Mice Exposed to Diagnostic Ultrasound In Utero Are Less Social and More Active in Social Situations Relative to Controls
Open accessAbstract
Clinical use of diagnostic ultrasound imaging during pregnancy has a long history of safety and diagnostic utility, as supported by numerous human case reports and epidemiological studies. However, there exist in vivo studies linking large but clinically relevant doses of ultrasound applied to mouse fetuses in utero to altered learning, memory, and neuroanatomy of those mice. Also, there exists a well‐documented significant increase in the likelihood of non‐right‐handedness in boys exposed to diagnostic ultrasound in utero, potentially relevant given the increased prevalence of autism in males, and reports of excess non‐right‐handedness in this population. Motivated by these observations, we applied 30 minutes of diagnostic ultrasound to pregnant mice at embryonic day 14.5 and assayed the social behavior of their male pups 3 weeks after their birth. The ultrasound‐exposed pups were significantly (P < 0.01) less interested in social interaction than sham‐exposed pups in a three‐chamber sociability test. In addition, they demonstrated significantly (P < 0.05) more activity relative to the sham‐exposed pups, but only in the presence of an unfamiliar mouse. These results suggest that fetal exposure to diagnostic ultrasound applied in utero can alter typical social behaviors in young mice that may be relevant for autism. There exist meaningful differences between the exposure of diagnostic ultrasound to mice versus humans that require further exploration before this work can usefully inform clinical practice. Future work should address these differences as well as clarify the extent, mechanisms, and functional effects of diagnostic ultrasound's interaction with the developing brain. Autism Res 2014, 7: 295–304. © 2013 International Society for Autism Research, Wiley Periodicals, Inc.
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Diagnostic ultrasound applied to pregnant mice yields less prosocial behaviors in offspring compared to sham-exposed controls.
“A study applying diagnostic ultrasound to pregnant mice yielded less prosocial behaviors in offspring compared to sham-exposed controls [120].”
From The contribution of environmental exposure to the etiology of autism spectrum disorder (2019) · cites this paper as [120]
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Cites
Transcranial Pulsed Ultrasound Stimulates Intact Brain Circuits
Tufail, Y., Matyushov, A. D., Baldwin, N. G., Tauchmann, M. L., Georges, J., Yoshihiro, A., Tillery, S. I. H., & Tyler, W. J. (2010) · Neuron · doi:10.1016/j.neuron.2010.05.008 · Cited by 958 · see citing works
Mouse behavioral tasks relevant to autism: Phenotypes of 10 inbred strains
MOY, S., NADLER, J., YOUNG, N., PEREZ, A., HOLLOWAY, L., BARBARO, R., BARBARO, J., WILSON, L., THREADGILL, D., & LAUDER, J. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.07.030 · Cited by 776 · see citing works
Maternal metabolic conditions and risk for autism and other neurodevelopmental disorders
Krakowiak, P., Walker, C. K., Bremer, A. A., Baker, A. S., Ozonoff, S., Hansen, R. L., & Hertz-Picciotto, I. (2012) · PEDIATRICS · doi:10.1542/peds.2011-2583 · Cited by 675 · see citing works
Automated Three‐Chambered Social Approach Task for Mice
Yang, M., Silverman, J. L., & Crawley, J. N. (2011) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0826s56 · Cited by 598 · see citing works
Designing mouse behavioral tasks relevant to autistic‐like behaviors
Crawley, J. N. (2004) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.20039 · Cited by 520 · see citing works
Ultrasound for fetal assessment in early pregnancy
Whitworth, M. K., Bricker, L., & Mullan, C. (2015) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd007058.pub3 · Cited by 497 · see citing works
The anatomical basis of mouse development
Kaufman, M. H., & Bard, J. (1999) · Medical Entomology and Zoology · Cited by 365 · see citing works
Advancing Maternal Age Is Associated With Increasing Risk for Autism: A Review and Meta-Analysis
Sandin, S., Hultman, C. M., Kolevzon, A. L., Gross, R., MacCabe, J. H., & Reichenberg, A. (2012) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2012.02.018 · Cited by 333 · see citing works
Prenatal exposure to ultrasound waves impacts neuronal migration in mice
Ang, E. S. B. C., Gluncic, V., Duque, A., Schafer, M. E., & Rakic, P. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605294103 · Cited by 265 · see citing works
Guidelines for safe work practices in human and animal medical diagnostic laboratories
Miller, M. J., Astles, R., Baszler, T. V., Chapin, K. C., Carey, R. A., Garcia, L. S., Gray, L. D., Larone, D. H., Pentella, M., Pollock, A., et al. (2012) · Cited by 209 · see citing works
Viñuela, A., Aparicio, M. A., Berrebi, A. S., & Saldaña, E. (2011) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2011.00001 · Cited by 182 · see citing works
Handedness patterns in autism suggest subtypes
Soper, H. V., Satz, P., Orsini, D. L., Henry, R. R., Zvi, J. C., & SCHULMAN, M. L. (1986) · Journal of Autism and Developmental Disorders · doi:10.1007/bf01531727 · Cited by 128 · see citing works
Newnham, J. P., Doherty, D. A., Kendall, G. E., Zubrick, S. R., LANDAU, L. I., & Stanley, F. J. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17516-8 · Cited by 128 · see citing works
Prevalence of autism spectrum disorders in an Icelandic birth cohort
Sæmundsen, E., Magnússon, P., Georgsdóttir, I., Egilsson, E., & Rafnsson, V. (2013) · BMJ Open · doi:10.1136/bmjopen-2013-002748 · Cited by 126 · see citing works
Matson, J. L., Rieske, R. D., & Williams, L. W. (2013) · Research in Developmental Disabilities · doi:10.1016/j.ridd.2013.05.021 · Cited by 124 · see citing works
Phillips, R. D. (2008) · Cited by 121 · see citing works
Ultrasonic imaging: safety considerations
Haar, G. T. (2011) · Interface Focus · doi:10.1098/rsfs.2011.0029 · Cited by 120 · see citing works
Postnatal lesion evidence against a primary role for the corpus callosum in mouse sociability
Yang, M., Clarke, A. M., & Crawley, J. N. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06714.x · Cited by 117 · see citing works
Lyall, K., Pauls, D. L., Spiegelman, D. L., Ascherio, A., & Santangelo, S. L. (2011) · Autism Research · doi:10.1002/aur.228 · Cited by 111 · see citing works
Principles of Behavioral Teratology
Vorhees, C. V. (1986) · Springer eBooks · doi:10.1007/978-1-4613-2189-7_2 · Cited by 110 · see citing works
Ultrasound for fetal assessment in early pregnancy
Whitworth, M. K., Bricker, L., Neilson, J. P., & Dowswell, T. (2010) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd007058.pub2 · Cited by 108 · see citing works
Handedness, eyedness and nasal cycle in children with autism
Dane, Ş., & Balci, N. (2007) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2007.03.005 · Cited by 103 · see citing works
Parental Age and Risk of Autism Spectrum Disorders in a Finnish National Birth Cohort
Lampi, K. M., Hinkka‐Yli‐Salomäki, S., Lehti, V., Helenius, H. Y. M., Gissler, M., Brown, A. S., & Sourander, A. (2013) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-013-1801-3 · Cited by 77 · see citing works
An incidence study of diagnosed autism-spectrum disorders among immigrants to The Netherlands
van der Ven, E., Termorshuizen, F., Laan, W., Breetvelt, E. J., van Os, J., & Selten, J. P. (2013) · Acta Psychiatrica Scandinavica · doi:10.1111/acps.12054 · Cited by 57 · see citing works
Signaling Mechanisms in Cortical Axon Growth, Guidance, and Branching
Kalil, K., Li, L., & Hutchins, B. I. (2011) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2011.00062 · Cited by 56 · see citing works
Fetal stimulation by pulsed diagnostic ultrasound.
Fatemi, M., Ogburn, P. L., & Greenleaf, J. F. (2001) · Journal of Ultrasound in Medicine · doi:10.7863/jum.2001.20.8.883 · Cited by 54 · see citing works
Tarantal, A. F., & Hendrickx, A. G. (1989) · Teratology · doi:10.1002/tera.1420390207 · Cited by 51 · see citing works
Ultrasound exposure of the foetal chick brain: effects on learning and memory
Schneider, M. E., Ayobi, Z., Lombardo, P., Brown, D., Kedang, B., & Gibbs, M. E. (2009) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2009.07.007 · Cited by 49 · see citing works
“Ultrasound Physics and Technology, How, Why and When?”
Mulloy, B. (2009) · Radiography · doi:10.1016/j.radi.2009.10.013 · Cited by 49 · see citing works
Salvesen, K. Å. (2002) · European Journal of Ultrasound · doi:10.1016/s0929-8266(02)00038-1 · Cited by 42 · see citing works
Hinoue, A., Fushiki, S., Nishimura, Y., & Shiota, K. (2001) · Developmental Brain Research · doi:10.1016/s0165-3806(01)00295-4 · Cited by 37 · see citing works
Compilation of reported biological effects data and ultrasound exposure levels
Stewart, H. D., Stewart, H. F., Moore, R. M., & Garry, J. (1985) · Journal of Clinical Ultrasound · doi:10.1002/jcu.1870130304 · Cited by 36 · see citing works
Diagnostic levels of ultrasound may disrupt myelination
Ellisman, M. H., Palmer, D. E., & André, M. P. (1987) · Experimental Neurology · doi:10.1016/0014-4886(87)90073-2 · Cited by 34 · see citing works
Epidemiological prenatal ultrasound studies
Salvesen, K. Å. (2006) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2006.07.013 · Cited by 30 · see citing works
Effect of Fetal Exposure to Ultrasound on the Behavior of the Adult Mouse
Devi, P. U., Suresh, R., & Hande, M. P. (1995) · Radiation Research · doi:10.2307/3579009 · Cited by 30 · see citing works
Antenatal Ultrasound and Risk of Autism Spectrum Disorders
Grether, J. K., Li, S. X., Yoshida, C. K., & Croen, L. (2009) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-009-0859-4 · Cited by 30 · see citing works
Do We Need to Restrict the Use of Doppler Ultrasound in the First Trimester of Pregnancy?
ter Haar, G., Abramowicz, J. S., Akiyama, I., Evans, D. H., Ziskin, M. C., & Maršál, K. (2013) · Ultrasound in Medicine & Biology · doi:10.1016/j.ultrasmedbio.2012.11.024 · Cited by 29 · see citing works
Prenatal exposure to ultrasound waves: is there a risk?
Abramowicz, J. S. (2007) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.3983 · Cited by 29 · see citing works
Effect of diagnostic ultrasound during the fetal period on learning and memory in mice
Suresh, R., Rao, T. R., Davis, E. M., Ovchinnikov, N. A., & Rae, A. M. (2007) · Annals of Anatomy - Anatomischer Anzeiger · doi:10.1016/j.aanat.2007.04.008 · Cited by 28 · see citing works
Stoch, Y. K., Williams, C. J., Granich, J., Hunt, A. M., Landau, L. I., Newnham, J. P., & Whitehouse, A. (2012) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-012-1526-8 · Cited by 25 · see citing works
Potential teratogenic effects of ultrasound on corticogenesis: Implications for autism
Williams, E. L., & Casanova, M. F. (2010) · Medical Hypotheses · doi:10.1016/j.mehy.2010.01.027 · Cited by 24 · see citing works
Conclusions Regarding Epidemiology for Obstetric Ultrasound
Abramowicz, J. S., Fowlkes, J. B., Skelly, A. C., Stratmeyer, M. E., & Ziskin, M. C. (2008) · Journal of Ultrasound in Medicine · doi:10.7863/jum.2008.27.4.637 · Cited by 22 · see citing works
Abramowicz, J. S. (2012) · Journal of Ultrasound in Medicine · doi:10.7863/jum.2012.31.8.1261 · Cited by 19 · see citing works
Sheiner, E., & Abramowicz, J. S. (2008) · Journal of Ultrasound in Medicine · doi:10.7863/jum.2008.27.4.499 · Cited by 18 · see citing works
Immune tolerance induction for treating inhibitors in people with congenital haemophilia A or B
Athale, A., Marcucci, M., & Iorio, A. (2014) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd010561.pub2 · Cited by 15 · see citing works
Stålberg, K., Axelssön, O., Haglund, B., Hultman, C. M., Lambe, M. P., & Kieler, H. (2009) · Ultrasound in Obstetrics and Gynecology · doi:10.1002/uog.7332 · Cited by 13 · see citing works
Effects of Prenatal Ultrasound Exposure on Adult Offspring Behavior in the Wistar Rat
Jensh, R. P., Lewin, P. A., Poczobutt, M. T., Goldberg, B. B., Oler, J., Goldman, M. P., & Brent, R. L. (1995) · Experimental Biology and Medicine · doi:10.3181/00379727-210-43937 · Cited by 13 · see citing works
Suresh, R., Devi, P. U., Ovchinnikov, N. A., & McRae‐Degueurce, A. (2002) · Life Sciences · doi:10.1016/s0024-3205(02)01642-9 · Cited by 13 · see citing works
FDA cautions against ultrasounds 'keepsake' images.
Rados, C. (2004) · PubMed · Cited by 10 · see citing works
Therapeutic ultrasound with an emphasis on applications to the brain
Mourad, P. D. (2012) · Elsevier eBooks · doi:10.1533/9780857096302.3.545 · Cited by 7 · see citing works
Self-citationReassessment of teratogenic risk from antenatal ultrasound
Williams, E. L., & Casanova, M. (2013) · Translational Neuroscience · doi:10.2478/s13380-013-0112-7 · Cited by 5 · see citing works
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- Authors
- McClintic, A. M., King, B. H., Webb, S. J., & Mourad, P. D.
- Affiliations
- University of Washington (US)
- Seattle Children's Hospital (US)
- Corresponding author
- Mourad, Pierre D.
- Venue
- Autism Research
- Publisher
- Wiley
- Published
- 2013-11-18
- Volume
- 7
- Issue
- 3
- Pages
- 295-304
- ISSN
- 1939-3792 (ISSN-L)
- 1939-3806
- PMC
- PMC4025980
- OpenAlex
- W2158535237
- Cited by
- 25
- References
- 53
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 1 · 2023: 3 · 2022: 1 · 2021: 1 · 2020: 3 · 2019: 2 · 2018: 3 · 2017: 2 · 2016: 2 · 2015: 2 · 2014: 1 · 2013: 1
- FWCI
- 1.09
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Autism Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute of Child Health and Human Development (P30 HD002274)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
- Physical Sciences › Engineering › Biomedical Engineering › Ultrasound and Hyperthermia Applications
- Keywords
- ultrasonography, prenatal ultrasound exposure, prenatal ultrasound, social behavior, sociability, autism spectrum disorder, mouse model, fetal brain development, non-right-handedness, exploratory activity
- MeSH terms
- Animals, Behavior, Animal, Female, Humans, Male, Pregnancy, Prenatal Exposure Delayed Effects, Risk Factors, Social Behavior, Ultrasonography, Prenatal, Mice
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