Background

The incidences of multiple primary malignancies have increased in recent years due to the increasing proportion of elderly patients in the general population, regular medical check-ups, and the increased number of cancer survivors [1].

Colorectal cancer (CRC) is the fourth most common malignancy and is the second leading cause of cancer-related mortality in the USA. Accurate preoperative staging is the most critical step for determining the optimal treatment option and surgical planning for patients with CRC [2]. Gastric cancer has reduced prevalence but poor prognoses. To improve the treatment, early detection and better evaluation should be sought [3].

MDCT scanning is an accurate imaging modality for the evaluation of synchronous double malignancies [4]. Warren and Gates studied the multiple primary malignant tumors condition and established some diagnostic criteria in 1932, after reviewing over 1200 case reports. These criteria are still being accepted at present [5]. Multiple primary malignancies (MPMs) in a single patient are rare. In literature reviews, the overall incidence is between 0.73 and 11.7% [6]. Our report reviews the MDCT findings of a series of cases with synchronous primary gastrointestinal tract malignancy and other solid primary malignancies.

Case presentation

This report was approved by the institutional research ethics review committee. Informed consent from the patient was waived. Our report included 34 patients with synchronous gastrointestinal tract carcinoma and other solid malignancies from November 2009 to September 2019—fourteen men and 20 women (mean age, 65.5 year; range, 52–82 years).

The triphasic abdominal and whole-body CT scanning were performed using 64 MDCT scanners (Brilliance 64; Philips Healthcare, Best, The Netherlands). MDCT diagnosed thirty-four patients with sixty-eight malignancies and pathologically proved to have primary gastrointestinal tract carcinoma with other primary malignant tumors. The highest number of GIT cases were colonic carcinomas detected in 70% (24/34) of the patients. The most frequent extra-gastrointestinal primary malignancy sites were renal cell and breast carcinomas, 17.6% (6/34) for each. The remaining types of tumors and their prevalence and their TNM staging are illustrated in Table 1 and Figs. 1, 2, 3 and 4. The main CT features of these tumors include the colonic and gastric carcinoma with irregular wall thickening, more than 10 mm. Periampullary malignances diagnosed by pancreatic head mass with double duct signs. The main CT appearance of renal cell and hepatocellular carcinomas were enhancement in arterial phase, washout on portal and delayed phases. The breast carcinoma was soft tissue mass with speculated margins. The prostatic carcinoma was enlarged heterogeneous prostate with disruption of prostatic capsule. The urinary bladder carcinoma was diagnosed by localized irregular wall thickness, more than 10 mm. The lymphoma was diagnosed with malignant lymphadenopathy. The ovarian carcinoma was diagnosed by cystic lesion with solid component and thick septae. The endometrial carcinoma was diagnosed by endometrial thickness, more than 18 mm. The bronchogenic carcinoma was diagnosed by lung mass of about 25 mm with speculated margins and associated with ipsilateral mediastinal malignant lymphadenopathy. The thyroid carcinoma was diagnosed by thyroid mass of about 45 mm across with irregular margins and fine granular calcifications.

Table 1 Characteristics of 34 patients with synchronous primary gastrointestinal tract carcinoma and other solid malignancies
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Fig. 1
figure 1

A 58-year-old male presented with bleeding per rectum. MDCT scan revealed right renal mass (arrows). It revealed enhancement on arterial phase (A), washout on portal (B) and delayed phases (C). Pathologically proved RCC. (D–F) MDCT scan revealed caecal mass (arrows) pathologically proved colonic carcinoma

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Fig. 2
figure 2

76-year-old male presented with follow-up during treatment for prostatic carcinoma. MDCT scan of pelvis revealed cecal mass (arrows) (A–C) with prostate carcinoma proved by transrectal biopsy (arrows) (D–F)

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Fig. 3
figure 3

60-year-old female presented with colonic obstruction. CT scan neck and chest revealed right lower cervical, mediastinal, right hilar and sub-carinal malignant lymphadenopathy (A–D). Biopsy revealed HD. CT scan abdomen (E, F) revealed splenic flexure cauliflower mass proved to be colonic carcinoma (curved arrows) (E, F). CT scan (G) revealed proximal intestinal obstruction (asterisks) with collapsed descending colon (arrow)

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Fig. 4
figure 4

64-year-old female presented with right breast pathologically proved carcinoma. MDCT scan (A) revealed right breast mass with right axillary malignant lymphadenopathy (arrow). MDCT scan (B–D) revealed periampullary mass (enhanced in arterial phase, washout in portal and delayed phases (arrows) (pathologically proved neuroendocrinal carcinoma)

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Warren and Gates criteria were applied to our report to identify extra-gastrointestinal primary malignancies [3]. Biopsy was done to exclude the possibilities of metastasis.

All primary gastrointestinal tract carcinoma and other synchronous malignancies were detected simultaneously except for one patient. This patient underwent a right mastectomy for breast carcinoma five months ago. During follow-up CT scanning, there was ascending colonic mass with regional malignant lymphadenopathy. This colonic mass proved pathologically as colonic carcinoma. Various details as patient gender, age at each tumor diagnosis, the primary site of origin, histopathology, and clinical-stage have been recorded (Table 1). The American Joint Committee on Cancer (AJCC) tumor-node-metastasis (TNM) staging is a universally accepted staging system for cancer [7]. Therefore, it has become the staging system in our report. Barcelona Clinic Liver Cancer (BCLC) staging system is the most commonly used for the evaluation of hepatocellular carcinoma (HCC) [8]. Therefore, it has become the staging system for HCC in our report. Warren and Gates proposed the criteria of synchronous double primary malignancies are now generally accepted [5].

Discussion

Synchronous primary multiple malignancies are tumors that present simultaneously or within six months of one another [9]. The diagnostic criteria of double primary malignancies were those proposed by Warren and Gates [5]. These criteria are given as follows: (1) each tumor must present a definitive picture of malignancy; (2) each tumor must be separate; and (3) the probability of one being a metastasis of the other must be reasonably excluded. The last decade has experienced a steady increase in the incidence of multiple primary malignancies (MPM) due to improved diagnostic techniques and the aging of the population [10].

All sixty-eight malignancies in our report underwent needle biopsy and histopathological evaluation. This agrees with the previous report that confirms the pathological proof of synchronous primary solid malignancies and establishes the histological origin of the primary neoplasm [11]. Elderly age is a risk factor for developing second primary malignancies [12], which manifested with our result, as the mean age was 65.5 years.

Our report used Multidetector CT scanning, which has an accurate assessment for preoperative evaluation of gastrointestinal malignancies [1, 13,14,15] and other primary sites in different body parts [16,17,18,19,20,21].

Incidentally detected renal cell tumors are generally smaller in size. The incidence of its detection is steadily growing due to the widespread use of imaging modalities for other medical problems [22, 23]. This agrees with our results as all six patients with renal cell carcinoma are incidental.

The MDCT findings of renal cell and hepatocellular carcinomas in the multiple primary malignancies are similar to that of RCC and HCC-alone patients [4]. This agrees with our results as characteristic CT findings were detected in all six patients with renal cell carcinoma and four patients with hepatocellular carcinoma.

The incidences of primary intra-abdominal malignancies such as renal, hepatic, and pancreatic cancer were higher in the synchronous group than in other groups. Most primary synchronous malignancies were detected during the preoperative workup, which revealed most were located in the intra-abdominal cavity [24]. This is with our report as synchronous extra-gastrointestinal tract primary malignancies represent 70% of abdominal malignancies, as illustrated in Table 1. The exact relationship between synchronous primary gastrointestinal tract malignancy and other primary malignancies remains unclear. It would be of clinical benefit to clarify what types of other primary malignancies occur in synchronous gastrointestinal tract malignancy.

Conclusion

In conclusion, Careful preoperative evaluation is recommended to detect this pattern of synchronous extra-gastrointestinal tumors. More reports of such cases should help clarify the mechanisms of this phenomenon and may lead to a new treatment strategy for synchronous gastrointestinal malignancy and other solid malignancies.