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Published in: EcoHealth 3/2017

01-09-2017 | Original Contribution

Varicella Coinfection in Patients with Active Monkeypox in the Democratic Republic of the Congo

Authors: Nicole A. Hoff, Douglas S. Morier, Neville K. Kisalu, Sara C. Johnston, Reena H. Doshi, Lisa E. Hensley, Emile Okitolonda-Wemakoy, Jean Jacques Muyembe-Tamfum, James O. Lloyd-Smith, Anne W. Rimoin

Published in: EcoHealth | Issue 3/2017

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Abstract

From 2006 to 2007, an active surveillance program for human monkeypox (MPX) in the Democratic Republic of the Congo identified 151 cases of coinfection with monkeypox virus and varicella zoster virus from 1158 suspected cases of human MPX (13%). Using clinical and socio-demographic data collected with standardized instruments by trained, local nurse supervisors, we examined a variety of hypotheses to explain the unexpectedly high proportion of coinfections among the sample, including the hypothesis that the two viruses occur independently. The probabilities of disease incidence and selection necessary to yield the observed sample proportion of coinfections under an assumption of independence are plausible given what is known and assumed about human MPX incidence. Cases of human MPX are expected to be underreported, and more coinfections are expected with improved surveillance.
Literature
go back to reference Berkson, J. 1946. ‘LIMITATIONS OF THE APPLICATION OF FOURFOLD TABLE ANALYSIS TO HOSPITAL DATA’, Biometrics Bulletin, 2.CrossRefPubMed Berkson, J. 1946. ‘LIMITATIONS OF THE APPLICATION OF FOURFOLD TABLE ANALYSIS TO HOSPITAL DATA’, Biometrics Bulletin, 2.CrossRefPubMed
go back to reference Breman, J. G., Kalisaruti, M. V. Steniowski, E. Zanotto, A. I. Gromyko, and I. Arita. 1980. ‘HUMAN MONKEYPOX, 1970-79’, Bulletin of the World Health Organization, 58: 165-82.PubMedPubMedCentral Breman, J. G., Kalisaruti, M. V. Steniowski, E. Zanotto, A. I. Gromyko, and I. Arita. 1980. ‘HUMAN MONKEYPOX, 1970-79’, Bulletin of the World Health Organization, 58: 165-82.PubMedPubMedCentral
go back to reference Breuer, Judith. 2004. ‘Varicella Zoster.’ in Arie J. Zuckerman, Jangu E. Banatvala, John R. Pattison, Paul D. Griffiths and Barry D. Schoub (eds.), Principles and practice of clinical virology (Wiley: Chichester; Hoboken, NJ). Breuer, Judith. 2004. ‘Varicella Zoster.’ in Arie J. Zuckerman, Jangu E. Banatvala, John R. Pattison, Paul D. Griffiths and Barry D. Schoub (eds.), Principles and practice of clinical virology (Wiley: Chichester; Hoboken, NJ).
go back to reference Fairley, C. K., and E. Miller. 1996. ‘Varicella-Zoster virus epidemiology - A changing scene?’, Journal of Infectious Diseases, 174.CrossRefPubMed Fairley, C. K., and E. Miller. 1996. ‘Varicella-Zoster virus epidemiology - A changing scene?’, Journal of Infectious Diseases, 174.CrossRefPubMed
go back to reference Feder, H. M., and D. M. Hoss. 2004. ‘Herpes zoster in otherwise healthy children’, Pediatric Infectious Disease Journal, 23: 451-57.CrossRefPubMed Feder, H. M., and D. M. Hoss. 2004. ‘Herpes zoster in otherwise healthy children’, Pediatric Infectious Disease Journal, 23: 451-57.CrossRefPubMed
go back to reference Friendly M (2013) Working with categorical data with R and the vcd and vcdExtra packages Friendly M (2013) Working with categorical data with R and the vcd and vcdExtra packages
go back to reference Garnett, G. P., M. J. Cox, D. A. P. Bundy, J. M. Didier, and J. Stcatharine. 1993. ‘THE AGE OF INFECTION WITH VARICELLA-ZOSTER VIRUS IN ST-LUCIA, WEST-INDIES’, Epidemiology and Infection, 110.CrossRefPubMedPubMedCentral Garnett, G. P., M. J. Cox, D. A. P. Bundy, J. M. Didier, and J. Stcatharine. 1993. ‘THE AGE OF INFECTION WITH VARICELLA-ZOSTER VIRUS IN ST-LUCIA, WEST-INDIES’, Epidemiology and Infection, 110.CrossRefPubMedPubMedCentral
go back to reference Graham, Andrea L., Isabella M. Cattadori, James O. Lloyd-Smith, Matthew J. Ferrari, and Ottar N. Bjørnstad. 2007. ‘Transmission consequences of coinfection: cytokines writ large?’, Trends in Parasitology, 23: 284-91.CrossRefPubMed Graham, Andrea L., Isabella M. Cattadori, James O. Lloyd-Smith, Matthew J. Ferrari, and Ottar N. Bjørnstad. 2007. ‘Transmission consequences of coinfection: cytokines writ large?’, Trends in Parasitology, 23: 284-91.CrossRefPubMed
go back to reference Greenland, S., J. Pearl, and J. M. Robins. 1999. ‘Causal diagrams for epidemiologic research’, Epidemiology, 10: 37-48.CrossRefPubMed Greenland, S., J. Pearl, and J. M. Robins. 1999. ‘Causal diagrams for epidemiologic research’, Epidemiology, 10: 37-48.CrossRefPubMed
go back to reference Hernan, M. A., and J. M. Robins. 2005. ‘A structural approach to observation bias’, American Journal of Epidemiology, 161: S100-S00.CrossRef Hernan, M. A., and J. M. Robins. 2005. ‘A structural approach to observation bias’, American Journal of Epidemiology, 161: S100-S00.CrossRef
go back to reference Hernán MA, Robins JM (2017) Causal inference: Part I: Causal inference without models, Boca Raton: Chapman & Hall/CRC, p 131 (forthcoming) Hernán MA, Robins JM (2017) Causal inference: Part I: Causal inference without models, Boca Raton: Chapman & Hall/CRC, p 131 (forthcoming)
go back to reference Jezek, Z., and F. Fenner. 1988. ‘MONOGRAPHS IN VIROLOGY VOL. 17. HUMAN MONKEYPOX.’ in, Jezek, Z. and F. Fenner. Monographs in Virology, Vol. 17. Human Monkeypox. X + 140p. S. Karger Ag: Basel, Switzerland; New York, New York, USA. Illus. Maps. Jezek, Z., and F. Fenner. 1988. ‘MONOGRAPHS IN VIROLOGY VOL. 17. HUMAN MONKEYPOX.’ in, Jezek, Z. and F. Fenner. Monographs in Virology, Vol. 17. Human Monkeypox. X + 140p. S. Karger Ag: Basel, Switzerland; New York, New York, USA. Illus. Maps.
go back to reference Jezek, Z., M. Szczeniowski, K. M. Paluku, and M. Mutombo. 1987. ‘HUMAN MONKEYPOX - CLINICAL-FEATURES OF 282 PATIENTS’, Journal of Infectious Diseases, 156: 293-98.CrossRefPubMed Jezek, Z., M. Szczeniowski, K. M. Paluku, and M. Mutombo. 1987. ‘HUMAN MONKEYPOX - CLINICAL-FEATURES OF 282 PATIENTS’, Journal of Infectious Diseases, 156: 293-98.CrossRefPubMed
go back to reference Jezek, Z., L. N. Khodakevich, and M. Szczeniowski. 1988. ‘HUMAN MONKEYPOX - CLINICAL AND EPIDEMIOLOGICAL FEATURES’, Zhurnal Mikrobiologii Epidemiologii I Immunobiologii: 23-30. Jezek, Z., L. N. Khodakevich, and M. Szczeniowski. 1988. ‘HUMAN MONKEYPOX - CLINICAL AND EPIDEMIOLOGICAL FEATURES’, Zhurnal Mikrobiologii Epidemiologii I Immunobiologii: 23-30.
go back to reference Jezek, Z., M. Szczeniowski, K. M. Paluku, M. Mutombo, and B. Grab. 1988. ‘HUMAN MONKEYPOX - CONFUSION WITH CHICKENPOX’, Acta Tropica, 45: 297-307.PubMed Jezek, Z., M. Szczeniowski, K. M. Paluku, M. Mutombo, and B. Grab. 1988. ‘HUMAN MONKEYPOX - CONFUSION WITH CHICKENPOX’, Acta Tropica, 45: 297-307.PubMed
go back to reference Kugelman, J. R., S. C. Johnston, P. M. Mulembakani, N. Kisalu, M. S. Lee, G. Koroleva, S. E. McCarthy, M. C. Gestole, N. D. Wolfe, J. N. Fair, B. S. Schneider, L. L. Wright, J. Huggins, C. A. Whitehouse, E. O. Wemakoy, J. J. Muyembe-Tamfum, L. E. Hensley, G. F. Palacios and A. W. Rimoin (2014). “Genomic variability of monkeypox virus among humans, Democratic Republic of the Congo.” Emerg Infect Dis 20(2): 232-239.CrossRefPubMedPubMedCentral Kugelman, J. R., S. C. Johnston, P. M. Mulembakani, N. Kisalu, M. S. Lee, G. Koroleva, S. E. McCarthy, M. C. Gestole, N. D. Wolfe, J. N. Fair, B. S. Schneider, L. L. Wright, J. Huggins, C. A. Whitehouse, E. O. Wemakoy, J. J. Muyembe-Tamfum, L. E. Hensley, G. F. Palacios and A. W. Rimoin (2014). “Genomic variability of monkeypox virus among humans, Democratic Republic of the Congo.” Emerg Infect Dis 20(2): 232-239.CrossRefPubMedPubMedCentral
go back to reference Kulesh, D. A., R. O. Baker, B. M. Loveless, D. Norwood, S. H. Zwiers, E. Mucker, C. Hartmann, R. Herrera, D. Miller, D. Christensen, L. P. Wasieloski, Jr., J. Huggins and P. B. Jahrling (2004). “Smallpox and pan-orthopox virus detection by real-time 3’-minor groove binder TaqMan assays on the roche LightCycler and the Cepheid smart Cycler platforms.” J Clin Microbiol 42(2): 601-609.CrossRefPubMedPubMedCentral Kulesh, D. A., R. O. Baker, B. M. Loveless, D. Norwood, S. H. Zwiers, E. Mucker, C. Hartmann, R. Herrera, D. Miller, D. Christensen, L. P. Wasieloski, Jr., J. Huggins and P. B. Jahrling (2004). “Smallpox and pan-orthopox virus detection by real-time 3’-minor groove binder TaqMan assays on the roche LightCycler and the Cepheid smart Cycler platforms.” J Clin Microbiol 42(2): 601-609.CrossRefPubMedPubMedCentral
go back to reference Kulesh, D. A., B. M. Loveless, D. Norwood, J. Garrison, C. A. Whitehouse, C. Hartmann, E. Mucker, D. Miller, L. P. Wasieloski, Jr., J. Huggins, G. Huhn, L. L. Miser, C. Imig, M. Martinez, T. Larsen, C. A. Rossi and G. V. Ludwig (2004). “Monkeypox virus detection in rodents using real-time 3’-minor groove binder TaqMan assays on the Roche LightCycler.” Lab Invest 84(9): 1200-1208.CrossRefPubMed Kulesh, D. A., B. M. Loveless, D. Norwood, J. Garrison, C. A. Whitehouse, C. Hartmann, E. Mucker, D. Miller, L. P. Wasieloski, Jr., J. Huggins, G. Huhn, L. L. Miser, C. Imig, M. Martinez, T. Larsen, C. A. Rossi and G. V. Ludwig (2004). “Monkeypox virus detection in rodents using real-time 3’-minor groove binder TaqMan assays on the Roche LightCycler.” Lab Invest 84(9): 1200-1208.CrossRefPubMed
go back to reference MacNeil, A., M. G. Reynolds, D. S. Carroll, K. Karem, Z. Braden, R. Lash, A. Moundeli, J. V. Mombouli, A. O. Jumaan, D. S. Schmid, and I. K. Damon. 2009. ‘Monkeypox or varicella? Lessons from a rash outbreak investigation in the Republic of the Congo’, Am J Trop Med Hyg, 80: 503-7.PubMed MacNeil, A., M. G. Reynolds, D. S. Carroll, K. Karem, Z. Braden, R. Lash, A. Moundeli, J. V. Mombouli, A. O. Jumaan, D. S. Schmid, and I. K. Damon. 2009. ‘Monkeypox or varicella? Lessons from a rash outbreak investigation in the Republic of the Congo’, Am J Trop Med Hyg, 80: 503-7.PubMed
go back to reference MacNeil, Adam, Mary G. Reynolds, Zach Braden, Darin S. Carroll, Vanda Bostik, Kevin Karem, Scott K. Smith, Whitni Davidson, Yu Li, Amba Moundeli, Jean-Vivien Mombouli, Aisha O. Jumaan, D. Scott Schmid, Russell L. Regnery, and Inger K. Damon. 2009. ‘Transmission of Atypical Varicella-Zoster Virus Infections Involving Palm and Sole Manifestations in an Area with Monkeypox Endemicity’, Clinical Infectious Diseases, 48: E6-E8.CrossRefPubMed MacNeil, Adam, Mary G. Reynolds, Zach Braden, Darin S. Carroll, Vanda Bostik, Kevin Karem, Scott K. Smith, Whitni Davidson, Yu Li, Amba Moundeli, Jean-Vivien Mombouli, Aisha O. Jumaan, D. Scott Schmid, Russell L. Regnery, and Inger K. Damon. 2009. ‘Transmission of Atypical Varicella-Zoster Virus Infections Involving Palm and Sole Manifestations in an Area with Monkeypox Endemicity’, Clinical Infectious Diseases, 48: E6-E8.CrossRefPubMed
go back to reference Maretic, Z., and M. P. M. Cooray. 1963. ‘COMPARISONS BETWEEN CHICKENPOX IN A TROPICAL AND A EUROPEAN COUNTRY’, Journal of Tropical Medicine and Hygiene, 66.PubMed Maretic, Z., and M. P. M. Cooray. 1963. ‘COMPARISONS BETWEEN CHICKENPOX IN A TROPICAL AND A EUROPEAN COUNTRY’, Journal of Tropical Medicine and Hygiene, 66.PubMed
go back to reference Marin, Mona, Tureka L. Watson, Sandra S. Chaves, Rachel Civen, Barbara M. Watson, John X. Zhang, Dana Perella, Laurene Mascola, and Jane F. Seward. 2008. ‘Varicella among Adults: Data from an Active Surveillance Project, 1995–2005’, Journal of Infectious Diseases, 197: S94-S100.CrossRefPubMed Marin, Mona, Tureka L. Watson, Sandra S. Chaves, Rachel Civen, Barbara M. Watson, John X. Zhang, Dana Perella, Laurene Mascola, and Jane F. Seward. 2008. ‘Varicella among Adults: Data from an Active Surveillance Project, 1995–2005’, Journal of Infectious Diseases, 197: S94-S100.CrossRefPubMed
go back to reference Meyer, H., M. Perrichot, M. Stemmler, P. Emmerich, H. Schmitz, F. Varaine, R. Shungu, F. Tshioko, and P. Formenty. 2002. ‘Outbreaks of disease suspected of being due to human monkeypox virus infection in the Democratic Republic of Congo in 2001’, Journal of Clinical Microbiology, 40.CrossRefPubMedPubMedCentral Meyer, H., M. Perrichot, M. Stemmler, P. Emmerich, H. Schmitz, F. Varaine, R. Shungu, F. Tshioko, and P. Formenty. 2002. ‘Outbreaks of disease suspected of being due to human monkeypox virus infection in the Democratic Republic of Congo in 2001’, Journal of Clinical Microbiology, 40.CrossRefPubMedPubMedCentral
go back to reference Meyer, P. A., J. F. Seward, A. O. Jumaan, and M. Wharton. 2000. ‘Varicella mortality: Trends before vaccine licensure in the United States, 1970-1994’, Journal of Infectious Diseases, 182.CrossRefPubMed Meyer, P. A., J. F. Seward, A. O. Jumaan, and M. Wharton. 2000. ‘Varicella mortality: Trends before vaccine licensure in the United States, 1970-1994’, Journal of Infectious Diseases, 182.CrossRefPubMed
go back to reference MOH (2011) Guide Technique pour la surveillance integree de la maladie et riposte: SIMR. In: Maladie DdLC, editor, 2nd ed. Kinshasa, DRC MOH (2011) Guide Technique pour la surveillance integree de la maladie et riposte: SIMR. In: Maladie DdLC, editor, 2nd ed. Kinshasa, DRC
go back to reference National Center for Immunization and Respiratory Diseases (NCIRD), Division of Viral Disease (2014) Shingles (herpes zoster)—clinical overview, Centers for Disease Control and Prevention, Accessed May 19 2014 National Center for Immunization and Respiratory Diseases (NCIRD), Division of Viral Disease (2014) Shingles (herpes zoster)—clinical overview, Centers for Disease Control and Prevention, Accessed May 19 2014
go back to reference Pearl, Judea. 2009. Causality: models, reasoning, and inference (Cambridge University Press: Cambridge; New York).CrossRef Pearl, Judea. 2009. Causality: models, reasoning, and inference (Cambridge University Press: Cambridge; New York).CrossRef
go back to reference Preblud, S. R. 1981. ‘AGE-SPECIFIC RISKS OF VARICELLA COMPLICATIONS’, Pediatrics, 68: 14-17.PubMed Preblud, S. R. 1981. ‘AGE-SPECIFIC RISKS OF VARICELLA COMPLICATIONS’, Pediatrics, 68: 14-17.PubMed
go back to reference R Core Team. 2013. “R: A Language and Environment for Statistical Computing.” In. Vienna, Austria: R Foundation for Statistical Computing. R Core Team. 2013. “R: A Language and Environment for Statistical Computing.” In. Vienna, Austria: R Foundation for Statistical Computing.
go back to reference Rimoin, Anne W., Prime M. Mulembakani, Sara C. Johnston, James O. Lloyd-Smith, Neville K. Kisalu, Timothee L. Kinkela, Seth Blumberg, Henri A. Thomassen, Brian L. Pike, Joseph N. Fair, Nathan D. Wolfe, Robert L. Shongo, Barney S. Graham, Pierre Formenty, Emile Okitolonda, Lisa E. Hensley, Hermann Meyer, Linda L. Wright, and Jean-Jacques Muyembe. 2010. ‘Major increase in human monkeypox incidence 30 years after smallpox vaccination campaigns cease in the Democratic Republic of Congo’, Proceedings of the National Academy of Sciences of the United States of America, 107: 16262-67.CrossRefPubMedPubMedCentral Rimoin, Anne W., Prime M. Mulembakani, Sara C. Johnston, James O. Lloyd-Smith, Neville K. Kisalu, Timothee L. Kinkela, Seth Blumberg, Henri A. Thomassen, Brian L. Pike, Joseph N. Fair, Nathan D. Wolfe, Robert L. Shongo, Barney S. Graham, Pierre Formenty, Emile Okitolonda, Lisa E. Hensley, Hermann Meyer, Linda L. Wright, and Jean-Jacques Muyembe. 2010. ‘Major increase in human monkeypox incidence 30 years after smallpox vaccination campaigns cease in the Democratic Republic of Congo’, Proceedings of the National Academy of Sciences of the United States of America, 107: 16262-67.CrossRefPubMedPubMedCentral
go back to reference Rothman, Kenneth J., Sander Greenland, and Timothy L. Lash. 2008. Modern epidemiology (Wolters Kluwer Health/Lippincott Williams & Wilkins: Philadelphia). Rothman, Kenneth J., Sander Greenland, and Timothy L. Lash. 2008. Modern epidemiology (Wolters Kluwer Health/Lippincott Williams & Wilkins: Philadelphia).
go back to reference Shchelkunov, S. N., A. V. Totmenin, I. V. Babkin, P. F. Safronov, O. I. Ryazankina, N. A. Petrov, V. V. Gutorova, E. A. Uvarova, M. V. Mikheev, J. R. Sisler, J. J. Esposito, P. B. Jahrling, B. Moss, and L. S. Sandakhchiev. 2001. ‘Human monkeypox and smallpox viruses: genomic comparison’, Febs Letters, 509: 66-70.CrossRefPubMed Shchelkunov, S. N., A. V. Totmenin, I. V. Babkin, P. F. Safronov, O. I. Ryazankina, N. A. Petrov, V. V. Gutorova, E. A. Uvarova, M. V. Mikheev, J. R. Sisler, J. J. Esposito, P. B. Jahrling, B. Moss, and L. S. Sandakhchiev. 2001. ‘Human monkeypox and smallpox viruses: genomic comparison’, Febs Letters, 509: 66-70.CrossRefPubMed
go back to reference Snoep, Jaapjan D., Alfredo Morabia, Sonia Hernández-Díaz, Miguel A. Hernán, and Jan P. Vandenbroucke. 2014. ‘Commentary: A structural approach to Berkson’s fallacy and a guide to a history of opinions about it’, International Journal of Epidemiology, 43: 515-21.CrossRefPubMedPubMedCentral Snoep, Jaapjan D., Alfredo Morabia, Sonia Hernández-Díaz, Miguel A. Hernán, and Jan P. Vandenbroucke. 2014. ‘Commentary: A structural approach to Berkson’s fallacy and a guide to a history of opinions about it’, International Journal of Epidemiology, 43: 515-21.CrossRefPubMedPubMedCentral
go back to reference Talukder YS, G. Kafatos, A. P. De Moira, J. Aquilina, S. P. Parker, N. S. Crowcroft, D. W. G. Brown, and J. Breuer. 2007. ‘The seroepidemiology of varicella zoster virus among pregnant Bangladeshi and white British women in the London Borough of Tower Hamlets, UK’, Epidemiology and Infection, 135: 1344-53.CrossRefPubMedPubMedCentral Talukder YS, G. Kafatos, A. P. De Moira, J. Aquilina, S. P. Parker, N. S. Crowcroft, D. W. G. Brown, and J. Breuer. 2007. ‘The seroepidemiology of varicella zoster virus among pregnant Bangladeshi and white British women in the London Borough of Tower Hamlets, UK’, Epidemiology and Infection, 135: 1344-53.CrossRefPubMedPubMedCentral
Metadata
Title
Varicella Coinfection in Patients with Active Monkeypox in the Democratic Republic of the Congo
Authors
Nicole A. Hoff
Douglas S. Morier
Neville K. Kisalu
Sara C. Johnston
Reena H. Doshi
Lisa E. Hensley
Emile Okitolonda-Wemakoy
Jean Jacques Muyembe-Tamfum
James O. Lloyd-Smith
Anne W. Rimoin
Publication date
01-09-2017
Publisher
Springer US
Published in
EcoHealth / Issue 3/2017
Print ISSN: 1612-9202
Electronic ISSN: 1612-9210
DOI
https://doi.org/10.1007/s10393-017-1266-5

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