A Critical Update of the Classification of Chiari and Chiari-like Malformations

Abstract

Chiari malformations are a group of craniovertebral junction anomalies characterized by the herniation of cerebellar tonsils below the foramen magnum, often accompanied by brainstem descent. The existing classification systems for Chiari malformations have expanded from the original four categories to nine, leading to debates about the need for a more descriptive and etiopathogenic terminology. This review aims to examine the various classification approaches employed and proposes a simplified scheme to differentiate between different types of tonsillar herniations. Furthermore, it explores the most appropriate terminology for acquired herniation of cerebellar tonsils and other secondary Chiari-like malformations. Recent advances in magnetic resonance imaging (MRI) have revealed a higher prevalence and incidence of Chiari malformation Type 1 (CM1) and identified similar cerebellar herniations in individuals unrelated to the classic phenotypes described by Chiari. As we reassess the existing classifications, it becomes crucial to establish a terminology that accurately reflects the diverse presentations and underlying causes of these conditions. This paper contributes to the ongoing discussion by offering insights into the evolving understanding of Chiari malformations and proposing a simplified classification and terminology system to enhance diagnosis and management.

Keywords: Arnold-Chiari Malformation; Chiari malformation; Classification; Rare diseases; Syringomyelia.

Figure 1

Posterior view (Left) and inferior view (Right) of the cerebellum and brainstem. BLm: Bivental lobe, medial part; CeT: Cerebellar tonsils; Fl: Flocculus; PV: Pyramid of vermis; TV: Tuber of vermis. From: Véronique Schotte, https://sites.uclouvain.be/braininteratlas/en/chapter/cerebellum. Images licensed under Creative Commons License 4.0 (https://creativecommons.org/licenses/by-nc/4.0/ (accessed on 7 June 2023) ).

Figure 2

Chiari type 1 malformation. Sagittal T1-weighted MRI (left) and T2-weighted coronal (right) of a 13-year-old girl referred to neurosurgery with clinical symptoms of dizziness and unstable gait for the last 18 months. Her symptoms progressed in the last three months when she started to report paresthesia in the lower right foot. She did not report headaches. Neurological examination was normal. MRI disclosed a widened foramen magnum, a short subocciput, and asymmetrical herniation of the cerebellar tonsils 19 mm below McRae’s line. The (right) tonsil (RT) was slightly more herniated than the (left). A small syrinx is observed in the midsagittal T1-weighted slice, just below the lowest tip of the tonsils (red arrow).

Figure 3

PubMed search conducted using the Medical Subject Headings term ‘Arnold-Chiari Malformation’ on 23 February 2023. MeSH terms are assigned manually by indexers of the National Library of Medicine. The search yielded 3925 records and showed an exponential growth in the number of papers indexed since the late 1960s. In the period 2010–2023, there was a plateau in the number of indexed studies. Since 2010, the average number of papers per year is above 130 (dashed dark-red line). The MeSH term was introduced in PubMed in 1966, when only 17 papers were indexed. Most papers indexed in PubMed are related to CM1. There is general agreement that CM3 and CM4 are rare, severe, embryological disorders that should be included under the Chiari eponym only for historical reasons.

Figure 4

(Left): Hans Chiari (1851–1916), an Austrian pathologist who, while working at the University of Prague, described the malformations now known as Chiari malformations. (Right): Figure 1 of Chiari’s paper published in 1895 [3] corresponding to the cerebellum of a six-year-old boy with a prior diagnosis of “Hemiplegia spastica”, who died of diphtheria and pneumonia. In his detailed report, Chiari described that the lateral and III ventricles were dilated but the IV ventricle was of normal size. The cerebellum, normally configured, presented a bilateral asymmetrical herniation of the cerebellar tonsils surrounding the medulla oblongata laterally and especially dorsally. The left tonsil ended at the level of the lower edge of the atlas and the right one above the upper edge of the atlas.

Figure 5

Spontaneous intracranial hypotension and reversible tonsillar herniation after successful epidural blood patches. A 25-year-old female presented with a history of severe orthostatic headaches in the last two years. (Upper row): Sagittal gadolinium-enhanced T1-weighted MRI showed intense diffuse contrast enhancement of the pachymeninges, tentorium, and superior sagittal and sigmoid sinus engorgement. The morphology of the PF was normal, and the vetricular size was slightly reduced for the patient’s age. A tonsillar herniation of 14 mm below the McRL is observed. Spinal MRI (not shown) disclosed a CSF leak at the left C7-Th1 level that was managed with three epidural blood patches. (Lower row): Complete resolution of the meningeal enhancement, repositioning of the cerebellar tonsils and reversal of the TH eight months after successful epidural blood patches with complete symptomatic relief.

Figure 6

Image of Prof. Miguel Marín-Padilla (1930–2023) in Jumilla, Spain in July 2020 (reproduced with permission of Siete Dias Jumilla). After graduating from the Granada University School of Medicine, Spain, Marín-Padilla emigrated to the U.S. He started his pathology residency at the Mallory Institute of Pathology in Boston, Massachusetts. Marín-Padilla specialized in infants and children and taught general pathology at the Dartmouth Hitchcock Medical Center, Hanover, NH, U.S. In 1981, Marín-Padilla and Marín-Padilla hypothesized paraxial mesodermal insufficiency as the main etiopathogenic factor in CM1 and CM2 and reproduced the axial skeletal abnormalities in hamsters using a single dose of vitamin A as a teratogen [77].

Figure 7

(Left): Image of a female Cavalier King Charles Spaniel. T. Voekle. The Cavalier King Charles Spaniel was recognized as a separate breed in 1945: https://rebrand.ly/cavalierdog (accessed on 7 June 2023). Cavaliers descend from the toy spaniels depicted in many 16–18th century paintings by famous artists such as Van Dyck (1599–1561) in The Three Eldest Children of Charles I. The Spaniels have flat heads and high-set ears and are a breed in which Chiari-like malformations and syringomyelia are highly prevalent. (Right): Reproduced with Permission of Elsevier Ltd., from [89]. In this figure, three sagittal T2-weighted MRI scans of the brain and cervical spine in a flexed position are shown. Top: a brachycephalic dog with a normal cervicomedullary junction; Middle: a Cavalier King Charles Spaniel with Chiari-like malformation; Bottom: a dog of the same breed showing syringomyelia in the cervical spinal cord.

Figure 8

Two adult patients with CM1 (left) and CM1.5 (right) in whom posterior fossa boundaries have been drawn by using the five-sided polygon and the additional Chamberlain’s line suggested by Raybaud and Jallo [1,6]. These five lines are easily drawn and visually analyzed, and their area has been shown to be a good surrogate for total PF volume and a useful predictor in distinguishing CM1 patients and controls [99]. For a detailed explanation see text. The six lines suggested by Raybaud and Jallo are: 1. Chamberlain’s line; 2. McRae’s line; 3. Clival and 4. Wackenheim line; 5. Incisural line; 6. Tentorial line; and 7 Supraoccipital line. In normal individuals, both the McRae and Chamberlain lines are superimposed (right) but diverge when the clivus is hypoplastic (left) and it indicates a short basiocciput and possible basilar impression. In most studies and clinical practice, tonsillar herniation is evaluated by measuring the distance from the most caudal aspect of the tonsils to a line running perpendicular to the McRL (dashed line).

Figure 9

Left: Human anatomical specimen with a midsagittal slice like the midsagittal T1-weighted gadolinium-enhanced MRI shown on the right, corresponding to a 35-year-old female scanned because of headaches. Aa-C1: anterior arch of C1; O: odontoid; CeT: cerebellar tonsil; (**) Cisterna magna. A common problem in assessing the tonsillar herniation (TH) in reference to the McRae line (McRL) is that midsaggital MRI sections when the slice thickness is >2 mm are prone to error because the medial part of the biventral lobe is difficult to differentiate from the CeT. In doubtful cases, Savy et al. recommend performing coronal MRI, preferably with thin sections, to establish whether any TH is present [107].

Figure 10

Two patients with CM 1.5. A 27-year-old female (a,b). with a clinical history of cough-headaches and and acute severe right cervicobrachial pain associated to patesthesiae of the right hand without motor weakness (a). T1W midsaggital MRI showing a 7 mm TH below the McRL (b). The obex-gracillis complex is 3 mm below the McRL (red arrow). (*) A large cervico-thoracic syryngomyelia extending from C2 to the conus medullaris (c,d). A 57-year-old female with a clinical history of cough-induced headaches, dizzines and patesthesiae in both hands (c). T1W midsagittal MRI showing a TH 4 mm below the McRL. The obex/nucleus gracillis position (red arrows) is 4 mm below the McRL and is better shown in the T2W MRI (d).