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

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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.

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References

  • Berkson, J. 1946. ‘LIMITATIONS OF THE APPLICATION OF FOURFOLD TABLE ANALYSIS TO HOSPITAL DATA’, Biometrics Bulletin, 2.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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).

    Google Scholar 

  • Fairley, C. K., and E. Miller. 1996. ‘Varicella-Zoster virus epidemiology - A changing scene?’, Journal of Infectious Diseases, 174.

    Article  PubMed  Google Scholar 

  • Feder, H. M., and D. M. Hoss. 2004. ‘Herpes zoster in otherwise healthy children’, Pediatric Infectious Disease Journal, 23: 451-57.

    Article  PubMed  Google Scholar 

  • Friendly M (2013) Working with categorical data with R and the vcd and vcdExtra packages

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Greenland, S., J. Pearl, and J. M. Robins. 1999. ‘Causal diagrams for epidemiologic research’, Epidemiology, 10: 37-48.

    Article  CAS  PubMed  Google Scholar 

  • Hastie, I. R. 1980. ‘VARICELLA-ZOSTER VIRUS AFFECTING IMMIGRANT NURSES’, Lancet, 2: 154-55.

    Article  CAS  PubMed  Google Scholar 

  • Hernan, M. A., and J. M. Robins. 2005. ‘A structural approach to observation bias’, American Journal of Epidemiology, 161: S100-S00.

    Article  Google Scholar 

  • Hernán MA, Robins JM (2017) Causal inference: Part I: Causal inference without models, Boca Raton: Chapman & Hall/CRC, p 131 (forthcoming)

  • 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.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Jezek, Z., L. N. Khodakevich, and M. Szczeniowski. 1988. ‘HUMAN MONKEYPOX - CLINICAL AND EPIDEMIOLOGICAL FEATURES’, Zhurnal Mikrobiologii Epidemiologii I Immunobiologii: 23-30.

    Google Scholar 

  • Jezek, Z., M. Szczeniowski, K. M. Paluku, M. Mutombo, and B. Grab. 1988. ‘HUMAN MONKEYPOX - CONFUSION WITH CHICKENPOX’, Acta Tropica, 45: 297-307.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • MOH (2011) Guide Technique pour la surveillance integree de la maladie et riposte: SIMR. In: Maladie DdLC, editor, 2nd ed. Kinshasa, DRC

  • 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

  • Pearl, Judea. 2009. Causality: models, reasoning, and inference (Cambridge University Press: Cambridge; New York).

    Book  Google Scholar 

  • Preblud, S. R. 1981. ‘AGE-SPECIFIC RISKS OF VARICELLA COMPLICATIONS’, Pediatrics, 68: 14-17.

    CAS  PubMed  Google Scholar 

  • R Core Team. 2013. “R: A Language and Environment for Statistical Computing.” In. Vienna, Austria: R Foundation for Statistical Computing.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rothman, Kenneth J., Sander Greenland, and Timothy L. Lash. 2008. Modern epidemiology (Wolters Kluwer Health/Lippincott Williams & Wilkins: Philadelphia).

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

A previous version of this article appeared as a chapter in Dr. Morier’s dissertation for the UCLA Department of Epidemiology. He would like to gratefully acknowledge the members of his doctoral committee for their contributions. Thanks to Monique Ambrose of the Lloyd-Smith lab group for her suggestions of probabilistic analyses.

Funding

This work was supported by the Faucett Catalyst Fund.

Author information

Authors and Affiliations

  1. UCLA Fielding School of Public Health, 41-275 CHS, 650 Charles E. Young Dr. South, Los Angeles, CA, 90095, USA

    Nicole A. Hoff, Douglas S. Morier, Reena H. Doshi, James O. Lloyd-Smith & Anne W. Rimoin

  2. National Institute of Allergy and Infectious Diseases, Bethesda, MD, USA

    Neville K. Kisalu & Lisa E. Hensley

  3. Vaccine Research Center, National Institute of Allergy and Infectious Diseases, Bethesda, MD, USA

    Sara C. Johnston

  4. United States Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, MD, USA

    Sara C. Johnston

  5. Kinshasa School of Public Health, Kinshasa, Democratic Republic of the Congo

    Emile Okitolonda-Wemakoy

  6. Institut National de Recherche Biomedicale, Kinshasa, Democratic Republic of the Congo

    Jean Jacques Muyembe-Tamfum

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  1. Nicole A. Hoff
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  2. Douglas S. Morier
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  9. James O. Lloyd-Smith
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Corresponding authors

Correspondence to Nicole A. Hoff or Anne W. Rimoin.

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Conflict of interest

The authors declare they have no conflicts.

Ethical approval

This study was reviewed and approved by the Ethics Committee of the Kinshasa School of Public Health, Kinshasa, DRC, and by the Institutional Review Board of Human Research Ethics at the University of California, Los Angeles.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Douglas S. Morier and Nicole A. Hoff are considered co-first authors for this manuscript.

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Hoff, N.A., Morier, D.S., Kisalu, N.K. et al. Varicella Coinfection in Patients with Active Monkeypox in the Democratic Republic of the Congo. EcoHealth 14, 564–574 (2017). https://doi.org/10.1007/s10393-017-1266-5

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  • DOI: https://doi.org/10.1007/s10393-017-1266-5

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