Introduction
According to GLOBOCAN 2020 [ 1 ], colorectal cancer (CRC) accounted for 1.93 million new cases (10.0% of all cancers) and 935,000 deaths (9.4% of all cancer deaths) worldwide, ranking third in incidence and second in cancer mortality.
By 2040, the global burden of CRC is projected to rise to 3.2 million new cases and 1.6 million deaths [ 2 ].
At diagnosis, ∼20% of patients have stage IV disease and up to ∼50% of initially localized cases will develop metastases over time [ 3 ]. The liver is the predominant site of spread, followed by lung and peritoneum/distant lymph nodes, while bone involvement is uncommon and synovial/soft-tissue metastases are rare in the absence of visceral disease. We report a case of right-colon adenocarcinoma with atypical metastatic spread to the left humeral head, patella with synovial dissemination, and soft tissues of the second finger, underscoring the diagnostic and management challenges of such unusual patterns.
Case report
A woman in her early 70s, with no relevant comorbidities and a negative family history for malignancy, was diagnosed in March 2018 with a moderately differentiated mucinous adenocarcinoma of the right colon (pT3N0, pMMR) ( Fig. 1 A). She underwent right hemicolectomy followed by adjuvant FOLFOX4 for 6 months, with regular surveillance thereafter. She remained disease-free until May 2021, when a solitary pulmonary metastasis was identified and treated with left lower lobectomy. Molecular profiling showed KRAS A146T mutation and microsatellite-stable (MSS) status. Fig. 1 Histological images stained with Hematoxylin-Eosin showing: (A) Primary mucinous adenocarcinoma infiltrating the large bowel; (B) Metastatic mucinous adenocarcinoma in the humerus, consisting of cribriform and anastomosing glands floating in mucin, infiltrating the bone ( asterisks: fragments of lamellar bone); (C) Metastatic mucinous adenocarcinoma in the subcutaneous tissue of the finger, characterized by cribriform glands with interspersed goblet cells, surrounded by bloody material (cell block technique); (D) Strong membranous staining for Cytokeratin 20 in neoplastic cells; (e) Strong and diffuse CDX2 immunostaining in the nuclei of neoplastic cells, confirming the colonic origin of the metastatic lesions. Fig 1
In January 2022, the patient presented with approximately one month of progressive left shoulder pain and reduced function. On examination, there was focal tenderness and painful limitation of passive range of motion at the left shoulder; the abdomen was soft and nontender; chest auscultation revealed reduced breath sounds at the left base. Key laboratory tests in January 2022 were largely unremarkable: WBC 6.03 × 10³/µL (4.0-10.0), hemoglobin 14.7 g/dL (12.5-16.0), platelets 199 × 10³/µL (150-400), creatinine 0.7 mg/dL (0.52-1.04), alkaline phosphatase 89 U/L (38-126), CRP <0.5 mg/dL (0-1); tumor markers showed CEA 4.4 ng/mL (0-3, mildly elevated) and CA19-9 <1.4 U/mL (0-39). Functional shoulder impairment prompted MRI ( Fig. 2 ) and subsequent PET scans, revealing a suspicious lesion at the head of the left humerus; core biopsy established metastatic mucinous adenocarcinoma ( Fig. 1 B). Fig. 2 MRI of the shoulder: (A) coronal FS-T2w and (B) axial T2w MRI sequences show the secondary involvement of both humeral head and surroundings soft tissues (white arrows). (C) X-ray and (D) ultrasound of the right hand show the lesion of the soft tissues of the proximal phalanx (white arrows), without any bone involvement. Fig 2
Given the diagnosis of isolated bone metastasis, she began FOLFIRI plus bevacizumab in March 2022, with denosumab for skeletal protection. Because of persistent pain, she received palliative radiotherapy 30 Gy (3000 cGy) to the shoulder, with symptomatic relief. With radiological stability and no other disease sites, a multidisciplinary board recommended local control; in July 2023 she underwent proximal humeral osteotomy and shoulder arthroplasty, with an uneventful postoperative course.
In December 2023, progressive left knee pain prompted PET/CT and MRI, which revealed extensive patellar infiltration with synovial thickening/nodularity and joint effusion ( Fig. 3 ). Concurrently, swelling of the right second finger led to ultrasound detection of a subcutaneous soft-tissue mass; fine-needle aspiration confirmed metastatic adenocarcinoma ( Fig. 1 C). Owing to the atypical pattern of spread, a liquid biopsy (Foundation One® Liquid CDx) reconfirmed KRAS A146T. Fig. 3 MRI of the knee: (A) Sagittal FS Tw2 sequence, (B) Axial T2w sequence, (C) Sagittal and (D) axial T1w FS sequences after contrast media administration show extensive secondary involvement of the patella (long white arrows), with joint effusion (short pink arrow), synovial thickening and nodularity (short green arrows). Additionally, enlarged lymph nodes are seen in the popliteal fossa (short red arrow). Fig 3
Because she had previously derived benefit, FOLFIRI plus bevacizumab with denosumab was restarted in January 2024 for six cycles. At reassessment, FDG uptake decreased on PET/CT, but MRI showed progressive synovial thickening and patellar infiltration, in parallel with persistent symptoms. As the patient did not receive immune checkpoint inhibitors, and considering structural progression rather than isolated metabolic fluctuation, we favoured true progression over pseudoprogression. Treatment was therefore switched to mFOLFOX6 plus bevacizumab with bisphosphonates. Shoulder pain remains controlled after surgery and radiotherapy; knee symptoms are medically managed pending further multidisciplinary evaluation.
Discussion
Among patients with metastatic CRC, the liver is the predominant site (70% of cases), followed by lung/thorax (32%). In colon cancer, the peritoneum is the third site (21%) and brain metastases are uncommon (5%) [ 4 ]. In recent years, there has been an increase in the incidence of bone metastases in patients with colorectal cancer, likely due to improved survival rates and diagnostic techniques. However, bone involvement across the disease course is still rare, accounting for 3%-7% of cases [ 5 ], with a 10-year incidence of only 2.7% [ 6 , 7 ]. Localisation to the shoulder and acrometastasis is rare, and localisation to the patella is even rarer due to its poor vascularisation and distal location. To date, only four cases of metastasis to the patella from colorectal cancer have been described ( Table 1 ) [ [8] , [9] , [10] ], and, to our knowledge, only one case report has described a shoulder metastasis from CRC [ 11 ]. Table 1 Reported cases of patellar metastasis secondary to colorectal cancer. Table 1 References Year of publication Age Sex Treatment(s) Survival (Months) Griener B 8 2001 57 M SR 4 Saglik et al 7 2008 43 M RT, CTX 6 Saglik et al 7 2008 67 M CTX 4 Gasagranda B 9 2014 51 M SR NR RT, radiotherapy; CTX, chemotherapy; SR, surgical resection; TKR, total knee replacement; NR, not reported.
Table 1
Reported cases of patellar metastasis secondary to colorectal cancer.
RT, radiotherapy; CTX, chemotherapy; SR, surgical resection; TKR, total knee replacement; NR, not reported.
| References | Year of publication | Age | Sex | Treatment(s) | Survival (Months) |
| Griener B 8 | 2001 | 57 | M | SR | 4 |
| Saglik et al 7 | 2008 | 43 | M | RT, CTX | 6 |
| Saglik et al 7 | 2008 | 67 | M | CTX | 4 |
| Gasagranda B 9 | 2014 | 51 | M | SR | NR |
In an older adult with a history of colorectal adenocarcinoma, a marrow-replacing bone lesion with cortical breach reasonably raises several possibilities, such as metastasis, solitary plasmacytoma/multiple myeloma, primary bone lymphoma, primary bone sarcoma (eg, chondrosarcoma), and osteomyelitis [ 12 ]. Before tissue sampling, all of these were plausible, as imaging features can overlap despite some helpful clues (eg, chondroid matrix for chondrosarcoma; infection markers/sequestrum for osteomyelitis; typical myeloma labs or additional osseous foci for plasmacytoma/myeloma). Primary bone lymphoma often shows a permeative marrow pattern with a disproportionately large extra-osseous soft-tissue component and relative early cortical preservation, although cortical breach can occur as the disease progresses. In our patient, MRI demonstrated a T1-hypointense/T2-hyperintense marrow-replacing humeral head lesion with cortical erosion, and PET/CT showed FDG avidity; infection markers were negative. This constellation favoured metastasis, but definitive diagnosis required biopsy, which confirmed metastatic mucinous adenocarcinoma.
Furthermore, synovial metastasis in colorectal cancer patients is extremely rare, with only 17 cases reported in the literature ( Table 2 ) [ [13] , [14] , [15] , [16] , [17] , [18] , [19] , [20] , [21] , [22] , [23] , [24] , [25] , [26] , [27] ]. In 80%-90% of colorectal cancer patients, the presence of bone metastases is generally associated with extraosseous multiorgan localizations, indicating a large burden of disease. These patients frequently present lung metastasis in 25% of cases and liver metastasis in 30% of cases. Therefore, a single bone localization in the absence of substantial visceral disease is extremely rare, as observed in our case [ 28 ]. Consequently, after performing the left shoulder bone biopsy and confirming the diagnosis of CRC metastasis, first-line treatment was initiated, suspecting micrometastatic spread not yet detectable on imaging. Surprisingly, no other localisations were detected in subsequent evaluations, and the disease remained confined to the shoulder. International guidelines recommend surgical treatment with curative intent in selected patients with a single localisation controlled by therapy [ 29 ]. This approach is considered standard practice for liver or lung metastases, with alternative local treatment options available aside from surgery [ 30 ]. However, the management of a single bone metastasis remains underexplored, likely due to the advanced stage at which the disease is typically diagnosed. Following consultation with the reference center, we elected to perform surgical resection of the shoulder metastasis with arthroplasty. This approach is grounded in robust scientific evidence from other malignancies, where arthroplasty in metastatic lesions has demonstrated improved clinical outcomes [ 31 ]. The appearance of the other synovial localisation involving the patella in the follow-up presents additional challenges. Although the mechanisms of synovial metastatic localisation are not fully understood, two main hypotheses are hematogenous spread or direct extension from an adjacent bone metastasis. Our case suggests the latter, as the extensive involvement of the patella likely led to synovial dissemination. In contrast, no synovial involvement was observed in the right shoulder. Of the 17 reported cases of synovial colorectal cancer metastases, only 6 involved bone. The case reported by Gasagranda et al. [ 9 ] is similar to ours due to the extensive patellar involvement, but it is unclear whether the soft tissue articular masses described were related to synovial lining involvement. In our case, neither cytological assessment of synovial fluid nor arthroscopic synovial biopsy was performed due to the patellar metastasis, which rendered these procedures unnecessary. The MRI findings were clear and confirmed by follow-up imaging, showing growing synovial involvement in the knee. It is important to note that metastatic synovial involvement can clinically mimic monoarticular arthritis, requiring a high level of suspicion in colorectal cancer patients [ 10 , 13 ]. Differential diagnosis on MRI includes synovial sarcoma, which typically affects adolescents and young adults, as well as other conditions causing synovial thickening, such as rheumatoid arthritis, pigmented villonodular synovitis, localised nodular synovitis, and synovial chondromatosis [ 10 ]. Therefore, biopsy is often mandatory for diagnosis. Even more unusual is the localization to the subcutaneous tissues of the second finger of the right hand. Soft tissue metastases from colorectal cancer typically occur by direct extension following surgery. However, acrometastasis, metastases distal to the elbow and knee, have been described, particularly in patients with multiorgan secondary involvement. The overall incidence of acrometastasis is 0.1% of all metastases, with those from colorectal cancer representing less than 10% [ 32 ]. The mechanisms underlying these unusual locations likely involve hematogenous and lymphatic pathways. Colorectal cancer patients with bone metastases have a poor prognosis, with a median survival of 7-9.4 months [ [33] , [34] , [35] ]. Patients with synovial metastasis have an average survival of 5 months from diagnosis [ [5] , [36] , [37] ], and those with acrometastases have an average survival of 6 months [ 38 ]. However, these data often reflect advanced disease with multiple sites of involvement, including extraosseous disease. On the other hand, as of the writing of this case report (July 2024), our patient remains alive since the initial diagnosis of metastasis to the left humerus (with a survival of 29 months) and metastasis to the patella with synovial involvement (survival of 8 months). The patient has not developed extraosseous metastases, making it difficult to predict the prognosis with the available data. Some prognostic factors to consider include multiple bone metastases, synchronous bone metastases, high levels of CEA, extra-bone metastases, and osteolytic lesions [ 39 ]. Given the unusual behaviour of the pathology, the atypical sites, and the survival, a liquid biopsy was performed better to understand the molecular characteristics of this atypical presentation. Compared to tissue biopsy, liquid biopsy can provide a better understanding of tumor heterogeneity, facilitate repeat detection, and perform real-time monitoring at the molecular level. This can help understand the tumor burden and genetic changes throughout the disease process, aiding in selecting and adjusting treatment plans. Ongoing trials are evaluating the use of liquid biopsy to guide therapeutic strategies in colorectal cancer patients, and these studies will clarify its effectiveness in predicting prognosis. However, there is still much to uncover regarding the role of liquid biopsy in metastatic colorectal cancer [ 40 ]. One of the limitations of this case is that, due to the absence of specific guidelines for solitary bone metastases, the management of the patient was based on epidemiological data (ie, the rare occurrence of bone metastases in the absence of multiorgan involvement) and the established surgical management of solitary liver and lung metastases. In reality, given the atypical location, it is currently difficult to say with certainty which radiological method can best help us monitor bone lesions. Moreover, it is important to consider that the initial MRI and PET findings in our patient were a direct result of the reported symptomatology. Therefore, it is also conceivable that during CT staging follow-up, these localizations and atypical manifestations of CRC, particularly acrometastases and localizations in joints such as the knee, may be missed. This is because CT staging protocols do not typically include these regions, based on the principle of radiation dose limitation and the technical limitations of the method. Given this limitation of CT, we believe it is essential that physicians be aware of the possibility of these atypical localizations and always maintain a high level of clinical suspicion. Table 2 Reported cases of synovial metastasis secondary to colorectal cancer. Table 2 References Year of publication Age Sex Location(s) Treatment(s) Survival (Months) Goldenberg et al. [15] 1975 62 F Knee RT, CTX 2 Graham et al. [16] 1976 51 F Hip RT NR Newton et al. [17] 1984 83 F Knee RT “short” MacAfee et al. [18] 1993 59 M TMJ SR, RT 12 Hatem et al. [19] 1997 61 M Knee NR NR Zissiadis et al. [20] 2000 59 M Knee RT 4 Beckers et al. [21] 2002 83 M Knee NR 3 Devis et al. [11] 2005 70 F Knee NR NR Ruparelia et al. [22] 2006 28 M Hip CTX 4 Capovilla et al. [23] 2006 74 F Shoulder CTX 5 Currall et al. [24] 2008 72 M Knee TKR, RT, 6 Rothenberg et al. [25] 2014 51 M Knee TKR NR Rothenberg et al. [25] 2014 62 M Hip/Knee SR NR Dhanda et al. [26] 2014 54 M Knee NR NR Ozler et al. [27] 2014 85 F Knee TKR NR Tapia Rico et al. [28] 2016 31 F Knee RT, CTX 5 Subhashini R et al. [14] 2021 60 F Knee NR NR RT, radiotherapy; CTX, chemotherapy; SR, surgical resection; TKR, total knee replacement; NR, not reported; TMJ, temporo-mandibular joint (table adapted and modified from Tapia Rico et al.).
Table 2
Reported cases of synovial metastasis secondary to colorectal cancer.
RT, radiotherapy; CTX, chemotherapy; SR, surgical resection; TKR, total knee replacement; NR, not reported; TMJ, temporo-mandibular joint (table adapted and modified from Tapia Rico et al.).
| References | Year of publication | Age | Sex | Location(s) | Treatment(s) | Survival (Months) |
| Goldenberg et al. [15] | 1975 | 62 | F | Knee | RT, CTX | 2 |
| Graham et al. [16] | 1976 | 51 | F | Hip | RT | NR |
| Newton et al. [17] | 1984 | 83 | F | Knee | RT | “short” |
| MacAfee et al. [18] | 1993 | 59 | M | TMJ | SR, RT | 12 |
| Hatem et al. [19] | 1997 | 61 | M | Knee | NR | NR |
| Zissiadis et al. [20] | 2000 | 59 | M | Knee | RT | 4 |
| Beckers et al. [21] | 2002 | 83 | M | Knee | NR | 3 |
| Devis et al. [11] | 2005 | 70 | F | Knee | NR | NR |
| Ruparelia et al. [22] | 2006 | 28 | M | Hip | CTX | 4 |
| Capovilla et al. [23] | 2006 | 74 | F | Shoulder | CTX | 5 |
| Currall et al. [24] | 2008 | 72 | M | Knee | TKR, RT, | 6 |
| Rothenberg et al. [25] | 2014 | 51 | M | Knee | TKR | NR |
| Rothenberg et al. [25] | 2014 | 62 | M | Hip/Knee | SR | NR |
| Dhanda et al. [26] | 2014 | 54 | M | Knee | NR | NR |
| Ozler et al. [27] | 2014 | 85 | F | Knee | TKR | NR |
| Tapia Rico et al. [28] | 2016 | 31 | F | Knee | RT, CTX | 5 |
| Subhashini R et al. [14] | 2021 | 60 | F | Knee | NR | NR |
Conclusion
CRC rarely metastasizes to bone and synovium in the absence of visceral disease. This case documents metachronous spread to the humeral head and patella with synovial involvement, plus an acrometastasis to the finger, highlighting diagnostic pitfalls and the value of combined MRI/PET-CT with biopsy to distinguish metastasis from mimickers. In a carefully selected patient, local control of an isolated bone lesion with resection/arthroplasty achieved durable symptom relief, while subsequent progression was managed with systemic therapy. Awareness of these uncommon patterns and the use of targeted imaging beyond routine CT fields may expedite diagnosis and inform individualized, multimodal management.
Patient consent and perspective
The patient provided written informed consent for the publication of this case report, including medical images. Although she is now in good general condition and able to perform almost all activities of daily living, she is still aware that the possibility of developing extraosseous disease is looming. Chemotherapy and pain management ensure an adequate quality of life, despite the need to wear a knee brace to support the fragile patellar situation and some limitation in shoulder movement due to the surgical intervention. However, the patient is aware that the treatments she has received and will continue to receive have allowed her to live a good life, and she is grateful for this. She is also pleased that her story is being told and that it may be useful to science, physicians, and future patients in similar conditions.
Ethical statement
This study adheres to the ethical standards outlined in the Declaration of Helsinki. The patient has provided informed consent for the publication of this case report (informed consent provided on June 4, 2024).
Author contributions
All authors of this article contributed to all stages of this article. All authors have read and approved the final version. Conceptualization: Giordana Di Mauro, Francesco Buemi. Methodology : Rosa Berenato. Collection and assembly of data: Carmine Fazzari; Review & Editing: Francesco Buemi, Anthea Miller; English review : Francesco Buemi; Supervision : Francesco Buemi
Availability of data and materials
The data are available. Requests for material must be addressed to the corresponding author with valid motivation and declaration of purpose of use.
Declaration of generative AI and AI-assisted technologies in the writing process
During the preparation of this work Francesco Buemi used ChatGPT in order to improve the English language. After using this tool/service, the authors reviewed and edited the content as needed and take full responsibility for the content of the publication.
Patient consent
The patient provided informed consent for the publication of this case report on June 4, 2024. However, due to Italian regulations on patient confidentiality, we are unable to submit the signed consent form. In accordance with these legal requirements, a copy of the signed consent can only be disclosed in exceptional circumstances, such as if specifically requested by the journal in the context of a legal issue or formal investigation. In such cases, the author will provide either the signed document or appropriate evidence confirming that consent was obtained.
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Competing Interests: The authors have declared that no competing interests exist.