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1. Characteristics of a nationwide cohort of patients presenting with isolated hypogonadotropic hypogonadism (IHH)

Author

Bonomi, M., Vezzoli, V., Krausz, C., Guizzardi, F., Vezzani, S., Simoni, M., Bassi, I., Duminuco, P., Di Iorgi, N., Giavoli, C., Pizzocaro, A., Russo, G., Moro, M., Fatti, L., Ferlin, A., Mazzanti, L., Zatelli, M. C., Cannavo, S., Isidori, A. M., Pincelli, A. I., Prodam, F., Mancini, A., Limone, P., Tanda, M. L., Gaudino, R., Salerno, M., Francesca, P., Maghnie, M., Maggi, M. C., Persani, L., Aimaretti, G., Altobell, M., Ambrosio, M. R., Andrioli, M., Angelett, G., Arecco, F., Arnald, G., Arosio, M., Balsamo, A., Baldassarr, M., Bartalena, L., Bazzon, N., Beccari, L., Beck-Peccoz, P., Bellastella, G., Bellizz, M., Benedicent, F., Bernasconi, S., Bizzarri, C., Bona, G., Bonadonna, S., Borrett, G., Boschetti, M., Brunani, A., Brunelli, V., Buz, F., Cacciatore, C., Cangiano, B., Cappa, M., Casalone, R., Cassio, A., Cavarzere, P., Cherubini, V., Ciampani, T., Cicognan, D., Cignarell, A., Cisternin, M., Colombo, P., Corbetta, S., Corciul, N., Corona, G., Cozzi, R., Crivellaro, C., Dalle Mule, I., Danesi, L., Eli, A. V. D., Degli Uberti, E., De Leo, S., Della Valle, E., De Marchi, M., Di Mambr, A., Fabbri, A., Foresta, C., Forti, G., Franceschi, A. R., Garolla, A., Ghezzi, M., Giacomozzi, C., Giusti, M., Grosso, E., Guabello, G., Guarneri, M. P., Grugni, G., Lanfranco, F., Lania, A., Lanzi, R., Larizza, L., Lenzi, A., Loche, S., Loli, P., Lombardi, V., Mandrile, G., Manieri, C., Mantovani, G., Marelli, S., Marzullo, M., Mencarelli, M. A., Migone, N., Motta, G., Neri, G., Padov, G., Parenti, G., Pasquino, B., Pia, A., Piantanida, E., Pignatti, E., Pilotta, A., Pivett, B., Pollazzon, M., Pontecorvi, A., Porcelli, P., Pozza, G. B., Pozzobon, G., Radetti, G., Razzore, P., Rocchett, L., Roncoron, R., Rossi, G., Sala, E., Salvatoni, A., Salvini, F., Secc, A., Segni, M., Selice, R., Sgaramella, P., Sileo, F., Sinisi, A. A., Sirchia, F., Spada, A., Tresoldi, A., Vigneri, R., Weber, G., Zucchini, S., Bassi I., Moro M., Pincelli A. I., Mancini A. (ORCID:0000-0002-7707-4564), Cappa M., Corbetta S., Corona G., Danesi L., Ghezzi M., Giusti M. (ORCID:0000-0001-5767-8785), Grugni G., Parenti G., Pontecorvi A. (ORCID:0000-0003-0570-6865), Sala E., Bonomi, M., Vezzoli, V., Krausz, C., Guizzardi, F., Vezzani, S., Simoni, M., Bassi, I., Duminuco, P., Di Iorgi, N., Giavoli, C., Pizzocaro, A., Russo, G., Moro, M., Fatti, L., Ferlin, A., Mazzanti, L., Zatelli, M. C., Cannavo, S., Isidori, A. M., Pincelli, A. I., Prodam, F., Mancini, A., Limone, P., Tanda, M. L., Gaudino, R., Salerno, M., Francesca, P., Maghnie, M., Maggi, M. C., Persani, L., Aimaretti, G., Altobell, M., Ambrosio, M. R., Andrioli, M., Angelett, G., Arecco, F., Arnald, G., Arosio, M., Balsamo, A., Baldassarr, M., Bartalena, L., Bazzon, N., Beccari, L., Beck-Peccoz, P., Bellastella, G., Bellizz, M., Benedicent, F., Bernasconi, S., Bizzarri, C., Bona, G., Bonadonna, S., Borrett, G., Boschetti, M., Brunani, A., Brunelli, V., Buz, F., Cacciatore, C., Cangiano, B., Cappa, M., Casalone, R., Cassio, A., Cavarzere, P., Cherubini, V., Ciampani, T., Cicognan, D., Cignarell, A., Cisternin, M., Colombo, P., Corbetta, S., Corciul, N., Corona, G., Cozzi, R., Crivellaro, C., Dalle Mule, I., Danesi, L., Eli, A. V. D., Degli Uberti, E., De Leo, S., Della Valle, E., De Marchi, M., Di Mambr, A., Fabbri, A., Foresta, C., Forti, G., Franceschi, A. R., Garolla, A., Ghezzi, M., Giacomozzi, C., Giusti, M., Grosso, E., Guabello, G., Guarneri, M. P., Grugni, G., Lanfranco, F., Lania, A., Lanzi, R., Larizza, L., Lenzi, A., Loche, S., Loli, P., Lombardi, V., Mandrile, G., Manieri, C., Mantovani, G., Marelli, S., Marzullo, M., Mencarelli, M. A., Migone, N., Motta, G., Neri, G., Padov, G., Parenti, G., Pasquino, B., Pia, A., Piantanida, E., Pignatti, E., Pilotta, A., Pivett, B., Pollazzon, M., Pontecorvi, A., Porcelli, P., Pozza, G. B., Pozzobon, G., Radetti, G., Razzore, P., Rocchett, L., Roncoron, R., Rossi, G., Sala, E., Salvatoni, A., Salvini, F., Secc, A., Segni, M., Selice, R., Sgaramella, P., Sileo, F., Sinisi, A. A., Sirchia, F., Spada, A., Tresoldi, A., Vigneri, R., Weber, G., Zucchini, S., Bassi I., Moro M., Pincelli A. I., Mancini A. (ORCID:0000-0002-7707-4564), Cappa M., Corbetta S., Corona G., Danesi L., Ghezzi M., Giusti M. (ORCID:0000-0001-5767-8785), Grugni G., Parenti G., Pontecorvi A. (ORCID:0000-0003-0570-6865), and Sala E.

Abstract

Objective: Isolated hypogonadotropic hypogonadism (IHH) is a rare disorder with pubertal delay, normal (normoosmic-IHH, nIHH) or defective sense of smell (Kallmann syndrome, KS). Other reproductive and nonreproductive anomalies might be present although information on their frequency are scanty, particularly according to the age of presentation. Design: Observational cohort study carried out between January 2008 and June 2016 within a national network of academic or general hospitals. Methods: We performed a detailed phenotyping of 503 IHH patients with: (1) manifestations of hypogonadism with low sex steroid hormone and low/normal gonadotropins; (2) absence of expansive hypothalamic/pituitary lesions or multiple pituitary hormone defects. Cohort was divided on IHH onset (PPO, pre-pubertal onset or AO, adult onset) and olfactory function: PPO-nIHH (n = 275), KS (n = 184), AO-nIHH (n = 36) and AO-doIHH (AO-IHH with defective olfaction, n = 8). Results: 90% of patients were classifed as PPO and 10% as AO. Typical midline and olfactory defects, bimanual synkinesis and familiarity for pubertal delay were also found among the AO-IHH. Mean age at diagnosis was signifcantly earlier and more frequently associated with congenital hypogonadism stigmata in patients with Kallmann's syndrome (KS). Synkinesis, renal and male genital tract anomalies were enriched in KS. Overweight/obesity are signifcantly associated with AO-IHH rather than PPO-IHH. Conclusions: Patients with KS are more prone to develop a severe and complex phenotype than nIHH. The presence of typical extra-gonadal defects and familiarity for PPO-IHH among the AO-IHH patients indicates a common predisposition with variable clinical expression. Overall, these fndings improve the understanding of IHH and may have a positive impact on the management of patients and their families.

Published
2018

2. Characteristics of a nationwide cohort of patients presenting with isolated hypogonadotropic hypogonadism (IHH)

Author

Marco Bonomi, Valeria Vezzoli, Csilla Krausz, Fabiana Guizzardi, Silvia Vezzani, Manuela Simoni, Ivan Bassi, Paolo Duminuco, Natascia Di Iorgi, Claudia Giavoli, Alessandro Pizzocaro, Gianni Russo, Mirella Moro, Letizia Fatti, Alberto Ferlin, Laura Mazzanti, Maria Chiara Zatelli, Salvo Cannavò, Andrea M Isidori, Angela Ida Pincelli, Flavia Prodam, Antonio Mancini, Paolo Limone, Maria Laura Tanda, Rossella Gaudino, Mariacarolina Salerno, Pregnolato Francesca, Mohamad Maghnie, Mario Maggi, Luca Persani, G Aimaretti, M Altobelli, M R Ambrosio, M Andrioli, G Angeletti, F Arecco, G Arnaldi, M Arosio, A Balsamo, M Baldassarri, L Bartalena, N Bazzoni, L Beccaria, P Beck-Peccoz, G Bellastella, M Bellizzi, F Benedicenti, S Bernasconi, C Bizzarri, G Bona, S Bonadonna, G Borretta, M Boschetti, A Brunani, V Brunelli, F Buzi, C Cacciatore, B Cangiano, M Cappa, R Casalone, A Cassio, P Cavarzere, V Cherubini, T Ciampani, D Cicognani, A Cignarelli, M Cisternino, P Colombo, S Corbetta, N Corciulo, G Corona, R Cozzi, C Crivellaro, I Dalle Mule, L Danesi, A V D’Elia, E degli Uberti, S De Leo, E Della Valle, M De Marchi, N Di Iorgi, A Di Mambro, A Fabbri, C Foresta, G Forti, A R Franceschi, A Garolla, M Ghezzi, C Giacomozzi, M Giusti, E Grosso, G Guabello, M P Guarneri, G Grugni, A M Isidori, F Lanfranco, A Lania, R Lanzi, L Larizza, A Lenzi, S Loche, P Loli, V Lombardi, M C Maggio, G Mandrile, C Manieri, G Mantovani, S Marelli, M Marzullo, M A Mencarelli, N Migone, G Motta, G Neri, G Padova, G Parenti, B Pasquino, A Pia, E Piantanida, E Pignatti, A Pilotta, B Pivetta, M Pollazzon, A Pontecorvi, P Porcelli, G B Pozzan, G Pozzobon, G Radetti, P Razzore, L Rocchetti, R Roncoroni, G Rossi, E Sala, A Salvatoni, F Salvini, A Secco, M Segni, R Selice, P Sgaramella, F Sileo, A A Sinisi, F Sirchia, A Spada, A Tresoldi, R Vigneri, G Weber, S Zucchini, Bonomi, Marco, Vezzoli, Valeria, Krausz, Csilla, Guizzardi, Fabiana, Vezzani, Silvia, Simoni, Manuela, Bassi, Ivan, Duminuco, Paolo, Di Iorgi, Natascia, Giavoli, Claudia, Pizzocaro, Alessandro, Russo, Gianni, Moro, Mirella, Fatti, Letizia, Ferlin, Alberto, Mazzanti, Laura, Zatelli Maria, Chiara, Cannavò, Salvo, Isidori Andrea, M., Pincelli Angela, Ida, Prodam, Flavia, Mancini, Antonio, Limone, Paolo, Tanda Maria, Laura, Gaudino, Rossella, Salerno, Mariacarolina, Francesca, Pregnolato, Maghnie, Mohamad, Maggi, Mario, Persani, Luca, Italian Network on Central, Hypogonadism., Zatelli, Maria Chiara, Cannavã², Salvo, Isidori, Andrea M., Pincelli, Angela Ida, Tanda, Maria Laura, Aimaretti, G., Altobell, M., Ambrosio, M. R., Andrioli, M., Angelett, G., Arecco, F., Arnald, G., Arosio, M., Balsamo, A., Baldassarr, M., Bartalena, L., Bazzon, N., Beccari, L., Beck-Peccoz, P., Bellastella, G., Bellizz, M., Benedicent, F., Bernasconi, S., Bizzarri, C., Bona, G., Bonadonna, S., Borrett, G., Boschetti, M., Brunani, A., Brunelli, V., Buz, F., Cacciatore, C., Cangiano, B., Cappa, M., Casalone, R., Cassio, A., Cavarzere, P., Cherubini, V., Ciampani, T., Cicognan, D., Cignarell, A., Cisternin, M., Colombo, P., Corbetta, S., Corciul, N., Corona, G., Cozzi, R., Crivellaro, C., Dalle Mule, I., Danesi, L., Eli, A. V. D., Degli Uberti, E., De Leo, S., Della Valle, E., De Marchi, M., Di Iorgi, N., Di Mambr, A., Fabbri, A., Foresta, C., Forti, G., Franceschi, A. R., Garolla, A., Ghezzi, M., Giacomozzi, C., Giusti, M., Grosso, E., Guabello, G., Guarneri, M. P., Grugni, G., Isidori, A. M., Lanfranco, F., Lania, A., Lanzi, R., Larizza, L., Lenzi, A., Loche, S., Loli, P., Lombardi, V., Maggi, M. C., Mandrile, G., Manieri, C., Mantovani, G., Marelli, S., Marzullo, M., Mencarelli, M. A., Migone, N., Motta, G., Neri, G., Padov, G., Parenti, G., Pasquino, B., Pia, A., Piantanida, E., Pignatti, E., Pilotta, A., Pivett, B., Pollazzon, M., Pontecorvi, A., Porcelli, P., Pozza, G. B., Pozzobon, G., Radetti, G., Razzore, P., Rocchett, L., Roncoron, R., Rossi, G., Sala, E., Salvatoni, A., Salvini, F., Secc, A., Segni, M., Selice, R., Sgaramella, P., Sileo, F., Sinisi, A. A., Sirchia, F., Spada, A., Tresoldi, A., Vigneri, R., Weber, G., Zucchini, S., Marco Bonomi, Valeria Vezzoli, Csilla Krausz, Fabiana Guizzardi, Silvia Vezzani, Manuela Simoni, Ivan Bassi, Paolo Duminuco, Natascia Di Iorgi, Claudia Giavoli, Alessandro Pizzocaro, Gianni Russo, Mirella Moro, Letizia Fatti, Alberto Ferlin, Laura Mazzanti, Maria Chiara Zatelli, Salvo Cannavò, Andrea M Isidori, Angela Ida Pincelli, Flavia Prodam, Antonio Mancini, Paolo Limone, Maria Laura Tanda, Rossella Gaudino, Mariacarolina Salerno, Pregnolato Francesca, Mohamad Maghnie, Mario Maggi, Luca Persani, Italian Network on Central Hypogonadism […, A. Cassio, …, S. Zucchini, ], Isidori, Andrea M, Weber, Giovanna, and Italian Network on Central, Hypogonadism

Subjects
0301 basic medicine, Male, Pediatrics, Synkinesis, Kallmann syndrome, diagnosis, genotype, Endocrinology, Diabetes and Metabolism, Gonadal Steroid Hormone, Cohort Studies, Olfaction Disorders, 0302 clinical medicine, Endocrinology, Olfaction Disorder, Young adult, Age of Onset, Gonadal Steroid Hormones, Gonadotropin, Pituitary Hormone, Isolated hypogonadotropic hypogonadism, General Medicine, isolated hypogonadotropic hypogonadism, pubertal delay, genetic-basis, gonadotropin-deficiency, Diabetes and Metabolism, Phenotype, Italy, Cohort, Female, complex, Cohort study, Human, Adult, medicine.medical_specialty, Adolescent, Gonadotropins, Humans, Hypogonadism, Obesity, Overweight, Pituitary Hormones, Young Adult, 030209 endocrinology & metabolism, NO, 03 medical and health sciences, Hypogonadotropic hypogonadism, Adolescent, Adult, Age of Onset, Cohort Studies, Female, Gonadal Steroid Hormones, Gonadotropins, Humans, Hypogonadis, Italy, Male, Obesity, Olfaction Disorders, Overweight, Phenotype, Pituitary Hormones, Synkinesis, Young Adult, Endocrinology, Diabetes and Metabolism, Endocrinology, Internal medicine, medicine, Isolated hypogonadotropic hypogonadism, Kallmann syndrome, Observational cohort study, gnrh deficiency, disease, business.industry, Settore MED/13 - ENDOCRINOLOGIA, isolated Hypogonadotropic hypogonadism, kallmann syndrome, medicine.disease, body regions, 030104 developmental biology, Sex steroid, linked kallmann-syndrome, heterogeneity, phenotype, Observational cohort study, Synkinesi, Age of onset, Cohort Studie, business
Abstract

Objective Isolated hypogonadotropic hypogonadism (IHH) is a rare disorder with pubertal delay, normal (normoosmic-IHH, nIHH) or defective sense of smell (Kallmann syndrome, KS). Other reproductive and non-reproductive anomalies might be present although information on their frequency are scanty, particularly according to the age of presentation. Design Observational cohort study carried out between January 2008 and June 2016 within a national network of academic or general hospitals. Methods We performed a detailed phenotyping of 503 IHH patients with: (1) manifestations of hypogonadism with low sex steroid hormone and low/normal gonadotropins; (2) absence of expansive hypothalamic/pituitary lesions or multiple pituitary hormone defects. Cohort was divided on IHH onset (PPO, pre-pubertal onset or AO, adult onset) and olfactory function: PPO-nIHH (n = 275), KS (n = 184), AO-nIHH (n = 36) and AO-doIHH (AO-IHH with defective olfaction, n = 8). Results 90% of patients were classified as PPO and 10% as AO. Typical midline and olfactory defects, bimanual synkinesis and familiarity for pubertal delay were also found among the AO-IHH. Mean age at diagnosis was significantly earlier and more frequently associated with congenital hypogonadism stigmata in patients with Kallmann’s syndrome (KS). Synkinesis, renal and male genital tract anomalies were enriched in KS. Overweight/obesity are significantly associated with AO-IHH rather than PPO-IHH. Conclusions Patients with KS are more prone to develop a severe and complex phenotype than nIHH. The presence of typical extra-gonadal defects and familiarity for PPO-IHH among the AO-IHH patients indicates a common predisposition with variable clinical expression. Overall, these findings improve the understanding of IHH and may have a positive impact on the management of patients and their families.

Published
2018

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