Immune activation is associated with increased gut microbial translocation in treatment-naive, HIV-infected children in a resource-limited setting

Journal of Acquired Immune Deficiency Syndromes

Volumn 66, Issue 1, 2014, Pages 16-24

  Pilakka Kanthikeel, Sudheesh ^a,c   Kris, Arheart ^a   Selvaraj, Anbalagan ^b   Swaminathan, Soumya ^b   Pahwa, Savita ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b INDIAN COUNCIL OF MEDICAL RESEARCH   (India)

^c FLORIDA INTERNATIONAL UNIVERSITY   (United States)

Author keywords

16S rDNA; HIV infected children; LPS; microbial translocation

Indexed keywords

DNA 16S; LIPOPOLYSACCHARIDE;

ARTICLE; CD4 LYMPHOCYTE COUNT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHILD; COHORT ANALYSIS; CONTROLLED STUDY; DNA SEQUENCE; EXHAUSTION; FEMALE; FOLLOW UP; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE ACTIVATION; IMMUNE EXHAUSTION; IMMUNOREACTIVITY; INFANT; INTESTINE FLORA; MAJOR CLINICAL STUDY; MALE; MICROBIAL TRANSLOCATION; PERINATAL PERIOD; PRIORITY JOURNAL; VIRUS LOAD;

ADOLESCENT; ANTIGENS, CD14; BACTERIAL TRANSLOCATION; CD4 LYMPHOCYTE COUNT; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CHILD; CHILD, PRESCHOOL; DNA, BACTERIAL; DNA, RIBOSOMAL; FEMALE; GASTROINTESTINAL TRACT; HIV INFECTIONS; HUMANS; INFANT; LIPOPOLYSACCHARIDES; MALE; VIRAL LOAD;

EID: 84898547210     PISSN: 15254135     EISSN: 10779450     Source Type: Journal    
DOI: 10.1097/QAI.0000000000000096     Document Type: Article

References (51)

1. Kotler DP, Reka S, Clayton F. Intestinal mucosal inflammation associated with human immunodeficiency virus infection. Dig Dis Sci. 1993; 38:1119-1127.
2. Heise C, Miller CJ, Lackner A, et al. Primary acute simian immunodeficiency virus infection of intestinal lymphoid tissue is associated with gastrointestinal dysfunction. J Infect Dis. 1994;169:1116-1120.
3. Jiang W, Lederman MM, Hunt P, et al. Plasma levels of bacterial DNA correlate with immune activation and the magnitude of immune restoration in persons with antiretroviral-treated HIV infection. J Infect Dis. 2009;199:1177-1185.
4. Ancuta P, Kamat A, Kunstman KJ, et al. Microbial translocation is associated with increased monocyte activation and dementia in AIDS patients. PLoS One. 2008;3:e2516.
5. Brenchley JM, Price DA, Schacker TW, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med. 2006;12:1365-1371.
6. Cassol E, Malfeld S, Mahasha P, et al. Persistent microbial translocation and immune activation in HIV-1-infected South Africans receiving combination antiretroviral therapy. J Infect Dis. 2010;202:723-733.
7. Giorgi JV, Hultin LE, McKeating JA, et al. Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J Infect Dis. 1999;179:859-870.
8. Fahey JL, Taylor JM, Manna B, et al. Prognostic significance of plasma markers of immune activation, HIV viral load and CD4 T-cell measurements. AIDS. 1998;12:1581-1590.
9. Marchetti G, Bellistri GM, Borghi E, et al. Microbial translocation is associated with sustained failure in CD4+ T-cell reconstitution in HIVinfected patients on long-term highly active antiretroviral therapy. AIDS. 2008;22:2035-2038.
10. Rajasuriar R, Booth D, Solomon A, et al. Biological determinants of immune reconstitution in HIV-infected patients receiving antiretroviral therapy: the role of interleukin 7 and interleukin 7 receptor alpha and microbial translocation. J Infect Dis. 2010;202:1254-1264.
11. Mavigner M, Cazabat M, Dubois M, et al. Altered CD4+ T cell homing to the gut impairs mucosal immune reconstitution in treated HIV-infected individuals. J Clin Invest. 2012;122:62-69.
12. Wallet MA, Rodriguez CA, Yin L, et al. Microbial translocation induces persistent macrophage activation unrelated to HIV-1 levels or T-cell activation following therapy. AIDS. 2010;24:1281-1290.
13. Papasavvas E, Pistilli M, Reynolds G, et al. Delayed loss of control of plasma lipopolysaccharide levels after therapy interruption in chronically HIV-1-infected patients. AIDS. 2009;23:369-375.
14. Kramski M, Gaeguta AJ, Lichtfuss GF, et al. Novel sensitive real-time PCR for quantification of bacterial 16S rRNA genes in plasma of HIVinfected patients as a marker for microbial translocation. J Clin Microbiol. 2011;49:3691-3693.
15. Kestens L, Vanham G, Gigase P, et al. Expression of activation antigens, HLA-DR and CD38, on CD8 lymphocytes during HIV-1 infection. AIDS. 1992;6:793-797.
16. Levacher M, Hulstaert F, Tallet S, et al. The significance of activation markers on CD8 lymphocytes in human immunodeficiency syndrome: staging and prognostic value. Clin Exp Immunol. 1992;90:376-382.
17. Day CL, Kaufmann DE, Kiepiela P, et al. PD-1 expression on HIVspecific T cells is associated with T-cell exhaustion and disease progression. Nature. 2006;443:350-354.
18. Sachdeva M, Fischl MA, Pahwa R, et al. Immune exhaustion occurs concomitantly with immune activation and decrease in regulatory T cells in viremic chronically HIV-1-infected patients. J Acquir Immune Defic Syndr. 2010;54:447-454.
19. Anderson KV. Toll signaling pathways in the innate immune response. Curr Opin Immunol. 2000;12:13-19.
20. Marchetti G, Tincati C, Silvestri G. Microbial translocation in the pathogenesis of HIV infection and AIDS. Clin Microbiol Rev. 2013;26:2-18.
21. Kourtis AP, Ibegbu CC, Wiener J, et al. Role of intestinal mucosal integrity in HIV Transmission to infants through Breast-feeding: the BAN study. J Infect Dis 2013;208:653-661.
22. Sherman MP. New concepts of microbial translocation in the neonatal intestine: mechanisms and prevention. Clin Perinatol. 2010;37:565-579.
23. Papasavvas E, Azzoni L, Foulkes A, et al. Increased microbial translocation in #180 days old perinatally human immunodeficiency virus-positive infants as compared with human immunodeficiency virus-exposed uninfected infants of similar age. Pediatr Infect Dis J. 30:877-882.
24. Pilakka-Kanthikeel S, Huang S, Fenton T, et al. Increased gut microbial translocation in HIV-infected children persists in virologic responders and virologic failures after antiretroviral therapy. Pediatr Infect Dis J. 2012;31:583-591.
25. Anselmi A, Vendrame D, Rampon O, et al. Immune reconstitution in human immunodeficiency virus type 1-infected children with different virological responses to anti-retroviral therapy. Clin Exp Immunol. 2007; 150:442-450.
26. Baroncelli S, Galluzzo CM, Pirillo MF, et al. Microbial translocation is associated with residual viral replication in HAART-treated HIV+ subjects with, 50copies/ml HIV-1 RNA. J Clin Virol. 2009; 46:367-370.
27. CDC. WHO case definitions of HIV for surveillance and revised clinical staging and immunological classification of HIV-related disease in adults and children. Geneva, Switzerland: World Health Organization; 2007.
28. Selvaraj A, Kanthikeel SP, Pk B, et al. Defective dendritic cell response to toll like receptor 7/8 agonists in perinatally HIV infected children. Pathog Dis. 2013;69:184-193.
29. Luzuriaga K, Sullivan JL. Pediatric HIV-1 infection: advances and remaining challenges. AIDS Rev. 2002;4:21-26.
30. de Martino M, Tovo PA, Galli L, et al. Prognostic significance of immunologic changes in 675 infants perinatally exposed to human immunodeficiency virus. The Italian Register for Human Immunodeficiency Virus Infection in Children. J Pediatr. 1991;119:702-709.
31. Hainline C, Taliep R, Sorour G, et al. Early Antiretroviral Therapy reduces the incidence of otorrhea in a randomized study of early and deferred antiretroviral therapy: evidence from the Children with HIV Early Antiretroviral Therapy (CHER) Study. BMC Res Notes. 2011;26: 448.
32. Laughton B, Cornell M, Grove D, et al. Early antiretroviral therapy improves neurodevelopmental outcomes in infants. AIDS. 2010;26:1685-1690.
33. Leinert C, Stahl-Hennig C, Ecker A, et al. Microbial translocation in simian immunodeficiency virus (SIV)-infected rhesus monkeys (Macaca mulatta). J Med Primatol. 39:243-251.
34. Fitzgerald F, Harris K, Doyle R, et al. Short communication: Evidence that microbial translocation occurs in HIV-infected children in the United Kingdom. AIDS Res Hum Retroviruses. 2013;29:1589-1593.
35. Marchetti G, Cozzi-Lepri A, Merlini E, et al. Microbial translocation predicts disease progression of HIV-infected antiretroviral-naive patients with high CD4+ cell count. AIDS. 2011;25:1385-1394.
36. Lopez M, Soriano V, Peris-Pertusa A, et al. Elite controllers display higher activation on central memory CD8 T cells than HIV patients successfully on HAART. AIDS Res Hum Retroviruses. 2011;27:157- 165.
37. Hunt PW, Brenchley J, Sinclair E, et al. Relationship between T cell activation and CD4+ T cell count in HIV-seropositive individuals with undetectable plasma HIV RNA levels in the absence of therapy. J Infect Dis. 2008;197:126-133.
38. Guadalupe M, Reay E, Sankaran S, et al. Severe CD4+ T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration following highly active antiretroviral therapy. J Virol. 2003;77:11708-11717.
39. Poles MA, Boscardin WJ, Elliott J, et al. Lack of decay of HIV-1 in gutassociated lymphoid tissue reservoirs in maximally suppressed individuals. J Acquir Immune Defic Syndr. 2006;43:65-68.
40. Brenchley JM, Schacker TW, Ruff LE, et al. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med. 2004;200:749-759.
41. Brenchley JM, Douek DC. The mucosal barrier and immune activation in HIV pathogenesis. Curr Opin HIV AIDS. 2008;3:356-361.
42. Balagopal A, Philp FH, Astemborski J, et al. Human immunodeficiency virus-related microbial translocation and progression of hepatitis C. Gastroenterology. 2008;135:226-233.
43. Appay V, Sauce D. Immune activation and inflammation in HIV-1 infection: causes and consequences. J Pathol. 2008;214:231-241.
44. Estes JD, Harris LD, Klatt NR, et al. Damaged intestinal epithelial integrity linked to microbial translocation in pathogenic simian immunodeficiency virus infections. PLoS Pathog. 2010;6:e1001052.
45. Salgado M, Rallon NI, Rodes B, et al. Long-term non-progressors display a greater number of Th17 cells than HIV-infected typical progressors. Clin Immunol. 2011;139:110-114.
46. Vesterbacka J, Nowak P, Barqasho B, et al. Kinetics of microbial translocation markers in patients on efavirenz or lopinavir/r based antiretroviral therapy. PLoS One. 2013;8:e55038.
47. Redd AD, Dabitao D, Bream JH, et al. Microbial translocation, the innate cytokine response, and HIV-1 disease progression in Africa. Proc Natl Acad Sci U S A. 2009;106:6718-6723.
48. Anas A, van der Poll T, de Vos AF. Role of CD14 in lung inflammation and infection. Crit Care. 2010;14:209.
49. Ayaslioglu E, Kalpaklioglu F, Kavut AB, et al. The role of CD14 gene promoter polymorphism in tuberculosis susceptibility. J Microbiol Immunol Infect. 2013;46:158-163.
50. Sauce D, Almeida JR, Larsen M, et al. PD-1 expression on human CD8 T cells depends on both state of differentiation and activation status. AIDS. 2007;21:2005-2013.
51. Agata Y, Kawasaki A, Nishimura H, et al. Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes. Int Immunol. 1996;8:765-772.