Brain (1995), 118, 119-129
Neurofibrillary tangles in Niemann-Pick disease
type C
Seth Love,
1
Leslie R. Bridges
3
and C. Patrick Case
2
* Department of Neuropathology, Frenchay Hospital, the
2
Departinent of Pathology, Southmead Hospital, Bristol
and the ^Department of Neuropathology, University of
Leeds, Leeds, UK
Correspondence to: Dr S. Love, Department of
Neuropathology, Frenchay Hospital, Bristol BS16 1LE, UK
Summary
Post-mortem neuropathological examination of five cases of
Niemann-Pick disease type C revealed neurofibrillary tangles
in many parts of the brain. Tangles were a consistent finding
in the hippocampus, hypothalamus, substantia innominata,
midbrain pons and medulla. Other regions of the brain in
which tangles were present included neocortex, basal ganglia,
thalamus, cerebellar cortex in one case, and dentate nucleus
in another. The tangles were argyrophilic, fluoresced under
ultraviolet light when stained with thioflavin S, and reacted
strongly with antibody to tau protein. Some of the tangles
could be immunostained for ubiquitin. Electron microscopy,
performed in one of the cases, showed the tangles to consist
of paired helical filaments ultrastructurally identical to those
of Alzheimer's disease. The distribution of the tangles in the
central nervous system as a whole and also within many
individual neurons corresponded fairly closely with that of
the abnormal storage material. Both the tangles and the
storage material extended into, and distended, the proximal
parts of many dendrites and axons. No A4/§ protein, either
in the form of plaques or in the walls of blood vessels, was
detected in any of the cases. Our findings suggest that
neurofibrillary tangles are a common feature of Niemann-
Pick disease type C and that their formation may be a
reaction to the abnormal storage material.
Keywords: Niemann-Pick disease type C; neurofibrillary tangles; paired helical filaments; tau protein
Introduction
The term Niemann-Pick disease includes several clinically
and biochemically distinct disorders. These were subdivided
by Crocker (1961) into types A, B, C and D on the basis of
the tempo of the disease and the pattern of organ involvement.
These different types of Niemann-Pick disease have been
further subclassified into group I, in which there is
sphingomyelinase deficiency, and group II, in which total
sphingomyelinase activity is normal. Group I includes types
A and B, and group II types C and D. Synonyms for Type
C Niemann-Pick disease include juvenile dystonic lipidosis,
ophthalmoplegic lipidosis, neurovisceral storage disease with
vertical supranuclear ophthalmoplegia and juvenile Niemann-
Pick disease with sea-blue histiocytes. This disorder
corresponds to Niemann-Pick disease type IIS in the scheme
of Spence and Callahan (1989). The onset of Niemann-
Pick disease type C may be in infancy, early childhood,
adolescence or, occasionally, in adulthood (Fink et ai, 1989;
Turpin et al., 1991). Clumsiness, ataxia, supranuclear gaze
paresis, seizures and psychomotor retardation are the
commonest neurological manifestations (Fink et at., 1989;
© Oxford University Press 1995
Spence and Callahan, 1989; Turpin et al., 1991). Other
features include myoclonus, narcolepsy and cataplexy. Turpin
et al. (1991) noted that a psychosis may be the only
manifestation of Niemann-Pick disease type C for several
years. Hepatosplenomegaly is usually present and may be
marked or, particularly in older-onset cases, mild or even
absent (Turpin et al., 1991; Hulette et al., 1992).
Neuropathological examination in cases of Niemann-Pick
disease type C reveals marked neuronal distension by weakly
or non-sudanophilic material that stains moderately well with
periodic acid-Schiff reagent (Lake, 1992). Other histological
features include the presence of swollen axons, particularly
in the brainstem and spinal cord, and foam cells in the bone
marrow, spleen and hepatic sinusoids.
Horoupian and Yang (1978), described a patient with type
C Niemann-Pick disease in whom Alzheimer-like neuro-
fibrillary tangles were found at autopsy. The tangles were
most numerous in the frontal and temporal lobes, insula and
basal ganglia, and were shown by electron microscopy to
consist of paired helical filaments.