Case Report Radiographic, Ultrasonographic and Postmortem Magnetic Resonance Imaging Features of Meningoencephalocele in a Calf with Tibial Hemimelia Syndrome

in with Abstract A 1-day-old, calf was presented for inability to stand and for evaluation of congenital anatomical and postural abnormalities. Physical examination revealed hypertrichosis, bilateral corneal edema, shortened hind limbs, an abdominal hernia and a fluctuant soft tissue swelling on the caudodorsal aspect of the head. Radiographs revealed a lucent line in the skull underlying an extracra-nial soft tissue swelling. Focal ultrasound (US) revealed an anechoic cystic structure contiguous with an intracranial fluid-filled cavity. Immediate postmortem magnetic resonance imaging (MRI) showed cranioschisis with two herniated meningeal sacs and focal parieto-occipital porencephaly. At necropsy, multiple intracranial, skeletal and abdominal defects were noted consistent with tibial hemimelia syndrome. Histopathology confirmed a meningoencephalocele that couldn’t be differentiated from a meningocele with US nor MRI.


Introduction
The tibial hemimelia syndrome is an unusual and lethal congenital disease consisting of brain, skeletal and reproductive system defects. Calves affected by this syndrome are stillborn or die shortly after birth. This syndrome has been mainly described in Galloway calves, but can affect other breeds [10,16]. Defects included in this syndrome are: non-fusion of the Müllerian ducts in female calves, cryptorchidism in male calves, and in both sexes hypertrichosis, cranioschisis, meningocele (MC) or meningoencephalocele (MEC), internal hydrocephalus, bilateral malformation, hypoplasia or agenesis of the tibia, femur and patella, open pelvis symphysis, and abdominal hernia [10,19].
Cranioschisis is a malformation of the skull resulting in an incomplete closure of the calvarium that can lead to an open-ing through which the intracranial tissue can protrude. A MC is a herniation of the meninges through a cranial defect containing cerebrospinal fluid (CSF). This need to be differentiated from a MEC, in which there is also herniation of brain tissue [3]. In human medicine their differentiation is important in terms of surgical planning prognosis and surgery outcome. These defects can be congenital, as illustrated here, but can also arise after trauma [17]. Congenital MCs and MECs have been reported in calves, lambs, foals, pigs, dogs, cats and humans [2,[4][5][6][7][8]14,15,21]. Case series in human medicine have shown that the size and content of the protruding meningeal sac has an impact on prognosis [18]. In human medicine, surgical intervention is the treatment of choice, based on the potential for recurrent meningitis, brain damage from herniation, and refractory seizures [20]. Surgical correction of MC has been previously described in calves [1,9].
A 26 kg, 1-day-old, Maine Anjou heifer calf was presented for evaluation of congenital anatomic and postural abnormalities. The calf had been unable to stand since birth. The dam had not had any calves born with congenital malformations in the past. This calf was born a twin and the other calf was reportedly normal at birth.
At presentation, the calf was relatively bright, alert, and responsive and had a weak suckle reflex. Physical examination revealed hypertrichosis, bilateral corneal edema, shortened hind limbs, enlarged stifles with minimal range of motion, a 20 cm diameter caudal abdominal hernia and a 1.5 cm fluctuant soft tissue swelling on the caudodorsal aspect of the head that was sensitive to palpation. The rest of the physical examination was unremarkable.
Given the above clinical findings a congenital anomaly such as tibial hemimelia syndrome or bovine arthrogryposis with other congenital defects were suspected.
Orthogonal radiographs of the head and right stifle ( Figure  1) were taken (Canon CXDI-80C Wireless Digital Radiography System, Melville, NY) using the settings of 1.2 mAs and 68 kVp.
A 2 x 1.5 cm focal well-defined oval-shaped increase in soft tissue opacity was present at the caudodorsal aspect of the skull. A dorsoventrally oriented S-shape lucent line was present rostroventrally to the soft tissue swelling. Radiographic diagnoses included a congenital anomaly such as cranioschisis with a MC or a MEC, a skull fracture with a hematoma or swelling, and an open fontanelle with a seroma or cyst. . An Sshaped lucent line (black arrowheads) was present at the level of the confluence between the parietal and occipital bones. A focal well-defined soft tissue swelling (white wide arrow) was present caudodorsally to the lucent line. Mediolateral and caudocranial (CdCr) radiographs of the right stifle (B, C) showing hypoplastic distal femur and proximal tibia and patella. The patella was luxated caudomedially (white arrow). On the edge of the CdCr radiograph part of an abdominal wall hernia with intestinal passage was seen (white arrowheads).
Radiographs of the right stifle showed a malformed distal femur, proximal tibia and patella. The distal femoral epiphysis was ovoid with rounded margins and without clear definition of the condyles and intercondylar fossa. The patella and the apophysis of the tibial tuberosity were small with rounded edges and displaced caudomedially. The findings were compatible with hypoplasia of the distal femur, proximal tibia and patella with concomitant medial patellar luxation and malformation of the tibial tuberosity apophysis. Additionally, there was an abdominal mass caudally to the pelvis and medially to the right stifle, containing gas-filled bowel loops and consistent with an abdominal wall hernia. Focal ultrasound (US) of the fluctuant swelling at the caudodorsal aspect of the head was performed (Technos MPX, Esaote, Indianapolis, IN) with an 8-14 MHz linear probe ( Figure 2). A 0.6 cm defect was detected at the caudodorsal aspect of the skull, traversing caudoventrally towards the junction between the left parietal and occipital bones. Through this defect, a well-defined, thin-walled (0.05 cm), oval-shaped anechoic cyst-like structure of 1.5 x 0.6 x 1.7 cm was present in the subcutaneous tissues communicating intracranially with an anechoic fluid-filled cavity. This intracranial cavity appeared contiguous with a moderately dilated left lateral ventricle. The right lateral ventricle was mildly dilated. The ultrasonographic diagnosis was cranioschisis and a MC communicating with a distended and misshapen left lateral ventricle.
Poor prognosis was given for return to ambulation for this calf and hence humane euthanasia of the calf was elected by the owner. An immediate postmortem magnetic resonance imaging (MRI) of the head was performed (1.5 T General Electric Signa, Milwaukee, WI) (Figure 3) to further characterize the lesions. The calf was positioned in sternal recumbency. Sequences included transverse and sagittal T1-weighted (T1W) and T2-weighted (T2W) and transverse fluid attenuated inversion recovery (FLAIR) images. Repetition time and echo time were 550.0-566.6 and 10.3-16.3 ms (T1W), 3000-4050 and 100.8-106.9 ms (T2W), and 8002.0 and 128.9 ms (FLAIR). Inversion time was 2000 ms on FLAIR images. Slice thickness was 1.5-3 mm, with a 0.5-1 mm interslice gap. Field of view was 22 x 22 cm with the matrix size of 288 × 224. Two asymmetric (left: 1.5 x 1.6 x 1.5 cm and right: 0.5 cm), fluid-filled structures were noted communicating the subarachnoid space with the subcutaneous tissues through two calvarial bone defects on each side of the midline of caudodorsal skull. The cystic structures were isointense to the CSF and surrounded by a thin, well-defined T1W hyperintense, T2W hypointense and FLAIR hyperintense wall. No brain tissue was seen protruding into these cystic structures. The left parieto-occipital cerebral cortex was severely atrophied focally, leading to a large intraaxial CSF-filled cavity that communicated with the largest cystic structure. A thin rim of residual neural parenchyma was still present at that level. The rest of the cortical mantle appeared thin with widened sulci. No communication between the cystic structures and the lateral ventricles was noted. Both lateral ventricles were asymmetrically enlarged (left > right) and the rest of the ventricular system was mildly generally dilated. No evidence CSF flow obstruction was noted in the ventricular system. Magnetic resonance imaging findings included cranioschisis, two MCs, focal left parieto-occipital porencephaly, presumed mild generalized cortical brain atrophy and compensatory hydrocephalus ex vacuo.
At necropsy (Figure 4), two fluid-filled pouches lined by a thin membrane and covered by alopecic skin protruded through two 0.6 cm defects in the parietal bones. No macroscopic evidence of herniated brain tissue within the meningeal sacs was noted. Histologically, the larger pouch included a meningeal layer, a portion of the left lateral ventricle and the compressed overlying cerebral parenchyma (MEC). The parietal bone sutures were incompletely fused and connected by a 4 mm band of connective tissue. The medial and lateral femoral and tibial condyles were bilaterally enlarged and rounded. Both patellae were displaced medially and fused with the medial femoral condyles. The medial meniscus was bilaterally missing. Histologically, the femoral growth plates had marked expansion of the resting layer of chondrocytes occupying more than half of the growth plate thickness. The number of osteoclasts was decreased in the primary spongiosa, with retained cartilage cores in the secondary spongiosa and diaphyseal trabecular bone. Trabeculae were bordered by a reduced number of mostly flattened osteoblasts. The marrow had few hematopoietic cells. A large abdominal hernia was present containing segments of the small intestine, spiral colon, and omasum. The ovaries and uterus were absent and the vaginal vault ended blindly 4 cm cranial to the vulva. Histologically, the abdominal wall at this level consisted of and external lining of skin followed by connective tissue without a layer of skeletal muscle.
This calf was diagnosed with tibial hemimelia syndrome due to the presence of multiple congenital defects including cranioschisis, MEC, hydrocephalus, uterine and ovarian agenesis, bilateral dysplastic tibiae, femora, and patellae, and ventral abdominal hernia.
Radiography [1,7], US [1,15], computed tomography [12,15] and MRI [21] have been previously used for the diagnosis of MEC in calves but to the authors' knowledge this is the first detailed imaging description of MEC in a calf using radiography, US and high field MRI. The previous MRI description was performed with a low field magnet and the MEC was fronto-ethmoidal protruding into the nasal cavity. Many other cranial and vertebral malformations were diagnosed in association with the MEC in that case.
In the present patient, MRI allowed the detection of an additional subcutaneous meningeal sac that was unnoticed during the clinical, radiographic and ultrasonographic examinations.
Interestingly, histopathology of the larger subcutaneous meningeal sac contained compressed cerebral parenchyma, confirming therefore a diagnosis of MEC and not MC as believed in the US and MRI examinations. No histopathology of the other smaller meningeal sac could be performed, not allowing a histological differentiation between a MC and a MEC.
On MRI, MEC can be differentiated from MC due to the presence of hyperintense T2W and FLAIR protruded parenchyma within the meningeal sac. These intensity changes can be due to gliosis of cerebral tissue, tissue inflammation, or edema [11]. Other concurrent intracranial malformations, including porencephaly and hydrocephalus ex vacuo, were noted in this case as previously described in dogs [11]. Porencephaly has been previously described in calves but not associated with MEC [13].
MRI is a non-invasive technique that can be used in neonatal bovines for assessing congenital anomalies of the brain that could be potentially treated surgically and detection of additional abnormalities that may influence the prognosis. Although the utility of MRI in the diagnosis of MC/MEC in calves may be limited because of the cost and availability of MRI systems.