DOI: 10.1002/pd.4500
RESEARCH LETTER
Suspected fetal brain metallic embolic microfragment detected by MR imaging Fabio Triulzi1, Monica Fumagalli2*, Roberto Fogliani3, Claudia Cinnante1, Sabrina Avignone1, Chiara Doneda4, Simona Boito3 and Fabio Mosca2 1
Division of Neuroradiology, Fondazione IRCCS Cà Granda Ospedale Maggiore Policlinico Milano, Milan, Italy NICU, Department of Clinical Sciences and Community Health, Fondazione IRCCS Cà Granda Ospedale Maggiore Policlinico Milano, Università degli Studi di Milano, Milan, Italy 3 Division of Prenatal Diagnosis, Fondazione IRCCS Cà Granda Ospedale Maggiore Policlinico Milano, Milan, Italy 4 Division of Radiology and Neuroradiology, Children’s Hospital “V. Buzzi”, Milan, Italy *Correspondence to: Monica Fumagalli. E-mail: [email protected] 2
Funding sources: None Conflicts of interest: None declared
Brain embolic metallic microfragments are reported as a very rare consequence of mechanical prosthetic heart valve implantation or angiographic procedures using stainless steel guide wires.1–5 Extremely small metallic microemboli, as small as 0.01 mg1, are not visible on computerised tomography (CT) but can be easily detected by magnetic resonance imaging (MRI) because of their strong local field inhomogeneity causing striking ferromagnetic susceptibility artefacts. We report a case of a presumed embolic brain metallic fragment detected in a fetus by fetal MRI and confirmed by postnatal brain MR. A 29-year-old pregnant woman, gravida 3, was referred at 23 weeks’ gestation because of red cell alloimmunization. A detailed ultrasound (US) examination was performed with a multiplanar approach, and no brain abnormalities were observed. US findings were consistent with fetal anaemia: the middle cerebral artery peak systolic velocity was 65 cm/s, corresponding to 2.2 MoM6. After obtaining informed consent, a blood sampling was obtained from the placental cord insertion showing severe fetal anaemia (haemoglobin 3.9 g/dL, haematocrit 11.2%), and a fetal intravascular transfusion was performed. The procedure was carried out under ultrasound guidance (Voluson-E8 Expert ultrasound machine equipped with a 5 MH probe, GE Healthcare Ultrasound, Zipf- Austria). An echotip disposable 20 Gauge spinal needle (Cook Medical) was used to inject 47 mL of O Rhesus negative donor packed red cells (haematocrit 56.5%) into the umbilical vein. No fetal anaesthesia was administered. At the end of the procedure, the fetal haemoglobin level was 18 g/dL, and the middle cerebral artery peak systolic velocity was 34 cm/s. Neither clinical nor ultrasonographic complications were observed immediately after the procedure. After 2 h, the fetal well-being was evaluated Prenatal Diagnosis 2015, 35, 197–199
by US, and the mother was discharged. At 24 weeks’ gestation an ultrasound scan showed an atypical cerebellar shape whereby a cerebellar haemorrhage was suspected. A fetal MRI was performed at 25 weeks showing a small cerebellum with a slight asymmetry between the hemispheres and a T2 hypointensity in the most inferior part, attributable to a focal cerebellar haemorrhage. A small rounded focal cortical hypointensity was observed as well in the right parietal region on single-shot fast spin echo T2 weighted imaging (Figure 1) and on diffusion images. This finding, although in an unusual location (as situated in the most outer part of the cerebral cortex), was considered, as well as the cerebellar hypointensity, compatible with a focal hemosiderin deposit. A second fetal MRI performed at 30 weeks’ gestation confirmed these findings. These results were interpreted as showing a possible haemorrhagic complication of either severe anaemia or intrauterine transfusion, and we counselled the parents on the possible long-term impact of the larger cerebellar haemorrhage. After receiving all of the information, the parents asked to continue fetal therapy with intrauterine transfusion. The fetus received another four transfusions at 25, 28, 31 and 33 weeks’ gestation, respectively, without any complications. The baby was delivered by caesarean section at 34 weeks’ gestation after premature rupture of membranes. A postnatal brain MR scan was carried out at 40 weeks corrected age. A severe cerebellar atrophy secondary to fetal cerebellar haemorrhage was observed. The MR images also confirmed the presence of a rounded focal striking hypointensity located in the right parietal cortex which was clearly visible on fast T2 weighted images (Figure 2) but also on T1 weighted images. The T2 focal hypointensity showed a peculiar strong artefactual signal with a partly hyperintense halo, and the hypointensity was clearly enhanced on both gradient echo and © 2014 John Wiley & Sons, Ltd.
F. Triulzi et al.
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Figure 1 Fetal MRI at 25 weeks’ gestation. Single-shot fast spin echo T2 weighted sequence showed a focal rounded cortical hypointensity in the parietal region (arrow)
Figure 2 Neonatal MRI at 40 weeks corrected age. Fast spin echo T2 weighted image showed a focal striking hypointensity (arrow) with some peripheral hyperintensity typically observed in the presence of ferromagnetic artefacts
susceptibility weighted images, where some other tiny focal hypointensities became evident in the right peritrigonal white matter and in the right cortical parietal region. In order to better define the origin of this signal inhomogeneity, a CT scan was performed. This study did not reveal any focal density alteration in the right parietal region. Based on these observations, the signal abnormality in the right parietal cortex was no longer interpreted as hemosiderin deposit, yet a brain embolic metallic microfragment was suspected.
Prenatal Diagnosis 2015, 35, 197–199
Intrauterine transfusion in case of severe fetal anaemia due to red cell alloimmunization or other causes is considered a relatively safe procedure7 with a survival fetal rate of about 85% (90% in non-hydropic versus 70% in hydropic fetuses)8. Medium-term and long-term neurological sequelae have been described mainly as a result of severe anaemia rather than as consequences of the procedure itself 9. Iatrogenic brain metallic microemboli are extremely rare, and potential sources of metallic microfragments have been identified in metallic prosthetic heart valves and intravascular stainless steel guide wire applications. The presence of the aforementioned signal abnormalities at the first MRI, performed at 25 weeks’ gestation, suggests a temporal correlation between the in utero intravascular transfusion procedure, performed at 23 weeks’ gestation, and the neuroimaging appearance. We have no other good explanation for the finding. To our knowledge, this is the first case of metallic microembolism which in retrospect was already detected on fetal MR. Several neuroimaging considerations support the hypothesis of a metallic embolus: (1) the signal hypointensity (distortion) increases in those sequences that are more influenced by field inhomogeneity, (2) the artefacts present a typical hyperintense halo on T2 weighted images10 and (3) a negative CT exam excludes other sources of artefactual hypointensity (calcium, bone, air). Although it cannot be proven with absolute certainty, the needle used for intrauterine transfusion would seem to be the most likely source of metallic microembolic fragments. We hypothesise that microscopic metallic deposits may have embolized from the needle introduced into the umbilical vein and may have reached the brain through the patent foramen ovale. A neurodevelopmental follow-up has been planned for this child. However, we are uncertain about the possibility to assess the clinical relevance of the brain metallic microfragment because of the co-existence of cerebellar atrophy, secondary to the intrauterine cerebellar haemorrhage, potentially affecting her long-term neurocognitive development. WHAT’S ALREADY KNOWN ABOUT THIS TOPIC? • Brain embolic metallic microfragments are a rare consequence of mechanical prosthetic heart valves implantation or angiographic procedures performed using stainless steel guide wires.
WHAT DOES THIS STUDY ADD? • In utero intravascular procedures may represent a potential source of brain metallic microembolism for the fetus. • Brain metallic microfragments can be detected by fetal and neonatal magnetic resonance imaging.
© 2014 John Wiley & Sons, Ltd.
Suspected fetal brain metallic embolic microfragment
199
REFERENCES 1. Jassal DS, Fast MD, McGinn G. Multifocal brain MRI hypointensities secondary to cardiac catheterization. Neurology 2000;54(10):2023–4. 2. Gorriño O, Oleaga L, de la Fuente R, et al. Intracranial artifact on magnetic resonance caused by embolization of microscopic metallic fragment. Neurologia 2004;19(10):766–8. 3. Naumann M, Hofmann E, Toyka KV. Multifocal brain MRI hypointensities secondary to embolic metal fragments from a mechanical heart valve prosthesis: a possible source of epileptic seizures. Neurology 1998;51(6):1766–7. 4. Roshal D, Snapp M, Friedman DP, Zangaladze A. Iatrogenic brain and cervical cord magnetic resonance imaging susceptibility artifacts from metallic microemboli. Arch Neurol 2011;68(1):132–3. 5. Wingerchuk DM, Krecke KN, Fulgham JR. Multifocal brain MRI artifacts secondary to embolic metal fragments. Neurology 1997; 49(5):1451–3.
Prenatal Diagnosis 2015, 35, 197–199
6. Mari G, for the Collaborative Group for Doppler Assessment of Blood Velocity in Anemic Fetuses. Noninvasive diagnosis by Doppler ultrasonography of fetal anemia due to maternal red-cell alloimmunization. N Engl J Med 2000;342:9–14. 7. Moise KJ Jr.. Management of rhesus alloimmunization in pregnancy. Obstet Gynecol 2008;112(1):164–76. 8. Papantoniou N, Sifakis S, Antsaklis A. Therapeutic management of fetal anemia: review of standard practice and alternative treatment options. J Perinat Med 2013;41(1):71–82. 9. Ghi T, Brondelli L, Simonazzi G, et al. Sonographic demonstration of brain injury in fetuses with severe red blood cell alloimmunization undergoing intrauterine transfusion. Ultrasound Obstet Gynecol 2004;23:428–31. 10. Hopper T, Vasilic B, Popea J, et al. Experimental and computational analyses of the effects of slice distortion from a metallic sphere in an MRI phantom. Magn Reson Imaging 2006, 24:1077–85.
© 2014 John Wiley & Sons, Ltd.
RESEARCH LETTER
Suspected fetal brain metallic embolic microfragment detected by MR imaging Fabio Triulzi1, Monica Fumagalli2*, Roberto Fogliani3, Claudia Cinnante1, Sabrina Avignone1, Chiara Doneda4, Simona Boito3 and Fabio Mosca2 1
Division of Neuroradiology, Fondazione IRCCS Cà Granda Ospedale Maggiore Policlinico Milano, Milan, Italy NICU, Department of Clinical Sciences and Community Health, Fondazione IRCCS Cà Granda Ospedale Maggiore Policlinico Milano, Università degli Studi di Milano, Milan, Italy 3 Division of Prenatal Diagnosis, Fondazione IRCCS Cà Granda Ospedale Maggiore Policlinico Milano, Milan, Italy 4 Division of Radiology and Neuroradiology, Children’s Hospital “V. Buzzi”, Milan, Italy *Correspondence to: Monica Fumagalli. E-mail: [email protected] 2
Funding sources: None Conflicts of interest: None declared
Brain embolic metallic microfragments are reported as a very rare consequence of mechanical prosthetic heart valve implantation or angiographic procedures using stainless steel guide wires.1–5 Extremely small metallic microemboli, as small as 0.01 mg1, are not visible on computerised tomography (CT) but can be easily detected by magnetic resonance imaging (MRI) because of their strong local field inhomogeneity causing striking ferromagnetic susceptibility artefacts. We report a case of a presumed embolic brain metallic fragment detected in a fetus by fetal MRI and confirmed by postnatal brain MR. A 29-year-old pregnant woman, gravida 3, was referred at 23 weeks’ gestation because of red cell alloimmunization. A detailed ultrasound (US) examination was performed with a multiplanar approach, and no brain abnormalities were observed. US findings were consistent with fetal anaemia: the middle cerebral artery peak systolic velocity was 65 cm/s, corresponding to 2.2 MoM6. After obtaining informed consent, a blood sampling was obtained from the placental cord insertion showing severe fetal anaemia (haemoglobin 3.9 g/dL, haematocrit 11.2%), and a fetal intravascular transfusion was performed. The procedure was carried out under ultrasound guidance (Voluson-E8 Expert ultrasound machine equipped with a 5 MH probe, GE Healthcare Ultrasound, Zipf- Austria). An echotip disposable 20 Gauge spinal needle (Cook Medical) was used to inject 47 mL of O Rhesus negative donor packed red cells (haematocrit 56.5%) into the umbilical vein. No fetal anaesthesia was administered. At the end of the procedure, the fetal haemoglobin level was 18 g/dL, and the middle cerebral artery peak systolic velocity was 34 cm/s. Neither clinical nor ultrasonographic complications were observed immediately after the procedure. After 2 h, the fetal well-being was evaluated Prenatal Diagnosis 2015, 35, 197–199
by US, and the mother was discharged. At 24 weeks’ gestation an ultrasound scan showed an atypical cerebellar shape whereby a cerebellar haemorrhage was suspected. A fetal MRI was performed at 25 weeks showing a small cerebellum with a slight asymmetry between the hemispheres and a T2 hypointensity in the most inferior part, attributable to a focal cerebellar haemorrhage. A small rounded focal cortical hypointensity was observed as well in the right parietal region on single-shot fast spin echo T2 weighted imaging (Figure 1) and on diffusion images. This finding, although in an unusual location (as situated in the most outer part of the cerebral cortex), was considered, as well as the cerebellar hypointensity, compatible with a focal hemosiderin deposit. A second fetal MRI performed at 30 weeks’ gestation confirmed these findings. These results were interpreted as showing a possible haemorrhagic complication of either severe anaemia or intrauterine transfusion, and we counselled the parents on the possible long-term impact of the larger cerebellar haemorrhage. After receiving all of the information, the parents asked to continue fetal therapy with intrauterine transfusion. The fetus received another four transfusions at 25, 28, 31 and 33 weeks’ gestation, respectively, without any complications. The baby was delivered by caesarean section at 34 weeks’ gestation after premature rupture of membranes. A postnatal brain MR scan was carried out at 40 weeks corrected age. A severe cerebellar atrophy secondary to fetal cerebellar haemorrhage was observed. The MR images also confirmed the presence of a rounded focal striking hypointensity located in the right parietal cortex which was clearly visible on fast T2 weighted images (Figure 2) but also on T1 weighted images. The T2 focal hypointensity showed a peculiar strong artefactual signal with a partly hyperintense halo, and the hypointensity was clearly enhanced on both gradient echo and © 2014 John Wiley & Sons, Ltd.
F. Triulzi et al.
198
Figure 1 Fetal MRI at 25 weeks’ gestation. Single-shot fast spin echo T2 weighted sequence showed a focal rounded cortical hypointensity in the parietal region (arrow)
Figure 2 Neonatal MRI at 40 weeks corrected age. Fast spin echo T2 weighted image showed a focal striking hypointensity (arrow) with some peripheral hyperintensity typically observed in the presence of ferromagnetic artefacts
susceptibility weighted images, where some other tiny focal hypointensities became evident in the right peritrigonal white matter and in the right cortical parietal region. In order to better define the origin of this signal inhomogeneity, a CT scan was performed. This study did not reveal any focal density alteration in the right parietal region. Based on these observations, the signal abnormality in the right parietal cortex was no longer interpreted as hemosiderin deposit, yet a brain embolic metallic microfragment was suspected.
Prenatal Diagnosis 2015, 35, 197–199
Intrauterine transfusion in case of severe fetal anaemia due to red cell alloimmunization or other causes is considered a relatively safe procedure7 with a survival fetal rate of about 85% (90% in non-hydropic versus 70% in hydropic fetuses)8. Medium-term and long-term neurological sequelae have been described mainly as a result of severe anaemia rather than as consequences of the procedure itself 9. Iatrogenic brain metallic microemboli are extremely rare, and potential sources of metallic microfragments have been identified in metallic prosthetic heart valves and intravascular stainless steel guide wire applications. The presence of the aforementioned signal abnormalities at the first MRI, performed at 25 weeks’ gestation, suggests a temporal correlation between the in utero intravascular transfusion procedure, performed at 23 weeks’ gestation, and the neuroimaging appearance. We have no other good explanation for the finding. To our knowledge, this is the first case of metallic microembolism which in retrospect was already detected on fetal MR. Several neuroimaging considerations support the hypothesis of a metallic embolus: (1) the signal hypointensity (distortion) increases in those sequences that are more influenced by field inhomogeneity, (2) the artefacts present a typical hyperintense halo on T2 weighted images10 and (3) a negative CT exam excludes other sources of artefactual hypointensity (calcium, bone, air). Although it cannot be proven with absolute certainty, the needle used for intrauterine transfusion would seem to be the most likely source of metallic microembolic fragments. We hypothesise that microscopic metallic deposits may have embolized from the needle introduced into the umbilical vein and may have reached the brain through the patent foramen ovale. A neurodevelopmental follow-up has been planned for this child. However, we are uncertain about the possibility to assess the clinical relevance of the brain metallic microfragment because of the co-existence of cerebellar atrophy, secondary to the intrauterine cerebellar haemorrhage, potentially affecting her long-term neurocognitive development. WHAT’S ALREADY KNOWN ABOUT THIS TOPIC? • Brain embolic metallic microfragments are a rare consequence of mechanical prosthetic heart valves implantation or angiographic procedures performed using stainless steel guide wires.
WHAT DOES THIS STUDY ADD? • In utero intravascular procedures may represent a potential source of brain metallic microembolism for the fetus. • Brain metallic microfragments can be detected by fetal and neonatal magnetic resonance imaging.
© 2014 John Wiley & Sons, Ltd.
Suspected fetal brain metallic embolic microfragment
199
REFERENCES 1. Jassal DS, Fast MD, McGinn G. Multifocal brain MRI hypointensities secondary to cardiac catheterization. Neurology 2000;54(10):2023–4. 2. Gorriño O, Oleaga L, de la Fuente R, et al. Intracranial artifact on magnetic resonance caused by embolization of microscopic metallic fragment. Neurologia 2004;19(10):766–8. 3. Naumann M, Hofmann E, Toyka KV. Multifocal brain MRI hypointensities secondary to embolic metal fragments from a mechanical heart valve prosthesis: a possible source of epileptic seizures. Neurology 1998;51(6):1766–7. 4. Roshal D, Snapp M, Friedman DP, Zangaladze A. Iatrogenic brain and cervical cord magnetic resonance imaging susceptibility artifacts from metallic microemboli. Arch Neurol 2011;68(1):132–3. 5. Wingerchuk DM, Krecke KN, Fulgham JR. Multifocal brain MRI artifacts secondary to embolic metal fragments. Neurology 1997; 49(5):1451–3.
Prenatal Diagnosis 2015, 35, 197–199
6. Mari G, for the Collaborative Group for Doppler Assessment of Blood Velocity in Anemic Fetuses. Noninvasive diagnosis by Doppler ultrasonography of fetal anemia due to maternal red-cell alloimmunization. N Engl J Med 2000;342:9–14. 7. Moise KJ Jr.. Management of rhesus alloimmunization in pregnancy. Obstet Gynecol 2008;112(1):164–76. 8. Papantoniou N, Sifakis S, Antsaklis A. Therapeutic management of fetal anemia: review of standard practice and alternative treatment options. J Perinat Med 2013;41(1):71–82. 9. Ghi T, Brondelli L, Simonazzi G, et al. Sonographic demonstration of brain injury in fetuses with severe red blood cell alloimmunization undergoing intrauterine transfusion. Ultrasound Obstet Gynecol 2004;23:428–31. 10. Hopper T, Vasilic B, Popea J, et al. Experimental and computational analyses of the effects of slice distortion from a metallic sphere in an MRI phantom. Magn Reson Imaging 2006, 24:1077–85.
© 2014 John Wiley & Sons, Ltd.
