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Research Article                                                                                                                                        Open Access

## Underidentification of Autism Spectrum Disorder in Females: A Case Series Illustrating the Unique Presentation of this Disorder in Young Women

Andrea Trubanova * , Katharine Donlon, Nicole L. Kreiser, Thomas H. Ollendick, Susan W. White

Department of Psychology, Virginia Tech, Blacksburg, VA, USA

*Corresponding author:

atruban@vt.edu

## Abstract

Background: Autism spectrum disorder (ASD) is diagnosed more often in males than females, with the male-to-female gender ratio reported to be around 4.3:1 to 5:1. It is possible that the underrecognition of ASD in females partially contributes to this uneven ratio. Recent attention has been placed on understanding the processes that give rise to this gender difference in ASD prevalence. Socialization may contribute to the unique presentation of ASD in females, which may underlie this condition's subsequent underidentification in this group.

Objective :  The  purpose  of  this  case  series  is  to  demonstrate  how  symptoms  of  ASD  may  uniquely  manifest  in  females without co-occurring intellectual impairment.

Method :  An  examination of three case examples of young women diagnosed with ASD will illustrate the processes that contribute to the atypical manifestation and underidentification of ASD in females.

Results :  Across  cases,  the  females  in  this  study  demonstrated  shared  symptom  presentations  within  three  domains:  1) unique core symptom manifestation (insistence on sameness, lack of social engagement, and social processing difficulties); 2) heightened psychiatric comorbidities with internalizing disorders (anxiety, depression, and borderline personality traits); and 3) emotional dysregulation. These three domains reflect specific processes that may help to explain the underidentification of ASD in females via diagnostic overshadowing.

Conclusions :  Consideration  of  atypical  symptom  presentations,  heightened  comorbidities,  and  emotion  regulation difficulties may help with the understanding of why ASD symptoms in females are commonly underidentified or identified later  than  they  are  in  males.  Social  difficulties  in  combination  with  internalizing  psychiatric  disorders  and  emotional dysregulation may lead to the development of a specific symptom presentation in females that obscures the detection of ASD symptoms. Suggestions for clinical practice are made to promote the accurate identification of ASD and to inform case formulation and treatment planning.

Keywords:

females, autism, autism spectrum disorder, comorbidity, diagnosis

Autism  spectrum  disorder  (ASD)  is  a  neurodevelopmental  disorder  that  is  characterized  by  social impairments and restricted and repetitive behaviors (1). Most recent estimates from the Centers for Disease  Control  and  Prevention  suggest  that  1  in  88 children  in  the  United  States  are  affected  by  ASD (2).  Although  ASD  affects both  genders,  estimates have  long  reflected  that  the  disorder  occurs  more frequently in males.  The  male-to-female  gender ratio has been reported to be between 4.3:1 and 5:1 (2-4),  and  the  ratio  is  even  larger  (between  5.75:1

and  16:1)  for  individuals  with  average  to  aboveaverage intelligence (3-6).

As  a  result  of  the  higher  prevalence  of  ASD  in males, the majority of research into ASD, including research that addresses phenotypic characterization and  measures  development,  has  been  conducted with  predominantly  male  samples  (7).  However,  a rapidly  growing  body  of  research  has  begun  to explore  gender  differences  with  respect  to  core ASD deficits, cognitive endophenotypes, and genetic factors in both  clinical and  high-risk infant sibling samples (8-11). A recent meta-analysis of the extant  literature  surrounding  gender  differences  in core ASD  deficits considered 22 peer-reviewed studies  in  this  domain  and  identified  an  increased severity of stereotyped and repetitive behavior among  males.  However,  no  gender  differences  in social  communication domains were apparent (12). Among  researchers  who  have  examined  gender differences involving ASD, there has been growing concern  with  the  underidentification  of  females (1;12-15), especially in those studies that have other methodological concerns (e.g., the inclusion of sample populations with a wide range of functioning  or  a  large  age  range).  As  such,  concerns  have been  raised  regarding  whether  the  current  understanding of the ASD phenotype is representative for both male and female populations. Given the possibility  of  differential  phenotypic  presentations  of ASD  among  females  (16),  concerns  have  been raised that females with  ASD  may  be  underidentified, especially if they do not have accompanying intellectual impairment (1;13-15). Indeed, females  who  are  identified  later  in  life  as  having ASD are less likely to have a documented diagnosis of ASD obtained during childhood (17,18).

A  number  of  biogenetic  explanations  have  been proposed to account for the gender discrepancy associated  with  ASD.  Most  suggest  either  a  greater genetic vulnerability in males or, alternatively, greater  protective  mechanisms  in  females.  The  extreme male brain theory (19) posits  that  autism  is  an  extreme form of the normal male profile. At the same time,  epigenetic  hypotheses,  including  the  imprinted-X liability threshold model (20), propose that an X-linked  protective  gene  affects  the  threshold  for ASD phenotype expression. An increasing body of research has pointed toward differential and multifactorial  genetic  and  hormonal influences that may lead  to  increased  risk  among  males  or  attenuated risk among females (16;21).

In  addition  to  the  biogenetic  theories  that  have been proposed to explain the differential occurrence of ASD among males and females, there are social and  cultural  mechanisms  that  suggest  that  ASD diagnoses  in  females  are  often  delayed  or  missed (10). Differential societal expectations for males and females-particularly  with  regard  to  the  social  and communication domains (e.g., expectations of empathy and warmth) and the differential modeling and social experiences that are common to females (e.g., more emotion-focused conversations with mothers and in peer groups) (22-26)-may serve to strengthen some of the core deficits experienced by females with ASD. In an attempt to meet social expectations,  females  with  ASD  may  closely  emulate peers or adopt social scripts (e.g., memorized social responses) (27). However, as a result of the discre- pancy between their core deficits and societal expectations, their difficulties may become increasingly  apparent  as  social  demands  increase  during development,  which  could  contribute  to  an  increased  risk  for  peer-related  difficulties  and  cooccurring internalizing difficulties.

The  purpose  of  this  article  is  to  provide  clinical examples of three primary processes that may lead to the underrecognition of ASD in young adult females without co-occurring intellectual disability: 1) females with ASD show unique core symptom manifestations related to rigidity, social engagement, and insight into social relationships; 2) they demonstrate heightened psychiatric comorbidities, particularly with internalizing disorders like anxiety and depression, which can mask the social difficulties that are characteristic of  ASD; and 3) they exhibit emotion regulation difficulties with regard to both upregulation  (e.g.,  lack  of  emotion  expression)  and downregulation  (e.g.,  control  of  extreme  emotion). These  processes,  which  have  been  extracted  from the  extant  research,  have  been  theorized  as  the possible reasons for the underidentification of ASD in females (15;28,29).

We  present  three  case  examples  of  young  adult females with ASD who were seen in a research clinic  at  a  large  university  in  the  Southeastern  United States.

Two of the females were seen in  the  context of individual therapy, and the third received a psychoeducational assessment in the clinic. They were the only  three  young  adult  females  with  ASD  seen  in the  clinic  for  therapy  or  assessment  within  the  4month  period  of  time  during  which  the  present study was being conceptualized and developed. All three females were administered the Anxiety Disorders Interview Schedule for DSM-IV (ADISIV),  which  is  a  comprehensive,  semi-structured, clinical interview that assesses for the diagnostic criteria for anxiety disorders presented in the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition (30).

'Brigitte' is an 18-year-old college freshman who lives by herself in a dorm on campus. She was diagnosed  with  ASD  during  middle  childhood.  Before the study, her diagnosis was verified in the research clinic with the use of the Autism Diagnostic Observation Schedule, Second Edition (ADOS-2), which is an empirically supported standardized assessment tool used for the diagnosis of ASD (31). Brigitte is in  the  process  of  earning  her  bachelor's  degree. 'Carina'  is  a  20-year-old  college  junior  who  lives with a roommate in a dorm on campus. She was diagnosed  with  ASD  during  her  late  teenage  years, and, like Brigitte,  her  diagnosis  was  verified  before the  study  with  the  ADOS-2.  Carina  is  earning  her bachelor's  degree.  'Jan'  is  a  26-year-old  graduate student who lives alone in an apartment off campus. She was diagnosed with ASD in the research clinic at the time of the study with the use of the ADOS2. Jan is earning her master's. 1

All  of  these  young  women  were  first  diagnosed when  they  were  older  than  the  average  age  of diagnosis.  Although  some  children  with  ASD  are diagnosed before the age of 3 years, the majority of children  receive  a  diagnosis  between  the  ages  of  4 and 6 years, which coincides with their entrance into the  school  system  (2).  Diagnosis  tends  to  be  later for individuals who are less classically impaired and for those without intellectual disability (32). Within this  segment  of  the  population,  as  compared  with their  male  peers,  females  with  ASD  are  identified and diagnosed later (17,18). Brigitte was diagnosed with ASD when she was in fourth grade, Carina was diagnosed before her senior year in high school, and Jan did not receive a diagnosis until graduate school. The delayed identification of ASD in each of these cases  illustrates  an  overarching  problem  with  the current ability  to  detect  and  accurately  assess  ASD traits as they are manifested in females.

## Unique Core Symptom Manifestation

Although research that examines gender differences with regard to core ASD deficits is limited, there has been  consistent  evidence  of  less  atypical  and  less severe  restricted  and  repetitive  behaviors  among females with ASD across various levels of functioning  as  compared  with  males  with  ASD  (12).  Findings have been less consistent with regard to gender differences involving social and  communication challenges,  although  some  evidence  suggests  that females experience less severe social difficulties during  childhood  (12;33-35)  and  worse  peer-related difficulties  during  later  childhood  and  adulthood (36,37).  In  the  only  study  that  investigated  gender differences in an adult sample, females were found to have fewer observable social and communication difficulties  and  greater  self-reported  social  difficulties as compared with males (38).

## Rigidity and Insistence on Sameness

Although  several  studies  have  shown  that  females with ASD  have  fewer  restrictive and  repetitive behaviors as compared with males (34;39), females with  ASD  may  express  restrictive  and  repetitive behaviors  in  a  unique  manner.  Although  none  of the  females  in  this  case  series  expressed  repetitive behavior,  all  three  demonstrated  clear  signs  of  the restricted  and  repetitive  behaviors  that  are  characteristic of ASD (e.g., cognitive and behavioral rigidity, insistence on sameness). Cognitive and behavior- al  rigidity emerged as the most impairing symptom within  the  restricted  and  repetitive  behavior  domain. For example, both Brigitte and Carina demonstrated a clear deficit with regard to perspective-taking across various situations. They were able to  identify  others'  viewpoints  when  prompted,  but they struggled to apply this knowledge outside of a structured setting.

1 Pseudonyms are used for the case studies, and all identifying information has been removed.

Brigitte  had  difficulty  understanding  why  someone  would  have  been  late  to  meet  her;  she  was never  late  because  she  viewed  herself  as  being considerate  of  other  people's  time.  In  a  structured setting, she  was  able to recognize that occasionally people are late because of situational circumstances, like  emergencies.  However,  when  discussing  her experiences  with  friends,  she  expressed  that  they were always late because they were inconsiderate of others  and  selfish.  Brigitte  attributed  her  friends' actions  to  their  personalities  despite  awareness  of the  possibility  that  other  situational  factors  may have contributed.

When attempting to understand others'  perspectives  about  social  interactions,  Carina  frequently rationalized that, because she would act in a specific manner, others should also act in the same manner. For instance, she demonstrated considerable difficulty understanding why  a friend may  not realize  that  she  was  feeling  down,  despite  the  fact that  she  did  not  communicate  her  feelings.  She explained  that  she  often  asked  friends  about  how they were feeling and could not understand why her friends would not do the same. Interestingly, when challenged to understand others' perspectives, Carina was able to generate alternative explanations for why others may have acted in certain ways that were  not  compatible  with  how  she  believed  they should  act.  However,  her  rigidity  was  apparent when  she  was  unable  to  accept  others'  behaviors, such  as  their  failing  to  realize  that  she  was  feeling down. She also struggled to apply perspective-taking skills outside of a structured setting. Carina consistently  demonstrated  difficulty  with  thinking abstractly and with deviating from preconceived notions about certain topics.

Jan  stated  that  she  was  'not  good  with  change' and  that  she  strongly  preferred  routine.  Although she reported a number of generalized worries about academics, her finances, and her health, Jan expressed  a  separate  worry  about  changes  in  her routine;  which  is  not  characteristic  of  traditional generalized  anxiety  disorder  (GAD).  She  experienced  anticipatory  anxiety  about  changes  in  her routine, including both  changes  that she could control  and  those  that  she  could  not  control.  For instance, Jan indicated that she would be upset if a class she did not enjoy was cancelled with short notice because she had planned to attend. Jan's desire for  sameness  caused  her  to  experience  worries above  and  beyond  her  traditional  GAD  worries about changing her routine and the discomfort that she would experience as a result. Jan also displayed a notable degree of cognitive rigidity when discussing topics that she found upsetting, such as driving. She asserted that 'very few people obey the rules  of  the  road,'  which  made  her  concerned  for her safety. Although she was presented with several examples that challenged her belief, Jan maintained that she would be unsafe driving because all of the other drivers on the road were dangerous. She also struggled to recognize factors (i.e., difficulty coping with emotion, lack of time-management skills, reluctance  to  engage  in  social  situations,  disorganization) that may have contributed to her difficulties in  multiple  domains,  such  as  with  family  relationships, academic  progress, social challenges,  and housework.  Instead,  she  repeatedly  explained  that, because she had ASD, she simply could not do certain things. Despite being challenged regarding this belief  and  encouraged  to  identify  other  variables that may  have affected her functioning across domains,  Jan consistently reverted back to the notion that her diagnosis was the only cause of her difficulties.

Although  insistence  on  sameness  and  cognitive inflexibility  are  often  seen  in  males  with  ASD,  the symptoms  described  here  are  the  most  prominent and impairing symptoms found within the restricted interests and repetitive behaviors domain seen among these females. These behavioral examples of cognitive  rigidity  and  preference  for  routine  were, for the most part, not apparent to individuals who were not familiar with these young women. In other words, these behavioral styles are not clearly atypical,  obviously  peculiar,  or  noticeable  to  most people. These symptoms also differ from the highly repetitive behaviors or unusual or intensely restricted  interests  that  are  more  frequently  seen  among males, which tend to be more easily recognized as a result  of  the  level  of  impairment  that  they  cause (40). Gender  differences  that  involve  symptom manifestation  within  the  restrictive  and  repetitive behaviors  domain  may  contribute  to  the  delayed assessment  and  diagnosis  of  ASD  among  young adult females.

## Social Ambivalence

Foremost among the challenges experienced by individuals  with  ASD  are  social  difficulties.  Brigitte and Jan both reported experiences of social ambivalence  or  of  a  strong  approach-avoidance conflict. They actively avoided situations that involved other people, especially when the activities were not task oriented or when they involved interacting with unfamiliar people. Both Brigitte and Jan were motivated to have friends, and they expressed interest in social interaction; however, they reported experiencing difficulties during social situations, and they were more comfortable being alone.

Brigitte reported on several occasions that she had interest in spending time with other people. However, the few times she engaged in social interactions, such as going to see a movie with members of  a  club  she  was  involved  in,  she  lost  interest almost  immediately  and  wanted  to  return  to  her room and be alone. Brigitte also reported that it was 'hard  to  connect  with  people  [her]  age'  and  that she  felt  'weird  and  [did]  not  want  to  scare  people away.' In addition, she reported that, although she wanted  to  make  new  friends,  she  did  not  like approaching  unfamiliar  people;  she  was  afraid  she would forget what she was saying in the middle of a sentence and appear 'stupid.' Feelings of apprehension  and  anxious  thoughts  (e.g.,  fear  of what  others  thought  of  her)  emerged  as  common contributors to Brigitte's lack of social engagement. Brigitte  also  indicated  that  she  wanted  to  sound more  confident  when  speaking.  Overall,  she  was much more comfortable talking with someone who initiated  a  conversation,  and  she  tended  to  remain alone in social situations when she was not approached.

Jan refused to engage in situations with more than seven  people  present.  Thus,  she  did  not  attend available  ASD  support  groups,  student  groups  at her church, or academic functions with other students.  Because  she  did  not  report  having  the opportunity to socialize  in  a  smaller  group  setting, Jan was virtually isolated from interacting with other people, with the exception of certain professors in her department. She attributed her refusal to engage in social situations to anxiety about interacting with others.  Specifically, Jan  expressed  that  she  was  unsure  about  how  to  discuss  topics  unrelated  to  her specific academic area of interest, and she was concerned  that  others  would  react  negatively  to  other topics of conversation that she introduced. Instead of  engaging  in  social  situations,  Jan  reported  that she spent the majority of her time focusing on her academics.

Although Carina demonstrated interest in engaging with others both individually and in group situations,  her  motivation  to  do  so  was  driven  in part  by  her  perception  of  herself  as  being  a  leader and  a  good  friend  to  others.  In  addition,  Carina indicated  that  a  main  factor  in  her  motivation  for seeking  and  maintaining  friendships  was the  desire for reciprocal cooperative relationships with others whom  she  could  rely  on  for  help.  For  instance, Carina stated that she wanted a friendship with her roommate  in  case  she  locked  herself  out  of  her dorm room and needed an extra key. She reported that  she  was  interested  in  establishing  friendships with  people  in  her  academic  department  so  that they  could  help  her  with  homework  if  she  was confused about something. Overall, Carina's interest  in  social  engagement  seemed  to  be  related to her rigid self-perception that she was a leader and a friend as well as her desire to have social resources available in times of need.

## Lack of Insight Regarding Friendships

Brigitte,  Carina,  and  Jan  demonstrated  difficulty with  social  information  processing.  Although  all three indicated that they had friends, they reported problems with their friendships, and they demonstrated a marked lack of insight into what a reciprocal friendship entails. Some of these difficulties stemmed  from  the  rigidity  discussed previously.

For example, Brigitte reported that she had been ignored  by  people  whom  she  considered  to  be friends,  and  she  reported  that  she  believed  her friends took advantage of her by only spending time with  her  when  they  needed  something  or  when nobody  else  was  around.  She  expressed  that  the primary  reason  that  one  of  her  friends  spent  time with  her  was  because  that  friend  'could  not  find anyone else that she could spend time with.' Brigitte  reported that most of her friendships were with older  individuals  (i.e.,  those  who  were  10  or  more years  her  senior)  because  people  her  age  did  not understand  her.  Brigitte's  attempt  to  understand others' behaviors led her to conclude that all people were  'liars' or 'selfish.' For  example,  Brigitte reported  an  incident  in  which  her  friends  did  not show  up  to  meet  her  for  a  get-together,  despite telling her that they would. She felt rejected, and she said  that  her  friends-like  all  people-were  liars. Despite  prompting,  she  could  not  provide  alternative  explanations  for  their  behavior.  In  another instance,  Brigitte  concluded  that  people  were  all 'selfish' when her friends were late to meet her for dinner.  She  indicated  that,  because  they  were  late, the dinner took more time and prevented her from getting  started  on  the  things  that  she  needed  to accomplish.  Brigitte  had  rigid  beliefs  about  what constituted friendships, and she tended to attribute actions to personalities when people did not adhere to her established convictions.

Carina expressed similarly strict and specific rules about friendships. She used these rules as a gauge to evaluate the quality of her friendships. She applied these rules harshly and definitively as a way to 'test' her friendships. For instance, Carina explained that an important indicator of friendship was whether or not a friend hugged her when she was feeling down. She also indicated that she measured friendships by counting how many times per month she interacted with  someone  (e.g.,  texting,  calling,  e-mailing,  instant messaging) and by noting how often the friend reciprocated her greeting when she passed them on campus.  Carina  explained  that  other  indicators  of true friendships were  a person's willingness to notify her if she was bothering him or her by texting too often, as well as how often a person agreed to spend time with her when she asked.

Jan identified two friendships that she maintained with people who lived locally. Both friendships were with women who were 20 to 30 years older than she was,  one  of  who  was  closely  involved  with  the supervision of her academic training. According to Jan,  she  considered  them  friends  because  she  had spoken  with  each  of  them  several  times  on  the phone  and  visited  each  of  their  homes  on  two  to three occasions 'in times of crisis.' Jan also indicated that she considered several people whom she  knew  during  her  childhood  as  friends,  even though  she  rarely  interacted  with  them  in  person. She  explained  that  she  initiated  contact  with  them via  e-mail  or Facebook on an occasional basis and then emphasized that they responded to her messages; this was done in an apparent attempt to illustrate the validity of her friendships.

## Heightened Psychiatric Comorbidity with Internalizing Disorders

Several  studies  have  found that  females  with  ASD experience higher levels of internalizing problems as compared with both males with ASD and typically developing females (41,42). In a sample of children and adolescents with ASD, Solomon and colleagues found that females had significantly more internalizing  symptoms  (e.g.,  a  combination  of  anxiety, depression,  and  somatic  symptoms)  as  compared with age-matched males with ASD and age-matched typically  functioning  female  peers  (42).  Furthermore,  females  with  ASD  in  the  sample  were  the only  study  participants  to  fall  within  the  clinical range on a self-report measure of depression (26% met the cut point). In both clinical and populationderived samples of children with ASD, higher levels of externalizing behaviors and aggression have been found (via school documentation and teacher report) in males as compared with females (18;34;41). This is reflective of population-level gender  differences  in  the  incidence  of  psychiatric disorders (e.g., higher levels of externalizing problems  among  males,  higher  levels  of  internalizing  disorders  among  females).  This  pattern  of comorbidity may lead to the increased likelihood of referral for diagnostic assessment for males, whereas females may have a decreased likelihood of referral  because  their  behaviors  may  not  be  as disruptive or as observable by third parties.

Brigitte, Carina, and Jan all experienced cooccurring symptoms of several different internalizing disorders. According to the adult version of the ADIS-IV (30), Brigitte met criteria for social anxiety disorder, GAD, and dysthymia. She reported that her anxiety began to cause distress during elementary school, when she was bullied by her peers. She expressed significant concern about dating, speaking in front of others, and saying the 'wrong things.' Her symptoms of social anxiety fluctuated depending on the status and quality of her friendships at a given time. Brigitte also indicated that she experienced generalized worries related to her family, her school performance, and her friendships and these interfered with her daily functioning. For example, she reported that her fear of academic failure in school interfered with her health because she was not getting enough sleep. Brigitte also indicated a history of major depressive episodes. She also reported persistent cognitive symptoms of depression, including being down on herself, thoughts of hopelessness and pessimism about her future.

Results of the ADIS-IV indicated that Carina also experienced clinically significant symptoms of social anxiety disorder, GAD, and major depressive disorder. She reported that her symptoms of social anxiety  began  during  middle  school,  when  she  became concerned that  others  would  notice  that  she was  'different.'  Carina  indicated  that  her  two  primary  areas  of  general  worry  were  related  to  being on time and losing friendships. She also experienced infrequent depressive episodes that were characterized by a lack of motivation, particularly related to the  completion  of  academic  assignments,  and  by  a loss of interest in preferred  activities,  including spending time with friends. Carina's bouts of depression  tended  to  be  related  to  perceiving  that she did not have any friends.

According to the results of her diagnostic assessment,  Jan  met  the  criteria  for  major  depressive disorder, social anxiety disorder, and GAD. Just as Carina  had  reported  about  her  social  anxiety,  Jan reported  that  her  symptoms  of  depression  began during  her  middle  childhood,  while  she  was  in middle school, where she initially perceived that she did not fit in with her peers. She indicated that her social  anxiety  was  driven  by  concerns  about  how people would respond to her efforts to communicate (e.g.,  conveying  her  ideas)  as  well  as apprehension about not connecting with unfamiliar people. Jan expressed that her symptoms of generalized  anxiety  centered  on  her  ability  to  relate  to others  and particularly on her  ability  to  experience success in her career.

## Borderline Personality Disorder Traits

In  addition  to  anxiety  and  depression,  these  three women exhibited a number of interpersonal behaviors  in  the  context  of  peer  relationships  that are characteristic of individuals with borderline personality disorder (BPD). As observed by several researchers,  the  symptoms  seen  in  females  with ASD  often  resemble  BPD  traits.  In  a  sample  of treatment-seeking women with BPD (n=41), Rydén and colleagues found that 15% of the females had ASD and that an additional 32% had autistic traits (43). Studies exploring the overlap of features between  BPD  and  ASD  have  identified  problems with identity, intense anger, self-damaging behavior, and  severe  problems  with  interpersonal  relationships  (44;45).  In  the  three  current  case  examples, self-damaging  behavior  and  problems  with  interpersonal relationships were unambiguously present. Also  common  were  intense  anger  and  problems with identity; these were less evident but still present.

For  example,  throughout  the  duration  of  her treatment, Brigitte reported problems with interpersonal relationships. She expressed that she felt that other people were the cause of her difficulties rather than anything that she herself was doing. She stated, 'In my head I keep thinking, I'm not the problem. I think other people are the problem. Because I try to be nice to people but I've been taken advantage of.' Despite  being  challenged  on  her  beliefs,  Brigitte maintained that she was never the problem and that she did everything she could to avoid inconveniencing other people. In addition, Brigitte's claims  that  'people  are  liars'  and  'all  people  are selfish'  are  similar  to  the  extreme  devaluation  of others and anger seen in people with BPD.

Also consistent with the pattern of unstable interpersonal relationships that is characteristic of BPD was Carina's report of using a 'friendship test'  to evaluate  the  quality  of  her  friendships.  Specifically, Carina indicated that she purposely did not communicate  feelings  of  sadness  to  her  friends because  she  was  interested  in  seeing  which  of  her friends  would  notice  or  intuit  that  she  was  feeling down and subsequently express concern. She reported that she  always  questioned  the  validity  of her friendships with specific people if they did not pass  her  'friendship  test.'  In  addition-and  also consistent with one  of  the  core  symptoms  of BPD-Carina seemed to struggle  with  finding  her sense  of  identity.  For  example,  she  had  difficulty adjusting when her older sister got married, because she  was  unsure  about  how  she  fit  into  her  sister's life  and  her  new  relationship.  Without  a  coherent understanding of her personal self, Carina attempted  to  define  herself  in  terms  of  specific roles; this may have left her vulnerable to experienc- ing  distress  when  she  was  no  longer  able  to  fulfill these  specific  roles.  Although  Carina  was  not  a 'natural  leader,'  she  viewed  herself  as  such  and worked hard to seek leadership opportunities (e.g., seeking  positions  of  leadership  in  multiple  clubs). Despite  experiencing  considerable  difficulty  with study skills and time management, Carina expressed on a number of occasions that she enjoyed serving as an academic role model for other students.

Jan  demonstrated several  characteristics  of  BPD, including  recurrent  suicidal  behavior  and  intense anger. She expressed significant resentment toward her parents because they did not seek an assessment or  treatment  for  her  social  difficulties  during  her childhood.  She  also  expressed  intense  frustration with  regard  to  the  services  provided  for  students with  ASD  at  the  university;  she  claimed  that  they were  too  'undergraduate  focused,'  and  she  stated that  this  frustration  was  'hard  to  get  out  of  [her] mind.'  In  addition, Jan  reported that she had experienced  suicidal  ideation  on  several  occasions. During one instance, Jan expressed threats of selfharm after she did not obtain the type of directive advice she was seeking from a clinician about how to manage a specific social interaction.

Although none of these three women had received prior BPD  diagnoses, the heightened presence  of  psychiatric  comorbidity  in  all  of  them represents an additional  process  through  which ASD  in  females  may  be  underrecognized.  The comorbid  internalizing disorders may  mask  the difficulties  that  are  specific  to  ASD.  In  a  series  of case  studies  of  6-  to  10-year-old  girls,  Kopp  and Gillberg found that young girls were often identified as  having  social  and  developmental difficulties  and seen by psychologists and other experts long before they received a diagnosis of ASD (46). In our three case examples, the symptoms related to anxiety and depressive disorders were often centered on relationships  and  friendships;  they  tended  to  begin during  elementary  or  middle  school,  when  female peer relationships become more intimate and complex (24;26). Interestingly, many of the thought processes and behaviors of the females in this case series were expressed as symptoms that were consistent  with  BPD.  It  may  be  that  their  anxiety and  depressive  symptoms,  in  combination  with difficulty understanding social relationships, leads to what  appear  to  be  traits  that  are  characteristic  of BPD. The co-occurring internalizing disorders often associated  with  ASD  in  females  and  the  dynamic interplay among their symptoms may lead to problems with differential diagnoses and subsequent delays in administration of appropriate treatments.

## Emotion Regulation Difficulties

Many individuals  with  ASD  struggle  with  emotion regulation (28,29). Emotion regulation is the ability to modify one's emotions to respond to situational demands  and  to  meet  one's  goals  (47).  Problems with  emotion  regulation  are  expressed  in  several different  ways,  including  recognition  of  emotion, expression of emotion (e.g., alexithymia), and management of emotion. Therefore, emotion regulation  not  only  refers  to  control  of  extreme emotions,  it  also  addresses  the  use  of  emotions productively. Emotions are often useful in situations  when  we  need  to  attend  to  or  change aspects of our lives or surroundings. Although some individuals  with  ASD  show  a  significant  lack  of emotional  expression,  others  have  difficulty  controlling  strong  emotions.  Both  of  these  aspects  of emotion regulation can have undesirable consequences.  In  females  with  ASD,  difficulties  with emotion regulation could result in later diagnoses of ASD and misdiagnoses as a result of the possibility that elevated levels of distress mimic other disorders. The females in the present study demonstrated marked difficulty with emotion regulation in terms of needing to both upregulate their emotional expression and downregulate their emotions.

Brigitte  and  Carina  each  demonstrated  the  clear need  to  upregulate  as  a  result  of  their  lack  of expressed emotion. Although both Brigitte and Carina  reported  feeling  emotions  such  as  happiness and  sadness,  they  reported  having  difficulty  with expressing their emotions, and they presented with flat  affects.  Brigitte  reported  that  she  was  often stressed  out  but  that  she  generally  elected  to  hide her  stress  from  others.  She  indicated  that  she  did not know why she chose to hide her emotions, but she noted that she did not want others to recognize when she was feeling stressed.  In  addition,  on  the basis of feedback that she received from her peers, she expressed a desire to take acting classes so that she  could  increase  the  animation  in  her  voice  and 'have  a  presence.'  Brigitte  also  self-reported  that one of her weaknesses was conveying interest when others were talking.

Although  Carina  indicated  on  several  occasions that she felt sad from time to time, she consistently denied that she experienced emotion when she was asked directly about these situations. When challenged about this notion and asked to consider specific  situations  that  she  had  encountered  (e.g., almost falling while climbing a waterfall), Carina responded logically (e.g., asking for details about the height of the waterfall and how many people were present)  and  explained  that  she  was  a  calm  and rational person whose behavior was driven by logic rather  than  emotion.  In  addition  to  her  difficulty with identifying emotions, Carina's rigid self- perception  that  she  was  calm  and  driven  by  logic precluded her from recognizing that she experienced  emotion,  which  ultimately  contributed to her flat affect.

Alternatively,  Jan  struggled  to  downregulate  her emotions; this was evidenced by angry outbursts as well as by suicidal ideation, which exclusively occurred in situations when  she had difficulty coping with emotions such as anxiety or frustration. In  addition,  when  speaking  about  her  generalized anxiety, she described feeling like she did not know 'how  to  manage  [her]  worries';  this  reportedly interfered with her daily functioning.

## Clinical Implications

Knowledge of the unique difficulties experienced by young, high-functioning, adult women with ASD is essential  to  better  understand  their  unique  phenotypic  presentation  and,  ultimately,  to  decrease  the underidentification of ASD in this population. The majority  of  the  research  into  ASD  has  focused  on males. As such, we likely face a gender bias in our knowledge  of  this  disorder.  However,  the  recent increase  in  the  number  of  studies  of  females  with ASD represents the growing interest in understanding more about gender differences in this population. In particular, empiric findings have centered  on  exploring  the  neurologic  phenotypes associated with ASD in females (8) and the differential  genetic  effects  of  ASD  markers  between  the sexes  (9).  Although  the  literature  has  started  to examine gender differences  as  they  apply  to  social and communication difficulties (48), it is difficult to draw  firm  conclusions  from  the  extant  empiric literature that addresses the social and communication  difficulties  experienced  by  females  with  ASD. The  majority  of  research  into  gender  differences among individuals  with  ASD  has  been  clouded  by the inclusion of participants with diverse age ranges and  levels  of  functioning.  Although  the  heterogeneity of participant samples is useful for researchers' abilities to generalize findings across samples, it can  lead  to difficulties  with  interpreting  gender differences  at  specific  stages  of  development.  In addition, most epidemiologic research only includes children  through  the  age  of  8  or  10  years  (2-4), which  is  a  problem  given  the  age  of  onset  of comorbid problems (49,50) and the later diagnosis of ASD in individuals without co-occurring intellectual  difficulties  (17,18).  Further  research  is  needed to  explore  gender  differences  at  various  developmental  and  functioning  levels.  Our  case  examples highlight  several  processes  that  could  affect  the identification of ASD in young women and potentially  in  girls  who  do  not  have  co-occurring intellectual impairment.

First, the reliance on unique core symptom manifestations (i.e., insistence on sameness, reluctance  to  engage  in  social  interactions  despite interest,  and  lack  of  social  insight)  is  one  process that results in ASD being underidentified in young adult  females.  The  three  women  described  in  this article portrayed  common  symptoms  related  to stereotyped  and  repetitive  behaviors,  social  withdrawal,  and  communication  difficulties;  these  are distinct  from  the  prototypic  symptoms  that  most individuals associate with ASD. These females exhibited  limited  insight  into  friendship  and  had difficulty  with  perspective  taking  in  the  social  and communication  domains.  However,  these  symptoms  are  distinguishable  from  the  more  severe social communication impairments listed in the Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition ,  such as a complete lack of eye contact and stereotyped  gestures  (2).  There  are  several  'red flags' for autism that are evident during early development, including the avoidance of eye contact, delayed speech and language skills, obsessive  and  sometimes  unusual  interests,  and  a lack of gestures (51). The subtler and more nuanced social  impairments  seen  in  females  with  ASD  may not be apparent until middle childhood, when social demands increase. When these symptoms are recognized,  many  practitioners  may  not  consider ASD  as  a  likely  diagnosis,  particularly  if  the  early signs  of  ASD  were  not  present  and  there  was  no diagnosis of ASD during early childhood.

Second,  the  women  in  this  study  experienced significant psychiatric comorbidity, particularly involving internalizing disorders such as anxiety and depression. Although females with ASD  share features of anxiety with neurotypical females, there are unique features of anxiety in this population that should be considered (52). The interaction between these symptoms and affected individuals' social difficulties may  ultimately resemble  traits that are characteristic of BPD. Rydén and colleagues found that, although individuals with ASD and BPD share several characteristics, there are marked differences (e.g.,  the  absence  of  substance  abuse  in  ASD)  that should be considered (43). The presence of psychiatric comorbidities serves as another process through  which  ASD  identification  may  be  delayed in  young adult females, because ASD may be misdiagnosed in the presence of a comorbid disorder. The  concept  of  diagnostic  overshadowing  is  often seen  in  situations  in  which  the  presence  of  an intellectual disability minimizes the diagnostic significance of an accompanying problem (53). This can  happen  because  the  accompanying  problem  is seen as a consequence of the primary diagnosis or because, by comparison, the accompanying problem may appear less problematic. This phenomenon can occur with the diagnosis of additional disorders in a person  with  ASD  as  well.  The  consequences  of misdiagnoses are substantial, because treatment may be delayed or misapplied. Treatments may need to be  modified  to  effectively  treat  such  symptoms  in individuals with ASD. Thus, when assessing young adult females for ASD, it is critical to be mindful of potential comorbid symptoms.

Third, it is possible that females with  ASD experience greater difficulty with emotion regulation than males in terms of needing to both upregulate and downregulate their emotional expression. When individuals  do  not  express  their  emotions,  it  can disguise their difficulties and their elevated levels of distress, thereby delaying the process of assessment and subsequent treatment.

There  are  several  limitations  that  apply  to  the current  case  series.  The  specific  ASD  symptom manifestations  and  processes  through  which  ASD identification  may  be  delayed  in  females  that  are described  in  this  paper  are  not  exhaustive.  Moreover,  because  ASD  is  a  heterogeneous  condition, not  every  young  adult  female  with  ASD  will  show deficits  in  all  of  these  domains,  and  many  will experience  other  difficulties  that  have  not  been described  here.  Another  limitation  of  this  study  is the lack of a control group for a direct comparison. However,  the  current  case  series  sought  to  use clinical  observations  to  illustrate  several  common symptom presentations that are specifically seen in this population.

When  assessing girls and young women  for possible  ASD,  it  is  important  to  carefully  consider the  factors  that  may  obscure  symptoms  that  are characteristic  of  the  condition.  It  is  recommended that the assessor probe for tendencies toward sameness  and  rigidity,  their  understanding  of  intangible aspects  of  friendships,  comorbid  symptomatology and its possible interaction with social relationships, and  difficulties  related  to  emotion  regulation.  An awareness of such processes may reduce the underidentification  and  diagnostic  overshadowing (misdiagnosis)  of  ASD  in  females.  Furthermore, understanding how these processes affect the manifestation of ASD in females may inform treatment  planning.  The  current  case  series  of  young adult females with ASD  without co-occurring intellectual impairment sheds light on the complexity  of these processes as well as on the importance of considering the degree to which they contribute to delays in the identification  of  ASD.  Future research is needed to further illuminate the differences in symptom manifestation across genders  and  stages  of  development  to  inform  the clinical assessment and treatment of individuals with ASD.

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## Acknowledgments

The authors would like to thank the three women discussed  in  this  article  for  providing  insight  into the presentation of ASD through their participation in the research clinic.