Plague Gives Surprises in the First Decade of the 21st Century in the United States and Worldwide

Thomas Butler Ross University School of Medicine, Portsmouth, Dominica, West Indies

Search for other papers by Thomas Butler in
Current site
Google Scholar
PubMed
Close
Restricted access

Plague is an ancient disease caused by the bacterium Yersinia pestis and transmitted by rodent flea bites that continues to surprise us with first-ever events. This review documents plague in human cases in the 1st decade of the 21st century and updates our knowledge of clinical manifestations, transmission during outbreaks, diagnostic testing, antimicrobial treatment, and vaccine development. In the United States, 57 persons were reported to have the disease, of which seven died. Worldwide, 21,725 persons were affected with 1,612 deaths, for a case-fatality rate of 7.4%. The Congo reported more cases than any other country, including two large outbreaks of pneumonic plague, surpassing Madagascar, which had the most cases in the previous decade. Two United States scientists suffered fatal accidental exposures: a wildlife biologist, who carried out an autopsy on a mountain lion in Arizona in 2007, and a geneticist with subclinical hemochromatosis in Chicago, who was handling an avirulent strain of Y. pestis in 2009. Antimicrobial drugs given early after the onset of symptoms prevented many deaths; those recommended for treatment and prophylaxis included gentamicin, doxycycline, and fluoroquinolones, although fluoroquinolones have not been adequately tested in humans. Fleas that do not have their guts blocked by clotted blood meals were shown to be better transmitters of plague than blocked fleas. Under development for protection against bioterrorist use, a subunit vaccine containing F1 and V antigens of Y. pestis was administered to human volunteers eliciting antibodies without any serious side effects. These events, although showing progress, suggest that plague will persist in rodent reservoirs mostly in African countries burdened by poverty and civil unrest, causing death when patients fail to receive prompt antimicrobial treatment.

Author Notes

* Address correspondence to Thomas Butler, Department of Microbiology and Immunology, Ross University School of Medicine, Portsmouth, Dominica, West Indies. E-mail: tbutler@rossmed.edu.dm

Author's address: Thomas Butler, Department of Microbiology and Immunology, Ross University School of Medicine, Portsmouth, Dominica, West Indies, E-mail: tbutler@rossmed.edu.dm.

  • 1.

    Stenseth NC, Atshabar BB, Begon M, Belmain SR, Bertherat E, Carniel E, Gage KL, Leirs H, Rahalison L, 2008. Plague: past, present, and future. PLoS Med 5: e3.

  • 2.

    Carniel E, 2003. Evolution of pathogenic Yersinia, some lights in the dark. Adv Exp Med Biol 529: 3–12.

  • 3.

    Bertherat E, Thullier P, Shako JC, England K, Kone M-L, Arntzen L, Tomaso H, Koyange L, Formenty P, Ekwanzala F, Crestani R, Ciglenecki I, Rahalison L, 2011. Lessons learned about pneumonic plague diagnosis from 2 outbreaks, Democratic Republic of the Congo. Emerg Infect Dis 17: 778–784.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Bertherat E, Lamine KM, Formenty P, Thullier P, Mondonge V, Mitifu A, Rahalison L, 2005. Epidemie de peste pulmonaire dans une camp minier de la Republique Du Congo: le réveil brutal d'un vieux fleau. Med Trop 65: 511–514.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Wang H, Cui Y, Wang Z, Wang X, Guo Z, Yan Y, Li C, Cui B, Xiao X, Yang Y, Qi Z, Wang G, Wei B, Yu S, He D, Chen H, Chen G, Song Y, Yang R, 2011. A dog-associated primary pneumonic plague in Qinghai Province, China. Clin Infect Dis 52: 185–190.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Bertherat E, Bekhoucha S, Chougrani S, Razik F, Duchemin JB, Houti L, Deharib L, Fayolle C, Makrerougrass B, Dali-Yahia R, Bellai L, Chaleb A, Tikhomirov E, Carniel E, 2007. Plague reappearance in Algeria after 50 years, 2003. Emerg Infect Dis 13: 1459–1462.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Bitam I, Ayyadurai S, Kernif T, Chetta M, Boulaghman N, Raoult D, Drancourt M, 2010. New rural focus of plague, Algeria. Emerg Infect Dis 16: 1639–1640.

  • 8.

    Cabanel N, Leclercq A, Chenal-Francisque V, Annajar B, Rajerison M, Bekkhoucha S, Bertherat E, Carniel E, 2013. Plague outbreak in Libya, 2009, unrelated to plague in Algeria. Emerg Infect Dis 19: 230–236.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Arbaji A, Kharabsheh S, Al-Azab S, Al-Kayed M, Amr ZS, Abu Baker M, Chu MC, 2005. A 12-case outbreak of pharyngeal plague following the consumption of camel meat in north-eastern Jordan. Ann Trop Med Parasitol 99: 789–793.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Leslie T, Whitehouse CA, Yingst S, Baldwin C, Kakar F, Mofleh J, Hami AS, Mustafa L, Omar F, Ayazi E, Rossi C, Noormal B, Ziar N, Kakar R, 2011. Outbreak of gastroenteritis caused by Yersinia pestis in Afghanistan. Epidemiol Infect 139: 728–735.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Wong D, Wild MA, Walburger MA, Higgins CL, Callahan M, Czarnecki LA, Lawaczeck EW, Levy CE, Patterson JG, Sunenshine R, Adem P, Paddock CD, Zaki SR, Petersen JM, Schriefer ME, Eisen RJ, Gage KL, Griffith KS, Weber IB, Spraker TR, Mead PS, 2009. Primary pneumonic plague contracted from a mountain lion carcass. Clin Infect Dis 49: e33–e38.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Anonymous, 2011. Fatal laboratory-acquired infection with an attenuated Yersinia pestis strain–Chicago, Illinois, 2009. Morb Mortal Wkly Rep 60: 201–205.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Chanteau S, Rahalison L, Ralafiarisoa L, Foulon J, Ratsitorhina M, Ratsifasoamanana L, Carniel E, Nato F, 2003. Development and testing of a rapid diagnostic test for bubonic and pneumonic plague. Lancet 361: 211–216.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Mwengee W, Butler T, Mgema S, Mhina G, Almasi Y, Bradley C, Formanik JB, Rochester CG, 2006. Treatment of plague with gentamicin or doxycycline in a randomized clinical trial in Tanzania. Clin Infect Dis 42: 614–621.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Dennis DT, Chow CC, 2004. Plague. Pediatr Infect Dis J 23: 69–72.

  • 16.

    Lazarus AA, Decker CF, 2004. Plague. Respir Care Clin 10: 83–98.

  • 17.

    Eisen RJ, Bearden SW, Wilder AP, Montenieri JA, Antolin MF, Gage KL, 2006. Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism explaining rapidly spreading plague epizootics. Proc Natl Acad Sci USA 103: 15380–15385.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Williamson ED, Flick-Smith HC, LeButt C, Rowland CA, Jones SM, Waters EL, Gwyther RJ, Miller J, Packer PJ, Irving M, 2005. Human immune response to a plague vaccine comprising recombinant F1 and V antigens. Infect Immun 73: 3598–3608.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Williamson ED, 2009. Plague. Vaccine 27: D56–D60.

  • 20.

    Cobbs CG, Chansolme DH, 2004. Plague. Dermatol Clin 22: 303–312.

  • 21.

    Comer JE, Sturdevant DE, Carmody AB, Virtaneva K, Gardner D, Long D, Rosenke R, Porcella SF, Hinnebusch BJ, 2010. Transcriptomic and innate immune response to Yersinia pestis in the lymph node during bubonic plague. Infect Immun 78: 5086–5098.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    DePaola W, Tang F, Kim I, Han M, Levin M, Ciletti N, Lin A, Anderson D, Schneewind O, Jabri B, 2008. Toll-like receptor 6 drives differentiation of tolerogenic dendritic cells and contributes to LcrV-mediated plague pathogenesis. Cell Host Microbe 4: 350–361.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Gould LH, Pape J, Ettestad P, Griffith KS, Mead PS, 2008. Dog-associated risk factors for human plague. Zoonoses Pub Hlth 55: 448–454.

  • 24.

    Margolis DA, Burns J, Reed SL, Ginsberg MM, O'Grady TC, Vinetz JM, 2008. Case report: septicemic plague in a community hospital in California. Am J Trop Med Hyg 78: 868–871.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Guarner J, Shieh W-J, Chu M, Perlman DC, Kool J, Gage KL, Ettestad P, Zaki SR, 2005. Persistent Yersinia pestis antigens in ischemic tissues of a patient with septicemic plague. Hum Pathol 36: 850–853.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Anonymous, 2010. Human plague: review of regional morbidity and mortality, 2004–2009. Wkly Epidemiol Rec 85: 40–45.

  • 27.

    Anonymous, 2009. Bubonic and pneumonic plague–Uganda, 2006. Morb Mortal Wkly Rep 58: 778–781.

  • 28.

    Anonymous, 2006. Plague, Democratic Republic of the Congo. Wkly Epidemiol Rec 81: 241–242.

  • 29.

    Anonymous, 2011. Two cases of human plague–Oregon, 2010. Morb Mortal Wkly Rep 60: 214.

  • 30.

    Neerinckx S, Bertherat E, Leirs H, 2010. Human plague occurrences in Africa: an overview from 1877 to 2008. Trans R Soc Trop Med Hyg 104: 97–103.

  • 31.

    Gage KL, Dennis DT, Orloski KA, Ettestad P, Brown TL, Reynolds PJ, Pape WJ, Fritz CL, Carter LG, Stein JD, 2000. Cases of cat-associated human plague in the western US, 1977–1998. Clin Infect Dis 30: 893–900.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Losada L, Varga JJ, Hostetler J, Radune D, Kim M, Durkin S, Schneewind O, Nierman WC, 2011. Genome sequencing and analysis of Yersinia pestis KIM D27, an avirulent strain exempt from select agent regulation. PLoS ONE 6: e19054.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Frank KM, Schneewind O, Shieh W-J, 2011. Investigation of a researcher's death due to septicemic plague. N Engl J Med 364: 2563–2564.

  • 34.

    Matsumura P, 2010. Remembering Malcolm J. Casadaban. J Bacteriol 192: 4261–4263.

  • 35.

    Quenee LE, Hermanas TM, Ciletti N, Louvei H, Miller NC, Elli D, Blaylock B, Mitchell A, Schroeder J, Krausz T, Kanabrocki J, Schneewind O, 2012. Hereditary hemochromatosis restores the virulence of plague vaccine strains. J Infect Dis 206: 1050–1058.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Anonymous, 2004. Human plague in 2002 and 2003. Wkly Epidemiol Rec 79: 301–306.

  • 37.

    Boothby E, Shako JC, Bertherat E, 2012. Can sputum collection practices for tuberculosis improve laboratory diagnosis of pneumonic plague in developing countries? Trop Med Int Health 17: 231–234.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Ayyadurai S, Flaudrops C, Raoult D, Drancourt M, 2010. Rapid identification and typing of Yersinia pestis and other Yersinia species by matrix-assisted laser desorption/ionization time-of-flight (MALDI-TOF) mass spectrometry. BMC Microbiol 10: 285.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Thomas RJ, Webber D, Collinge A, Stagg AJ, Bailey SC, Nunez A, Gates A, Jayasekera PN, Taylor RR, Eley S, Titball RW, 2009. Different pathologies but equal levels of responsiveness to the recombinant F1 and V antigen vaccine and ciprofloxacin in a murine model of plague caused by small- and large-particle aerosols. Infect Immun 77: 1315–1323.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Steward J, Lever MS, Russell P, Beedham RJ, Stagg AJ, Taylor RR, Brooks TJ, 2004. Efficacy of the latest fluoroquinolones against experimental Yersinia pestis. Int J Antimicrob Agents 24: 609–612.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Urich SK, Chalcraft L, Schriefer ME, Yockey BM, Petersen JM, 2012. Lack of antimicrobial resistance in Yersinia pestis isolates from 17 countries in the Americas, Africa, and Asia. Antimicrob Agents Chemother 56: 555–558.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Gage KL, Kosoy MY, 2005. Natural history of plague: perspectives from more than a century of research. Annu Rev Entomol 50: 505–528.

  • 43.

    Begon M, Klassovskiy N, Ageyev V, Suleimenov B, Atshabar B, Bennett M, 2006. Epizootologic parameters for plague in Kazakhstan. Emerg Infect Dis 12: 268–273.

  • 44.

    Duplantier J-M, Duchemin J-B, Chanteau S, Carniel E, 2005. From the recent lessons of the Malagasy foci towards a global understanding of the factors involved in plague reemergence. Vet Res 36: 437–453.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45.

    Drancourt M, Houhamdi L, Raoult D, 2006. Yersinia pestis as a telluric, human ectoparasite-borne organism. Lancet Infect Dis 6: 234–241.

  • 46.

    Ayyadurai S, Houhamdi L, Lepidi H, Nappez C, Raoult D, Drancourt M, 2008. Long-term persistence of virulent Yersinia pestis in soil. Microbiol 154: 2865–2871.

  • 47.

    Houhamdi L, Lepidi H, Drancourt M, Raoult D, 2006. Experimental model to evaluate the human body louse as a vector of plague. J Infect Dis 194: 1589–1596.

  • 48.

    Pujol C, Bliska JB, 2005. Turning Yersinia pathogenesis outside in: subversion of macrophage function by intracellular yersiniae. Clin Immunol 114: 216–226.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 49.

    Smiley ST, 2008. Current challenges in the development of vaccines for pneumonic plague. Expert Rev Vaccines 7: 209–221.

Past two years Past Year Past 30 Days
Abstract Views 2056 1408 45
Full Text Views 919 46 10
PDF Downloads 463 24 1
 

 

 

 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save