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ORIGINAL ARTICLE
Year : 2018  |  Volume : 31  |  Issue : 3  |  Page : 1030-1035

Role of color Doppler ultrasonography in differentiating benign and malignant cervical lymphadenopathy


Department of Radiology, Faculty of Medicine, Menoufia University, Menoufia, Egypt

Date of Submission05-Feb-2017
Date of Acceptance30-Apr-2017
Date of Web Publication31-Dec-2018

Correspondence Address:
Reham M Elshiekh
Department of Radiology, Faculty of Medicine, Menoufia University, Menoufia
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_96_17

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  Abstract 


Objective
The aim of the present study was to identify the role of color Doppler ultrasonography in differentiating benign and malignant enlarged cervical lymph nodes.
Background
Cervical lymphadenopathy is a common presenting symptom and sign for a variety of diseases ranging from subtle infections to life-threatening head and neck malignancies. Ultrasound is a useful imaging tool for the initial evaluation of cervical lymph nodes because it has high sensitivity (98%) and specificity (95%), particularly when combined with fine-needle aspiration cytology.
Patients and methods
The present study included 40 (27 male and 13 female) patients with cervical lymphadenopathy. Cases were divided into two main groups: the inflammatory group and the neoplastic group. The inflammatory group was further divided into the nonspecific group and the tuberculous group. The neoplastic group was further divided into the primary group and the metastatic group. The lymph nodes were subjected to sonographic and Doppler studies, which were correlated with clinical and pathological diagnoses obtained either by lymph node biopsy or after surgical excision whenever possible.
Results
Regarding the vascular pattern of each lymph node, our study showed that there was a different pattern of vascularity for each type of lymphadenopathy. Regarding the resistivity index, this study also showed that the sensitivity and specificity of the resistivity index for detecting malignant lymph nodes were 50 and 100%, respectively. Therefore, the value of spectral Doppler ultrasonography evaluation of intranodal vascular resistance is limited in routine clinical practice.
Conclusion
High-resolution ultrasonography has an important role in differentiating benign and malignant lymphadenopathy based on the shape (longitudinal/transverse ratio), hila, cortical thickness, cortical echogenicity, intranodal necrosis, pattern of vascularity, and resistivity index of the nodes.

Keywords: color Doppler ultrasonography, lymphadenopathy, vascular resistance


How to cite this article:
Elzawawy MS, Azab SM, Elshiekh RM. Role of color Doppler ultrasonography in differentiating benign and malignant cervical lymphadenopathy. Menoufia Med J 2018;31:1030-5

How to cite this URL:
Elzawawy MS, Azab SM, Elshiekh RM. Role of color Doppler ultrasonography in differentiating benign and malignant cervical lymphadenopathy. Menoufia Med J [serial online] 2018 [cited 2019 Jan 20];31:1030-5. Available from: http://www.mmj.eg.net/text.asp?2018/31/3/1030/248773




  Introduction Top


High-resolution ultrasonography is a useful imaging modality for evaluating cervical lymphadenopathy because of its high sensitivity (98%) and specificity (95%) when combined with fine-needle aspiration cytology (FNAC)[1]. Using color/power Doppler ultrasonography, the vasculature of lymph nodes can also be evaluated, which provides additional information.

The most common causes for malignant cervicofacial lymphadenopathy are lymphoma and metastases. Metastases in cervical lymph nodes are common in head and neck cancers and non-head and neck cancers[2]. Evaluation of cervical lymphadenopathy is important for patients with head and neck cancers, as it helps in assessing patient prognosis and selection of treatment methods[2]. Tuberculous lymphadenitis is common because of the high prevalence of AIDS in the world. Therefore, an accurate diagnosis of tuberculous lymphadenitis is essential[3].

Color Doppler ultrasonography provides information on blood flow and nodal morphology. The use of higher-frequency transducers improves the ability to detect low-velocity signals from superficial structures. Although vessels in inflamed lymph nodes are dilated, vessels in lymph nodes involved in metastases may be compressed by tumor cells, and therefore the vascular resistance in the vessels of inflamed lymph nodes may decrease because of vasodilatation, and vascular resistance of lymph nodes involved in metastasis may increase because of compression by tumor cells[4].

The aim of this study was to evaluate the role of high-resolution as well as color Doppler ultrasonography in differentiating benign and malignant cervical lymphadenopathy.


  Patients and Methods Top


This retrospective study was carried out on 40 (27 male and 13 female) patients with cervical lymphadenopathy, aged 7–74 years. Participants were divided into two main groups: the inflammatory group (n = 16) and the neoplastic group (n = 24). The inflammatory group was further divided into the nonspecific group (n = 13) and the tuberculous group (n = 3). The neoplastic group was further divided into the primary group (n = 16) and the metastatic group (n = 8).

All patients were subjected to detailed history taking and clinical examination. The study was approved by Ethics Committee of Menoufia Faculty of Medicine, and informed consent was obtained from all patients. The ultrasonographic examination was performed using Mindray and Toshiba ultrasonography machines (toshiba company, Japan) with a 7.5-MHz linear transducer. Patients were positioned supine with their necks hyperextended. A pillow or a triangular soft pad was placed under the shoulder or the lower neck for support. The examination was started with a transverse scan of the submental area. Subsequently, the patient's head was turned to one side, and the other side was examined. Scanning was performed in the following sequence: submandibular area, parotid, upper cervical, middle cervical, lower cervical, and supraclavicular lymph nodes.

Other investigations

Computed tomography of the neck was performed in 27 patients (tuberculosis, lymphoma, and metastasis).

FNAC was carried out in 26 patients (tuberculosis, lymphoma, and metastasis).

Open biopsy was performed for one of the metastatic lymph nodes.

Statistical analysis

Data were collected and entered into the computer using statistical package for social sciences (version 20; SPSS Inc., Chicago, Illinois, USA) program for statistical analysis.

Data from questionnaires were entered as numerical or categorical variables, as appropriate.

The following two types of statistics were performed.

Descriptive statistics

Quantitative data are presented as mean, SD, and range.

Qualitative data are expressed as frequencies and percentages.

Analytical statistics

Fisher's exact test was used for analytical statistics.

A P value less than 0.05 was considered statistically significant.

The χ2-test was used to measure the association between qualitative variables.


  Results Top


This study included 40 (27 male and 13 female) patients. Their ages ranged from 7 to 74 years. Presence of a cervical mass was the main problem. Out of the studied 40 patients, 16 (40%) patients were finally diagnosed as having lymphoma, eight (20%) patients had metastatic lymph nodes, three (7.5%) patients had tuberculous lymphadenitis, and the remaining 13 (32.5%) patients had nonspecific inflammation [Figure 1],[Figure 2],[Figure 3].
Figure 1: Case no. 1. A metastatic lymph node from a case of nasopharyngeal carcinoma (by fine-needle aspiration cytology). Grayscale ultrasonography (a) showed that lymph nodes were round in shape (longitudinal/transverse ratio <2) and had a heterogenous echo texture with absent hilum. Doppler ultrasonography (b and c) showed mixed (peripheral and central) vascularity and resistivity index >0.7.

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Figure 2: Case no. 2. Non-Hodgkin lymphoma (by fine-needle aspiration cytology). Grayscale ultrasonography (a) showed that the lymph nodes were round in shape (longitudinal/transverse ratio <2), with hypoechoic texture and absent hilum. Doppler ultrasonography (b) showed peripheral vascularity, with resistivity index <0.7.

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Figure 3: Case no. 3. Nonspecific lymphadenitis (by medical treatment and follow-up). Grayscale ultrasonography (a) showed that the lymph nodes were oval (longitudinal/transverse ratio <2), with homogenous echo texture and preserved narrow central hilum. Doppler ultrasonography (b and c) showed hilar vascularity, with resistivity index <0.7.

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Regarding the shape of the lymph nodes, 13 (81%) inflammatory nodes were oval shaped and the remaining three (19%) were round in shape. Overall, 13 (81%) lymphomatous nodes were round and the remaining three (19%) were oval in shape. Six (75%) metastatic nodes were round and the remaining two (25%) were oval in shape [Table 1].
Table 1: Distribution of the longitudinal/transverse ratio in different lymph nodes

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Regarding the hila of the lymph nodes, 15 (93%) inflammatory nodes and one (6%) lymphomatous node showed central echogenic, wide hila. Two (12.5%) lymphomatous nodes and one (12.5%) metastatic node showed narrow, fatty hila. One (6%) inflammatory node (tuberculous), 13 (81%) lymphomatous nodes, and seven (87.5%) metastatic nodes showed lost hila [Table 2].
Table 2: Distribution of hilar classes in different lymph nodes

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Regarding the vascular pattern of lymph nodes, our study showed that 92% of the nonspecific inflammatory nodes (12 of 13) showed hilar/central pattern of vascularity and 8% (one of 13) showed peripheral vascularity. In all, 66.5% of the tuberculous nodes (two of three) showed hilar vascularity, and 33.5% (one of three) showed peripheral pattern of vascularity. Overall, 37.5% of the lymphomatous nodes (six of 16) showed hilar vascularity, 56.5% (nine of 16) showed mixed (hilar and peripheral) vascularity, and only 6% (one of 16) showed peripheral vascularity. In all, 75% of metastatic nodes (six of eight) showed peripheral pattern of vascularity and 25% (two of eight) showed mixed pattern of vascularity [Table 3].
Table 3: Distribution of vascular patterns in the studied lymph nodes

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Regarding the resistivity index (RI) with a cutoff point of 0.7, this study showed that all lymph nodes with RI value greater than 0.7 were malignant (either primary or metastatic), but not all the lymph nodes with RI value less than 0.7 were benign: 57% of lymph nodes with RI less than 0.7 (16 of 28) were benign and 43% (12 of 28) were of primary nodal affection [Table 4].
Table 4: Distribution of resistivity index values in the studied lymph nodes

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This study also showed that the sensitivity and specificity of RI for detecting malignant lymph nodes were 50 and 100%, respectively [Table 5].
Table 5: Sensitivity, specificity, and accuracy of resistivity index in diagnosing malignant cervical lymph nodes

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  Discussion Top


The diagnosis of malignant lymphadenopathy is crucial for therapeutic planning in patients with suspected malignant neoplasms and for pretreatment staging in patients with primary malignant tumors of the head and neck.

Ultrasound was used to assess the normal, metastatic, and reactive lymph nodes in the present study by observing certain sonographic features such as size, shape, nodal borders, echogenic hilum, internal echogenicity, and intranodal necrosis.

The present study was conducted on 40 patients with suspected enlarged cervical lymph nodes, with ages ranging from 7 to 74 years.

The ‘shape’ of normal and reactive lymph nodes is usually oval, whereas malignant lymph nodes and tuberculous lymph nodes tend to be round[5]. Although pathological lymph nodes are usually round, occasionally normal submandibular and parotid lymph nodes can also be round in shape[6]. Therefore, the shape of lymph nodes cannot be a sole criterion for the ultrasonographic diagnosis.

A short-to-long axis (S/L) or long-to-short axis (L/S) ratio can be used to assess the nodal shape. An S/L ratio less than 0.5 (or L/S ratio >2) indicates an oval-shaped or fusiform-shaped node, whereas an S/L ratio greater than 0.5 (or L/S ratio <2) indicates a round-shaped lymph node.

Sakai et al.[7] stated that nodal shape is a valuable parameter in differentiating malignant and metastatic nodes from benign ones. Other studies have also provided similar results[8],[9]. In our study as well, shape was a valuable parameter, as 81% of inflammatory nodes were elliptical/oval in shape and 80% of malignant nodes (primary and metastatic) were round in shape.

The ‘echogenic hilum’ is mainly the result of multiple medullary sinuses, each of which acts as an acoustic interface that partially reflects the ultrasound waves and produces an echogenic structure[10].

In our study, echogenic hila were found in 93% (15 nodes) of nonmalignant nodes and 6.5% (one node) of lymphomatous nodes. Loss of echogenic hila were noted in 81% (13 nodes) of lymphomatous nodes and in 87% (seven nodes) of metastatic nodes. Therefore, according to our study, the presence of central echogenic hilus can be used as a diagnostic marker, and is suggested as a sign of benignity. Similar findings were reported by Moritz et al.[11].

Regarding ‘echogenicity’, reactive, tuberculous, and lymphadenitis nodes are hypoechoic when compared with adjacent muscles[12]. Malignant nodes are predominantly hypoechoic except in the case of metastatic lymph nodes of papillary carcinoma of the thyroid, which are commonly hyperechoic[12],[13]. Therefore, hypoechogenicity is not a useful diagnostic sign[14],[10].

Considering the internal echogenicity, the present study confirmed that 87.5% of benign/reactive, 100% of lymphomatous, and 87.5% of metastatic nodes were hypoechoic.

Lymph nodes with ‘intranodal necrosis’, regardless of their size, are pathologic. Necrosis is a late event in tumor infiltration of lymph nodes. It may manifest as a true cystic area (cystic necrosis) within the lymph node (anechoic/hypoechoic area) or present as an ill-defined, hyperechoic area (not as echogenic as the hilus) within a lymph node (coagulation necrosis)[5]. Unlike the echogenic hilus, coagulation necrosis is not continuous with the adjacent fat, and the two are readily differentiated.

Intranodal necrosis is common in papillary carcinoma of the thyroid, squamous cell carcinoma, lymphomatous nodes after radiotherapy, tuberculous nodes, and septic adenitis[15],[16].

Therefore, in the presence of intranodal cystic necrosis, wherever applicable, tuberculous lymphadenitis should always be considered in the differential diagnosis, and needle aspiration is required for cytology and microbiology.

In the present study, 62% (five nodes) of the metastatic nodes and 12.5% (two nodes) of benign nodes showed intranodal necrosis, with sensitivity of 20% and specificity of 87%. Similar findings were reported by Ying et al.[17].

We assessed the vascular pattern by assessing the presence and distribution of intranodal vessels and by evaluating RI within intranodal vessels.

Evaluation of the vascular pattern of cervical lymph nodes has been reported to be highly reliable, with a reliability of 85%[18]. On power Doppler ultrasound, ∼90% of normal neck lymph nodes with a maximum transverse diameter greater than 5 mm will show hilar vascularity[19]. Reactive lymph nodes tend to have a central hilar vascular pattern[20]. Peripheral or mixed vascularity (the presence of both hilar and peripheral vascularity) are common in metastatic nodes[21],[19]. Therefore, the presence of peripheral vessels in lymph nodes is a useful indicator of malignancy. In this study, eight lymph nodes showed peripheral color flow signal, which were further confirmed as six metastatic nodes, one lymphomatous node, and one tuberculous node by FNAC. This study supported the fact that peripheral flow is suggestive of metastatic nodes, which is similar to a previous study performed by Ying and colleagues[19],[22],[23] and Dangore et al.[24]. The reason for peripheral flow can be destruction of hilar vascularity by tumor cells and may result in the induction of vascular supply from the peripheral pre-existing vessels or from vessels in the perinodal soft tissue[25].

Twenty nodes showed central vascular flow: 14 nodes were reactive and six were metastatic, by FNAC. This finding was consistent with the studies of Dangore-Khasbage et al.[20] and Ying et al.[22], suggesting that the presence of central flow is an indicator of reactive nodes. Eleven lymph nodes showed mixed vascularity, which were confirmed as lymphomatous (n = 9) and metastatic (n = 2) by FNAC. This finding was consistent with the findings of Dangore et al.[24] and Ying et al.[23].

Using spectral Doppler ultrasonography, the vascular resistance (RI) of the intranodal vessels can be estimated. However, the role of vascular resistance in distinguishing malignant and benign nodes remains controversial and inconsistent. It has been reported that the RI of metastatic nodes is higher compared with reactive nodes[14]. However, other studies suggest that metastatic nodes may have lower or similar vascular resistances compared with benign lymph nodes[26],[27].

Previous studies by Steinkamp et al.[28] and Chang et al.[27] recommend different cutoff points of RI (0.6, 0.7, and 0.8) for distinguishing between malignant and reactive nodes with different sensitivities (47–81%) and specificities (81–100%).

In the present study, we found that the optimal cutoff for RI for differentiating malignant and reactive lymph nodes was 0.7. All the benign lymph nodes had RIs less than 0.7, whereas 50% of malignant lymph nodes showed RIs less than 0.7, and the remaining showed RIs greater than 0.7, with a sensitivity of 50% and specificity of 100%. These findings are consistent with the previous studies performed by Ying et al.[19], Dangore-Khasbage et al.[20], and Dangore et al.[24].

The increase in RI of malignant nodes can be justified by the theory that cell production in metastatic nodes can increase the pressure on internal structures such as vessels and consequently increase their RI.

At present, imaging clearly plays an essential role in the evaluation of disease in cervical lymph nodes and should be a part of any thorough work-up of patients with head and neck cancer.

The changes in the shape, hila, cortex, echogenicity, and matting of lymph nodes as well as the presence of intranodal necrosis at ultrasonography are valuable in differentiating benign and malignant nodes. Repeated negative findings at percutaneous biopsy should not delay open biopsy in patients with nodal findings that are suspicious at ultrasonography. The decision concerning whether nodal biopsy is required and which nodes are most likely to provide useful diagnostic data are facilitated by using the sonographic criteria described above.


  Conclusion Top


High-resolution ultrasonography can differentiate between benign and malignant lymphadenopathy on the basis of the shape (longitudinal/transverse ratio), hila, cortical thickness, cortical echogenicity, and intranodal necrosis of nodes.

Regarding the vascular pattern of each node, it was observed that the hilar pattern was predominant in benign lymph nodes, whereas the subcapsular pattern was predominant in malignant lymph nodes.

A RI of more than 0.7 showed sensitivity in detecting malignant lymphadenopathy in 50% cases. Therefore, the value of spectral Doppler ultrasonography in evaluating intranodal vascular resistance is limited in routine clinical practice.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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