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March 10, 2020; 94 (10) Article

Speech production differences in English and Italian speakers with nonfluent variant PPA

Elisa Canu, Federica Agosta, Giovanni Battistella, Edoardo G. Spinelli, Jessica DeLeon, Ariane E. Welch, Maria Luisa Mandelli, H. Isabel Hubbard, Andrea Moro, Giuseppe Magnani, Stefano F. Cappa, Bruce L. Miller, Massimo Filippi, Maria Luisa Gorno-Tempini
First published January 10, 2020, DOI: https://doi.org/10.1212/WNL.0000000000008879
Elisa Canu
From the Neuroimaging Research Unit (E.C., F.A., E.G.S., M.F.), Institute of Experimental Neurology, Division of Neuroscience, Neurology Unit (G.M., M.F.), and Neurophysiology Unit (M.F.), IRCCS San Raffaele Scientific Institute; Vita-Salute San Raffaele University (F.A., E.G.S., M.F.), Milan, Italy; Memory and Aging Center (G.B., J.D., A.E.W., M.L.M., H.I.H., B.L.M., M.L.G.-T.), UCSF, San Francisco, CA; University School for Advanced Studies IUSS Pavia (A.M., S.F.C.); and IRCCS S. Giovanni di Dio Fatebenefratelli (S.F.C.), Brescia, Italy.
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Federica Agosta
From the Neuroimaging Research Unit (E.C., F.A., E.G.S., M.F.), Institute of Experimental Neurology, Division of Neuroscience, Neurology Unit (G.M., M.F.), and Neurophysiology Unit (M.F.), IRCCS San Raffaele Scientific Institute; Vita-Salute San Raffaele University (F.A., E.G.S., M.F.), Milan, Italy; Memory and Aging Center (G.B., J.D., A.E.W., M.L.M., H.I.H., B.L.M., M.L.G.-T.), UCSF, San Francisco, CA; University School for Advanced Studies IUSS Pavia (A.M., S.F.C.); and IRCCS S. Giovanni di Dio Fatebenefratelli (S.F.C.), Brescia, Italy.
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Giovanni Battistella
From the Neuroimaging Research Unit (E.C., F.A., E.G.S., M.F.), Institute of Experimental Neurology, Division of Neuroscience, Neurology Unit (G.M., M.F.), and Neurophysiology Unit (M.F.), IRCCS San Raffaele Scientific Institute; Vita-Salute San Raffaele University (F.A., E.G.S., M.F.), Milan, Italy; Memory and Aging Center (G.B., J.D., A.E.W., M.L.M., H.I.H., B.L.M., M.L.G.-T.), UCSF, San Francisco, CA; University School for Advanced Studies IUSS Pavia (A.M., S.F.C.); and IRCCS S. Giovanni di Dio Fatebenefratelli (S.F.C.), Brescia, Italy.
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Edoardo G. Spinelli
From the Neuroimaging Research Unit (E.C., F.A., E.G.S., M.F.), Institute of Experimental Neurology, Division of Neuroscience, Neurology Unit (G.M., M.F.), and Neurophysiology Unit (M.F.), IRCCS San Raffaele Scientific Institute; Vita-Salute San Raffaele University (F.A., E.G.S., M.F.), Milan, Italy; Memory and Aging Center (G.B., J.D., A.E.W., M.L.M., H.I.H., B.L.M., M.L.G.-T.), UCSF, San Francisco, CA; University School for Advanced Studies IUSS Pavia (A.M., S.F.C.); and IRCCS S. Giovanni di Dio Fatebenefratelli (S.F.C.), Brescia, Italy.
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Jessica DeLeon
From the Neuroimaging Research Unit (E.C., F.A., E.G.S., M.F.), Institute of Experimental Neurology, Division of Neuroscience, Neurology Unit (G.M., M.F.), and Neurophysiology Unit (M.F.), IRCCS San Raffaele Scientific Institute; Vita-Salute San Raffaele University (F.A., E.G.S., M.F.), Milan, Italy; Memory and Aging Center (G.B., J.D., A.E.W., M.L.M., H.I.H., B.L.M., M.L.G.-T.), UCSF, San Francisco, CA; University School for Advanced Studies IUSS Pavia (A.M., S.F.C.); and IRCCS S. Giovanni di Dio Fatebenefratelli (S.F.C.), Brescia, Italy.
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Ariane E. Welch
From the Neuroimaging Research Unit (E.C., F.A., E.G.S., M.F.), Institute of Experimental Neurology, Division of Neuroscience, Neurology Unit (G.M., M.F.), and Neurophysiology Unit (M.F.), IRCCS San Raffaele Scientific Institute; Vita-Salute San Raffaele University (F.A., E.G.S., M.F.), Milan, Italy; Memory and Aging Center (G.B., J.D., A.E.W., M.L.M., H.I.H., B.L.M., M.L.G.-T.), UCSF, San Francisco, CA; University School for Advanced Studies IUSS Pavia (A.M., S.F.C.); and IRCCS S. Giovanni di Dio Fatebenefratelli (S.F.C.), Brescia, Italy.
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Maria Luisa Mandelli
From the Neuroimaging Research Unit (E.C., F.A., E.G.S., M.F.), Institute of Experimental Neurology, Division of Neuroscience, Neurology Unit (G.M., M.F.), and Neurophysiology Unit (M.F.), IRCCS San Raffaele Scientific Institute; Vita-Salute San Raffaele University (F.A., E.G.S., M.F.), Milan, Italy; Memory and Aging Center (G.B., J.D., A.E.W., M.L.M., H.I.H., B.L.M., M.L.G.-T.), UCSF, San Francisco, CA; University School for Advanced Studies IUSS Pavia (A.M., S.F.C.); and IRCCS S. Giovanni di Dio Fatebenefratelli (S.F.C.), Brescia, Italy.
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H. Isabel Hubbard
From the Neuroimaging Research Unit (E.C., F.A., E.G.S., M.F.), Institute of Experimental Neurology, Division of Neuroscience, Neurology Unit (G.M., M.F.), and Neurophysiology Unit (M.F.), IRCCS San Raffaele Scientific Institute; Vita-Salute San Raffaele University (F.A., E.G.S., M.F.), Milan, Italy; Memory and Aging Center (G.B., J.D., A.E.W., M.L.M., H.I.H., B.L.M., M.L.G.-T.), UCSF, San Francisco, CA; University School for Advanced Studies IUSS Pavia (A.M., S.F.C.); and IRCCS S. Giovanni di Dio Fatebenefratelli (S.F.C.), Brescia, Italy.
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Andrea Moro
From the Neuroimaging Research Unit (E.C., F.A., E.G.S., M.F.), Institute of Experimental Neurology, Division of Neuroscience, Neurology Unit (G.M., M.F.), and Neurophysiology Unit (M.F.), IRCCS San Raffaele Scientific Institute; Vita-Salute San Raffaele University (F.A., E.G.S., M.F.), Milan, Italy; Memory and Aging Center (G.B., J.D., A.E.W., M.L.M., H.I.H., B.L.M., M.L.G.-T.), UCSF, San Francisco, CA; University School for Advanced Studies IUSS Pavia (A.M., S.F.C.); and IRCCS S. Giovanni di Dio Fatebenefratelli (S.F.C.), Brescia, Italy.
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Giuseppe Magnani
From the Neuroimaging Research Unit (E.C., F.A., E.G.S., M.F.), Institute of Experimental Neurology, Division of Neuroscience, Neurology Unit (G.M., M.F.), and Neurophysiology Unit (M.F.), IRCCS San Raffaele Scientific Institute; Vita-Salute San Raffaele University (F.A., E.G.S., M.F.), Milan, Italy; Memory and Aging Center (G.B., J.D., A.E.W., M.L.M., H.I.H., B.L.M., M.L.G.-T.), UCSF, San Francisco, CA; University School for Advanced Studies IUSS Pavia (A.M., S.F.C.); and IRCCS S. Giovanni di Dio Fatebenefratelli (S.F.C.), Brescia, Italy.
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Stefano F. Cappa
From the Neuroimaging Research Unit (E.C., F.A., E.G.S., M.F.), Institute of Experimental Neurology, Division of Neuroscience, Neurology Unit (G.M., M.F.), and Neurophysiology Unit (M.F.), IRCCS San Raffaele Scientific Institute; Vita-Salute San Raffaele University (F.A., E.G.S., M.F.), Milan, Italy; Memory and Aging Center (G.B., J.D., A.E.W., M.L.M., H.I.H., B.L.M., M.L.G.-T.), UCSF, San Francisco, CA; University School for Advanced Studies IUSS Pavia (A.M., S.F.C.); and IRCCS S. Giovanni di Dio Fatebenefratelli (S.F.C.), Brescia, Italy.
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Bruce L. Miller
From the Neuroimaging Research Unit (E.C., F.A., E.G.S., M.F.), Institute of Experimental Neurology, Division of Neuroscience, Neurology Unit (G.M., M.F.), and Neurophysiology Unit (M.F.), IRCCS San Raffaele Scientific Institute; Vita-Salute San Raffaele University (F.A., E.G.S., M.F.), Milan, Italy; Memory and Aging Center (G.B., J.D., A.E.W., M.L.M., H.I.H., B.L.M., M.L.G.-T.), UCSF, San Francisco, CA; University School for Advanced Studies IUSS Pavia (A.M., S.F.C.); and IRCCS S. Giovanni di Dio Fatebenefratelli (S.F.C.), Brescia, Italy.
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Massimo Filippi
From the Neuroimaging Research Unit (E.C., F.A., E.G.S., M.F.), Institute of Experimental Neurology, Division of Neuroscience, Neurology Unit (G.M., M.F.), and Neurophysiology Unit (M.F.), IRCCS San Raffaele Scientific Institute; Vita-Salute San Raffaele University (F.A., E.G.S., M.F.), Milan, Italy; Memory and Aging Center (G.B., J.D., A.E.W., M.L.M., H.I.H., B.L.M., M.L.G.-T.), UCSF, San Francisco, CA; University School for Advanced Studies IUSS Pavia (A.M., S.F.C.); and IRCCS S. Giovanni di Dio Fatebenefratelli (S.F.C.), Brescia, Italy.
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Maria Luisa Gorno-Tempini
From the Neuroimaging Research Unit (E.C., F.A., E.G.S., M.F.), Institute of Experimental Neurology, Division of Neuroscience, Neurology Unit (G.M., M.F.), and Neurophysiology Unit (M.F.), IRCCS San Raffaele Scientific Institute; Vita-Salute San Raffaele University (F.A., E.G.S., M.F.), Milan, Italy; Memory and Aging Center (G.B., J.D., A.E.W., M.L.M., H.I.H., B.L.M., M.L.G.-T.), UCSF, San Francisco, CA; University School for Advanced Studies IUSS Pavia (A.M., S.F.C.); and IRCCS S. Giovanni di Dio Fatebenefratelli (S.F.C.), Brescia, Italy.
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Speech production differences in English and Italian speakers with nonfluent variant PPA
Elisa Canu, Federica Agosta, Giovanni Battistella, Edoardo G. Spinelli, Jessica DeLeon, Ariane E. Welch, Maria Luisa Mandelli, H. Isabel Hubbard, Andrea Moro, Giuseppe Magnani, Stefano F. Cappa, Bruce L. Miller, Massimo Filippi, Maria Luisa Gorno-Tempini
Neurology Mar 2020, 94 (10) e1062-e1072; DOI: 10.1212/WNL.0000000000008879

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Abstract

Objective To understand whether the clinical phenotype of nonfluent/agrammatic primary progressive aphasia (nfvPPA) could present differences depending on the patient’s native language.

Methods In this cross-sectional study, we analyzed connected speech samples in monolingual English (nfvPPA-E) and Italian speakers (nfvPPA-I) who were diagnosed with nfvPPA and matched for age, sex, and Mini-Mental State Examination scores. Patients also received a comprehensive neuropsychological battery. All patients and 2 groups of age-matched healthy controls underwent an MRI scan with 3D T1-weighted sequences. Connected speech measures and the other cognitive features were compared between patient groups. MRI variables, in terms of gray matter volume, were compared between each patient group and the corresponding controls.

Results Compared to nfvPPA-E, nfvPPA-I had fewer years of education and shorter reported disease duration. The 2 groups showed similar regional atrophy compatible with clinical diagnosis. Patients did not differ in nonlanguage domains, comprising executive scores. Connected speech sample analysis showed that nfvPPA-E had significantly more distortions than nfvPPA-I, while nfvPPA-I showed reduced scores in some measures of syntactic complexity. On language measures, Italian speakers performed more poorly on syntactic comprehension.

Conclusions nfvPPA-E showed greater motor speech impairment than nfvPPA-I despite higher level of education and comparable disease severity and atrophy changes. The data also suggest greater grammatical impairment in nfvPPA-I. This study illustrates the need to take into account the possible effect of the individual's spoken language on the phenotype and clinical presentation of primary progressive aphasia variants.

Glossary

AMAP=
adaptive maximum a posteriori;
ANOVA=
analysis of variance;
CAT12=
Computational Anatomy Toolbox;
FOV=
field of view;
GM=
gray matter;
lvPPA=
logopenic variant of primary progressive aphasia;
MMSE=
Mini-Mental State Examination;
MPRAGE=
magnetization-prepared rapid acquisition gradient echo;
nfvPPA=
nonfluent/agrammatic primary progressive aphasia;
nfvPPA-E=
English-speaking patients with nonfluent/agrammatic primary progressive aphasia;
nfvPPA-I=
Italian-speaking patients with nonfluent/agrammatic primary progressive aphasia;
PCC=
posterior cingulate cortex;
PPA=
primary progressive aphasia;
ROI=
region of interest;
SMA=
supplementary motor area;
svPPA=
semantic variant of primary progressive aphasia;
TE=
echo time;
TPM=
tissue probability map;
TR=
repetition time;
UCSF=
University of California, San Francisco;
VBM=
voxel-based morphometry;
WAB=
Western Aphasia Battery

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Received April 3, 2019.
  • Accepted in final form September 11, 2019.
  • © 2020 American Academy of Neurology
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