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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Recurrent and Sustained Viral Infections in Primary Immunodeficiencies</title><author><name sortKey="Ruffner, Melanie A" sort="Ruffner, Melanie A" uniqKey="Ruffner M" first="Melanie A." last="Ruffner">Melanie A. Ruffner</name><affiliation><nlm:aff id="aff1"><institution>The Children’s Hospital of Philadelphia</institution>,<addr-line>Philadelphia, PA</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Sullivan, Kathleen E" sort="Sullivan, Kathleen E" uniqKey="Sullivan K" first="Kathleen E." last="Sullivan">Kathleen E. Sullivan</name><affiliation><nlm:aff id="aff1"><institution>The Children’s Hospital of Philadelphia</institution>,<addr-line>Philadelphia, PA</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Henrickson, Sarah E" sort="Henrickson, Sarah E" uniqKey="Henrickson S" first="Sarah E." last="Henrickson">Sarah E. Henrickson</name><affiliation><nlm:aff id="aff1"><institution>The Children’s Hospital of Philadelphia</institution>,<addr-line>Philadelphia, PA</addr-line>,<country>United States</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">28674531</idno><idno type="pmc">5474473</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5474473</idno><idno type="RBID">PMC:5474473</idno><idno type="doi">10.3389/fimmu.2017.00665</idno><date when="2017">2017</date><idno type="wicri:Area/Pmc/Corpus">004A04</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">004A04</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Recurrent and Sustained Viral Infections in Primary Immunodeficiencies</title><author><name sortKey="Ruffner, Melanie A" sort="Ruffner, Melanie A" uniqKey="Ruffner M" first="Melanie A." last="Ruffner">Melanie A. Ruffner</name><affiliation><nlm:aff id="aff1"><institution>The Children’s Hospital of Philadelphia</institution>,<addr-line>Philadelphia, PA</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Sullivan, Kathleen E" sort="Sullivan, Kathleen E" uniqKey="Sullivan K" first="Kathleen E." last="Sullivan">Kathleen E. Sullivan</name><affiliation><nlm:aff id="aff1"><institution>The Children’s Hospital of Philadelphia</institution>,<addr-line>Philadelphia, PA</addr-line>,<country>United States</country></nlm:aff></affiliation></author><author><name sortKey="Henrickson, Sarah E" sort="Henrickson, Sarah E" uniqKey="Henrickson S" first="Sarah E." last="Henrickson">Sarah E. Henrickson</name><affiliation><nlm:aff id="aff1"><institution>The Children’s Hospital of Philadelphia</institution>,<addr-line>Philadelphia, PA</addr-line>,<country>United States</country></nlm:aff></affiliation></author></analytic><series><title level="j">Frontiers in Immunology</title><idno type="eISSN">1664-3224</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Viral infections are commonplace and often innocuous. Nevertheless, within the population of patients with primary immunodeficiencies (PIDDs), viral infections can be the feature that drives a diagnostic evaluation or can be the most significant morbidity for the patient. This review is focused on the viral complications of PIDDs. It will focus on respiratory viruses, the most common type of viral infection in the general population. Children and adults with an increased frequency or severity of respiratory viral infections are often referred for an immunologic evaluation. The classic teaching is to investigate humoral function in people with recurrent sinopulmonary infections, but this is often interpreted to mean recurrent bacterial infections. Recurrent or very severe viral infections may also be a harbinger of a primary immunodeficiency as well. This review will also cover persistent cutaneous viral infections, systemic infections, central nervous system infections, and gastrointestinal infections. In each case, the specific viral infections may drive a diagnostic evaluation that is specific for that type of virus. This review also discusses the management of these infections, which can become problematic in patients with PIDDs.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Campbell, H" uniqKey="Campbell H">H Campbell</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gruber, C" uniqKey="Gruber C">C Gruber</name></author><author><name sortKey="Keil, T" uniqKey="Keil T">T Keil</name></author><author><name sortKey="Kulig, M" uniqKey="Kulig M">M Kulig</name></author><author><name sortKey="Roll, S" uniqKey="Roll S">S Roll</name></author><author><name sortKey="Wahn, U" uniqKey="Wahn U">U Wahn</name></author><author><name sortKey="Wahn, V" uniqKey="Wahn V">V Wahn</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Monto, As" uniqKey="Monto A">AS Monto</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Aligne, Ca" uniqKey="Aligne C">CA 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Immunol</journal-id><journal-id journal-id-type="iso-abbrev">Front Immunol</journal-id><journal-id journal-id-type="publisher-id">Front. Immunol.</journal-id><journal-title-group><journal-title>Frontiers in Immunology</journal-title></journal-title-group><issn pub-type="epub">1664-3224</issn><publisher><publisher-name>Frontiers Media S.A.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28674531</article-id><article-id pub-id-type="pmc">5474473</article-id><article-id pub-id-type="doi">10.3389/fimmu.2017.00665</article-id><article-categories><subj-group subj-group-type="heading"><subject>Immunology</subject><subj-group><subject>Review</subject></subj-group></subj-group></article-categories><title-group><article-title>Recurrent and Sustained Viral Infections in Primary Immunodeficiencies</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Ruffner</surname><given-names>Melanie A.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/443183"></uri></contrib><contrib contrib-type="author"><name><surname>Sullivan</surname><given-names>Kathleen E.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1">*</xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/133432"></uri></contrib><contrib contrib-type="author"><name><surname>Henrickson</surname><given-names>Sarah E.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/443178"></uri></contrib></contrib-group><aff id="aff1"><sup>1</sup><institution>The Children’s Hospital of Philadelphia</institution>,<addr-line>Philadelphia, PA</addr-line>,<country>United States</country></aff><author-notes><fn fn-type="edited-by"><p>Edited by: Antonio Condino-Neto, University of São Paulo, Brazil</p></fn><fn fn-type="edited-by"><p>Reviewed by: Alexandra Freeman, National Institutes of Health, United States; Elham Hossny, Ain Shams University, Egypt; Jolan Eszter Walter, University of South Florida, United States</p></fn><corresp content-type="corresp" id="cor1">*Correspondence: Kathleen E. Sullivan, <email>sullivank@email.chop.edu</email></corresp><fn fn-type="other" id="fn001"><p>Specialty section: This article was submitted to Primary Immunodeficiencies, a section of the journal Frontiers in Immunology</p></fn></author-notes><pub-date pub-type="epub"><day>19</day><month>6</month><year>2017</year></pub-date><pub-date pub-type="collection"><year>2017</year></pub-date><volume>8</volume><elocation-id>665</elocation-id><history><date date-type="received"><day>01</day><month>3</month><year>2017</year></date><date date-type="accepted"><day>22</day><month>5</month><year>2017</year></date></history><permissions><copyright-statement>Copyright © 2017 Ruffner, Sullivan and Henrickson.</copyright-statement><copyright-year>2017</copyright-year><copyright-holder>Ruffner, Sullivan and Henrickson</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p></license></permissions><abstract><p>Viral infections are commonplace and often innocuous. Nevertheless, within the population of patients with primary immunodeficiencies (PIDDs), viral infections can be the feature that drives a diagnostic evaluation or can be the most significant morbidity for the patient. This review is focused on the viral complications of PIDDs. It will focus on respiratory viruses, the most common type of viral infection in the general population. Children and adults with an increased frequency or severity of respiratory viral infections are often referred for an immunologic evaluation. The classic teaching is to investigate humoral function in people with recurrent sinopulmonary infections, but this is often interpreted to mean recurrent bacterial infections. Recurrent or very severe viral infections may also be a harbinger of a primary immunodeficiency as well. This review will also cover persistent cutaneous viral infections, systemic infections, central nervous system infections, and gastrointestinal infections. In each case, the specific viral infections may drive a diagnostic evaluation that is specific for that type of virus. This review also discusses the management of these infections, which can become problematic in patients with PIDDs.</p></abstract><kwd-group><kwd>virus</kwd><kwd>primary immunodeficiency</kwd><kwd>morbidity</kwd><kwd>herpes</kwd><kwd>papillomavirus</kwd><kwd>norovirus</kwd><kwd>enterovirus</kwd></kwd-group><counts><fig-count count="2"></fig-count><table-count count="3"></table-count><equation-count count="0"></equation-count><ref-count count="132"></ref-count><page-count count="13"></page-count><word-count count="10674"></word-count></counts></article-meta></front><body><sec sec-type="introduction" id="S1"><title>Introduction</title><p>Frequent infections are a common reason for physician visits. Distinguishing a pattern or a type of infection that suggests an immunodeficiency as opposed to part of the normal susceptibility to infection can be a challenge. Common causes of recurrent infections are allergies, anatomical contributions, secondary immune deficiency, and an unusual burden of exposures. Primary immunodeficiencies (PIDDs) are much less common and therefore difficult to appreciate during the wealth of infections that are typically seen in a physician’s practice. During the first 5 years of life, children can experience six to eight respiratory tract infections per year. These tend to peak in the winter months and daycare attendance, exposure to smokers, and atopy can increase this frequency significantly (<xref rid="B1" ref-type="bibr">1</xref>–<xref rid="B4" ref-type="bibr">4</xref>). Respiratory tract infections in adults are somewhat less common; however, three to five respiratory tract infections per year in adults are typical (<xref rid="B5" ref-type="bibr">5</xref>). Recurrent sinus infections, pneumonia, and bronchitis are common signs of an immunodeficiency, recognizing that frequent bacterial infections of the respiratory track are often a harbinger of antibody disorders, the most common type of primary immunodeficiency. This review will address recurrent and sustained viral infections for which there are fewer studies to assist the physician in the identification of patients with potential immunodeficiency. This review will address unusual viral respiratory tract infections, systemic viral infections, infections of the brain and meninges, and cutaneous viral infections. Unusual viral infections can be a sign or complication of PIDD. There are several excellent reviews that address the overall approach to suspected PIDD (<xref rid="B6" ref-type="bibr">6</xref>–<xref rid="B8" ref-type="bibr">8</xref>). Bacterial infections are generally highlighted, and therefore this review will focus on unusual and severe viral infections.</p></sec><sec id="S2"><title>Respiratory Viral Infections in PIDD</title><p>Respiratory viruses are extremely common in most patients with PIDDs (<xref rid="B9" ref-type="bibr">9</xref>, <xref rid="B10" ref-type="bibr">10</xref>). In most cases, they represent nuisance infections that can be a predisposing condition leading to bacterial superinfection. In patients with antibody defects, respiratory infections fall into this category. Although defense against recurrence of respiratory tract viruses is mediated largely by antibody, eradication of an infecting virus is mediated largely by the T cell compartment. Respiratory viral infections are therefore more significant in patients with T cell immune deficiencies. Today, many newborns with severe combined immune deficiency (SCID) are detected by newborn screening; however, this is not true in all parts of the world, nor is it true in all states in the USA. A study by the PIDTC found that 21% of their cohort had a respiratory infection prior to transplant with the most common being parainfluenza followed by RSV, rhinovirus, and influenza (<xref rid="B11" ref-type="bibr">11</xref>). Although other types of infections were more common as presenting features in this cohort, respiratory infections were among the least likely to resolve prior to transplant. All viral infections are typically prolonged in patients with T cell defects. However, in SCID, there are no T cells and a simple respiratory virus will progress relentlessly unless a hematopoietic stem cell transplant (HSCT) allows the infant to develop a competent immune system (Figure <xref ref-type="fig" rid="F1">1</xref>) (<xref rid="B11" ref-type="bibr">11</xref>). The specific pathogens to which children with T cell defects are susceptible include all of those common in the general population. RSV, influenza, and rhinovirus are typically the most prevalent during the respiratory season (<xref rid="B12" ref-type="bibr">12</xref>). Coronavirus and metapneumovirus have been increasingly recognized as causing respiratory infections. Exposures will dictate the pattern of viral infections in patients with T cell defects. The severity of disease is a result of both the degree of T cell compromise and the nature of the infecting virus. Any patient with prolonged viral infections is at risk for bacterial superinfection. It is not, therefore, uncommon to see a mixed picture of viral and bacterial infections. Additionally, severe T cell defects are associated with compromised antibody production, also contributing to a mixed infection picture.</p><fig id="F1" position="float"><label>Figure 1</label><caption><p>Chest radiograph of a term male infant with X-linked severe combined immune deficiency and RSV pneumonitis, which was rapidly fatal despite adjunctive use of IVIG and inhaled ribavirin. He was treated with an infusion of maternal haplo-identical hematopoietic stem cells at 18 days of life. He was admitted at 10 days old <bold>(A)</bold> and died at 27 days old <bold>(B)</bold> due to worsening respiratory status. Note the absent thymus.</p></caption><graphic xlink:href="fimmu-08-00665-g001"></graphic></fig><p>T cell defects are associated with a generally increased predisposition to viral infections. IRF7 deficiency, in contrast, is associated with a selective susceptibility to influenza (<xref rid="B13" ref-type="bibr">13</xref>). It is otherwise uncommon to see an isolated susceptibility to a respiratory virus. The single reported patient had a severe primary infection with influenza associated with poor production of type I and type III interferons.</p><sec id="S2-1"><title>Diagnostic Approach</title><p>There are many specific genetic types of immunodeficiencies associated with T cell deficiency, and the diagnostic considerations are different depending on the age of the patient. Infants with a prolonged or severe respiratory viral infection should be evaluated for SCID, and patients of any age with dysmorphic features or other associated features should be evaluated for chromosome 22q11.2 deletion syndrome (<xref rid="B14" ref-type="bibr">14</xref>). Most states now have a newborn screening program to detect SCID. The results can be accessed to identify significant T cell lymphopenia in early infancy. Newborn screening has significantly improved survival of infants with SCID. There are, however, significant T cell disorders not identified by this test, and therefore, T cell disorders still represent a concern in the setting of a prolonged viral infection. T cell enumeration is often the quickest way to screen for T cell defects. The vast majority of T cell deficiency conditions will have low T cell numbers or at least low CD4/CD45RA (naïve) T cell counts. Additional studies include proliferative studies, exclusion of HIV, and sequencing panels to identify inborn errors of immunity.</p></sec><sec id="S2-2"><title>Management</title><p>Management of respiratory tract infections in non-SCID T cell defects is largely supportive with optimization of bronchodilators, antiviral therapy if available and attention to nutrition (<xref rid="B12" ref-type="bibr">12</xref>). Management of respiratory tract infections in SCID is highly problematic. There is a race to replace the immune system before the virus can progress to the point of no return. This race is highly dependent on the type of transplant donor, type of conditioning, and type of transplant, but respiratory infections clearly impact the transplant outcome (<xref rid="B11" ref-type="bibr">11</xref>). Any adjunctive measure to improve respiratory status should be sought.</p></sec></sec><sec id="S3"><title>Systemic Viral Infections in PIDD</title><p>Children with severe T cell defects are also susceptible to systemic viral infections. Patients with SCID are extremely susceptible to progressive infection with cytomegalovirus (CMV) as well as other systemic viral infections. Infants with suspected SCID should be protected from exposures such as breast milk, transfusions, potentially infected siblings, live viral vaccines, and caregivers.</p><p>There is another circumstance in which susceptibility to gamma-herpes viruses such as CMV and Epstein–Barr virus (EBV) occurs. Table <xref ref-type="table" rid="T1">1</xref> lists conditions in which gamma-herpes virus susceptibility dominates the clinical picture. Patients with cytolytic T cell defects (with or without concomitant NK cell defects) exhibit a unique susceptibility to these gamma-herpes viruses (<xref rid="B15" ref-type="bibr">15</xref>). In some circumstances, the susceptibility is almost entirely limited to susceptibility to either severe mononucleosis or hemophagocytic lymphohistiocytosis (HLH). HLH is characterized by excessive immune activation and can be diagnosed either by a molecular diagnosis consistent with HLH or clinically when patients meet five out of eight criteria: fever, splenomegaly, cytopenias affecting two or more blood lineages, hypertriglyceridemia and/or hypofibrinogenemia, hemophagocytosis, low/absent natural killer cell activity, hyperferritinemia, and high soluble interleukin-2 receptor levels (<xref rid="B16" ref-type="bibr">16</xref>). Any patient presenting with exceptionally severe mononucleosis or HLH should be screened for the HLH defects.</p><table-wrap id="T1" position="float"><label>Table 1</label><caption><p>EBV susceptibility.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1">Phenotype</th><th valign="top" align="left" rowspan="1" colspan="1">Gene defect</th><th valign="top" align="left" rowspan="1" colspan="1">Viral susceptibility</th><th valign="top" align="left" rowspan="1" colspan="1">Other features</th></tr></thead><tbody><tr><td align="left" valign="top" rowspan="1" colspan="1">EBV viremia</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>ITK</italic></td><td align="left" valign="top" rowspan="1" colspan="1">EBV</td><td align="left" valign="top" rowspan="1" colspan="1">Lymphoma</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">EBV viremia</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>MAGT1</italic></td><td align="left" valign="top" rowspan="1" colspan="1">EBV</td><td align="left" valign="top" rowspan="1" colspan="1">Lymphoma</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">EBV viremia</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>CD27</italic></td><td align="left" valign="top" rowspan="1" colspan="1">EBV</td><td align="left" valign="top" rowspan="1" colspan="1">Low IgG</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">EBV viremia</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>CORO1A</italic></td><td align="left" valign="top" rowspan="1" colspan="1">Many viruses</td><td align="left" valign="top" rowspan="1" colspan="1">Lymphoma</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">EBV HLH</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>SH2D1A</italic></td><td align="left" valign="top" rowspan="1" colspan="1">EBV</td><td align="left" valign="top" rowspan="1" colspan="1">Lymphoma, dysgammaglobulinemia, and vasculitis</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">EBV HLH</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>XIAP</italic></td><td align="left" valign="top" rowspan="1" colspan="1">EBV</td><td align="left" valign="top" rowspan="1" colspan="1">Hypogammaglobulinemia</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">EBV lymphoma</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>MCM4</italic></td><td align="left" valign="top" rowspan="1" colspan="1">EBV, CMV</td><td align="left" valign="top" rowspan="1" colspan="1">Malignancy, short stature, adrenal insufficiency</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">Primary familial HLH</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>PRF1, UNC13D, STX11, STXBP3</italic></td><td align="left" valign="top" rowspan="1" colspan="1">EBV, CMV, others</td><td align="left" valign="top" rowspan="1" colspan="1"></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">Pigmentary dilution with HLH</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>LYST, RAB27A, AP3B1, BLOC1S6</italic></td><td align="left" valign="top" rowspan="1" colspan="1">EBV, CMV, others</td><td align="left" valign="top" rowspan="1" colspan="1">Pigmentary dilution</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">EBV susceptibility with broad infectious susceptibility</td><td align="left" valign="top" rowspan="1" colspan="1">Leaky SCID, most combined immunodeficiencies, <italic>WASP, WIPF1, PLCG2, PRKCD, ORAI1, STIM1, IKBKG, CASP8, STAT1</italic> GOF, <italic>DOCK8, GATA2</italic></td><td align="left" valign="top" rowspan="1" colspan="1">Many viral susceptibilities</td><td align="left" valign="top" rowspan="1" colspan="1">Gene dependent</td></tr></tbody></table><table-wrap-foot><p><italic>GOF, gain of function; LOF, loss of function; EBV, Epstein–Barr virus; HLH, hemophagocytic lymphohistiocytosis; CMV, cytomegalovirus; SCID, severe combined immune deficiency; IgG, immunoglobulin G</italic>.</p></table-wrap-foot></table-wrap><p>A second phenotype with susceptibility to EBV has a smoldering or even asymptomatic presentation. These patients generally have an increased risk of lymphoma due to chronic EBV, but the manifestations of EBV may be subtle or absent. The X-linked disorder due to deficiency of <italic>MAGT1</italic> is associated with a mild susceptibility to other infections but chronic EBV. Similar conditions include deficiencies of <italic>CD27, CTPS1, RASGRP1, CD70</italic>, and <italic>MCM4</italic>. The importance in recognizing this group is due to their unpredictable capacity to control EBV and the risk of lymphoreticular malignancies.</p><p>Nearly all of the leaky SCID types and the combined immunodeficiencies are associated with an increased risk of CMV and EBV (<xref rid="B17" ref-type="bibr">17</xref>, <xref rid="B18" ref-type="bibr">18</xref>). This set of disorders can have a broad phenotype including Omenn’s phenotype, autoimmunity, granulomas, and infections (<xref rid="B18" ref-type="bibr">18</xref>–<xref rid="B23" ref-type="bibr">23</xref>). In these patients, EBV and CMV can drive progression to malignancy, and they require careful monitoring. Leaky SCID has been defined as T cell lymphopenia (CD3 300–1,500 cells/mm<sup>3</sup>); functional impairment as defined by proliferative responses, absence of maternal engraftment, and most often having identified hypomorphic mutations in genes associated with SCID.</p><sec id="S3-1"><title>Diagnostic Approach</title><p>When the consideration is prolonged infection with gamma-herpes viruses without HLH, T cell counts and function can be helpful as supporting information but often genetic testing is the quickest approach. For HLH disorders, enumerating the HLH criteria is a useful exercise. CD163 staining of the bone marrow can be a sensitive way to identify active hemophagocytosis, but this is not required for the diagnosis (<xref rid="B15" ref-type="bibr">15</xref>, <xref rid="B16" ref-type="bibr">16</xref>, <xref rid="B24" ref-type="bibr">24</xref>). Additional maneuvers are measurement of IL-2R in the serum and CD107a on the surface as a marker for degranulation. HLH can occur without an underlying PIDD, and thus genetic analysis is often central to the management. Nearly always an underlying PIDD will require HSCT as definitive therapy, whereas HLH due to uncommon infections such as <italic>Leishmania</italic>, certain influenza viruses, and arboviruses will not require HSCT.</p></sec><sec id="S3-2"><title>Management</title><p>Management of systemic viral infections relies on the availability of antiviral compounds. For CMV, therapy is often begun with ganciclovir or valganciclovir (<xref rid="B25" ref-type="bibr">25</xref>, <xref rid="B26" ref-type="bibr">26</xref>). Foscarnet may be added if the virus is resistant or progressive in spite of adequate ganciclovir (<xref rid="B27" ref-type="bibr">27</xref>). Bone marrow toxicity from ganciclovir may also require a change to foscarnet. EBV in some cases is treated with rituximab to eliminate one important reservoir of virus (<xref rid="B28" ref-type="bibr">28</xref>). When HLH is present, a systemic approach to stabilize the patient and treat the underlying inflammation is essential (<xref rid="B29" ref-type="bibr">29</xref>). Risks and benefits of antiviral therapy must be carefully weighed as all approaches can have significant adverse events. Management decisions are often impacted by subsequent transplant strategies.</p></sec></sec><sec id="S4"><title>Chronic Viral Skin Infections in Primary Immunodeficiency</title><p>Cutaneous manifestations are common in PIDD. As many as two-thirds of the patients have cutaneous manifestations at some point. Atopy, infection, and inflammatory lesions have all been described, and there may be interplay between the features (<xref rid="B30" ref-type="bibr">30</xref>). Awareness of common skin infections is important both to aid in the early diagnosis and also in the treatment of potentially life-threatening infections that can begin in the skin. Bacterial infections are one of the most common findings in PIDD. For example, folliculitis, abscesses, and impetigo are typical in neutrophil defects. Similarly, a significant subset of PIDD diagnoses is associated with fungal infections. These can be seen both in T cell defects as well as defects of the myeloid compartment. Chronic mucocutaneous candidiasis is most often due to defects that affect the Th17 cell production or function. These diseases generally do not overlap those with a susceptibility to cutaneous viral infections. One exception is <italic>STAT1</italic> gain-of-function (GOF) mutations that render patients susceptible to a broad range of cutaneous infections. Viral infections of the skin are not nearly as common but are much more suggestive of PIDD. Severe herpes infections and papillomavirus are particularly characteristic of PIDD and can become the most notable feature in a patient. Chronic herpes virus and papillomavirus, in turn, predispose to cutaneous carcinoma and surveillance becomes important for this evolution. In this section, we will provide a brief synopsis about the individual disorders associated with susceptibility to papillomavirus.</p><sec id="S4-1"><title>Papillomaviridae</title><p>There are more than 200 strains of human papillomavirus (HPV). The diverse strains have variable malignant potential and tissue tropism. HPV causes warts in the general population with an incidence of cutaneous warts (Figure <xref ref-type="fig" rid="F2">2</xref>) that range from 1 to 12% (<xref rid="B31" ref-type="bibr">31</xref>–<xref rid="B33" ref-type="bibr">33</xref>). School age children have been estimated to have a cutaneous warts prevalence of over 40% (<xref rid="B34" ref-type="bibr">34</xref>). While sexually active women 20–24 years of age have a prevalence of genital papillomavirus of nearly 50% (<xref rid="B35" ref-type="bibr">35</xref>), clinically significant genital warts occur in only 5% of women (<xref rid="B36" ref-type="bibr">36</xref>). Genital HPV infection has been associated with malignant transformation, leading to the development of the first vaccine intended to prevent cancer. Worldwide, 5% of cancer is caused by HPV (<xref rid="B37" ref-type="bibr">37</xref>). Nearly all T cell disorders can be associated with increased susceptibility to warts; however, there is a small group of PIDDs that have warts as a cardinal feature (<xref rid="B38" ref-type="bibr">38</xref>). In these patients, the warts are recurrent, severe, and resistant to therapy. In most cases, the specific papillomaviruses are identical to those in the general population, and the appearance of the warts is the same as in the general population. In epidermodysplasia verruciformis (EV), however, there is a broader susceptibility to HPV types. In addition, the cutaneous manifestations are often atypical. Table <xref ref-type="table" rid="T2">2</xref> compares the features of the different conditions described below.</p><fig id="F2" position="float"><label>Figure 2</label><caption><p>Bilateral plantar warts on a patient who had experienced 5 years of immune suppression for a cardiac transplant. Deep palmoplantar warts such as those in the top panel are referred to as myrmecila and can be painful. The small black markings are characteristic and represent small blood vessels that have grown into the exophytic lesion. Photo credit: Marissa J. Perman, MD.</p></caption><graphic xlink:href="fimmu-08-00665-g002"></graphic></fig><table-wrap id="T2" position="float"><label>Table 2</label><caption><p>Cutaneous viral infections in primary immunodeficiencies.</p></caption><table frame="hsides" rules="rows"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1">Viral family</th><th valign="top" align="left" rowspan="1" colspan="1">Virus</th><th valign="top" align="left" rowspan="1" colspan="1">Increased susceptibility in which PID</th><th valign="top" align="left" rowspan="1" colspan="1">Other features</th></tr></thead><tbody><tr><td align="left" valign="top" rowspan="1" colspan="1">Papillomaviridae</td><td align="left" valign="top" rowspan="1" colspan="1">HPV</td><td align="left" valign="top" rowspan="1" colspan="1">Ataxia telangiectasia; <italic>DOCK8</italic>; EV (<italic>EVER1, EVER2, RHOH</italic>; <italic>LCK</italic>); <italic>GATA2</italic>; Idiopathic T cell lymphopenia; Netherton syndrome; <italic>STK4/MST1</italic>; WHIM (<italic>CXCR4</italic>); WILD, <italic>CARMIL2/RLTPR</italic>, Clouston’s syndrome</td><td align="left" valign="top" rowspan="1" colspan="1"><list list-type="simple"><list-item><p>EV: warts are often flat, appearing as actinic keratosis or seborrhea-like lesions and can have increased susceptibility to unusual HPV strains. No other infectious susceptibility</p></list-item><list-item><p>DOCK8, GATA2: also include susceptibility to HSV. Progressive lymphopenia seen</p></list-item></list></td></tr><tr><td align="left" valign="top" rowspan="3" colspan="1">Herpesviridae</td><td align="left" valign="top" rowspan="1" colspan="1">HHV8/KSHV</td><td align="left" valign="top" rowspan="1" colspan="1">IFNGR1, OX40</td><td align="left" valign="top" rowspan="1" colspan="1">Susceptibility to mycobacteria</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">HSV</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>DOCK8</italic>; <italic>GATA2</italic>; <italic>NEMO</italic>; <italic>STAT1 GOF</italic>; <italic>STK4</italic>; <italic>CXCR4</italic>; Wiskott–Aldrich syndrome (WAS)</td><td align="left" valign="top" rowspan="1" colspan="1"><list list-type="simple"><list-item><p><italic>DOCK8, NEMO, STAT1</italic> GOF: broad infectious susceptibility</p></list-item><list-item><p><italic>CXCR4</italic>: pancytopenia, abnormal neutrophils</p></list-item><list-item><p>WAS: thrombocytopenia, eczema</p></list-item></list></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">VZV</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>DOCK8</italic>; <italic>GATA2</italic>; <italic>STAT3</italic> GOF; <italic>IFNGR1</italic>; <italic>RHOH</italic>; <italic>STAT</italic>1 GOF; <italic>STK4</italic></td><td align="left" valign="top" rowspan="1" colspan="1"><list list-type="simple"><list-item><p><italic>DOCK8, NEMO, STAT1</italic> GOF: broad infectious susceptibility</p></list-item><list-item><p><italic>CXCR4</italic>: pancytopenia, abnormal neutrophils</p></list-item><list-item><p>WAS: thrombocytopenia, eczema</p></list-item></list></td></tr><tr><td align="left" valign="top" rowspan="2" colspan="1">Poxviridae</td><td align="left" valign="top" rowspan="1" colspan="1">MCV</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>DOCK8</italic>; <italic>GATA2</italic>; <italic>IKBKG</italic>; <italic>STAT1</italic> GOF; <italic>STK4</italic>; <italic>CXCR4</italic>; <italic>CARMIL2/RLTPR</italic></td><td align="left" valign="top" rowspan="1" colspan="1"><list list-type="simple"><list-item><p><italic>DOCK8, IKBKG, STAT1</italic> GOF: broad infectious susceptibility</p></list-item><list-item><p><italic>CXCR4</italic>: pancytopenia, abnormal neutrophils</p></list-item><list-item><p>WAS: thrombocytopenia, eczema</p></list-item></list></td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1">Orf virus</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>STAT1</italic> GOF</td><td align="left" valign="top" rowspan="1" colspan="1"><list list-type="simple"><list-item><p>Broad infectious susceptibility</p></list-item></list></td></tr></tbody></table><table-wrap-foot><p><italic>GOF, gain of function; LOF, loss of function; HPV, human papilloma virus; HSV, herpes simplex virus; EV, epidermodysplasia verruciformis; WHIM, warts, hypogammaglobulinemia, infections, and myelokathexis</italic>.</p></table-wrap-foot></table-wrap><sec id="S4-1-1"><title><italic>DOCK8</italic> Deficiency</title><p>Patients with <italic>DOCK8</italic> deficiency have a complex combined immunodeficiency secondary to disrupted cytoskeletal rearrangement (<xref rid="B39" ref-type="bibr">39</xref>). This includes an inability to properly assemble the immune synapse that fosters the signaling cascades required for lymphocyte memory differentiation (<xref rid="B40" ref-type="bibr">40</xref>). Lymphocyte migration through tissues is also compromised, contributing to the susceptibility to cutaneous infections (<xref rid="B39" ref-type="bibr">39</xref>). T cell counts are typically low for age, and there is impaired memory differentiation that may be progressive with age (<xref rid="B41" ref-type="bibr">41</xref>). Clinical features resemble that seen in Wiskott–Aldrich syndrome (WAS) including low IgM and elevated IgE and IgA. Patients have significant atopy, infections, impaired specific antibody responses and poor memory B cell responses, increased rates of malignancy, elevated IgE, and eosinophilia and are highly susceptible to cutaneous viral infections. Early in life, the atopic manifestations may dominate while the infectious susceptibility evolves. Skin infections are most often caused by HPV (including increased risk of malignant transformation of skin lesions), herpes simplex virus (HSV), molluscum contagiosum virus, and varicella zoster virus (<xref rid="B42" ref-type="bibr">42</xref>). HSCT has been shown to be curative (<xref rid="B43" ref-type="bibr">43</xref>).</p></sec><sec id="S4-1-2"><title>Epidermodysplasia Verruciformis</title><p>The term EV refers to a group of disorders in which patients are susceptible to beta-HPV with severe diffuse warts, and there is a striking increase in the rate of skin carcinomas (<xref rid="B44" ref-type="bibr">44</xref>). <italic>EVER1/TMC6</italic> and <italic>EVER2/TMC8</italic> inactivating mutations cause autosomal recessive (AR) EV. EVER proteins are intracellular zinc transporters, and mutations lead to altered cell activation and a more permissive environment for HPV. Interestingly, the only infectious susceptibility is to HPV. Most patients present in childhood, but the appearance of the warts can lead to misdiagnosis as seborrhea or tinea versicolor. The warts are generally worse on sun-exposed skin for reasons that are not clear. The specific HPV types are not necessarily those seen in the general population as wart-associated. The therapy in EV is usually local control since the susceptibility does not relate to hematopoietic cell dysfunction; there is no role for HSCT.</p></sec><sec id="S4-1-3"><title><italic>LCK</italic> Deficiency</title><p><italic>LCK</italic> deficiency causes atypical EV with CD4 T cell deficiency as well as recurrent pneumonia and severe warts complicated by non-melanoma skin cancer (<xref rid="B45" ref-type="bibr">45</xref>). To date, only a single patient with <italic>LCK</italic> deficiency has been described, leading to uncertainty in the full spectrum of infectious susceptibility. Therapy is not clear for the same reason, but HSCT would be expected to be curative.</p></sec><sec id="S4-1-4"><title><italic>CARMIL2/RLTPR</italic> </title><p>Three Norwegian families have been identified with increased viral cutaneous infections (warts and molluscum contagiosum) as well as dermatitis and pneumonia. The four affected family members were found to share a single variant in this gene, with some evidence for a role in T cell activation (<xref rid="B46" ref-type="bibr">46</xref>).</p></sec><sec id="S4-1-5"><title><italic>RHOH</italic> Deficiency</title><p>Mutations in the <italic>RHOH</italic> gene (an atypical Rho GTPase) cause susceptibility to EV-type HPV strains, due to alterations in T cell activation and homing (<xref rid="B47" ref-type="bibr">47</xref>). Naïve T cell counts are low, and there is poor skin homing of T cells, with an increase in effector memory T cells in the setting of altered T cell receptor signaling. <italic>RHOH</italic> deficiency infectious susceptibility was largely limited to HPV in the two siblings identified. In mice, the defect was correctable by transfer of wild-type bone marrow, suggesting that this is a potential treatment.</p></sec><sec id="S4-1-6"><title><italic>IKBKG</italic> Deficiency (<italic>NEMO</italic>)</title><p>Hypomorphic mutations in the central kinase of the canonical NFκB pathway lead to increased susceptibility to warts (<xref rid="B48" ref-type="bibr">48</xref>). This PIDD is associated with fine sparse hair, dental defects, and a broad susceptibility to infections including opportunistic infections. The spectrum of phenotypes is among the broadest among PIDDs. Lymphedema, osteopetrosis, susceptibility to pneumocystis and other fungi, mycobacterial susceptibility, and viral susceptibility call all be associated with <italic>IKBKG</italic> deficiency. Inflammatory bowel disease is also common. Cutaneous viral infections are common in this population but are not usually the dominant feature. Among the PIDD in this section, this is a disorder where the benefit of HSCT is unclear because HSCT outcomes have been poor.</p></sec><sec id="S4-1-7"><title><italic>GATA2</italic> Deficiency</title><p><italic>GATA2</italic> mutations yield a complex set of phenotypes. Patients tend to have monocytopenia and low NK and B cell counts and have susceptibility to HPV, among other infections (<xref rid="B49" ref-type="bibr">49</xref>). The laboratory defects are progressive with age and correlate with increasing infection burden. Clinical features include lymphedema, risk of malignancy, and pulmonary alveolar proteinosis. Infections include fungal infections and cutaneous viral infections. The cutaneous viral infections can be the most prominent feature but there is a wide-ranging phenotypic heterogeneity (<xref rid="B50" ref-type="bibr">50</xref>, <xref rid="B51" ref-type="bibr">51</xref>). The cutaneous viral infections and genital HPV are associated with a high rate of malignant transformation.</p></sec><sec id="S4-1-8"><title><italic>STAT1</italic> GOF</title><p>Patients with <italic>STAT1</italic> GOF mutations can present with dramatic autoimmunity, usually including enteropathy and endocrinopathies, or they can have a picture with a pronounced infectious susceptibility. Susceptibility to candida is common, but cutaneous viral infections can also be problematic (<xref rid="B52" ref-type="bibr">52</xref>, <xref rid="B53" ref-type="bibr">53</xref>). The viral infections can become more problematic as immune suppression is used to control the enteropathy.</p></sec><sec id="S4-1-9"><title>Netherton Syndrome</title><p>Patients with Netherton syndrome (secondary to <italic>SPINK5</italic> mutations) demonstrate congenital ichthyosis and have higher susceptibility to EV-associated HPV strains (<xref rid="B53" ref-type="bibr">53</xref>, <xref rid="B54" ref-type="bibr">54</xref>). Although Netherton syndrome can have a mild humoral immune deficiency, the susceptibility to warts seems to be a result of disrupted local response to infection (<xref rid="B55" ref-type="bibr">55</xref>). The warts are generally controllable with local measures.</p></sec><sec id="S4-1-10"><title><italic>MST1</italic> Deficiency</title><p>Serine–threonine kinase 4 (STK4), encoded by a gene called <italic>MST1</italic>, affects the FOXO1 transcription factor and thus impacts T cell lifespan and has been shown to increase susceptibility to HPV infections (<xref rid="B56" ref-type="bibr">56</xref>), as well as causing B cell lymphopenia. The phenotype also includes susceptibility to EBV and cutaneous viral infections.</p></sec><sec id="S4-1-11"><title>Warts, Hypogammaglobulinemia, Infections, and Myelokathexis (WHIM) Syndrome</title><p>Warts, hypogammaglobulinemia, infections, and myelokathexis syndrome is caused by an autosomal dominant (AD) GOF mutation in <italic>CXCR4</italic>, which leads to increased susceptibility to HPV (<xref rid="B57" ref-type="bibr">57</xref>, <xref rid="B58" ref-type="bibr">58</xref>). Varying degrees of pancytopenia can be seen, and hypogammaglobulinemia occurs in many (but not all) patients. Warts can be the most prominent susceptibility, but neutropenia and hypogammaglobulinemia can drive diverse infectious susceptibilities. COPD and cutaneous carcinoma have been observed (<xref rid="B59" ref-type="bibr">59</xref>). WHIM can be treated with plerixafor or topical control measures for the warts.</p></sec><sec id="S4-1-12"><title>WILD Syndrome</title><p>WILD (warts, depressed cell-mediated immunity, primary lymphedema, and anogenital dysplasia) is also correlated with severe warts without a known genetic etiology (<xref rid="B60" ref-type="bibr">60</xref>). Of note, this diagnosis does not lead to EV-defining HPV strain infections. A recent study demonstrates a case of a patient whose warts improved after quadrivalent HPV vaccination (<xref rid="B61" ref-type="bibr">61</xref>).</p></sec><sec id="S4-1-13"><title>Clouston Syndrome</title><p>An ectodermal dysplasia syndrome with alterations in hair and nails (not generally in teeth) which can present with eccrine syringofibroadenomatosis that is reminiscent of EV and is associated with HPV infection (<xref rid="B62" ref-type="bibr">62</xref>).</p></sec><sec id="S4-1-14"><title>Other Settings</title><p>Idiopathic CD4 T cell lymphopenia is associated with increased risk of cutaneous warts (<xref rid="B63" ref-type="bibr">63</xref>), and SCID patients post-HSCT can have an increased risk of warts, especially with specific underlying mutations (<xref rid="B64" ref-type="bibr">64</xref>, <xref rid="B65" ref-type="bibr">65</xref>).</p></sec><sec id="S4-1-15"><title>Management</title><p>Management of cutaneous warts typically progresses from low level removal approaches involving topical therapy (freezing, electrosurgery, curettage, laser, chemical softening, and cantharidin) to immune stimulants (imiquimod and antigens), bleomycin, and antiviral therapy including cidofovir (<xref rid="B66" ref-type="bibr">66</xref>). Genital warts are treated with conceptually the same approach. Management of genital warts also includes special considerations for pregnancy, partners, and screening for malignancy (<xref rid="B67" ref-type="bibr">67</xref>–<xref rid="B69" ref-type="bibr">69</xref>). Interferon a2 and GM-CSF have been used successfully for papillomavirus (<xref rid="B70" ref-type="bibr">70</xref>, <xref rid="B71" ref-type="bibr">71</xref>). In severe cases, therapy can be very unsatisfying. HSCT can result in prompt eradication, though <italic>JAK3</italic> mutations and common γ chain SCID can have significant warts post-HSCT, which may be in part due to poor NK cell function (<xref rid="B64" ref-type="bibr">64</xref>). Topical cidofovir has recently been shown in a case report to be effective in some of these patients (<xref rid="B72" ref-type="bibr">72</xref>). In one case, regression was observed after papillomavirus vaccination (<xref rid="B61" ref-type="bibr">61</xref>).</p></sec></sec><sec id="S4-2"><title>Herpesviridae</title><p>The Herpes family of DNA viruses includes nine viruses pathogenic for humans; CMV, EBV, HHV6a/b, HHV7, HSV1, HSV2, and KSHV, not all of which have skin tropism. Almost any type of T cell dysfunction is associated with an increased frequency of cutaneous HSV. The PIDD with a high likelihood of chronic or disfiguring cutaneous herpes are <italic>DOCK8, GATA2, NEMO/IKBKG, STK4, WAS, STAT1</italic> GOF, and WHIM (<italic>CXCR4</italic> mutations) as described above in association with warts. These same syndromes can manifest with severe primary varicella and an increased frequency and severity of zoster (<xref rid="B73" ref-type="bibr">73</xref>). Varicella and zoster can also be seen in settings with altered proportions of T cell subsets, as in <italic>STAT3</italic> LOF deficient patients (AD-hyper IgE syndrome) (<xref rid="B74" ref-type="bibr">74</xref>) or cytokine signaling defects as seen in <italic>IFNGR1</italic> mutations (<xref rid="B75" ref-type="bibr">75</xref>). Thus, susceptibility to herpes viruses occurs in a broad range of T cells defects and is often part of a complex of susceptibility to many cutaneous viral infections. Herpes viruses can be particularly persistent and cause significant morbidity and mortality. Carcinoma is a feared consequence of recurrent or persistent infection and can be difficult to distinguish from persistently infected skin.</p><sec id="S4-2-1"><title>Management</title><p>Management includes acyclovir, valacyclovir, or famciclovir as initial options. IL-2 therapy has been used successfully in WAS (<xref rid="B76" ref-type="bibr">76</xref>). In WAS, it specifically improves NK cell function (<xref rid="B77" ref-type="bibr">77</xref>). Type I and type II interferons have been used successfully in model systems (<xref rid="B78" ref-type="bibr">78</xref>, <xref rid="B79" ref-type="bibr">79</xref>). Small studies of non-PIDD populations have supported its use in patients (<xref rid="B80" ref-type="bibr">80</xref>–<xref rid="B83" ref-type="bibr">83</xref>). Management should focus on prevention of recurrences and healing of cutaneous lesions. Malignant transformation relates in complex ways to persistence of infection.</p></sec></sec><sec id="S4-3"><title>Poxviridae</title><p>Poxviridae are double stranded DNA viruses. Molluscipoxvirus (i.e., molluscum contagiosum virus or MCV), orthopoxvirus (i.e., smallpox), parapoxvirus, and yatapoxvirus are the four genera that can infect humans. Susceptibility to poxviridae tends to be associated with susceptibility to other cutaneous viral infections. Therefore, many of the disorders described above have an increased susceptibility to poxviridae. Molluscum contagiosum in the most common pox virus infection in humans and in the general population is a self-limited infection with minimal residua (<xref rid="B84" ref-type="bibr">84</xref>). Severe molluscum contagiosum can be seen in <italic>DOCK8</italic> deficiency, <italic>STK4</italic> deficiency (<xref rid="B56" ref-type="bibr">56</xref>), <italic>GATA2, NEMO, STAT1</italic> GOF, and WHIM syndrome. Molluscum can be a significant issue for patients with WAS, as described in the Herpesviridae section. In addition, Orf virus, found in pasture animals, was found in a single patient with <italic>STAT1</italic> GOF (<xref rid="B85" ref-type="bibr">85</xref>). Similar to herpes virus susceptibility described above, molluscum can be seen with nearly any T cell defect and typically arises in that setting as part of a susceptibility to many cutaneous viruses.</p><sec id="S4-3-1"><title>Management</title><p>Initial management of molluscum in a PIDD patient is control of spread through curettage, topical therapy such as salicylate, cantharidin, or immune stimulation with imiquimod (<xref rid="B86" ref-type="bibr">86</xref>, <xref rid="B87" ref-type="bibr">87</xref>). Other topical approaches have also been used successfully. Retreatment 2–4 weeks later is often required. If addressed early, spread may be controlled and the outbreak contained. For diffuse disease or disease that spreads despite all attempts at control, type I interferon (interferon a2) has been suggested (<xref rid="B88" ref-type="bibr">88</xref>, <xref rid="B89" ref-type="bibr">89</xref>). Intralesional immunotherapy with live antigen has been promoted but is contraindicated in PIDD patients with T cell defects (<xref rid="B90" ref-type="bibr">90</xref>, <xref rid="B91" ref-type="bibr">91</xref>).</p></sec></sec><sec id="S4-4"><title>Persistent Vaccine-Stain Rubella Infection</title><p>Three studies have identified persistent vaccine-strain rubella in patients with moderate T cell defects (<xref rid="B91" ref-type="bibr">91</xref>–<xref rid="B93" ref-type="bibr">93</xref>). Most of the patients have had ataxia telangiectasia but a wide range of PIDD diagnoses have been seen. Generally, the patients have had sufficient T cell function to be leading relatively normal lives and the immune deficiency might not even be recognized at the time of the MMR vaccine administration. The manifestations have been largely cutaneous granulomas although chronic inflammation at other sites has been observed (<xref rid="B91" ref-type="bibr">91</xref>). Persistence of virus due to compromised T cell control and acquisition of mutations that may further impact clearance is the proposed mechanism.</p></sec><sec id="S4-5"><title>Diagnostic Considerations for Patients with Cutaneous Viral Infections</title><p>The above conditions are derived from defects in T cell, NK cell, and local tissue immunity. It is therefore nearly impossible to systematically screen for gene defects related to cutaneous viral infection susceptibility. A reasonable start is to define T cells both quantitatively and functionally. If that is unrevealing and the phenotype suggests a PIDD, then whole exome sequencing may be appropriate.</p></sec></sec><sec id="S5"><title>Gastrointestinal (GI) Viral Infections</title><p>Chronic diarrhea (>6 weeks) is a frequent finding in PIDD patients. Given that the etiologies of chronic diarrhea in immunodeficient patients can be diverse, it is important to first distinguish if the diarrhea is infectious, malabsorptive, or inflammatory in nature as there are multiple types of PIDD that can present with autoimmune enteropathy or inflammatory bowel disease (<xref rid="B94" ref-type="bibr">94</xref>–<xref rid="B96" ref-type="bibr">96</xref>). PIDD patients are susceptible to multiple types of GI pathogens, and this section will focus on GI viruses. The concerted action of both the innate and adaptive immune system is necessary for viral clearance (<xref rid="B97" ref-type="bibr">97</xref>, <xref rid="B98" ref-type="bibr">98</xref>). Therefore, there are a number of combined immunodeficiency phenotypes that result in susceptibility to GI viral pathogens, which manifest as prolonged illness as well as prolonged asymptomatic viral shedding.</p><sec id="S5-1"><title>Norovirus</title><p>Persistent infection with norovirus resulting in prolonged viral shedding and symptomatic disease has been noted in patients with SCID and various secondary immunodeficiency states (<xref rid="B99" ref-type="bibr">99</xref>). In a series of pediatric PIDD patients, it was the most frequently isolated virus at 20.6%, with patients with SCID, major histocompatibility complex II deficiency, CD40L deficiency, and agammaglobulinemia represented in this series (<xref rid="B100" ref-type="bibr">100</xref>). Norovirus shedding can be prolonged in the stool of patients who were immunosuppressed following infection and norovirus can be part of multiple infections in the GI tract (<xref rid="B101" ref-type="bibr">101</xref>). In CVID, norovirus infection has been linked to development of severe enteropathy with prolonged viral carriage over the course of years (<xref rid="B102" ref-type="bibr">102</xref>). In several patients in this series, clearance of norovirus resulted in normalization of the GI enteropathy.</p><p>A concern about norovirus is the great difficulty in public health containment. A patient with PIDD who is shedding for a prolonged period of time is not only themselves at risk but also places those around at risk. Norovirus is a common pathogen in the general population, and exposures are therefore common. Norovirus is spread from the moment of illness to several days after clinical recovery. Both vomit and feces can spread virus. The virus lives on surfaces for up to 20 days, and alcohol-based cleaners are not completely effective. Patients with chronic norovirus should use bleach to clean surfaces. Vigorous hand washing with soap and water is also effective.</p></sec><sec id="S5-2"><title>Hepatitis C</title><p>In the early 1990s, the United States FDA recommended that hepatitis C positive donors be excluded from the plasma donor pool resulting in loss of neutralizing hepatitis C viral antibodies from IVIG (<xref rid="B103" ref-type="bibr">103</xref>). Hepatitis C virus (HCV) infection was subsequently reported from several countries, which was due to the presence of contaminating HCV virus from the small numbers of seronegative HCV positive donors (<xref rid="B103" ref-type="bibr">103</xref>–<xref rid="B106" ref-type="bibr">106</xref>). The severity of hepatitis seen in immunodeficient patients was variable, but subsets of patients with primary hypogammaglobulinemia were observed to have a more severe course of hepatitis, which in some cases was rapidly fatal (<xref rid="B103" ref-type="bibr">103</xref>, <xref rid="B105" ref-type="bibr">105</xref>, <xref rid="B106" ref-type="bibr">106</xref>). Younger age and early treatment with IFN were associated with better overall outcomes (<xref rid="B103" ref-type="bibr">103</xref>, <xref rid="B106" ref-type="bibr">106</xref>). Following adoption of PCR screening for HCV and viral inactivation processes with solvent–detergent or pasteurization there have been no subsequent reports of IVIG-associated HCV since 1996 (<xref rid="B107" ref-type="bibr">107</xref>). This cautionary tale supports surveillance of PIDD patients who have risk factors for HCV: blood product exposure, including IV drug use, infants born to HCV positive mothers, high-risk sexual behavior, shared personal items with potential blood exposure among HCV positive individuals. Today, therapy for HCV should improve outcomes compared to the cohort in the early 1990s.</p></sec><sec id="S5-3"><title>Other GI Viruses</title><p>Adenovirus, enterovirus, and rotavirus have been isolated from single PIDD patients with chronic diarrhea, and the true incidence is not known (<xref rid="B100" ref-type="bibr">100</xref>). Chronic rotavirus infection has been described in patients with SCID and agammaglobulinemia (<xref rid="B108" ref-type="bibr">108</xref>). In patients with immunodeficiency, rotavirus can be poorly contained within the GI tract. On investigation at autopsy, active rotavirus replication has been identified in the liver and kidney of patients with SCID, complete DiGeorge syndrome, and acquired-immunodeficiency syndrome, illustrating poor control of viral replication in the setting of profound immunodeficiency (<xref rid="B109" ref-type="bibr">109</xref>). An important consideration is that SCID has been associated with susceptibility to the live rotavirus vaccine (<xref rid="B110" ref-type="bibr">110</xref>). Indeed, vaccine-strain illness is cleared only after immune reconstitution (<xref rid="B110" ref-type="bibr">110</xref>, <xref rid="B111" ref-type="bibr">111</xref>).</p><p>CVID and agammaglobulinemia can rarely have prolonged asymptomatic shedding of vaccine-strain polio following immunization with live-attenuated oral polio vaccine, which can pose risk to other immunocompromised members of the community (<xref rid="B112" ref-type="bibr">112</xref>–<xref rid="B114" ref-type="bibr">114</xref>). Additionally, central nervous system (CNS) infection can occur in agammaglobulinemia (see below). These are the main reasons that live polio vaccination is no longer used in the USA.</p></sec><sec id="S5-4"><title>Management</title><p>Care for chronic GI viral infections in PIDD is primarily supportive: optimizing hydration and nutrition. Orally administered immunoglobulin G (IgG) has been demonstrated to be effective as a therapy for chronic infectious diarrhea in antibody deficient patients (<xref rid="B115" ref-type="bibr">115</xref>, <xref rid="B116" ref-type="bibr">116</xref>). Oral IgG survives passage through the stomach and is bioavailable (<xref rid="B116" ref-type="bibr">116</xref>). Antiviral therapies are untested; however, they could be considered in severe disease.</p></sec></sec><sec id="S6"><title>Viral Infections of the CNS in PIDD</title><p>Viral infections of the CNS confer significant morbidity and mortality in the general population (<xref rid="B117" ref-type="bibr">117</xref>–<xref rid="B119" ref-type="bibr">119</xref>). Therefore, they are not often considered to be indicators of primary immunodeficiency. There are two circumstances where an infection of the CNS is often associated with a primary immunodeficiency: atypical herpes simplex encephalitis and CNS enteroviral disease.</p><sec id="S6-1"><title>Herpes Simplex Encephalitis</title><p>Herpes simplex encephalitis in the general population is most typically seen in newborns and is typically caused by herpes simplex type 2. Infection occurs at the time of delivery and infants present in the second week of life with agitation, obtundation, or seizures. Adults can develop herpes simplex encephalitis (<xref rid="B120" ref-type="bibr">120</xref>). Underlying immune compromise can be a risk factor for adult-onset herpes simplex encephalitis, and today HIV is the most common associated condition in adults. Herpes simplex encephalitis outside of the neonatal period may therefore suggest an immunodeficiency. Among PIDD, defects in the toll-like receptor pathway are most strongly associated with this infection (Table <xref ref-type="table" rid="T3">3</xref>) (<xref rid="B121" ref-type="bibr">121</xref>). Approximately 5% of children with herpes simplex encephalitis have defects in the toll-like receptor pathway (<xref rid="B122" ref-type="bibr">122</xref>). Patients with these defects may present in childhood or adulthood, and some patients with just keratitis have been described (<xref rid="B123" ref-type="bibr">123</xref>). Recognition is important because therapy can be tailored if the defect is known. Surveillance and prevention of relapses is important. Several of these defects are inherited in an AD fashion, and therefore recognition of these PIDD is critical not only for management of the patient but also surveillance for other family members. A population study suggested that there may be additional defects inherited in an AR fashion yet to be defined (<xref rid="B123" ref-type="bibr">123</xref>). A key consideration is that the described toll-like receptor pathway defects are due to loss of local control in the CNS. Antibody and T cell responses are normal, and indeed, local mucosal recurrences are uncommon. As a consequence, testing of the hematopoietic cells is not revealing typically.</p><table-wrap id="T3" position="float"><label>Table 3</label><caption><p>Causes of increased susceptibility to herpes simplex encephalitis.</p></caption><table frame="hsides" rules="groups"><tbody><tr><td align="left" valign="top" rowspan="1" colspan="1"><italic>TLR3</italic> [autosomal dominant (AD)]</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"><italic>TRIF</italic> [autosomal recessive (AR)]</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"><italic>UNC93B1</italic> (AR)</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"><italic>TRAF3</italic> (AD)</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"><italic>TBK1</italic> (AD)</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"><italic>IRF3</italic> (AD)</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"><italic>STAT1</italic> (AR)</td></tr><tr><td align="left" valign="top" rowspan="1" colspan="1"><italic>IKBKG</italic> (XL)</td></tr></tbody></table></table-wrap></sec><sec id="S6-2"><title>Enteroviral Meningoencephalitis</title><p>Viral meningoencephalitis due to a prolonged infection with enterovirus is strongly suggestive of a specific class of PIDD. Enteroviruses are the most common cause of viral meningitis in the general population manifesting as acute onset headache with gradual resolution over days to a few weeks. In patients with agammaglobulinemia, manifestations are quite different (<xref rid="B124" ref-type="bibr">124</xref>). These children typically present with regression of developmental milestones. Ataxia or clumsiness may be noted by parents or on examination. Features early on are subtle, and the slow progression can lead to efforts at mitigation with physical therapy or behavioral strategies. In a patient with a known humoral immune deficiency, the index of suspicion should be high and a workup should not be delayed if there are clear neurologic signs or symptoms. CNS infection in patients with agammaglobulinemia has a very poor prognosis. There can be other phenotypes associated with enteroviral disease in patients with agammaglobulinemia; however, CNS infection is the most common. Dermatomyositis and hepatitis have been described and have progressed in some cases to CNS infection. Treatment for enteroviral disease includes high dose immunoglobulin and when available, drugs directed at enterovirus.</p><p>A unique subset of CNS enteroviral infections occurs in either SCID or agammaglobulinemia with live-attenuated polio vaccine. Wild-type polio, occurring in three serotypes, has been nearly eradicated. Even early on, it was recognized that the live-attenuated vaccine could cause disease (<xref rid="B125" ref-type="bibr">125</xref>) and that patients with hypogammaglobulinemia could excrete virus for years (<xref rid="B126" ref-type="bibr">126</xref>, <xref rid="B127" ref-type="bibr">127</xref>). Currently, circulating wild-type polio is seen only in Afghanistan and Pakistan although virus can be isolated in sewage from other countries supporting ongoing risk for immunodeficient individuals (<xref rid="B128" ref-type="bibr">128</xref>). Vaccine-associated poliomyelitis can be due to infection of an immune deficient individual and spread to the CNS or to revertants of vaccine-strain virus (<xref rid="B129" ref-type="bibr">129</xref>, <xref rid="B130" ref-type="bibr">130</xref>). In the latter case, even normal hosts can have overt paralytic disease. Vaccine-associated poliomyelitis can appear as acute flaccid paralysis or with a meningoencephalitis in immunodeficient individuals. The prognosis has generally been poor (<xref rid="B131" ref-type="bibr">131</xref>).</p></sec><sec id="S6-3"><title>Diagnostic Approaches</title><p>Testing for defects related to herpes simplex encephalitis often involves genetic sequencing although functional analyses are available on a research basis. Table <xref ref-type="table" rid="T3">3</xref> lists the currently recognized genetic causes of susceptibility to herpes simplex encephalitis.</p><p>The diagnosis of enteroviral meningoencephalitis in PIDD patients requires a specific description. In a patient with agammaglobulinemia detection of enterovirus is surprisingly difficult. PCR analysis of cerebrospinal fluid or stool (less specific) should be performed. However, it is not unusual for children with agammaglobulinemia and suggestive clinical features to require a brain biopsy for diagnosis. The biopsy tissue can be tested for enterovirus by PCR. In a patient who presents with CNS enteroviral disease, identification of an immune deficiency is critical because of the prognostic implications. The strong association of CNS enteroviral disease with agammaglobulinemia supports a strategy that begins with enumeration of peripheral blood B cells by flow cytometry. Only if that is negative and there are no other secondary immune deficiencies should alternatives such as CD40L or CVID be sought. A reasonable secondary screen would be to measure immunoglobulin levels and responses to vaccines.</p></sec><sec id="S6-4"><title>Management</title><p>Management of herpes simplex encephalitis requires specific antiviral approaches as well as attention to seizures, increased intracranial pressure, and a comprehensive intensive care approach. Acyclovir delivered intravenously is the cornerstone of management. One should consider a prolonged course of oral therapy after initial management that could include oral acyclovir or valacyclovir because the relapse rate is high in these toll-like receptor pathway defects. The role of steroids is controversial. One small study of immune competent children supported the use of beta-interferon (<xref rid="B132" ref-type="bibr">132</xref>), and it could be argued that interferons specifically mitigate the underlying defect in the toll-like receptor pathway disorders.</p><p>Management of CNS enteroviral disease in agammaglobulinemia has recently been reviewed (<xref rid="B124" ref-type="bibr">124</xref>). In the USA, antiviral drugs are not available, but pocapavir is under study and may become available. High dose IVIG has been proposed as therapeutic, but survival rates remain dismal and functional outcomes are poor.</p></sec></sec><sec id="S7"><title>Summary</title><p>Viral infections are a common cause of morbidity in patients with PIDDs. They can be a clue to the diagnosis when persistent or unusually severe and can represent a significant management challenge.</p></sec><sec id="S8"><title>Author Contributions</title><p>MR, SH, and KS collectively conceived and wrote the manuscript.</p></sec><sec id="S9"><title>Conflict of Interest Statement</title><p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p></sec></body><back><fn-group><fn fn-type="financial-disclosure"><p><bold>Funding.</bold> The Wallace Chair of Pediatrics supports KS. 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