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Year : 2020  |  Volume : 16  |  Issue : 1  |  Page : 60-65

Multidetector computed tomography evaluation of synchronous lymphoma and other solid malignancies

1 Department of Radiology, Public Health and Community Medicine, Mansoura Faculty of Medicine, Mansoura University, Mansoura, Egypt
2 Department of Surgical Oncology, Mansoura University, Mansoura, Egypt
3 Department of Medical Oncology, Oncology Center, Mansoura University, Mansoura, Egypt
4 Department of Clinical Hematology, Mansoura University, Mansoura, Egypt
5 Department of Internal Medicine, Mansoura University, Mansoura, Egypt
6 Department of Chest Medicine, Mansoura University, Mansoura, Egypt
7 Department of Endemic Medicine, Mansoura University, Mansoura, Egypt
8 Department of Clinical Oncology and Nuclear Medicine, Mansoura University, Mansoura, Egypt
9 Department of Pathology, Mansoura University, Mansoura, Egypt
10 Department of Occupational Health and Industrial Medicine, Public Health and Community Medicine, Mansoura Faculty of Medicine, Mansoura University, Mansoura University, Mansoura, Egypt

Date of Submission07-Apr-2017
Date of Acceptance06-Apr-2018
Date of Web Publication29-Oct-2018

Correspondence Address:
Adel El-Badrawy
1 Omar Ben Abdel-Aziz from Gehan Street, Mansoura
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jcrt.JCRT_325_17

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 > Abstract 

Objective: The objective of this study is to review the multidetector computed tomography (MDCT) findings of synchronous lymphoma and other solid malignancies.
Patients and Methods: This retrospective study included 18 patients confirmed with diagnosis of lymphoma and other solid malignancies. They were 8 women and 10 men (mean age, 62.5 year; range, 44–73 years). CT scanning was performed on one of the two systems: 64 MDCT in 11 patients and 6 MDCT in 7 patients. All 36 malignancies were underwent pathological evaluation.
Results: All cases were confirmed pathologically. Lymphomas were Hodgkin disease ( n = 5 patients) and non-Hodgkin lymphoma ( n = 13 patients). Hepatocellular carcinoma was detected in five patients. Bronchogenic carcinoma was detected in two patients. Renal cell carcinoma was detected in two patients. Breast carcinoma was detected in two patients. Prostatic carcinoma was detected in two patients. Gastric carcinoma was detected in two patients. Endometrial carcinoma was detected in one patient. Colonic carcinoma was detected in one patient. Thyroid carcinoma was detected in one patient.
Conclusions: MDCT scanning is accurately imaging modality for the evaluation of synchronous lymphoma and other solid malignancies. More reports and accumulation of such cases should help to clarify the mechanisms, contribute to a further understanding of this phenomenon, and may lead to a new treatment strategy for synchronous lymphoma and other solid malignancies.

Keywords: Computed tomography, lymphoma, synchronous malignancy

How to cite this article:
El-Badrawy A, Gadelhak B, Helmy EM, Farouk O, Fady T, Refky B, Elzaafarany M, Emarah Z, Taalab MM, Eisa N, El-Etreby SA, Bahgat MH, El-Badrawy MK, Elalfy H, Besheer T, El-Mesery A, Akl MF, Megahed N, Khashaba EO. Multidetector computed tomography evaluation of synchronous lymphoma and other solid malignancies. J Can Res Ther 2020;16:60-5

How to cite this URL:
El-Badrawy A, Gadelhak B, Helmy EM, Farouk O, Fady T, Refky B, Elzaafarany M, Emarah Z, Taalab MM, Eisa N, El-Etreby SA, Bahgat MH, El-Badrawy MK, Elalfy H, Besheer T, El-Mesery A, Akl MF, Megahed N, Khashaba EO. Multidetector computed tomography evaluation of synchronous lymphoma and other solid malignancies. J Can Res Ther [serial online] 2020 [cited 2020 Jun 6];16:60-5. Available from: http://www.cancerjournal.net/text.asp?2020/16/1/60/244454

 > Introduction Top

Hodgkin disease (HD) and non-Hodgkin lymphoma (NHL) comprise approximately 5%–6% of all malignancies.[1] The incidence of multiple primary malignant neoplasms is increasing as a result of aging of the population and advances in medical technology.[2] Warren and Gates studied the multiple primary malignant tumors' condition and established, after the review of over 1200 case reports, some diagnostic criteria in 1932. These criteria are still commonly accepted at the present time.[3] Multiple primary malignant tumors in a single patient are relatively rare. In reviews of the literature regarding multiple primary malignant tumors, the overall occurrence rate of multiple primary malignancies (MPMs) is between 0.73% and 11.7%.[4] In this retrospective study, we review multidetector computed tomography (MDCT) findings of 18 cases with synchronous lymphoma and other solid malignancies.

 > Patients and Methods Top


The study was approved by the institutional research ethics review committee and informed consent from patient was waived due to the retrospective design of this study. This retrospective study included 18 patients with synchronous lymphoma and other solid malignancies between March 2009 and January 2017. They were 8 women and 10 men (mean age, 62.5 years; range, 44–73 years). All 18 patients had ultrasonography. Eleven patients were hepatitis C virus (HCV) positive as well as five patients were hepatitis C and B viruses. Hepatitis virus was not detected in two patients. Pathological diagnoses of all 36 malignancies were confirmed in all 18 patients. Laboratory abnormalities were detected in all cases. These abnormalities on admission showed the following results: mild elevated total bilirubin: 1.03–2 mg/dL (normal 0.1–1.1), aspartate aminotransferase: 17–90 IU/mL (normal up to 40), alanine aminotransferase: 15–70 IU/L (normal up to 40), white blood cell: 4.6–12.7 k/uL (normal 4–11), red blood cell: 2.30–5.31 m/uL (normal 4.1–5.9), hemoglobin: 6.8–14.5 g/dL (normal 12.5–17.5), PLT: 37–350 k/uL (normal 140–450), serum creatinine: 0.98–1.2 mg/dl (normal 0.9–1.3), and Lactate dehydrogenase (LDH): 250–1050 U/I (normal 100–190). Although characteristic CT findings were detected in all 18 patients, fine-needle aspiration cytology was done to exclude possibility of metastases and confirm histopathological diagnosis. All lymphomas and other synchronous malignancies were detected at the same time. The inclusion criteria of patients in this study were the presence of two neoplastic locations that confirmed by histopathological examination, with distinct histopathology in the two locations. The exclusion criteria were patients without a clear histopathological confirmation of each tumor and then also the patients whom the second tumor has suspected to be a metastasis of the first location. Various details such as patient's age at time of each tumor diagnosis, sex, site of origin, histology, and clinical stage have been recorded [Table 1]. The Barcelona Clinic Liver Cancer (BCLC) staging system has come to be widely accepted in clinical practice.[5] Therefore, it has become the staging system that is used for five hepatocellular carcinomas (HCCs). The criteria of double primary malignancies were those proposed by Warren and Gates are now generally accepted.[3]
Table 1: Characteristics of 18 patients with synchronous lymphoma and other solid malignancies

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Computed tomography technique

Whole-body and triphasic abdominal CT scanning was performed on one of the two systems: Brilliance 64, Philips Healthcare, Best, The Netherlands, in 11 patients and SOMATOM Emotion 6, Siemens, Germany, in 7 patients. The pre- and postcontrast series were taken using a 3-mm slice thickness. Arterial and delayed phases were done for abdominal examination. Portal phase was done for whole body. The postcontrast study was performed using 120 mL of low-osmolar nonionic contrast medium (ioversol, Optiray 350) at a flow rate of 5 mL/s. Patients were requested to hold their breath during the precontrast phase and the three phases of acquisition. Automated bolus tracking with bolus detection at the level of the descending aorta above the diaphragm ensured accurate timing of the data acquisition in an early arterial phase. Portal venous phase was performed with an effective delay of 55–60 s after initiation of the contrast material injection. The delayed phase was performed with an effective delay of 3–6 min. All images were transferred to the workstation (Extended Brilliance Workspace V3.5.0.2254) for postprocessing. The images were viewed on the lung, soft tissue, and bone setting.

Image interpretation

Data interpretation and image analysis were focused on the following aspects on the initial CT scan: precontrast attenuation of the lesions, density in all phases (arterial, portal, and delayed phases), number of lesions, vascular invasion, lymph node involvement, and other abdominal organs as well as metastatic spread. Whole-body CT scanning was evaluated for all groups of lymph nodes and other organs of the body as well as bony or pulmonary metastases. All malignancies were evaluated for local, lymphatic, hematogenous, or transcoelomic spread if suspected according to the primary site of tumor. Tumor size, internal architecture, organ of origin, tissue invasion, vascular encasement, calcifications, and metastases were evaluated. Operative findings of seven malignancies were compared with MDCT findings. Tumor staging of all 36 malignancies was evaluated [Table 1].

 > Results Top

Our study applied the criteria of Warren and Gates to identify lymphomas and other primary malignancies.[3] All 36 malignancies were accurately characterized, evaluated, and staged. The primary site of lymphoma was lymph nodes (10/18), spleen (4/18), lymph nodes and muscles (2/18), oropharynx (1/18), and stomach (1/18). The most frequent sites of other synchronous malignancies were HCC (5/18), followed by lung (2/18), kidney (2/18), breast (2/18), prostate (2/18), stomach (2/18), endometrium (1/18), colon (1/18), and thyroid (1/18). Lymphomas were NHL (13/18) and HD (5/18). Ann Arbor staging of lymphomas were Stage I (6/18), IE (3/18), II (5/18), IIE (1/18), III (2/18), and IV (1/18). According to BCLC staging system, the HCC staging was Stage A (2 patients) and B (3 patients) [Figure 1]. Two patients with bronchogenic carcinoma were Stage IIIB [Figure 2]. One patient with renal cell carcinoma (RCC) was Stage III [Figure 3] and other patient was Stage IV. Breast carcinoma staging was Stage IIA and IIB. Prostatic carcinoma staging was Stage III [Figure 4]. One patient with gastric carcinoma was Stage IIIC and other patient was IIA. Endometrial carcinoma staging was Stage IVB (FIGO staging). Colonic carcinoma staging was Stage IIIB. Thyroid carcinoma was Stage IVA. MDCT findings were correlated with operated seven patients.
Figure 1: A 67-year-old male patient presented with left inguinal swelling. Triphasic computed tomography scan (a-d) revealed segment III hepatic focal lesion heterogeneous enhancement in arterial phase (a and b), washout in portal (c), and delayed (d) phases with left PV thrombus. Evidence of multiple malignant abdominal lymphadenopathy. Computed tomography scan pelvis (e) and inguinal region (f) revealed bilateral pelvic and left inguinal malignant lymphadenopathy. Biopsy from hepatic focal lesion revealed hepatocellular carcinoma and excision left inguinal lymph node revealed non-Hodgkin lymphoma

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Figure 2: A 67-year-old male presented with respiratory symptoms. Computed tomography scan revealed the right upper bronchogenic mass invading superior vena cava (a and b) (pathologically proved bronchogenic carcinoma) and splenic heterogeneous mass (c) (pathological proved non-Hodgkin lymphoma)

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Figure 3: A 58-year-old male presented with fever and weight loss. Initial computed tomography scan (a-d) revealed splenic and left renal soft-tissue masses. Fine-needle aspiration cytology from splenic focal lesion revealed non-Hodgkin lymphoma and patient managed accordingly. On follow-up, computed tomography scan (e-h) revealed marked regression of splenic focal lesion with progression of the left renal mass. Fine-needle aspiration cytology from renal mass revealed renal cell carcinoma

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Figure 4: A 73-year-old male patient presented with right upper cervical swelling. Computed tomography scan (a-c) revealed multiple right upper cervical malignant lymphadenopathy. Biopsy revealed Hodgkin disease. Computed tomography scan pelvis (d-f) revealed enlarged heterogeneous prostate with capsule disruption. Biopsy revealed prostatic carcinoma

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 > Discussion Top

Synchronous multiple malignancies are secondary lesions that present simultaneously or within 6 months following the development of the initial malignancy.[6] The criteria of double primary malignancies were those proposed by Warren and Gates.[3] These criteria are (i) each tumor must present a definitive picture of malignancy, (ii) each must be distinct, and (iii) the probability of one being a metastasis of the other must be reasonably excluded. Multiple cancers occurring in the same organ were identified as a single cancer in that organ. The last decade had experienced a steady increase in the incidence of MPM.[7] CT remains the standard imaging modality for initial staging of malignant lymphoma because of its widespread availability and relatively low cost.[1],[8]

Biopsy remains a critical diagnostic tool recommended in diagnosis of synchronous solid malignancies to confirm the histological origin of the primary neoplasm and to provide the best therapeutic algorithm based on the correct diagnosis.[9] All 36 malignancies in this study underwent histopathological evaluation. Elderly age is certainly a risk factor for the development of second primary malignancies.[7],[10] This coincides with our result as mean age was 62.5 years.

The incidence of intra-abdominal cancers such as kidney, liver, and pancreatic cancer were higher in the synchronous group than in other groups. Most synchronous cancers were detected during the preoperative workup with the result that most were located in the intra-abdominal cavity.[11] This coincides with our result as synchronous extra lymphoma primary malignancies were 13/18 cases of intra-abdominal malignancy.

MDCT is highly effective for the evaluation and characterization of HCC, bronchogenic, renal, breast, prostate, endometrial, and colonic masses.[12],[13],[14],[15],[16],[17],[18],[19] This coincides with our results as MDCT revealed accurately all 36 malignancies.

The characteristic of HCC imaging in MPMs was similar to that of HCC-alone patients. Dynamic CT can provide useful information for the differential diagnosis for hepatic nodules.[20] This coincides with our results. The frequency of synchronous malignancies varies according to the geographical setting of the study.[21],[22],[23] Our result shows that the most common extra lymphoma malignancy is HCC (5/18). This is may be due to high incidence of HCC and lymphoma with HCV that agree with previous studies.[24],[25]

The association between chronic hepatitis viral infection and diverse lymphoproliferative disorders has been extensively studied.[24],[26] Our study revealed that 11 patients were HCV positive. Five patients were hepatitis C and B viruses. This coincides with previous study of Di Stasi et al .[25] However, this result does not agree with other series reported relatively low incidence of B-cell lymphoproliferative disorders in HCC patients.[21],[27] This difference may be due to relative small number of cases and may be due to geographical setting Diffuse large B- or T-cell lymphoma and centrocytic lymphoma can coexist with RCC.[28] Our results revealed two cases of RCC associating NHL. Cui et al .[29] report five cases of synchronous solid tumor and hematological malignancy. They are myeloma and lung cancer (1/5), chronic myelogenous leukemia (1/5), lymphoma and cancer colon (1/5), myeloma and cancer colon (1/5), and lymphoma and gastric carcinoma (1/5). Our results agree with this finding in that there is higher incidence of hematological malignancy with other solid malignancy but the difference in type of hematological and other solid malignancies. This difference may be due to geographical setting.

 > Conclusions Top

The possibility of synchronous lymphoma and other solid malignancies should always be considered during pretreatment evaluation. CT scanning is promising technique in the evaluation of synchronous double malignancies. Pathology or cytology may aid in the final diagnosis and should be performed. Further new staging for combination of synchronous double malignancies may be inserted for new treatment strategies. Immunological and genetic aspects of synchronous double malignancies must be evaluated. We believe that a study of patients from a multicenter and multigeographic area would reach conclusions more powerful.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

 > References Top

Kwee TC, Kwee RM, Nievelstein RA. Imaging in staging of malignant lymphoma: A systematic review. Blood 2008;111:504-16.  Back to cited text no. 1
Sato S, Shinohara N, Suzuki S, Harabayashi T, Koyanagi T. Multiple primary malignancies in Japanese patients with renal cell carcinoma. Int J Urol 2004;11:269-75.  Back to cited text no. 2
Warren S, Gates O. Multiple primary malignant tumors. Am J Cancer 1932;16:1358-414.  Back to cited text no. 3
Demandante CG, Troyer DA, Miles TP. Multiple primary malignant neoplasms: Case report and a comprehensive review of the literature. Am J Clin Oncol 2003;26:79-83.  Back to cited text no. 4
Forner A, Reig ME, de Lope CR, Bruix J. Current strategy for staging and treatment: The BCLC update and future prospects. Semin Liver Dis 2010;30:61-74.  Back to cited text no. 5
Yun HR, Yi LJ, Cho YK, Park JH, Cho YB, Yun SH, et al. Double primary malignancy in colorectal cancer patients – MSI is the useful marker for predicting double primary tumors. Int J Colorectal Dis 2009;24:369-75.  Back to cited text no. 6
Mariotto AB, Rowland JH, Ries LA, Scoppa S, Feuer EJ. Multiple cancer prevalence: A growing challenge in long-term survivorship. Cancer Epidemiol Biomarkers Prev 2007;16:566-71.  Back to cited text no. 7
Armitage JO. Staging non-Hodgkin lymphoma. CA Cancer J Clin 2005;55:368-76.  Back to cited text no. 8
Maida M, Macaluso FS, Galia M, Cabibbo G. Hepatocellular carcinoma and synchronous liver metastases from colorectal cancer in cirrhosis: A case report. World J Hepatol 2013;5:696-700.  Back to cited text no. 9
Hayat MJ, Howlader N, Reichman ME, Edwards BK. Cancer statistics, trends, and multiple primary cancer analyses from the surveillance, epidemiology, and end results (SEER) program. Oncologist 2007;12:20-37.  Back to cited text no. 10
Eom BW, Lee HJ, Yoo MW, Cho JJ, Kim WH, Yang HK, et al. Synchronous and metachronous cancers in patients with gastric cancer. J Surg Oncol 2008;98:106-10.  Back to cited text no. 11
Choi JY, Lee JM, Sirlin CB. CT and MR imaging diagnosis and staging of hepatocellular carcinoma: Part I. Development, growth, and spread: Key pathologic and imaging aspects. Radiology 2014;272:635-54.  Back to cited text no. 12
Furlan A, Marin D, Vanzulli A, Patera GP, Ronzoni A, Midiri M, et al. Hepatocellular carcinoma in cirrhotic patients at multidetector CT: Hepatic venous phase versus delayed phase for the detection of tumour washout. Br J Radiol 2011;84:403-12.  Back to cited text no. 13
Tang W, Wu N, OuYang H, Huang Y, Liu L, Li M, et al. The presurgical T staging of non-small cell lung cancer: Efficacy comparison of 64-MDCT and 3.0 T MRI. Cancer Imaging 2015;15:14.  Back to cited text no. 14
Kamel AI, Badawy MH, Elganzoury H, Elkhouly A, Elesaily K, Eldahshan S, et al. Clinical versus pathologic staging of renal tumors: Role of multi-detector CT urography. Electron Physician 2016;8:1791-5.  Back to cited text no. 15
Moschetta M, Scardapane A, Lorusso V, Rella L, Telegrafo M, Serio G, et al. Role of multidetector computed tomography in evaluating incidentally detected breast lesions. Tumori 2015;101:455-60.  Back to cited text no. 16
Schieda N, Al-Dandan O, Shabana W, Flood TA, Malone SC. Is primary tumor detectable in prostatic carcinoma at routine contrast-enhanced CT? Clin Imaging 2015;39:623-6.  Back to cited text no. 17
Tsili AC, Tsampoulas C, Dalkalitsis N, Stefanou D, Paraskevaidis E, Efremidis SC, et al. Local staging of endometrial carcinoma: Role of multidetector CT. Eur Radiol 2008;18:1043-8.  Back to cited text no. 18
Choi SJ, Kim HS, Ahn SJ, Jeong YM, Choi HY. Evaluation of the growth pattern of carcinoma of colon and rectum by MDCT. Acta Radiol 2013;54:487-92.  Back to cited text no. 19
Lim JH, Choi D, Kim SH, Lee SJ, Lee WJ, Lim HK, et al. Detection of hepatocellular carcinoma: Value of adding delayed phase imaging to dual-phase helical CT. AJR Am J Roentgenol 2002;179:67-73.  Back to cited text no. 20
Wong LL, Lurie F, Takanishi DM Jr. Other primary neoplasms in patients with hepatocellular cancer: Prognostic implications? Hawaii Med J 2007;66:204, 206-8.  Back to cited text no. 21
Hong S, Jeong SH, Lee SS, Chung JW, Yang SW, Chung SM, et al. Prevalence and outcomes of extrahepatic primary malignancy associated with hepatocellular carcinoma in a Korean population. BMC Cancer 2015;15:146.  Back to cited text no. 22
Fernández-Ruiz M, Guerra-Vales JM, Castelbón-Fernández FJ, Llenas-García J, Caurcel-Díaz L, Colina-Ruizdelgado F, et al. Multiple primary malignancies in spanish patients with hepatocellular carcinoma: Analysis of a hospital-based tumor registry. J Gastroenterol Hepatol 2009;24:1424-30.  Back to cited text no. 23
Suriawinata A, Thung SN. Hepatitis C virus and malignancy. Hepatol Res 2007;37:397-401.  Back to cited text no. 24
Di Stasi M, Sbolli G, Fornari F, Cavanna L, Rossi S, Buscarini E, et al. Extrahepatic primary malignant neoplasms associated with hepatocellular carcinoma: High occurrence of B cell tumors. Oncology 1994;51:459-64.  Back to cited text no. 25
Himoto T, Miyauchi Y, Nomura K, Fushitani T, Kurokohchi K, Masaki T, et al. Coexistence of splenic non-Hodgkin's lymphoma with hepatocellular carcinoma in a patient with chronic hepatitis C. Dig Dis Sci 2006;51:70-6.  Back to cited text no. 26
de Pangher Manzini V, Calucci F, Terpin MM, Loru F, Brollo A, Ramani L, et al. Multiple primary malignant tumors in patients with hepatocellular carcinoma. A review of 29 patients. Tumori 1996;82:245-8.  Back to cited text no. 27
Ohsawa M, Hashimoto M, Yasunaga Y, Shingu N, Aozasa K. Characteristics of non-Hodgkin's lymphoma complicated by renal cell malignancies. Oncology 1998;55:482-6.  Back to cited text no. 28
Cui Y, Liu T, Zhou Y, Ji Y, Hou Y, Jin W, et al. Five cases report of solid tumor synchronously with hematologic malignancy. Cancer Res Treat 2012;44:63-8.  Back to cited text no. 29


  [Figure 1], [Figure 2], [Figure 3], [Figure 4]

  [Table 1]


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