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Imaging differences between enchondroma and atypical cartilaginous tumor: Insights from a reference center
, Filipe Vargasb, Pedro Netoa, Francisco Serraa, João Nelasa, Catarina Soutoa, Manuel Carrapatosoa, Pedro Cardosoa,b, Vânia Oliveiraa,b
⁎Corresponding author: Gonçalo Vieira da Silva. antoniog.vieiradasilva@gmail.com
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Received: ,
Accepted: ,
This article was originally published by Reed Elsevier India Pvt. Ltd. and was migrated to Scientific Scholar after the change of Publisher.
Abstract
Abstract
Differentiating enchondromas from atypical cartilaginous tumors (ACTs) is crucial for optimal patient management, as ACTs often require surgical intervention or surveillance, whereas enchondromas are typically managed conservatively.
This study aims to identify imaging markers that aid in distinguishing these entities through a comprehensive analysis of radiographic and magnetic resonance imaging (MRI) features.
This retrospective study included 50 patients diagnosed with ACT or enchondroma between 2013 and 2024. Imaging variables analyzed included tumor size, lobulation, matrix calcification, endosteal scalloping, periosteal reaction, cortical expansion, fat entrapment, T2-weighted hypersignal, heterogeneity, and cortical discontinuity. The distribution in short and long bones was also assessed. Statistical analysis used the Chi-square test for categorical variables and the Kruskal-Wallis test for continuous variables.
Regarding final diagnosis, most patients had enchondromas (72 %, n = 36), followed by ACTs (20 %, n = 10) and chondrosarcomas (8 %, n = 4). ACTs showed a significant increase in tumor size and a preference for long bones (p < 0.05) compared to enchondromas. Endosteal scalloping demonstrated a strong trend toward significance (p = 0.051). Other radiologic characteristics had no significant difference.
Tumor size and endosteal scalloping emerge as key markers in differentiating ACTs from enchondromas. However, the limited sample size and borderline statistical significance in some variables highlight the need for further research.
Keywords
Atypical cartilaginous tumor
Enchondroma
Imaging characteristics
Chondrosarcoma
1 Introduction
Benign central cartilaginous tumors, such as enchondromas, are typically well-delineated, slow-growing, and non-metastasizing lesions.1 They often present as incidental findings during imaging for unrelated conditions and have an excellent prognosis following curettage or marginal excision.2 In contrast, malignant tumors, such as conventional high-grade chondrosarcomas, exhibit aggressive behavior with cortical destruction, soft tissue extension, and potential for distant metastasis.1 Between these two extremes lie tumors of intermediate malignant potential, the atypical cartilaginous tumors (ACTs) which are associated with local aggressiveness and a low but not negligible risk of recurrence or malignant transformation.3 (see Figs. 1–4)
The terminology surrounding cartilaginous tumors has evolved. The World Health Organization (WHO) reclassified low-grade (grade 1) chondrosarcomas of the appendicular skeleton as atypical cartilaginous tumor in its 2013 and 2020 updates, reflecting their locally aggressive yet non-metastatic behavior.4 In the axial skeleton, tumors with identical histologic features are typically classified as grade 1 chondrosarcomas due to their more aggressive clinical behavior and higher likelihood of recurrence or metastasis.5 This nomenclature change emphasizes the importance of lesion location in determining biological potential and therapeutic approach.5
Imaging and histological appearance of cartilaginous tumors can vary widely, often mimicking both benign and malignant processes.3 A key diagnostic dilemma in musculoskeletal oncology is the differentiation between enchondromas and ACTs.3 Enchondromas are benign lesions composed of mature hyaline cartilage, frequently affecting the short tubular bones of the hands and feet, but also found in the metaphysis of long bones. These tumors are usually asymptomatic but can present with pain or pathologic fracture.3 ACTs, on the other hand, exhibit features of local invasiveness without significant metastatic potential and are mostly located in the long bones of the appendicular skeleton.6
On imaging, central cartilaginous tumors typically present as lytic lesions with varying degrees of intralesional calcification, often described as “rings and arcs” pattern.7,8 Features suggestive of malignancy include deep endosteal scalloping (greater than two-thirds of the cortical thickness), cortical breakthrough, periosteal reaction, soft tissue extension, and associated bone marrow or soft tissue edema.9,10 Magnetic resonance imaging (MRI) is particularly valuable in assessing intramedullary and soft tissue extension, as well as in evaluating peritumoral edema and the presence of aggressive features.8,10
Despite advancements in imaging, no single modality has demonstrated sufficient sensitivity and specificity to reliably differentiate enchondromas from ACTs, particularly in lesions located in long bones.11 Histological evaluation is significantly limited.12 In fact, grading of cartilaginous tumors is notoriously difficult, with significant interobserver variability, especially between ACTs and benign enchondromas. This difficulty is compounded by sampling errors during biopsy and the intrinsic heterogeneity of these tumors.12
To address these challenges, several imaging-based scoring systems and classification protocols have been proposed. The Birmingham Atypical Cartilaginous Tumor Imaging Protocol (BACTIP)13 and the Radiological Atypical Cartilaginous Tumor Scoring System (RAS30)14 are among the tools developed to aid in the differentiation between enchondromas and ACTs. These algorithms integrate clinical, imaging, and demographic data to improve diagnostic accuracy and assist in determining appropriate management strategies.
The treatment strategy for cartilaginous tumors must be individualized, balancing the risks of overtreatment against the potential for local recurrence or sarcomatous degeneration and tumor progression.15 For enchondromas, particularly those that are asymptomatic and stable on imaging, conservative treatment is indicated. Conversely, ACTs were often managed with intralesional curettage (with or without adjuvants), or wide excision depending on the anatomic site, size, growth behavior, and clinical presentation.2,5,15
Pain is a critical but nonspecific clinical symptom. While pain is classically associated with malignant lesions, it can also occur in benign active or aggressive lesions, particularly in the presence of a pathologic fracture or mechanical irritation. Therefore, pain alone should not be considered definitive for malignancy and must be interpreted in the context of imaging and histologic findings.16
Multidisciplinary evaluation in specialized centers with experience in bone tumor management is essential for accurate diagnosis and optimal treatment planning. Integration of radiologic, clinical, and histologic data—ideally within the context of a tumor board—is the most effective approach for decision-making in these complex cases.17,18 Given the rarity of these tumors and the diagnostic challenges they pose, referral to tertiary centers with expertise in musculoskeletal oncology is strongly recommended.18,19
In this context, the present study aims to review and analyze imaging, clinical, and histological characteristics of central cartilaginous tumors at the appendicular skeleton, to differentiate between enchondromas and atypical cartilaginous tumors.18,20 By synthesizing current evidence and applying structured diagnostic frameworks, we seek to contribute to the standardization of the diagnostic process and support the development of evidence-based management protocols. Improved accuracy in distinguishing these cartilaginous lesions is critical not only for avoiding unnecessary aggressive treatments but also for ensuring timely and appropriate intervention in cases with malignant potential.21,22
2 Methods
2.1 Patients and methods
Data of 50 patients diagnosed with enchondroma or ACT in bones of the appendicular skeleton was retrospectively collected since 2013 (the year when grade 1 chondrosarcoma was reclassified as ACT), in a single tertiary center. Information was retrieved from digital medical records. Initially, a demographic characterization of the sample was performed by analyzing gender and age at diagnosis.
The imaging variables assessed included: maximum diameter, lobulation, matrix calcification (< or > ⅔), periosteal reaction, cortical expansion and bulging, endosteal scalloping, penetration of the inner cortex, fat entrapment, hypersignal and heterogeneity on T2-weighted imaging, bone marrow edema, and invasion or edema of the surrounding soft tissues. The variables hypersignal, fat entrapment, and heterogeneity on T2 were only evaluated in patients who underwent MRI; therefore, those who did not were excluded from this evaluation. Additionally, a comparative analysis between short and long bones of the appendicular skeleton was performed.
Regarding tumor size, lesions were categorized into three groups: <40 mm, 40–80 mm, and ≥80 mm. This cutoff was based on the BACTIP protocol.
The definitive diagnosis was based not only on imaging findings but also on incisional biopsy (core biopsy) and histological report after surgery, when patients underwent surgery.
2.2 Statistical analysis
Qualitative variables were described using absolute frequencies (n) and percentages (%), while continuous variables were presented as mean and standard deviation. The Pearson Chi-square test was used for comparisons of categorical variables. The Kruskal-Wallis test was applied to compare continuous variables. The statistical analysis was performed using IBM SPSS Statistics for Windows, version 28.0.1.0 (IBM Corp., Armonk, N.Y., USA). A p-value of <0.05 was considered statistically significant.
2.3 Ethical responsibilities
This retrospective study was approved by our institution's Ethics Committee.
3 Results
3.1 Sample characterization
This retrospective study included 50 patients, the majority of whom were female (72 %, n = 36). The mean age at diagnosis was 41.22 years, ranging from 5 to 83 years. Regarding final diagnosis, 72 % (n = 36) of patients were diagnosed with enchondroma, 20 % (n = 10) with atypical cartilaginous tumors (ACTs), and 8 % (n = 4) with high-grade chondrosarcoma. Notably, 28 % (n = 14) of patients initially received an imaging-based diagnosis of ACTs; however, four of these cases were later confirmed as high-grade chondrosarcoma based on postoperative histological results.
The most frequently affected sites were long bones, accounting for 66 % (n = 33) of cases, with the proximal humerus being the most common location (18 %, n = 9). Short bones of the hand were also a relevant location, affecting 26 % (n = 13) of patients. The laterality distribution was equal, with 52 % (n = 26) of cases on the right side and 48 % (n = 24) on the left.
Regarding clinical outcomes, at last follow-up, 66 % (n = 33) of patients had no evidence of disease after treatment, 28 % (n = 14) were alive with the disease (managed conservatively), and 6 % (n = 3) succumbed to disease progression. Table 1 summarizes the characteristics of the study population. Table 2 presents the imaging characteristics of the lesions.
| Variable | n (%) |
| Gender | |
| Male | 14 (28) |
| Female | 36 (72) |
| Age at Diagnosis (years)∗ | 41.22 (5-83)a |
| Final Diagnosis | |
| Enchondroma | 36 (72) |
| ACT | 10 (20) |
| High-grade Chondrosarcoma | 4 (8) |
| Laterality | |
| Right | 26 (52) |
| Left | 24 (48) |
| Outcome | |
| No evidence of disease | 33 (66) |
| Alive with disease | 14 (28) |
| Dead due to disease | 3 (6) |
| Location | |
| Proximal humerus | 9 (18) |
| Proximal femur | 5 (10) |
| Femoral diaphysis | 2 (4) |
| Distal femur | 9 (18) |
| Proximal tibia | 2 (4) |
| Proximal fibula | 2 (4) |
| Distal radius | 2 (4) |
| Scapula | 2 (4) |
| Hand bone | 13 (26) |
| Foot bone | 4 (8) |
| Total short bones | 17 (34) |
| Total long bones | 33 (66) |
| Imaging Variables, n (%) | Enchondroma (n = 36) | ACT (n = 10) | p-Value b |
| Size (mm) a | 31.0 (8.2–90.0) | 87.1 (25.0–255.0) | p < 0.001 |
| <40 mm | 26 (72.2) | 2 (20.0) | p < 0.001 |
| 40–80 mm | 9 (25.0) | 3 (30.0) | |
| ≥80 mm | 1 (2.8) | 5 (50.0) | |
| Lobulation | 13 (36.1) | 7 (70.0) | p = 0.093 |
| Calcification ≥ ⅔ | 19 (52.8) | 7 (70) | p = 0.632 |
| Periosteal Reaction | 0 (0.0) | 0 (0.0) | |
| Expansion | 16 (44.4) | 5 (50.0) | p = 1.000 |
| Endosteal scalloping | 18 (50) | 8 (80.0) | p = 0.051 |
| Cortical Penetration | 22 (61.1) | 6 (60.0) | p = 0.376 |
| Bone Edema | 4 (40.0) | 4 (40.0) | p = 0.185 |
| Soft Tissue Extension | 1 (2.8) | 0 (0.0) | |
| Soft Tissue Edema | 1 (2.8) | 1 (25.0) | |
| Location | p = 0.041 | ||
| Short Bone | 16 (44.4) | 1 (10.0) | |
| Long Bone | 20 (55.6) | 9 (90.0) | |
| Hyperintensity on T2 | 9 (100) | 9 (100) | p = 0.633 |
| Fat Entrapment | 3 (16.7) | 0 (0.0) | p = 0.386 |
| Heterogeneous T2 | 15 (83.3) | 7 (77.8) | p = 1.000 |
3.2 Imaging analysis
The mean tumor size was 31.0 mm for enchondromas (range: 8.2–90.0 mm), significantly increasing in ACTs and high-grade chondrosarcomas, with mean values of 87.1 mm (range: 25.0–255.0 mm) and 97.0 mm (range: 38.0–130.0 mm), respectively. This size difference between enchondromas and ACTs was statistically significant (p < 0.001), as was the difference between enchondromas and high-grade chondrosarcomas (p = 0.004).
Among enchondromas, 72.2 % (n = 26) measured <40 mm, 25 % (n = 9) were 40–80 mm, and only 2.8 % (n = 1) exceeded 80 mm. In contrast, 20 % (n = 2) of ACTs were <40 mm, 30 % (n = 3) were 40–80 mm, and 50 % (n = 5) were ≥80 mm. Similarly, in high-grade chondrosarcomas, no tumors measured <40 mm, 25 % (n = 1) were 40–80 mm, and 75 % (n = 3) exceeded 80 mm.
Other imaging characteristics, such as lobulation and matrix calcification >⅔, varied across tumor types but did not reach statistical significance (p > 0.05). However, endosteal scalloping was more frequent in ACTs (80 %) and high-grade chondrosarcomas (100 %) compared to enchondromas (50 %), with a p-value approaching significance (p = 0.051).
Short bone involvement was observed in 44.4 % of enchondromas and 10 % of ACTs, while long bones were affected in 55.6 % of enchondromas and 90 % of ACTs. The association of short bone location with enchondromas was statistically significant (p = 0.041).
Additional imaging features revealed no periosteal reaction in any of the tumors. Cortical expansion was identified in 44.4 % of enchondromas, 50 % of ACTs, and 50 % of high-grade chondrosarcomas. Inner cortical penetration was more frequent in high-grade chondrosarcomas (100 %) compared to 61.1 % in enchondromas and 60 % in ACTs. Bone marrow edema was present in 13.9 % of enchondromas, 40 % of ACTs, and 25 % of high-grade chondrosarcomas. Soft tissue extension and soft tissue edema were rare, occurring in only 2.8 % of enchondromas (associated with pathological fracture). None of these variables reached statistical significance.
Among patients who underwent MRI, hypersignal on T2-weighted imaging was observed in 88.6 % of enchondromas, with no significant differences between tumor types. Fat entrapment was rare in enchondromas (16.7 %) and absent in ACTs, whereas heterogeneous T2 signal was identified in 83.3 % of enchondromas and in similar proportions across other tumor types.
3.3 Statistical analysis of additional variables
Analysis of additional variables (Table 3) revealed that biopsy was performed in 47.2 % (n = 17) of patients with enchondromas and in all patients, preoperatively, diagnosed with ACT (n = 14). Pathological fractures were identified in 13.9 % of enchondroma cases, whereas no cases were reported among ACT patients. Conservative treatment was adopted in 38.9 % (n = 14) of enchondroma cases, while all ACT patients underwent surgical treatment. Local recurrence was observed in 8.3 % (n = 3) of enchondromas and 10 % (n = 1) of ACTs. No cases of distant metastases were reported in patients with enchondromas, whereas metastases were identified in 3 ACT patients (21.4 %), including 2 of the 4 high-grade chondrosarcomas and 1 ACT case that experienced local recurrence and progressed to high-grade chondrosarcoma.
| Variables | Enchondroma (n = 36) | ACT (n = 10) | Chondrosarcoma (n = 4) | Total, n (%) |
| Biopsy | 17 (47.2) | 14 (100.0) | 30 (60.0) | |
| Pathological fracture | 5 (13.9) | 0 (0.0) | 0 (0.0) | 5 (10.0) |
| Conservative treatment | 14 (38.9) | 0 (0.0) | 0 (0.0) | 14 (28.0) |
| Local recurrence | 3 (8.3) | 1 (10.0) | 0 (0.0) | 4 (8.0) |
| Metastatic disease | 0 (0.0) | 1 (10.0) | 2 (50.0) | 3 (6.0) |
| Final outcome | ||||
| No evidence of disease | 22 (61.1) | 9 (90.0) | 2 (50.0) | 33 (66.0) |
| Living with disease | 14 (38.9) | 0 (0.0) | 0 (0.0 %) | 14 (28.0) |
| Death due to disease | 0 (0.0) | 1 (10.0) | 2 (50.0) | 3 (6.0) |
Regarding final outcomes, patients with enchondromas exhibited a favorable prognosis, with 61.1 % (n = 22) showing no evidence of disease post-treatment. Additionally, a considerable proportion, 38.9 % (n = 14), remained alive with asymptomatic disease and were managed through imaging surveillance rather than surgical intervention. Among ACT patients, 90 % (n = 9) showed no evidence of disease progression. However, one case (10 %) resulted in mortality due to tumor progression following local recurrence, with subsequent distant metastases to the lungs.
The four cases initially diagnosed with ACT but postoperatively confirmed as having high-grade chondrosarcoma were all immediately submitted to wide resection and endoprosthetic reconstruction after the histological report came out. No local recurrences were observed in any case (margins were all negative). From the total of 4 patients, 50 % (n = 2) developed systemic disease (lung metastases) and succumbed to metastatic disease, whereas the remaining 50 % (n = 2) had no evidence of disease and remain under oncologic surveillance. This mortality rate highlights the aggressive nature and challenging prognosis associated with high-grade chondrosarcomas when compared to enchondromas or ACTs.
4 Discussion
The core focus of this research was the imagiologic distinction between enchondromas and ACTs, a differentiation that is crucial for therapeutic decision-making. The lack of need for intervention in enchondromas strongly contrasts with the necessity for close monitoring, intralesional treatment, or wide resection in ACTs, highlighting the vital importance of diagnostic accuracy. Our analysis reinforced that the integration of clinical, imaging, and histological data enhances the distinction between these lesions, corroborating previous studies that emphasize the value of imaging features in CT and, especially, MRI.13,14
This study revealed a statistically significant increase in tumor size when comparing enchondromas with ACTs (and high-grade chondrosarcomas). Tumor size emerged as a significant distinguishing marker, particularly lesions larger than 40 mm, which are suggestive of ACTs. This aligns with the previously established notion that enchondromas are smaller compared to ACTs, as supported by prior studies.9
Endosteal scalloping was found to be a potentially significant variable (p = 0.051) for distinguishing ACTs. In fact, Patel et al. (2019) incorporated this criterion into the Radiological Aggressiveness Score (RAS) as an important parameter for differentiating chondrosarcomas from enchondromas.14,23 Endosteal scalloping reflects a greater local aggressiveness and destructive potential of these lesions. The RAS study also validated the correlation of imaging criteria with histological grades in cartilaginous tumors, suggesting that future studies could refine and optimize these scoring systems.14 Although periosteal reaction was not observed, penetration of the inner cortical bone was identified in high-grade chondrosarcomas, corroborating the notion that these tumors exhibit a more invasive and aggressive behavior.11
Furthermore, although some variables did not reach statistical significance, they may still hold diagnostic relevance, an aspect that could be explored in future studies with larger sample sizes. The practice of performing biopsies reflected the need for diagnostic precision, as a considerable proportion of enchondromas underwent this procedure, demonstrating that uncertainty persists despite technological advancements.9
The RAS study highlighted that periosteal reaction on radiographs, endosteal scalloping and cortical defect on CT, multilobulated lesion, soft tissue mass, abnormal signal in adjacent bone marrow and soft tissue extension on MRI, and increased uptake on bone scintigraphy are differentiating variables between enchondromas and chondrosarcomas.14
Another significant aspect of our study was the prevalence of tumors in long and short bones. The distribution of enchondromas in short bones was notably high at 44.4 % (p = 0.041), consistent with recent literature.3 This predominance may support the hypothesis that tumor aggressiveness is higher in more vascularized areas.3
Pathological fractures were identified in 13.9 % of enchondromas (mostly in short bones). This complication often raises suspicions of malignancy, and in chondrosarcomas, they may have prognostic implications.2 However, their presence in enchondromas suggests that this characteristic alone is insufficient to determine the tumor's aggressive nature. This observation reinforces the need for a holistic diagnostic approach and suggests caution in interpreting pathological fractures as a strong indicator of malignancy.2
This study has several limitations, including its retrospective nature, the small sample size, and its execution at a single center. Additionally, no ACT included in the study was treated conservatively and monitored. A third group of high-grade chondrosarcomas was not included to study imaging features since, on one hand, the objective was to differentiate ACTs from enchondromas, and on the other, there is a consensus on the greater imaging and clinical aggressiveness of high-grade chondrosarcomas, with histology frequently confirming malignancy.17
In four cases, the initial biopsy diagnosis was ACT, but postoperative analysis confirmed them as high-grade chondrosarcomas, underscoring the heterogeneity of these lesions, where areas or foci of different grades may coexist during malignant degeneration. This highlights the importance of referring these cases to specialized centers with experienced multidisciplinary teams, as even then, underdiagnoses can occur.18,19
No cases of tumor progression were observed in enchondromas. In ACTs, one case experienced local recurrence and revealed upgrade to high-grade chondrosarcoma, eventually progressing to systemic disease (lung metastases). The results emphasize that patients with enchondromas and ACTs usually remain asymptomatic or disease-free.3
This research highlights the persistent challenge in differentiating enchondromas and ACTs, even with advancements in diagnostic methods. The inherent subjectivity in interpreting radiological variables and interobserver variability in imaging and histological assessment emphasize the necessity for more robust, consensus-based guidelines.16
The pertinence of our study is underscored by the conclusions of the 2024 Birmingham Orthopaedic Oncology Meeting (BOOM), a consensus conference that brought together international experts and achieved agreement based on scientific evidence in 19 out of 21 key questions discussed. Extraosseous soft tissue extension, cortical destruction, and perilesional bone or soft tissue edema on MRI were identified as strong positive predictive indicators for distinguishing high-grade chondrosarcomas from benign, intermediate, or low-grade cartilaginous tumors. There was broad consensus that purely intraosseous cartilaginous lesions have negligible metastatic potential. Conversely, the presence of an extraosseous soft tissue mass was recognized as a significant prognostic factor for metastatic progression. Biopsy remains an essential diagnostic tool in high-grade lesions with clinically and radiologically aggressive features, but is no longer routinely indicated for benign or intermediate-grade cartilaginous tumors due to its diagnostic limitations. The consensus further emphasized the need for ongoing multicenter studies with larger sample sizes to refine diagnostic accuracy and therapeutic approaches.16,17
Then, the most recent evidence points toward a more conservative approach for both pathologies, with aggressive treatment (wide resections) reserved for cases exhibiting aggressive changes suggestive of degeneration to high-grade chondrosarcoma during imaging follow-up (MRI).17
There is an ongoing need for a standardized, multidisciplinary diagnostic and therapeutic framework, ideally implemented in specialized centers. Such an approach could minimize inter-center discrepancies, optimize resource allocation, and enhance treatment efficacy and patient quality of life for these complex, heterogeneous, and biologically unpredictable pathologies.17
5 Conclusion
This study underscores the clinical relevance of differentiating enchondromas from ACTs through a multidisciplinary approach combining clinical, imaging, and histological data. Tumor size ≥40 mm and pronounced endosteal scalloping emerged as key features suggestive of ACT, while enchondromas were more commonly located in short bones.
These findings are consistent with existing literature and contribute to refining diagnostic criteria. The heterogeneity and overlapping features between ACTs and enchondromas highlight the need for improved diagnostic accuracy to avoid under- or overtreatment.
Further prospective, multicenter studies are needed to validate these findings and to delineate reliable imaging markers that can assist in early identification of aggressive behavior or progression to high-grade chondrosarcoma.
In summary, this research supports the growing emphasis on specialized multidisciplinary care and the urgent need for standardized, evidence-based guidelines to improve outcomes and reduce variability in the management of central cartilaginous tumors.
CRediT authorship contribution statement
Gonçalo Vieira da Silva: Conceptualization, Investigation, Writing – original draft. Filipe Vargas: Software. Pedro Neto: Resources. Francisco Serra: Data curation. João Nelas: Writing – review & editing. Catarina Souto: Visualization. Manuel Carrapatoso: Formal analysis. Pedro Cardoso: Project administration. Vânia Oliveira: Methodology, Validation, Supervision.
Patient consent statement
As this study was retrospective and involved the analysis of de-identified clinical data, formal patient consent was not required. All patient data was handled in accordance with institutional ethical guidelines and privacy regulations.
Ethical responsibilities
This retrospective study was approved by our institution's Ethics Committee.
Funding statement
This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
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