Language and Literacy in Turner Syndrome
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1 Language and Literacy in Turner Syndrome L Melissa M. Murphy, PhD Language problems can be associated with specific genetic syndromes, such as Klinefelter syndrome and fragile X syndrome, even in the absence of intellectual and developmental disabilities. Turner syndrome, a relatively common genetic disorder, is caused by the complete or partial absence of 1 of the 2 X chromosomes typically present in women. The syndrome is characterized by a distinct profile of physical and neuropsychological characteristics. The language characteristics of Turner syndrome have received considerably less attention than other cognitive domains, such as executive function and visual spatial ability. The present article focuses on describing the language and literacy characteristics associated with Turner syndrome, which are generally considered to be areas of relative strength. Related cognitive skills, such as executive function, and clinical implications are also discussed. Key words: executive function, genetic syndrome, language, literacy, Turner syndrome ANGUAGE PROBLEMS can be associated with specific genetic syndromes, such as Klinefelter syndrome and fragile X syndrome, even in the absence of intellectual and developmental disabilities. The study of language strengths and weaknesses associated with specific genetic disorders may inform professionals' understanding of both typical and atypical language development. Turner syndrome is a relatively common genetic disorder characterized by a distinct profile of physical and neuropsychological characteristics. In contrast to aspects of cognition, such as executive function and visual spatial ability, the language characteristics associated with Turner syndrome have received considerably less attention (Inozemtseva, Matute, Zarabozo, & Ramírez-Dueñas, 2002; Temple & Carney, 1996; Van Borsel, Dhooge, Verhoye, Derde, & Curfs, 1999). Following a brief review of Turner syndrome, the present article focuses on describing the language and liter- Autbor Affiliation: School of Education, College of Notre Dame of Maryland, Baltimore. Corresponding Author: Melissa M. Murphy, PhD, School of Education, College of Notre Dame of Maryland, 4701 North Charles St, Baltimore, MD (mmurphy@ndm.edu). acy characteristics associated with Turner syndrome. Related cognitive skills and clinical implications also are discussed. TURNER SYNDROME The prevalence of Turner syndrome is about 1:2,000 to 3,000 live female births (Davenport, Hooper, & Zegar, 2007). The syndrome is caused by the partial or complete loss of one of the two X chromosomes typically present in female individuals. The loss of the X chromosome occurs spontaneously (i.e., rather than being inherited). The absence of two X chromosomes in the female with Turner syndrome results in ovarian dysgenesis, which interferes with the ability of the ovaries to produce estrogen, a hormone that is associated with pubertal maturation (as reviewed by Ross, Roeltgen, Feuillan, Kushner, & Cutler, 2000a) and select aspects of cognitive function (Ross, 2005; Ross, Roeltgen, Feuillan, Kushner, & Cutler, 1998; Ross et al., 2000a). As with other genetic syndromes, it is important to recognize the considerable individual variability in the manifestation of the syndrome phenotype. However, there are core features of the phenotype that are quite common among affected individuals. 187
2 188 Classic physical characteristics include short stature, webbed neck, and broad chest. Although intellectual and developmental disabilities are not typically associated with Turner syndrome,* girls with this syndrome are at increased risk for learning disabilities, especially in mathematics. Full-scale IQ scores tend to be in the low average to average range (Mazzocco, 2001; Rovet, 1993; Rovet, Szekely, & Hockenberry, 1994; Tamm, Menon, & Reiss, 2003; Temple & Carney, 1993; Waber, 1979). Even with full-scale IQ scores in the average range, the syndrome is characterized by relative strengths in verbal abilities, with verbal IQ scores often exceeding performance IQ scores (as reviewed by Mazzocco, 2006). Areas of difficulty include mathematics achievement, executive function, processing speed, sustained attention, and visual spatial ability. (See Davenport et al., [2007] for additional information on Turner syndrome.) Together, the profile of strong verbal abilities coupled with weaker performance in specific cognitive domains has led to broad diagnoses such as "nonverbal learning disability." However, such labels may be misleading (Mazzocco, 2006). For example, speechlanguage difficulties (Van Borsel et al., 1999) and language impairments in oral fluency skills (Temple, 2002) and the use of syntactic structures (Inozemtseva et al., 2002) have been reported. Furthermore, difficulty in select cognitive domains, such as mathematics, executive function, and visual spatial ability, may reflect specific rather than widespread difficulties (Mazzocco, 2006). The following sections address what is known about literacy and language in Turner syndrome. Literacy skills are considered separately from spoken language. In an effort to reflect the complexity of language, the latter topic will be divided into sections reflecting speech characteristics, knowledge of words and their meaning (semantic or vocabulary * A small number of cases of Turner syndrome have a ring chromosome karyotype, which is associated with intellectual and developmental disabilities. skills), understanding of the rules for combining words to form phrases and sentences (syntactic skills), and oral expression. Table 1 summarizes strengths and challenges in specific aspects of language among girls with Turner syndrome. LITERACY AND LANGUAGE Literacy Reading The general consensus across several studies is that reading is an area of strength for girls with Turner syndrome (Alexander & Money, 1965; Rovet, 1993; Temple & Carney, 1996). Achievement in reading is at or above age level for the majority of girls with Turner syndrome (Alexander & Money, 1965; Temple, 2006; Temple & Carney, 1996). Many of the component processes required for reading, such as phonological processing and decoding skills, also are at or above the appropriate range for a given age (Mazzocco, 2001; Murphy & Mazzocco, 2008; Murphy, Mazzocco, Gerner, & Henry, 2006). Consistent with the notion of superior reading skills, Murphy and Mazzocco (2008) found no differences in reading speed, fluency, and accuracy between fifth-grade girls with Turner syndrome and their peers after matching for IQ. Similarly, Temple and Carney (1996) reported that 8- to 12-year-old girls with Turner syndrome score at or above their predicted reading age on text reading, single word reading (regular and irregular), and infrequent word reading (akin to reading nonwords). However, weaknesses in reading achievement, decoding ability, and word identification have been reported (Ross & Zinn, 1999; Rovet, 1993). Although findings generally support the notion of strength in word knowledge and phonological reading skills among girls with Turner syndrome, it is important to recognize that there are areas of relative weakness and variability in the extent to which each individual child may manifest specific phenotypic characteristics.
3 189 Successful reading requires comprehension of what has been read as well as the ability to recognize words. Possible difficulties with reading comprehension have been reported (Pennington, Bender, Puck, Salbenblatt, & Robinson, 1982; Rovet, 1993); however, the findings are inconsistent. For example, Alexander and Money (1965) found that about half of the girls they studied had reading comprehension scores below age level. In contrast, Temple and Carney (1996) report an advantage on reading comprehension for girls with Turner syndrome relative to their peers. Possible reasons for these inconsistent findings are discussed subsequently. Writing Limited information is available about writing in Turner syndrome; however, writing skills represent an area of parental concern
4 190 (Rovet, 1993). Consistent with reading, spelling ability appears to be in the average range for a given age (Rovet, 1993). No studies of written composition were found. Hearing Ear infections and hearing loss are frequently associated with Turner syndrome and may have an effect on speech and language development (Clark, 1989; Gungör, Böke, Belgin, & Turçbilek, 2000; Van Borsel et al., 1999). Gungör et al. (2000) documented a history of middle ear infections among more than half (68%) of the individuals with Turner syndrome ages 6-38 years they studied, with about a quarter of participants reporting persistent ear infections (Gungör et al., 2000). About a third of the 38 participants reported hearing loss at the time of evaluation, and no participants had normal hearing in both ears for the full range of audible frequencies. Conductive hearing loss within the speech frequency range (500-2,000 Hz) varied from mild to severe across left and right ears, with the majority of participants experiencing some type of hearing loss in at least one ear. At high frequencies (8-18 khz), hearing loss was observed in almost all cases (~99%). Although outside the typical speech frequency range, hearing in the high-frequency range may be important for speech perception amid significant background noise (Gungör et al., 2000). Language Speech-language The prevalence, extent, and nature of speech-language difficulties in Turner syndrome have received only cursory attention, which may be due partially to a lack of overt language deficits and average verbal IQ scores among persons with Turner syndrome. Clinical reports suggest that speech-language difficulties associated with the syndrome may be common but subtle (Jung, 1989). Consistent with this notion, Van Borsel et al. (1999) reported that about a quarter of 128 participants with Turner syndrome in their research were receiving or had received treatment for speech-language concerns. Articulation diffi- culties, delayed language development, and stuttering were the main reasons for receiving therapy, suggesting that attention to speechlanguage concerns in Turner syndrome may be important. However, these results must be interpreted with caution due to the lack of a comparison group and the use of a clinically based sample of participants who were being seen for head and neck abnormalities. Receptive and expressive language Vocabulary Overall, vocabulary skills appear to represent an area of strength in Turner syndrome (Temple, 2002). Word knowledge and receptive vocabulary of girls with Turner syndrome is generally well within the average range (Rae et al., 2004; Temple, 2002). In addition, girls with Turner syndrome have been reported to have a greater understanding and knowledge of low frequency vocabulary words (e.g., protractor) than their age-matched peers in the general population (Temple, 2002). Of note is that the small sample sizes in most studies and wide range of individual variability limit the interpretability and generalizability of findings. For example, Temple (2002) reported no differences in naming ability (as measured by the Boston Naming Test) between 10 girls with Turner syndrome (ages 9-12 years, M 10 years) and a comparison group of girls from the general population; whereas Rae et al. (2004) reported lower scores on the Boston Naming Test for nine girls with Turner syndrome (ages 8-12 years, M 10 years) relative their comparison group. Despite strong vocabulary skills, impairments in verbal fluency have been reported among girls with Turner syndrome relative to age-matched peers (Rae et al., 2004; Romans, Roeltgen, Kushner, & Ross, 1997; Temple, 2002; Temple & Carney, 1996). For example, girls with Turner syndrome produce significantly fewer words than their peers when asked to recall words beginning with a specific letter (e.g., "g"). Such impairments are not attributable to inadequate number of
5 191 words in the lexicon or to difficulty accessing the stored lexical information (Temple, 2002). Instead, qualitative differences in the types of words retrieved and number of errors made suggest the use of atypical strategies when retrieving words (Temple, 2002). Syntax Minimal information is available concerning the specific syntactic processing skills of girls with Turner syndrome. Again, lack of attention to this language domain may reflect the relative strengths in verbal IQ typically associated with Turner syndrome. Results from the studies that specifically examine syntactic processing are inconsistent. Rovet and Netley (1982) reported no differences between adolescent girls with Turner syndrome and ageand verbal IQ-matched peers in accuracy on a sentence judgment task that required judging the accuracy of a sentence in relation to a picture. This pattern of results was replicated in a pair of dizygotic twins, only one of whom had Turner syndrome. Consistent with these results, syntactic complexity of utterances (as measured by mean length of utterance) measured in an expressive language sample does not appear to distinguish girls with Turner syndrome from their peers (Temple, 2002). In contrast, accuracy differences on a syntactic processing task were observed by Inozemetseva et al. (2002). This group reported that adolescent girls with Turner syndrome had difficulty processing complex syntactic structures relative to age, grade, and socioeconomic status-matched peers, especially when the syntactic structures involved spatial information, such as describing the location of an object relative to other objects. However, the methods of this study are not well specified. The exclusive reliance on experimenterdesigned measures of syntactic processing in this study with no reported reliability or validity information makes it difficult to determine the precise nature of the observed syntactical difficulties and how the findings compare to those of others (e.g., Rovet & Netley, 1982; Temple, 2002). Oral expression Despite evidence of deficits in executive function, which may affect language development, almost no information exists on language use in contexts such as conversing about familiar topics or narrating a story. Two studies involving oral expression have provided mixed results. Language use during initial social interactions with an unfamiliar interlocutor does not distinguish girls with Turner syndrome from age-matched peers (Mazzocco et al., 2006), nor are expressive language differences apparent on narrative tasks such as describing a picture or explaining how to organize a party (Temple, 2002). On these narrative tasks no differences in narrative length (as measured by total number of utterances), word count, or the syntactic complexity of utterances (as measured by mean length of utterance) have been reported between girls with Turner syndrome and their peers (Temple, 2002). In the same narrative study, Temple (2002) reported differences between girls with Turner syndrome and their peers when detailing the events of the prior day. These narratives were significantly shorter both in terms of word count and total number of utterances among girls with Turner syndrome relative to peers. It is difficult to assess the extent to which executive function demands (specifically temporal vs. planning demands) or impairments in episodic memory may account for the differences recounting events versus describing a picture or explaining how to do something (Temple, 2002). However, as discussed subsequently, further examination of the language ability of individuals with Turner syndrome may provide important insight into the contributions of executive function to language learning and use. THE CONTRIBUTION OF COGNITION TO LANGUAGE DEVELOPMENT Apart from reading ability, overall language ability has received considerably less attention than other aspects of neuropsychological
6 192 function, such as executive function and visual spatial ability. Lack of attention to language reflects, in part, perceived strengths in reading and vocabulary skills. However, the limited evidence available suggests that language ability and development, particularly in the areas of oral narration and pragmatics, warrant additional attention. Impairments in selected aspects of executive function are well documented in Turner syndrome as reviewed by Mazzocco and Mc- Closkey (2005) and Murphy and Mazzocco (2008). Deficits have been reported on working memory tasks that require inhibition (Kirk, Mazzocco, & Kover, 2005), such as the Stroop task. Also reported are poor verbal fluency skills, such as quickly naming phonologically related items (e.g., words beginning with the letter "A"; Temple, 2002). However, not all aspects of executive function are impaired; goal-oriented planning and organizing skills are intact (Temple, 2002; Temple, Carney, & Mullarkey, 1996). For example, impairments are not reported on tasks that do not require rapid (or timed) responses, such as the Wisconsin Card Sort. Thus, performance difficulties may be limited to, or magnified by, tasks that require rapid responses or overt timing (Murphy & Mazzocco, 2008; Rovet et al., 1994). Executive functions are implicated in complex language activities, such as engaging in conversation, narrating a story, monitoring comprehension, and using a full range of writing processes. Select deficits in language use may arise as a result of impairments in executive function. For example, poor inhibition may contribute to difficulty with topic maintenance. Similarly, slowed processing speed may pose a challenge during conversation, a task that requires completing several tasks online simultaneously. At present, a detailed understanding of the language characteristics associated with Turner syndrome is lacking, making it difficult to assess specific cognitive contributions to language development. What is known is that girls with Turner syndrome are vulnerable to difficulty in social functioning (Ross, Zinn, & McCauley, 2000b), which requires, in part, both language and cognitive skills. For example, girls with Turner syndrome engage in fewer social activities and have fewer friends than their peers (McCauley, Kay, Ito, & Treder, 1987). Other reports suggest social discomfort (Keysor, Mazzocco, McLeod, & Hoehn-Saric, 2002), shyness and inhibition, and difficulty expressing emotions, especially during adolescence (Rovet, 2004). In addition, difficulties are reported in select aspects of social cognition, such as face processing (Lawrence et al., 2003a) and judging mental states (Lawrence, Kuntsi, Coleman, Campbell, & Skuse, 2003b) that may contribute to social interaction. Exploring the specific language characteristics in Turner syndrome and their relation to executive function and social cognition may provide information about the cognitive contributions to language development or at least help further characterize the complexity of language and cognition. CLINICAL IMPLICATIONS Among individuals with Turner syndrome as a group, difficulties in specific areas of language are apparent despite average verbal IQ scores and age-appropriate reading levels. Moreover, impairments in executive processes related to language suggest that complex language activities, such as narration and conversation, may be challenging for some individuals with Turner syndrome. Together, the cognitive and linguistic profile associated with Turner syndrome in general suggests a number of implications for parents and professionals. First, it may be important to distinguish between literacy (e.g., reading) and language skills (e.g., oral expression) when assessing verbal ability among persons with Turner syndrome. Relative strengths in reading and vocabulary skills may not reflect a global strength in language but rather may mask difficulty with specific complex language tasks. Moreover, assessing language ability across multiple contexts (e.g., conversation and narration) rather than in a single context will provide a detailed profile of language ability.
7 193 Second, understanding the profile of both cognitive and linguistic abilities associated with Turner syndrome may have important implications for intervention. For example, addressing limitations in executive function skills, such as poor inhibition, may be helpful for strengthening language, especially oral expression skills. Reinforcing metacognitive skills, such as monitoring comprehension and reviewing-revising written work, may also lead to improvements in overall communication skills. At the same time, relative strengths in language and literacy may provide a means by which to help practice and strengthen cognitive and social cognitive skills. For example, reading a story and discussing what each character knows, thinks, and feels, uses strengths in reading to promote social cognitive skills. Third, additional research is required to describe the nature and extent of the language difficulties in Turner syndrome across the life span, especially in the areas of language learning and use. Although the general consensus across studies supports strength in verbal skills in Turner syndrome, findings across studies are sometimes inconsistent and do not reflect a developmental perspective on how language characteristics may change over time. The reasons for these inconsistencies are unclear. Small sample sizes, varied comparison groups (e.g., age-matched vs. IQmatched), and overreliance on clinic-based samples across studies may contribute to in- consistent findings (Ross et al., 2000b). Alternatively, inconsistent findings may reflect differences in cognitive demands across tasks or the wide range of individual variability associated with the syndrome. CONCLUSION Even among individuals with a shared etiology, as in Turner syndrome, it is important to recognize that there is variability in the extent to which each individual child may manifest specific phenotypic characteristics and that the manifestation of these characteristics may change over the course of development. Among individuals with Turner syndrome, individual differences may arise as a result of factors such as varied environments, amount of estrogen production, and differences arising as a function of whether the retained X chromosome is maternal or paternal in origin (parental imprinting; Ross & Zinn, 1999). Regardless of the source (or sources) of individual differences, clinicians, educators, parents, and other professionals who work with persons with Turner syndrome should recognize that each individual may vary in her specific profile of strengths and challenges. Thus, assessment and intervention efforts should be guided by the specific psycho-educational profile of the individual child rather than phenotypic characteristics associated with the syndrome as a whole. REFERENCES
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