andother investigations, like computed tomography, magneticresonance imaging and newer positron emission tomographyare expensive for the average income patient in our country.

    Ultrasonography being a noninvasive and radiation freemodality can be used as a powerful tool in assessment of regionallymph nodes in oral cancer.4,7 Hence, the study was undertakenwith the following aim and objective: (1) To evaluate the roleof grayscale ultrasonography in differentiation of benign from

    malignant lymph nodes in oral cancer patients. (2) To correlatethe ultrasonographic features with TNM staging and FNACfindings of cervicofacial lymph nodes.

    MATERIALS AND METHODS

    A total of 34 patients were included in the study. Patients withhistopathologically proved oral cancer and oral cancerpresenting with enlarged cervicofacial lymph nodes wereincluded in the study. Other known causes for cervicofaciallymphadenopathy like oral infection, tuberculosis, sarcoidosisetc. were excluded. Patients presenting with enlarged palpablecervicofacial lymph node were subjected to clinical examinationand TNM staging was done. Clinical criteria used fordifferentiating malignant nodes were: (i) Lymph node withapproximate size larger than 1 cm in diameter; (ii) a hard, stonyhard or indurated consistency; (iii) fixation to underlyingstructures, implying that the tumor cells had invaded throughthe capsule of the lymph node. The patients were subjected to

    10.5005/jp-journals-10011-1105

  • Grayscale Ultrasonography in the Assessment of Regional Lymph Nodes in Oral Cancer and its Correlation with TNM Staging and FNAC

    Journal of Indian Academy of Oral Medicine and Radiology, April-June 2011;23(2):104-107 105

    JIAOMR

    ultrasonographic examination. If more than one node werepresent then the node with largest diameter was subjected tofurther investigation. The node was assessed for nodal diameter,ratio of maximum longitudinal diameter to maximum transversediameter (L/T) and echogenicity of the lymph node. Based onthe echogenicity, the lymph node was classified as eitherhomogeneous (Fig. 1) or heterogeneous (Fig. 2).

    Following the ultrasonographic examination, the lymphnodes showing lower value of L/T (Fig. 3) (which tend to haveround shape) and heterogenecity were considered as probablemetastatic nodes and subjected to the fine needle aspirationcytology test. Each lymph node was evaluated pathologicallywith an emphasis on the presence or absence of malignant cellsin the smear by an experienced pathologist.

    For comparison of nodal diameter, echogenicity of nodeand ratio of maximum longitudinal to transverse diameter,t-test was applied within each group and in order to correlatethe ultrasonographic features with TNM staging and FNACfindings, Chi-square test was done within each group.

    RESULTS

    Since the p-value is less than 0.05, so the difference betweenthe two groups was found to be statistically significant. Thistest leads to the conclusion that the heterogeneous lymph nodestend to have greater nodal diameter than the homogeneous groupof lymph nodes (Table 1).

    Although the values in Table 2 show that the heterogeneousgroup of lymph nodes is having L/T value lesser than thehomogeneous group, the difference between the two groupswas not found to be statistically significant with p-value > 0.05(0.2076) (Table 2).

    There was significant correlation between the findings ofclinical and ultrasonographic examination as both have detectedthe N1 and N2 status equally and it was found to be statisticallysignificant with p < 0.05 (Table 3).

    There was significant correlation between the findings ofultrasonographic examination and FNAC results for detectionof metastasis (M) and it was found to be statistically significantwith p-value less than 0.05 (0.0007) (Table 4). Ultrasonographyhad a sensitivity of 75% and specificity of 86% in detecting themetastatic nodes when compared with FNAC taken as standardfor detection of metastatic nodes.

    DISCUSSION

    For the evaluation of lymph nodes, ultrasound scanning hasone particular advantage over all other axial imaging methods,in that it allows free rotation of the scanning plane and easyidentification of the largest diameter of a node, which has beensuggested to be an objective criterion for characterizingmalignant lymph nodes.2

    Our study showed that there is significant correlationbetween size of the node and heterogenecity of the lymph nodewhich has been found to be a good indicator of the involvementof node by metastatic cells as it will alter the normal pattern ofechogenicity of the lymph node.8,9

    In reactive nodal disease, the pathogen (microorganism orcellular debris) initially reaches the nodal cortex and induceslymphocyte proliferation within lymphoid follicles andFig. 1: Homogeneous node

    Fig. 2: Heterogeneous node Fig. 3: ABtransverse diameter; CDlongitudinal diameter;L/T = CD/AB

  • Ankur Aggarwal et al

    106JAYPEE

    Table. 1: Comparison of mean nodal diameter of cases with homogeneous and heterogeneous findings

    Findings Mean SD t-value p-value

    Homogeneous 9.65 1.62 5.16 0.0001

    Heterogeneous 15.16 4.52

    Table. 4: Comparison of values of M after ultrasonographic examination and FNAC results

    Ultrasound FNAC results t-value p-value

    Non-metastatic Metastatic

    Non-metastatic 20 3 11.52 0.0007

    Metastatic 3 8

    Table. 2: Comparison of mean L/T of cases with homogeneous and heterogeneous findings

    Findings Mean SD t-value p-value

    Homogeneous 1.69 0.431.29 0.2076

    Heterogeneous 1.48 0.43

    Table. 3: Comparison of values of N after clinical and ultrasonographic examination

    Clinical Ultrasound t-value p-value

    N1 N2

    N1 19 0 33 0.0001

    N2 0 15

    sinusoidal enlargement and margination of macrophages, whichlead to widening of the cortex. In malignant disease, however,the changes occurring within the lymph node are somewhatdifferent in nature. The process involves infiltration of the nodeby malignant tissue, which is more likely to result in earlydistortion of internal nodal architecture showing asheterogenecity on ultrasound.3,10 Out of total 11 metastaticnodes in our study, eight were found to depict this feature onultrasonographic examination.

    Our study has shown that the grayscale ultrasonography canbe used to assess the suspicious node. Out of 34 cases, grayscaleultrasonography positively assessed the node in 28 cases (20cases being nonmetastatic and 8 being metastatic) whencompared with FNAC findings. Thus, in our study ultra-sonography was found to have a sensitivity of 75% andspecificity of 86% in detecting the metastatic nodes.

    Although our study did not show statistically significantcorrelation between L/T values as compared to echogenicity ofnode, it showed that heterogeneous nodes tend to have lesservalue of L/T parameter. Luigi Solbiati et al (1992) concludedthat 71% of nodes with L/T smaller than 1.5 (roundish shape)are malignant, whereas 84% of nodes with L/T value greaterthan 2 (oval shape) are benign.

    The best method and current reference standard for staginglymph node metastases is histopathologic examination, whichis the gold standard. Ophelia Dsouza et al (2000) conductedthe clinical, ultrasonographic and histopathological examination

    of cervical lymph nodes in head and neck cancer patients andconcluded that ultrasonography had a sensitivity of 47.6% andspecificity of 77.7%.11 However, this is an invasive surgicalprocedure in which complications and morbidity may occur. Inour study we have used a combination of noninvasive(ultrasonography) and a minimally invasive (FNAC) techniquecausing minimal discomfort for the patient. To the best of ourknowledge, our study is the first of its kind correlating grayscaleultrasonography with TNM staging and FNAC findings in theassessment of metastatic node in oral cancer. Thus, the resultsof our study may be considered to be valid in assessing themetastatic lymph nodes by noninvasive grayscale ultrasono-graphy in oral cancer patients.

    One disadvantage of ultrasonography is that the changes ininternal architecture of the lymph nodes cannot be recognizedin deeper lymph nodes. The possible explanations for this canbe the decreasing contrast resolution because of signalattenuation with increasing distance of the object of interestfrom US probe and the poorer spatial resolution of US probesused for analyzing deeper structure.

    CONCLUSION

    Our study led to the conclusion that there is a significant relationbetween the size of the node and echogenicity of the node. Bothof these parameters may be used to assess the metastatic nodes.Its significance lies in the fact that the lymph node status can beassessed successfully by ultrasonography preoperatively, and

  • Grayscale Ultrasonography in the Assessment of Regional Lymph Nodes in Oral Cancer and its Correlation with TNM Staging and FNAC

    Journal of Indian Academy of Oral Medicine and Radiology, April-June 2011;23(2):104-107 107

    JIAOMR

    the need for extensive surgeries like commando operation canbe obviated in some cases and the treatment can be rendered ina more precise manner reducing the morbidity and improvingthe prognosis.

    With advances in technology now, other forms ofultrasonography, such as contrast-enhanced grayscaleultrasonography,12 color Doppler sonography, power Dopplersonography and real time ultrasound elastography13 areavailable, which may be used for more accurate assessment ofmetastatic nodes. Future studies with advanced forms ofultrasonography need to be done as ultrasonography is a cost-effective, radiation free modality which can be used easily atthe bed side of the patient and can be repeated at regular intervalson patients without causing any radiation hazard.

    REFERENCES1. Shah Jatin p, Johnson Newell W, Batsakis John G. Book on

    oral cancer (1st ed) 2003.2. Pierre Vassalo, Karl Wernecke. Differentiation of benign from

    malignant superficial lymphadenopathy: The role of highresolution US. Radiology 1992;183:215-20.

    3. Ahuja A, Ying M. The use of sonography in differentiatingcervical lymphomatous lymph nodes from cervical metastaticlymph nodes. Clinical Radiology 1996;51:186-90.

    4. Ahuja A, King Ann. Lymph node hilus: Grayscale and powerDoppler sonography of cervical nodes. J Ultrasound Med2001;20:987-92.

    5. Calabrese L, Bruschini R. Role of sentinel lymph node biopsyin oral cancer. Acta Otorhinolaryngol Ital 2006;26:345-49.

    6. Michael Ying, Anil Ahuja. Ultrasound evaluation of neck lymphnodes. Asum ultrasound bulletin Aug 2003;6(3).

    7. Ahuja Anil, Ying Michael. An overview of neck nodesonography. Investigative radiology June 2002;37(6):333-42.

    8. Hayashi Takafumi, Ito Jusuke. The clinical significance offollow-up sonography in the detection of cervical lymph nodemetastases in patients with stage I or II squamous cell carcinomaof the tongue. Oral Surg Oral Med Oral Pathol Oral RadiolEndod 2003;96:112-17.

    9. Solbiati Luigi, Cioffi Vincenzo. Ultrasonography of the neck.Radiologic Clinic of North America Sep 1992;30(5).

    10. To EWH, Tsang WM. Is neck ultrasound necessary for earlystage oral tongue carcinoma with clinically no neck? Dento-maxillofacial Radiology 2003;32:156-59.

    11. DSouza Ophelia, Hasan Suhel. Cervical lymph node metastasesin head and neck malignancy: A clinical/ultrasonographic/histopathological comparative study. Indian Journal ofOtolaryngology and Head and Neck Surgery 2003;55(2):90-93.

    12. Roberto Stramare, Elena Scagliori. The role of contrast-enhancedgrayscale. Ultrasonography in the differential diagnosis ofsuperficial lymph nodes. Ultrasound Quarterly Mar2010;26(1):45-51.

    13. Bhatia Kunwar SS, Carmen CM. Cho real-time qualitativeultrasound elastography of cervical lymph nodes in routineclinical practice: Interobserver agreement and correlation withmalignancy. Ultrasound in Medicine and Biology Dec2010;36(12):1990-97.