Publications by authors named "Françoise Borson-Chazot"

158 Publications

Role of DNA repair variants and diagnostic radiology exams in differentiated thyroid cancer risk: a pooled-analysis of two case-control studies.

Cancer Epidemiol Biomarkers Prev 2021 Apr 7. Epub 2021 Apr 7.

UMR 1018, INSERM

Background: Given the increased use and diversity of diagnostic procedures, it is important to understand genetic susceptibility to radiation-induced thyroid cancer.

Methods: Based on self-declared diagnostic radiology examination records in addition to existing literature, we estimated the radiation dose delivered to the thyroid gland from diagnostic procedures during childhood and adulthood in two case-control studies conducted in France. A total of 1071 differentiated thyroid cancer (DTC) cases and 1188 controls from the combined studies were genotyped using a custom-made Illumina OncoArray DNA chip. We focused our analysis on variants in genes involved in DNA damage response and repair pathways, representing a total of 5817 single-nucleotide polymorphisms in 571 genes. We estimated the odds ratio per milli-Gray (OR/mGy) of the radiation dose delivered to the thyroid gland using conditional logistic regression. We then used an unconditional logistic regression model to assess the association between DNA repair gene variants and DTC risk. We performed a meta-analysis of the two studies.

Results: The OR/mGy was 1.02 (95% CI: 1.00, 1.03). We found significant associations between DTC and rs7164173 in CHD2 (p = 5.79 10-5), rs6067822 in NFATc2 (p = 9.26 10-5), rs1059394 and rs699517 both in ENOSF1/THYS, rs12702628 in RPA3, and an interaction between rs7068306 in MGMT and thyroid radiation doses (p= 3.40 10-4).

Conclusions: Our results suggest a role for variants in CDH2, NFATc2, ENOSF1/THYS, RPA3 and MGMT in DTC risk.

Impact: CDH2, NFATc2, ENOSF1/THYS and RPA3 have not previously been shown to be associated with DTC risk.
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http://dx.doi.org/10.1158/1055-9965.EPI-20-1142DOI Listing
April 2021

What Is the Quality of Life in Patients Treated with Levothyroxine for Hypothyroidism and How Are We Measuring It? A Critical, Narrative Review.

J Clin Med 2021 Mar 30;10(7). Epub 2021 Mar 30.

Service d'Endocrinologie, Maladies Métaboliques et Nutrition, Pôle Cardio-Vasculaire et Métabolique, Hôpital Larrey, CHU de Toulouse, 31059 Toulouse, France.

Thyroid hormone replacement therapy (THRT, generally using oral levothyroxine (LT4)) is a safe, effective means of treating hypothyroidism. However, a proportion of LT4-treated patients with biochemically normal thyroid function tests complain of persistent symptoms that impact their health-related quality of life (QoL). The objectives of this critical, narrative review of the literature were to identify studies of QoL in LT4-treated patients with hypothyroidism, examine the instruments used to measure QoL, determine whether normal QoL is restored by THRT, and identify factors associated with QoL. The PubMed database was searched from 1 January 2000 to 31 December 2020. A total of 809 publications were screened, 129 full-text articles were retrieved, and 58 were analyzed. The studies of overt hypothyroidism evidenced an improvement in psychological and emotional well-being after three to six months of THRT with LT4, although contrasting results were found for patients with subclinical hypothyroidism. Combination treatment with LT4 and liothyronine was not generally associated with better QoL. In hypothyroidism, QoL appears to be influenced by a number of physiological, behavioral, cognitive and/or lifestyle factors that are not strictly related to thyroid hormone levels.
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http://dx.doi.org/10.3390/jcm10071386DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8037475PMC
March 2021

Recurrence-free survival analysis in locally advanced pheochromocytoma: first appraisal.

J Clin Endocrinol Metab 2021 Mar 30. Epub 2021 Mar 30.

Endocrine oncology unit, Gustave Roussy, F-94805, Villejuif, France.

Context: Locally advanced pheochromocytoma (LAP) behavior remains unknown.

Objective: To characterize this population and its recurrence-free survival (RFS).

Design: A retrospective multicentric study run within the ENDOCAN-COMETE network and GTE from 2003 to 2018.

Setting: 11 French Referral centers.

Patients: Patients with LAP as defined by capsular invasion, vascular invasion, adipose tissue invasion and/or positive locoregional lymph nodes at diagnosis without evidence of distant metastasis.

Main Outcome Measures: Recurrence was defined as the reappearance of the tumor, including local site and/or distant metastasis. The primary endpoint was RFS analysis. The secondary endpoints were characterization, overall survival (OS) and prognostic factors of recurrence.

Results: Among 950 patients, 90 exhibited LAP criteria (9%). 55 met the inclusion criteria (median age: 53 years-old, 61% males, 14% with a germline mutation, 84% with a catecholamine excess). LAP was defined by 31 (56%) capsular invasions, 27 (49%) fat invasions, 6 (11%) positive lymph nodes and 22 (40%) vascular invasions. After a median follow-up of 54 months (range, 6-180), 12 patients (22%) had recurrences and 3 (5%) died of a metastatic disease. Median RFS was 115 months (range, 6-168). The recurrences were local in 2 patients, distant in 2 and both local and distant in 8 patients. Median OS of patients was not reached. Size above 6.5cm (p=0.019) and Ki-67>2% (p=0.028) were identified as independent significant prognostic factors in multivariate analysis.

Conclusions: LAP represents 9% of pheochromocytoma's population and is characterized by a metastatic behavior. This study paved the way of a future pathological TNM classification.
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http://dx.doi.org/10.1210/clinem/dgab202DOI Listing
March 2021

Treatment of moderate to severe orbitopathy: Current modalities and perspectives.

Ann Endocrinol (Paris) 2021 Mar 4. Epub 2021 Mar 4.

Service d'endocrinologie et maladies métaboliques, pôle cardiovasculaire et métabolique, CHU Larrey, 24, chemin de Pouvourville, 31400 Toulouse, France.

Graves' orbitopathy (GO) is the primary cause of exophthalmos in adults. It appears in 30 to 50% of patients with Graves' disease. About 5% are moderate-to-severe cases that might be see-threatening or lead to long term disabling sequelae. Recommendations have been established in 2016 by the European thyroid association (ETA) and the European group on Grave's orbitopathy (EUGOGO), suggesting a wide use of corticosteroids in moderate to severe forms. However, disappointing results have been reported in 20 to 30% of cases. Improved understanding of pathophysiological mechanisms has allowed the use of non-specific immunomodulatory agents, currently under evaluation, and which place in the therapeutic strategy remains to be determined. Very recently, new promising therapeutic advances have emerged with the identification of new therapeutic targets, such as the TSH receptor and IGF-1 receptor complex.
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http://dx.doi.org/10.1016/j.ando.2021.02.001DOI Listing
March 2021

[Myxoid variant of adrenocortical carcinoma].

Ann Pathol 2021 Apr 3;41(2):186-191. Epub 2021 Feb 3.

Service d'anatomie et cytologie pathologiques, hôpital Lyon Sud, hospices civils de Lyon, Pierre-Bénite, France; Service de chirurgie digestive et endocrinienne, hôpital Lyon Sud, hospices civils de Lyon, Pierre-Bénite, France; Service d'endocrinologie, groupement hospitalier Est, hospices civils de Lyon, Bron, France; Service d'oncologie médicale, hôpital Lyon Sud, hospices civils de Lyon, Pierre-Bénite, France; Cancer Research Center of Lyon, INSERM1052 CNRS5286, Lyon 1 University, Lyon, France. Electronic address:

We report two cases of patients presenting myxoid variant of adrenocortical carcinoma (ACC). This very rare variant is characterized by a tumoral proliferation organized in trabeculae, cords or even pseudo-glands within an acellular myxoid materiel stained by Alcian Blue and negative for PAS. Tumor cells have a small to medium size and have little atypia. Their immunohistochemical profil (positivity of Synaptophysin, SF1, Melan A, Vimentin and Inhibin, with a weak or negative pancytokeratin expression) eliminate the main differential diagnoses (metastasis of a myxoid adenocarcinoma and soft tissue myxoid tumor). Many scoring systems have been proposed in order to evaluate the risk of malignancy of these lesions: the Weiss score seems less efficient to evaluate malignancy in this variant than the reticulinic algorithm or the Helsinki score. Prognosis of myxoid variant of ACC seems worse than classical ACC.
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http://dx.doi.org/10.1016/j.annpat.2020.12.010DOI Listing
April 2021

Multiethnic genome-wide association study of differentiated thyroid cancer in the EPITHYR consortium.

Int J Cancer 2021 Feb 2. Epub 2021 Feb 2.

University Paris-Saclay, UVSQ, Inserm, Gustave Roussy, CESP, Team "Epidemiology of radiations", Villejuif, France.

Incidence of differentiated thyroid carcinoma (DTC) varies considerably between ethnic groups, with particularly high incidence rates in Pacific Islanders. DTC is one of the cancers with the highest familial risk suggesting a major role of genetic risk factors, but only few susceptibility loci were identified so far. In order to assess the contribution of known DTC susceptibility loci and to identify new ones, we conducted a multiethnic genome-wide association study (GWAS) in individuals of European ancestry and of Oceanian ancestry from Pacific Islands. Our study included 1554 cases/1973 controls of European ancestry and 301 cases/348 controls of Oceanian ancestry from seven population-based case-control studies participating to the EPITHYR consortium. All participants were genotyped using the OncoArray-500K Beadchip (Illumina). We confirmed the association with the known DTC susceptibility loci at 2q35, 8p12, 9q22.33 and 14q13.3 in the European ancestry population and suggested two novel signals at 1p31.3 and 16q23.2, which were associated with thyroid-stimulating hormone levels in previous GWAS. We additionally replicated an association with 5p15.33 reported previously in Chinese and European populations. Except at 1p31.3, all associations were in the same direction in the population of Oceanian ancestry. We also observed that the frequencies of risk alleles at 2q35, 5p15.33 and 16q23.2 were significantly higher in Oceanians than in Europeans. However, additional GWAS and epidemiological studies in Oceanian populations are needed to fully understand the highest incidence observed in these populations.
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http://dx.doi.org/10.1002/ijc.33488DOI Listing
February 2021

ESE audit on management of Adult Growth Hormone Deficiency in clinical practice.

Eur J Endocrinol 2020 Dec 1. Epub 2020 Dec 1.

R Verkauskiene, Institute of Endocrinology, Medical Academy, Lithuanian University of Health Sciencies, Kaunas, Lithuania.

Guidelines recommend adults with pituitary disease in whom GH therapy is contemplated, to be tested for GH deficiency (AGHD); however, clinical practice is not uniform.

Aims: 1) To record current practice of AGHD management throughout Europe and benchmark it against guidelines; 2) To evaluate educational status of healthcare professionals about AGHD.

Design: On-line survey in endocrine centres throughout Europe.

Patients And Methods: Endocrinologists voluntarily completed an electronic questionnaire regarding AGHD patients diagnosed or treated in 2017-2018.

Results: Twenty-eight centres from 17 European countries participated, including 2139 AGHD patients, 28% of childhood-onset GHD. Aetiology was most frequently non-functioning pituitary adenoma (26%), craniopharyngioma (13%) and genetic/congenital mid-line malformations (13%). Diagnosis of GHD was confirmed by a stimulation test in 52% (GHRH+arginine, 45%; insulin-tolerance, 42%, glucagon, 6%; GHRH alone and clonidine tests, 7%); in the remaining, ≥3 pituitary deficiencies and low serum IGF-I were diagnostic. Initial GH dose was lower in older patients, but only women <26 years were prescribed a higher dose than men; dose titration was based on normal serum IGF-I, tolerance and side-effects. In one country, AGHD treatment was not approved. Full public reimbursement was not available in four countries and only in childhood-onset GHD in another. AGHD awareness was low among non-endocrine professionals and healthcare administrators. Postgraduate AGHD curriculum training deserves being improved.

Conclusion: Despite guideline recommendations, GH replacement in AGHD is still not available or reimbursed in all European countries. Knowledge among professionals and health administrators needs improvement to optimize care of adults with GHD.
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http://dx.doi.org/10.1530/EJE-20-1180DOI Listing
December 2020

Adherence to growth hormone therapy guidelines in a real-world French cohort of adult patients with growth hormone deficiency.

Ann Endocrinol (Paris) 2021 Feb 5;82(1):59-68. Epub 2020 Dec 5.

Novo Nordisk, 100 Esplanade du Général de Gaulle, 92400 Paris, France.

Objective: Using real-world data from patients with growth hormone deficiency (GHD), we evaluated whether clinical practice in France adheres to international guidelines regarding somatropin dose adjustment, and assessed the long-term effectiveness and safety of somatropin.

Methods: Data were obtained from a national prospective systematic longitudinal routine follow-up programme of naive/non-naive adults with childhood-onset (CO) or adult-onset (AO) GHD treated with Norditropin® (Novo Nordisk A/S).

Results: Between 2003 and 2006, 331 treatment-naive and non-naive adults with severe GHD were enrolled and followed for a median duration of approximately 5 years; 328 patients were available for analysis. At baseline, mean patient age was 39.2 years; median standard deviation score (SDS) for insulin-like growth factor-1 (IGF-1) level was -2.2 in naive patients, subsequently fluctuating between -0.1 and +0.3 SDS during the study period. Mean GH doses ranged between 0.25 and 0.51mg/day (naive patients) and 0.39 and 0.46mg/day (non-naive patients). Despite generally receiving a higher somatropin dose, women (naive/non-naive) tended to have lower IGF-1 levels than men. Median somatropin dose was consistently higher in patients with CO-GHD than patients with AO-GHD. Extreme IGF-1 values (<-2 or >+2 SDS) were not systematically accompanied by somatropin dose adjustments. Waist circumference improved in approximately one third of patients, at a mean 3.5 years. Somatropin was well tolerated; there were no cardiovascular or cerebrovascular events during the 5-year analysis period.

Conclusion: Current clinical practice of physicians in France follows international guidelines regarding somatropin dose adjustment in adults with GHD. However, dose adjustments are not always sufficient, notably in women, and treatment effects may have been delayed due to low somatropin dose (Clinical trial registration NCT01580605).
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http://dx.doi.org/10.1016/j.ando.2020.11.007DOI Listing
February 2021

Progression of incidence and estimate of net survival from papillary thyroid cancers diagnosed between 2008 and 2016 in France.

Ann Endocrinol (Paris) 2020 Dec 5;81(6):530-538. Epub 2020 Dec 5.

FRANCIM, 1, avenue Irène-Joliot-Curie, 31059 Toulouse, France.

Background: After several decades of increasing incidence of papillary thyroid cancer (PTC), a change in this trend has been recently observed, particularly in the United States. This is attributed to the impact of new guidelines for the management of thyroid disease. The objective of this study was to describe the recent situation in France in terms of incidence and survival, taking account of tumor size.

Methods: Data from the FRANCIM network cancer registries, covering around 25% of the French metropolitan population, were analyzed. Distribution according to tumor size was determined in terms of frequency, trends in incidence and spatial distribution for the period 2008-2016. Analysis of net survival considered gender, age and tumor size.

Results: Cancers of size≤5mm were predominant in patients diagnosed between 55 and 74 years of age. Incidence of≤5mm tumors in women and of 5-10mm tumors in men began declining in the early 2010s. Incidence of 10-20mm and 20-40mm tumors in men increased significantly throughout the period 2008-2016. For both men and women, the incidence of the largest tumors (>40mm) also increased, but not significantly. The spatial distribution of incidence showed great heterogeneity. Net survival was generally high, although decreasing with age and tumor size.

Conclusion: The recent epidemiological situation in France is consistent with the hypothesis of recent progress in medical management of thyroid pathologies. Variations in incidence should be monitored for both small (<10mm) and larger tumors, and notably>40mm tumors. Net survival is generally high, although decreasing with age and tumor size.
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http://dx.doi.org/10.1016/j.ando.2020.11.006DOI Listing
December 2020

Screening of a Large Cohort of Asymptomatic SDHx Mutation Carriers in Routine Practice.

J Clin Endocrinol Metab 2021 Mar;106(3):e1301-e1315

Department of Nuclear Medicine, Pitié-Salpêtrière Hospital, Sorbonne University, Paris, France.

Context: When an SDHx mutation is identified in a patient with a pheochromocytoma (PCC) or a paraganglioma (PGL), predictive genetic testing can detect mutation carriers that would benefit from screening protocols.

Objective: To define the tumor detection rate in a large cohort of asymptomatic SDHX mutation carriers.

Design And Setting: Retrospective multicentric study in 6 referral centers.

Patients: Between 2005 and 2019, 249 asymptomatic SDHx (171 SDHB, 31 SDHC, 47 SDHD) mutation carriers, with at least 1 imaging work-up were enrolled.

Results: Initial work-up, including anatomical (98% of subjects [97-100% according to center]) and/or functional imaging (67% [14-90%]) detected 48 tumors in 40 patients. After a negative initial work-up, 124 patients benefited from 1 to 9 subsequent follow-up assessments (mean: 1.9 per patient), with a median follow-up time of 5 (1-13) years. Anatomical (86% [49-100 %]) and/or functional imaging (36% [7-60 %]) identified 10 new tumors (mean size: 16 mm [4-50]) in 10 patients. Altogether, 58 tumors (55 paraganglioma [PGL], including 45 head and neck PGL, 2 pheochromocytoma [PCC], 1 gastrointestinal stromal tumor [GIST]), were detected in 50 patients (22 [13%] SDHB, 1 [3.2%] SDHC, and 27 [57%] SDHD), with a median age of 41 years old [11-86], 76% without catecholamine secretion and 80% during initial imaging work-up.

Conclusions: Imaging screening enabled detection of tumors in 20% of asymptomatic SDHx mutation carriers, with a higher detection rate in SDHD (57%) than in SDHB (13%) and SDHC (3%) mutation carriers, arguing for a gene-by-gene approach. Prospective studies using well-defined protocols are needed to obtain strong and useful data.
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http://dx.doi.org/10.1210/clinem/dgaa888DOI Listing
March 2021

ENSAT registry-based randomized clinical trials for adrenocortical carcinoma.

Eur J Endocrinol 2021 Feb;184(2):R51-R59

Klinik für Endokrinologie, Diabetologie und Klinische Ernährung, Universitätsspital Zürich, Zürich, Switzerland.

Adrenocortical carcinoma (ACC) is an orphan disease lacking effective systemic treatment options. The low incidence of the disease and high cost of clinical trials are major obstacles in the search for improved treatment strategies. As a novel approach, registry-based clinical trials have been introduced in clinical research, so allowing for significant cost reduction, but without compromising scientific benefit. Herein, we describe how the European Network for the Study of Adrenal Tumours (ENSAT) could transform its current registry into one fit for a clinical trial infrastructure. The rationale to perform randomized registry-based trials in ACC is outlined including an analysis of relevant limitations and challenges. We summarize a survey on this concept among ENSAT members who expressed a strong interest in the concept and rated its scientific potential as high. Legal aspects, including ethical approval of registry-based randomization were identified as potential obstacles. Finally, we describe three potential randomized registry-based clinical trials in an adjuvant setting and for advanced disease with a high potential to be executed within the framework of an advanced ENSAT registry. Thus we, therefore, provide the basis for future registry-based trials for ACC patients. This could ultimately provide proof-of-principle of how to perform more effective randomized trials for an orphan disease.
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http://dx.doi.org/10.1530/EJE-20-0800DOI Listing
February 2021

Anti-PD1 and Anti-PDL1-Induced Hypophysitis: A Cohort Study of 17 Patients with Longitudinal Follow-Up.

J Clin Med 2020 Oct 13;9(10). Epub 2020 Oct 13.

Service d'Endocrinologie, Diabète, Nutrition, Centre Hospitalier Lyon Sud, Hospices Civils de Lyon, 69310 Pierre-Bénite, France.

Hypophysitis, secondary to programmed cell death 1 protein (PD1) and programmed cell death 1 ligand 1 (PDL1) inhibitors, were thought to be rare, with only a few studies describing more than one case with long-term follow-up. The aim of the present study was to describe the clinical, laboratory, and morphological characteristics of PD1/PDL1 inhibitor-induced hypophysitis, and its long-term course. This cohort study was conducted at the University Hospital of Lyon, France, with longitudinal follow-up of patients. Seventeen cases of PD1/PDL1 inhibitor-induced hypophysitis were included. The median time to onset of hypophysitis was 28 weeks (range: 10-46). At diagnosis, 16 patients complained of fatigue, 12 of nausea or loss of appetite, while headache was rare. We found no imaging pituitary abnormality. All patients presented adrenocorticotropic hormone (ACTH) deficiency; other pituitary deficiencies were less common ( = 7). At last follow-up (median: 13 months), ACTH deficiency persisted in all but one patient and one patient recovered from gonadotropic deficiency. PD1/PDL1 inhibitor-induced hypophysitis is a clinical entity different from those associated to cytotoxic T-lymphocyte antigen-4 (CTLA4) inhibitors, with less obvious clinical and radiological signs, and probably a different mechanism. The paucity of symptoms demonstrates the need for systematic hormonal follow-up for patients receiving PD1/PDL1 inhibitors.
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http://dx.doi.org/10.3390/jcm9103280DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7601962PMC
October 2020

A key role for conservative treatment in the management of pituitary apoplexy.

Endocrine 2021 Jan 21;71(1):168-177. Epub 2020 Sep 21.

Hospices Civils de Lyon, Endocrinology Department, Reference Center for Rare Pituitary Diseases HYPO, 59 Pinel Boulevard, 69677, Bron, France.

Purpose: The management of pituitary apoplexy, a rare emergency neuroendocrine condition, is controversial. The aim of the present study is to compare the outcomes of patients with pituitary apoplexy managed either by a conservative or surgical approach.

Methods: A retrospective cohort study including patients diagnosed between 2007 and 2018 in a tertiary French university hospital. Pituitary Apoplexy Score (PAS) was retrospectively applied in the perspective of therapeutic decision support.

Results: Forty-six patients were treated for pituitary apoplexy either with conservative management (n = 27) or surgery (n = 19). At initial evaluation, visual field defects (VFD) and visual acuity impairment were more frequent in patients from the surgery group. At 1 year there were no statistical differences in the rates of complete/near-complete resolution of VFD (100 vs. 91.7%), visual acuity impairment (100 vs. 87.5%), and cranial nerve palsies (83.3 vs. 100%), between conservative and surgical treatment groups. There were more endocrine deficits at 1 year in the surgical group (p = 0.029). PAS (n = 41) was 3.4 on average in the early surgery group and 1.3 in the conservative treatment/delayed surgery group. Among patients with a score < 4, 31.3% were operated at first line and did not present better outcomes than patients managed conservatively. In all, 88.9% of patients with a score ≥ 4 underwent surgery.

Conclusions: PAS may be a reliable parameter for defining therapeutic strategy. Patients with non-severe and nonprogressive neuro-ophthalmological deficits can be managed conservatively without negative impact on outcomes, thus surgery should be reserved only for those patients with a PAS ≥ 4.
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http://dx.doi.org/10.1007/s12020-020-02499-8DOI Listing
January 2021

Cytological features and nuclear scores: Diagnostic tools in preoperative fine needle aspiration of indeterminate thyroid nodules with RAS or BRAF K601E mutations?

Cytopathology 2021 01 12;32(1):37-44. Epub 2020 Oct 12.

Centre de Biologie et Pathologie Sud, Centre Hospitalier Lyon Sud, Pierre Bénite, France.

Introduction: The cytological diagnosis of follicular-patterned thyroid lesions is challenging, especially since the World Health Organisation classification has recognised non-invasive follicular thyroid neoplasm with papillary-like features. These entities are often classified as indeterminate on cytology. Molecular testing has been proposed to help classify indeterminate nodules. RAS and K601E BRAF mutations are mostly encountered in follicular-patterned lesions, but their diagnostic value is not well established. Nuclear scores have also been proposed to help classify indeterminate lesions.

Objective: To investigate the correlation between cytological features and histology and to assess nuclear scores in a series of indeterminate RAS or BRAF K601E positive thyroid nodules.

Methods: The cytological parameters of 69 indeterminate RAS or BRAF K601E-positive thyroid nodules were evaluated. The Strickland and Maletta scores and a new nuclear score were assessed. Diagnosis of malignant, benign or indolent neoplasms was confirmed in each case by histology. Malignant and indolent nodules were considered surgical nodules, and adenomas non-surgical nodule.

Results: Surgical nodules were associated with the presence of ground glass nuclei (P = .001), grooves (P < .001) or irregular nuclear membranes (P = .01) on cytology. Nuclear scores were more often ≥2 in surgical nodules compared to benign ones (P < .001), with high sensitivity, but a low negative predictive value.

Conclusions: Analysis of nuclear features is useful to distinguish non-surgical from surgical nodules in indeterminate FNAs. Although nuclear scores are not ideal rule-out tests for indeterminate RAS or BRAF K601E positive nodules, they seem useful to screen non-molecular tested or non-mutated indeterminate FNAs. This work shows that meticulous analysis of nuclear features on cytological specimens can be useful to distinguish non-surgical nodules (adenoma) from surgical nodules in indeterminate FNAs. Although nuclear scores are not rule-out tests for indeterminate RAS or BRAF K601E positive nodules, they are useful in screening non-molecular tested or non-mutated indeterminate FNAs for surgery.
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http://dx.doi.org/10.1111/cyt.12904DOI Listing
January 2021

Influence of Care Pathway on Thyroid Nodule Surgery Relevance: A Historical Cohort Study.

J Clin Med 2020 Jul 17;9(7). Epub 2020 Jul 17.

Health Services and Performance Research Lab (EA 7425 HESPER), Université Claude Bernard Lyon 1, 69100 Villeurbanne, France.

Background: Guidelines recommend using fine-needle aspiration cytology (FNAC) to guide thyroid nodule surgical indication. However, the extent to which these guidelines are followed remains unclear. This study aimed to analyze the quality of the preoperative care pathway and to evaluate whether compliance with the recommended care pathway influenced the relevance of surgical indications.

Methods: Nationwide historical cohort study based on data from a sample (1/97th) of French health insurance beneficiaries. Evaluation of the care pathway of adult patients operated on between 2012 and 2015 during the year preceding thyroid nodule surgery. The pathway containing only FNAC was called "FNAC", the pathway including an endocrinology consultation (ENDO) with FNAC was called "FNAC+ENDO", whereas the no FNAC pathway was called "NO FNAC". The main outcome was the malignant nature of the nodule.

Results: Among the 1080 patients included in the study, "FNAC+ENDO" was found in 197 (18.2%), "FNAC" in 207 (19.2%), and "NO FNAC" in 676 (62.6%) patients. Cancer diagnosis was recorded in 72 (36.5%) "FNAC+ENDO" patients and 66 (31.9%) "FNAC" patients, against 119 (17.6%) "NO FNAC" patients. As compared to "NO FNAC", the "FNAC+ENDO" care pathway was associated with thyroid cancer diagnosis (OR 2.67, 1.88-3.81), as was "FNAC" (OR 2.09, 1.46-2.98). Surgeries performed in university hospitals were also associated with thyroid cancer diagnosis (OR 1.61, 1.19-2.17). Increasing the year for surgery was associated with optimal care pathway (2015 vs. 2012, OR 1.52, 1.06-2.18).

Conclusions: The recommended care pathway was associated with more relevant surgical indications. While clinical guidelines were insufficiently followed, compliance improved over the years.
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http://dx.doi.org/10.3390/jcm9072271DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7408692PMC
July 2020

Letter to the Editor: "Changes in Thyroid Function Across Adolescence: a Longitudinal Study".

J Clin Endocrinol Metab 2020 08;105(8)

Hospices Civils de Lyon, Groupement Hospitalier Est, Fédération d'Endocrinologie, Bron cedex.

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http://dx.doi.org/10.1210/clinem/dgaa313DOI Listing
August 2020

Primary hyperparathyroidism as first manifestation in multiple endocrine neoplasia type 2A: an international multicenter study.

Endocr Connect 2020 Jun;9(6):489-497

Department of ORL Head & Neck Surgery and Audiology, Odense University Hospital, Odense, Denmark.

Objective: Multiple endocrine neoplasia type 2A (MEN 2A) is a rare syndrome caused by RET germline mutations and has been associated with primary hyperparathyroidism (PHPT) in up to 30% of cases. Recommendations on RET screening in patients with apparently sporadic PHPT are unclear. We aimed to estimate the prevalence of cases presenting with PHPT as first manifestation among MEN 2A index cases and to characterize the former cases.

Design And Methods: An international retrospective multicenter study of 1085 MEN 2A index cases. Experts from MEN 2 centers all over the world were invited to participate. A total of 19 centers in 17 different countries provided registry data of index cases followed from 1974 to 2017.

Results: Ten cases presented with PHPT as their first manifestation of MEN 2A, yielding a prevalence of 0.9% (95% CI: 0.4-1.6). 9/10 cases were diagnosed with medullary thyroid carcinoma (MTC) in relation to parathyroid surgery and 1/10 was diagnosed 15 years after parathyroid surgery. 7/9 cases with full TNM data were node-positive at MTC diagnosis.

Conclusions: Our data suggest that the prevalence of MEN 2A index cases that present with PHPT as their first manifestation is very low. The majority of index cases presenting with PHPT as first manifestation have synchronous MTC and are often node-positive. Thus, our observations suggest that not performing RET mutation analysis in patients with apparently sporadic PHPT would result in an extremely low false-negative rate, if no other MEN 2A component, specifically MTC, are found during work-up or resection of PHPT.
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http://dx.doi.org/10.1530/EC-20-0163DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7354718PMC
June 2020

[Checkpoint inhibitors-induced hypophysitis].

Bull Cancer 2020 Apr 19;107(4):490-498. Epub 2020 Mar 19.

Hospices civils de Lyon, fédération d'endocrinologie, 28, avenue Doyen-Lépine, 69677 Bron cedex, France; ImmuCare, institut de cancérologie des hospices civils de Lyon (IDCRC-HCL), Lyon, France; Université de Lyon, université Claude-Bernard-Lyon-1, Lyon, France.

Checkpoint inhibitors immunotherapy is more and more prescribed in oncology, causing new immune related endocrine adverse events. Hypophysitis occurs in approximately 10 % of patients treated with anti-CTLA4. It occurs two to three months after initiation of the immunotherapy. The initial presentation is characterized, in typical forms, by the association of headache, asthenia and hyponatremia. Hormonal exploration usually shows ACTH, gonadotropic and thyrotropic deficiencies. ACTH deficiency may be life-threatening and requires urgent supplementation, without awaiting for biological results. MRI is warranted in order to exclude differential diagnoses, such as pituitary metastases. Hypophysitis induced by anti-PD1/PDL1 seems to be a different nosologic entity characterized by a later onset and a less symptomatic presentation. Biologically ACTH deficiency seems to be constant and permanent, and often isolated. Treatment requires high-dose steroids only in case of severe tumor syndrome (resistant headache, visual disturbance) or acute decompensation of ACTH deficiency. Patients always need lifelong hormonal supplementation of pituitary deficits and must be followed and educated specifically. Immunotherapy can be delayed during the acute phase, but can be secondarily continued if there is an oncological benefit. As it is a pauci-symptomatic but potentially life-threatening complication, biological screening must be systematic in patients treated with checkpoint inhibitors.
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http://dx.doi.org/10.1016/j.bulcan.2020.01.012DOI Listing
April 2020

Age- and Sex-Specific TSH Upper-Limit Reference Intervals in the General French Population: There Is a Need to Adjust Our Actual Practices.

J Clin Med 2020 Mar 14;9(3). Epub 2020 Mar 14.

Hospices Civils de Lyon, Fédération d'Endocrinologie, Groupement Hospitalier Est, F-69677 Bron cedex, France.

It is well known that thyroid dysfunction increases with age. This study is aimed to determine reference intervals, in males and females, suitable for thyroid disease exploration during adult life using routinely collected serum thyrotropin (TSH) data in a tertiary center from 2007 to 2018. Over 11 years, 295,775 TSH levels were measured in a single lab. Among the 156,025 TSH results available for analysis, 90,538 values were from female subjects, 82,019 were from patients aged >60 years and 26,825 were from patients aged >80 years. By using an indirect approach, we determined reference values of TSH adapted to age and sex, and we then evaluated the proportion of patients who would have been reclassified with these reference values. The median TSH ranged from 1.2-1.4 mUI/L during the study period. The upper limit of reference range of TSH increased with age; in females the median to 97.5th percentile values increased continuously from the age of 30 years to the oldest age group. Using new calculated reference values in patients with TSH above the conventional upper-limit reference value (4 mUI/L), the proportion of results reclassified as within the reference interval among patients aged >60 years ranged, according to age group, from 50.5% to 65.1% of females and from 33.0% to 37.7% of males. The use of TSH age-specific and sex-specific upper-limit reference values led to the reclassification of a great number of samples, notably among women. This suggests that age-specific TSH upper-limit reference intervals in daily practice should be used in order to avoid misclassification.
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http://dx.doi.org/10.3390/jcm9030792DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7141356PMC
March 2020

Metformin and everolimus in neuroendocrine tumours: A synergic effect?

Clin Res Hepatol Gastroenterol 2020 11 4;44(6):954-960. Epub 2020 Mar 4.

Service d'oncologie médicale, hôpital Edouard-Herriot, hospices civils de Lyon, Pavillon E, UJOMM, 69437 Lyon, France; University of Lyon, Univsersité de Lyon 1, Lyon, France. Electronic address:

Objective: To explore potential synergy in effectiveness between metformin and everolimus, 2 inhibitors of the mTOR pathway, for neuroendocrine tumours (NET).

Design And Methods: A cohort of patients with advanced gastroenteropancreatic or lung NETs treated by everolimus were stratified in to those without diabetes, those with diabetes and without metformin, and those with diabetes with metformin. The primary endpoint was the median progression-free survival (PFS).

Results: A total of 213 patients were included, 165 of which were non-diabetic; among diabetic patients, 19 were treated with metformin and 29 with others anti-diabetic drugs. No significant difference in median PFS [95%CI] was found between the three groups: 10.05 months [8.27;11.83] for non-diabetic patients, 15.24 [19.88;49.43] for diabetic w/metformin, and 9.03 months [4.01;14.06] for diabetic w/o metformin group. In univariate analysis, factors significantly associated with longer PFS was a functioning NET, a number of metastatic sites<3, the absence of lung metastasis, and an uptake on Octreoscan®, but not the absence of metformin use; only uptake on Octreoscan® remained significant in multivariate analysis.

Conclusions: In contrast with the literature, we did not find a synergy between everolimus and metformin in NET. Prospective studies are underway to improve the comprehension of the potential synergy regarding population and tumour type.
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http://dx.doi.org/10.1016/j.clinre.2020.02.011DOI Listing
November 2020

SST5 expression and USP8 mutation in functioning and silent corticotroph pituitary tumors.

Endocr Connect 2020 Feb 1. Epub 2020 Feb 1.

H Lasolle, Service d'Endocrinologie, Centre de Référence des Maladies Rares de l'Hypophyse HYPO, Groupement Hospitalier Est, Hospices Civils de Lyon, Bron, France.

Objective: Somatostatin receptor type 5 (SST5) is inconsistently expressed by corticotroph tumors, with higher expression found in corticotropinomas having ubiquitin-specific protease 8 (USP8) mutations. Aims were to study the correlation between characteristics of corticotropinomas and SST5 expression/USP8 mutation status and to describe the response to pasireotide in 5 patients.

Design: Retrospective cohort study.

Methods: Clinico-biochemical, radiological and pathological data of 62 patients, operated for a functioning or silent corticotropinoma between 2013 and 2017, were collected. SST5 expression was measured by immunohistochemistry (clone UMB-4, Abcam, IRS>1 being considered positive) and Sanger sequencing was performed on 50 tumors to screen for USP8 mutations.

Results: SST5 expression was positive in 26/62 pituitary tumors. A moderate or strong IRS was found in 15/58 corticotropinomas and in 13/35 functioning corticotropinomas. Among functioning tumors, those expressing SST5 were more frequent in women (22/24 vs 9/15, P=0.04) and had a lower grade (P=0.04) compared to others. USP8 mutations were identified in 13/50 pituitary tumors and were more frequent in functioning compared to silent tumors (11/30 vs 2/20, P=0.05). SST5 expression was more frequent in USP8mut vs USP8wt tumors (10/11 vs 7/19, P=0.007). Among treated patients, normal urinary free cortisol levels were obtained in 3 patients (IRS 0, 2, 6) while a 4-fold decrease was observed in one patient (IRS 4).

Conclusion: SST5 expression appears to be associated with functioning, USP8mut and lower grade corticotropinomas. A correlation between SST5 expression or USP8mut and response to pasireotide remains to be confirmed.
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http://dx.doi.org/10.1530/EC-20-0035DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7077525PMC
February 2020

Evolution of macroprolactinomas during pregnancy: A cohort study of 85 pregnancies.

Clin Endocrinol (Oxf) 2020 05 4;92(5):421-427. Epub 2020 Feb 4.

Service d'Endocrinologie - Diabète - Nutrition, Centre Hospitalier Universitaire de Reims, Reims, France.

Objective: Pregnancy in patients with macroprolactinomas has been associated with a higher risk of pituitary tumour growth. However, the incidence and risk factors remain unclear. We aimed to evaluate the evolution of macroprolactinomas during pregnancy and to identify potential risk factors.

Design, Patients And Measurements: This is a two-centre, retrospective, observational study. All patients with macroprolactinomas, treated with a dopamine receptor agonist (DA), and who had at least one pregnancy were included.

Results: There were a total of 85 viable pregnancies in 46 patients with macroprolactinomas. At diagnosis, mean size of pituitary adenomas was 17.9 ± 8.2 mm (10-43 mm) and mean plasma prolactin level was 1012.2 ± 1606.1 µg/L (60-7804 µg/L). Tumour growth-related symptoms were identified 12 times in 9 patients (19.6%) including 3 cases of apoplexy. Restarting, changing and/or increasing DA treatment was effective in 10 cases. Emergency surgery had to be performed twice (due to pituitary apoplexy). Patients with tumour progression tended to present with larger tumours after initial treatment and before pregnancy (9.9 vs 5.9 mm; P = .0504 and 11.5 vs 7.3 mm; P = .0671, respectively), whereas adenoma size at diagnosis did not seem to be a significant factor. The obstetrical outcomes were comparable to the general population.

Conclusions: Symptomatic growth of macroprolactinoma during pregnancy occurred in 19.6% of medically treated patients. This risk seems higher for patients with poor initial tumour response to the DA treatment. Tumour progression is generally well controlled with medical treatment during pregnancy.
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http://dx.doi.org/10.1111/cen.14162DOI Listing
May 2020

[Thyroid dysfunctions secondary to cancer immunotherapy].

Bull Cancer 2020 Feb 24;107(2):262-271. Epub 2019 Dec 24.

Hospices civils de Lyon, hôpital Lyon Sud, service d'endocrinologie diabète nutrition, 165, chemin du Grand Revoyet, 69310 Pierre-Bénite, France; ImmuCare, Institut de cancérologie des hospices civils de Lyon (IDCRC-HCL), 69003 Lyon, France; Université de Lyon, université Claude Bernard Lyon 1, 69100 Lyon, France.

The immune checkpoint inhibitors (CPI) such as anti-PD(L)1 or anti-CTLA4 had improved long-term patients' outcomes in different malignancies. Thyroid disorders are the most frequent endocrine side effects from CPI reported in clinical trials and in clinical routine practice. The incidence of thyroid dysfunction is variable according to ICP used (more frequent under anti-programmed cell death 1 (PD1) or anti-programmed cell death-ligand 1 (PDL1)). Most thyroid dysfunctions have been reported to occur 2 to 4 courses after CPI initiation. The clinical symptoms are generally nonspecific (asthenia, weight change, rarely cardiac rhythm disorder). These thyroid dysfunctions are commonly painless thyroiditis with a biphasic evolution: thyrotoxicosis followed by a secondary hypothyroidism frequently definitive. Diagnosis is made on a thyroid test (TSH and FT4). In most cases, no further exam is necessary. Beta blockers therapy is recommended in symptomatic thyrotoxicosis with palpitations. Thyroid hormones therapy will be introduced quickly in case of hypothyroidism. Thyroid dysfunctions are not a contra-indication to the continuation of immunotherapy. Due to the high frequency of these complications, close monitoring of the thyroid status is recommended under CPI.
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http://dx.doi.org/10.1016/j.bulcan.2019.10.005DOI Listing
February 2020

Should the GCM2 gene be tested when screening for familial primary hyperparathyroidism?

Eur J Endocrinol 2020 Jan;182(1):57-65

Service de Biochimie et Biologie Moléculaire 'Hormonologie, Métabolisme-Nutrition, Oncologie', CHU Lille, Lille, France.

Objective: Primary hyperparathyroism (PHPT) is a disease with either sporadic or inherited presentation. Germline mutations responsible for this disease can be found in different genes, the most frequently involved being MEN1, CDC73 = HRPT2 and CASR. During the last few years, new genes have been described as responsible for the development of PHPT such as GCM2. These genes are not systematically included in PHPT genetic screening yet. The aim of this work was to assess the importance of GCM2 genetic analysis in PHPT to determine if this gene should be included in gene panel investigated for this disease.

Design And Methods: The TENGEN network (French Oncogenetic Network of Neuroendocrine Tumors) collected and interpreted allelic variants according to the clinical characteristics of the GCM2-positive patients identified through genetic testing performed in French laboratories (713 patients with PHPT).

Results: From 713 patients with PHPT included in this study, 85 (6.6%) carried at least one GCM2 variant. A total of 12 variants classified as uncertain significance or likely pathogenic were reported in 47 patients. Their mean age at PHPT diagnosis was 49 years. Additionally, the investigation of a large family showed that GCM2 variants could be associated with low penetrance.

Conclusion: We provide a description and interpretation for GCM2 variants identified in a French population. We suggest that this gene should be included in genetic screening of patients with PHPT and propose the follow-up of asymptomatic patients carrying such variants for calcemia.
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http://dx.doi.org/10.1530/EJE-19-0641DOI Listing
January 2020

Diagnosis, pathology, and management of TSH-secreting pituitary tumors. A single-center retrospective study of 20 patients from 1981 to 2014.

Ann Endocrinol (Paris) 2019 Sep 26;80(4):216-224. Epub 2019 Jul 26.

Université de Lyon, Lyon1, 69372 Lyon, France; Inserm U1052, CNRS UMR5286, Cancer Research Center of Lyon, Lyon, France; Fédération d'endocrinologie, centre de référence maladies rares hypophysaire HYPO, groupement hospitalier Est, hospices Civils de Lyon, 59, boulevard Pinel, 69677 Bron cedex, France. Electronic address:

TSH (thyroid-stimulating hormone)-secreting tumors are the rarest type of pituitary tumor. The objective of this study was to describe initial presentation and follow-up in patients presenting TSH-secreting tumors and to characterize the pathological features, based on a cohort of 20 patients treated in our referral center, between 1981 and 2014. Most of the patients (75%) were female, aged around 50 years (mean: 50±13 years). Initial symptoms were hyperthyroidism (8/20) and/or tumor mass-related symptoms. Median time to diagnosis was 18 months. Biochemical hyperthyroidism was found in 15 patients. Most of the tumors were macroadenomas (75%) and 30% were invasive. Seventeen patients underwent transsphenoidal surgery. All tumors expressed TSH, with>50% positive cells. Eleven were monohormonal and 6 plurihormonal, expressing βTSH plus growth hormone (GH) and/or prolactin (PRL). Both subtypes showed high expression of Pit-1 and SSTR somatostatin receptors. SSTR was slightly expressed in the plurihormonal subtype. Ki-67 index was elevated (≥3%) in only one tumor. Signs of hyperthyroidism were more frequent in the plurihormonal than in the monohormonal subtype. At final follow-up (median: 34.79±66.7 months), 75% of the patients were in complete remission after surgery; persistent hyperthyroidism was controlled by somatostatin analogs, alone (n=3) or associated to radiotherapy (n=1). The multidisciplinary approach promoted early diagnosis and control of hyperthyroidism by neurosurgical treatment, associated to somatostatin analogs or not. Clinical/pathological correlations highlighted the variations in immune profiles and in clinical and biological symptoms.
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http://dx.doi.org/10.1016/j.ando.2019.06.006DOI Listing
September 2019

Pheochromocytoma, paragangliomas, and pituitary adenoma: An unusual association in a patient with an SDHD mutation. Case report.

Medicine (Baltimore) 2019 Jul;98(30):e16594

Department of Endocrinology, Hospices Civils de Lyon, Fédération d'Endocrinologie.

Rationale: Pituitary adenomas and paragangliomas are both rare endocrine diseases. Paragangliomas (PGL)/pheochromocytomas (PHEO) are part of an inherited syndrome in about 30% to 40% of cases. Among familial cases, mutations of the succinate dehydrogenase (SDH) subunit genes (succinate dehydrogenase subunit [SDH]B, SDHC, SDHD, succinate dehydrogenase subunit AF2 [SDHAF2] , and SDHA) are the most common cause.

Patient Concerns: We here report a 31-year-old patient with a known SDHD mutation whose disease has been revealed by a left PHEO during childhood and who presented at age 29 years a large paraganglioma of the right jugular foramen, a concomitant PHEO of the left adrenal and 2 retroperitoneal paragangliomas. A pituitary incidentaloma was found during investigations on a fluorodeoxyglucose (FDG)-positron emission tomography (PET) (FDG-PET).

Diagnosis: A pituitary magnetic resonance imaging (MRI) confirmed the presence of a 14 mm pituitary macroadenoma. The pituitary function was normal except for hypogonadotropic hypogonadism. On examination of the fundus, a diagnosis of Pseudo Foster-Kennedy syndrome was made due to a venous compression of the right jugular vein caused by the paraganglioma (PGL). The pituitary adenoma was not compressive to the optic chiasm.

Interventions: A treatment with acetazolamide was started in order to improve intracranial hypertension. The patient couldn't benefit of a surgical approach for the paraganglioma of the right jugular foramen; the patient has been treated with stereotactic radiosurgery (Gamma Knife).

Outcomes: The most recent MRI revealed that the right jugular foramen PGL is stable and the latest visual assessment demonstrated stability despite a recent reduction in acetazolamide dosage. A surveillance by MRI of the pituitary adenoma has been planned.

Lessons: The association of a pituitary adenoma to paragangliomas within a same patient is very uncommon and raises the question of related physiopathological mechanisms.
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http://dx.doi.org/10.1097/MD.0000000000016594DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6708967PMC
July 2019

Predicting early post-operative remission in pituitary adenomas: evaluation of the modified knosp classification.

Pituitary 2019 Oct;22(5):467-475

Fédération d'Endocrinologie, Centre de Référence Maladies Rares hypophysaires, Groupement Hospitalier Est, Hospices Civils de Lyon, 69677, Bron, France.

Purpose: Cavernous sinus invasion by pituitary adenomas is an important prognostic factor for evaluating the possibilities of complete remission and to guide patient management. A widely used Magnetic Resonance Imaging grading system, suggested by Knosp in 1993, has recently been revised by the same group. The aims of our study were to apply this revised grading system to our surgical series, to determine its association with surgical outcomes, gross-total resection (GTR) and endocrinological remission (ER), paying particular attention to grades 3A and 3B, which represent the novelty of this revised classification.

Methods: We included consecutive patients who underwent endoscopic endonasal surgery for a macroadenoma from September 2012 to December 2016. MRI images were reviewed and classified according to the revised Knosp classification. Surgical reports indicated the intra-operative CS invasion. GTR and ER were evaluated on 3-months post-operative MRI and endocrine evaluation.

Results: 254 patients were included in this study. We found a total rate of cavernous sinus invasion of 18.4%. Different outcomes were observed for each grade, with an increased rate of cavernous sinus invasion with each grade. Per-operative rates of invasion were 61.5 and 78.6% in grades 3A and 3B respectively. GTR was negatively correlated with the grade, while rates were 55.8% and 30.0% for grades 3A and 3B respectively.

Conclusion: The revised Knosp radiological classification contributes to the prediction of surgical outcomes and early ER in pituitary adenomas. To manage, as precisely as possible, the risk of early recurrence in pituitary adenomas, clinicians should also consider other recognized prognostic factors, such as the proliferative status of the tumor.
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http://dx.doi.org/10.1007/s11102-019-00976-6DOI Listing
October 2019

The medical treatment of radioiodine-refractory differentiated thyroid cancers in 2019. A TUTHYREF network review.

Bull Cancer 2019 Sep 11;106(9):812-819. Epub 2019 Jun 11.

Department of nuclear medicine and endocrine tumors, Gustave-Roussy, Villejuif, France.

Patients with radioiodine-refractory (RAIR) differentiated thyroid carcinoma (DTC) represent a challenging subgroup of DTC because they are at higher risk of cancer-related death. Multidisciplinary discussions can assess the role and the nature of local treatments, but also determine the optimal timing for first-line antiangiogenic therapy as some of these patients can be followed for several months or years without any treatment. In this review, we will examine the definition of RAIR-DTC, the different treatment options and finally some of the most recent cancer research breakthroughs for RAIR-DTC.
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http://dx.doi.org/10.1016/j.bulcan.2019.04.012DOI Listing
September 2019