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Increased rates of secondary bacterial infections, including Enterococcus bacteremia, in patients hospitalized with coronavirus disease 2019 (COVID-19)
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- Catherine DeVoe, Mark R. Segal, Lusha Wang, Kim Stanley, Sharline Madera, Joe Fan, Jonathan Schouest, Renee Graham-Ojo, Amy Nichols, Priya A. Prasad, Rajani Ghale, Christina Love, Yumiko Abe-Jones, Kirsten N. Kangelaris, Sarah L. Patterson, Deborah S. Yokoe, Charles R. Langelier
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- Journal:
- Infection Control & Hospital Epidemiology / Volume 43 / Issue 10 / October 2022
- Published online by Cambridge University Press:
- 06 September 2021, pp. 1416-1423
- Print publication:
- October 2022
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Objective:
We compared the rates of hospital-onset secondary bacterial infections in patients with coronavirus disease 2019 (COVID-19) with rates in patients with influenza and controls, and we investigated reports of increased incidence of Enterococcus infections in patients with COVID-19.
Design:Retrospective cohort study.
Setting:An academic quaternary-care hospital in San Francisco, California.
Patients:Patients admitted between October 1, 2019, and October 1, 2020, with a positive SARS-CoV-2 PCR (N = 314) or influenza PCR (N = 82) within 2 weeks of admission were compared with inpatients without positive SARS-CoV-2 or influenza tests during the study period (N = 14,332).
Methods:National Healthcare Safety Network definitions were used to identify infection-related ventilator-associated complications (IVACs), probable ventilator-associated pneumonia (PVAP), bloodstream infections (BSIs), and catheter-associated urinary tract infections (CAUTIs). A multiple logistic regression model was used to control for likely confounders.
Results:COVID-19 patients had significantly higher rates of IVAC and PVAP compared to controls, with adjusted odds ratios of 4.7 (95% confidence interval [CI], 1.7–13.9) and 10.4 (95 % CI, 2.1–52.1), respectively. COVID-19 patients had higher incidence of BSI due to Enterococcus but not BSI generally, and whole-genome sequencing of Enterococcus isolates demonstrated that nosocomial transmission did not explain the increased rate. Subanalyses of patients admitted to the intensive care unit and patients who required mechanical ventilation revealed similar findings.
Conclusions:COVID-19 is associated with an increased risk of IVAC, PVAP, and Enterococcus BSI compared with hospitalized controls, which is not fully explained by factors such as immunosuppressive treatments and duration of mechanical ventilation. The mechanism underlying increased rates of Enterococcus BSI in COVID-19 patients requires further investigation.
Contributors
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- By Mitchell Aboulafia, Frederick Adams, Marilyn McCord Adams, Robert M. Adams, Laird Addis, James W. Allard, David Allison, William P. Alston, Karl Ameriks, C. Anthony Anderson, David Leech Anderson, Lanier Anderson, Roger Ariew, David Armstrong, Denis G. Arnold, E. J. Ashworth, Margaret Atherton, Robin Attfield, Bruce Aune, Edward Wilson Averill, Jody Azzouni, Kent Bach, Andrew Bailey, Lynne Rudder Baker, Thomas R. Baldwin, Jon Barwise, George Bealer, William Bechtel, Lawrence C. Becker, Mark A. Bedau, Ernst Behler, José A. Benardete, Ermanno Bencivenga, Jan Berg, Michael Bergmann, Robert L. Bernasconi, Sven Bernecker, Bernard Berofsky, Rod Bertolet, Charles J. Beyer, Christian Beyer, Joseph Bien, Joseph Bien, Peg Birmingham, Ivan Boh, James Bohman, Daniel Bonevac, Laurence BonJour, William J. Bouwsma, Raymond D. Bradley, Myles Brand, Richard B. Brandt, Michael E. Bratman, Stephen E. Braude, Daniel Breazeale, Angela Breitenbach, Jason Bridges, David O. Brink, Gordon G. Brittan, Justin Broackes, Dan W. Brock, Aaron Bronfman, Jeffrey E. Brower, Bartosz Brozek, Anthony Brueckner, Jeffrey Bub, Lara Buchak, Otavio Bueno, Ann E. Bumpus, Robert W. Burch, John Burgess, Arthur W. Burks, Panayot Butchvarov, Robert E. Butts, Marina Bykova, Patrick Byrne, David Carr, Noël Carroll, Edward S. Casey, Victor Caston, Victor Caston, Albert Casullo, Robert L. Causey, Alan K. L. Chan, Ruth Chang, Deen K. Chatterjee, Andrew Chignell, Roderick M. Chisholm, Kelly J. Clark, E. J. Coffman, Robin Collins, Brian P. Copenhaver, John Corcoran, John Cottingham, Roger Crisp, Frederick J. Crosson, Antonio S. Cua, Phillip D. Cummins, Martin Curd, Adam Cureton, Andrew Cutrofello, Stephen Darwall, Paul Sheldon Davies, Wayne A. Davis, Timothy Joseph Day, Claudio de Almeida, Mario De Caro, Mario De Caro, John Deigh, C. F. Delaney, Daniel C. Dennett, Michael R. DePaul, Michael Detlefsen, Daniel Trent Devereux, Philip E. Devine, John M. Dillon, Martin C. Dillon, Robert DiSalle, Mary Domski, Alan Donagan, Paul Draper, Fred Dretske, Mircea Dumitru, Wilhelm Dupré, Gerald Dworkin, John Earman, Ellery Eells, Catherine Z. Elgin, Berent Enç, Ronald P. Endicott, Edward Erwin, John Etchemendy, C. Stephen Evans, Susan L. Feagin, Solomon Feferman, Richard Feldman, Arthur Fine, Maurice A. Finocchiaro, William FitzPatrick, Richard E. Flathman, Gvozden Flego, Richard Foley, Graeme Forbes, Rainer Forst, Malcolm R. Forster, Daniel Fouke, Patrick Francken, Samuel Freeman, Elizabeth Fricker, Miranda Fricker, Michael Friedman, Michael Fuerstein, Richard A. Fumerton, Alan Gabbey, Pieranna Garavaso, Daniel Garber, Jorge L. A. Garcia, Robert K. Garcia, Don Garrett, Philip Gasper, Gerald Gaus, Berys Gaut, Bernard Gert, Roger F. Gibson, Cody Gilmore, Carl Ginet, Alan H. Goldman, Alvin I. Goldman, Alfonso Gömez-Lobo, Lenn E. Goodman, Robert M. Gordon, Stefan Gosepath, Jorge J. E. Gracia, Daniel W. Graham, George A. Graham, Peter J. Graham, Richard E. Grandy, I. Grattan-Guinness, John Greco, Philip T. Grier, Nicholas Griffin, Nicholas Griffin, David A. Griffiths, Paul J. Griffiths, Stephen R. Grimm, Charles L. Griswold, Charles B. Guignon, Pete A. Y. Gunter, Dimitri Gutas, Gary Gutting, Paul Guyer, Kwame Gyekye, Oscar A. Haac, Raul Hakli, Raul Hakli, Michael Hallett, Edward C. Halper, Jean Hampton, R. James Hankinson, K. R. Hanley, Russell Hardin, Robert M. Harnish, William Harper, David Harrah, Kevin Hart, Ali Hasan, William Hasker, John Haugeland, Roger Hausheer, William Heald, Peter Heath, Richard Heck, John F. Heil, Vincent F. Hendricks, Stephen Hetherington, Francis Heylighen, Kathleen Marie Higgins, Risto Hilpinen, Harold T. Hodes, Joshua Hoffman, Alan Holland, Robert L. Holmes, Richard Holton, Brad W. Hooker, Terence E. Horgan, Tamara Horowitz, Paul Horwich, Vittorio Hösle, Paul Hoβfeld, Daniel Howard-Snyder, Frances Howard-Snyder, Anne Hudson, Deal W. Hudson, Carl A. Huffman, David L. Hull, Patricia Huntington, Thomas Hurka, Paul Hurley, Rosalind Hursthouse, Guillermo Hurtado, Ronald E. Hustwit, Sarah Hutton, Jonathan Jenkins Ichikawa, Harry A. Ide, David Ingram, Philip J. Ivanhoe, Alfred L. Ivry, Frank Jackson, Dale Jacquette, Joseph Jedwab, Richard Jeffrey, David Alan Johnson, Edward Johnson, Mark D. Jordan, Richard Joyce, Hwa Yol Jung, Robert Hillary Kane, Tomis Kapitan, Jacquelyn Ann K. Kegley, James A. Keller, Ralph Kennedy, Sergei Khoruzhii, Jaegwon Kim, Yersu Kim, Nathan L. King, Patricia Kitcher, Peter D. Klein, E. D. Klemke, Virginia Klenk, George L. Kline, Christian Klotz, Simo Knuuttila, Joseph J. Kockelmans, Konstantin Kolenda, Sebastian Tomasz Kołodziejczyk, Isaac Kramnick, Richard Kraut, Fred Kroon, Manfred Kuehn, Steven T. Kuhn, Henry E. Kyburg, John Lachs, Jennifer Lackey, Stephen E. Lahey, Andrea Lavazza, Thomas H. Leahey, Joo Heung Lee, Keith Lehrer, Dorothy Leland, Noah M. Lemos, Ernest LePore, Sarah-Jane Leslie, Isaac Levi, Andrew Levine, Alan E. Lewis, Daniel E. Little, Shu-hsien Liu, Shu-hsien Liu, Alan K. L. Chan, Brian Loar, Lawrence B. Lombard, John Longeway, Dominic McIver Lopes, Michael J. Loux, E. J. Lowe, Steven Luper, Eugene C. Luschei, William G. Lycan, David Lyons, David Macarthur, Danielle Macbeth, Scott MacDonald, Jacob L. Mackey, Louis H. Mackey, Penelope Mackie, Edward H. Madden, Penelope Maddy, G. B. Madison, Bernd Magnus, Pekka Mäkelä, Rudolf A. Makkreel, David Manley, William E. Mann (W.E.M.), Vladimir Marchenkov, Peter Markie, Jean-Pierre Marquis, Ausonio Marras, Mike W. Martin, A. P. Martinich, William L. McBride, David McCabe, Storrs McCall, Hugh J. McCann, Robert N. McCauley, John J. McDermott, Sarah McGrath, Ralph McInerny, Daniel J. McKaughan, Thomas McKay, Michael McKinsey, Brian P. McLaughlin, Ernan McMullin, Anthonie Meijers, Jack W. Meiland, William Jason Melanson, Alfred R. Mele, Joseph R. Mendola, Christopher Menzel, Michael J. Meyer, Christian B. Miller, David W. Miller, Peter Millican, Robert N. Minor, Phillip Mitsis, James A. Montmarquet, Michael S. Moore, Tim Moore, Benjamin Morison, Donald R. Morrison, Stephen J. Morse, Paul K. Moser, Alexander P. D. Mourelatos, Ian Mueller, James Bernard Murphy, Mark C. Murphy, Steven Nadler, Jan Narveson, Alan Nelson, Jerome Neu, Samuel Newlands, Kai Nielsen, Ilkka Niiniluoto, Carlos G. Noreña, Calvin G. Normore, David Fate Norton, Nikolaj Nottelmann, Donald Nute, David S. Oderberg, Steve Odin, Michael O’Rourke, Willard G. Oxtoby, Heinz Paetzold, George S. Pappas, Anthony J. Parel, Lydia Patton, R. P. Peerenboom, Francis Jeffry Pelletier, Adriaan T. Peperzak, Derk Pereboom, Jaroslav Peregrin, Glen Pettigrove, Philip Pettit, Edmund L. Pincoffs, Andrew Pinsent, Robert B. Pippin, Alvin Plantinga, Louis P. Pojman, Richard H. Popkin, John F. Post, Carl J. Posy, William J. Prior, Richard Purtill, Michael Quante, Philip L. Quinn, Philip L. Quinn, Elizabeth S. Radcliffe, Diana Raffman, Gerard Raulet, Stephen L. Read, Andrews Reath, Andrew Reisner, Nicholas Rescher, Henry S. Richardson, Robert C. Richardson, Thomas Ricketts, Wayne D. Riggs, Mark Roberts, Robert C. Roberts, Luke Robinson, Alexander Rosenberg, Gary Rosenkranz, Bernice Glatzer Rosenthal, Adina L. Roskies, William L. Rowe, T. M. Rudavsky, Michael Ruse, Bruce Russell, Lilly-Marlene Russow, Dan Ryder, R. M. Sainsbury, Joseph Salerno, Nathan Salmon, Wesley C. Salmon, Constantine Sandis, David H. Sanford, Marco Santambrogio, David Sapire, Ruth A. Saunders, Geoffrey Sayre-McCord, Charles Sayward, James P. Scanlan, Richard Schacht, Tamar Schapiro, Frederick F. Schmitt, Jerome B. Schneewind, Calvin O. Schrag, Alan D. Schrift, George F. Schumm, Jean-Loup Seban, David N. Sedley, Kenneth Seeskin, Krister Segerberg, Charlene Haddock Seigfried, Dennis M. Senchuk, James F. Sennett, William Lad Sessions, Stewart Shapiro, Tommie Shelby, Donald W. Sherburne, Christopher Shields, Roger A. Shiner, Sydney Shoemaker, Robert K. Shope, Kwong-loi Shun, Wilfried Sieg, A. John Simmons, Robert L. Simon, Marcus G. Singer, Georgette Sinkler, Walter Sinnott-Armstrong, Matti T. Sintonen, Lawrence Sklar, Brian Skyrms, Robert C. Sleigh, Michael Anthony Slote, Hans Sluga, Barry Smith, Michael Smith, Robin Smith, Robert Sokolowski, Robert C. Solomon, Marta Soniewicka, Philip Soper, Ernest Sosa, Nicholas Southwood, Paul Vincent Spade, T. L. S. Sprigge, Eric O. Springsted, George J. Stack, Rebecca Stangl, Jason Stanley, Florian Steinberger, Sören Stenlund, Christopher Stephens, James P. Sterba, Josef Stern, Matthias Steup, M. A. Stewart, Leopold Stubenberg, Edith Dudley Sulla, Frederick Suppe, Jere Paul Surber, David George Sussman, Sigrún Svavarsdóttir, Zeno G. Swijtink, Richard Swinburne, Charles C. Taliaferro, Robert B. Talisse, John Tasioulas, Paul Teller, Larry S. Temkin, Mark Textor, H. S. Thayer, Peter Thielke, Alan Thomas, Amie L. Thomasson, Katherine Thomson-Jones, Joshua C. Thurow, Vzalerie Tiberius, Terrence N. Tice, Paul Tidman, Mark C. Timmons, William Tolhurst, James E. Tomberlin, Rosemarie Tong, Lawrence Torcello, Kelly Trogdon, J. D. Trout, Robert E. Tully, Raimo Tuomela, John Turri, Martin M. Tweedale, Thomas Uebel, Jennifer Uleman, James Van Cleve, Harry van der Linden, Peter van Inwagen, Bryan W. Van Norden, René van Woudenberg, Donald Phillip Verene, Samantha Vice, Thomas Vinci, Donald Wayne Viney, Barbara Von Eckardt, Peter B. M. Vranas, Steven J. Wagner, William J. Wainwright, Paul E. Walker, Robert E. Wall, Craig Walton, Douglas Walton, Eric Watkins, Richard A. Watson, Michael V. Wedin, Rudolph H. Weingartner, Paul Weirich, Paul J. Weithman, Carl Wellman, Howard Wettstein, Samuel C. Wheeler, Stephen A. White, Jennifer Whiting, Edward R. Wierenga, Michael Williams, Fred Wilson, W. Kent Wilson, Kenneth P. Winkler, John F. Wippel, Jan Woleński, Allan B. Wolter, Nicholas P. Wolterstorff, Rega Wood, W. Jay Wood, Paul Woodruff, Alison Wylie, Gideon Yaffe, Takashi Yagisawa, Yutaka Yamamoto, Keith E. Yandell, Xiaomei Yang, Dean Zimmerman, Günter Zoller, Catherine Zuckert, Michael Zuckert, Jack A. Zupko (J.A.Z.)
- Edited by Robert Audi, University of Notre Dame, Indiana
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- The Cambridge Dictionary of Philosophy
- Published online:
- 05 August 2015
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- 27 April 2015, pp ix-xxx
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- By Rhonda A. Alexis, Graciela Argote-Romero, Amanda K. Brown, Veronica O. Busso, Julie Chen, Vidya Chidambaran, Smokey J. Clay, Andrew J. Costandi, Mary A. Felberg, John Fiadjoe, Kenneth R. Goldschneider, Diane Gordon, Erin A. Gottlieb, Amy Graham-Carlson, Nancy S. Hagerman, Stephen Robert Hays, Lisa D. Heyden, Normidaris Jimenez, Tae W. Kim, Rachel A. Koll, Rebecca Laurich, Yang Liu, Mohamed Mahmoud, Jagroop Mavi, Matthew Mitchell, David L. Moore, Jacquelyn W. Morillo-Delerme, Pablo Motta, Vanessa A. Olbrecht, Olutoyin A. Olutoye, Carlos L. Rodriguez, Joanna L. Rosing, Senthilkumar Sadhasivam, Catherine P. Seipel, Shakeel A. Siddiqui, Matthew D. Sjoblom, Paul Stricker, Rajeev Subramanyam, Alexandra Szabova, Kha M. Tran, Premal M. Trivedi, Luigi Viola, Nitin Wadhwa, David A. Young
- Edited by David A. Young, Baylor College of Medicine, Texas, Olutoyin A. Olutoye, Baylor College of Medicine, Texas
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- Handbook of Critical Incidents and Essential Topics in Pediatric Anesthesiology
- Published online:
- 05 November 2014
- Print publication:
- 13 October 2014, pp xv-xviii
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- By Graeme J.M. Alexander, Heung Bae Kim, Michael Burch, Andrew J. Butler, Tanveer Butt, Roy Calne, Edward Cantu, Robert B. Colvin, Paul Corris, Charles Crawley, Hiroshi Date, Francis L. Delmonico, Bimalangshu R. Dey, Kate Drummond, John Dunning, John D. Firth, John Forsythe, Simon M. Gabe, Robert S. Gaston, William Gelson, Paul Gibbs, Alex Gimson, Leo C. Ginns, Samuel Goldfarb, Ryoichi Goto, Walter K. Graham, Simon J.F. Harper, Koji Hashimoto, David G. Healy, Hassan N. Ibrahim, David Ip, Fadi G. Issa, Neville V. Jamieson, David P. Jenkins, Dixon B. Kaufman, Kiran K. Khush, Heung Bae Kim, Andrew A. Klein, John Klinck, Camille Nelson Kotton, Vineeta Kumar, Yael B. Kushner, D. Frank. P. Larkin, Clive J. Lewis, Yvonne H. Luo, Richard S. Luskin, Ernest I. Mandel, James F. Markmann, Lorna Marson, Arthur J. Matas, Mandeep R. Mehra, Stephen J. Middleton, Giorgina Mieli-Vergani, Charles Miller, Sharon Mulroy, Faruk Özalp, Can Ozturk, Jayan Parameshwar, J.S. Parmar, Hari K. Parthasarathy, Nick Pritchard, Cristiano Quintini, Axel O. Rahmel, Chris J. Rudge, Stephan V.B. Schueler, Maria Siemionow, Jacob Simmonds, Peter Slinger, Thomas R. Spitzer, Stuart C. Sweet, Nina E. Tolkoff-Rubin, Steven S.L. Tsui, Khashayar Vakili, R.V. Venkateswaran, Hector Vilca-Melendez, Vladimir Vinarsky, Kathryn J. Wood, Heidi Yeh, David W. Zaas, Jonathan G. Zaroff
- Edited by Andrew A. Klein, Clive J. Lewis, Joren C. Madsen
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- Organ Transplantation
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- 07 September 2011
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- 11 August 2011, pp vii-x
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- By Sayeda Abu-Amero, Ivo Brosens, Jan Brosens, Graham J. Burton, Anthony M. Carter, Judith E. Cartwright, Brianna Cloke, Christophe L. Depoix, Sascha Drewlo, Caroline Dunk, Qi Fu, Luca Fusi, David Haig, Myriam C. Hanssens, Frans M. Helmerhorst, Pak Chung Ho, Eric Jauniaux, S. Ananth Karumanchi, Marc J. N. C. Keirse, Eliyahu V. Khankin, T. Yee Khong, Stephen R. Killick, Chong Jai Kim, John C. P. Kingdom, Juan Pedro Kusanovic, Robert H. Lane, Piotr Lesny, Robert D. Martin, Robert A. McKnight, Kari K. Melve, Ashley Moffett, Gudrun E. Moore, Linda Morgan, Ernest Hung Yu Ng, Robert Pijnenborg, Leslie Proctor, Sarosh Rana, Roberto Romero, Rolv Skjaerven, Gordon C. S. Smith, Robert N. Taylor, May Lee Tjoa, Lars J. Vatten, Lisbeth Vercruysse, Guy St. J. Whitley
- Edited by Robert Pijnenborg, Ivo Brosens, Roberto Romero
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- Placental Bed Disorders
- Published online:
- 06 July 2010
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- 03 June 2010, pp ix-xii
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Molecular epidemiology of Helicobacter pylori: separation of H. pylori from East Asian and non-Asian countries
- Y. YAMAOKA, M. S. OSATO, A. R. SEPULVEDA, O. GUTIERREZ, N. FIGURA, J. G. KIM, T. KODAMA, K. KASHIMA, D. Y. GRAHAM
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- Journal:
- Epidemiology & Infection / Volume 124 / Issue 1 / February 2000
- Published online by Cambridge University Press:
- 01 February 2000, pp. 91-96
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The predominant H. pylori strain circulating among geographic locations differs with regard to the genomic structure. This study determined whether structural subtypes of the cagA 3′ repeat region could be used to identify the population of origin of H. pylori isolates. We examined 600 cagA-positive H. pylori (Colombia, 100; USA, 100; France, 100; Canada, 20; Italy, 20; Korea, 100; Japan, 100; Hong Kong, 20; Taiwan, 20; Vietnam, 20). The cagA 3′ region was amplified by PCR using primers specific to Japanese and Western 3′ cagA gene sequences. PCR using Japanese cagA primers resulted in PCR products in 99·6% of strains from East Asia but no non-Asian strains. Conversely, PCR using Western cagA primers resulted in amplicons in 100% of non-Asian strains, and only one from East Asia. cagA genotyping is useful for molecular epidemiological studies as strains can be completely separated by differences in the cagA 3′ region.
Episodic memory in semantic dementia: Implications for the roles played by the perirhinal and hippocampal memory systems in new learning
- Kim S. Graham, John R. Hodges
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- Journal:
- Behavioral and Brain Sciences / Volume 22 / Issue 3 / June 1999
- Published online by Cambridge University Press:
- 01 June 1999, pp. 452-453
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Aggleton & Brown (A&B) propose that the hippocampal-anterior thalamic and perirhinal-medial dorsal thalamic systems play independent roles in episodic memory, with the hippocampus supporting recollection-based memory and the perirhinal cortex, recognition memory. In this commentary we discuss whether there is experimental support for the A&B model from studies of long-term memory in semantic dementia.
On the relationship between knowledge and memory for pictures: Evidence from the study of patients with semantic dementia and Alzheimer's disease
- KIM S. GRAHAM, JAMES T. BECKER, JOHN R. HODGES
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- Journal:
- Journal of the International Neuropsychological Society / Volume 3 / Issue 6 / November 1997
- Published online by Cambridge University Press:
- 01 November 1997, pp. 534-544
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Current views of long-term memory presume that both the hippocampal complex and the neocortex play interactive, but separate, roles in the storage of memories. While the neocortex is considered the eventual and permanent store for our memories, the encoding of recently experienced events is thought to be initially dependent upon the hippocampus and closely related structures. Neuropsychological studies have demonstrated that damage to the medial temporal lobe results in a retrograde amnesia extending back in time, with better preservation of older memories. The converse pattern has been shown in patients with semantic dementia, who have focal atrophy of the inferolateral temporal neocortex, but relative sparing of the hippocampal complex (Graham & Hodges, 1997). Here we demonstrate that such patients can show relatively preserved new learning on a forced-choice recognition memory test (based on real and chimeric animals), while patients in the early amnestic phase of Alzheimer's disease show severely impaired learning on the same test. This result provides support for the view that new learning is primarily dependent upon the hippocampus and related structures. (JINS, 1997, 3, 534–544.)