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#redirect[[Yersinia pestis infection causes]]
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{{Yersinia pestis infection}}
 
{{About0|Yersinia pestis infection}}
 
{{CMG}}; {{AE}} Esther Lee, M.A.; {{Rim}}; {{JS}}
 
==Overview==
''[[Yersinia pestis]]'' (''[[Y. pestis]]''), a rod-shaped [[facultative anaerobe]] with bipolar staining (giving it a safety pin appearance) causes the [[infection]] in mammals and humans.<ref name=Baron>{{cite book | author = Collins FM | title = Pasteurella, Yersinia, and Francisella. ''In:'' Baron's Medical Microbiology ''(Baron S ''et al'', eds.)| edition = 4th | publisher = Univ. of Texas Medical Branch | year = 1996 | url = http://www.ncbi.nlm.nih.gov/books/bv.fcgi?rid=mmed.section.1611 | isbn = 0-9631172-1-1 }}</ref>  The [[bacteria]] maintain their existence in a cycle involving rodents and their fleas.  The genus [[Yersinia]] is [[gram-negative]], bipolar staining coccobacilli, and, similarly to other [[Enterobacteriaceae]], it has a fermentative [[metabolism]]. ''Y. pestis'' produces an [[antiphagocytic]] slime. The organism is [[motile]] when isolated, but becomes nonmotile in the mammalian host.
 
==Taxonomy==
[[Bacteria]]; [[Proteobacteria]]; [[Proteobacteria#Gammaproteobacteria|Gammaproteobacteria]]; [[Enterobacteriales]]; ''[[Yersinia]]''; [[Yersinia pestis]]
 
==Biology==
{| style="float: right;"
| [[File:Yersinia pestis fluorescent.jpeg|200px|thumb|none|Yersinia pestis, Direct Fluorescent Antibody Stain (DFA), 200x Magnification <SMALL>Courtesy: ''[http://phil.cdc.gov/phil/home.asp Public Health Image Library (PHIL), Centers for Disease Control and Prevention (CDC)]''<ref>{{Cite web | title = http://phil.cdc.gov/phil/details.asp | url = http://phil.cdc.gov/phil/details.asp}}</ref></SMALL>]]
|-
| [[File:Yersinia2.jpg|200px|thumb|none|Photomicrograph of Yersinia (Pasteurella) pestis, sometimes referred to as Bacillus pestis. <SMALL>Courtesy: ''[http://phil.cdc.gov/phil/home.asp Public Health Image Library (PHIL), Centers for Disease Control and Prevention (CDC)]''<ref>{{Cite web | title = http://phil.cdc.gov/phil/details.asp | url = http://phil.cdc.gov/phil/details.asp}}</ref></SMALL>]]
|}
[[Yersinia pestis]] is a [[motility|nonmotile]], non-[[spore]]-forming, [[Gram-negative]], non-[[lactose]] fermenting, ovoid and "safety-pin-shaped" (bipolar appearance when stained) [[bacillus]].  It is an [[enterobacteriaceae]] commonly measuring 0.75x1.5 μm. On [[cell culture]]s, it grows on sheep-blood agar, as grayish translucent colonies. It also grows on MacConkey and [[nutrient]]-rich broths.<ref name="Koirala2006">{{cite journal|last1=Koirala|first1=Janak|title=Plague: Disease, Management, and Recognition of Act of Terrorism|journal=Infectious Disease Clinics of North America|volume=20|issue=2|year=2006|pages=273–287|issn=08915520|doi=10.1016/j.idc.2006.02.004}}</ref>
 
[[Yersinia pestis]] only survives for a few hours on physical surfaces, being very sensitive to high temperatures, sunlight and disinfectants.<ref name="Koirala2006">{{cite journal|last1=Koirala|first1=Janak|title=Plague: Disease, Management, and Recognition of Act of Terrorism|journal=Infectious Disease Clinics of North America|volume=20|issue=2|year=2006|pages=273–287|issn=08915520|doi=10.1016/j.idc.2006.02.004}}</ref><ref name="pmid8993858">{{cite journal| author=Perry RD, Fetherston JD| title=Yersinia pestis--etiologic agent of plague. | journal=Clin Microbiol Rev | year= 1997 | volume= 10 | issue= 1 | pages= 35-66 | pmid=8993858 | doi= | pmc=PMC172914 | url=http://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=8993858  }} </ref><ref name="pmid10852811">{{cite journal| author=Gage KL, Dennis DT, Orloski KA, Ettestad P, Brown TL, Reynolds PJ et al.| title=Cases of cat-associated human plague in the Western US, 1977-1998. | journal=Clin Infect Dis | year= 2000 | volume= 30 | issue= 6 | pages= 893-900 | pmid=10852811 | doi=10.1086/313804 | pmc= | url=http://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=10852811  }} </ref>
 
[[Yersinia pestis]] is thought to have evolved from [[Yersinia pseudotuberculosis]] about 1500 - 2000 years ago. According to its behavior towards [[nitrate]] and [[glycerol]], [[Yersinia pestis]] may be classified as:<ref name="Koirala2006">{{cite journal|last1=Koirala|first1=Janak|title=Plague: Disease, Management, and Recognition of Act of Terrorism|journal=Infectious Disease Clinics of North America|volume=20|issue=2|year=2006|pages=273–287|issn=08915520|doi=10.1016/j.idc.2006.02.004}}</ref>
* ''Biovar Antiqua''
:* Nitrate reduction: positive
:* Glycerol reduction: positive
 
* ''Biovar Medievalis''
:* Nitrate reduction: negative
:* Glycerol use: positive
 
* ''Biovar Orientalis''
:* Nitrate reduction: positive
:* Glycerol use: negative
 
===Genome===
The complete [[genome|genomic]] sequence is available for two of the three sub-species of [[yersinia pestis]]:
* Strain KIM - Biovar Medievalis<ref>{{cite journal | author = Deng W| title = Genome Sequence of Yersinia pestis KIM | journal = Journal of Bacteriology | year = 2002 | volume = 184 | issue = 16 | pages = 4601&ndash;4611 | doi= 10.1128/JB.184.16.4601-4611.2002 | pmid=12142430 | pmc = 135232 | author-separator = , | display-authors = 1 | last2 = Burland | first2 = V. | last3 = Plunkett Iii | first3 = G. | last4 = Boutin | first4 = A. | last5 = Mayhew | first5 = G. F. | last6 = Liss | first6 = P. | last7 = Perna | first7 = N. T. | last8 = Rose | first8 = D. J. | last9 = Mau | first9 = B.}}</ref>
* Strain CO92 - Biovar Orientalis<ref>{{cite journal | author = Parkhill J| title = Genome sequence of Yersinia pestis, the causative agent of plague | journal = Nature | year = 2001 | volume = 413 | issue = 6855| pages = 523&ndash;527 | doi = 10.1038/35097083 | pmid = 11586360 | author-separator = , | display-authors = 1 | last2 = Wren | first2 = B. W. | last3 = Thomson | first3 = N. R. | last4 = Titball | first4 = R. W. | last5 = Holden | first5 = M. T. G. | last6 = Prentice | first6 = M. B. | last7 = Sebaihia | first7 = M. | last8 = James | first8 = K. D. | last9 = Churcher | first9 = C.}}</ref>
 
As of 2006, the [[genomic sequence]] of a [[strain]] of ''biovar Antiqua'' has been completed.<ref name="pmid16740952">{{cite journal |author=Chain PS |title=Complete Genome Sequence of Yersinia pestis Strains Antiqua and Nepal516: Evidence of Gene Reduction in an Emerging Pathogen |journal=J. Bacteriol. |volume=188 |issue=12 |pages=4453–63 |year=2006 |pmid=16740952 |doi=10.1128/JB.00124-06 |pmc=1482938 |author-separator=, |author2=Hu P |author3=Malfatti SA |display-authors=3 |last4=Radnedge |first4=L. |last5=Larimer |first5=F. |last6=Vergez |first6=L. M. |last7=Worsham |first7=P. |last8=Chu |first8=M. C. |last9=Andersen |first9=G. L.}}</ref> Similar to the other [[pathogenic]] [[strains]], there are signs of mutations causing loss of function. The [[chromosome]] of strain KIM is 4,600,755 base pairs long; the [[chromosome]] of strain CO92 is 4,653,728 base pairs long.
 
Similarly to other [[enterobacteriaceae]] ([[Yersinia pseudotuberculosis|Yersinia pseudotuberculosis]] and [[Yersinia enterocolitica|Yersinia enterocolitica]]), [[Yersinia pestis]] is host to the ''[[plasmid]] pCD1''.  In addition, it also hosts two other [[plasmids]], ''pPCP1'' (also called pPla or pPst) and ''pMT1'' (also called pFra) that are not carried by the other Yersinia species.
* pFra codes for a [[phospholipase D]] that is important for the ability of [[Yersinia pestis]] to be transmitted by fleas.
* pPla codes for a [[protease]], Pla, that activates [[plasminogen]] in human hosts and is a very important [[virulence factor]] for pneumonic plague.<ref name="pmid17255510">{{cite journal| author=Lathem WW, Price PA, Miller VL, Goldman WE| title=A plasminogen-activating protease specifically controls the development of primary pneumonic plague. | journal=Science | year= 2007 | volume= 315 | issue= 5811 | pages= 509-13 | pmid=17255510 | doi=10.1126/science.1137195 | pmc= | url=http://www.ncbi.nlm.nih.gov/entrez/eutils/elink.fcgi?dbfrom=pubmed&tool=sumsearch.org/cite&retmode=ref&cmd=prlinks&id=17255510  }} </ref>
 
Together, these [[plasmids]], and a [[pathogenicity island]] called HPI, encode several [[pathogenic]] [[proteins]], characteristic of [[Yersinia pestis]]. Among other things, these [[virulence factors]] are required of:
* [[Bacterial]] adhesion
* Injection of [[proteins]] into the host cell
* Invasion of the host cell (via a Type III secretion system)
* Acquisition and binding of [[iron]] from [[red blood cell]], via siderophores
 
A comprehensive and comparative [[proteomics]] analysis of [[Yersinia pestis]] strain KIM was performed in 2006.<ref>{{cite journal | author = Hixson K| title = Biomarker candidate identification in Yersinia pestis using organism-wide semiquantitative proteomics | journal = Journal of Proteome Research | year = 2006 | volume = 5 | issue = 11 | pages = 3008–3017 | pmid = 16684765  | doi = 10.1021/pr060179y | author-separator = , | display-authors = 1 | last2 = Adkins | first2 = Joshua N. | last3 = Baker | first3 = Scott E. | last4 = Moore | first4 = Ronald J. | last5 = Chromy | first5 = Brett A. | last6 = Smith | first6 = Richard D. | last7 = McCutchen-Maloney | first7 = Sandra L. | last8 = Lipton | first8 = Mary S. | last9 = Heffron | first9 = F}}</ref> The analysis focused on the transition to a growth condition mimicking growth in host cells.
 
==Tropism==
[[Yersinia pestis]] shows [[tropism]] for [[lymphoid tissue]].
 
==Natural Reservoir==
Plague is primarily a disease of rodents. The [[infection]] is maintained in natural foci of the disease in wild rodent colonies, through [[transmission]] between rodents, by their flea ectoparasites.<ref name=CDC>{{cite web | title = Plague | url = http://www.cdc.gov/plague/healthcare/clinicians.html }}</ref>
 
 
==Gallery==
<gallery>
Image: Enterobacteria34.jpeg| Gram-negative Yersinia pestis bacteria, which was grown on a medium of sheep’s blood agar (SBA) 72hrs. <SMALL><SMALL>''[http://phil.cdc.gov/phil/home.asp From Public Health Image Library (PHIL).] ''<ref name=PHIL> {{Cite web | title = Public Health Image Library (PHIL) | url = http://phil.cdc.gov/phil/home.asp}}</ref></SMALL></SMALL>
Image: Enterobacteria31.png| Ulcerated skin lesion at a plague inoculation site caused by the Gram-negative bacterium, Yersinia pestis. <SMALL><SMALL>''[http://phil.cdc.gov/phil/home.asp From Public Health Image Library (PHIL).] ''<ref name=PHIL> {{Cite web | title = Public Health Image Library (PHIL) | url = http://phil.cdc.gov/phil/home.asp}}</ref></SMALL></SMALL>
Image: Enterobacteria29.jpeg| Blood smear reveals presence of Gram-negative Yersinia pestis plague bacteria. <SMALL><SMALL>''[http://phil.cdc.gov/phil/home.asp From Public Health Image Library (PHIL).] ''<ref name=PHIL> {{Cite web | title = Public Health Image Library (PHIL) | url = http://phil.cdc.gov/phil/home.asp}}</ref></SMALL></SMALL>
Image: Enterobacteria22.jpeg| Gram-negative Yersinia pestis bacteria, which were cultured on a sheep blood agar (SBA) medium 120 hrs (20x mag). <SMALL><SMALL>''[http://phil.cdc.gov/phil/home.asp From Public Health Image Library (PHIL).] ''<ref name=PHIL> {{Cite web | title = Public Health Image Library (PHIL) | url = http://phil.cdc.gov/phil/home.asp}}</ref></SMALL></SMALL>
Image: Enterobacteria21.jpeg| Gram-negative Yersinia pestis bacteria, which were cultured on a sheep blood agar (SBA) medium 120 hrs (20x mag). <SMALL><SMALL>''[http://phil.cdc.gov/phil/home.asp From Public Health Image Library (PHIL).] ''<ref name=PHIL> {{Cite web | title = Public Health Image Library (PHIL) | url = http://phil.cdc.gov/phil/home.asp}}</ref></SMALL></SMALL>
Image: Enterobacteria20.jpeg| Gram-negative Yersinia pestis bacteria, which were cultured on a sheep blood agar (SBA) medium 24 hrs (10x mag). <SMALL><SMALL>''[http://phil.cdc.gov/phil/home.asp From Public Health Image Library (PHIL).] ''<ref name=PHIL> {{Cite web | title = Public Health Image Library (PHIL) | url = http://phil.cdc.gov/phil/home.asp}}</ref></SMALL></SMALL>
Image: Enterobacteria19.jpeg| Gram-negative Yersinia pestis bacteria, which were cultured on a sheep blood agar (SBA) medium 72 hrs (10x mag). <SMALL><SMALL>''[http://phil.cdc.gov/phil/home.asp From Public Health Image Library (PHIL).] ''<ref name=PHIL> {{Cite web | title = Public Health Image Library (PHIL) | url = http://phil.cdc.gov/phil/home.asp}}</ref></SMALL></SMALL>
Image: Bubonic plague16.jpeg| Hematoxylin-eosin stained (H&E) photomicrograph reveals  histopathologic changes in a lymph node tissue sample in a case of fatal human plague. <SMALL><SMALL>''[http://phil.cdc.gov/phil/home.asp From Public Health Image Library (PHIL).] ''<ref name=PHIL> {{Cite web | title = Public Health Image Library (PHIL) | url = http://phil.cdc.gov/phil/home.asp}}</ref></SMALL></SMALL>
Image: Bubonic plague05.jpeg| Hematoxylin-eosin stained lung tissue sample revealed the histopathologic changes indicative of what was diagnosed as a case of fatal human plague from the country of Nepal (125x mag). <SMALL><SMALL>''[http://phil.cdc.gov/phil/home.asp From Public Health Image Library (PHIL).] ''<ref name=PHIL> {{Cite web | title = Public Health Image Library (PHIL) | url = http://phil.cdc.gov/phil/home.asp}}</ref></SMALL></SMALL>
Image: Bubonic plague15.jpeg| Chest x-ray of a plague patient revealing bilateral infection, greater on the patient's left side, which was diagnosed as a case of pneumonic plague, caused by Yersinia pestis. <SMALL><SMALL>''[http://phil.cdc.gov/phil/home.asp From Public Health Image Library (PHIL).] ''<ref name=PHIL> {{Cite web | title = Public Health Image Library (PHIL) | url = http://phil.cdc.gov/phil/home.asp}}</ref></SMALL></SMALL>
Image: Bubonic plague14.jpeg| Fingertips of patient’s right hand exhibited the signs of what is known as acral gangrene caused by the bacterium, Yersinia pestis. <SMALL><SMALL>''[http://phil.cdc.gov/phil/home.asp From Public Health Image Library (PHIL).] ''<ref name=PHIL> {{Cite web | title = Public Health Image Library (PHIL) | url = http://phil.cdc.gov/phil/home.asp}}</ref></SMALL></SMALL>
Image: Bubonic plague12.jpeg| Patient acquired a plague infection through abrasions on his upper right leg. <SMALL><SMALL>''[http://phil.cdc.gov/phil/home.asp From Public Health Image Library (PHIL).] ''<ref name=PHIL> {{Cite web | title = Public Health Image Library (PHIL) | url = http://phil.cdc.gov/phil/home.asp}}</ref></SMALL></SMALL>
Image: Bubonic plague04.jpeg| Lung tissue sample revealed the histopathologic changes indicative of fatal human plague (125x mag). <SMALL><SMALL>''[http://phil.cdc.gov/phil/home.asp From Public Health Image Library (PHIL).] ''<ref name=PHIL> {{Cite web | title = Public Health Image Library (PHIL) | url = http://phil.cdc.gov/phil/home.asp}}</ref></SMALL></SMALL>
</SMALL>
Image: Bubonic plague01.jpeg| Purple-colored Yersinia pestis bacteria on the proventricular spines of a Xenopsylla cheopis flea. <SMALL><SMALL>''[http://phil.cdc.gov/phil/home.asp From Public Health Image Library (PHIL).] ''<ref name=PHIL> {{Cite web | title = Public Health Image Library (PHIL) | url = http://phil.cdc.gov/phil/home.asp}}</ref></SMALL>
</gallery>
 
==References==
 
{{Reflist|2}}
 
[[Category:Dermatology]]
[[Category:Pulmonology]]
[[Category:Hematology]]
[[Category:Disease]]
[[Category:Needs content]]
[[Category:Infectious disease]]
[[Category:Emergency medicine]]
[[Category:Medicine]]

Latest revision as of 00:45, 30 July 2020

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This page is about microbiologic aspects of the organism(s).  For clinical aspects of the disease, see Yersinia pestis infection.

Editor-In-Chief: C. Michael Gibson, M.S., M.D. [1]; Associate Editor(s)-in-Chief: Esther Lee, M.A.; Rim Halaby, M.D. [2]; João André Alves Silva, M.D. [3]

Overview

Yersinia pestis (Y. pestis), a rod-shaped facultative anaerobe with bipolar staining (giving it a safety pin appearance) causes the infection in mammals and humans.[1] The bacteria maintain their existence in a cycle involving rodents and their fleas. The genus Yersinia is gram-negative, bipolar staining coccobacilli, and, similarly to other Enterobacteriaceae, it has a fermentative metabolism. Y. pestis produces an antiphagocytic slime. The organism is motile when isolated, but becomes nonmotile in the mammalian host.

Taxonomy

Bacteria; Proteobacteria; Gammaproteobacteria; Enterobacteriales; Yersinia; Yersinia pestis

Biology

Yersinia pestis, Direct Fluorescent Antibody Stain (DFA), 200x Magnification Courtesy: Public Health Image Library (PHIL), Centers for Disease Control and Prevention (CDC)[2]
Photomicrograph of Yersinia (Pasteurella) pestis, sometimes referred to as Bacillus pestis. Courtesy: Public Health Image Library (PHIL), Centers for Disease Control and Prevention (CDC)[3]

Yersinia pestis is a nonmotile, non-spore-forming, Gram-negative, non-lactose fermenting, ovoid and "safety-pin-shaped" (bipolar appearance when stained) bacillus. It is an enterobacteriaceae commonly measuring 0.75x1.5 μm. On cell cultures, it grows on sheep-blood agar, as grayish translucent colonies. It also grows on MacConkey and nutrient-rich broths.[4]

Yersinia pestis only survives for a few hours on physical surfaces, being very sensitive to high temperatures, sunlight and disinfectants.[4][5][6]

Yersinia pestis is thought to have evolved from Yersinia pseudotuberculosis about 1500 - 2000 years ago. According to its behavior towards nitrate and glycerol, Yersinia pestis may be classified as:[4]

  • Biovar Antiqua
  • Nitrate reduction: positive
  • Glycerol reduction: positive
  • Biovar Medievalis
  • Nitrate reduction: negative
  • Glycerol use: positive
  • Biovar Orientalis
  • Nitrate reduction: positive
  • Glycerol use: negative

Genome

The complete genomic sequence is available for two of the three sub-species of yersinia pestis:

  • Strain KIM - Biovar Medievalis[7]
  • Strain CO92 - Biovar Orientalis[8]

As of 2006, the genomic sequence of a strain of biovar Antiqua has been completed.[9] Similar to the other pathogenic strains, there are signs of mutations causing loss of function. The chromosome of strain KIM is 4,600,755 base pairs long; the chromosome of strain CO92 is 4,653,728 base pairs long.

Similarly to other enterobacteriaceae (Yersinia pseudotuberculosis and Yersinia enterocolitica), Yersinia pestis is host to the plasmid pCD1. In addition, it also hosts two other plasmids, pPCP1 (also called pPla or pPst) and pMT1 (also called pFra) that are not carried by the other Yersinia species.

Together, these plasmids, and a pathogenicity island called HPI, encode several pathogenic proteins, characteristic of Yersinia pestis. Among other things, these virulence factors are required of:

  • Bacterial adhesion
  • Injection of proteins into the host cell
  • Invasion of the host cell (via a Type III secretion system)
  • Acquisition and binding of iron from red blood cell, via siderophores

A comprehensive and comparative proteomics analysis of Yersinia pestis strain KIM was performed in 2006.[11] The analysis focused on the transition to a growth condition mimicking growth in host cells.

Tropism

Yersinia pestis shows tropism for lymphoid tissue.

Natural Reservoir

Plague is primarily a disease of rodents. The infection is maintained in natural foci of the disease in wild rodent colonies, through transmission between rodents, by their flea ectoparasites.[12]


Gallery

References

  1. ↑ Collins FM (1996). Pasteurella, Yersinia, and Francisella. In: Baron's Medical Microbiology (Baron S et al, eds.) (4th ed.). Univ. of Texas Medical Branch. ISBN 0-9631172-1-1.
  2. ↑ "http://phil.cdc.gov/phil/details.asp". External link in |title= (help)
  3. ↑ "http://phil.cdc.gov/phil/details.asp". External link in |title= (help)
  4. ↑ 4.0 4.1 4.2 Koirala, Janak (2006). "Plague: Disease, Management, and Recognition of Act of Terrorism". Infectious Disease Clinics of North America. 20 (2): 273–287. doi:10.1016/j.idc.2006.02.004. ISSN 0891-5520.
  5. ↑ Perry RD, Fetherston JD (1997). "Yersinia pestis--etiologic agent of plague". Clin Microbiol Rev. 10 (1): 35–66. PMC 172914. PMID 8993858.
  6. ↑ Gage KL, Dennis DT, Orloski KA, Ettestad P, Brown TL, Reynolds PJ; et al. (2000). "Cases of cat-associated human plague in the Western US, 1977-1998". Clin Infect Dis. 30 (6): 893–900. doi:10.1086/313804. PMID 10852811.
  7. ↑ Deng W; et al. (2002). "Genome Sequence of Yersinia pestis KIM". Journal of Bacteriology. 184 (16): 4601&ndash, 4611. doi:10.1128/JB.184.16.4601-4611.2002. PMC 135232. PMID 12142430. Unknown parameter |author-separator= ignored (help)
  8. ↑ Parkhill J; et al. (2001). "Genome sequence of Yersinia pestis, the causative agent of plague". Nature. 413 (6855): 523&ndash, 527. doi:10.1038/35097083. PMID 11586360. Unknown parameter |author-separator= ignored (help)
  9. ↑ Chain PS; Hu P; Malfatti SA; et al. (2006). "Complete Genome Sequence of Yersinia pestis Strains Antiqua and Nepal516: Evidence of Gene Reduction in an Emerging Pathogen". J. Bacteriol. 188 (12): 4453–63. doi:10.1128/JB.00124-06. PMC 1482938. PMID 16740952. Unknown parameter |author-separator= ignored (help)
  10. ↑ Lathem WW, Price PA, Miller VL, Goldman WE (2007). "A plasminogen-activating protease specifically controls the development of primary pneumonic plague". Science. 315 (5811): 509–13. doi:10.1126/science.1137195. PMID 17255510.
  11. ↑ Hixson K; et al. (2006). "Biomarker candidate identification in Yersinia pestis using organism-wide semiquantitative proteomics". Journal of Proteome Research. 5 (11): 3008–3017. doi:10.1021/pr060179y. PMID 16684765. Unknown parameter |author-separator= ignored (help)
  12. ↑ "Plague".
  13. ↑ 13.00 13.01 13.02 13.03 13.04 13.05 13.06 13.07 13.08 13.09 13.10 13.11 13.12 13.13 "Public Health Image Library (PHIL)".
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