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Prenatal diagnosis of intraconal lymphatic malformation on fetal magnetic resonance imaging
Journal Pre-proof Prenatal diagnosis of intraconal lymphatic malformation on fetal MRI Crystal SY. Cheung, MD FRCSC, Edward Yang, MD PhD, Richard L. Robertson, MD, Iason S. Mantagos, MD PII:
S1091-8531(20)30019-7
DOI:
https://doi.org/10.1016/j.jaapos.2019.12.005
Reference:
YMPA 3135
To appear in:
Journal of AAPOS
Received Date: 22 September 2019 Revised Date:
3 December 2019
Accepted Date: 12 December 2019
Please cite this article as: Cheung CS, Yang E, Robertson RL, Mantagos IS, Prenatal diagnosis of intraconal lymphatic malformation on fetal MRI, Journal of AAPOS (2020), doi: https://doi.org/10.1016/ j.jaapos.2019.12.005. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Copyright © 2020, American Association for Pediatric Ophthalmology and Strabismus. Published by Elsevier Inc. All rights reserved.
Prenatal diagnosis of intraconal lymphatic malformation on fetal magnetic resonance imaging Crystal S. Y. Cheung, MD, FRCSC,a Edward Yang, MD, PhD,b Richard L. Robertson, MD,b and Iason S. Mantagos, MD, PhDa Author affiliations: aDepartment of Ophthalmology, Boston Children’s Hospital, Boston, Massachusetts; bDepartment of Radiology, Boston Children’s Hospital, Boston, Massachusetts Submitted September 22, 20219. Revision accepted December 12, 2019. Correspondence: Crystal SY Cheung, MD, FRCSC, Boston Children’s Hospital, 300 Longwood Avenue, Fegan 4, Boston, MA 02115 (email: [email protected]). Word count: 896
Lymphatic malformations are benign hamartomatous tumors present at birth but usually diagnosed in early childhood. We report a case of prenatal diagnosis of an isolated unilateral retrobulbar lymphatic malformation with fetal magnetic resonance imaging (MRI). This was first detected at 27 weeks’ gestational age. Postnatal ocular examinations at 4 days and 5 weeks of age showed no signs of optic nerve compromise. Postnatal MRI at 18 days of age showed slight increase in size of the lesion, and no intracranial vascular malformations were detected. Case Report A small cystic orbital lesion was detected in an unborn infant at 27 weeks’ gestational age (GA) on fetal magnetic resonance imaging (MRI), which the patient’s mother (gravid 3, para 1) had undergone as a control subject in a research study (see eSupplement 1A, available at jaapos.org). At 36 weeks’ GA, a repeat fetal MRI was performed, according to the research protocol, and a 7 mm cystic lesion in the intraconal space without intracranial abnormities was identified (Figure 1). There was no family history of periorbital vascular malformations in childhood. A comprehensive ophthalmic examination was performed at 4 days of age at Boston Children’s Hospital. Visual acuity was blink to light in each eye, without a relative afferent pupillary defect. Extraocular motility was limited by age but full in both eyes. On external examination, there was no discoloration or swelling of the eyelid. Mild resistance to retropulsion of the right eye was appreciated, but no clinical proptosis was found, and no proptosis was observed with crying. Intraocular pressure was 9 mm Hg in the right eye, 8 mm Hg in the left eye. On dilated fundus examination there was no optic nerve swelling or pallor. Cycloplegic refraction was +1.00 +1.25 ×090 in the right eye and +1.25 +1.00 ×090 in the left eye.
A follow-up MRI with contrast of the brain and orbits was performed at 18 days of age. It showed a slightly increased, well-demarcated 10 × 10 × 11 mm lobulated T2-weighted hyperintense nonenhancing lesion in the right retrobulbar intraconal orbit consistent with a lymphatic malformation (Figure 2). There was associated superomedial displacement of the right optic nerve without clear optic nerve signal abnormality (eSupplement 1B). There were no intracranial abnormalities. A repeat comprehensive ophthalmic examination was performed at 5 weeks of age, and no significant changes were noted. Discussion Conventional prenatal ultrasound examination is used as the first tool in the assessment for fetal structural abnormalities. In the last three decades, fetal MRI has continued to evolve and has become a useful adjunct to ultrasound, especially in the workup of fetal head and neck pathology.1 Since the inception of fetal MRI in the early 1980s there have been no proven harmful effects to the human fetus from limited exposure to the electromagnetic fields of MRI.2-4 In addition, there have been no long-term adverse effects demonstrated in children who were imaged as fetuses.4 To our knowledge, this is the first case report describing the detection of an isolated orbital lymphatic malformation with fetal MRI in the literature. Previous reports of prenatal diagnosis of lymphatic malformations with fetal MRI were of the neck.5 Lymphatic malformations are typically found in the neck and axilla and less frequently originate in the orbit.6 Lymphatic malformations account for 0.3%-4% of all orbital masses.7 Approximately 50% of orbital lymphatic malformation have both intraconal and extraconal compartments,8 and 22% of lesions are intraconal alone.9 In one series 50% of patients with orbital lymphatic malformations had associated intracranial vascular anomalies.10
The GA at which orbital lymphatic malformations are first detected has not been previously reported. According to the American College of Obstetricians and Gynecologists, the optimal timing for assessing fetal anatomy by ultrasound examination is 18-22 weeks’ GA.11 In studies investigating the prenatal diagnosis of head and neck lymphatic malformations using ultrasound or fetal MRI, the diagnosis occurred between 18 and 30 weeks’ GA.12 The onset of the orbital lymphatic malformation in our patient occurred prior to 27 weeks’ GA. Periorbital lymphatic malformations are often present at birth, and 77% patients develop symptoms in the first decade of life.8,9 Early presentation of periorbital lymphatic malformation may be associated with greater risk of complications and subnormal visual acuity.8 These malformations may progressively enlarge or remain clinically unapparent until they hemorrhage, which results in a mass effect that can lead to compressive optic neuropathy, globe displacement, restriction of eye movement, and amblyopia. In one series of 42 patients, 33% had amblyopia and 7% had strabismus.9 In our patient, although the MRI showed displacement of the optic nerve (eSupplement 1C), there was no clinical evidence of optic neuropathy. She also did not have any strabismus on repeated postnatal examinations. To date, our patient remains asymptomatic. The natural history of lymphatic malformations is variable and unpredictable. Although the majority of them can be observed, when intervention is required, management can be difficult.9 Early detection of this lymphatic malformation on fetal MRI, especially given the retrobulbar location in our patient, allows close monitoring for growth with the goal to preserve visual function and cosmesis. Literature Search An electronic search was conducted on August 30, 2019, using the MEDLINE database (1980 to
the present). Results were limited to articles published in English. An initial search used the MeSH terms orbital tumors, lymphangioma, and lymphatic malformation. The search was repeated with the additional qualifiers pediatric and children. All study designs were included.
References 1.
Kathary N, Bulas DI, Newman KD, Schonberg RL. MRI imaging of fetal neck masses with airway compromise: utility in delivery planning. Pediatr Radiol 2001;31:727-31.
2.
Schwartz JL, Crooks LE. NMR imaging produces no observable mutations or cytotoxicity in mammalian cells. Am J Roentgenol 1982;139:583-5.
3.
Thomas A, Morris PG. The effects of NMR exposure on living organisms. I. A microbial assay. Br J Radiol 1981;54:615-21.
4.
Baker PN, Johnson IR, Harvey PR, Gowland PA, Mansfield P. A three-year follow-up of children imaged in utero with echoplanar magnetic resonance. Am J Obstet Gynecol 1994;170:32-3.
5.
Rossi AC, Prefumo F. Additional value of fetal magnetic resonance imaging in the prenatal diagnosis of central nervous system anomalies: a systematic review of the literature. Ultrasound Obstet Gynecol 2014;44:388-93.
6.
Nihn, TN, Nihn, TX. Cystic hygroma in children: A report of 126 Cases. J Pediatr Surg 1974;9:191-5.
7.
Shields JA, Shields CL, Scartozzi R. Survey of 1264 patients with orbital tumors and simulating lesions. The 2002 Montomery Lecture, Part 1. Ophthalmology 2004;111:9971008.
8.
Tunc, M, Sadri E, Char DH. Orbital lymphangioma: An analysis of 26 patients. Br J Ophthalmol 1999;83:76.
9.
Greene AK, Burrows PE, Smith L, Mulliken JB. Periorbital lymphatic malformation: clinical course and management in 42 patients. Plast Reconstr Surg 2005;115:22-30.
10.
Katz SE, Rootman, J, Vangveeravong S, Graeb D. Combined venous lymphatic
malformations of the orbit (so-called lymphangiomas): association with noncontiguous intracranial vascular anomalies. Ophthalmology 1998;105:176-84. 11.
Committee on Practice Bulletins—Obstetrics and the American Institute of Ultrasound in Medicine. Practice Bulletin No. 175: Ultrasound in pregnancy. Obstet Gynecol 2016;128:e241-56.
12.
Tonni G, Granese T, Santana EFM, et al. Prenatally diagnosed fetal tumors of the head and neck: a systematic review with antenatal and postnatal outcomes over the past 20 year. J Perinat Med 2017;45:149-65.
Legends FIG 1. Repeat fetal magnetic resonance imaging performed using multiplanar half-Fourier acquired single-shot turbo spin-echo (HASTE), diffusion-tensor imaging (DTI), fast imaging with steady-state free precession (true FISP) sequences at 36 weeks’ gestational age showing 7 mm intraconal cystic lesion. FIG 2. Axial view of well-demarcated 10 × 10 × 11 mm lobulated lesion in the right retrobulbar intraconal orbit on T1-weighted post-contrast imaging.
S1091-8531(20)30019-7
DOI:
https://doi.org/10.1016/j.jaapos.2019.12.005
Reference:
YMPA 3135
To appear in:
Journal of AAPOS
Received Date: 22 September 2019 Revised Date:
3 December 2019
Accepted Date: 12 December 2019
Please cite this article as: Cheung CS, Yang E, Robertson RL, Mantagos IS, Prenatal diagnosis of intraconal lymphatic malformation on fetal MRI, Journal of AAPOS (2020), doi: https://doi.org/10.1016/ j.jaapos.2019.12.005. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Copyright © 2020, American Association for Pediatric Ophthalmology and Strabismus. Published by Elsevier Inc. All rights reserved.
Prenatal diagnosis of intraconal lymphatic malformation on fetal magnetic resonance imaging Crystal S. Y. Cheung, MD, FRCSC,a Edward Yang, MD, PhD,b Richard L. Robertson, MD,b and Iason S. Mantagos, MD, PhDa Author affiliations: aDepartment of Ophthalmology, Boston Children’s Hospital, Boston, Massachusetts; bDepartment of Radiology, Boston Children’s Hospital, Boston, Massachusetts Submitted September 22, 20219. Revision accepted December 12, 2019. Correspondence: Crystal SY Cheung, MD, FRCSC, Boston Children’s Hospital, 300 Longwood Avenue, Fegan 4, Boston, MA 02115 (email: [email protected]). Word count: 896
Lymphatic malformations are benign hamartomatous tumors present at birth but usually diagnosed in early childhood. We report a case of prenatal diagnosis of an isolated unilateral retrobulbar lymphatic malformation with fetal magnetic resonance imaging (MRI). This was first detected at 27 weeks’ gestational age. Postnatal ocular examinations at 4 days and 5 weeks of age showed no signs of optic nerve compromise. Postnatal MRI at 18 days of age showed slight increase in size of the lesion, and no intracranial vascular malformations were detected. Case Report A small cystic orbital lesion was detected in an unborn infant at 27 weeks’ gestational age (GA) on fetal magnetic resonance imaging (MRI), which the patient’s mother (gravid 3, para 1) had undergone as a control subject in a research study (see eSupplement 1A, available at jaapos.org). At 36 weeks’ GA, a repeat fetal MRI was performed, according to the research protocol, and a 7 mm cystic lesion in the intraconal space without intracranial abnormities was identified (Figure 1). There was no family history of periorbital vascular malformations in childhood. A comprehensive ophthalmic examination was performed at 4 days of age at Boston Children’s Hospital. Visual acuity was blink to light in each eye, without a relative afferent pupillary defect. Extraocular motility was limited by age but full in both eyes. On external examination, there was no discoloration or swelling of the eyelid. Mild resistance to retropulsion of the right eye was appreciated, but no clinical proptosis was found, and no proptosis was observed with crying. Intraocular pressure was 9 mm Hg in the right eye, 8 mm Hg in the left eye. On dilated fundus examination there was no optic nerve swelling or pallor. Cycloplegic refraction was +1.00 +1.25 ×090 in the right eye and +1.25 +1.00 ×090 in the left eye.
A follow-up MRI with contrast of the brain and orbits was performed at 18 days of age. It showed a slightly increased, well-demarcated 10 × 10 × 11 mm lobulated T2-weighted hyperintense nonenhancing lesion in the right retrobulbar intraconal orbit consistent with a lymphatic malformation (Figure 2). There was associated superomedial displacement of the right optic nerve without clear optic nerve signal abnormality (eSupplement 1B). There were no intracranial abnormalities. A repeat comprehensive ophthalmic examination was performed at 5 weeks of age, and no significant changes were noted. Discussion Conventional prenatal ultrasound examination is used as the first tool in the assessment for fetal structural abnormalities. In the last three decades, fetal MRI has continued to evolve and has become a useful adjunct to ultrasound, especially in the workup of fetal head and neck pathology.1 Since the inception of fetal MRI in the early 1980s there have been no proven harmful effects to the human fetus from limited exposure to the electromagnetic fields of MRI.2-4 In addition, there have been no long-term adverse effects demonstrated in children who were imaged as fetuses.4 To our knowledge, this is the first case report describing the detection of an isolated orbital lymphatic malformation with fetal MRI in the literature. Previous reports of prenatal diagnosis of lymphatic malformations with fetal MRI were of the neck.5 Lymphatic malformations are typically found in the neck and axilla and less frequently originate in the orbit.6 Lymphatic malformations account for 0.3%-4% of all orbital masses.7 Approximately 50% of orbital lymphatic malformation have both intraconal and extraconal compartments,8 and 22% of lesions are intraconal alone.9 In one series 50% of patients with orbital lymphatic malformations had associated intracranial vascular anomalies.10
The GA at which orbital lymphatic malformations are first detected has not been previously reported. According to the American College of Obstetricians and Gynecologists, the optimal timing for assessing fetal anatomy by ultrasound examination is 18-22 weeks’ GA.11 In studies investigating the prenatal diagnosis of head and neck lymphatic malformations using ultrasound or fetal MRI, the diagnosis occurred between 18 and 30 weeks’ GA.12 The onset of the orbital lymphatic malformation in our patient occurred prior to 27 weeks’ GA. Periorbital lymphatic malformations are often present at birth, and 77% patients develop symptoms in the first decade of life.8,9 Early presentation of periorbital lymphatic malformation may be associated with greater risk of complications and subnormal visual acuity.8 These malformations may progressively enlarge or remain clinically unapparent until they hemorrhage, which results in a mass effect that can lead to compressive optic neuropathy, globe displacement, restriction of eye movement, and amblyopia. In one series of 42 patients, 33% had amblyopia and 7% had strabismus.9 In our patient, although the MRI showed displacement of the optic nerve (eSupplement 1C), there was no clinical evidence of optic neuropathy. She also did not have any strabismus on repeated postnatal examinations. To date, our patient remains asymptomatic. The natural history of lymphatic malformations is variable and unpredictable. Although the majority of them can be observed, when intervention is required, management can be difficult.9 Early detection of this lymphatic malformation on fetal MRI, especially given the retrobulbar location in our patient, allows close monitoring for growth with the goal to preserve visual function and cosmesis. Literature Search An electronic search was conducted on August 30, 2019, using the MEDLINE database (1980 to
the present). Results were limited to articles published in English. An initial search used the MeSH terms orbital tumors, lymphangioma, and lymphatic malformation. The search was repeated with the additional qualifiers pediatric and children. All study designs were included.
References 1.
Kathary N, Bulas DI, Newman KD, Schonberg RL. MRI imaging of fetal neck masses with airway compromise: utility in delivery planning. Pediatr Radiol 2001;31:727-31.
2.
Schwartz JL, Crooks LE. NMR imaging produces no observable mutations or cytotoxicity in mammalian cells. Am J Roentgenol 1982;139:583-5.
3.
Thomas A, Morris PG. The effects of NMR exposure on living organisms. I. A microbial assay. Br J Radiol 1981;54:615-21.
4.
Baker PN, Johnson IR, Harvey PR, Gowland PA, Mansfield P. A three-year follow-up of children imaged in utero with echoplanar magnetic resonance. Am J Obstet Gynecol 1994;170:32-3.
5.
Rossi AC, Prefumo F. Additional value of fetal magnetic resonance imaging in the prenatal diagnosis of central nervous system anomalies: a systematic review of the literature. Ultrasound Obstet Gynecol 2014;44:388-93.
6.
Nihn, TN, Nihn, TX. Cystic hygroma in children: A report of 126 Cases. J Pediatr Surg 1974;9:191-5.
7.
Shields JA, Shields CL, Scartozzi R. Survey of 1264 patients with orbital tumors and simulating lesions. The 2002 Montomery Lecture, Part 1. Ophthalmology 2004;111:9971008.
8.
Tunc, M, Sadri E, Char DH. Orbital lymphangioma: An analysis of 26 patients. Br J Ophthalmol 1999;83:76.
9.
Greene AK, Burrows PE, Smith L, Mulliken JB. Periorbital lymphatic malformation: clinical course and management in 42 patients. Plast Reconstr Surg 2005;115:22-30.
10.
Katz SE, Rootman, J, Vangveeravong S, Graeb D. Combined venous lymphatic
malformations of the orbit (so-called lymphangiomas): association with noncontiguous intracranial vascular anomalies. Ophthalmology 1998;105:176-84. 11.
Committee on Practice Bulletins—Obstetrics and the American Institute of Ultrasound in Medicine. Practice Bulletin No. 175: Ultrasound in pregnancy. Obstet Gynecol 2016;128:e241-56.
12.
Tonni G, Granese T, Santana EFM, et al. Prenatally diagnosed fetal tumors of the head and neck: a systematic review with antenatal and postnatal outcomes over the past 20 year. J Perinat Med 2017;45:149-65.
Legends FIG 1. Repeat fetal magnetic resonance imaging performed using multiplanar half-Fourier acquired single-shot turbo spin-echo (HASTE), diffusion-tensor imaging (DTI), fast imaging with steady-state free precession (true FISP) sequences at 36 weeks’ gestational age showing 7 mm intraconal cystic lesion. FIG 2. Axial view of well-demarcated 10 × 10 × 11 mm lobulated lesion in the right retrobulbar intraconal orbit on T1-weighted post-contrast imaging.