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. Author manuscript; available in PMC: 2013 Jun 1.
Published in final edited form as: J Autism Dev Disord. 2012 Jun;42(6):1120–1126. doi: 10.1007/s10803-011-1359-x

Brief Report: Approaches to 31P-MRS in Awake, Non-Sedated Children With and Without Autism Spectrum Disorder

Laura C Erickson *, Ashley A Scott-Van Zeeland *,§, Gavin Hamilton ‡, Alan Lincoln , Beatrice A Golomb *,†
PMCID: PMC3668346  NIHMSID: NIHMS456988  PMID: 21979108

Abstract

We piloted a suite of approaches aimed to facilitate a successful series of up to four brain and muscle 31Phosphorus-Magnetic Resonance Spectroscopy (31P-MRS) scans performed in one session in 12 awake, non-sedated subjects (ages 6 – 18), 6 with autism spectrum disorders (ASD) and 6 controls. We targeted advanced preparation, parental input, physical comfort, short scan protocols, allocation of extra time, and subject emotional support. 100% of subjects completed at least one brain scan and one leg muscle scan: 42 of 46 attempted scans were completed (91%), with failures dominated by exercise muscle scans (completed in 6/6 controls but 3/6 cases). One completed scan lacked usable data unrelated to subject/scan procedure (orthodonture affected a frontal brain scan). As a group, these methods provide a foundation for conduct and enhancement of future MR studies in pediatric subjects with ASD.

Keywords: Autism, ASD, Magnetic Resonance, energetics, muscle, brain, awake

Imaging techniques such as magnetic resonance imaging (MRI) are commonly employed in children and adolescents with autism spectrum disorders (ASD). Successful completion of MR protocols is often compromised by participant inattention and non-compliance (Corbett and Constantine 2006; Sturm et al. 2004), anxiety (Gillott and Standen 2007; Gillott et al. 2001), fatigue, and sensory (auditory and tactile) sensitivity (Cascio et al. 2008; Kern et al. 2006; Rogers et al. 2003), leading to higher failure rates in younger children (Raschle et al. 2009; Poldrack et al. 2002; Byars et al. 2002) and those with conditions such as ASD (Yerys et al. 2009).

Approaches to overcome these obstacles in ASD commonly included “chemical restraint” (Rosenberg et al. 1997) or sedation (Ross et al. 2005). Use of natural sleep (Almli et al. 2007; Nordahl et al. 2008) and mock scanners (Rosenberg et al. 1997) have been heralded as fostering scanning success without pharmacologic intervention (Raschle et al. 2009; Nordahl et al. 2008). However, sleep or sedation may still alter functional and energetic characteristics of the brain (germane to fMRI, 31P-MRS) (Scharf et al. 2008; Dworak et al. 2010), and energetic assessments may benefit from muscle exercise/recovery testing that necessarily requires non-sleeping, non-sedated subjects. Sedation and separate mock scanner visits raise costs (Vanderby et al. 2010) and increase the time burden on families. Additionally, clinicians and some researchers may have neither access to mock scanners, nor sufficient resources to permit lengthy acclimation to the scanner room. Here, we describe a suite of approaches aimed at producing successful brain and muscle scanning, in this case 31Phosphorus-Magnetic Resonance Spectroscopy (31P-MRS) of brain and skeletal muscle in awake, non-sedated children and adolescents with and without ASD. These scans were conducted without chemical restraint, natural sleep, or extensive mock scanner exposure. The paper elucidates the demands associated with successful scanning of challenging populations like those with ASD, and the methods described provide a broad approach for clinical evaluation with relevance to other imaging modalities and populations.

Methods

Participants

Twelve participants, comprising six ASD cases (age 6 to 18 years old) and six age and gender-matched controls, were scanned at the University of California, San Diego Bydder MR Center. ASD cases were confirmed through Autism Diagnostic Observation Schedule (ADOS-G) (Lord et al. 2000) and Autism Diagnostic Interview-Revised (ADI-R) (Lord et al. 1994; Cicchetti et al. 2008) testing by The Center for Autism Research, Evaluation and Service. Two of these subjects also evidenced generalized anxiety disorder (GAD) and social anxiety disorder (SAD) (determined by author AL based on history of symptoms reported during the ADI-R evaluation and observations during the ADOS), which magnify challenges associated with the scanning process. This small (pilot) study was conducted as part of a consortium award supported by Autism Speaks, aimed to assess mitochondrial dysfunction in ASD via several approaches (of which 31P-MRS energetic assessment was one). Recruitment of cases and matched controls was conducted by our consortium collaborators, who sought ASD cases suspected to have energetic challenges, based on considerations like fatigue or history of hypotonia. The primary focus of recruiting investigators was not the 31P-MRS protocol. Age less than 6 years precluded participation in the 31P-MRS protocol. Additionally one older boy (8 years), considered unlikely to complete the 31P-MRS procedure, was not referred on discretion of the referring nurse. Thus, findings need not refer to very young or most highly impaired subjects.

Scanning

For this study, generous time was allocated for each 31P-MRS visit (2 hours), more so for ASD (3.5 hours) to enable participants to acclimate to study staff and the MR environment. However, while this study benefited from extended scanning sessions, our intent where possible was to identify methods to expedite scan procedures and maximize the likelihood of successful scans in shorter sessions in the future. One subject received a second scanning visit, with further ‘second’ visits precluded by funding constraints. Scanning parameters were optimized to minimize scan time (brain scans: 6 minutes each; resting leg: 6 minutes; exercise: 13 minutes) with subject positioning and shimming limited to approximately 5 minutes per scan.

Scan Preparation

(a) Selection of Study Staff: Study staff were selected to be patient and have experience working with children with developmental disabilities. Dr. Scott-Van Zeeland, who oversaw all 31P-MRS scanning visits, had extensive scanning experience specifically with ASD. (b) Advance Preparation: Participants and parents received a research brochure, frequently asked questions flyer, informational letter, electronic recording of 31P-MRS noises, and You-Tube videos posted by other research groups that outlined general MR procedures and safety (Raub 2009; Hudac 2008). Participants’ parents were encouraged to hold “practice” visits at home in a semi-enclosed area (i.e., under the legs of a chair or stool) while playing MRS noises and encouraging children to lie still for minutes at a time. For ASD cases, multiple preparatory phone and email contacts with parents were vital to addressing questions, fostering rapport, and anticipating/overcoming child-specific challenges. For example, one participant with high repetitive behaviors was encouraged to bring an MRS-compatible favorite object (stuffed rabbit) to ease anxiety and reduce repetitive behaviors while in the scanning. All participants and their parents were encouraged to bring their child’s favorite movie and/or music selection to reduce anxiety and provide a distraction during scan set-up. c) Approaches for Physical Comfort and Anxiety Reduction: ASDs are associated with sensory abnormalities (including auditory and tactile hypersensitivity) (Kern et al. 2006; Rogers et al. 2003; Kern et al. 2007) and anxiety (Gillott et al. 2001; Gillott and Standen 2007). Weighted blankets were used to reduce movement and, perhaps through deep touch pressure, anxiety (Grandin 1992; Edelson et al. 1999). Child-friendly 8 or 13lb two-sided (fleece or smooth cotton) blankets were employed (depending on child’s size). The child selected which texture contacted their body to reduce sensory irritation. Complete high-resolution coverage of the brain in a single scan (mandating a birdcage coil) was not required since our study was limited to localized 31P-MRS. Therefore a less threatening 31P-MR surface coil was used to acquire spectra, with the body coil sufficient for shimming and low resolution localization imaging. A transparent plexiglass three-sided head box was created to allow positioning of the surface coil for frontal and occipital 31P-MRS scans and reducing motion artifact, while minimizing claustrophobia/anxiety. Removable interior foam pads were used for comfort and neck support. Thin foam padding covered the head coil to mimic a pillow (reducing novelty and threat). Headphones with optional earplugs are standard to reduce noise associated with MR scans. These permitted communication with study staff and played movie audio and/or music. Mirrored glasses permitted subjects to view a movie projected outside of the MR scanner.

Emotional Comfort

To reduce scan-related anxiety and non-compliance, we sought to provide the subject with familiar individuals, objects, and audiovisual stimuli, and encouraged inclusion of the person with whom they were most comfortable/secure (complementing physical approaches to reduce scanner anxiety above, e.g. transparent headbox, pillow-like coil covering, and weighted blanket). Subjects exerted significant control over the scan environment, including the video, audio, weighted blanket texture, and the individuals interacting with them during the procedures including presence of their parent during the 31P-MRS procedure. A staff member remained in the magnet room throughout the protocol for all cases to provide an additional layer of safety monitoring, quality control (i.e., motion), and participant comfort.

To further maximize compliance, we individualized our approach based on subjects’ comfort and interests. For example, some children chose to have a parent enter the scanner or lie with them in the scanner first, while others favored bringing stuffed animal into the scanner. Another child preferred to listen to his favorite song (Pokemon theme song) on repeat until the brain scan was complete rather than watch a video, which was the more common preference. For yet another, a participant’s father served as the intermediary providing instructions to a child with high social anxiety and low communication skills. Finally, for a child interested in Jimmy Neutron, we created a game in which the MR scanner was termed “the spaceship” or “the rocket” and the outside technician room “the control center.” Subsequently we modified the approach, instead offering the subject the opportunity to crawl inside “the cave” (which he elected to do).

Table 1 provides a recap of challenges encountered, approaches implemented, and the respective outcome.

Table 1.

General Challenges, Approaches and Outcomes

Challenge Approaches Implemented Outcomes
Reluctance to enter scanner room We created a friendly environment inside the scanner room. The study staff and the parents familiarized themselves with the MR scanner room. The movie played in the background. One subject brought her stuffed animal into the scanner room. Entered scanner room
Reluctance to enter scanner One subject appeared to be afraid of the moving table. We allowed this subject to crawl into the scanner like a cave. Another subject had the opportunity to watch a parent go into the scanner first. Entered scanner
Difficulty remaining still in the scanner We played the statue game. Study staff aimed for high efficiency once subject was inside scanner. Advance preparation for scanning visit was important. Remained still in scanner
Difficulty tolerating noises during scanning We placed headphones onto subject. One subject did not want to wear the headphones, we allowed him to start his scan with earplugs only. Once the subject heard the loud MR sounds, he was interested in receiving the headphones. Used headphones to muffle noise, tolerated procedure
Difficulty following ergometer directions We practiced with each subject outside of scanner and created a game out of the exercise portion. When the subject began to fatigue, we encouraged and cheered the subject on. All controls and the final three cases were able to completely understand the directions.
Achieving physical comfort in scanner We used weighted blankets scaled to subject size and with preferred side touching subject (fleece vs. cotton), specialized head-box, and head coil pillow. All subjects achieved satisfactory physical comfort to complete scan.
Achieving emotional comfort Subjects chose a movie they liked, music they preferred, and presence of parents in scanning room, if subject desired. They watched others get into the machine if they preferred. As above, one subject’s stuffed animal accompanied her in the scanner (scanning results for the latter are not available). All subjects achieved satisfactory emotional comfort to complete scan.
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Results

All subjects successfully completed at least one resting brain scan, as well as the resting muscle scan, without sedation, sleep, or use of a mock scanner. A successful scan for purposes of this report was defined by completion of scanning protocols with collection of data. Table 2 reports scan success and other scanning/behavioral notes for each subject.

Table 2.

Successful Scans and Other Behavioral and Scanning Notes

Subject Brain Scans Leg Muscle Scans Other Behavioral and Scanning Notes
Frontal Occipital Resting Exercise
Case 1 Yes Not attempted Yes Attempted - Unsuccessful Comprehension: Subject was lower-functioning and mostly understood directions. All directions were administered by subject’s father per subject’s comfort level.
Occipital: Scan was not attempted due to subject fatigue after other scans.
Exercise: Subject attempted exercise but did not adequately fatigue, data inadequate.
Control 1 Yes Yes Yes Yes Comprehension: Subject was compliant and understood all directions.
Successful Scans
Case 2 Unable to obtain Yes Yes Unable to obtain Comprehension: Subject was lower-functioning and did not understand directions.
Frontal: Subject would not lie inside specialized head box.
Exercise: Subject did not understand directions.
Control 2 Yes Yes Yes Yes Comprehension: Subject was compliant and understood all directions.
Successful Scans
Case 3 Yes Not attempted Yes Unable to obtain Comprehension: Subject was lower-functioning and did not understand directions.
Occipital: Scan was not attempted due to fatigue after successful frontal and resting muscle scans.
Exercise: Subject did not understand directions.
Control 3 Yes Yes Yes Yes Comprehension: Subject was compliant and understood all directions.
Successful Scans
Case 4 Yes Yes Yes Yes Comprehension: Subject was high-functioning and understood all directions.
Successful Scans
Control 4 Yes Yes Yes Yes Comprehension: Subject was compliant and understood all directions.
Successful Scans
Case 5 Yes Yes Yes Yes Comprehension: Subject was high-functioning and understood all directions.
Successful Scans
Control 5 Yes Yes Yes Yes Comprehension: Subject was compliant and understood all directions.
Frontal: The scanning process was completed successfully in terms of actions of subject and scanning actions. However the subject wore braces that created a large artifact, rendering frontal data unusable.
Case 6 Yes Yes Yes Yes Comprehension: Subject was high-functioning and understood all directions.
Successful Scans
Control 6 Yes Yes Yes Yes Comprehension: Subject was compliant and understood all directions.
Successful Scans
Total Subjects/Total Scans 11/12 10/10 12/12 9/12
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Successful exercise 31P-MRS required muscles to be adequately fatigued. All control subjects and the final three of six ASD cases also had successful exercise scans. Exercise instructions were challenging for younger and more impaired ASD cases. (The first ASD case attempted the exercise but did not fatigue the desired muscle. The other two could not understand the instructions.) As we gained experience, we increased emphasis on creating a relationship with the subject, prior practice outside the scanner, and active encouragement of subjects throughout the exercise portion of the scan, which facilitated successful exercise scanning in the later subjects. Not surprisingly, exercise scans, which required more cooperation and cognitive competence, had lower success than resting muscle or brain scans, but the specific exercise-associated demands are less likely to generalize to other scan settings.

Table 3 reports scan success rates to the nearest percent, stratified by case status and age (above/below 10 years). Forty-two of 46 scans were successful (91%, with case success 82%, control success 100%; 2-sided p<0.05, Mantel-Haenszel chi-square). Success was 97% for older subjects (>10 years) vs. 80% for younger, but this difference did not meet significance. Data were usable in each “successful” scan except one frontal scan (control) in which the subject’s extensive braces led to artifact (again, recruitment did not prioritize suitability for the scanning portion of the consortium effort).

Table 3.

Percentage of Success Stratified by Case Status and Age

Scan Domain N All subjects Stratified by ASD Case Status Stratified by Age
Cases Controls < 10 years > 10 years
Frontal Brain 12 92% 83% 100% 75% 100%
Occipital Brain 10 100% 100% 100% 100% 100%
Total Brain 22 95% 90% 100% 86% 100%
Resting Leg Muscle 12 100% 100% 100% 100% 100%
Exercise Leg Muscle 12 75% 50% 100% 50% 88%
Total Leg Muscle 24 88% 75% 100% 75% 94%
Total Brain and Leg Muscle 46 91% 82% 100% 80% 97%
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Discussion

Recap of findings

Success was achieved in 12 of 12 children (with and without ASD) for at least one brain magnetic resonance scan, and for the resting muscle scan, without sedation, sleep, or use of a mock scanner. This was accomplished by combining approaches to foster success, focused on advance preparation, attention to physical and emotional comfort and control, individualization of approach, and ongoing encouragement. These approaches may benefit other groups seeking to perform magnetic resonance assessments (or other imaging) without access to mock scanners, who seek to avoid altered brain states associated with sleep or sedation.

Fit with existing literature

Our findings comport with and extend prior reports: children pose greater obstacles for magnetic resonance scanning (Raschle et al. 2009; Poldrack et al. 2002), challenges are greater with younger age (Kern et al. 2006; Byars et al. 2002; Yerys et al. 2009), and magnified with conditions such as ASD (Kern et al. 2006; Yerys et al. 2009). We built on others’ successes, and findings support relaxation (Raschle et al. 2009), high quality personal interactions (Poldrack et al. 2002; Clark and Rutter 1981), and strong parental input (Nordahl et al. 2008) to enhance comfort and compliance. Nordahl et al. also employed video in a small number of awake subjects (1 case, 3 typically developing) (Nordahl et al. 2008). The challenge of sustained attention in ASD has been found to track with task complexity, and success is therefore fostered by tasks that are simple and structured (Clark and Rutter 1981) and perhaps repetitive (Garretson et al. 1990). Bringing children to the facility before the day of the scan has been previously reported not to increase success (Byars et al. 2002). Here, we unite previously successful approaches and incorporate additional elements, such as having the child share the scan process with a comforting object, providing verbal encouragement throughout any times of difficulty (for our protocol, the exercise component), and tying the experience, via play, to interests of the child.

Limitations

Our sample was small and likely biased by exclusion by the referral source of those children they thought would not cooperate for scanning. We did not see the youngest or most impaired ASD subjects. We did, however, have subjects with marked social and language impairment represented, indicating that it may be possible to successfully scan a broader group of children than has been thought. The strategies to overcome challenges were implemented in aggregate, precluding assessment of the impact of any single component of this approach. It is also possible that the video and music input used to reduce movement could influence regional waking MR assessments of some kinds (Iwaki et al. 1997; Eldar et al. 2007); however, these approaches at least permit assessments in the waking state and may provide a means for relative consistency of brain focus during awake testing. Future studies can seek to examine at least in more cooperative children whether and in what way these approaches influence results.

Implications

The approaches developed and piloted to enhance success in this setting (31P-MRS in children and adolescents with ASD and controls) target comfort, familiarity, security, control, and overall pleasure of the experience. Benefits of such approaches may transcend the scan modality (extending beyond 31P-MRS to other MR, CT, and imaging studies); and the specific patient population, fostering scanning success and quality of data procured, without sleep or sedation, both in, and beyond, investigations of ASD.

Acknowledgments

This research was conducted as part of an Autism Speaks Consortium High Risk High Impact Grant titled Mitochondria and Autism sub-award to Dr. Golomb (#7278). We gratefully thank Dr. Richard Haas, Gail Reiner and Dr. Douglas C. Wallace for the referrals of our subjects. We thank John Firebaugh, Richard Znamirowski, and Dr. Graeme Bydder from the UCSD Bydder MR Center for their technical help, support, and contributions to this project; and Richard Znamirowski for creating the transparent head box and movie screen. We thank Dr. Alan Lincoln and Rebecca McNally Keehn from the Center Autism Research and Evaluation and Service for their expertise and evaluations of our subject population. We thank Juliet Parish for her involvement and contributions to early phases of this effort. We thank Sabrina Koperski for excellent editorial and administrative assistance.

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