Three-dimensional visualization and quantitative analysis of embryonic and fetal thigh muscles using magnetic resonance and phase-contrast X-ray imaging

Aronsson, D.D., Goldberg, M.J., Kling, T.F., Jr. & Roy, D.R. (1994)

Developmental dysplasia of the hip. Pediatrics, 94(2 Pt 1), 201–­208.

https://doi.org/10.1542/peds.94.2.201

Bardeen, C.R. (1906) Development and variation of the nerves and the

musculature of the inferior extremity and of the neighboring regions of the trunk in man. American Journal of Anatomy, 6(1), 259–­

390. https://doi.org/10.1002/aja.10000​60108

Bardeen, C.R. & Lewis, W.H. (1901) Development of the limbs, body-­wall

and back in man. American Journal of Anatomy, 1(1), 1–­35. https://

doi.org/10.1002/aja.10000​10102

Buckingham, M., Bajard, L., Chang, T., Daubas, P., Hadchouel, J.,

Meilhac, S. et al. (2003) The formation of skeletal muscle: from

somite to limb. Journal of Anatomy, 202(1), 59–­

68. https://doi.

org/10.1046/j.1469-­7580.2003.00139.x

Castiello, U. & Parma, V. (2018) Fetal kinematics: basic outcomes and

translational outlook. ACS Chemical Neuroscience, 9(2), 165–­166.

https://doi.org/10.1021/acsch​emneu​ro.8b00016

Charles, J.P., Suntaxi, F. & Anderst, W.J. (2019) In vivo human lower limb

muscle architecture dataset obtained using diffusion tensor imaging. PLoS One, 14(10), e0223531. https://doi.org/10.1371/journ​

al.pone.0223531

Christ, B. & Brand-­

Saberi, B. (2002) Limb muscle development. The

International Journal of Developmental Biology, 46(7), 905–­914.

de Vries, J.I. & Fong, B.F. (2006) Normal fetal motility: an overview.

Ultrasound in Obstetrics & Gynecology: The Official Journal of the

International Society of Ultrasound in Obstetrics and Gynecology,

27(6), 701–­711. https://doi.org/10.1002/uog.2740

Delaurier, A., Burton, N., Bennett, M., Baldock, R., Davidson, D., Mohun,

T.J. et al. (2008) The mouse limb anatomy atlas: an interactive 3D

tool for studying embryonic limb patterning. BMC Developmental

Biology, 8, 83. https://doi.org/10.1186/1471-­213x-­8-­83

Diogo, R., Siomava, N. & Gitton, Y. (2019) Development of human limb

muscles based on whole-­mount immunostaining and the links between ontogeny and evolution. Development, 146(20), dev180349.

https://doi.org/10.1242/dev.180349

Fedorov, A., Beichel, R., Kalpathy-­C ramer, J., Finet, J., Fillion-­Robin,

J.C., Pujol, S. et al. (2012) 3D slicer as an image computing platform for the quantitative imaging network. Magnetic

Resonance Imaging, 30(9), 1323–­1341. https://doi.org/10.1016/j.

mri.2012.05.001

Greiner, T.M. (2002) The morphology of the gluteus maximus during

human evolution: prerequisite or consequence of the upright bipedal posture? Human Evolution, 17, 79–­

94. https://doi.

org/10.1007/bf024​36430

Hadlock, F.P., Harrist, R.B., Deter, R.L. & Park, S.K. (1982) Fetal femur

length as a predictor of menstrual age: sonographically measured.

American Journal of Roentgenology, 138(5), 875–­878. https://doi.

org/10.2214/ajr.138.5.875

Hadlock, F.P., Harrist, R.B., Carpenter, R.J., Deter, R.L. & Park, S.K.

(1984) Sonographic estimation of fetal weight. The value of

femur length in addition to head and abdomen measurements.

Radiology, 150(2), 535–­

5 40. https://doi.org/10.1148/radio​

logy.150.2.6691115

Hogervorst, T. & Vereecke, E.E. (2014) Evolution of the human hip.

Part 2: muscling the double extension. Journal of Hip Preservation

Surgery, 2(1), 3–­14. https://doi.org/10.1093/jhps/hnu014

Huang, A.H. (2017) Coordinated development of the limb musculoskeletal system: tendon and muscle patterning and integration with

the skeleton. Developmental Biology, 429(2), 420–­428. https://doi.

org/10.1016/j.ydbio.2017.03.028

Huang, A.H., Riordan, T.J., Pryce, B., Weibel, J.L., Watson, S.S., Long,

F. et al. (2015) Musculoskeletal integration at the wrist underlies

the modular development of limb tendons. Development, 142(14),

2431–­2441. https://doi.org/10.1242/dev.122374

Ishida, H. (1972) On the muscular composition of lower extremities of

apes based on the relative weight. Journal of the Anthropological

Society of Nippon, 80(2), 125–­145. https://doi.org/10.1537/ase19​

11.80.125

Ito, J. (1996) Morphological analysis of the human lower extremity

based on the relative muscle weight. Okajimas Folia Anatomica

Japonica,

73(5),

247–­

251.

https://doi.org/10.2535/ofaj1​

936.73.5_247

Kanahashi, T., Yamada, S., Tanaka, M., Hirose, A., Uwabe, C., Kose,

K. et al. (2016) A novel strategy to reveal the latent abnormalities in human embryonic stages from a large embryo collection. Anatomical Record, 299(1), 8–­24. https://doi.org/10.1002/

ar.23281

Kurjak, A., Vecek, N., Hafner, T., Bozek, T., Funduk-­Kurjak, B. & Ujevic,

B. (2002) Prenatal diagnosis: what does four-­dimensional ultrasound add? Journal of Perinatal Medicine, 30(1), 57–­62. https://doi.

org/10.1515/JPM.2002.008

Lieberman, D.E., Raichlen, D.A., Pontzer, H., Bramble, D.M. & Cutright-­

Smith, E. (2006) The human gluteus maximus and its role in running. Journal of Experimental Biology, 209(11), 2143–­2155. https://

doi.org/10.1242/jeb.02255

Lu, Y., Yang, T., Luo, H., Deng, F., Cai, Q., Sun, W. et al. (2016)

Visualization and quantitation of fetal movements by real-­

time

three-­dimensional ultrasound with live xPlane imaging in the first

trimester of pregnancy. Croatian Medical Journal, 57(5), 474–­481.

https://doi.org/10.3325/cmj.2016.57.474

Lüchinger, A.B., Hadders-­Algra, M., van Kan, C.M. & de Vries, J.I. (2008)

Fetal onset of general movements. Pediatric Research, 63(2), 191–­

195. https://doi.org/10.1203/pdr.0b013​e3181​5ed03e

Matsuda, Y., Ono, S., Otake, Y., Handa, S., Kose, K., Haishi, T. et al. (2007)

Imaging of a large collection of human embryo using a super-­parallel

MR microscope. Magnetic Resonance in Medical Sciences: MRMS: An

Official Journal of JAPAN Society of Magnetic Resonance in Medicine,

6(3), 139–­146. https://doi.org/10.2463/mrms.6.139

Nishimura, H., Takano, K., Tanimura, T. & Yasuda, M. (1968) Normal and

abnormal development of human embryos: first report of the analysis of 1,213 intact embryos. Teratology, 1(3), 281–­290. https://doi.

org/10.1002/tera.14200​10306

Nowlan, N.C. (2015) Biomechanics of foetal movement. European Cells &

Materials, 29, 1–­21. https://doi.org/10.22203/​eCM.v029a01

1323

YAMAGUCHI et al.

Okada, M., Morimoto, M. & Kimura, T. (1996) Mobility of hindlimb joints

in Japanese macaques (Macaca fuscata) as influenced by biarticular

musculature. Folia Primatologica; International Journal of Primatology,

66(1–­4), 181–­191. https://doi.org/10.1159/00015​7193

O'Rahilly, R. & Gardner, E. (1975) The timing and sequence of events in

the development of the limbs in the human embryo. Anatomy and

Embryology, 148(1), 1–­23. https://doi.org/10.1007/bf003​15559

Pooh, R.K., Shiota, K. & Kurjak, A. (2011) Imaging of the human embryo

with magnetic resonance imaging microscopy and high-­resolution

transvaginal 3-­dimensional sonography: human embryology in the

21st century. American Journal of Obstetrics and Gynecology, 204(1),

77.e1–­77.e16. https://doi.org/10.1016/j.ajog.2010.07.028

Rodríguez, J.I., Garcia-­

Alix, A., Palacios, J. & Paniagua, R. (1988a)

Changes in the long bones due to fetal immobility caused by neuromuscular disease. A radiographic and histological study. The

Journal of Bone and Joint Surgery, 70(7), 1052–­1060. https://doi.

org/10.2106/00004​623-­19887​0 070-­0 0014

Rodríguez, J.I., Palacios, J., García-­

Alix, A., Pastor, I. & Paniagua, R.

(1988b) Effects of immobilization on fetal bone development. A

morphometric study in newborns with congenital neuromuscular diseases with intrauterine onset. Calcified Tissue International,

43(6), 335–­339. https://doi.org/10.1007/bf025​53275

Schneider, C.A., Rasband, W.S. & Eliceiri, K.W. (2012) NIH image to

ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671–­675.

https://doi.org/10.1038/nmeth.2089

Smith, B.R., Johnson, G.A., Groman, E.V. & Linney, E. (1994) Magnetic

resonance microscopy of mouse embryos. Proceedings of the

National Academy of Sciences of the United States of America, 91(9),

3530–­3533. https://doi.org/10.1073/pnas.91.9.3530

Smith, B.R., Linney, E., Huff, D.S. & Johnson, G.A. (1996) Magnetic resonance microscopy of embryos. Computerized Medical Imaging

and Graphics, 20(6), 483–­

490. https://doi.org/10.1016/s0895​

-­6111(96)00046​-­8

Stalling, D., Westerhoff, M. & Hege, H.-­C . (2005) Amira: a highly interactive system for visual data63 analysis. In: The visualization handbook. Amsterdam: Elsevier, pp. 749–­767. https://doi.org/10.1016/

b978-­01238​7582-­2/50040​-­x

Suzuki, Y., Matsubayashi, J., Ji, X., Yamada, S., Yoneyama, A., Imai, H.

et al. (2019) Morphogenesis of the femur at different stages of normal human development. PLoS One, 14(8), e0221569. https://doi.

org/10.1371/journ​al.pone.0221569

Tickle, C. (2015) How the embryo makes a limb: determination, polarity and identity. Journal of Anatomy, 227(4), 418–­430. https://doi.

org/10.1111/joa.12361

Verbruggen, S.W., Kainz, B., Shelmerdine, S.C., Hajnal, J.V., Rutherford,

M.A., Arthurs, O.J. et al. (2018) Stresses and strains on the

human fetal skeleton during development. Journal of the Royal

Society Interface, 15(138), 20170593. https://doi.org/10.1098/

rsif.2017.0593

Warmbrunn, M.V., de Bakker, B.S., Hagoort, J., Alefs-­de Bakker, P.B. &

Oostra, R.J. (2018) Hitherto unknown detailed muscle anatomy

in an 8-­week-­old embryo. Journal of Anatomy, 233(2), 243–­254.

https://doi.org/10.1111/joa.12819

Wilde, S., Feneck, E.M., Mohun, T.J. & Logan, M. (2021) 4D formation

of human embryonic forelimb musculature. Development, 148(4),

dev194746. https://doi.org/10.1242/dev.194746

Yamaguchi, Y. & Yamada, S. (2018) The Kyoto collection of human embryos and fetuses: history and recent advancements in modern

methods. Cells, Tissues, Organs, 205(5–­6), 314–­319. https://doi.

org/10.1159/00049​0672

Yamaguchi, Y., Miyazaki, R., Kamatani, M., Uwabe, C., Makishima,

H., Nagai, M. et al. (2018) Three-­dimensional models of the segmented human fetal brain generated by magnetic resonance imaging. Congenital Anomalies, 58(2), 48–­55. https://doi.org/10.1111/

cga.12229

Yoneyama, A., Yamada, S. & Takeda, T. (2011) Fine biomedical imaging using X-­

ray phase-­

sensitive technique. In: Gargiulo, G. (Ed.)

Advanced biomedical engineering. Rijeka: InTech, pp. 107–­

128.

https://doi.org/10.5772/20456

Zihlman, A.L., McFarland, R.K. & Underwood, C.E. (2011) Functional

anatomy and adaptation of male gorillas (Gorilla gorilla gorilla) with comparison to male orangutans (Pongo pygmaeus).

Anatomical Record, 294(11), 1842–­1855. https://doi.org/10.1002/

ar.21449

Ziylan, T. & Murshid, K.A. (2003) An assessment of femur growth parameters in human fetuses and their relationship to gestational age.

Turkish Journal of Medical Sciences, 33, 27–­32.

S U P P O R T I N G I N FO R M AT I O N

Additional supporting information can be found online in the

Supporting Information section at the end of this article.

How to cite this article: Yamaguchi, Y., Murase, A., Kodama, R.,

Yamamoto, A., Imai, H. & Yoneyama, A. et al. (2022) Threedimensional visualization and quantitative analysis of

embryonic and fetal thigh muscles using magnetic resonance

and phase-contrast X-ray imaging. Journal of Anatomy, 241,

1310–­1323. Available from: https://doi.org/10.1111/joa.13764

...