International Journal of Pediatric Otorhinolaryngology 78 (2014) 530–537
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Theory-of-mind in adolescents and young adults with Alstro¨m syndrome Hans Erik Fro¨lander a,b,e,g,*, Claes Mo¨ller a,b,c,e,f, Jan D. Marshall h, Annette Sundqvist d,e,f, Berit Ro¨nna˚sen a,b,e,g, Lil Falkensson i, Bjo¨rn Lyxell d,e,f Health Academy, O¨rebro University, O¨rebro SE 701 82, Sweden Audiological Research Centre, O¨rebro University Hospital, O¨rebro SE 701 85, Sweden c Department of Audiology, O¨rebro University Hospital, O¨rebro SE 701 85, Sweden d Department of Behavioral Science and Learning, Linko¨ping University, Linko¨ping SE 581 83, Sweden e The Swedish Institute for Disability Research, Linko¨ping, Sweden f The Linnaeus Centre HEAD, Linko¨ping, Sweden g Research on Hearing and Deafness (HEAD) Graduate School, Linko¨ping, Sweden h The Jackson laboratory, Bar Harbor, ME, USA i The Swedish National Expert Team for the Diagnoses of Deafblindness, National Resource Centre, Lund, SE 223 50, Sweden a
b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 1 October 2013 Received in revised form 19 December 2013 Accepted 20 December 2013 Available online 9 January 2014
Objective: The study focuses on theory-of-mind in adolescents and young adults with Alstro¨m syndrome (ALMS). ALMS, an autosomal recessive syndrome causes juvenile blindness, sensorineural hearing loss, cardiomyopathy, endocrinological disorders and metabolic dysfunction. Theory-of-mind (ToM) refers to the ability to impute mental states to one self and to others. Clinical observations have revealed an increased occurrence of deviances in mental state understanding in ALMS. In the present study ToM will be examined and related to working memory (WM), verbal ability and sensory loss. Methods: Twelve young individuals (16–37 years) with ALMS and 24 nondisabled individuals matched on age, gender and educational level participated. ToM was assessed by means of a multiple task that taxes the ability to understand thoughts and feelings of story characters’. WM was examined by means of a reading span task and verbal ability by means of a vocabulary test. Results: The ALMS group performed at significantly lower levels in ToM tasks and displayed a higher variability in performance than the control group. Individuals with ALMS and a relatively poor level performance provided fewer correct mental state inferences in ToM tasks than ALMS individuals with relatively higher performance levels. ALMS individuals with relatively high performance levels made as many correct inferences in ToM tasks as the control group, but their inferences were more often incomplete. Vocabulary skills and educational level, but not WM-capacity predicted ToM performance. Degree of deafblindness did not have an impact on ToM. Age of onset of visual loss but not hearing loss related to ToM. Conclusions: The individuals with ALMS display a high degree of heterogeneity in terms of ToM, where some individuals reached performance levels comparable to nondisabled individuals. The results are discussed with respect to how cognitive and verbal abilities and factors related to the disability affect ToM. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Alstro¨m syndrome (ALMS) Deafblindness Theory-of-mind Working memory Verbal ability Dual sensory loss
1. Introduction The structure of the human brain reflects the cognitive demands of living in bonded social groups. Development of an
¨ rebro University, School of Health and Medical * Corresponding author at: O ¨ rebro, Sweden. Tel.: +46104735458. Sciences, Fakultetsgatan 1, 70112 O E-mail addresses: [email protected], [email protected] (H.E. Fro¨lander). 0165-5876/$ – see front matter ß 2014 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijporl.2013.12.038
ability to understand mental states is indispensable to our species [1]. Theory-of-mind (ToM) refers to the capacity to impute mental states to self and to others [2]. Mental states have been suggested to develop through reorganizations of thoughts, based on input from others within the social environment [3,4]. ToM has also been described as a basic innate biological ability merely triggered by the environment [5–7]. Deficiency in ToM is the core and universal trait of Autism spectrum disorders (ASD) [5,8]. There is a high degree of heterogeneity among individuals with ASD, but even individuals with high functioning forms remain socially disabled [9].
H.E. Fro¨lander et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 530–537
Deficiencies are also found in different syndromal populations with an atypical development, such as individuals with Downs syndrome [10], Fragile X syndrome [11,12], Williams syndrome [13], and CHARGE syndrome [14]. The purpose of the present study is to examine the development of ToM in individuals with Alstro¨m syndrome (ALMS) and how it is related to sensory loss and development of working memory capacity and verbal ability. ALMS is an autosomal recessive single gene disorder, causing a severe progressive combined auditory and visual impairment. ALMS is, thus, an acquired deafblindness [15]. Deafblindness is predominantly genetic, and more than 50 hereditary syndromes cause acquired deafblindness [16]. The prevalence of deafblindness has been estimated to be 14/100 000 persons [17], whereas ALMS has a prevalence of less than one per million [18]. ALMS is characterized by a progressive development of multi-systemic pathology. Sensorineural hearing loss with a varied age of onset slowly develops in the first decade, and usually progresses to moderate or severe hearing loss in the following decades. Otitis media is frequent, causing additive conductive loss. With better medical care and prolonged life span it is obvious that the hearing loss in patients over 30 years of age is profound with a need for Cochlear implant (CI). Visual loss progresses much more rapidly than hearing loss. Although there is some variability in age of onset, dysfunction is typically demonstrated within a few weeks after birth. Retinal dystrophy leads to Retinitis pigmentosa (RP) and juvenile blindness in 90% by age of 16. Cone dystrophy occurs first, so visual experience in early childhood primarily comes from rods which are responsible for peripheral and night vision [18]. ALMS mimics the metabolic syndrome with obesity, insulin resistance, type II diabetes mellitus and hypertriglyceridemia. There is a high incidence of additional multiple endocrine abnormalities, cardiomyopathy, pulmonary fibrosis, restrictive lung disease, progressive hepatic and renal failure leading to a reduced life expectancy [19]. ALMS is a unique condition that may highlight mechanisms of importance in the development of ToM. It is reasonable to assume that a dual sensory impairment will have an impact on sociocognitive development [20]. However, few studies have investigated this issue in populations of children and adults with deafblindness. Families and professionals observing individuals with ALMS describe difficulties in understanding mental states of others. Autism spectrum behaviors have been reported in individuals with ALMS [19]. Studies of children with congenital deafness or blindness, have pointed out that lack of sensory and social exposure may be responsible for a delayed development of ToM [21–24] [25]. The impairment as such – more than the severity – has an impact on ToM. Deaf children with CI or hearing aids are as delayed in ToM as late signing deaf children [26], and children with severe visual impairment are as delayed in ToM as children with blindness [22]. In addition, the cumulative consequences of dual loss must be taken in account. The impact of two sensory impairments together is multiplied and intensified [15]. A cognitive impairment or delay is generally not an observed feature in ALMS, although a minority of the population has an intellectual disability [27,28]. However mild to moderate delay in
531
early receptive language is seen in many children with ALMS [28,29]. Previous studies have demonstrated that working-memory capacity (WMC) contributes to the development of ToM in children and adolescents with a typical development [30–35]. Working memory capacity in ALMS has not previously been examined and the relation between WMC and ToM in this population remains, thus, to be solved. WMC refers to the capacity to hold and process information over a short period of time [36] and moderates the extent to which the own knowledge is attributed to others’ mental states in individuals’ with typical development [37]. A certain level of WMC is necessary to develop ToM, but beyond a critical level may not cause further improvement to ToM [38]. The development of cognitive skills is closely interconnected to development of language skills [39], and ToM is linked to general verbal ability [40]. This might serve as one explanation why adults with developmental language disorders in childhood perform poorly on tasks that assess various aspects of ToM [41]. Understanding of mental states necessitates an understanding of the meaning of words [42]. This is exemplified by the observation that deaf children with signing skills acquired later in life have delayed ToM, in contrast to native signers with signing parents [43]. In addition interpersonal experiences from early years predict mental state reasoning in deafness [44], and also relate to mental state reasoning in blindness [24]. Clinical observations reveal a higher frequency of deviations from a typical trend of development of ToM in individuals with ALMS. In the present study we will examine ToM in ALMS in comparison to individuals with normal hearing and vision. We will explore how verbal ability, working memory capacity and onset and degree of sensory loss may contribute to this development. 2. Method 2.1. Participants Twelve young adults with ALMS in the age from 16 to 37 years (six females) participated in the study. All had moderate to severe sensorineural hearing loss. The visual impairment varied from severe impairment to blindness without residual sight. All participants were native English speakers. Nine of them were from the USA, two from the UK and one from the SAR. None of the participants had any additional disability that would affect their performance in the tasks used in the study. Background-information was obtained from medical records and responses to the Alstro¨m Syndrome International questionnaire [45] (Table 1). Hearing impairment (HI) was categorized according to WHO recommendations in four categories; profound (>81 dB better ear), severe (61–80 dB better ear), moderate (41–60 dB better ear) and mild (26–40 dB better ear) [46]. Visual impairment (VI) was categorized into five categories; blindness (no light perception), nearblindness (light perception), profound (visual acuity worse than 20/400), severe (visual acuity worse than 20/200) and moderate (visual acuity worse than 20/70) VI [46]. The score on HI and VI were added to achieve a combined degree of deafblindness (range 2–9) [47]. Data on onset of hearing
Table 1 Participant characteristics (mean sd) for nondisabled individuals (n = 24), individuals with ALMS (n = 12), individuals with ALMS and better ToM (n = 6), and individuals with ALMS and poorer ToM (n = 6).
Age (year) Gender Onset hearing impairment (months) Onset visual impairment (months)
Nondisabled
ALMS
p
ALMS better ToM
ALMS poorer ToM
p
27.9 (4.4) 24 (12 females)
26.7 (6.5) 12 (6 females) 8.9 (6.7) 8.1 (13.4)
ns
29.5 (6.9) 6 (4 females) 5.8 (3.7) 7.7 (4.3)
23.8 (5.1) 6 (2 females) 12.4 (8.8) 0.6 (1.3)
ns ns
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Theory-of-mind in adolescents and young adults with Alstro¨m syndrome Hans Erik Fro¨lander a,b,e,g,*, Claes Mo¨ller a,b,c,e,f, Jan D. Marshall h, Annette Sundqvist d,e,f, Berit Ro¨nna˚sen a,b,e,g, Lil Falkensson i, Bjo¨rn Lyxell d,e,f Health Academy, O¨rebro University, O¨rebro SE 701 82, Sweden Audiological Research Centre, O¨rebro University Hospital, O¨rebro SE 701 85, Sweden c Department of Audiology, O¨rebro University Hospital, O¨rebro SE 701 85, Sweden d Department of Behavioral Science and Learning, Linko¨ping University, Linko¨ping SE 581 83, Sweden e The Swedish Institute for Disability Research, Linko¨ping, Sweden f The Linnaeus Centre HEAD, Linko¨ping, Sweden g Research on Hearing and Deafness (HEAD) Graduate School, Linko¨ping, Sweden h The Jackson laboratory, Bar Harbor, ME, USA i The Swedish National Expert Team for the Diagnoses of Deafblindness, National Resource Centre, Lund, SE 223 50, Sweden a
b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 1 October 2013 Received in revised form 19 December 2013 Accepted 20 December 2013 Available online 9 January 2014
Objective: The study focuses on theory-of-mind in adolescents and young adults with Alstro¨m syndrome (ALMS). ALMS, an autosomal recessive syndrome causes juvenile blindness, sensorineural hearing loss, cardiomyopathy, endocrinological disorders and metabolic dysfunction. Theory-of-mind (ToM) refers to the ability to impute mental states to one self and to others. Clinical observations have revealed an increased occurrence of deviances in mental state understanding in ALMS. In the present study ToM will be examined and related to working memory (WM), verbal ability and sensory loss. Methods: Twelve young individuals (16–37 years) with ALMS and 24 nondisabled individuals matched on age, gender and educational level participated. ToM was assessed by means of a multiple task that taxes the ability to understand thoughts and feelings of story characters’. WM was examined by means of a reading span task and verbal ability by means of a vocabulary test. Results: The ALMS group performed at significantly lower levels in ToM tasks and displayed a higher variability in performance than the control group. Individuals with ALMS and a relatively poor level performance provided fewer correct mental state inferences in ToM tasks than ALMS individuals with relatively higher performance levels. ALMS individuals with relatively high performance levels made as many correct inferences in ToM tasks as the control group, but their inferences were more often incomplete. Vocabulary skills and educational level, but not WM-capacity predicted ToM performance. Degree of deafblindness did not have an impact on ToM. Age of onset of visual loss but not hearing loss related to ToM. Conclusions: The individuals with ALMS display a high degree of heterogeneity in terms of ToM, where some individuals reached performance levels comparable to nondisabled individuals. The results are discussed with respect to how cognitive and verbal abilities and factors related to the disability affect ToM. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Alstro¨m syndrome (ALMS) Deafblindness Theory-of-mind Working memory Verbal ability Dual sensory loss
1. Introduction The structure of the human brain reflects the cognitive demands of living in bonded social groups. Development of an
¨ rebro University, School of Health and Medical * Corresponding author at: O ¨ rebro, Sweden. Tel.: +46104735458. Sciences, Fakultetsgatan 1, 70112 O E-mail addresses: [email protected], [email protected] (H.E. Fro¨lander). 0165-5876/$ – see front matter ß 2014 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijporl.2013.12.038
ability to understand mental states is indispensable to our species [1]. Theory-of-mind (ToM) refers to the capacity to impute mental states to self and to others [2]. Mental states have been suggested to develop through reorganizations of thoughts, based on input from others within the social environment [3,4]. ToM has also been described as a basic innate biological ability merely triggered by the environment [5–7]. Deficiency in ToM is the core and universal trait of Autism spectrum disorders (ASD) [5,8]. There is a high degree of heterogeneity among individuals with ASD, but even individuals with high functioning forms remain socially disabled [9].
H.E. Fro¨lander et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 530–537
Deficiencies are also found in different syndromal populations with an atypical development, such as individuals with Downs syndrome [10], Fragile X syndrome [11,12], Williams syndrome [13], and CHARGE syndrome [14]. The purpose of the present study is to examine the development of ToM in individuals with Alstro¨m syndrome (ALMS) and how it is related to sensory loss and development of working memory capacity and verbal ability. ALMS is an autosomal recessive single gene disorder, causing a severe progressive combined auditory and visual impairment. ALMS is, thus, an acquired deafblindness [15]. Deafblindness is predominantly genetic, and more than 50 hereditary syndromes cause acquired deafblindness [16]. The prevalence of deafblindness has been estimated to be 14/100 000 persons [17], whereas ALMS has a prevalence of less than one per million [18]. ALMS is characterized by a progressive development of multi-systemic pathology. Sensorineural hearing loss with a varied age of onset slowly develops in the first decade, and usually progresses to moderate or severe hearing loss in the following decades. Otitis media is frequent, causing additive conductive loss. With better medical care and prolonged life span it is obvious that the hearing loss in patients over 30 years of age is profound with a need for Cochlear implant (CI). Visual loss progresses much more rapidly than hearing loss. Although there is some variability in age of onset, dysfunction is typically demonstrated within a few weeks after birth. Retinal dystrophy leads to Retinitis pigmentosa (RP) and juvenile blindness in 90% by age of 16. Cone dystrophy occurs first, so visual experience in early childhood primarily comes from rods which are responsible for peripheral and night vision [18]. ALMS mimics the metabolic syndrome with obesity, insulin resistance, type II diabetes mellitus and hypertriglyceridemia. There is a high incidence of additional multiple endocrine abnormalities, cardiomyopathy, pulmonary fibrosis, restrictive lung disease, progressive hepatic and renal failure leading to a reduced life expectancy [19]. ALMS is a unique condition that may highlight mechanisms of importance in the development of ToM. It is reasonable to assume that a dual sensory impairment will have an impact on sociocognitive development [20]. However, few studies have investigated this issue in populations of children and adults with deafblindness. Families and professionals observing individuals with ALMS describe difficulties in understanding mental states of others. Autism spectrum behaviors have been reported in individuals with ALMS [19]. Studies of children with congenital deafness or blindness, have pointed out that lack of sensory and social exposure may be responsible for a delayed development of ToM [21–24] [25]. The impairment as such – more than the severity – has an impact on ToM. Deaf children with CI or hearing aids are as delayed in ToM as late signing deaf children [26], and children with severe visual impairment are as delayed in ToM as children with blindness [22]. In addition, the cumulative consequences of dual loss must be taken in account. The impact of two sensory impairments together is multiplied and intensified [15]. A cognitive impairment or delay is generally not an observed feature in ALMS, although a minority of the population has an intellectual disability [27,28]. However mild to moderate delay in
531
early receptive language is seen in many children with ALMS [28,29]. Previous studies have demonstrated that working-memory capacity (WMC) contributes to the development of ToM in children and adolescents with a typical development [30–35]. Working memory capacity in ALMS has not previously been examined and the relation between WMC and ToM in this population remains, thus, to be solved. WMC refers to the capacity to hold and process information over a short period of time [36] and moderates the extent to which the own knowledge is attributed to others’ mental states in individuals’ with typical development [37]. A certain level of WMC is necessary to develop ToM, but beyond a critical level may not cause further improvement to ToM [38]. The development of cognitive skills is closely interconnected to development of language skills [39], and ToM is linked to general verbal ability [40]. This might serve as one explanation why adults with developmental language disorders in childhood perform poorly on tasks that assess various aspects of ToM [41]. Understanding of mental states necessitates an understanding of the meaning of words [42]. This is exemplified by the observation that deaf children with signing skills acquired later in life have delayed ToM, in contrast to native signers with signing parents [43]. In addition interpersonal experiences from early years predict mental state reasoning in deafness [44], and also relate to mental state reasoning in blindness [24]. Clinical observations reveal a higher frequency of deviations from a typical trend of development of ToM in individuals with ALMS. In the present study we will examine ToM in ALMS in comparison to individuals with normal hearing and vision. We will explore how verbal ability, working memory capacity and onset and degree of sensory loss may contribute to this development. 2. Method 2.1. Participants Twelve young adults with ALMS in the age from 16 to 37 years (six females) participated in the study. All had moderate to severe sensorineural hearing loss. The visual impairment varied from severe impairment to blindness without residual sight. All participants were native English speakers. Nine of them were from the USA, two from the UK and one from the SAR. None of the participants had any additional disability that would affect their performance in the tasks used in the study. Background-information was obtained from medical records and responses to the Alstro¨m Syndrome International questionnaire [45] (Table 1). Hearing impairment (HI) was categorized according to WHO recommendations in four categories; profound (>81 dB better ear), severe (61–80 dB better ear), moderate (41–60 dB better ear) and mild (26–40 dB better ear) [46]. Visual impairment (VI) was categorized into five categories; blindness (no light perception), nearblindness (light perception), profound (visual acuity worse than 20/400), severe (visual acuity worse than 20/200) and moderate (visual acuity worse than 20/70) VI [46]. The score on HI and VI were added to achieve a combined degree of deafblindness (range 2–9) [47]. Data on onset of hearing
Table 1 Participant characteristics (mean sd) for nondisabled individuals (n = 24), individuals with ALMS (n = 12), individuals with ALMS and better ToM (n = 6), and individuals with ALMS and poorer ToM (n = 6).
Age (year) Gender Onset hearing impairment (months) Onset visual impairment (months)
Nondisabled
ALMS
p
ALMS better ToM
ALMS poorer ToM
p
27.9 (4.4) 24 (12 females)
26.7 (6.5) 12 (6 females) 8.9 (6.7) 8.1 (13.4)
ns
29.5 (6.9) 6 (4 females) 5.8 (3.7) 7.7 (4.3)
23.8 (5.1) 6 (2 females) 12.4 (8.8) 0.6 (1.3)
ns ns
