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 Risk factors for community acquired methicillin-resistant Staphylococcus aureus colonization and infection among HIV-infected patients. 

Authors:
Marcos Gabriel Pinheiro1, Maria Teresa Campos Vieira2, F�bio Aguiar-Alves1,3,  Claudete Ara�jo Cardoso2

Institutional affiliations:
P�s Gradua��o em Patologia - Faculdade de Medicina - Universidade Federal Fluminense - Rio de Janeiro � Brazil.
Departamento Materno Infantil - Faculdade de Medicina - Hospital Universit�rio Ant�nio Pedro - P�s Gradua��o em Ci�ncias M�dicas - Universidade Federal Fluminense - Rio de Janeiro � Brazil. 
P�lo Universit�rio de Nova Friburgo - Universidade Federal Fluminense - Rio de Janeiro � Brazil.

Abstract
Staphylococcus aureus is a major pathogen in nosocomial infections. Community acquired methicillin resistant S. aureus (CA-MRSA) is an important agent in infections of skin and soft tissue which can be found among patients without contact to the hospital environment. These bacteria can lead to more serious infections such as polymyositis, myositis, osteomyelitis, endocarditis, septic arthritis, necrotizing pneumonia and necrotizing fasciitis. In HIV-infected patients, S. aureus has significant action causing infections and contributing for their morbidity. Colonization and infection by CA-MRSA of HIV-infected people are more common than in the general population, thus contributing to an increased morbidity and mortality in these patients. This paper is intended to be a review article addressing risk factors for colonization and infection with Staphylococcus aureus among HIV-infected patients. The study has been done with a literature review covering major points related to risk factors for MRSA acquisition, as well as the relationship among HIV-infected patients under highly active antiretroviral therapy (HAART) and MRSA colonization and infection. The evolution of colonization and infection has evolved considerably and became common among HIV-infected patients. The interactions with the immunocompromised host and microrganism are complex and involve defects in immunity of the HIV-infected patient. 

Keywords: HIV, Staphylococcus aureus, MRSA and CA-MRSA.

Introduction
Staphylococcus aureus was firstly reported in 1960s and became one of the major pathogens of nosocomial infections with an increasing prevalence in hospitals worldwide [1, 2].
Infections by methicillin-resistant S. aureus with a source within the community (CA-MRSA) have been observed among patients without risk factors, classically associated with infection. This is a crucial agent of skin and soft tissue infections, which can also lead to severe community-acquired infections such as myositis, polymyositis, osteomyelitis, endocarditis, septic arthritis, necrotizing pneumonia and necrotizing fasciitis. Furthermore, CA-MARSA infections may show high recurrence rates, about 15% in adults and 12-28% in children [3].

Methodology
We searched PubMed (MEDLINE) from 1980 until 2013, using the keywords �HIV�, �Staphylococcus aureus�, �MRSA� and �CA-MRSA� to identify relevant references. We also reviewed major articles on MRSA in the general population to provide comparison data. 

Risk factors for MRSA colonization
In HIV-infected patients, S. aureus has significant action causing infections and contributing for the morbidity of these patients [4]. Colonization of patients HIV-infected occurs more frequently than in the general population, thus contributing to an increased number of infections in such patients [4].
HIV-infected patients are more likely to be colonized by S. aureus than HIV-uninfected subjects [4]. In fact, for the majority of the authors, HIV has been identified as an independent risk factor for methicillin-resistant S. aureus (MRSA) colonization [5].  In this population it has been considered determinant factors for the colonization, as: the immunologic and virologic conditions (low CD4 cell counts <200 cels/mm3 and high HIV viral load); recent antibiotics use and mainly the broad spectrum antibiotic treatment; the presence of central venous catheter and underlying dermatologic disease; illicit drug use; and the duration of hospital stay prior MRSA colonization [5-10]. In contrast, for some authors, there is no consensus if the intravenous drug use, previous MRSA infections and shared towels could be associated with higher risk for MRSA colonization. However, the use of trimethoprim-sulphamethoxazol may have a protective action, decreasing MRSA colonization [6].
Risk factors for MRSA colonization among HIV-infected patients can be mentioned as people of ages and younger men, low CD4 count and high viral load. It Eand beta-lactam antimicrobials might increase the risk for MRSA colonization. Previous hospitalization, use of public restroom, carriers of sexually transmitted diseases and multiple sexual partners were also seen as factors that increase the risk for MRSA colonization [11]. Hospitalization (for any reason other than the skin infection) and ciprofloxacin use (before infection for patient cases) were associated with the MRSA skin infection. HIV-infected men who have sex with men presents a greater risk of MRSA colonization and infection [10]. High blood levels of HIV viral load can also be associated with MRSA colonization and recurrent infections. Intravenous drug use, high risk sexual behavior, compromised immune status and lack of treatment with trimethoprim-sulfamethoxazole prophylaxis can also contribute for MRSA colonization [12].
The incidence of MRSA colonization and infection decreased in HIV-infected patients since the introduction of HAART [11].

HAART therapy and MRSA colonization
After the introduction of the highly active antiretroviral therapy (HAART), in 1996, there was an important decrease in severe immunosupression of the HIV-infected patients. After that, the sociodemographic and behavioural factors became the most significative risk factor determining MRSA colonization and infections, especially among the population of men who have sex with men, with various sexual partners, with no use of condoms and having anonymous sexual activity [4, 7, 11].
Several studies have established a causal relationship between nasal carriers of S. aureus and the subsequent development of staphylococcal infections, demonstrating,   in most cases, that the invasive strain is indistinguishable from colonizing strains. For many authors the nasal colonization by CA-MRSA is correlated with increased risk for developing invasive disease [13-19]. 
Weinke et al have demonstrated a prevalence of S. aureus nasal colonization of about 44% among the HIV-infected patients in comparison with 33% observed in HIV-uninfected patients [20]. Recently, Chacko et al observed that 46 (76.7%) of the 60 HIV-infected patients studied were colonized by S. aureus [5]. The importance of this colonization in HIV-infected patients is due to the increased morbidity and mortality caused by this pathogen in this group of patients and mainly because that the colonization increases the risk for infection. Frequently, the infection is caused by the same colonizing strain [6].
	The prevalence of the colonization among HIV-infected patients varies from 1.6 to 34.8%, depending on the population studied, with the highest prevalence been observed among in-patients (17-34%) when compared with out-patients (0-17%) [21-23]. In a retrospective study of 900 HIV-infected out-patients,  Ramsetty et al noted that 72 (8%) patients were colonized by MRSA and that 15% (55.5%) of them developed MRSA infection subsequently, mostly skin and soft tissue infectious (SSTIs) [9].  
In the HAART era the prevalence of MRSA colonization has decreased and is about 4% (0-17%) while in general population it�s about 1.5% [24]. The MRSA colonization can occur in different sites like nasopharynx, genital and perianal areas and can be persistent or intermittent. In 2009, Shet et al showed that the chance of detection of MRSA nasal colonization among HIV-infected patients increases when nares cultures are repeated in three different moments in time [6]. So, if only a single sample is collected, the rate for missing true carriers increases up to 20%, probably due to the occurrence of intermittent MRSA colonization. In fact, in recent studies, about 38-39% of the subjects were persistent carriers while about 62% showed an intermittent standard of colonization [4, 21, 25]. 

MRSA and invasive infections
Another controversial point is if MRSA colonization always precedes MRSA infections in general population. For the majority of the studies among HIV-infected patients there is a high association between MRSA colonization and subsequent infection, especially in the case of perianal MRSA colonization and the development of SSTIs. The infecting and colonizing strains were usually identical, as showed by Pulsed-gel electrophoresis (PGPE) [6, 12, 26, 27]. In fact, MRSA infections have increased among HIV-infected patients and can be 6 to 18-fold more frequent in this population in comparison with HIV-uninfected persons. About 17% of all S. aureus infections in HIV-infected patients are due to MRSA [28-30]. The most common infection in this population is SSTIs and CA-MRSA strains are the main etiologic agents. The clinical presentation of SSTIs is represented by abscesses and also cellulitis, furuncles, folliculitis, ulcerations, impetigo and necrotizing fasciitis. In the HAART era, about 85% of MRSA infection in HIV-infected patients is SSTIs [31]. It affects predominantly the extremities but nowadays it has been described more frequently in perigenital areas, associated with high-risk sexual behavior [32]. 
MRSA also causes bacteremia mainly in HIV-infected patients with CD4 count <200cels/mm3, injection drug use and severe kidney disease [11, 33-35]. Bacteremia increases the risk of endocarditis [4]. Other invasive infections among HIV-infected patients caused by MRSA include osteomyelitis, meningitis, pericarditis, necrotizing pneumonia, renal abscess, joint infection and septic pulmonary emboli [25, 36]. In the HAART era the risk of bacteremia among HIV-infected patients has decreased although it still remains 16-fold higher in comparison with HIV-uninfected persons [38]. It depends on the immune status being low CD4 counts and high HIV viral load associated with increased risk for CA-MRSA infections [4, 39]. Despite these data, the risk of CA-MRSA infections remains high among HIV-infected patients even with better results for CD4 cells counts [4, 39, 43]. Ramsetty et al noted a reduction of 84% in the risk for MRSA colonization or infection in HIV-infected receiving HAART [9].  
The recurrence of MRSA infections is more commonly observed among HIV-infected patients [12, 40]. Diep et al in a cohort study with HIV-infected patients found a recurrence rate about 71% [41, 42]. In the HAART era with the decreased HIV viral load serum levels and the elevation of the CD4 levels it is expected a dramatic decrease in the recurrence of MRSA infections. However, elevated recurrence rates continues to occur even among those patients with high CD4 cell counts, suggesting that there must be other factors associated. In fact, the increase in MRSA colonization among patients with high-risk sexual behavior and drug use, leading to more frequent hospitalization could explain the recurrence of MRSA infections within this population [7, 40, 43].

Immune factors of HIV-infected patients with MRSA
 	The first cell line in host defense against S. aureus is composed by neutrophils. Monocytes and B lymphocytes can also be affected by the HIV infection. HIV-infected patients show an important neutrophils dysfunction. Many functions of the neutrophils can be affected by the HIV infection like the neutrophils chemotaxis, the adhesion capacity to the endothelium, the neutrophils phagocytosis, the number of neutrophils and the neutrophils apoptosis. Ellis and colleagues in 1988 demonstraded a reduction of more than 45% in neutrophils� chemotaxis among HIV-infected patients in comparison with healthy controls. Since in asymptomatic HIV patients, the reduction of neutrophils� chemotaxis was 29.8% in comparison with the healthy controls [44]. It can also occur an important increase in deregulation of L-selectin expression with the decrease of CD4 counts. The L-selectin is an adhesion molecule necessary to the adhesion of the neutrophils to the endothelium. Murphy et al have also demonstrated that it can occur an important decrease in the phagocytic oxidative capacity of neutrophils in HIV-infected, determining a reduced capacity of intracellular bacterial killing [45].
  Neutropenia observed in HIV-infected patients is due to multifactorial factors like treatment-related toxicities, nutritional deficiency and bone marrow invasion of opportunistic infections [44, 46]. Patients HIV-infected have an important decrease in viability of the neutrophils occurring an accelerated apoptosis, probably due to the oxidative stress caused by HIV conditions [47]. 
In HIV-infected individuals it is also possible to be observed an important decrease in monocyte chemotaxis and abnormalities in B-lymphocytes functions with a production of dysfunctional antibodies. Both factors lead HIV-infected patients to a   higher risk for bacterial infections in comparison with HIV-uninfected persons [4, 48, 49].      

HIV X MRSA X children
HIV-infected children are exposed to multiple antimicrobial agents and about 30% of those are also receiving HAART due to low CD4 count. Several episodes of opportunistic infections lead to the use of multiple classes of antimicrobials, therefore children HIV-infected have greater ease of acquiring these infections than those who are not [50].
Several factors seem to be crucial for the nasal carrier state of CA-MRSA in healthy children, such as age (higher prevalence in patients older than two years), greater number of siblings, family size (considering crowding in residence as a risk factor for colonization), day care attendance, close physical contact between children and caregivers, maternal smoking, low maternal education and behavioral traits that favor the contact [51, 52].
Behavioral habits that favor a strict physical contact provide an increased frequency of respiratory or skin infections. Most often, these infectious episodes are treated with antibiotics, which have made   these sites conducive environments for selection and amplification of pathogens resistance [53].
MRSA infections among children and young adults have increased due to certain risk factors such as prolonged hospitalization, recent surgery and indwelling catheter. Community-associated MRSA (CA-MRSA) infections have affected high rates of children, predominantly on hospital infections MRSA (HA-MRSA), and the immunodeficiency is the main mediator of MRSA infections occurrence in HIV-infected children and adolescents [54].
Bacterial diseases have a significant morbidity and mortality among children worldwide and S. aureus has been recognized as a major cause of these infections in community and hospital environments. Although bacterial infections are a major cause of morbidity and mortality, data for causing organisms and comparisons of HIV-infected and uninfected are limited [55].

Therapy for MRSA in HIV-infected patients
Antimicrobials as clindamicyn, doxycycline, and trimethoprim-sulfamethoxazole (TMP-SMX) are recommended for empirical treatment of CA-MRSA skin and soft tissue infections. Usually TMP-SMX is more frequently used against CA-MRSA isolates [34]. 
TMP-SMX is used for immunosuppressed HIV-infected adults and children as prophylactic therapy in opportunistic infections. The correct use of antiretroviral drugs has reduced the importance of TMP-SMX prophylaxis in developed countries. In places that coverage antiretroviral therapy is limited and there is confirmation of HIV infection in children 18 months old, using TMP-SMX prophylaxis remains vital in treating these infections.
The cost-effectiveness and drug resistance has been discussed in some places as a negative point regarding the use. There is also the question regarding the induction of microbial resistance to other classes of antibiotics. Nevertheless, the remaining vision is that TMP-SMX reduces the development of multidrug resistance by preventing infection with hospitalization and exposure to other antibiotics [56].

Conclusion
The epidemiology of MRSA has evolved in both colonization and infection as became common among HIV-infected patients. Behavioral, social, environmental, biologic, host HIV-specific risk factors, and, probably, the combination of all these, play a key role in explaining significant increased prevalence and the incidence observed worldwide. The interactions with the immunocompromised host organism are complex and involve defects of immunity related to HIV-infected patients.
Patients HIV-infected have a higher risk of acquiring MRSA infection than patients HIV-uninfected.
Although CA-MRSA infection has been reported independently of immune status or HAART use, the risk appears to be higher in severely immunossupressed patients.


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