Publications by authors named "Cesare Piazza"

151 Publications

Gene Expression Profiling of Olfactory Neuroblastoma Helps Identify Prognostic Pathways and Define Potentially Therapeutic Targets.

Cancers (Basel) 2021 May 21;13(11). Epub 2021 May 21.

Medical Oncology Unit, Department of Medical and Surgical Specialties, Radiological Sciences and Public Health, ASST Spedali Civili of Brescia, University of Brescia, 25123 Brescia, Italy.

Olfactory neuroblastoma (ONB) is a rare sinonasal neoplasm with a peculiar behavior, for which limited prognostic factors are available. Herein, we investigate the transcriptional pathways altered in ONB and correlate them with pathological features and clinical outcomes. We analyze 32 ONB patients treated with curative intent at two independent institutions from 2001 to 2019 for whom there is available pathologic and clinical data. We perform gene expression profiling on primary ONB samples and carry out functional enrichment analysis to investigate the key pathways associated with disease-free survival (DFS). The median age is 53.5 years; all patients undergo surgery and a pure endoscopic approach is adopted in the majority of cases (81.2%). Most patients have advanced disease (stages III-IV, 81.2%) and 84.4% undergo adjuvant (chemo)radiotherapy. The median follow-up is 35 months; 11 (26.8%) patients relapse. Clinical characteristics (gender, stage and Hyams' grade) are not associated with the outcomes. In contrast, TGF-beta binding, EMT, IFN-alpha response, angiogenesis, IL2-STAT5 and IL6-JAK-STAT3 signaling pathways are enriched in patients experiencing recurrence, and significantly associated with shorter DFS. Clustering of transcriptional profiles according to pathological features indicates two distinct molecular groups, defined by either cytokeratin-positive or -negative immunostaining. Definition of the characterizing ONB transcriptomic pathways may pave the way towards tailored treatment approaches.
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http://dx.doi.org/10.3390/cancers13112527DOI Listing
May 2021

Salvage surgery for residual or recurrent laryngeal squamous cell carcinoma after (Chemo)radiotherapy: Oncological outcomes and prognostic factors.

Eur J Surg Oncol 2021 May 26. Epub 2021 May 26.

Coordinator of the International Head and Neck Scientific Group, Padua, Italy.

Nonsurgical primary treatment of early and advanced laryngeal squamous cell carcinoma, employing radiotherapy with or without chemotherapy, is considered a standard of care in many centers throughout the world. When patients have persistent or recurrent disease after non-surgical treatment, salvage surgery is frequently the only remaining potentially curative treatment. Depending on the extent of the residual/recurrent disease, different surgical salvage options are at the surgeon's disposal. In selected cases with limited local disease, salvage transoral laser microsurgery, transoral robotic surgery and open partial laryngectomies can be employed to achieve cure while preserving laryngeal function. For more advanced cases total laryngectomy is necessary. Identifying situations with unacceptable results from surgical salvage may guide future therapies.
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http://dx.doi.org/10.1016/j.ejso.2021.05.035DOI Listing
May 2021

Endoscopic Subtemporal Epidural Key-Hole Approach: Quantitative Anatomical Analysis of Three Surgical Corridors.

World Neurosurg 2021 May 22. Epub 2021 May 22.

Unit of Neurosurgery, University of Brescia, Department of Medical and Surgical Specialties, Radiologic Sciences, and Public Health; University of Brescia, Brescia, Italy.

Background: The endoscope-assisted subtemporal key-hole epidural approach (ESKEA) has been recently described. The aim of this study was to measure working volumes and exposure of key areas of the middle cranial fossa (MCF) provided by this approach.

Methods: Four fresh frozen cadaver heads were dissected to analyze 3 modular corridors (1A, 1B, and 2) harvested through ESKEA. A step-by-step dissection was performed, and key anatomical landmarks were recorded. GTxEyesII-ApproachViewer was used to quantify the working volume and exposure of 4 different regions (spheno-orbital, parasellar, superior petrous apex, and squamo-petrous). For each corridor, 3 incremental degrees of temporal dural retraction (5, 10, and 15 mm) were tested.

Results: The working volume of all corridors progressively increased with degree of retraction: corridors 1A, 1B, and 2 showed a gain in working volume of 21%, 27%, and 19% from 5 mm to 10 mm retraction, respectively, and a gain of 40%, 45%, and 44% from 5 mm to 15 mm retraction, respectively. The spheno-orbital area was exposed (27-45%) through corridor 1A and exposure significantly increased with the degree of retraction. Corridor 1B provided optimal exposure of parasellar areas (86-100%) and superior petrous apex (70-87%) regardless of the degree of retraction. The squamo-petrous area was satisfactorily addressed through corridor 2 (88%) only with the highest degree of retraction.

Conclusions: ESKEA can be conceived as a modular approach: the three surgical corridors have specific working volumes, which are clearly influenced by the degree of temporal lobe retraction, and provide exposure of different MCF areas.
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http://dx.doi.org/10.1016/j.wneu.2021.05.055DOI Listing
May 2021

Immunotherapy for the prevention of high-risk oral disorders malignant transformation: the IMPEDE trial.

BMC Cancer 2021 May 17;21(1):561. Epub 2021 May 17.

Medical Oncology Unit, Department of Medical and Surgical Specialities, Radiological Sciences and Public Health University of Brescia, ASST-Spedali Civili, Piazzale Spedali Civili 1, 25123, Brescia, Italy.

Background: Oral Potentially Malignant Disorders (OPMD) have a non-negligible malignant transformation rate of up to 8%. Loss of heterozygosity (LOH) in critical chromosomal loci has proven to be the most effective marker in defining the risk of transformation and it is found in about 28% of OPMD and may therefore identify patients carrying higher risk. To date, clinical management of OPMD is limited to surgical excision and clinical surveillance, which however do not fully prevent oral cancer development. Immune system has been shown to play a key role in transformation surveillance mechanism and an immunosuppressive imbalance may be responsible for progression to cancer. Given all these considerations, we designed a clinical trial with the aim to prevent OPMD neoplastic transformation and revert the LOH status.

Methods: This is a phase II, open label, single arm, multicentric trial involving Italian referral centres and expected to enrol 80 patients out of a total of 175 screened. Patients who meet all inclusion criteria and test positive for LOH after an incisional biopsy of the OPMD will undergo a short course of immunotherapy with 4 administration of avelumab. After 6 months since treatment start, resection of the entire OPMD will be performed and LOH assessment will be repeated. The follow-up for malignant transformation and safety assessment will last 30 months from the end of treatment, for a total planned study duration of approximately 5.5 years.

Discussion: Restoring the activity of immune system through checkpoint inhibitor may play a crucial role against malignant transformation of OPMD by reverting the balance in favour of immune control and preventing cancer occurrence.

Trial Registration: This trial was prospectively registered in ClinicalTrials.gov as NCT04504552 on 7th August 2020.
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http://dx.doi.org/10.1186/s12885-021-08297-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8130439PMC
May 2021

Step-by-Step Cadaver Dissection and Surgical Technique for Compartmental Tongue and Floor of Mouth Resection.

Front Oncol 2021 23;11:613945. Epub 2021 Apr 23.

Department of Otorhinolaryngology - Head and Neck Surgery, "San Maurizio" Hospital, Bolzano, Italy.

Background: The aim of oral cancer surgery is tumor removal within clear margins of healthy tissue: the latter definition in the literature, however, may vary between 1 and 2 cm, and should be intended in the three dimensions, which further complicates its precise measurement. Moreover, the biological behavior of tongue and floor of mouth cancer can be unpredictable and often eludes the previously mentioned safe surgical margins concept due to the complexity of tongue anatomy, the intricated arrangements of its intrinsic and extrinsic muscle fibers, and the presence of rich neurovascular and lymphatic networks within it. These structures may act as specific pathways of loco-regional tumor spread, allowing the neoplasm to escape beyond its visible macroscopic boundaries. Based on this concept, in the past two decades, compartmental surgery (CS) for treatment of oral tongue and floor of mouth cancer was proposed as an alternative to more traditional transoral resections.

Methods: The authors performed three anatomical dissections on fresh-frozen cadaver heads that were injected with red and blue-stained silicon. All procedures were documented by photographs taken with a professional reflex digital camera.

Results: One of these step-by-step cadaver dissections is herein reported, detailing the pivotal points of CS with the aim to share this procedure at benefit of the youngest surgeons.

Conclusions: We herein present the CS step-by-step technique to highlight its potential in improving loco-regional control by checking all possible routes of tumor spread. Correct identification of the anatomical space between tumor and nodes (T-N tract), spatial relationships of extrinsic tongue muscles, as well as neurovascular bundles of the floor of mouth, are depicted to improve knowledge of this complex anatomical area.
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http://dx.doi.org/10.3389/fonc.2021.613945DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8104033PMC
April 2021

Metrics of pN-staging in oral squamous cell carcinoma: An analysis of 1,905 patients.

Eur J Cancer 2021 Jun 19;150:33-41. Epub 2021 Apr 19.

Department of Otorhinolaryngology, Region Hospital West Jutland, Holstebro, Denmark; Department of Clinical Medicine, Aarhus University, Aarhus C, Denmark.

Background: We aimed to compare the predictive performance of pN-categories in oral squamous cell carcinoma (OSCC) encompassing the most recent 8th edition (TNM8), its predecessor (TNM7), and a newly proposed algorithm (pN-N), which classifies patients according to the number of positive lymph nodes and extranodal extension.

Methods: Consecutive, primary OSCC patients from seven previously published cohorts were included and classified according to the three pN-classifications: TNM7, TNM8 and pN-N. Overall survival probabilities were summarised with the Kaplan-Meier method. We added each of the three metrics to a Cox regression adjusted for pT-category, lymph nodal yield, age, sex, radiotherapy and chemotherapy, and trained these models in one institution. We evaluated the predictive performance in the remaining six institutions and assessed the predicted 5-year risk of death using the area under the receiver operating characteristics curve (AUC) and Brier scores.

Results: All 1,905 included patients were classified according to TNM7 and pN-N. A subset of 1,575 patients was additionally classified according to TNM8, leading to upstaging in 27.0%. The pN-N ranked overall best determined by the obtained AUC and Brier scores. In contrast to pN-N, TNM7 and TNM8 both suffered from disproportionate patient distribution across pN-categories and poor pN-categorial discrimination on overall survival.

Conclusions: The TNM8 pN-classification designates a larger subset to more advanced disease stages but failed to show improvement of its predictive performance compared to TNM7. The pN-categories of TNM7/8 are disproportionate and inconsistently discriminated. The pN-N conveyed the best measures of prognosis and should be considered in future TNM iterations.
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http://dx.doi.org/10.1016/j.ejca.2021.03.019DOI Listing
June 2021

Deep Learning for Automatic Segmentation of Oral and Oropharyngeal Cancer Using Narrow Band Imaging: Preliminary Experience in a Clinical Perspective.

Front Oncol 2021 24;11:626602. Epub 2021 Mar 24.

Department of Advanced Robotics, Istituto Italiano di Tecnologia, Genoa, Italy.

Introduction: Fully convoluted neural networks (FCNN) applied to video-analysis are of particular interest in the field of head and neck oncology, given that endoscopic examination is a crucial step in diagnosis, staging, and follow-up of patients affected by upper aero-digestive tract cancers. The aim of this study was to test FCNN-based methods for semantic segmentation of squamous cell carcinoma (SCC) of the oral cavity (OC) and oropharynx (OP).

Materials And Methods: Two datasets were retrieved from the institutional registry of a tertiary academic hospital analyzing 34 and 45 NBI endoscopic videos of OC and OP lesions, respectively. The dataset referring to the OC was composed of 110 frames, while 116 frames composed the OP dataset. Three FCNNs (U-Net, U-Net 3, and ResNet) were investigated to segment the neoplastic images. FCNNs performance was evaluated for each tested network and compared to the gold standard, represented by the manual annotation performed by expert clinicians.

Results: For FCNN-based segmentation of the OC dataset, the best results in terms of Dice Similarity Coefficient (Dsc) were achieved by ResNet with 5(×2) blocks and 16 filters, with a median value of 0.6559. In FCNN-based segmentation for the OP dataset, the best results in terms of Dsc were achieved by ResNet with 4(×2) blocks and 16 filters, with a median value of 0.7603. All tested FCNNs presented very high values of variance, leading to very low values of minima for all metrics evaluated.

Conclusions: FCNNs have promising potential in the analysis and segmentation of OC and OP video-endoscopic images. All tested FCNN architectures demonstrated satisfying outcomes in terms of diagnostic accuracy. The inference time of the processing networks were particularly short, ranging between 14 and 115 ms, thus showing the possibility for real-time application.
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http://dx.doi.org/10.3389/fonc.2021.626602DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8024583PMC
March 2021

Endoscopic-assisted multi-portal compartmental resection of the masticatory space in oral cancer: Anatomical study and preliminary clinical experience.

Oral Oncol 2021 Jun 4;117:105269. Epub 2021 Apr 4.

Unit of Otorhinolaryngology, "San Maurizio" Hospital of Bolzano, Bolzano, Italy.

Objectives: To present an anatomical cadaver dissection study and our preliminary surgical experience with endoscopic-assisted multi-portal compartmental resection of the masticatory space (MS) in locally advanced oral squamous cell carcinoma (OSCC) of the retromolar area.

Materials And Methods: Two fresh-frozen cadaver heads were dissected in the Laboratory of Anatomy to define the surgical steps of an endoscopic-assisted multi-portal compartmental approach to the MS. After this preclinical anatomical study, patients affected by locally advanced OSCC originating from the retromolar area with extension to the MS were prospectively enrolled and operated at two Italian referral centers for head and neck cancer between October 2019 and May 2020.

Results: Surgical technique of endoscopic-assisted multi-portal compartmental resection of the MS was preclinically defined step by step in 3 phases: transnasal, transoral/trancervical, and multi-portal. Compartmental resection of the MS was successfully completed in all specimens (4 MSs dissected). The surgical technique was subsequently applied in 3 patients affected by primary OSCC of the retromolar area, providing satisfactory results in terms of negative resection margins and local control.

Conclusions: Multi-portal compartmental resection of the MS combining the transnasal and transoral/transcervical corridors is technically feasible. Such an approach to the MS in locally advanced OSCC provides different angles of incidence to the target and full control of tumor margins.
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http://dx.doi.org/10.1016/j.oraloncology.2021.105269DOI Listing
June 2021

Clinical and histopathological risk factors for distant metastasis in head and neck cancer patients.

Acta Otorhinolaryngol Ital 2021 Feb;41(1):6-17

Department of Otorhinolaryngology, Maxillofacial and Thyroid Surgery, Fondazione IRCCS, National Cancer Institute of Milan, University of Milan, Milan, Italy.

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http://dx.doi.org/10.14639/0392-100X-N0879DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7982761PMC
February 2021

Validation of the European Laryngological Society classification of glottic vascular changes as seen by narrow band imaging in the optical biopsy setting.

Eur Arch Otorhinolaryngol 2021 Jul 12;278(7):2397-2409. Epub 2021 Mar 12.

IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Purpose: In 2016, the European Laryngological Society (ELS) proposed a classification for vascular changes occurring in glottic lesions as visible by narrow band imaging (NBI), based on the dichotomic distinction between longitudinal vessels (not suspicious) and perpendicular ones (suspicious). The aim of our study was to validate this classification assessing the interobserver agreement and diagnostic test performance in detecting the final histopathology.

Methods: A retrospective study was carried out by reviewing clinical charts, preoperative videos, and final pathologic diagnosis of patients submitted to transoral microsurgery for laryngeal lesions in two Italian referral centers. In each institution, two physicians, independently re-assessed each case applying the ELS classification.

Results: The cohort was composed of 707 patients. The pathologic report showed benign lesions in 208 (29.5%) cases, papillomatosis in 34 (4.8%), squamous intraepithelial neoplasia (SIN) up to carcinoma in situ in 200 (28.2%), and squamous cell carcinoma (SCC) in 265 (37.5%). The interobserver agreement was extremely high in both institutions (k = 0.954, p < 0.001 and k = 0.880, p < 0.001). Considering the diagnostic performance for identification of at least SIN or SCC, the sensitivity was 0.804 and 0.902, the specificity 0.793 and 0.581, the positive predictive value 0.882 and 0.564, and the negative predictive value 0.678 and 0.908, respectively.

Conclusion: The ELS classification for NBI vascular changes of glottic lesions is a highly reliable tool whose systematic use allows a better diagnostic evaluation of suspicious laryngeal lesions, reliably distinguishing benign ones from those with a diagnosis of papillomatosis, SIN or SCC, thus paving the way towards confirmation of the optical biopsy concept.
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http://dx.doi.org/10.1007/s00405-021-06723-7DOI Listing
July 2021

Evidence and controversies in management of thyroglossal duct cyst carcinoma.

Curr Opin Otolaryngol Head Neck Surg 2021 Apr;29(2):113-119

Department of Otorhinolaryngology - Head and Neck Surgery, ASST Spedali Civili of Brescia.

Purpose Of Review: The aim of this study was to analyse the rational of the possible therapeutic approaches to thyroglossal duct cyst carcinomas (TGDCCa), especially in consideration of their potential airway involvement, discussing the most debated issues concerning employment of thyroidectomy, neck dissection and adjuvant treatments.

Recent Findings: The literature is unanimous in defining the Sistrunk procedure as the baseline of surgical treatment of TGDCCa, and in equating the vast majority of thyroid-like TGDCCas to classic thyroid cancers from a biological point of view, while the rarer squamous cell carcinomas seem to behave more aggressively. Thyroidectomy, neck dissection and radioactive iodine treatment are considered for high-risk lesions, with the addition of customized partial resection of laryngeal cartilages when airway involvement is encountered. Furthermore, the analysis of thyroid mutational markers has promise for accurate prevision of more aggressive clinical behaviours.

Summary: Even if rare, clinicians should be aware of TGDCCa due to the possibility of incidental diagnosis and, in the case of more advanced clinical scenarios, for its potential airway involvement. Sistrunk procedure combined with thyroidectomy, neck dissection and adjuvant therapy provide excellent results in high-risk patients. Additional study of pathological thyroid markers in TGDCCa is desirable to allow more individualized treatments.
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http://dx.doi.org/10.1097/MOO.0000000000000699DOI Listing
April 2021

Open partial horizontal laryngectomy and adjuvant (chemo)radiotherapy for laryngeal squamous cell carcinoma: results from a multicenter Italian experience.

Eur Arch Otorhinolaryngol 2021 Feb 18. Epub 2021 Feb 18.

Otolaryngology Service, Vittorio Veneto Hospital, Vittorio Veneto (TV), Italy.

Purpose: To evaluate the functional and oncologic outcomes of adjuvant (chemo)radiation [(C)RT] after open partial horizontal laryngectomies (OPHLs).

Methods: Multicenter retrospective evaluation of 130 patients (116 males, 14 females) submitted between 1995 and 2017 to OPHL Types II and III for laryngeal cancer and receiving adjuvant (C)RT for one or more of the following risk factors at histopathologic examination of the surgical specimen: pT4a and/or > pN2a categories, close/positive resection margins, or presence of both perineural (PNI) and lympho-vascular invasion (LVI). The primary study endpoints were evaluation of the presence of tracheostomy and/or gastrostomy at last follow-up, and calculation of laryngo-esophageal dysfunction-free survival (LEDFS).

Results: Mean age of the study cohort was 60.8 ± 8.9 years (median, 62; interquartile range [IQR], 13). Mean follow-up was 50.7 ± 39.4 months (range 24-188; median, 38; IQR, 51). Adjuvant therapy consisted of CRT in 53 (41%) patients, and RT alone in 77 (59%). Five-year LEDFS was 85%. Overall survival was 71.5%, while 13% of patients remained tracheostomy- and 3% gastrostomy-dependent at the last follow-up. The only significant variable in predicting survival (p = 0.020) was tracheostomy dependence: it was maintained in 7.5% of subjects after OPHL Type II and in 34% of those submitted to OHPL Type III (p < 0.001).

Conclusions: In selected patients affected by advanced laryngeal cancer, OPHLs Type II and III have a relatively good laryngeal safety profile and provide favorable oncologic outcomes even in case of need for adjuvant (C)RT.
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http://dx.doi.org/10.1007/s00405-021-06651-6DOI Listing
February 2021

Videomics: bringing deep learning to diagnostic endoscopy.

Curr Opin Otolaryngol Head Neck Surg 2021 Apr;29(2):143-148

Unit of Otorhinolaryngology - Head and Neck Surgery, ASST Spedali Civili of Brescia, Department of Medical and Surgical Specialties, Radiological Sciences, and Public Health, University of Brescia, Brescia, Italy.

Purpose Of Review: Machine learning (ML) algorithms have augmented human judgment in various fields of clinical medicine. However, little progress has been made in applying these tools to video-endoscopy. We reviewed the field of video-analysis (herein termed 'Videomics' for the first time) as applied to diagnostic endoscopy, assessing its preliminary findings, potential, as well as limitations, and consider future developments.

Recent Findings: ML has been applied to diagnostic endoscopy with different aims: blind-spot detection, automatic quality control, lesion detection, classification, and characterization. The early experience in gastrointestinal endoscopy has recently been expanded to the upper aerodigestive tract, demonstrating promising results in both clinical fields. From top to bottom, multispectral imaging (such as Narrow Band Imaging) appeared to provide significant information drawn from endoscopic images.

Summary: Videomics is an emerging discipline that has the potential to significantly improve human detection and characterization of clinically significant lesions during endoscopy across medical and surgical disciplines. Research teams should focus on the standardization of data collection, identification of common targets, and optimal reporting. With such a collaborative stepwise approach, Videomics is likely to soon augment clinical endoscopy, significantly impacting cancer patient outcomes.
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http://dx.doi.org/10.1097/MOO.0000000000000697DOI Listing
April 2021

Long-term Olfactory and Gustatory Dysfunction May Be Related to Neural Damage.

Otolaryngol Head Neck Surg 2021 Feb 9:194599821994845. Epub 2021 Feb 9.

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http://dx.doi.org/10.1177/0194599821994845DOI Listing
February 2021

Predictive nomograms for oral tongue squamous cell carcinoma applying the American Joint Committee on Cancer/Union Internationale Contre le Cancer 8th edition staging system.

Head Neck 2021 Apr 2;43(4):1043-1055. Epub 2021 Feb 2.

Department of Head and Neck Oncology, Amrita Institute of Medical Sciences, Amrita Vishwa Vidyapeetham, Kochi, India.

Background: Nomograms applying the 8th edition of the TNM staging system aimed at predicting overall (OS), disease-specific (DSS), locoregional recurrence-free (LRRFS) and distant recurrence-free survivals (DRFS) for oral tongue squamous cell carcinoma (OTSCC) are still lacking.

Methods: A training cohort of 438 patients with OTSCC was retrospectively enrolled from a single institution. An external validation set of 287 patients was retrieved from two independent institutions.

Results: Internal validation of the multivariable models for OS, DSS, DRFS and LRRFS showed a good calibration and discrimination results with optimism-corrected c-indices of 0.74, 0.75, 0.77 and 0.70, respectively. The external validation confirmed the good performance of OS, DSS and DRFS models (c-index 0.73 and 0.77, and 0.73, respectively) and a fair performance of the LRRFS model (c-index 0.58).

Conclusions: The nomograms herein presented can be implemented as useful tools for prediction of OS, DSS, DRFS and LRRFS in OTSCC.
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http://dx.doi.org/10.1002/hed.26554DOI Listing
April 2021

Genome-wide study of salivary miRNAs identifies miR-423-5p as promising diagnostic and prognostic biomarker in oral squamous cell carcinoma.

Theranostics 2021 1;11(6):2987-2999. Epub 2021 Jan 1.

'Angelo Nocivelli' Institute of Molecular Medicine, University of Brescia and ASST Spedali Civili di Brescia, Brescia, Italy.

Survival rates of oral squamous cell carcinoma (OSCC) remained substantially unchanged over the last decades; thus, additional prognostic tools are strongly needed. Salivary miRNAs have emerged as excellent non-invasive cancer biomarker candidates, but their association with OSCC prognosis has not been investigated yet. In this study, we analyzed global salivary miRNA expression in OSCC patients and healthy controls, with the aim to define its diagnostic and prognostic potential. Saliva was collected from patients with newly diagnosed untreated primary OSCC and healthy controls. Global profiling of salivary miRNAs was carried out through a microarray approach, while signature validation was performed by quantitative real-time PCR (RT-qPCR). A stringent statistical approach for microarray and RT-qPCR data normalization was applied. The diagnostic performance of miRNAs and their correlation with OSCC prognosis were comprehensively analyzed. In total, 25 miRNAs emerged as differentially expressed between OSCC patients and healthy controls and, among them, seven were significantly associated with disease-free survival (DFS). miR-106b-5p, miR-423-5p and miR-193b-3p were expressed at high levels in saliva of OSCC patients and their combination displays the best diagnostic performance (ROC - AUC = 0.98). Moreover, high expression of miR-423-5p was an independent predictor of poor DFS, when included in multivariate survival analysis with the number of positive lymph nodes - the only significant clinical prognosticator. Finally, we observed a significant decrease in miR-423-5p expression in matched post-operative saliva samples, suggesting its potential cancer-specific origin. Salivary miRNAs identified in our cohort of patients show to be accurate in OSCC detection and to effectively stratify patients according to their likelihood of relapse. These results, if validated in an independent set of patients, could be particularly promising for screening/follow-up of high-risk populations and useful for preoperative prognostic assessment.
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http://dx.doi.org/10.7150/thno.45157DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7806472PMC
January 2021

Long-term Oncologic Outcomes of 1188 Tis-T2 Glottic Cancers Treated by Transoral Laser Microsurgery.

Otolaryngol Head Neck Surg 2021 Jan 5:194599820983727. Epub 2021 Jan 5.

Department of Otorhinolaryngology-Head and Neck Surgery, University of Genoa, IRCCS Ospedale Policlinico San Martino, Genoa, Italy.

Objective: To evaluate long-term disease-specific survival (DSS) and organ preservation (OP) rates in patients affected by Tis-T2 glottic squamous cell carcinoma (SCC) treated by carbon dioxide transoral laser microsurgery (CO TOLMS).

Study Design: Single-center retrospective cohort study.

Setting: Tertiary academic hospital.

Methods: The study included patients treated by CO TOLMS for Tis-T2 glottic SCC at the Department of Otorhinolaryngology-Head and Neck Surgery of the University of Brescia, Italy, from 1988 to 2018. The male:female ratio was 11.2:1, and the mean age was 64 years (range, 31-95). T categories were distributed as follows: 124 (10%) Tis, 646 (54%) T1a, 172 (15%) T1b, and 246 (21%) T2.

Results: Ten- and 20-year DSS rates were 97.6% and 96.3%, respectively, and 10- and 20-year OP rates were 94.7% and 93%. During the follow-up, 91% of patients were treated by CO TOLMS alone, while the remaining needed adjunctive treatments. Assessing the impact of multiple sessions of CO TOLMS, DSS showed no significant difference in terms of patients treated by 1, 2, or >2 procedures. Conversely, patients treated by >2 sessions of CO TOLMS showed a significantly worse OP rate.

Conclusions: Our series validates CO TOLMS as a long-term treatment strategy for early glottic SCC. Salvage CO TOLMS provided optimal results in terms of DSS and OP in patients with recurrence after previous transoral surgery.
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http://dx.doi.org/10.1177/0194599820983727DOI Listing
January 2021

A roadmap of six different pathways to improve survival in laryngeal cancer patients.

Curr Opin Otolaryngol Head Neck Surg 2021 Apr;29(2):65-78

Department of Otorhinolaryngology - Head and Neck Surgery, ASST Spedali Civili of Brescia, Department of Medical and Surgical Specialties, University of Brescia, Brescia, Italy.

Purpose Of Review: Laryngeal cancer continues to require improvement in earlier stage diagnosis and better imaging delineation of disease, and hence 'more evidence-based' selection of treatment, as recent evidence suggests that related mortality, in the last decades, has not significantly decreased worldwide. Even though the reasons are not fully understood, there persists an urgency for a review and development of future strategies to embrace such clinical and diagnostic challenges from a political, societal, as well as scientific and clinical points of view.

Recent Findings: This review of the published literature suggests that survival improvement in laryngeal cancer may be achieved by fuelling and combining at least some or all of six targeted agendas: documentation of disease global incidence and national burden monitoring; development and implementation of high-quality cancer registries; education on risk factors and hazardous habits associated with laryngeal cancer for the general population; active modification of proven at-risk population lifestyles; centralization of treatment; and use of machine learning of gathered 'big data' and their integration into approaches for the optimization of prevention and treatments strategies.

Summary: Laryngeal cancer should be tackled on several fronts, commencing with disease monitoring and prevention, up to treatment optimisation. Available modern resources offer the possibility to generate significant advances in laryngeal cancer management. However, each nation needs to develop a comprehensive approach, which is an essential prerequisite to obtain meaningful improvement on results.
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http://dx.doi.org/10.1097/MOO.0000000000000684DOI Listing
April 2021

Multidisciplinary Management of Radiation-Induced Salivary Gland Carcinomas in the Modern Radiotherapy Era.

Cancers (Basel) 2020 Dec 14;12(12). Epub 2020 Dec 14.

Radiotherapy Unit, National Center of Oncological Hadrontherapy (CNAO), 27100 Pavia, Italy.

Clinical data of ri-SGCs patients treated between 2015 and 2019 at a tertiary cancer center and a national hadron therapy facility were reviewed. Latent time (LT) from first RT to ri-SGCs diagnosis, overall (OS), and disease-free survival (DFS) were assessed. Thirteen patients developed 14 ri-SGCs (one patient had 2 synchronous ri-SCGs), after a median LT of 23 years (range 16-34). Parotid was the primary site in 8 cases (57%) and salivary duct carcinoma was the most frequent histotype (29%). Nine patients (69%) underwent surgery (Sx). Among them, 4 patients (31%) underwent Sx alone, 5 received post-operative treatments: 3 (23%) photon-based (X) reRT, one (8%) protons and carbon ions, one (8%) carbon ions only. One patient (8%) received definitive XRT. The remaining 3 patients (23%) received androgen deprivation therapy. With a median follow-up of 48 months (range 24-72), median OS and PFS were 74 and 24 months, respectively. In the subgroup of AR ri-SGCs, median PFS and OS were 12 and 74 months, respectively. Given the rarity of ri-SGCs, this work adds further knowledge to the paucity of literature. The management of these malignancies is extremely complex requiring a multidisciplinary treatment approach.
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http://dx.doi.org/10.3390/cancers12123769DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7765068PMC
December 2020

Metastatic Squamous Cell Carcinoma to the Cervical Lymph Nodes From an Unknown Primary Cancer: Management in the HPV Era.

Front Oncol 2020 10;10:593164. Epub 2020 Nov 10.

International Head and Neck Scientific Group, Padua, Italy.

Background: Patients with metastases in the lymph nodes of the neck and no obvious primary tumor, neck cancer with unknown primary (NCUP), represent a management challenge. A majority of patients have metastatic squamous cell carcinoma (SCC), although other histologies do occur.

Methods: We comprehensively reviewed the literature, compared available guidelines, and conferred with an international team of experts.

Results: Positron emission tomography-computed tomography (PET-CT) and fine needle aspiration (FNA) under ultrasound guidance increase accuracy of diagnosis. Immunohistochemistry (IHC), determination of human papilloma virus (HPV) status, by p16 staining or by hybridization (ISH), and next-generation gene sequencing can guide us regarding probable primary sites and tumor biology. Narrow Band Imaging (NBI) has been introduced for the early detection of subtle mucosal lesions. Direct laryngoscopy (DL) and tonsillectomy have long been procedures used in the search for a primary site. More recently, TransOral Robotic Surgery (TORS) or Transoral LASER Microsurgery (TLM) have been introduced for lingual tonsillectomy.

Conclusions: New technologies have been developed which can better detect, diagnose, and treat occult primary tumors. Decisions regarding therapy are based on the primary tumor site (if discovered) and N stage. Options include neck dissection with or without postoperative adjuvant therapy, primary irradiation, or combined chemotherapy with irradiation. The preferred treatment of patients whose primary remains unidentified is controversial.
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http://dx.doi.org/10.3389/fonc.2020.593164DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7685177PMC
November 2020

Radiation-Induced Sarcomas of the Head and Neck: A Systematic Review.

Adv Ther 2021 01 13;38(1):90-108. Epub 2020 Nov 13.

Coordinator of the International Head and Neck Scientific Group, Padua, Italy.

Introduction: As a result of the increased use of radiotherapy (RT) and improved long-term overall survival of patients with cancers of the head and neck (HN), the frequency of radiation-induced sarcomas of the head and neck (RISHN) may be increasing. The main objective of this systematic review was to determine the existing evidence on the frequency, treatment, and outcome of RISHN.

Methods: Using PRISMA guidelines we conducted a systematic review of the literature published from 2000 to 2020.

Results: Our review includes data of 560 patients from 64 articles. The total frequency of RISHNs among the reviewed series was 0.15%. The most frequent location of the primary tumor treated by RT was the nasopharynx. The mean RT dose used was 62 Gy, mean latency interval between irradiation and occurrence of RISHN was 11.1 years, and the most common RISHN location was the sinonasal region. Osteosarcoma was the principal histology, followed by fibrosarcoma. Surgery was the most frequently applied treatment modality. Of all patients with RISHN, 40.7% died of this disease after a mean interval of 13.9 months.

Conclusions: Notwithstanding the increased use of RT, the number of reported RISHNs has not increased substantially during the past two decades. Surgery with wide margins forms the best therapeutic option for these cases, but the outcome remains poor.
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http://dx.doi.org/10.1007/s12325-020-01556-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7854400PMC
January 2021

Head and neck adult-type soft tissues sarcomas: survival analysis and comparison between the last two editions of the TNM staging system.

Eur Arch Otorhinolaryngol 2020 Nov 5. Epub 2020 Nov 5.

Department of Otorhinolaryngology, Maxillofacial and Thyroid Surgery, Fondazione IRCCS, National Cancer Institute of Milan, University of Milan, 20133, Milan, Italy.

Purpose: Head and neck soft tissues sarcomas (HNSTS) are a heterogeneous group of rare tumours. The 8th edition of the TNM staging system (8TNM) considered these lesions separately for the first time. The aim of this study is to assess its effectiveness and identify the most significant prognostic factors for HNSTS.

Methods: A retrospective survival analysis on 101 HNSTS operated between 1995 and 2015 at the National Cancer Institute of Milan was carried out. The variables considered were pathological stage (according to both the 7TNM and 8TNM), site, histotype, depth, grading, surgical radicality, (neo)adjuvant radiotherapy and/or chemotherapy.

Results: According to the 7TNM, the T category distribution was 35 T1a, 23 T1b, 11 T2a, and 32 T2b. Applying the 8TNM, the distribution changed to 19 T1, 18 T2, 35 T3, and 29 T4. Five-year overall and disease-specific survivals were 74.3 and 76.2%, respectively. Univariate analysis demonstrated an increased hazard ratio (HR) for deep lesions invading adjacent structures, high-grade, surgery with close/microscopically positive margins, and chemotherapy. Multivariate analysis confirmed an increased HR for deep location and size > 5 cm, G2-G3 tumours, and marginal surgery. No significant difference was found among T categories of the 8TNM.

Conclusion: The present study underlines the negative prognostic impact of depth, size > 5 cm, high grade, and marginal treatment for HNSTS. Our results did not allow to validate the 8TNM staging system since, apparently, it was not associated with meaningful prognostic stratification. Further studies with wider multicentric cohorts should, however, be performed to obtain more powerful statistical data.
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http://dx.doi.org/10.1007/s00405-020-06452-3DOI Listing
November 2020

COVID-19 screening protocols for preoperative assessment of head and neck cancer patients candidate for elective surgery in the midst of the pandemic: A narrative review with comparison between two Italian institutions.

Oral Oncol 2021 01 14;112:105043. Epub 2020 Oct 14.

Section of Otorhinolaryngology-Head and Neck Surgery, Azienda Ospedaliera di Padova, University of Padua, Padua, Italy.

Background: Preoperative screening had a key role in planning elective surgical activity for head and neck cancer (HNC) during the COVID-19 pandemic.

Methods: All patients undergoing surgery for HNC at two Italian referral hospitals (University of Padua and National Cancer Institute [NCI]) during the peak of the COVID-19 epidemic in Italy were included. Accuracy of screening protocols was assessed.

Results: In the Padua protocol, 41 patients were screened by pharyngeal swab. The entire sample (100%) was admitted to surgery, diagnostic accuracy was 100%. In the NCI protocol, 23 patients underwent a telephone interview, blood test, and chest CT. Twenty patients (87%) were negative and were directly admitted to surgery. In the remaining 3 (13%), pharyngeal swab was performed. The screening was repeated until a negative chest CT was found. Diagnostic accuracy was 85%.

Conclusions: Dedicated screening protocols for COVID-19 allow to safely perform elective HNC surgery.
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http://dx.doi.org/10.1016/j.oraloncology.2020.105043DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7556777PMC
January 2021

Intraoral ultrasonography in the assessment of DOI in oral cavity squamous cell carcinoma: a comparison with magnetic resonance and histopathology.

Eur Arch Otorhinolaryngol 2020 Oct 21. Epub 2020 Oct 21.

IRCCS Policlinico San Martino, Largo Rosanna Benzi, 10, 16132, Genoa, Italy.

Objective: The first-line therapeutic approach for oral cavity squamous cell carcinoma (OCSCC) is complete surgical resection. Preoperative assessment of depth of invasion (cDOI) is crucial to plan the surgery. Magnetic resonance (MR) and intraoral ultrasonography (IOUS) have been shown to be useful tools for assessment of DOI. The present analysis investigates the accuracy of MR and IOUS in evaluating DOI in OCSCC compared to histological evaluation (pDOI).

Materials And Methods: Forty-nine previously untreated patients with cT1-T3 OCSCC were reviewed. Nine patients were staged with MR alone, 10 with IOUS alone, and 30 with both MR and IOUS.

Results: Mean difference between cDOI and pDOI values of 0.2 mm (95% CI - 1.0-1.3 mm) and between cDOI and pDOI of 0.3 mm (95% CI - 1.0-1.6 mm). Spearman R between cDOI and pDOI was R = 0.83 and between cDOI and pDOI was R = 0.76. Both radiological techniques showed high performance for the correct identification, with the optimum cut-off of 5 mm, of patients with a pDOI ≥ 4 mm and amenable to a neck dissection, with an AUC of 0.92 and 0.82 for MR and IOUS, respectively.

Conclusion: Both examinations were valid approaches for preoperative determination of DOI in OCSCC, although with different cost-effectiveness profiles and indications.
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http://dx.doi.org/10.1007/s00405-020-06421-wDOI Listing
October 2020

Role of IMRT/VMAT-Based Dose and Volume Parameters in Predicting 5-Year Local Control and Survival in Nasopharyngeal Cancer Patients.

Front Oncol 2020 24;10:518110. Epub 2020 Sep 24.

Radiotherapy Unit 2, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, Milan, Italy.

This study aimed to look into the relationship between intensity-modulated-radiotherapy (IMRT)- or volumetric-modulated-arc-therapy (VMAT)-based dose-volume parameters and 5-year outcome for a consecutive series of non-metastatic nasopharyngeal cancer (NPC) patients (pts) treated in a single institution in a non-endemic area in order to identify potential prognostic factors. A retrospective analysis of consecutive non-metastatic NPC pts treated curatively with IMRT or VMAT and chemotherapy (CHT) between 2004 and 2014 was conducted. One patient was in stage I (0.7%), and 24 pts (17.5%) were in stage II, 38 pts (27.7%) in stage III, 29 pts (21.2%) in stage IVA, and 45 pts (32.8%) in stage IVB. Five pts (3.6%) received radiotherapy (RT) alone. Of the remaining 132 pts (96.4%), 30 pts (21.9%) received CHT concomitant to RT, and 102 pts (74.4%) were treated with induction CHT followed by RT-CHT. IMRT was given with standard fractionation at a total dose of 70 Gy. Clinical outcomes investigated in the study were local control (LC), disease-free survival (DFS), and overall survival (OS). Kaplan-Meier (KM) analysis was performed for the outcomes considering dose and coverage parameters, staging, and RT technique. Overall, 137 pts were eligible for this retrospective analysis. With a median follow-up of 70 months (range 12-143), actuarial rates at 5 years were LC 90.4, DFS 77.2, and OS 82.8%. For this preliminary study, T stage was dichotomized as T1, T2, T3 vs. T4. At 5 years, the group T1-T2-T3 reported an LC of 93%, a DFS of 79%, and an OS of 88%, whereas T4 pts reported LC, DFS, and OS, respectively, of 56, 50, and 78%. Pts with V95% > 95.5% had better LC ( = 0.006). Pts with D99% > 63.8 Gy had better LC ( = 0.034) and OS ( = 0.005). The threshold value of 43.2 cm of GTVT was prognostic for LC ( = 0.016). To predict the risk of local recurrence at 5 years, we constructed a nomogram which combined GTVT with D99% relative to HRPTV. We demonstrated the prognostic value of some dose-volume parameters, although in a retrospective series, this is potentially useful to improve planning procedure. In addition, for the first time in a non-endemic area, a threshold value of GTVT, prognostic for LC, has been confirmed.
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http://dx.doi.org/10.3389/fonc.2020.518110DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7541899PMC
September 2020

European Laryngological Society position paper on laryngeal dysplasia Part II: diagnosis, treatment, and follow-up.

Eur Arch Otorhinolaryngol 2021 Jun 14;278(6):1723-1732. Epub 2020 Oct 14.

Department of Otorhinolaryngology-Head and Neck Surgery, ASST Spedali Civili of Brescia, University of Brescia, Brescia, Italy.

Purpose Of Review: To give an overview of the current knowledge regarding the diagnosis, treatment, and follow-up of laryngeal dysplasia (LD) and to highlight the contributions of recent literature. The diagnosis of LD largely relies on endoscopic procedures and on histopathology. Diagnostic efficiency of endoscopy may be improved using videolaryngostroboscopy (VLS) and bioendoscopic tools such as Narrow Band Imaging (NBI) or Storz Professional Image Enhancement System (SPIES). Current histological classifications are not powerful enough to clearly predict the risk to carcinoma evolution and technical issues such as sampling error, variation in epithelial thickness and inflammation hamper pathological examination. Almost all dysplasia grading systems are effective in different ways. The 2017 World Health Organization (WHO) system should prove to be an improvement as it is slightly more reproducible and easier for the non-specialist pathologist to apply. To optimize treatment decisions, surgeons should know how their pathologist grades samples and preferably audit their transformation rates locally. Whether carcinoma in situ should be used as part of such classification remains contentious and pathologists should agree with their clinicians whether they find this additional grade useful in treatment decisions. Recently, different studies have defined the possible utility of different biomarkers in risk classification. The main treatment modality for LD is represented by transoral laser microsurgery. Radiotherapy may be indicated in specific circumstances such as multiple recurrence or wide-field lesions. Medical treatment currently does not have a significant role in the management of LD. Follow-up for patients treated with LD is a fundamental part of their care and investigations may be supported by the same techniques used during diagnosis (VLS and NBI/SPIES).
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http://dx.doi.org/10.1007/s00405-020-06406-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8131286PMC
June 2021

European Laryngological Society position paper on laryngeal dysplasia Part I: aetiology and pathological classification.

Eur Arch Otorhinolaryngol 2021 Jun 13;278(6):1717-1722. Epub 2020 Oct 13.

Department of Otorhinolaryngology- Head and Neck Surgery, ASST Spedali Civili of Brescia, University of Brescia, Brescia, Italy.

Purpose Of Review: To give an overview of the current knowledge regarding the aetiology, epidemiology, and classification of laryngeal dysplasia (LD) and to highlight the contributions of recent literature. As most cases of dysplasia occur at the glottic level and data on diagnosis and management are almost exclusively from this location, laryngeal dysplasia in this position paper is taken to be synonymous with dysplasia of the vocal folds. LD has long been recognized as a precursor lesion to laryngeal squamous cell carcinoma (SCC). Tobacco and alcohol consumption are the two single most important etiological factors for the development of LD. There is currently insufficient evidence to support a role of reflux. Although varying levels of human papillomavirus have been identified in LD, its causal role is still uncertain, and there are data suggesting that it may be limited. Dysplasia has a varying presentation including leukoplakia, erythroleukoplakia, mucosal reddening or thickening with exophytic, "tumor-like" alterations. About 50% of leukoplakic lesions will contain some form of dysplasia. It has become clear that the traditionally accepted molecular pathways to cancer, involving accumulated mutations in a specific order, do not apply to LD. Although the molecular nature of the progression of LD to SCC is still unclear, it can be concluded that the risk of malignant transformation does rise with increasing grade of dysplasia, but not predictably so. Consequently, grading systems are inherently troubled by the weak correlation between the degree of the dysplasia and the risk of malignant transformation. The best data on LD grading and outcomes come from the Ljubljana group, forming the basis for the World Health Organization classification published in 2017.
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http://dx.doi.org/10.1007/s00405-020-06403-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8131293PMC
June 2021

Emergent tracheostomy during the pandemic of COVID-19: Slovenian National Recommendations.

Eur Arch Otorhinolaryngol 2021 Jul 5;278(7):2209-2217. Epub 2020 Sep 5.

University Department of Otorhinolaryngology and Cervicofacial Surgery, University Medical Centre Ljubljana, Zaloška 2, 1000, Ljubljana, Slovenia.

Purpose: Emergent tracheostomy under local anaesthesia is a reliable method of airway management when orotracheal intubation is not possible. COVID-19 is spread through aerosol making the emergent tracheostomy a high-risk procedure for surgeons. The surgical establishment of the air conduit in emergency scenarios must be adjusted for safety reasons.

Methods: To establish the Slovenian National Guidelines for airway management in cannot intubate-cannot ventilate situations in COVID-19 positive patients.

Results: Good communication and coordination between surgeon and anaesthesiologist is absolutely necessary. Deep general anaesthesia, full muscle relaxation and adequate preoxygenation without intubation are initial steps. The surgical cricothyrotomy is performed quickly, the thin orotracheal tube is inserted, the cuff is inflated and ventilation begins. Following patient stabilisation, the conversion to the tracheostomy is undertaken with the following features: skin infiltration with vasoconstrictor, a vertical incision, avoidance of electrical devices in favour of classical manners of haemostasis, the advancement of the tube towards the carina, performing the tracheal window in complete apnoea following adequate oxygenation, the insertion of non-fenestrated canulla attached to a heat and moisture exchanger, the fixation of canulla with stitches and tapes, and the cricothyrotomy entrance closure. Appropriate safety equipment is equally important.

Conclusion: The goal of the guidelines is to make the procedure safer for medical teams, without harming the patients. Further improvements of the guidelines will surely appear as COVID-19 is a new entity and there is not yet much experience in handling it.
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http://dx.doi.org/10.1007/s00405-020-06318-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7473826PMC
July 2021

Laryngeal Compartmentalization Does Not Affect the Prognosis of T3-T4 Laryngeal Cancer Treated by Upfront Total Laryngectomy.

Cancers (Basel) 2020 Aug 11;12(8). Epub 2020 Aug 11.

IRCCS Ospedale Policlinico San Martino, 16132 Genoa, Italy.

A picture is emerging in which advanced laryngeal cancers (LCs) are potentially not homogeneous and may be characterized by subpopulations which, if identified, could allow selection of patients amenable to organ preservation treatments in contrast to those to be treated with total laryngectomy (TL). This work aims to analyze a multicentric cohort of T3-T4a LCs treated by upfront TL, investigating the clinical and pathological features that can best predict oncologic outcomes. A total of 149 previously untreated patients who underwent TL for T3-T4a LC at four institutions were analyzed. Survival and disease-control were considered as the main outcomes. A secondary end-point was the identification of covariates associated with nodal status, investigating also the tumor thickness. T and N categories were significantly associated with both overall and disease-specific survival. The number of positive nodes and tracheal involvement were associated with loco-regional failure; post-cricoid area invasion and extra-nodal extension with distant failure. Posterior laryngeal compartment involvement was not a significant prognostic feature, by either univariable and multivariable analyses. These results support the conclusion that laryngeal compartmentalization has no impact on survival in patients treated by upfront TL and the current TNM staging system remains a robust prognosticator in advanced LC.
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http://dx.doi.org/10.3390/cancers12082241DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7463701PMC
August 2020