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PhD in Veterinary Sciences for Animal Health and Food Safety

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Logo di PhD in Veterinary Sciences for Animal Health and Food Safety

Davide Giacobino

Phd thesis

Re-evaluation of the clinical tumour-nodes-metastasis (TNM) staging system for canine oral malignant melanoma

 1) Background

Malignant melanoma is the most common oral tumor in dogs, accounting for up to 40% of malignant oral tumors in this species. It exhibits highly aggressive biological behavior, with a strong ability to locally invade tissues and a high metastatic rate. It can present with different appearances, sizes, and degrees of pigmentation. The most common intraoral locations include the gums, lips and cheeks, palate, and, less frequently, the tongue and tonsils. Typically, patients present with general clinical symptoms such as hypersalivation, dysphagia, halitosis, and pain.

Diagnosis, in addition to clinical examination, can be achieved through cytology of the primary tumor and lymph nodes, but primarily through histological examination and imaging diagnostics. These techniques help define the histological characteristics of melanoma, and determine the clinical stage of the patient, thus providing prognostic indications.

Malignant oral melanoma is clinically classified according to the TNM system, initially proposed by Owen for veterinary medicine in 1980 and later modified and simplified by Bergman in 2007 for this specific tumor. The TNM system assigns a clinical stage that describes the anatomical extent of the tumor in the patient, based on three parameters:

  • The size of the primary tumor (measured as its maximum diameter).
  • The status of regional lymph nodes.
  • The presence or absence of distant metastases.

This system has several limitations, especially when compared to the TNM system used in human medicine. Specifically, the veterinary TNM system does not consider:

  • Invasion of surrounding tissues and anatomical spaces.
  • Various histological factors recognized as prognostic indicators.
  • The wide range of size variations among canine patients.

Moreover, the TNM classification in human medicine is continuously updated based on ongoing research, unlike its veterinary counterpart.

2) Specific aims of the project, Methods, Results

The goal of this project was to update the TNM system by modifying its parameters to provide more precise prognostic indications. The aim was to define different clinical stages, each associated with distinct outcomes, and to aid in therapeutic decision-making, guiding the choice of appropriate treatments, the need for more or less invasive surgery, the number of lymph nodes to remove, and the necessity for adjuvant therapies.

The project was divided into two phases:

  • The first study focused on the N parameter, evaluating the presence or absence of lymph node metastases and the role of lymphadenectomy in staging and prognosis.
  • The second study examined the size of the primary tumor, incorporating anatomical location and histological parameters.

First study

Currently, despite there is a consensus on local control of OMM, the modalities of head and neck lymphadenectomy for clinical staging and their impact on prognosis remain an area of ongoing research and debate. Currently, bilateral removal of mandibular and medial retropharyngeal lymph nodes is recommended, while the parotid lymph node is usually omitted as it appears to be less frequently involved. Moreover, the presence or absence of lymph node metastases can only be accurately determined through post-surgical histological examination, as cytology and imaging diagnostics have low accuracy.

The study aimed to:

  • Evaluate the prognostic impact of lymph node metastases at the time of diagnosis.
  • Identify the most effective approach to lymphadenectomy.

A total of 77 dogs were divided into two groups based on the presence (group A) or absence (Group B) of lymph node metastases and were then further stratified based on the type of lymphadenectomy performed—ipsilateral (Group 1) or bilateral (Group 2), and whether the medial retropharyngeal lymph node was removed.

The inclusion criteria required the surgical removal of the primary tumor and regional lymphadenectomy, followed by histological evaluation. Only dogs vaccinated against CSPG4 were included, to ensure a more homogeneous study population. Dogs must not present distant metastases, severe comorbidities, and must have a minimum of one year of follow-up.

For each dog, the collected data included age, gender, weight, breed, tumour size and localization, clinical and at imaging enlargement of head and neck LNs, type of surgery performed (en bloc excision, including mandibulectomy and maxillectomy) and pattern of regional lymphadenectomy (ipsilateral or bilateral mandibular +/- medial retropharyngeal nodes), definitive TNM stage after LN histology and adjuvant treatment adopted (anti-CSPG4 DNA electrovaccination; second surgery and/or radiotherapy or electrochemotherapy at local recurrence occurrence; and metronomic therapy at disease's progression)

Statistical Analysis

The analyses were carried out using GraphPad Prism (version 10.3.1 for Windows, GraphPad Software, San Diego, California, www.graphpad.com), with statistical significance set at a P < .05. The data were summarized using descriptive statistics, and were indicated as mean, median and range. Distribution was checked graphically using the Shapiro-Wilk Test; Mann-Whitney and Kruskal-Wallis tests were used to assess statistical differences among different groups regarding age, weight, stages, MC, Ki67, CSPG4 expression and clinical tumour stage. The median disease-free interval (DFI) and survival time (MST) were evaluated using the Kaplan-Meier method; the log-rank test was used to calculate the DFI and MST of the dogs in the treatment groups. The DFI of dogs was calculated from the day of surgery to the first tumour recurrence or metastasis while the survival time (ST) as the period from the day of surgery to the patient's death. Dogs which died from non-COMM-related causes, those lost to follow-up and those still alive at the end of the study were censored. Finally, the Fisher's exact test was used to test a potential association between the different patterns of neck lymphadenectomy and the probability of local recurrence and/or metastasis and to assess the relationships between LN metastasis and primary tumour size and location within the oral cavity

Results

When patients were grouped based on lymph node status, the median survival time (MST) and disease-free interval (DFI) were higher in dogs without lymph node metastases, although the difference was not statistically significant. The ipsilateral mandibular lymph node was identified as the most commonly affected lymphatic center.

Additionally, no statistically significant differences were observed in MST and DFI when the population was stratified by the type of lymphadenectomy. Similarly, no significant differences were found when comparing the group where only the ipsilateral mandibular lymph node was removed with the group where all regional lymph nodes were removed bilaterally.

Moreover, no association was found between the presence of lymph node metastases at diagnosis and the size or location of the primary tumor, the risk of recurrence, or the likelihood of distant metastases. Similarly, no association was observed between the type of lymphadenectomy performed and the risk of disease progression.

Conclusions

The lymph node metastasis rate observed in this study aligns with previously reported data. Lymph node status does not appear to have a significant prognostic impact. 

Lymphadenectomy type does not seem to influence the risk of recurrence or new metastases. Although radical lymphadenectomy ensures the highest detection rate of metastatic nodes, ipsilateral mandibular lymphadenectomy appears to be a good option, reducing surgical burden without compromising patient outcomes. However, sentinel lymph node mapping techniques should be improved to ensure precise removal of the first draining lymphatic station.

The main limitations of the study include its retrospective nature, the limited number of cases, particularly in some stratified groups, and the absence of a control group in which lymphadenectomy was not performed

Second Study 

It is well established in the literature that the ability to achieve complete resection of an oral tumor depends on its size and location within the oral cavity. Large tumors located caudally are less likely to have clean surgical margins.

However, describing tumor size alone does not account for the anatomical differences between breeds; for example, a 3 cm tumor can have a completely different impact if located in the mouth of a Labrador compared to a Pinscher.

Additionally, as previously mentioned, the TNM system only considers size and does not take into account histological tumor characteristics.

The objectives of this study were to develop a tumor-specific index for each dog, introduce prognostic histological factors, and evaluate the ability of this new parameter to predict patient outcomes.

A new Index I, defined as the ratio between tumor size and skull size of the patient, was created, and compared it to the T parameter. Then the index was improved by incorporating histological characteristics.

Next, dogs were classified into groups based on Index I, stratifying them accordingly to MST. 

Using CT scans, I measured the tumor implant surface as well as the surfaces of the mandible and maxilla across different CT projections, based on the tumor's position. This allowed me to define Index I as the ratio between the tumor implant surface and the sum of the mandibular and maxillary surfaces

I specifically chose tumor implantation surface area because it represents the actual connection between the tumor and the patient, making it a more reliable measurement.

The study included all dogs that underwent pre-surgical staging with skull CT scans, had surgical removal of the primary tumor and regional lymph nodes followed by histological evaluation, had no distant metastases or severe comorbidities, and had at least one year of follow-up.

I collected all clinical and histological data, focusing on tumor size, location, and CT measurements of both the tumor and skull dimensions.

The study enrolled 60 dogs, and as a first step, I performed a Spearman correlation between T and I values and the oncological endpoints: MST (Median Survival Time), DFI (Disease-Free Interval), and TTR (Time to Recurrence).

Both parameters were significantly and inversely correlated, confirming a relationship between Index I and patient outcomes. This serves as a preliminary test to validate the potential effectiveness of the proposed method.

I then used Cox proportional hazards regression to evaluate the influence of I and T on median survival time.

When comparing the two models, the one based on Tumor-to-Head Index (I) appeared superior, as evidenced by:

  • Greater statistical significance (lower p-value).
  • Narrower confidence intervals, indicating a more precise risk estimate.
  • A lower Akaike Information Criterion (AIC), reflecting better predictive capability.

Next, I incorporated histological factors into the model to improve its reliability. However, Index I maintained its significance only when combined with bone invasion. The inclusion of other factors, such as Ki67 and mitotic index, led to the loss of statistical significance of I and did not add value to the model. Furthermore, bone invasion was associated with a significantly higher risk of tumor-related death compared to other parameters, including Index I. This suggests that bone invasion may have a stronger and independent prognostic role compared to other histological factors.

As the next step, I divided Index I into three classes, using the first and third quartile values as cutoff points.

Survival curves plotted for these three classes revealed a significant log-rank test for trend.

When analyzing pairwise comparisons:

  • Despite a noticeable difference in survival (in days), there was no statistically significant difference between Class 1 and Class 2, as shown in the graph.
  • However, a significant difference was observed between Class 2 and Class 3.

The class-based stratification of Index I was statistically associated with the presence of lymph node metastases at diagnosis. However, no association was found between Index I classes and progressive disease. When analyzing recurrence and distant metastases, no association was found with recurrence, but there was an association with the development of distant metastases

Conclusions

Index I appears to be a more sensitive and reliable indicator than T in predicting patient outcomes. Histological prognostic factors described in the literature do not seem to significantly influence survival or provide additional prognostic insights, except for bone invasion. Stratification of Index I into classes may be useful for treatment planning.

For example: A dog with a Class 1 tumor, having a lower probability of lymph node metastases, could undergo a more selective lymphadenectomy. Conversely, a dog with a Class 3 tumor, associated with a higher risk of distant metastases, should receive adjuvant therapies.

This study has several limitations, including its retrospective nature and the limited number of cases. Moreover, some dogs received different adjuvant treatments and were monitored at varying intervals, which is why this study only evaluated MST (Median Survival Time) and not DFI (Disease-Free Interval). Furthermore, the surgeon's skill in removing the primary tumor was not considered, which may have influenced the evaluation of histological margins and the risk of local recurrence

Conclusion

In this project, I did not consider the M parameter, as it is recognized as the factor with the greatest impact on patient outcome, both in human and veterinary medicine, reducing the relative importance of other parameters. Furthermore, the presence of distant metastases usually excludes patients from curative-intent treatments (surgery/radiotherapy), preventing an adequate histological and prognostic evaluation.

The presence of lymph node metastases, if surgically removed, does not appear to significantly affect patient survival. However, since there is no untreated control group, it is not possible to directly compare prognostic differences. To optimize treatment, it is crucial to implement sentinel lymph node mapping in oral melanomas, reducing the surgical burden while ensuring the removal of potentially metastatic lymph nodes.

Regarding the primary tumor description, Index I appears to be a more effective prognostic indicator than parameter T. However, it is necessary to identify new histological parameters that can further strengthen the proposed model, enhancing its predictive accuracy and prognostic precision.

 

4) Bibliography

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  5. Camerino M, Giacobino D, Manassero L, et al.  Prognostic impact of bone invasion in canine oral malignant melanoma treated by surgery and anti-CSPG4 vaccination: A retrospective study on 68 cases (2010–2020). Vet Comp Oncol 2022; 20: 189–197.
  6. Chiti LE, Stefanello D, Manfredi M, et al To map or not to map the cN0 neck: Impact of sentinel lymph node biopsy in canine head and neck tumours.. Vet Comp Oncol 2021;19(4):661-670.
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  8. Giacobino D, Camerino M, Riccardo F, et al. Difference in outcome between curative intent vs marginal excision as a first treatment in dogs with oral malignant melanoma and the impact of adjuvant CSPG4-DNA electrovaccination: A retrospective study on 155 cases. Vet Comp Oncol 2021; 19(4):651-660.
  9. Goldschmidt S, Stewart N, Ober C, et al. Contrast-enhanced and indirect computed tomography lymphangiography accurately identifies the cervical lymphocenter at risk for metastasis in pet dogs with spontaneously occurring oral neoplasia. PLoS One 2023; 18(3):e0282500.
  10. Green K and Boston SE. Bilateral removal of the mandibular and medial retropharyngeal lymph nodes through a single ventral midline incision for staging of head and neck cancers in dogs: a description of surgical technique. Vet Comp Oncol 2017; 15(1):208-214.
  11. Grimes JA, Matz BM, Christopherson PW, Koehler JW, Cappelle KK, Hlusko KC, Smith A. Agreement Between Cytology and Histopathology for Regional Lymph Node Metastasis in Dogs with Melanocytic Neoplasms. Vet Pathol 2017; 54:579–587.
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  15. Kim WS, Vinayak A, Powers B. Comparative Review of Malignant Melanoma and Histologically Well-differentiated Melanocytic Neoplasm in The Oral Cavity of Dogs. Vet Sci 2021;8(11):261.
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  18. Menghini TL, Schwarz T, Dancer S, Gray C, MacGillivray T, Bowlt Blacklock KL. Contrast-enhanced CT predictors of lymph nodal metastasis in dogs with oral melanoma. Vet Radiol Ultrasound 2023; 64(4):694-705.
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Research activities

Periods in a foreign laboratory

  • Faculty of Veterinary Medicine, University of Lisbon, Portugal. Two months from January 24th to March 24th, 2024, under the supervision of Prof. Dr. Lisa Mestrinho, Assistant professor, dipl. ACVD.
  • Faculty of Veterinary Medicine, University of Vienna, Austria. Two months from August 1st to September 30th, 2024, at. under the supervision of Dr. Chiara Kocher, resident ECVS, Prof. Eva Schnabl-Feichter, dipl. ECVS; Prof. Brigitte Degasperi, Dipl. ECVS, Prof. Gabriele Gradner, Dipl. ECVS.

Research products:

Selected Peer-reviewed Publications: Scopus ID 57189063112, https://orcid.org/0000-0001-8906-9490, 24 papers; h-index 9.

  • Giacobino, D; Olimpo, M; Ferraris, E; Martinelli, G; Maniscalco, L; Camerino, M; Riccardo, F; Tarone, L; Cino, M; Dentini, A; Iussich, S; Lardone, E; Manassero, L; De Maria, R; Cavallo, F; Buracco, P; Morello, E. “Different patterns of regional lymphadenectomies in dogs with oral malignant melanoma and prognostic impact of the postoperative lymph node status and metastasis distribution: a retrospective study on 77 cases.” has been successfully submitted online and is presently being given full consideration for publication in Veterinary and Comparative Oncology.
  • Silva ML, Martinho I, Rocha M, Martano M, Spindler KP, Buracco P, Giacobino D, Florindo HF, Mestrinho LA. Relative Tumour Volume in Canine Oral Melanoma Staging and Prognosis. Vet Comp Oncol. 2024 Dec;22(4):641-650.
  • Gola C, Maniscalco L, Iussich S, Morello E, Olimpo M, Martignani E, Accornero P, Giacobino D, Mazzone E, Modesto P, Varello K, Aresu L, De Maria R. Hypoxia-associated markers in the prognosis of oral canine melanoma. Vet Pathol. 2024 Sep;61(5):721-731.
  • Tarone L, Giacobino D, Camerino M, Maniscalco L, Iussich S, Parisi L, Giovannini G, Dentini A, Bolli E, Quaglino E, Merighi IF, Morello E, Buracco P, Riccardo F, Cavallo F. “A chimeric human/dog-DNA vaccine against CSPG4 induces immunity with therapeutic potential in comparative preclinical models of osteosarcoma”. Mol Ther. 2023 Aug 2;31(8):2342-2359.
  • Olimpo M, Ferraris EI, Parisi L, Buracco P, Rizzo SG, Giacobino D, Degiovanni A, Maniscalco L, Morello E. “Diagnostic Findings and Surgical Management of Three Dogs Affected by Osseous Metaplasia Secondary to a Salivary Mucocele”. Animals (Basel). 2023 May 5;13(9):1550.
  • Carroll M, Morello E, Olimpo M, Giacobino D, Buracco P, Ferraris E. “Random mucosal rotating flaps for rostral to mid maxillary defect reconstruction: 26 dogs (2000-2019)”. J Small Anim Pract 2023;64(3):149-60.
  • Ferraris EI, Olimpo M, Giacobino D, Manassero L, Iussich S, Lardone E, Camerino M, Buracco P, Morello EM. “Sentinel lymph node mapping with computed tomography lymphography for mast cell tumours and a comparison between regional and sentinel lymph node histological status: Sixty-two cases”. Vet Comp Oncol 2023.
  • Olimpo M, Buracco P, Ferraris EI, Piras LA, Maniscalco L, Giacobino D, Degiovanni A, Morello E. “Surgical excision of intramuscular sarcomas: Description of three cases in dogs”. Animals 2023;13(2).
  • Tarone L, Mareschi K, Tirtei E, Giacobino D, Camerino M, Buracco P, Morello E, Cavallo F, Riccardo F. “Improving osteosarcoma treatment: Comparative oncology in action”. Life 2022;12(12).
  • Maniscalco L, Varello K, Morello E, Montemurro V, Olimpo M, Giacobino D, Abbamonte G, Gola C, Iussich S, Bozzetta E. “Investigating a prognostic factor for canine hepatocellular carcinoma: Analysis of different histological grading systems and the role of PIVKA-II”. Vet Sci 2022;9(12).
  • Lardone E, Sarotti D, Giacobino D, Ferraris E, Franci P. “Thoracic epidural anaesthesia vs intrathecal morphine in dogs undergoing major thoracic and abdominal surgery: Clinical study”. BMC Vet Res 2022;18(1).
  • Riccardo F, Tarone L, Camerino M, Giacobino D, Iussich S, Barutello G, Arigoni M, Conti L, Bolli E, Quaglino E, Merighi IF, Morello E, Dentini A, Ferrone S, Buracco P, Cavallo F. “Antigen mimicry as an effective strategy to induce CSPG4-targeted immunity in dogs with oral melanoma: A veterinary trial”. J Immunother Cancer 2022;10(5).
  • Camerino M, Giacobino D, Manassero L, Iussich S, Riccardo F, Cavallo F, Tarone L, Olimpo M, Lardone E, Martano M, Del Magno S, Buracco P, Morello E. “Prognostic impact of bone invasion in canine oral malignant melanoma treated by surgery and anti-CSPG4 vaccination: A retrospective study on 68 cases (2010–2020)”. Vet Comp Oncol 2022;20(1):189-97.
  • Tarone L, Giacobino D, Camerino M, Ferrone S, Buracco P, Cavallo F, Riccardo F. “Canine melanoma immunology and immunotherapy: Relevance of translational research”. Front Vet Sci 2022;9.
  • Giacobino D, Camerino M, Riccardo F, Cavallo F, Tarone L, Martano M, Dentini A, Iussich S, Lardone E, Franci P, Valazza A, Manassero L, Del Magno S, De Maria R, Morello E, Buracco P. “Difference in outcome between curative intent vs marginal excision as a first treatment in dogs with oral malignant melanoma and the impact of adjuvant CSPG4-DNA electrovaccination: A retrospective study on 155 cases”. Vet Comp Oncol 2021 Dec;19(4):651-60.

Poster presentation at Games of Research 15 December 2022 “A chimeric Human-Dog CPSG4 DNA vaccine as part of a multimodal treatment for canine oral malignant melanoma” Davide Giacobino, Mariateresa Camerino, Federica Riccardo, Lidia Tarone, Erica Ilaria Ferraris, Matteo Olimpo, Giuseppina Barutello, Maddalena Arigoni, Selina Iussich, Elena Lardone, Emanuela Morello, Soldano Ferrone, Paolo Buracco, Federica Cavallo

Poster presentation at 21st International Conference on Progress in Vaccination against Cancer (PIVAC 22) 26-28 September 2022 “A chimeric Human-Dog CPSG4 DNA vaccine as part of a multimodal treatment for canine oral malignant melanoma” Davide Giacobino, Mariateresa Camerino, Federica Riccardo, Lidia Tarone, Erica Ilaria Ferraris, Matteo Olimpo, Giuseppina Barutello, Maddalena Arigoni, Selina Iussich, Elena Lardone, Emanuela Morello, Soldano Ferrone, Paolo Buracco, Federica Cavallo

Oral Presentation at 77Th Sisvet Conference, 12-14 June 2024. Refining the TNM staging system for canine oral Malignant Melanoma: A novel approach for primary tumour escription and the role of lymphadenectomy Giacobino, S. Rizzo, M. Olimpo, E. Ferraris, P. Buracco, L. Parisi, E. Morello.

Last update: 12/02/2025 12:31

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