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Cytomegalovirus Infections in Solid Organ Transplantation: a Review

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Cytomegalovirus Infections in Solid Organ Transplantation: a Review Review Article Infection & http://dx.doi.org/10.3947/ic.2013.45.3.260 Infect Chemother 2013;45(3):260-271 Chemotherapy pISSN 2093-2340 · eISSN 2092-6448 Cytomegalovirus Infections in Solid Organ Transplantation: A Review Poornima Ramanan, and Raymund R Razonable Division of Infectious Diseases, Department of Medicine and the William J von Liebig Transplant Center Mayo Clinic, Rochester, Minnesota 55905, USA Cytomegalovirus (CMV) continues to have a tremendous impact in solid organ transplantation despite remarkable advances in its diagnosis, prevention and treatment. It can affect allograft function and increase patient morbidity and mortality through a number of direct and indirect effects. Patients may develop asymptomatic viremia, CMV syndrome or tissue-invasive disease. Late-onset CMV disease continues to be a major problem in high-risk patients after completion of antiviral prophylaxis. Emerg- ing data suggests that immunologic monitoring may be useful in predicting the risk of late onset CMV disease. There is now increasing interest in the development of an effective vaccine for prevention. Novel antiviral drugs with unique mechanisms of action and lesser toxicity are being developed. Viral load quantification is now undergoing standardization, and this will permit the generation of clinically relevant viral thresholds for the management of patients. This article provides a brief overview of the contemporary epidemiology, clinical presentation, diagnosis, prevention and treatment of CMV infection in solid organ trans- plant recipients. Key Words: Cytomegalovirus, Transplant, Diagnosis, Prevention, Treatment Introduction cluding transplant recipients. In order to reduce the impact of CMV on transplant outcomes, there have been remarkable ef- Human cytomegalovirus (CMV) is a member of the Beta- forts to improving its diagnosis, prevention, and treatment. herpesvirinae subfamily under the Herpesviridae family [1]. Despite these significant advances in its diagnosis and thera- Discovered in the 1950s [2, 3], CMV is one of the largest py, CMV continues to have a major impact on patient and al- known human viruses [4]. While most infections in immuno- lograft survival among solid organ transplant (SOT) recipients competent individuals are benign and self-limited, CMV is an through a variety of direct and indirect effects. important cause of morbidity and mortality in individuals with underdeveloped or compromised immune function, in- Received: June 26, 2013 Corresponding Author : Raymund R Razonable Division of Infectious Diseases, Department of Medicine and the William J von Liebig Transplant Center, Mayo Clinic, 200 First Street SW Rochester, Minnesota 55905, USA Tel: +01-507-284-3747, Fax: +01-507-255-7767 E-mail: [email protected] This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and repro- duction in any medium, provided the original work is properly cited. Copyrights © 2013 by The Korean Society of Infectious Diseases | Korean Society for Chemotherapy www.icjournal.org www.icjournal.org http://dx.doi.org/10.3947/ic.2013.45.3.260 • Infect Chemother 2013;45(3):260-271 261 Epidemiology nor and recipient, the type of organ transplanted, the net state of the host immunosuppression and viral factors. Patients CMV is a ubiquitous virus, with a worldwide distribution. without immunity against CMV-seronegative (R-) who receive Infection is usually acquired early in life through contact with an organ transplant from CMV seropositive donor (D+) are at infected body fluids such as saliva. The seroprevalence of highest risk of primary CMV disease resulting from the reacti- CMV varies geographically and is higher in developing coun- vation of latent virus transmitted in the allograft [12]. The tries, with rates reaching up to 100%, likely resulting from “high-risk” D+/R- patients lack the ability to mount an effec- poor socio-economic status and over-crowding which facili- tive immune response against CMV due to pharmacological tate viral transmission through close contacts [5]. In the Unit- immunosuppression and therefore, carry the highest risk of ed States, the CMV seroprevalence is about 50% among acquiring CMV infection and disease after solid organ trans- adults, although it is higher in women, older individuals, and plantation. those with lower household income [6]. Lung and small bowel transplant recipients carry a higher CMV establishes lifelong latency in a variety of cells follow- risk of acquiring CMV disease compared to kidney and liver ing primary infection, which may lead to reactivation and in- transplant recipients; this may be explained by the intensity of termittent viral shedding. Prior to implementation of wide- immunosuppression and the amount of lymphoid tissue spread routine CMV prophylaxis among SOT recipients, CMV transplanted [13, 14]. disease typically occurs during the first three months after Transplant recipients who are severely immunocompro- transplantation. The epidemiology has changed, as late-onset mised are at higher risk of CMV disease. The net state of im- CMV disease has emerged in high-risk CMV donor-positive/ munosuppression is a dynamic entity that is influenced by recipient-negative (D+/R-) patients after the completion of an- many determinants such as the dose, duration and type of im- tiviral prophylaxis. The incidence of CMV infection and dis- munosuppressive agents, innate and adaptive host immune ease varies by the type of organ transplant, the serostatus of defects, age, and underlying comorbidities [15]. The use of donor and recipient, and the prevention strategies used. In a lymphocyte depleting agents such as anti-lymphocyte globu- recent study involving kidney and liver transplant recipients lin (ALG), anti-thymocyte globulin (ATG), OKT3 (anti CD3 who received valganciclovir prophylaxis, the 1-year incidence antibody) and alemtuzumab (anti-CD52 antibody) inhibit of CMV disease was 19.2% and 31.3%, respectively in D+/R- CMV specific immune reconstitution and have been associat- group, but was only 2.5% and 3.2%, respectively, in D-/R- group ed with increased risk of CMV disease[12, 16, 17], especially if [7]. In heart recipients who received universal antiviral pro- they are used for the treatment of acute allograft rejection phylaxis in the first month after transplant followed by pre- [18]. emptive therapy, the cumulative incidence of CMV infection There is a bidirectional relationship between CMV and al- and disease during the first year was 47% and 7.5% (3.6% in lograft rejection [12]. Allograft rejection creates a pro-inflam- low risk and 25% in high risk group), respectively [8]. The inci- matory environment that can reactivate CMV, and the treat- dence of CMV disease among lung transplant recipients who ment for allograft rejection severely impairs the ability to received antiviral prophylaxis for 6 to 12 months was 14.9%, mount an immune response to control viral replication. Al- with a higher incidence (26.6%) in D+/R- group [9]. Most cases lograft rejection was strongly associated with the occurrence of CMV disease in patients who received antiviral prophylaxis of late onset CMV disease in CMV D+/R- liver and kidney occur after cessation of antiviral drug administration, hence transplant patients [18]. Conversely, CMV upregulates anti- the term “late-onset CMV disease”, and they occur predomi- gens, and this results in alloreactivity and facilitates allograft nantly in CMV mismatch (D+/R-) SOT recipients. Late-onset rejection. CMV disease remains associated with allograft failure and Some newer immunosuppressive drugs have been associat- mortality [10, 11]. ed with a lower risk of CMV infection. In particular, the use of mTOR inhibitors such as everolimus has been associated with a lower risk of CMV infection and disease [19]. Infection with Risk factors other herpes viruses (HHV-6 and HHV-7) may predispose to CMV disease, but does not have any effect on clinical out- The risk of acquiring CMV disease in SOT recipients de- come [20]. pends on a number of factors such as the serostatus of the do- Defects in innate immune responses have been associated 262 Ramanan P, et al. • CMV in SOT recipients www.icjournal.org with increased risk of CMV infection and disease in SOT re- organ transplanted, CMV disease can manifest as hepatitis, cipients, whose adaptive immune responses are rendered in- nephritis, pneumonitis, myocarditis and pancreatitis in liver, effective by immunosuppressive drugs. Examples of innate or kidney, lung, heart and pancreas transplant recipients, respec- CMV-specific immune defects include Toll-like receptor (TLR) tively [12]. gene polymorphisms, mannose binding lectin (MBL) defi- CMV is known to cause a number of indirect effects due to ciency or polymorphism [21, 22], chemokine and cytokine de- its immunomodulatory properties [32, 33]. This property has fects including increased IL-10 expression [23], deficiency in been implicated in the association between CMV and the in- CMV-specific CD4+ and CD8+ T cells [24, 25], programmed creased risk of bacteremia [34], invasive fungal infections [35], cell death 1 [23] and immune evasion genes expression [26] . recurrent hepatitis C after liver transplant [36] and malignan- TLRs are part of innate immunity that detect a broad range of cies such as Ebstein-Barr virus (EBV) associated post-trans- pathogens. TLR2 recognizes
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