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Olfactory Evaluation in Children: Application to the CHARGE Syndrome

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Olfactory Evaluation in Children: Application to the CHARGE Syndrome Olfactory Evaluation in Children: Application to the CHARGE Syndrome Christel Chalouhi, MD*; Patrick Faulcon, MD‡; Christine Le Bihan, MD§; Lucie Hertz-Pannier, MD, PhD࿣; Pierre Bonfils, MD, PhD‡; and Ve´ronique Abadie, MD, PhD* ABSTRACT. Objective. To find an efficient tool for ABBREVIATIONS. CHARGE, coloboma, congenital heart disease, testing olfactory function in children and use it to inves- choanal atresia, mental and growth retardation, genital anomalies, tigate a group of children with CHARGE (coloboma, and ear malformations and hearing loss; PEA, phenylethylalcohol. congenital heart disease, choanal atresia, mental and growth retardation, genital anomalies, and ear malforma- tions and hearing loss) syndrome. lfaction has always been and remains the Methods. We adapted for children an olfaction test most neglected sense in studies of child de- that had just been validated in an adult French popula- Ovelopment and behavior, the main reasons tion and investigated a control group of 25 healthy chil- being the poor knowledge concerning the role of dren aged 6 to 13 years. We then tested the olfactory olfaction in human development and behavior and capacity of a group of 14 children with CHARGE syn- the lack of available tools for investigating olfaction, drome, aged 6 to 18 years. A questionnaire was com- in particular in children. Development of the olfac- pleted with the parents about their children’s feeding tory system begins very early in the human embryo; difficulties and their ability to recognize odors in every- olfactory bulbs have their definitive structure at day day life. We recorded and scored the histories of feeding 56. Then, cells of the olfactory placode differentiate behavior anomalies, the visual and auditory status, and to gonadotropic cells and migrate to the hypotha- current intellectual levels. MRI of the olfactory tracts and lamic region along the terminal nerve (cranial nerve bulbs was analyzed for 9 of 14 children. 0), the olfactory nerve (cranial nerve 1), and the Results. We showed that healthy children have sim- ilar olfactory function to that of the adult control group, vomeronasal nerve. One part of the olfactory system which was representative of the general population, projects to the anterior part of the hypothalamus for without any difference for either gender or age. We also odor perception and discrimination; the other showed that all children with CHARGE syndrome had projects to the limbic system and the hippocampus olfactory deficiency. Half of them were anosmic, and the for the behavioral impact of olfaction and olfactory others had olfactory residual function (hyposmic). We emotional memory.1 The Jacobson vomeronasal or- found no association between olfactory deficiency and gan is a fetal structure that reduces after birth and feeding behavior, visual or auditory impairment, or in- that allows the transmission of odors through aque- tellectual level. Parental subjective evaluations were ac- ous middles, in particular amniotic fluid.2 Several curate for only half of the group. All of the MRIs showed data have shown that olfaction is functional during anomalies of the olfactory tracts and bulbs varying from prenatal life.3–6 At birth, newborns have highly effi- moderate hypoplasia to complete aplasia, without any cient olfactory abilities, allowing them to discrimi- relation between the radiologic and the functional re- nate the odor of their mother’s skin or milk from sults. those of other mothers7,8 and to modify their feeding Conclusions. Olfaction can be assessed in children, behavior according to the milk flavor.9,10 In mice, even the young and disabled. Our results support the proposition that rhinencephalon anomalies should be olfaction is crucial at birth to lead the pups to their included as a major criterion for the diagnosis of mother’s nipples, and anosmic mice die shortly after 11 CHARGE syndrome. Pediatrics 2005;116:e81–e88. URL: birth because they cannot find them. All of these www.pediatrics.org/cgi/doi/10.1542/peds.2004-1970; data suggest that human neonatal olfaction probably CHARGE syndrome, olfaction in children, olfactory defi- plays a role both in mother-child bonding and in ciency. newborns’ feeding behavior. During the first years of life, the role of olfaction is probably important, al- though few studies have demonstrated this, princi- From the *General Pediatrics Unit, §Pediatrics Radiology Unit, and ࿣Biosta- pally because olfaction evaluation is difficult in this tistics Unit, Hoˆpital Necker Enfants Malades, Paris, France; and ‡Depart- age range. Nevertheless, in a previous study, we ment of Otolaryngology Head Neck Surgery, Unite´Centre National de la showed that reproducible behavioral modifications Recherche Scientifique UPRESSA 7060, Hoˆpital Europeen Georges Pompi- (breathing rhythm, mobility, and sight) indicate that dou, Paris, France. Accepted for publication Nov 22, 2004. healthy infants and toddlers (3 months to 3 years) 12 doi:10.1542/peds.2004-1970 have good olfaction abilities. Several studies have No conflict of interest declared. shown that olfaction improves from the age when it Reprint requests to (V.A.) Hoˆpital Necker-Enfants Malades, 149 Rue de becomes testable (7–8 years of age) until the age of Se`vres, 75743 Paris Cedex 15, France. E-mail: [email protected] ϳ40 years.13–16 These observations may be attribut- hop-paris.fr PEDIATRICS (ISSN 0031 4005). Copyright © 2005 by the American Acad- able to the methods of olfaction testing and are dis- emy of Pediatrics. cussed later. After puberty, girls have better olfaction www.pediatrics.org/cgi/doi/10.1542/peds.2004-1970Downloaded from www.aappublications.org/news by guest PEDIATRICSon September 26,Vol. 2021 116 No. 1 July 2005 e81 abilities than boys.17,18 From the age of ϳ40 years, Patients With CHARGE Syndrome olfaction abilities decrease, which partly explains an- Fourteen children with CHARGE syndrome were included. orexia in the elderly.18 The role of olfaction in adults The group consisted of 8 girls aged 7.5 to 18 years (mean Ϯ SD: is likely involved in several fields, such as appetite, 12.5 Ϯ 4) and 6 boys aged 6 to 10 years (mean Ϯ SD: 7.8 Ϯ 1.4). The diagnosis of CHARGE syndrome was made according to Blake emotional memory, and sexual bonding. However, and Amiel’s criteria (5 major criteria or 4 major criteria and 3 few studies can prove these roles. Studies on behav- minor criteria30,31). We asked the families to participate when their ior in adults with olfaction disorders, in particular child had speech and mental age corresponding to a 5- or 6-year patients with Kallmann syndrome, are rare and do level. Their visual ability had to be good enough to allow them to not show major effects of hyposmia, suggesting that recognize drawings representing the odors on 10 10-cm pictures. Six patients had peripheral risk factors for olfaction deficit: pa- hyposmic patients compensate for their deficit by tients 2 and 3 had cleft lip and palate; patients 2, 3, 8, and 9 had other sensorial and cognitive means.19–21 Moreover, transient tracheostomy; and patients 5, 9, and 14 had unilateral in humans, especially in Western and so-called de- choanal atresia. Patient 14 had previously been tested with a veloped cultures, the sense of smell is not well taught different method. She was excluded from the results but included in the association calculation and the discussion. or stimulated. Parents and children of both groups all were volunteers for this CHARGE syndrome (coloboma, congenital heart prospective study. Consent of all of the families was obtained in disease, choanal atresia, mental and growth retarda- accordance with the ethics rules of our hospital. tion, genital anomalies, and ear malformations and hearing loss) is a congenital malformative picture Olfactory Tests that was described 25 years ago.22,23 In addition to The French Biolfa olfactory test, recently validated in healthy young adults, was adapted to children.29 The Biolfa test uses 2 the defects cited in the acronym, other anomalies series of 30-mL glass sniff bottles that contain odorous chemical have been described. Some of them have a high substances. The first series measure the olfactory thresholds of 3 frequency, such as vestibular anomalies, facial dys- different substances (eugenol, aldehyde C14, and phenyl ethyl morphism, asymmetrical facial palsy, and brainstem alcohol [PEA; quantitative trial]). The second series is an odor dysfunction, whereas others have a lower frequency, identification test to determine quality of olfactory function using a large panel of odors that are common to Southern European such as renal, esophageal, osseous, and cerebral mal- countries (qualitative trial). formations.24–26 Once the structural anomalies are repaired, children with CHARGE have to overcome Olfactory Thresholds multiple sensory impairments, such as visual, audi- The threshold test consisted of aqueous dilutions of 3 compo- tory, and balance impairments. Olfaction has never nents (eugenol, aldehyde C14, and PEA), the mean detection been investigated in patients with CHARGE syn- thresholds of which (0.5, 0.15, and 7.5 ppm, respectively) were published by the French Association for Normalization in 1989.32 drome, although several arguments suggest that ol- These concentrations defined the level 3 on the difficulty scale of faction dysfunction is crucial in this malformative 9 concentration levels used in the test (Table 1). The lowest con- condition. First, most children with CHARGE syn- centration at which 1 of these odors was detected was termed drome have initial, severe, and long-lasting feeding “detection threshold.” In each test, we asked the child which of 2 disorders that are poorly explained by their swallow- stimuli (an odor or a blank), presented sequentially and in random order, smelled stronger (the forced-choice procedure). The first ing disorders alone. Second, children with CHARGE test began at the third level of difficulty. When a child failed to syndrome may have genital anomalies as a result of detect an odor, the next test was performed at the next higher hypothalamic luteinizing hormone-releasing hor- concentration level.
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