Ultrasound and fetal magnetic resonance imaging: Clinical performance in the prenatal diagnosis of orofacial clefts and mandibular abnormalities
Corresponding Author
Gabriele Tonni
Prenatal Diagnostic Centre, Department of Obstetrics and Neonatology, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), AUSL Reggio Emilia, Reggio Emilia, Italy
Correspondence
Gabriele Tonni, Prenatal Diagnostic Centre, Department of Obstetrics and Neonatology, and Researcher, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), AUSL Reggio Emilia, Reggio Emilia, Italy.
Email: [email protected]
Search for more papers by this authorAlberto Borges Peixoto
Department of Obstetrics and Gynecology, Federal University of Triângulo Mineiro (UFTM), Uberaba, Brazil
Search for more papers by this authorHeron Werner
Department of Fetal Medicine, Clínica de Diagnóstico por Imagem (CDPI - DASA), Rio de Janeiro, Brazil
Search for more papers by this authorGianpaolo Grisolia
Department of Obstetrics and Gynecology, Carlo Poma Hospital, ASST Mantova, Mantova, Italy
Search for more papers by this authorRodrigo Ruano
Division of Maternal-Fetal Medicine, UH Jackson Fetal Care, Miller School of Medicine, University of Miami, Miami, Florida, USA
Search for more papers by this authorFrancisco Sepulveda
FETALMED–Maternal-Fetal Diagnostic Center, Fetal Imaging Unit, Santiago, Chile
Search for more papers by this authorWaldo Sepulveda
FETALMED–Maternal-Fetal Diagnostic Center, Fetal Imaging Unit, Santiago, Chile
Search for more papers by this authorEdward Araujo Júnior
Department of Obstetrics, Paulista School of Medicine, Federal University of São Paulo (EPM-UNIFESP), São Paulo, Brazil
Search for more papers by this authorCorresponding Author
Gabriele Tonni
Prenatal Diagnostic Centre, Department of Obstetrics and Neonatology, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), AUSL Reggio Emilia, Reggio Emilia, Italy
Correspondence
Gabriele Tonni, Prenatal Diagnostic Centre, Department of Obstetrics and Neonatology, and Researcher, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS), AUSL Reggio Emilia, Reggio Emilia, Italy.
Email: [email protected]
Search for more papers by this authorAlberto Borges Peixoto
Department of Obstetrics and Gynecology, Federal University of Triângulo Mineiro (UFTM), Uberaba, Brazil
Search for more papers by this authorHeron Werner
Department of Fetal Medicine, Clínica de Diagnóstico por Imagem (CDPI - DASA), Rio de Janeiro, Brazil
Search for more papers by this authorGianpaolo Grisolia
Department of Obstetrics and Gynecology, Carlo Poma Hospital, ASST Mantova, Mantova, Italy
Search for more papers by this authorRodrigo Ruano
Division of Maternal-Fetal Medicine, UH Jackson Fetal Care, Miller School of Medicine, University of Miami, Miami, Florida, USA
Search for more papers by this authorFrancisco Sepulveda
FETALMED–Maternal-Fetal Diagnostic Center, Fetal Imaging Unit, Santiago, Chile
Search for more papers by this authorWaldo Sepulveda
FETALMED–Maternal-Fetal Diagnostic Center, Fetal Imaging Unit, Santiago, Chile
Search for more papers by this authorEdward Araujo Júnior
Department of Obstetrics, Paulista School of Medicine, Federal University of São Paulo (EPM-UNIFESP), São Paulo, Brazil
Search for more papers by this authorAbstract
Cleft lip, with or without cleft palate, is the most common congenital craniofacial anomaly and the second most common birth defect worldwide. Micrognathia is a rare facial malformation characterized by small, underdeveloped mandible and frequently associated with retrognathia. Second- and third-trimester prenatal ultrasound is the standard modality for screening and identification of fetal orofacial abnormalities, with a detection rate in the low-risk population ranging from 0% to 73% for all types of cleft. The prenatal ultrasonography detection can also be performed during the first trimester of pregnancy. Given the potential limitations of obstetric ultrasound for examining the fetal face, such as suboptimal fetal position, shadowing from the surrounding bones, reduce amniotic fluid around the face, interposition of fetal limbs, umbilical cord and placenta, and maternal habitus/abdominal scars, the use of adjunct imaging modalities can enhance prenatal diagnosis of craniofacial anomalies in at-risk pregnancies. Fetal magnetic resonance imaging (MRI) is a potentially useful second-line investigation for the prenatal diagnosis of orofacial malformations with a pooled sensitivity of 97%. In this review, we discuss the role of ultrasound and fetal MRI in the prenatal assessment of abnormalities of the upper lip, palate, and mandible.
Open Research
DATA AVAILABILITY STATEMENT
Data sharing not applicable to this article as no datasets were generated or analyzed during this review.
REFERENCES
- 1Stewart RE. Craniofacial malformations: clinical and genetic considerations. Pediatr Clin North Am. 1978; 25: 485-515.
- 2Vanderas AP. Incidence of cleft lip, cleft palate, and cleft lip and palate among races: a review. Cleft Palate J. 1987; 24: 216-225.
- 3Stoll C, Alembik Y, Dott B, Roth MP. Associated malformations in cases with oral clefts. Cleft Palate Craniofac J. 2000; 37: 41-47.
- 4Tonni G, Rosignoli L, Palmisano M, Sepulveda W. Early detection of cleft lip by three-dimensional transvaginal ultrasound in niche mode in a fetus with trisomy 18 diagnosed by celocentesis. Cleft Palate Craniofac J. 2016; 53: 745-748.
- 5Arangio P, Manganaro L, Pacifici A, Basile E, Cascone P. Importance of fetal MRI in evaluation of craniofacial deformities. J Craniofac Surg. 2013; 24: 773-776.
- 6Pugash D, Brugger PC, Bettelheim D, Prayer D. Prenatal ultrasound and fetal MRI: the comparative value of each modality in prenatal diagnosis. Eur J Radiol. 2008; 68: 214-226.
- 7Descamps MJ, Golding SJ, Sibley J, et al. MRI for definitive in utero diagnosis of cleft palate: a useful adjunct to antenatal care? Cleft Palate Craniofac J. 2010; 47: 578-585.
- 8Rosignoli L, Tonni G. Uniletaral agenesis of the mandible associated with 4p−/10q duplication in a paternal carrier state: multidisciplinary management of a complex case. In: G Tonni, W Sepulveda, AE Wong, eds. Prenatal Diagnosis of Orofacial Malformations. Springer International Publishing; 2017: 199-204.
10.1007/978-3-319-32516-3_18 Google Scholar
- 9Tonni G, Sepulveda W, Wong AE. What we know and what we should know about cleft lip and palate. In: G Tonni, W Sepulveda, AE Wong, eds. Prenatal Diagnosis of Orofacial Malformations. Springer International Publishing; 2017: 3-7.
10.1007/978-3-319-32516-3_1 Google Scholar
- 10Chaoui R, Orosz G, Heling KS, Sarut-Lopez A, Nicolaides KH. Maxillary gap at 11-13 weeks' gestation: marker of cleft lip and palate. Ultrasound Obstet Gynecol. 2015; 46: 665-669.
- 11Sepulveda W, Wong AE, Martinez-Ten P, et al. Retronasal triangle: a sonographic landmark for the screening of cleft palate in the first trimester. Ultrasound Obstet Gynecol. 2010; 35: 7-13.
- 12Tonni G, Grisolia G, Sepulveda W. Early prenatal diagnosis of orofacial clefts: evaluation of the retronasal triangle using a new three-dimensional reslicing technique. Fetal Diagn Ther. 2013; 34: 31-37.
- 13Wu S, Han J, Zhen L, Ma Y, Li D, Liao C. Prospective ultrasound diagnosis of orofacial clefts in the first trimester. Ultrasound Obstet Gynecol. 2021; 58: 134-137.
- 14De Robertis V, Rembouskos G, Fanelli T, et al. Cleft palate with or without cleft lip: the role of retronasal triangle view and maxillary gap at 11-14 weeks. Fetal Diagn Ther. 2019; 46: 353-359.
- 15Sepulveda W, Wong AE, Viñals F, Andreeva E, Adzehova N, Martinez-ten P. Absent mandibular gap in the retronasal triangle view: a clue to the diagnosis of micrognathia in the first trimester. Ultrasound Obstet Gynecol. 2012; 39: 152-156.
- 16Martinez-Ten P, Adiego B, Illescas T, et al. First-trimester diagnosis of cleft lip and palate using three-dimensional ultrasound. Ultrasound Obstet Gynecol. 2012; 40: 40-46.
- 17Maarse W, Bergé SJ, Pistorius L, et al. Diagnostic accuracy of transabdominal ultrasound in detecting prenatal cleft lip and palate: a systematic review. Ultrasound Obstet Gynecol. 2010; 35: 495-502.
- 18Maarse W, Pistorius LR, Van Eeten WK, et al. Prenatal ultrasound screening for orofacial clefts. Ultrasound Obstet Gynecol. 2011; 38: 434-439.
- 19To WW. Prenatal diagnosis and assessment of facial clefts: where are we now? Hong Kong Med J. 2012; 18: 146-152.
- 20Salomon LJ, Alfirevic Z, Berghella V, et al. ISUOG practice guidelines (updated): performance of the routine mid-trimester fetal ultrasound scan. Ultrasound Obstet Gynecol. 2022; 59: 840-856.
- 21Rotten D, Levaillant JM. Two- and three-dimensional sonographic assessment of the fetal face. 1. A systematic analysis of the normal face. Ultrasound Obstet Gynecol. 2004; 23: 224-231.
- 22Benacerraf BR, Bromley B, Jelin AC. Society for maternal-fetal medicine. Paramedian orofacial cleft. Am J Obstet Gynecol. 2019; 221: B8-B12.
- 23Pilu G, Segata M. A novel technique for visualization of the normal and cleft fetal secondary palate: angled insonation and three-dimensional ultrasound. Ultrasound Obstet Gynecol. 2007; 29: 166-169.
- 24Fuchs F, Grosjean F, Captier G, Faure JM. The 2D axial transverse views of the fetal face: a new technique to visualize the fetal hard palate; methodology description and feasibility. Prenat Diagn. 2017; 37: 1353-1359.
- 25Frisova V, Cojocaru L, Turan S. A new two-dimensional sonographic approach to the assessment of the fetal hard and soft palates. J Clin Ultrasound. 2021; 49: 8-11.
- 26AIUM practice parameter for the performance of detailed second- and third-trimester diagnostic obstetric ultrasound examinations. J Ultrasound Med. 2019; 38: 3093-3100.
- 27Tutschek B, Blaas HK, Abramowicz J, et al. Three-dimensional ultrasound imaging of the fetal skull and face. Ultrasound Obstet Gynecol. 2017; 50: 7-16.
- 28Saikh D, Mercer NS, Sohan K, et al. Prenatal diagnosis of cleft lip and palate. Br J Plast Surg. 2001; 54: 288-289.
- 29Tonni G, Centini G, Rosignoli L. Prenatal screening for fetal face and clefting in a prospective study on low-risk population: can 3- and 4-dimensional ultrasound enhance visualization and detection rate? Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2005; 100: 420-426.
- 30Tessier P. Anatomical classification facial, cranio-facial and latero-facial clefts. J Maxillofac Surg. 1976; 4: 69-92.
- 31Kernahan DA, Stark RB. A new classification for cleft lip and cleft palate. Plast Reconstr Surg Transplant Bull. 1958; 22: 435-441.
- 32Millard T, Richman LC. Different cleft conditions, facial appearance, and speech: relationship to psychological variables. Cleft Palate Craniofac J. 2001; 38: 68-75.
- 33Martinez-Ten P, Sepulveda W, Wong AE, et al. The role of 2D/3D/4D ultrasound in the prenatal assessment of cleft lip and palate. In: G Tonni, W Sepulveda, AE Wong, eds. Prenatal Diagnosis of Orofacial Malformations. Springer International Publishing; 2017: 43-59.
10.1007/978-3-319-32516-3_4 Google Scholar
- 34Cash C, Set P, Coleman N. The accuracy of antenatal ultrasound in the detection of facial clefts in a low-risk screening population. Ultrasound Obstet Gynecol. 2001; 18: 432-436.
- 35Tonni G, Lituania M. OmniView algorithm: a novel 3-dimensional sonographic technique in the study of the fetal hard and soft palates. J Ultrasound Med. 2012; 31: 313-318.
- 36Campbell S, Lees C, Moscoso G, Hall P. Ultrasound antenatal diagnosis of cleft palate by a new technique: the 3D "reverse face" view. Ultrasound Obstet Gynecol. 2005; 25: 12-18.
- 37Platt LD, Devore GR, Pretorius DH. Improving cleft palate/cleft lip antenatal diagnosis by 3-dimensional sonography: the "flipped face" view. J Ultrasound Med. 2006; 25: 1423-1430.
- 38Martinez-Ten P, Perez-Pedregoza J, Santacruz B, et al. Three-dimensional ultrasound diagnosis of cleft palate: 'reverse face', 'flipped face' or 'oblique face'—which method is best? Ultrasound Obstet Gynecol. 2009; 33: 399-406.
- 39Gillham JC, Anand S, Bullen PJ. Antenatal detection of cleft lip with or without cleft palate: incidence of associated chromosomal and structural anomalies. Ultrasound Obstet Gynecol. 2009; 34: 410-415.
- 40Offerdal K, Jebens N, Syvertsen T, Blaas HGK, Johansen OJ, Eik-Nes SH. Prenatal ultrasound detection of facial clefts: a prospective study of 49,314 deliveries in a non-selected population in Norway. Ultrasound Obstet Gynecol. 2008; 31: 639-646.
- 41Lituania M, Tonni G. Bifid uvula and familial stickler syndrome diagnosed prenatally before the sonographic "equals sign" landmark. Arch Gynecol Obstet. 2013; 288: 483-487.
- 42Tonni G, Grisolia G. Fetal uvula: navigating and lightening the soft palate using HDlive. Arch Gynecol Obstet. 2013; 288: 239-244.
- 43Paladini D. Fetal micrognathia: almost always an ominous finding. Ultrasound Obstet Gynecol. 2010; 35: 377-384.
- 44Rotten D, Levaillant JM, Martinez H, le pointe HD, Vicaut É. The fetal mandible: a 2D and 3D sonographic approach to the diagnosis of retrognathia and micrognathia. Ultrasound Obstet Gynecol. 2002; 19: 122-130.
- 45Otto C, Platt LD. The fetal mandible measurement: an objective determination of fetal jaw size. Ultrasound Obstet Gynecol. 1991; 1: 12-17.
- 46Paladini D, Morra T, Teodoro A, et al. Objective diagnosis of micrognathia in the fetus: the jaw index. Obstet Gynecol. 1999; 93: 382-386.
- 47Chitty LS, Campbell S, Altman DG. Measurement of the fetal mandible-feasibility and construction of a centile chart. Prenat Diagn. 1993; 13: 749-756.
- 48Watson WJ, Katz VL. Sonographic measurement of the fetal mandible: standards for normal pregnancy. Am J Perinatol. 1993; 10: 226-228.
- 49Zalel Y, Gindes L, Achiron R. The fetal mandible: an in utero sonographic evaluation between 11 and 31 weeks' gestation. Prenat Diagn. 2006; 26: 163-167.
- 50Goldstein I, Reiss A, Rajamim BS, Tamir A. Nomogram of maxillary bone length in normal pregnancies. J Ultrasound Med. 2005; 24: 1229-1233.
- 51Tsai MY, Lan KC, Ou CY, Chen JH, Chang SY, Hsu TY. Assessment of the facial features and chin development of fetuses with use of serial three-dimensional sonography and the mandibular size monogram in a Chinese population. Am J Obstet Gynecol. 2004; 190: 541-546.
- 52de Jong-Pleij EA, Ribbert LS, Manten GT, et al. Maxilla-nasion-mandible angle: a new method to assess profile anomalies in pregnancy. Ultrasound Obstet Gynecol. 2011; 37: 562-569.
- 53Lee W, McNie B, Chaiworapongsa T, et al. Three-dimensional ultrasonographic presentation of micrognathia. J Ultrasound Med. 2002; 21: 775-781.
- 54Menezes AG, Araujo Junior E, Lopes J, et al. Prenatal diagnosis and physical model reconstruction of agnathia-otocephaly with limb deformities (absent ulna, fibula and digits) following maternal exposure to oxymetazoline in the first trimester. J Obstet Gynecol Res. 2016; 42: 1016-1020.
- 55Wang LM, Leung KY, Tang M. Prenatal evaluation of 571 facial clefts by three-dimensional extended imaging. Prenat Diagn. 2007; 27: 722-729.
- 56Sepulveda W, Ximenes R, Wong AE, Sepulveda F, Martinez-ten P. Fetal magnetic resonance imaging and three-dimensional ultrasound in clinical practice: applications in prenatal diagnosis. Best Pract Res Clin Obstet Gynaecol. 2012; 26: 593-624.
- 57Laifer-Narin S, Schlechtweg K, Lee J, et al. A comparison of early versus late prenatal magnetic resonance imaging in the diagnosis of cleft palate. Ann Plast Surg. 2019; 82(4 S Suppl 3): S242-S246.
- 58Manganaro L, Tomei A, Fierro F, et al. Fetal MRI as a complement to US in the evaluation of cleft lip and palate. Radiol Med. 2011; 116: 1134-1148.
- 59Sepulveda F, Gruber GM, Prayer D. Magnetic resonance imaging (MRI) in the evaluation of the fetal face. In: G Tonni, W Sepulveda, AE Wong, eds. Prenatal Diagnosis of Orofacial Malformations. Cham; 2017: 119-130.
10.1007/978-3-319-32516-3_8 Google Scholar
- 60Mirsky DM, Shekdar KV, Bilaniuk LT. Fetal MRI: head and neck. Magn Reson Imaging Clin N Am. 2012; 20: 605-618.
- 61Van der Hoek-Snieders H, van den Heuvel A, van Os-Medendorp H, et al. Diagnostic accuracy of fetal MRI to detect cleft palate: a meta-analysis. Eur J Pediatr. 2020; 179: 29-38.
- 62Lakshmy SR, Deepa S, Rose N, Mookan S, Agnees J. First-trimester sonographic evaluation of palatine clefts: a novel diagnostic approach. J Ultrasound Med. 2017; 36: 1397-1414.
- 63Li W-J, Wang X-Q, Yan RL, Xiang JW. Clinical significance of first-trimester screening of the retronasal triangle for identification of primary cleft palate. Fetal Diagn Ther. 2015; 38: 135-141.
- 64Berggren H, Hansson E, Uvemark A, Svensson H, Sladkevicius P, Becker M. Prenatal ultrasound detection of cleft lip, or cleft palate, or both, in southern Sweden, 2006-2010. J Plast Surg Hand Surg. 2012; 46: 69-74.
- 65Gindes L, Weissmann-Brenner A, Zajicek M, et al. Three-dimensional ultrasound demonstration of the fetal palate in high-risk patients: the accuracy of prenatal visualization. Prenat Diagn. 2013; 33: 436-441.
- 66Fleurke-Rozema JH, van de Kamp K, Bakker MK, Pajkrt E, Bilardo CM, Snijders RJM. Prevalence, diagnosis and outcome of cleft lip with or without cleft palate in The Netherlands. Ultrasound Obstet Gynecol. 2016; 48: 458-463.