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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">An animal model that reflects human disease: the common marmoset (<italic>Callithrix jacchus</italic>)</title><author><name sortKey="Carrion, Ricardo" sort="Carrion, Ricardo" uniqKey="Carrion R" first="Ricardo" last="Carrion">Ricardo Carrion</name><affiliation><nlm:aff id="aff0005">Department of Virology and Immunology, Texas Biomedical Research Institute, San Antonio, TX 78227, USA</nlm:aff></affiliation><affiliation><nlm:aff id="aff0010">Southwest National Primate Research Center, Texas Biomedical Research Institute, San Antonio, TX 78227, USA</nlm:aff></affiliation></author><author><name sortKey="Patterson, Jean L" sort="Patterson, Jean L" uniqKey="Patterson J" first="Jean L" last="Patterson">Jean L. Patterson</name><affiliation><nlm:aff id="aff0005">Department of Virology and Immunology, Texas Biomedical Research Institute, San Antonio, TX 78227, USA</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">22709521</idno><idno type="pmc">3378983</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3378983</idno><idno type="RBID">PMC:3378983</idno><idno type="doi">10.1016/j.coviro.2012.02.007</idno><date when="2012">2012</date><idno type="wicri:Area/Pmc/Corpus">001733</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001733</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">An animal model that reflects human disease: the common marmoset (<italic>Callithrix jacchus</italic>)</title><author><name sortKey="Carrion, Ricardo" sort="Carrion, Ricardo" uniqKey="Carrion R" first="Ricardo" last="Carrion">Ricardo Carrion</name><affiliation><nlm:aff id="aff0005">Department of Virology and Immunology, Texas Biomedical Research Institute, San Antonio, TX 78227, USA</nlm:aff></affiliation><affiliation><nlm:aff id="aff0010">Southwest National Primate Research Center, Texas Biomedical Research Institute, San Antonio, TX 78227, USA</nlm:aff></affiliation></author><author><name sortKey="Patterson, Jean L" sort="Patterson, Jean L" uniqKey="Patterson J" first="Jean L" last="Patterson">Jean L. Patterson</name><affiliation><nlm:aff id="aff0005">Department of Virology and Immunology, Texas Biomedical Research Institute, San Antonio, TX 78227, USA</nlm:aff></affiliation></author></analytic><series><title level="j">Current Opinion in Virology</title><idno type="ISSN">1879-6257</idno><idno type="eISSN">1879-6265</idno><imprint><date when="2012">2012</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Highlights</title><p>► The common marmoset is a new world primate weighing between 350 and 400 g. ► Marmosets are exquisite NHP models for viral, protozoan, bacterial agents as well as prions. ► Marmosets have emerged as a viable model for studying high biocontainment pathogens. ► Models have been described for Ebola, Marburg, Lassa, SARS-CoA and EEE viruses. ► Use of marmosets will accelerate development of countermeasures to high consequence pathogens.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Abbott, D H" uniqKey="Abbott D">D.H. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Curr Opin Virol</journal-id><journal-id journal-id-type="iso-abbrev">Curr Opin Virol</journal-id><journal-title-group><journal-title>Current Opinion in Virology</journal-title></journal-title-group><issn pub-type="ppub">1879-6257</issn><issn pub-type="epub">1879-6265</issn><publisher><publisher-name>Elsevier</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">22709521</article-id><article-id pub-id-type="pmc">3378983</article-id><article-id pub-id-type="publisher-id">S1879-6257(12)00034-X</article-id><article-id pub-id-type="doi">10.1016/j.coviro.2012.02.007</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>An animal model that reflects human disease: the common marmoset (<italic>Callithrix jacchus</italic>)</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Carrion</surname><given-names>Ricardo</given-names><suffix>Jr</suffix></name><xref rid="aff0005" ref-type="aff">1</xref><xref rid="aff0010" ref-type="aff">2</xref></contrib><contrib contrib-type="author"><name><surname>Patterson</surname><given-names>Jean L</given-names></name><email>jpatters@txbiomed.org</email><xref rid="aff0005" ref-type="aff">1</xref></contrib></contrib-group><aff id="aff0005"><label>1</label>Department of Virology and Immunology, Texas Biomedical Research Institute, San Antonio, TX 78227, USA</aff><aff id="aff0010"><label>2</label>Southwest National Primate Research Center, Texas Biomedical Research Institute, San Antonio, TX 78227, USA</aff><pub-date pub-type="pmc-release"><day>13</day><month>3</month><year>2012</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub"><month>6</month><year>2012</year></pub-date><pub-date pub-type="epub"><day>13</day><month>3</month><year>2012</year></pub-date><volume>2</volume><issue>3</issue><fpage>357</fpage><lpage>362</lpage><permissions><copyright-statement>Copyright © 2012 Elsevier B.V. All rights reserved.</copyright-statement><copyright-year>2012</copyright-year><copyright-holder>Elsevier B.V.</copyright-holder><license><license-p>Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.</license-p></license></permissions><abstract abstract-type="graphical"><title>Highlights</title><p>► The common marmoset is a new world primate weighing between 350 and 400 g. ► Marmosets are exquisite NHP models for viral, protozoan, bacterial agents as well as prions. ► Marmosets have emerged as a viable model for studying high biocontainment pathogens. ► Models have been described for Ebola, Marburg, Lassa, SARS-CoA and EEE viruses. ► Use of marmosets will accelerate development of countermeasures to high consequence pathogens.</p></abstract><abstract><p>The common marmoset is a new world primate belonging to the Callitrichidae family weighing between 350 and 400 g. The marmoset has been shown to be an outstanding model for studying aging, reproduction, neuroscience, toxicology, and infectious disease. With regard to their susceptibility to infectious agents, they are exquisite NHP models for viral, protozoan and bacterial agents, as well as prions. The marmoset provides the advantages of a small animal model in high containment coupled with the immunological repertoire of a nonhuman primate and susceptibility to wild type, non-adapted viruses.</p></abstract></article-meta></front><body><sec id="sec0005"><title>Introduction</title><p id="par0005">The common marmoset is a new world primate belonging to the Callitrichidae family. The animals are native to the Atlantic coastal forests in northeastern Brazil, but the supply for research comes from National Primate Research Centers, pharmaceutical companies, and breeding facilities [<xref rid="bib0005" ref-type="bibr">1</xref>]. It is small in size with adults weighing 350–400 g. The lifespan of marmosets is relatively compact compared to other nonhuman primates (NHPs), with animals reaching maturity by 18–24 months of age, producing offspring by three years of age and reaching old age by 8 years of age [<xref rid="bib0010" ref-type="bibr">2</xref>]. The compressed lifespan of the marmoset is attractive in scientific research because the number of marmosets available for research can be scaled up quickly when the need arises and then naturally reduced when large numbers of animals are not needed [<xref rid="bib0005" ref-type="bibr">1</xref>, <xref rid="bib0015" ref-type="bibr">3••</xref>].</p><p id="par0010">The marmoset has been shown to be an outstanding model for studying aging, reproduction, neuroscience, toxicology, and infectious disease [<xref rid="bib0015" ref-type="bibr">3<sup>••</sup></xref>]. With regard to their susceptibility to infectious agent, they are exquisite NHP models for viral, protozoan and bacterial agents, as well as prions [<xref rid="bib0015" ref-type="bibr">3••</xref>, <xref rid="bib0020" ref-type="bibr">4</xref>, <xref rid="bib0025" ref-type="bibr">5•</xref>, <xref rid="bib0030" ref-type="bibr">6</xref>, <xref rid="bib0035" ref-type="bibr">7•</xref>, <xref rid="bib0040" ref-type="bibr">8</xref>, <xref rid="bib0045" ref-type="bibr">9•</xref>, <xref rid="bib0050" ref-type="bibr">10</xref>, <xref rid="bib0055" ref-type="bibr">11•</xref>, <xref rid="bib0060" ref-type="bibr">12</xref>]. That they do not carry herpes b virus (<italic>Macacine herpesvirus 1</italic>), unlike macaques, which harbor the virus, is an especially desirable trait for those who handle the monkeys [<xref rid="bib0015" ref-type="bibr">3<sup>••</sup></xref>]. For the purposes of this review, the focus is on the use of marmosets in high biocontainment, highlighting how they reflect human disease.</p></sec><sec id="sec0010"><title>Marmoset as a small animal model for hemorrhagic fever</title><p id="par0015">Hemorrhagic fever is an often-fatal disease caused by RNA viruses belonging primarily to bunyaviridae, arenaviridae and filoviridae families. Because of the high morbidity they induce and the lack of approved vaccines and therapies, many of these viruses can only be handled safely using Biosafety level 4 practices. Disease severity, imported cases of disease from patients that traveled to endemic areas, and the potential use of this agent as a biological weapon underscore the need to understand its viral pathogenesis as well as to develop intervention strategies [<xref rid="bib0065" ref-type="bibr">13</xref>, <xref rid="bib0070" ref-type="bibr">14</xref>, <xref rid="bib0075" ref-type="bibr">15</xref>, <xref rid="bib0080" ref-type="bibr">16</xref>]. The unique characteristics of the marmoset make it especially suited for high biocontainment research. In particular, the small size of the animal as opposed to larger NHP species makes husbandry less cumbersome and time-consuming thus using these monkeys at high containment is safer and less expensive than using larger NHP counterparts. In addition, current small animal models for some hemorrhagic fever diseases require the use of rodent-adapted viruses, which have been shown not to be especially predictive of efficacy in NHPs. The marmoset has the advantage that it is susceptible to infection with wild-type viruses, which is desirable for testing vaccines and therapeutics.</p></sec><sec id="sec0015"><title>Arenavirus induced hemorrhagic fever</title><sec id="sec0020"><title>Lassa fever</title><p id="par0020">Lassa virus, a member of the Arenaviridae family, is the causative agent of Lassa fever. The fatal disease affects more than 300 000 people a year in western Africa and has an overall instance of fatality of 1–2%. The virus is transmitted from a natural rodent reservoir to humans via contaminated rodent excreta or by close contact with infected individuals [<xref rid="bib0065" ref-type="bibr">13</xref>]. Following an incubation period of 7–18 days, the disease is marked by a gradual onset of symptoms including fever, weakness and malaise. As the disease progresses, nausea, vomiting, diarrhea and abdominal pain are often observed. Hemorrhage on mucosal surfaces, such as conjunctival hemorrhages or gastrointestinal or vaginal bleeding, occurs in less than 20% of the cases. Late stages of the disease are marked by shock, seizures and coma, culminating in death [<xref rid="bib0065" ref-type="bibr">13</xref>].</p><p id="par0025">It has been demonstrated that a single subcutaneous inoculation of common marmosets with Lassa virus resulted in a systemic viral disease with fatal outcome and histological features similar to those described in fatal disease in humans [<xref rid="bib0035" ref-type="bibr">7<sup>•</sup></xref>]. The experimental infection resulted in a systemic viral disease with high viremia, elevated liver enzymes and decreased levels of albumin in plasma; weight loss; and severe morbidity 15–20 days after inoculation. Histological analysis of tissue from infected animals identified lesions comparable to those described in human cases of fatal Lassa fever, and included hepatic and adrenal necrosis, lymphoid depletion, and interstitial nephritis [<xref rid="bib0035" ref-type="bibr">7•</xref>, <xref rid="bib0050" ref-type="bibr">10</xref>]. The model also demonstrated that the virus induces alterations in target tissues that would be expected to impair adaptive immune responses [<xref rid="bib0035" ref-type="bibr">7<sup>•</sup></xref>] consistent with the observations of immunosuppression contributing to Lassa disease progression in humans [<xref rid="bib0085" ref-type="bibr">17</xref>].</p><p id="par0030">In fatal Lassa fever cases and Lassa virus-infected experimental animals the liver is one of the most affected organs participating in a systemic breakdown [<xref rid="bib0090" ref-type="bibr">18</xref>, <xref rid="bib0095" ref-type="bibr">19</xref>, <xref rid="bib0100" ref-type="bibr">20</xref>]. The most prominent morphological features of Lassa virus-inducible hepatitis in common marmosets were: (i) multifocal hepatic necrosis with mild inflammation presented predominantly by HAM56-positive macrophages; (ii) near absence of CD20-positive, CD8-positive, or CD3-positive lymphocytes in necrotic foci; (iv) the complete lack of expression of MHC-II antigen; and (v) hepatocyte proliferation as judged by positive Ki67 staining. These findings suggest evasion of the normal immune response as a virulence factor in the development of Lassa virus-induced hepatitis [<xref rid="bib0035" ref-type="bibr">7<sup>•</sup></xref>].</p><p id="par0035">Lymphoid depletion, a major finding in humans, was also observed in the spleen and lymph nodes of Lassa virus-infected marmosets. These changes were most pronounced in lymph nodes marked by loss of follicles and infiltration by large numbers of histiocytes. In addition to liver tissues, a marked reduction in the intensity of HLA-DR staining was also observed in lymph nodes in Lassa virus-infected marmosets. Alterations in the spleen included reduction in overall numbers of CD3-positive and CD20-positive lymphocytes in Lassa-infected marmosets [<xref rid="bib0035" ref-type="bibr">7<sup>•</sup></xref>]. The immunosuppressive phenotype of Lassa virus infection was previously based on detection of proinflammatory cytokines and immunomodulatory molecules in culture medium of human cells infected <italic>in vitro</italic> [<xref rid="bib0105" ref-type="bibr">21</xref>, <xref rid="bib0110" ref-type="bibr">22</xref>, <xref rid="bib0115" ref-type="bibr">23</xref>, <xref rid="bib0120" ref-type="bibr">24</xref>], in plasma of experimentally infected animals [<xref rid="bib0125" ref-type="bibr">25</xref>], or in Lassa fever patients [<xref rid="bib0085" ref-type="bibr">17</xref>].</p></sec><sec id="sec0025"><title>Argentine hemorrhagic fever</title><p id="par0040">Junin virus is the causative agent of Argentine hemorrhagic fever, for which no licensed vaccine or specific antiviral exists in the United States [<xref rid="bib0130" ref-type="bibr">26</xref>]. Humans become infected by inhalation of aerosolized rodent excrement or blood or direct contact with infected animals. The mortality rate for the disease is 15–30%. Early clinical symptoms of infection include fever, fatigue, nausea, and mild hemorrhaging (petechiae), usually in skin or mucosal tissues [<xref rid="bib0135" ref-type="bibr">27</xref>, <xref rid="bib0140" ref-type="bibr">28</xref>]. The initial targets, such as macrophages, recruit additional sentinel cells, through the secretion of cytokines and chemokines, leading to disseminated viral infection. Disseminated infection leads to lack of immune control, increased endothelial leakage and platelet defects.</p><p id="par0045">Common marmosets were successfully used for pathogenesis and protection studies with Junin virus [<xref rid="bib0145" ref-type="bibr">29</xref>, <xref rid="bib0150" ref-type="bibr">30</xref>, <xref rid="bib0155" ref-type="bibr">31</xref>, <xref rid="bib0160" ref-type="bibr">32</xref>, <xref rid="bib0165" ref-type="bibr">33</xref>]. Infection of <italic>Callithrix jacchus</italic> with the prototype strain of Junin virus produced a fatal disease with multifocal hemorrhages and characteristic microscopic lesions such as meningoencephalitis, lymphocytic depletion of lymphatic tissue, hepatocytic necrosis, interstitial pneumonia, and a variable decrease in bone marrow cellularity [<xref rid="bib0145" ref-type="bibr">29</xref>]. High virus concentrations correlated with lesions and with the presence of virus antigen [<xref rid="bib0145" ref-type="bibr">29</xref>].</p></sec><sec id="sec0030"><title>Filovirus induced hemorrhagic fever</title><p id="par0050">The family Filoviridae predominantly consists of two genera – Ebolavirus (EBOV) and Marburgvirus (MARV). The genera EBOV comprises five species: the prototype, Zaire; Sudan; Bundibugyo; Taï Forest (the virus formerly known as ‘Ivory Coast’); and Reston. EBOV Zaire, Sudan and Bundibugyo, as well as MARV, are responsible for sporadic, highly lethal outbreaks of severe hemorrhagic fever in both humans and apes in sub-Saharan Africa, with mortality rates sometimes approaching 90% [<xref rid="bib0170" ref-type="bibr">34</xref>]. Although the primary animal host for the filoviruses is still somewhat unclear, as with other tropical viral diseases, bats have been strongly implicated as a possible reservoir [<xref rid="bib0175" ref-type="bibr">35</xref>, <xref rid="bib0180" ref-type="bibr">36</xref>]. However, the description of EBOV Reston in pigs in Asia [<xref rid="bib0185" ref-type="bibr">37</xref>] serves as a warning about the potential ease with which these viruses may arise and spread in diverse species and populations. No FDA-approved vaccines or specific treatments are currently available for filoviruses, although recent advances in vaccine development are promising.</p><p id="par0055">The common marmoset is susceptible to experimental infection with viruses from the family Filoviridae [<xref rid="bib0045" ref-type="bibr">9<sup>•</sup></xref>]. The intramuscular inoculation of as little as 10 PFU of either EBOV or MARV induced pathological features similar to those observed in human disease. Most notably, animals experienced thrombocytopenia, neutrophilia and disseminated intravascular coagulation [<xref rid="bib0045" ref-type="bibr">9<sup>•</sup></xref>]. Marmosets had high virus loads in blood and tissue regardless of dose of virus or agent. Furthermore, the small NHP experienced a disease syndrome comparable to what has been reported in other NHP models currently used to study filovirus disease.</p><p id="par0060">Inoculation of marmosets with Zaire ebolavirus resulted in an acute disease. Marmosets experienced anorexia coinciding with the onset of fever. Shortly after these initial findings, anorexia and varying degrees of recumbency were observed, culminating in prostration and death at 4–5 days post-challenge [<xref rid="bib0045" ref-type="bibr">9<sup>•</sup></xref>]. Previous work has shown that intramuscular inoculation of macaques with MARV results in a similar course of disease; however, overall disease progression was delayed [<xref rid="bib0190" ref-type="bibr">38</xref>, <xref rid="bib0195" ref-type="bibr">39</xref>, <xref rid="bib0200" ref-type="bibr">40</xref>]. Experimental inoculation of marmosets with MARV also results in delayed onset of disease, with death occurring 3–4 days later than seen with marmosets infected with EBOV. However, the course of Marburg disease in marmosets was more rapid than that seen in macaques, with death occurring several days sooner than in macaques [<xref rid="bib0045" ref-type="bibr">9<sup>•</sup></xref>].</p><p id="par0065">Marmosets infected with either of the filoviruses display neutrophilia, lymphopenia and thrombocytopenia. These hematological abnormalities are also seen in human infection [<xref rid="bib0205" ref-type="bibr">41</xref>, <xref rid="bib0210" ref-type="bibr">42</xref>, <xref rid="bib0215" ref-type="bibr">43•</xref>]. Shortly after infection, overall platelet counts decreased while neutrophil numbers increased, with a concomitant decrease in lymphocyte numbers. In addition, infected marmosets showed biochemical signs of liver involvement early in infection with elevated markers of liver function (ALT, ALP, GGT). Gross examination of the liver revealed hepatomegaly with pale foci throughout all lobes while microscopic examination of sections from the liver revealed necrosis with mild to moderate inflammation [<xref rid="bib0045" ref-type="bibr">9</xref>]. Similar findings have been documented in the macaque model of filovirus infection and in fatal human cases [<xref rid="bib0215" ref-type="bibr">43•</xref>, <xref rid="bib0220" ref-type="bibr">44</xref>, <xref rid="bib0225" ref-type="bibr">45</xref>].</p><p id="par0070">Fatal human cases are characterized by hemorrhage and bleeding at site of venipuncture and other coagulation abnormalities. The coagulopathy observed in humans at times exists in the absence of rash: only 50% of patients infected with EBOV develop a maculopapular rash [<xref rid="bib0235" ref-type="bibr">47</xref>]. Marmosets do not develop a petechial rash when infected with either MARV or EBOV and in this respect appear to be more similar to the African green monkey model of filovirus infection [<xref rid="bib0190" ref-type="bibr">38</xref>, <xref rid="bib0230" ref-type="bibr">46</xref>]. Further evidence that the marmoset mimics human disease is that microscopic examination of tissue from EBOV-infected animals showed widespread fibrin deposition that is a hallmark of coagulation abnormalities [<xref rid="bib0200" ref-type="bibr">40</xref>, <xref rid="bib0225" ref-type="bibr">45</xref>, <xref rid="bib0240" ref-type="bibr">48</xref>]. EBOV infection of the marmoset caused a severe disseminated viral infection characterized principally by microthrombosis in multiple organs (disseminated intravasculature coagulation). MARV-infected animals displayed moderate fibrin deposition in the spleen. These findings are similar to those seen in human infection and in the macaque [<xref rid="bib0200" ref-type="bibr">40</xref>, <xref rid="bib0215" ref-type="bibr">43•</xref>, <xref rid="bib0225" ref-type="bibr">45</xref>, <xref rid="bib0240" ref-type="bibr">48</xref>]. Interestingly, signs of coagulopathy characteristic of primate infections are observed variably in rodent models [<xref rid="bib0190" ref-type="bibr">38</xref>, <xref rid="bib0245" ref-type="bibr">49</xref>, <xref rid="bib0250" ref-type="bibr">50</xref>].</p></sec></sec><sec id="sec0035"><title>Marmoset as a model for encephalitis</title><p id="par0075">Eastern Equine Encephalitis (EEE) is an arthropod borne viral encephalitis endemic in North America along the United States Atlantic Coast affecting humans and equines. Severe cases of human infection begin with fever, chills, headache, and vomiting and then rapidly progress to disorientation, seizure and coma owing to encephalitis. EEEV causes greater than 30% mortality and there is no specific treatment. Because alphaviruses are highly infectious by aerosol route, development of countermeasures is of high priority.</p><p id="par0080">Intranasal exposure to a North American strain of EEEV caused lethal encephalitis in marmosets [<xref rid="bib0030" ref-type="bibr">6</xref>]. A decrease in leukocytes was observed in NA EEEV-infected marmosets within 24–48 h of infection, followed by marked leukocytosis before death or euthanasia. Similar to human cases [<xref rid="bib0255" ref-type="bibr">51</xref>], leukocytosis in the marmosets was composed of a mixture of lymphocytes and granulocytes.</p><p id="par0085">The pathological lesions in the CNS of the NA EEEV-infected marmosets were similar to those described for human cases [<xref rid="bib0255" ref-type="bibr">51</xref>, <xref rid="bib0260" ref-type="bibr">52</xref>, <xref rid="bib0265" ref-type="bibr">53</xref>, <xref rid="bib0270" ref-type="bibr">54</xref>], where EEEV causes neuronal loss, neuronophagia, perivascular cuffs, focal and diffuse accumulations of inflammatory cells and leptomeningitis in the CNS. Vascular lesions with breakdown in the structure of the vessel wall and the appearance of thrombi and extravasation of red blood cells have often been noted. Foci of necrosis in the gray and white matter have also been reported in severe EEE cases of the disease. Areas of the CNS most frequently subject to severe lesions include the cerebral cortex, basal ganglia, thalamus, hippocampus, and brainstem. By contrast, lesions in the cerebellum and spinal cord are not common findings in human EEE.</p><p id="par0090">South American EEEV strain BeAr436087 was attenuated in infected marmosets, a finding consistent with data derived from mouse studies. There have been only two reported fatal human encephalitis cases of EEE in South America [<xref rid="bib0275" ref-type="bibr">55</xref>]. Humans are most probably exposed in South America but do not develop apparent infection with EEEV because of poor infectivity and/or a virulence of South American strains [<xref rid="bib0280" ref-type="bibr">56</xref>].</p></sec><sec id="sec0040"><title>Marmoset as a model for SARS</title><p id="par0095">Severe acute respiratory syndrome (SARS) emerged in 2002 and infected 8000 people, causing death in 11% of the cases [<xref rid="bib0285" ref-type="bibr">57</xref>, <xref rid="bib0290" ref-type="bibr">58</xref>]. Humans infected primarily present with pneumonitis but may also develop hepatic, gastrointestinal, and renal pathology. Older people were more often associated with increased SARS pathogenicity and death resulting from acute respiratory distress syndrome [<xref rid="bib0295" ref-type="bibr">59</xref>, <xref rid="bib0300" ref-type="bibr">60</xref>]. Intratracheal inoculation of marmosets with cell culture supernatant containing SARS-CoV develops disease with features similar to human disease [<xref rid="bib0055" ref-type="bibr">11<sup>•</sup></xref>]. Mononuclear cell interstitial pneumonitis, accompanied by multinucleated syncytial cells, edema, and bronchiolitis, was observed in most SARS-infected animals while alveolar macrophages and type-1 pneumocytes appeared to be the site of viral antigen localization. Furthermore, pulmonary tissue extracts obtained at necropsy as well as tracheobronchial lymph node and myocardium had detectable levels of viral RNA. Hepatic inflammation was observed in most animals, predominantly as a multifocal lymphocytic hepatitis accompanied by necrosis of individual hepatocytes [<xref rid="bib0055" ref-type="bibr">11<sup>•</sup></xref>]. These findings provide evidence that the marmoset is a relevant NHP to study SARS-CoV pathogenesis.</p></sec><sec id="sec0045"><title>Conclusions</title><p id="par0100">The marmoset has emerged as a viable NHP model for studying high biocontainment infectious disease agents (<xref rid="tbl0005" ref-type="table">Table 1</xref>). Advantages of using the marmoset are that they mimic human disease, are small in size, provide a cost savings over larger NHP species, require husbandry techniques that are less time consuming, and have fewer biosafety considerations because they are not known to carry endogenous virus harmful to humans. Marmosets, because they are NHPs, provide distinct advantages over rodent species including an immunological repertoire that more closely resembles humans. As testing of vaccines and therapies to high consequence pathogens advances, more robust animal models to validate countermeasures will be required [<xref rid="bib0305" ref-type="bibr">61</xref>].<table-wrap position="float" id="tbl0005"><label>Table 1</label><caption><p>Disease agents.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left">Disease</th><th align="center">Agent</th><th align="center">Route</th><th align="center">Main feature</th></tr></thead><tbody><tr><td align="left">Ebola hemorrhagic fever</td><td align="left">Ebola Zaire (Kikwit)</td><td align="left">Intramuscular</td><td align="left">Viremia, hemorrhage, thrombocytopenia, neutrophilia, increase hepatic enzymes, DIC</td></tr><tr><td align="left">Marburg hemorrhagic fever</td><td align="left">Marburg (Musoke)</td><td align="left">Intramuscular</td><td align="left">Viremia, hemorrhage, thrombocytopenia, neutrophilia, increase hepatic enzymes, moderate fibrin deposition</td></tr><tr><td align="left">Lassa hemorrhagic fever</td><td align="left">Lassa (Josiah)</td><td align="left">Subcutaneous</td><td align="left">Viremia, elevated liver enzymes, multifocal hepatic necrosis, lymphoid depletion, MHC-II and CD20 lymphocytes suppression</td></tr><tr><td align="left">Argentine hemorrhagic fever</td><td align="left">Junin (XJ Strain)</td><td align="left">Intramuscular</td><td align="left">Multifocal hemorrhage, lymphocytic depletion, hepatocellular necrosis, viremia</td></tr><tr><td align="left">Eastern Equine Encephalitis</td><td align="left">EEE (FL93-939)</td><td align="left">Intranasal</td><td align="left">Encephalitis, neuronophagia, perivascular cuffing, leptomeningitis</td></tr><tr><td align="left">SARS</td><td align="left">SARS-CoV (Urbani)</td><td align="left">Intratracheal</td><td align="left">Viral RNA in pulmonary extracts, interstitial pneumonitis and Bronchiolitis</td></tr></tbody></table></table-wrap></p><p id="par0105">Because of the sporadic nature of many high consequence pathogens, the incidence of these agents is not predictable and therefore phase III efficacy trials are not feasible. The US Food and Drug Administration (FDA) declared a new regulation in 2002 as an alternative licensing pathway for pharmaceutical products that target highly lethal pathogens when evaluation in the field is not possible. The ‘animal rule’ will allow approval provided that satisfactory efficacy data are generated in two animal models. In the case of viral hemorrhagic fever, the marmoset offers advantages over rodent species as an alternative small animal model. With regard to filovirus research, in addition to needing rodent adapted virus, mouse and guinea pig filovirus models have not been good predictors of efficacy in higher species. The marmoset model provides the advantages of a small animal model in high containment coupled with the immunological repertoire of an NHP and susceptibility to wild type, non-adapted viruses. Undoubtedly, increased use of marmoset models will accelerate pre-clinical development of vaccines and therapeutics to high consequence pathogens.</p></sec><sec id="sec0050"><title>References and recommended reading</title><p id="par0110">Papers of particular interest, published within the period of review, have been highlighted as:<list list-type="simple" id="lis0005"><list-item id="lsti0005"><p id="par0115">• of special interest</p></list-item><list-item id="lsti0010"><p id="par0120">•• of outstanding interest</p></list-item></list></p></sec></body><back><ref-list id="bibl0005"><title>References</title><ref id="bib0005"><label>1</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Abbott</surname><given-names>D.H.</given-names></name><name><surname>Barnett</surname><given-names>D.K.</given-names></name><name><surname>Colman</surname><given-names>R.J.</given-names></name><name><surname>Yamamoto</surname><given-names>M.E.</given-names></name><name><surname>Schultz-Darken</surname><given-names>N.J.</given-names></name></person-group><article-title>Aspects of common marmoset basic biology and life history important for biomedical research</article-title><source>Comp Med</source><volume>53</volume><year>2003</year><fpage>339</fpage><lpage>350</lpage><pub-id pub-id-type="pmid">14524409</pub-id></element-citation></ref><ref id="bib0010"><label>2</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Abbott</surname><given-names>D.H.</given-names></name><name><surname>Hearn</surname><given-names>J.P.</given-names></name></person-group><article-title>Physical, hormonal and behavioural aspects of sexual development in the marmoset monkey, <italic>Callithrix jacchus</italic></article-title><source>J Reprod Fertil</source><volume>53</volume><year>1978</year><fpage>155</fpage><lpage>166</lpage><pub-id pub-id-type="pmid">417178</pub-id></element-citation></ref><ref id="bib0015"><label>3••</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Mansfield</surname><given-names>K.</given-names></name></person-group><article-title>Marmoset models commonly used in biomedical research</article-title><source>Comp Med</source><volume>53</volume><year>2003</year><fpage>383</fpage><lpage>392</lpage><pub-id pub-id-type="pmid">14524414</pub-id></element-citation><note><p>This review summarizes the utility of marmosets in biomedical research setting.</p></note></ref><ref id="bib0020"><label>4</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Frigerio</surname><given-names>M.J.</given-names></name><name><surname>Rondinonne</surname><given-names>S.N.</given-names></name><name><surname>Calello</surname><given-names>M.A.</given-names></name><name><surname>Golfera</surname><given-names>H.</given-names></name><name><surname>Weissenbacher</surname><given-names>M.C.</given-names></name></person-group><article-title><italic>Callithrix jacchus</italic> infection with Junin virus. 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resources in the age of biodefense</article-title><source>ILAR J</source><volume>46</volume><year>2005</year><fpage>15</fpage><lpage>22</lpage><pub-id pub-id-type="pmid">15644560</pub-id></element-citation></ref></ref-list><ack><title>Acknowledgements</title><p>We would like to thank Sandra Rios, Maria Messenger and Jennifer Meehan for technical assistance in preparing this manuscript. We would also like to acknowledge a <funding-source id="gs0005">NIH laboratory construction grant</funding-source> (C06 RR12087) and the <funding-source id="gs0010">Southwest National Primate Research Center</funding-source> base grant (P51 482RR013986).</p></ack></back></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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