Abstract
Background/objective
The olfactory bulb (OB) and pubertal development have a close relationship as they share a common ontogenetic origin. The aim of this study was to analyze the potential relationship between precocious puberty (PP) in girls as a sign of early pubertal timing and their OB volume as an indicator of its functional activity.
Design
In the study group (n = 125), OB volume, pituitary height (PH), body mass index (BMI) and body surface (S) variables were retrospectively investigated in 49 girls included in the PP group and 76 healthy girls constituting the control group. Volumetric and length measurements were performed on a magnetic resonance imaging (MRI) scan by using manual segmentation of slices.
Results
The mean OB volume (73.41 ± 17.21 mm3) and PH (4.96 ± 1.01 mm) were significantly higher in the PP group (p = 0.001 and p = 0.001, respectively). The mean volume difference between the right and left bulbs (1.52 ± 1.87) was higher in the PP group (p = 0.03). The body surface (1.05 ± 0.16 m2) was larger in the PP group (p = 0.09). There was a high correlation between the OB volume and PH (r125 = 0.716). There was a moderate correlation between the body surface and OB volume (r125 = 654), and a weak correlation between the former (S) and the PH (r125 = 452).
Conclusions
This study showed that there is a strong correlation between increased OB volume and PH in cases with PP. It indicates that increased OB volume may be a strong clue that olfactory functions play a role in pubertal timing in humans, although it does not show definitive proof of a causal relationship.
Acknowledgments
We would like to thank our colleagues for valuable advices and tecnical assistance.
Authors contributions: Murat Karaoglan participated in the design of the study, planned and thought the study; Hale Çolakoğlu Er measured the olfactory bulb volume and pituitary height on cranial MRI.
Research funding: None declared.
Employment or leadership: None declared.
Honorarium: None declared.
Competing interests: The authors declare that they have no competing interests.
References
1. Bear DM, Lassance JM, Hoekstra HE, Datta SR. The Evolving neural and genetic architecture of vertebrate olfaction. Curr Biol 2016;26:R1039–9.10.1016/j.cub.2016.09.011Search in Google Scholar PubMed PubMed Central
2. Donato Jr J, Elias CF. The ventral premammillary nucleus links metabolic cues and reproduction. Front Endocrinol (Lausanne) 2011;2:57.10.3389/fendo.2011.00057Search in Google Scholar PubMed PubMed Central
3. Kasumyan AO. The olfactory system in fish: structure, function, and role in behavior. J Ichthyol 2004;44(Suppl. 2):S180–223.Search in Google Scholar
4. Hughes GM, Teeling EC, Higgins DG. Loss of olfactory function in hominin evolution. PLoS One 2014;9:e84714.10.1371/journal.pone.0084714Search in Google Scholar PubMed PubMed Central
5. Wray S. From nose to brain: development of gonadotropin-releasing hormone-1 neurons. J Neuroendocrinol 2010;22:743–53.10.1111/j.1365-2826.2010.02034.xSearch in Google Scholar PubMed PubMed Central
6. Yoon H, Enquist LW, Dulac C. Olfactory inputs to hypothalamic neurons controlling reproduction and fertility. Cell 2005;123:669–82.10.1016/j.cell.2005.08.039Search in Google Scholar PubMed
7. Hochberg Z, Belsky J. Evo-devo of human adolescence: beyond disease models of early puberty. BMC Med 2013;11:113.10.1186/1741-7015-11-113Search in Google Scholar PubMed PubMed Central
8. Hochberg Z. Evo-devo of child growth III: premature juvenility as an evolutionary trade-off. Horm Res Paediatr 2010;73:430–7.10.1159/000282109Search in Google Scholar PubMed
9. Ellison PT, Reiches MW, Shattuck-Faegre H, Breakey A, Konecna M, et al. Puberty as a life history transition. Ann Hum Biol 2012;39:352–60.10.3109/03014460.2012.693199Search in Google Scholar PubMed
10. Lledo PM, Merkle FT, Alvarez-Buylla A. Origin and function of olfactory bulb interneuron diversity. Trends Neurosci 2008;31:392–400.10.1016/j.tins.2008.05.006Search in Google Scholar PubMed PubMed Central
11. Jouhanneau M, Szymanski LA, Keller M. Female puberty acceleration by male odour in mice: neural pathway and behavioural consequences. Biochem Soc Trans 2014;42:878–81.10.1042/BST20140048Search in Google Scholar PubMed
12. Szymanski LA, Keller M. Activation of the olfactory system in response to male odors in female prepubertal mice. Neurons. Behav Brain Res 2014;271:30–8.10.1016/j.bbr.2014.05.051Search in Google Scholar PubMed
13. Nummela S, Pihlström H, Puolamäki K, Fortelius M, Hemilä S, et al. Exploring the mammalian sensory space: co-operations and trade-offs among senses. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2013;199:1077–92.10.1007/s00359-013-0846-2Search in Google Scholar PubMed
14. Karaoglan M, Keskin M, Kul S, Ozkur A. A diagnostic scoring system to distinguish precocious puberty from premature thelarche based on clinical and laboratory findings. Iran J Pediatr 2018;28:e64118.10.5812/ijp.64118Search in Google Scholar
15. Doğan A, Bayar Muluk N, Şahan MH, Asal N, Inal M, et al. Olfactory bulbus volume and olfactory sulcus depth in migraine patients: an MRI evaluation. Eur Arch Otorhinolaryngol 2018;275:2005–11.10.1007/s00405-018-5029-xSearch in Google Scholar PubMed
16. Sarafoleanu C, Mella C, Georgescu M, Perederco C. The importance of the olfactory sense in the human behavior and evolution. J Med Life 2009;2:196–8.Search in Google Scholar PubMed
17. Bhutta MF. Sex and the nose: human pheromonal responses. J R Soc Med 2007;100:268–74. Review.10.1177/014107680710000612Search in Google Scholar PubMed PubMed Central
18. Asaba A, Hattori T, Mogi K, Kikusui T. Sexual attractiveness of male chemicals and vocalizations in mice. Front Neurosci 2014;8:231.10.3389/fnins.2014.00231Search in Google Scholar PubMed PubMed Central
19. D’Aniello B, Semin GR, Scandurra A, Pinelli C. The vomeronasal organ: a neglected organ. Front Neuroanat 2017;11:70.10.3389/fnana.2017.00070Search in Google Scholar PubMed PubMed Central
20. Hummel T, Smitka M, Puschmann S, Gerber JC, Schaal B, et al. Correlation between olfactory bulb volume and olfactory function in children and adolescents. Exp Brain Res 2011;214:285–291.10.1007/s00221-011-2832-7Search in Google Scholar PubMed
21. Rombaux P, Duprez T, Hummel T. Olfactory bulb volume in the clinical assessment of olfactory dysfunction. Rhinology 2009;47:3–9.Search in Google Scholar PubMed
22. Boehm U, Bouloux PM, Dattani MT, de Roux N, Dodé C, et al. Expert consensus document: European Consensus Statement on congenital hypogonadotropic hypogonadism–pathogenesis, diagnosis and treatment. Nat Rev Endocrinol 2015;11:547–64.10.1038/nrendo.2015.112Search in Google Scholar PubMed
23. MacColl G, Quinton R. Kallmann’s syndrome: bridging the gaps. J Pediatr Endocrinol Metab 2005;18:541–3.10.1515/JPEM.2005.18.6.541Search in Google Scholar PubMed
24. Bonomi M, Vezzoli V, Krausz C, Guizzardi F, Vezzani S, et al. Characteristics of a nationwide cohort of patients presenting with isolated hypogonadotropic hypogonadism (IHH). Eur J Endocrinol 2018;178:23–32.10.1530/EJE-17-0065Search in Google Scholar PubMed
25. Oboti L, Pérez-Gómez A, Keller M, Jacobi E, Birnbaumer L, et al. A wide range of pheromone-stimulated sexual and reproductive behaviors in female mice depend on G protein Gαo. BMC Biol 2014;12:31.10.1186/1741-7007-12-31Search in Google Scholar PubMed PubMed Central
26. Richardson HN, Nelson AL, Ahmed EI, Parfitt DB, Romeo RD, et al. Female pheromones stimulate release of luteinizing hormone and testosterone without altering GnRH mRNA in adult male Syrian hamsters (Mesocricetus auratus). Gen Comp Endocrinol 2004; 138:211–7.10.1016/j.ygcen.2004.06.008Search in Google Scholar PubMed
27. Leslie Cameron E. Olfactory perception in children. World J Otorhinolaryngol Head Neck Surg 2018;4:57–66.10.1016/j.wjorl.2018.02.002Search in Google Scholar PubMed PubMed Central
28. Oliveira-Pinto AV, Santos RM, Coutinho RA, Oliveira LM, Santos GB, et al. Sexual dimorphism in the human olfactory bulb: females have more neurons and glial cells than males. PLoS One 2014;9:e111733.10.1371/journal.pone.0111733Search in Google Scholar PubMed PubMed Central
29. Tither JM, Ellis BJ. Impact of fathers on daughters’ age at menarche: a genetically and environmentally controlled sibling study. Dev Psychol 2008;44:1409–20.10.1037/a0013065Search in Google Scholar PubMed
30. Prosser HM, Bradley A, Caldwell MA. Olfactory bulb hypoplasia in Prokr2 null mice stems from defective neuronal progenitor migration and differentiation. Eur J Neurosci 2007;26:3339–44.10.1111/j.1460-9568.2007.05958.xSearch in Google Scholar PubMed PubMed Central
31. Libri DV, Kleinau G, Vezzoli V, Busnelli M, Guizzardi F, et al. Germline prokineticin receptor 2 (PROKR2) variants associated with central hypogonadism cause differental modulation of distinct intracellular pathways. J Clin Endocrinol Metab 2014; 99:E458–63.10.1210/jc.2013-2431Search in Google Scholar PubMed
32. Garcia-Falgueras A, Junque C, Giménez M, Caldú X, Segovia S, et al. Sex differences in the human olfactory system. Brain Res 2006;1116:103–11.10.1016/j.brainres.2006.07.115Search in Google Scholar PubMed
33. Sharafuddin MJ, Luisiri A, Garibaldi LR, Fulk DL, Klein JB, et al. MR imaging diagnosis of central precocious puberty: importance of changes in the shape and size of the pituitary gland. AJR Am J Roentgenol 1994;162:1167–73.10.2214/ajr.162.5.8166005Search in Google Scholar PubMed
34. Bianco SD. A potential mechanism for the sexual dimorphism in the onset of puberty and incidence of idiopathic central precocious puberty in children: sex-specific kisspeptin as an integrator of puberty signals. Front Endocrinol (Lausanne) 2012;3:149.10.3389/fendo.2012.00149Search in Google Scholar PubMed PubMed Central
35. Pfister S, Weber T, Härtig W, Schwerdel C, Elsaesser R, et al. Novel role of cystic fibrosis transmembrane conductance regulator in maintaining adult mouse olfactory neuronal homeostasis. J Comp Neurol 2015;523:406–30.10.1002/cne.23686Search in Google Scholar PubMed
36. Gittleman JL. Carnivore olfactory bulb size: allometry, phylogeny and ecology. J Zool 1991;225:253–72.10.1111/j.1469-7998.1991.tb03815.xSearch in Google Scholar
37. Sorokowska A, Schriever VA, Gudziol V, Hummel C, Hähner A, et al. Changes of olfactory abilities in relation to age: odor identification in more than 1400 people aged 4 to 80 years. Eur Arch Otorhinolaryngol 2015;272:1937–44.10.1007/s00405-014-3263-4Search in Google Scholar PubMed PubMed Central
38. Corfield JR, Price K, Iwaniuk AN. Diversity in olfactory bulb size in birds reflects allometry, ecology, and phylogeny. Front Neuroanat 2015;9:102.10.3389/fnana.2015.00102Search in Google Scholar PubMed PubMed Central
© 2019 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Original Articles
- Association of the 3′UTR polymorphism (rs11665896) in the FGF21 gene with metabolic status and nutrient intake in children with obesity
- Future glycemic control of children diagnosed with type 1 diabetes mellitus at toddler and preschool/school age
- Children with type 1 diabetes of early age at onset – immune and metabolic phenotypes
- Determination of cerebral edema with serial measurement of optic nerve sheath diameter during treatment in children with diabetic ketoacidosis: a longitudinal study
- Association between inflammation, oxidative stress, vitamin D, copper and zinc with pre-obesity and obesity in school children from the city of Podgorica, Montenegro
- Phenotypic diversity and correlation with the genotypes of pseudohypoaldosteronism type 1
- Start low, go slowly – mental abnormalities in young prolactinoma patients under cabergoline therapy
- Primary ovarian insufficiency in an adolescent population: clinical phenotype and diagnostic approach
- Novel combined insulin-like 3 variations of a single nucleotide in cryptorchidism
- Evaluation of the abdominopelvic region using MRI in patients with primary amenorrhea
- Benefits of aerobic training in girls with precocious puberty: involvement of CRP and cortisol
- The relationship between the olfactory bulb and precocious puberty: from the nose to the pituitary
- Short Communication
- Experience with intramuscular glucagon for infants with early neonatal hypoglycemia
- Case Reports
- A novel GATA6 variant in a boy with neonatal diabetes and diaphragmatic hernia: a familial case with a review of the literature
- Nephrogenic diabetes insipidus in a 15-year-old Hispanic female with a novel AQP2 mutation
- Pediatric stroke as the presenting symptom of new-onset type 1 diabetes mellitus without DKA: case report and literature review
- Panhypopituitarism from neurosarcoidosis in an adolescent: case report and literature review
Articles in the same Issue
- Frontmatter
- Original Articles
- Association of the 3′UTR polymorphism (rs11665896) in the FGF21 gene with metabolic status and nutrient intake in children with obesity
- Future glycemic control of children diagnosed with type 1 diabetes mellitus at toddler and preschool/school age
- Children with type 1 diabetes of early age at onset – immune and metabolic phenotypes
- Determination of cerebral edema with serial measurement of optic nerve sheath diameter during treatment in children with diabetic ketoacidosis: a longitudinal study
- Association between inflammation, oxidative stress, vitamin D, copper and zinc with pre-obesity and obesity in school children from the city of Podgorica, Montenegro
- Phenotypic diversity and correlation with the genotypes of pseudohypoaldosteronism type 1
- Start low, go slowly – mental abnormalities in young prolactinoma patients under cabergoline therapy
- Primary ovarian insufficiency in an adolescent population: clinical phenotype and diagnostic approach
- Novel combined insulin-like 3 variations of a single nucleotide in cryptorchidism
- Evaluation of the abdominopelvic region using MRI in patients with primary amenorrhea
- Benefits of aerobic training in girls with precocious puberty: involvement of CRP and cortisol
- The relationship between the olfactory bulb and precocious puberty: from the nose to the pituitary
- Short Communication
- Experience with intramuscular glucagon for infants with early neonatal hypoglycemia
- Case Reports
- A novel GATA6 variant in a boy with neonatal diabetes and diaphragmatic hernia: a familial case with a review of the literature
- Nephrogenic diabetes insipidus in a 15-year-old Hispanic female with a novel AQP2 mutation
- Pediatric stroke as the presenting symptom of new-onset type 1 diabetes mellitus without DKA: case report and literature review
- Panhypopituitarism from neurosarcoidosis in an adolescent: case report and literature review