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Title: Co-infections by non-interacting pathogens are not independent: deriving new tests of interaction

Authors:
ORCiD logo [1];  [2];  [3];  [4];  [5];  [6];  [7];  [8];  [9];  [10]
  1. Los Alamos National Laboratory
  2. Université de Rennes
  3. Texas Tech University
  4. Oregon State University
  5. University of Tennessee, Knoxville
  6. Osnabrück University
  7. Imperial College London
  8. Cornell University
  9. Wright State University
  10. University of Cambridge
Publication Date:
Research Org.:
Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Laboratory Directed Research and Development (LDRD) Program
OSTI Identifier:
1603988
Report Number(s):
[LA-UR-19-23586]
[Journal ID: 1545-7885 (Electronic)]
Grant/Contract Number:  
[89233218CNA000001]
Resource Type:
Accepted Manuscript
Journal Name:
PLoS biology (Online)
Additional Journal Information:
[Journal Name: PLoS biology (Online); Journal Volume: 17; Journal Issue: 12]
Country of Publication:
United States
Language:
English
Subject:
Biological Science; Mathematics

Citation Formats

Manore, Carrie Anna, Hamelin, Frédéric M., Allen, Linda J.S., Bokil, Vrushali A., Gross, Louis J., Hilker, Frank M., Jeger, Michael J., Power, Alison G., Rúa, Megan A., and Cunniffe, Nik J. Co-infections by non-interacting pathogens are not independent: deriving new tests of interaction. United States: N. p., 2019. Web. doi:10.1371/journal.pbio.3000551.
Manore, Carrie Anna, Hamelin, Frédéric M., Allen, Linda J.S., Bokil, Vrushali A., Gross, Louis J., Hilker, Frank M., Jeger, Michael J., Power, Alison G., Rúa, Megan A., & Cunniffe, Nik J. Co-infections by non-interacting pathogens are not independent: deriving new tests of interaction. United States. doi:10.1371/journal.pbio.3000551.
Manore, Carrie Anna, Hamelin, Frédéric M., Allen, Linda J.S., Bokil, Vrushali A., Gross, Louis J., Hilker, Frank M., Jeger, Michael J., Power, Alison G., Rúa, Megan A., and Cunniffe, Nik J. Tue . "Co-infections by non-interacting pathogens are not independent: deriving new tests of interaction". United States. doi:10.1371/journal.pbio.3000551.
@article{osti_1603988,
title = {Co-infections by non-interacting pathogens are not independent: deriving new tests of interaction},
author = {Manore, Carrie Anna and Hamelin, Frédéric M. and Allen, Linda J.S. and Bokil, Vrushali A. and Gross, Louis J. and Hilker, Frank M. and Jeger, Michael J. and Power, Alison G. and Rúa, Megan A. and Cunniffe, Nik J.},
abstractNote = {},
doi = {10.1371/journal.pbio.3000551},
journal = {PLoS biology (Online)},
number = [12],
volume = [17],
place = {United States},
year = {2019},
month = {12}
}

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Works referenced in this record:

Prevalence and implications of multiple-strain infections
journal, November 2011


The importance of multiparasitism: examining the consequences of co-infections for human and animal health
journal, October 2015


The nature and consequences of coinfection in humans
journal, September 2011


Multiparasite communities in animals and humans: frequency, structure and pathogenic significance
journal, March 1998


Malaria‐Filaria Coinfection in Mice Makes Malarial Disease More Severe unless Filarial Infection Achieves Patency
journal, February 2005

  • Graham, Andrea L.; Lamb, Tracey J.; Read, Andrew F.
  • The Journal of Infectious Diseases, Vol. 191, Issue 3
  • DOI: 10.1086/426871

Importance of Sequence and Timing in Parasite Coinfections
journal, February 2019

  • Karvonen, Anssi; Jokela, Jukka; Laine, Anna-Liisa
  • Trends in Parasitology, Vol. 35, Issue 2
  • DOI: 10.1016/j.pt.2018.11.007

Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence
journal, June 2010

  • Rigaud, Thierry; Perrot-Minnot, Marie-Jeanne; Brown, Mark J. F.
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 277, Issue 1701
  • DOI: 10.1098/rspb.2010.1163

Co-infection alters population dynamics of infectious disease
journal, January 2015

  • Susi, Hanna; Barrès, Benoit; Vale, Pedro F.
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms6975

Multiple infections and the evolution of virulence
journal, January 2013

  • Alizon, Samuel; de Roode, Jacobus C.; Michalakis, Yannis
  • Ecology Letters, Vol. 16, Issue 4
  • DOI: 10.1111/ele.12076

Parasite competition hidden by correlated coinfection: using surveys and experiments to understand parasite interactions
journal, March 2011

  • Johnson, Pieter T. J.; Buller, Ian D.
  • Ecology, Vol. 92, Issue 3
  • DOI: 10.1890/10-0570.1

Parasite–Parasite Interactions in the Wild: How To Detect Them?
journal, December 2015

  • Hellard, Eléonore; Fouchet, David; Vavre, Fabrice
  • Trends in Parasitology, Vol. 31, Issue 12
  • DOI: 10.1016/j.pt.2015.07.005

Synergies and antagonisms in virus interactions
journal, November 2016


The reliability of observational approaches for detecting interspecific parasite interactions: comparison with experimental results
journal, June 2014

  • Fenton, Andy; Knowles, Sarah C. L.; Petchey, Owen L.
  • International Journal for Parasitology, Vol. 44, Issue 7
  • DOI: 10.1016/j.ijpara.2014.03.001

Species Interactions in a Parasite Community Drive Infection Risk in a Wildlife Population
journal, October 2010


Estimating the number of multiple-species geohelminth infections in human communities
journal, December 1995


Methods for estimation of associations between multiple species parasite infections
journal, February 2001


Colonisation by Streptococcus pneumoniae and Staphylococcus aureus in healthy children
journal, June 2004


Multiple parasite infections and their relationship to self-reported morbidity in a community of rural Cote d'Ivoire
journal, May 2004

  • Raso, G.
  • International Journal of Epidemiology, Vol. 33, Issue 5
  • DOI: 10.1093/ije/dyh241

Cross-sectional relationship between HIV, lymphatic filariasis and other parasitic infections in adults in coastal northeastern Tanzania
journal, June 2006

  • Nielsen, N. O.; Simonsen, P. E.; Magnussen, P.
  • Transactions of the Royal Society of Tropical Medicine and Hygiene, Vol. 100, Issue 6
  • DOI: 10.1016/j.trstmh.2005.08.016

Human Papillomavirus Infection with Multiple Types: Pattern of Coinfection and Risk of Cervical Disease
journal, April 2011

  • Chaturvedi, Anil K.; Katki, Hormuzd A.; Hildesheim, Allan
  • The Journal of Infectious Diseases, Vol. 203, Issue 7
  • DOI: 10.1093/infdis/jiq139

Multiple Human Papillomavirus Infections and Type Competition in Men
journal, November 2011

  • Rositch, Anne F.; Poole, Charles; Hudgens, Michael G.
  • The Journal of Infectious Diseases, Vol. 205, Issue 1
  • DOI: 10.1093/infdis/jir709

Malaria and related outcomes in patients with intestinal helminths: a cross-sectional study
journal, November 2012

  • Degarege, Abraham; Legesse, Mengistu; Medhin, Girmay
  • BMC Infectious Diseases, Vol. 12, Issue 1
  • DOI: 10.1186/1471-2334-12-291

Tuberculosis-Human Immunodeficiency Virus (HIV) co-infection in Ethiopia: a systematic review and meta-analysis
journal, December 2018

  • Teweldemedhin, Mebrahtu; Asres, Negasi; Gebreyesus, Hailay
  • BMC Infectious Diseases, Vol. 18, Issue 1
  • DOI: 10.1186/s12879-018-3604-9

Evolutionary and Epidemiological Implications of Multiple Infection in Plants
journal, January 2016


Dynamics of Multiple Infection and Within‐Host Competition in Genetically Diverse Malaria Infections
journal, November 2005

  • de Roode, Jacobus C.; Helinski, Michelle E. H.; Anwar, M. Ali
  • The American Naturalist, Vol. 166, Issue 5
  • DOI: 10.1086/491659

Population dynamic interference among childhood diseases
journal, November 1998

  • Rohani, P.; Earn, D. J.; Finkenstädt, B.
  • Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 265, Issue 1410
  • DOI: 10.1098/rspb.1998.0537

Ecological interference between fatal diseases
journal, April 2003

  • Rohani, P.; Green, C. J.; Mantilla-Beniers, N. B.
  • Nature, Vol. 422, Issue 6934
  • DOI: 10.1038/nature01542

Aggregation and distribution of strains in microparasites
journal, April 1999

  • Lord, C. C.; Barnard, B.; Day, K.
  • Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 354, Issue 1384
  • DOI: 10.1098/rstb.1999.0432

Age profile of immunity to influenza: Effect of original antigenic sin
journal, March 2012


Capturing the dynamics of pathogens with many strains
journal, March 2015

  • Kucharski, Adam J.; Andreasen, Viggo; Gog, Julia R.
  • Journal of Mathematical Biology, Vol. 72, Issue 1-2
  • DOI: 10.1007/s00285-015-0873-4

Emphasizing the ecology in parasite community ecology
journal, March 2007


True versus False Parasite Interactions: A Robust Method to Take Risk Factors into Account and Its Application to Feline Viruses
journal, January 2012


To be or not to be associated: power study of four statistical modeling approaches to identify parasite associations in cross-sectional studies
journal, May 2014

  • Vaumourin, Elise; Vourc'h, Gwenaël; Telfer, Sandra
  • Frontiers in Cellular and Infection Microbiology, Vol. 4
  • DOI: 10.3389/fcimb.2014.00062

Statistical Inference for Multi-Pathogen Systems
journal, August 2011


Identifying the Interaction Between Influenza and Pneumococcal Pneumonia Using Incidence Data
journal, June 2013


Inferring Pathogen Type Interactions Using Cross-sectional Prevalence Data: Opportunities and Pitfalls for Predicting Type Replacement
journal, January 2018


Detecting within-host interactions from genotype combination prevalence data
journal, December 2019


Heterologous Immunity in Human Malaria
journal, September 1973

  • Cohen, Joel E.
  • The Quarterly Review of Biology, Vol. 48, Issue 3
  • DOI: 10.1086/407705

Multiple Infections by the Anther Smut Pathogen Are Frequent and Involve Related Strains
journal, January 2007


Multiple-Strain Infections of Borrelia afzelii : A Role for Within-Host Interactions in the Maintenance of Antigenic Diversity?
journal, April 2013

  • Andersson, Martin; Scherman, Kristin; Råberg, Lars
  • The American Naturalist, Vol. 181, Issue 4
  • DOI: 10.1086/669905

Multiplicity and Diversity of Plasmodium vivax Infections in a Highly Endemic Region in Papua New Guinea
journal, December 2011


Extensive multiplex PCR diagnostics reveal new insights into the epidemiology of viral respiratory infections
journal, March 2016

  • Nickbakhsh, S.; Thorburn, F.; Von Wissmann, B.
  • Epidemiology and Infection, Vol. 144, Issue 10
  • DOI: 10.1017/S0950268816000339

Diversity and Composition of Viral Communities: Coinfection of Barley and Cereal Yellow Dwarf Viruses in California Grasslands
journal, March 2009

  • Seabloom, Eric W.; Hosseini, Parviez R.; Power, Alison G.
  • The American Naturalist, Vol. 173, Issue 3
  • DOI: 10.1086/596529

Co-infection of Ticks: The Rule Rather Than the Exception
journal, March 2016

  • Moutailler, Sara; Valiente Moro, Claire; Vaumourin, Elise
  • PLOS Neglected Tropical Diseases, Vol. 10, Issue 3
  • DOI: 10.1371/journal.pntd.0004539

A Longitudinal Study of Human Malaria in the West African Savanna in the Absence of Control Measures: Relationships between Different Plasmodium Species, in Particular P. Falciparum and P. Malariae *
journal, September 1980

  • Thomas, Anthony; Molineaux, Louis; Cohen, Joel E.
  • The American Journal of Tropical Medicine and Hygiene, Vol. 29, Issue 5
  • DOI: 10.4269/ajtmh.1980.29.725

Opposite outcomes of coinfection at individual and population scales
journal, July 2018

  • Gorsich, Erin E.; Etienne, Rampal S.; Medlock, Jan
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 29
  • DOI: 10.1073/pnas.1801095115

Detecting parasite associations within multi-species host and parasite communities
journal, October 2019

  • Dallas, Tad A.; Laine, Anna-Liisa; Ovaskainen, Otso
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 286, Issue 1912
  • DOI: 10.1098/rspb.2019.1109

Maximum likelihood estimation in log-linear models
journal, April 2012

  • Fienberg, Stephen E.; Rinaldo, Alessandro
  • The Annals of Statistics, Vol. 40, Issue 2
  • DOI: 10.1214/12-AOS986

Modeling the Interruption of the Transmission of Soil-Transmitted Helminths by Repeated Mass Chemotherapy of School-Age Children
journal, December 2014

  • Truscott, James; Hollingsworth, T. Déirdre; Anderson, Roy
  • PLoS Neglected Tropical Diseases, Vol. 8, Issue 12
  • DOI: 10.1371/journal.pntd.0003323

Link between the numbers of particles and variants founding new HIV-1 infections depends on the timing of transmission
journal, January 2019

  • Thompson, Robin N.; Wymant, Chris; Spriggs, Rebecca A.
  • Virus Evolution, Vol. 5, Issue 1
  • DOI: 10.1093/ve/vey038

Optimising and Communicating Options for the Control of Invasive Plant Disease When There Is Epidemiological Uncertainty
journal, April 2015

  • Cunniffe, Nik J.; Stutt, Richard O. J. H.; DeSimone, R. Erik
  • PLOS Computational Biology, Vol. 11, Issue 4
  • DOI: 10.1371/journal.pcbi.1004211

Modeling when, where, and how to manage a forest epidemic, motivated by sudden oak death in California
journal, May 2016

  • Cunniffe, Nik J.; Cobb, Richard C.; Meentemeyer, Ross K.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 20
  • DOI: 10.1073/pnas.1602153113

Seven challenges for metapopulation models of epidemics, including households models
journal, March 2015


Role of genetic heterogeneity in determining the epidemiological severity of H1N1 influenza
journal, March 2018

  • Sambaturu, Narmada; Mukherjee, Sumanta; López-García, Martín
  • PLOS Computational Biology, Vol. 14, Issue 3
  • DOI: 10.1371/journal.pcbi.1006069

Superspreading and the effect of individual variation on disease emergence
journal, November 2005

  • Lloyd-Smith, J. O.; Schreiber, S. J.; Kopp, P. E.
  • Nature, Vol. 438, Issue 7066
  • DOI: 10.1038/nature04153

The community ecology of pathogens: coinfection, coexistence and community composition
journal, March 2015

  • Seabloom, Eric W.; Borer, Elizabeth T.; Gross, Kevin
  • Ecology Letters, Vol. 18, Issue 4
  • DOI: 10.1111/ele.12418

Community Structure: A Neutral Model Analysis
journal, February 1976

  • Caswell, Hal
  • Ecological Monographs, Vol. 46, Issue 3
  • DOI: 10.2307/1942257

The Assembly of Species Communities: Chance or Competition?
journal, December 1979

  • Connor, Edward F.; Simberloff, Daniel
  • Ecology, Vol. 60, Issue 6
  • DOI: 10.2307/1936961

Null Model Analysis of Species Co-Occurrence Patterns
journal, September 2000


Statistical challenges in null model analysis
journal, November 2011


Can Competition Be Detected Using Species Co-Occurrence Data?
journal, February 1987


Exact stochastic simulation of coupled chemical reactions
journal, December 1977

  • Gillespie, Daniel T.
  • The Journal of Physical Chemistry, Vol. 81, Issue 25
  • DOI: 10.1021/j100540a008

Solutions of ordinary differential equations as limits of pure jump markov processes
journal, April 1970

  • Kurtz, Thomas G.
  • Journal of Applied Probability, Vol. 7, Issue 1
  • DOI: 10.2307/3212147

Construction of Equivalent Stochastic Differential Equation Models
journal, March 2008

  • Allen, Edward J.; Allen, Linda J. S.; Arciniega, Armando
  • Stochastic Analysis and Applications, Vol. 26, Issue 2
  • DOI: 10.1080/07362990701857129