• 1.

    Sun HY, Sheng WH, Tsai MS, Lee KY, Chang SY, Hung CC, 2014. Hepatitis B virus coinfection in human immunodeficiency virus-infected patients: a review. World J Gastroenterol 20: 1459814614.

    • Search Google Scholar
    • Export Citation
  • 2.

    Huang AJ, Núñez M, 2015. Outcomes in HIV/HBV-coinfected patients in the tenofovir era are greatly affected by immune suppression. J Int Assoc Provid AIDS Care 14: 360368.

    • Search Google Scholar
    • Export Citation
  • 3.

    Alemu A, Shiferaw Y, Addis Z, Mathewos B, Birhan W, 2013. Effect of malaria on HIV/AIDS transmission and progression. Parasit Vectors 6: 18.

  • 4.

    Morgado MG, Barcellos C, Pina MF, Bastos FI, 2000. Human immunodeficiency virus/acquired immunodeficiency syndrome and tropical diseases: a Brazilian perspective. Mem Inst Oswaldo Cruz 95 (Suppl 1): 145151.

    • Search Google Scholar
    • Export Citation
  • 5.

    Harms G, Feldmeier H, 2005. The impact of HIV infection on tropical diseases. Infect Dis Clin North Am 19: 121135.

  • 6.

    World Health Organization, 2014. Dengue and Severe Dengue [Internet]. Updated March 2014. Available at: http://www.who.int/mediacentre/factsheets/fs117/en/.

    • Search Google Scholar
    • Export Citation
  • 7.

    Weaver SC, Vasilakis N, 2009. Molecular evolution of dengue viruses: contributions of phylogenetics to understanding the history and epidemiology of the preeminent arboviral disease. Infect Genet Evol 9: 523540.

    • Search Google Scholar
    • Export Citation
  • 8.

    Watt G, Kantipong P, Jongsakul K, 2003. Decrease in human immunodeficiency virus type 1 load during acute dengue fever. Clin Infect Dis 36: 10671069.

    • Search Google Scholar
    • Export Citation
  • 9.

    Gonzalez D, Limonta D, Bandera JF, Perez J, Kouri G, Guzman MG, 2009. Dual infection with dengue virus 3 and human immunodeficiency virus 1 in Havana, Cuba. J Infect Dev Ctries 3: 318320.

    • Search Google Scholar
    • Export Citation
  • 10.

    Siong WC, Ching TH, Jong GC, Pang CS, Vernon LJ, Sin LY, 2008. Dengue infections in HIV patients. Southeast Asian J Trop Med Public 39: 260265.

  • 11.

    Mendes W da S, Branco M dos R, Medeiros MN, 2006. Clinical case report: dengue hemorrhagic fever in a patient with acquired immunodeficiency syndrome. Am J Trop Med Hyg 74: 905907.

    • Search Google Scholar
    • Export Citation
  • 12.

    Pang J, Thein TL, Lye DC, Leo YS, 2015. Differential clinical outcome of dengue infection among patients with and without HIV infection: a matched case-control study. Am J Trop Med Hyg 92: 11561162.

    • Search Google Scholar
    • Export Citation
  • 13.

    Torrentes-Carvalho A, Hottz ED, Marinho CF, da Silva JB, de Oliveira Pinto LM, Fialho LG, Bozza FA, Cunha RV, Damasco PV, Kubelka CF, de Azeredo EL, 2016. Characterization of clinical and immunological features in patients coinfected with dengue virus and HIV. Clin Immunol 164: 95105.

    • Search Google Scholar
    • Export Citation
  • 14.

    Soriano V, Poveda E, Vispo E, Barreiro P, 2013. Hepatitis B in HIV-infected patients. Clin Liver Dis 17: 489501.

  • 15.

    Samanta J, Sharma V, 2015. Dengue and its effects on liver. World J Clin Cases 3: 125131.

  • 16.

    Agarwal MP, Giri S, Sharma V, Roy U, Gharsangi K, 2011. Dengue causing fulminant hepatitis in a hepatitis B virus carrier. Biosci Trends 5: 4445.

  • 17.

    Tang Y, Kou Z, Tang X, Zhang F, Yao X, Liu S, Jin X, 2008. Unique impacts of HBV co-infection on clinical and laboratory findings in a recent dengue outbreak in China. Am J Trop Med Hyg 79: 154158.

    • Search Google Scholar
    • Export Citation
  • 18.

    Wan Z, Xie G, Wu Y, Liu F, Xin S, You S, Liu H, Li C, Li D, 2016. Cytokines elevated in patients with HBV-related acute-on-chronic liver failure promote NK cell mediated cytotoxicity through TRAIL. Dig Liver Dis 48: 528535.

    • Search Google Scholar
    • Export Citation
  • 19.

    Law WP, Duncombe CJ, Mahanontharit A, Boyd MA, Ruxrungtham K, Lange JM, Phanuphak P, Cooper DA, Dore GJ, 2004. Impact of viral hepatitis co-infection on response to antiretroviral therapy and HIV disease progression in the HIV-NAT cohort. AIDS 18: 11691177.

    • Search Google Scholar
    • Export Citation
  • 20.

    Stylianou E, Aukrust P, Kvale D, Müller F, Frøland SS, 1999. IL-10 in HIV infection: increasing serum IL-10 levels with disease progression—down-regulatory effect of potent anti-retroviral therapy. Clin Exp Immunol 116: 115120.

    • Search Google Scholar
    • Export Citation
  • 21.

    Aukrust P, Müller F, Lien E, Nordoy I, Liabakk NB, Kvale D, Espevik T, Frøland SS, 1999. Tumor necrosis factor (TNF) system levels in human immunodeficiency virus-infected patients during highly active antiretroviral therapy: persistent TNF activation is associated with virologic and immunologic treatment failure. J Infect Dis 179: 7482.

    • Search Google Scholar
    • Export Citation
  • 22.

    Malavige GN, Huang LC, Salimi M, Gomes L, Jayaratne SD, Ogg GS, 2012. Cellular and cytokine correlates of severe dengue infection. PLoS One 7: e50387.

  • 23.

    McLinden JH, Stapleton JT, Chang Q, Xiang J, 2008. Expression of the dengue virus type 2 NS5 protein in a CD4+ T cell line inhibits HIV replication. J Infect Dis 198: 860863.

    • Search Google Scholar
    • Export Citation
  • 24.

    Xiang J, McLinden JH, Rydze RA, Chang Q, Kaufman TM, Klinzman D, Stapleton JT, 2009. Viruses within the Flaviviridae decrease CD4 expression and inhibit HIV replication in human CD4+ cells. J Immunol 183: 78607869.

    • Search Google Scholar
    • Export Citation
  • 25.

    López-Lemus UA, Vásquez C, Vázquez-Campuzano R, Valle-Reyes S, Guzmán-Bracho C, Araiza-Garaygordobil D, Rebolledo-Prudencio N, Delgado-Enciso I, Espinoza-Gómez F, 2014. Dengue virus serotype 1 non-structural protein NS5 expression interferes with HIV replication in a CD4+ T-cell line. Am J Trop Med Hyg 90: 418421.

    • Search Google Scholar
    • Export Citation
  • 26.

    De Clercq E, Schols D, 2001. Inhibition of HIV infection by CXCR4 and CCR5 chemokine receptor antagonists. Antivir Chem Chemother 12 (Suppl 1): 1931.

    • Search Google Scholar
    • Export Citation
  • 27.

    Diepolder HM, Gerlach JT, Zachoval R, Hoffmann RM, Jung MC, Wierenga EA, Scholz S, Santantonio T, Houghton M, Southwood S, Sette A, Pape GR, 1997. Immunodominant CD4+ T-cell epitope within nonstructural protein 3 in acute hepatitis C virus infection. J Virol 71: 60116019.

    • Search Google Scholar
    • Export Citation
  • 28.

    González R, Ataíde R, Naniche D, Menéndez C, Mayor A, 2012. HIV and malaria interactions: where do we stand? Expert Rev Anti Infect Ther 10: 153165.

    • Search Google Scholar
    • Export Citation
  • 29.

    Rabello A, Orsini M, Disch J, 2003. Leishmania/HIV co-infection in Brazil: an appraisal. Ann Trop Med Parasitol 97 (Suppl 1): 1728.

  • 30.

    Rocha A, de Meneses AC, da Silva AM, Ferreira MS, Nishioka SA, Burgarelli MK, Almeida E, Turcato Júnior G, Metze K, Lopes ER, 1994. Pathology of patients with Chagas disease and acquired immunodeficiency syndrome. Am J Trop Med Hyg 50: 261268.

    • Search Google Scholar
    • Export Citation
 
 
 
 

 

 
 

 

 

 

 

 

 

Dengue Infection in a Human Immunodeficiency Virus-1 Positive Patient Chronically Infected with Hepatitis B Virus in Western Mexico

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  • 1 School of Medicine, University of Colima, Colima, México.
  • | 2 State Cancer Institute, Department of Health, Colima, México.
  • | 3 Department of Internal Medicine, Regional Hospital of Colima, Department of Health, Colima, México.
  • | 4 Center for Gene Therapy, Hematologic Malignancies and Stem Cell Transplantation Institute, City of Hope, Duarte, California.

Human immunodeficiency virus (HIV) and dengue coinfection has not been extensively studied. We report herein a case of dengue serotype 1 infection in an HIV-1-positive patient coinfected with hepatitis B virus (HBV) in Colima State, Mexico. CD4+ cells and HIV-1 viremia remained at normal levels, and no severe complications were observed during this multiple viral infection. The alanine transaminase and aspartate transaminase values were elevated before and during dengue infection. Surprisingly, these parameters were significantly reduced 2 months later. Because of the lack of evidence regarding this multiple viral interaction, further research is required to understand the biologic and clinical course of dengue infection in HIV-1/HBV coinfected patients, especially in tropical regions where dengue virus transmission is highly active.

Introduction

Human immunodeficiency virus/hepatitis B virus (HIV/HBV) coinfection is common throughout the world. Previous reports have estimated that 10% of HIV-positive patients are coinfected with HBV worldwide, which may accelerate progression of liver failure.1,2 Moreover, the interaction of HIV with other tropical agents is associated with accelerated HIV/acquired immunodeficiency syndrome (AIDS) disease progression. For example, malaria and HIV coinfection is related to CD4+ cell activation and an increase in the levels of proinflammatory cytokine expression. This enables rapid HIV-1 replication and a consequently accelerated progression of HIV/AIDS disease.35

Dengue is a tropical and subtropical mosquito-borne disease. According to the World Health Organization6, 2.5 billion persons are at risk for contracting dengue infection, resulting in an estimated incidence of 50–100 million cases per year worldwide. There are four different dengue virus serotypes (DENV-1 to 4) that cause infection. They are genetically different, but share similar epidemiologic behavior.7

HIV/DENV coinfection has not been extensively studied. To date, six clinical reports have described the clinical presentations of dengue infection in HIV-1-infected patients.813 These reports suggest that HIV/DENV coinfection results in a benign clinical progression of dengue disease, as well as suppression of HIV-1 replication during the acute phase of dengue infection.810 Here in we report a case of DENV-1 infection in an HIV-1-positive patient chronically infected with HBV in Colima State, Mexico, an endemic tropical region for DENV transmission.

Case Report

In 2009, a 52-year-old woman infected with HIV-1 and HBV was admitted to the Regional Hospital of Colima with clinical suspicion of dengue infection. Upon admission, the patient had 2-day progression of intermittent fever (> 38.2°C), intense headache (especially behind the eyes), fatigue, muscle and joint pain (ankles, knees, and elbows), and abdominal bloating. The patient was alert and oriented to person, place, and time, and her general condition was good. The conventional tourniquet test did not show the presence of capillary fragility (6 petechiae/in2). Physical examination was unremarkable, except for hyperemic oropharynx. On the 4th day, her state of health improved, fever disappeared, and she was asymptomatic. During this event, the patient continued to take highly active antiretroviral treatment (HAART; lamivudine, zidovudine, and efavirenz), and only oral acetaminophen 500 mg tablet every 8 hours was added to her management. Dengue diagnosis was confirmed through detection of the DENV NS1 antigen with the SD Bioline Dengue Rapid Duo Test® (Yongin-si, Gyeonggi-do, Republic of Korea), following the manufacturer's instructions. The molecular identification carried out with reverse transcription polymerase chain reaction (RT-PCR) and automated sequencing at McLab (San Francisco, CA) showed the presence of DENV-1 strain DENV-1/MX/BID-V3664/2006 (GenBank no. GQ868499), with a similarity of 99%. Follow-up of the HIV-1 viremia at the InDRE (Department of Health, Mexico) showed undetectable levels (< 40 HIV-1 RNA copies/mL) during dengue infection and 6 months after the multiple viral infection. Blood hematologic, viremia, and serum biochemical values before, during, and after dengue infection are shown in Table 1. The values before dengue infection were obtained from the medical records of the study patient. The chronicity of HBV infection was corroborated through serologic tests, and the patient was found to be positive for hepatitis B surface antigen (HBsAg) and anti-hepatitis B core (anti-HBc) and negative for IgM anti-HBc.

Table 1

Laboratory results of the HIV-1/HBV coinfected patient before, during, and after dengue infection

ParameterR1R2R3
Leukocytes(103/μL)6.32.64.5
Lymphocytes (%)30.434.446
Monocytes (%)9.38.87.1
Eosinophils (%)1.60.03.6
Basophils (%)0.02.00.3
Neutrophils (%)58.754.843
Hemoglobin (g/dL)15.71514
Hematocrit (%)46.245.942.1
Platelets (× 103)340194275
Globulins (g/dL)3.103.103.10
Albumin (g/dL)4.304.504.40
ALT (IU/L)92.010524
AST (IU/L)90.010338
CD4+ (cells/μL)461
HIV viral load (HIV-1 RNA copies/mL)Undetectable*UndetectableUndetectable

ALT = alanine transaminase; AST = aspartate transaminase; HBV = hepatitis B virus; HIV = human immunodeficiency virus. R1 = results 2 months before dengue infection; R2 = results during dengue infection; R3 = results 2 months after dengue infection.

HIV-1 viral load 6 months before dengue infection.

HIV-1 viral load 6 months after dengue infection.

The patient voluntarily agreed to participate in this study, signing statements of informed consent, and it was approved by the Ethics Committee of the School of Medicine, University of Colima, and the Institutional Review Board of the Department of Health (Colima State, Mexico).

Discussion

The high incidence of dual infections of HIV with other tropical agents is an important problem that requires special attention. The results presented herein (Table 1) suggest that there were no severe clinical complications during this multiple viral infection. CD4+ cells remained at normal levels during dengue infection. Despite the fact that there is presently no evidence about the clinical complications of dengue infection in HIV-1/HBV coinfected patients, previous reports have shown that HBV infection leads to an increase in liver failure in HIV-positive patients treated with HAART.2,14 Our results showed that alanine transaminase and aspartate transaminase hepatic enzyme values were high before dengue infection, due to the HBV infection. However, a slight increase during dengue infection was observed. After 2 months, the hepatic enzyme levels were normal (Table 1). Most certainly, dengue infection is associated with acute liver failure in both HIV-uninfected patients and HBV-infected patients,15,16 thus suggesting an alteration in cytokine production. This was supported by the observation of low levels of interleukin 6 (IL-6) and tumor necrosis factor α (TNF-α) in patients with dengue and HBV infection and similar levels of IL-10, IL-4, and interferon γ expression in both the group of dengue patients with HBV infection and the group without HBV infection.17 It is possible that the altered cytokine production profile plays an important role in regulating the inflammatory response,18 which could lead to an unpredictable clinical course and unknown progression of liver failure in patients infected with HIV, HBV, and DENV. At this point, it is unclear whether dengue infection results in accelerated liver failure progression in HIV/HBV coinfected patients. Our observations suggest that dengue infection did not cause significant liver damage, but a significant decrease in the levels of hepatic enzyme expression was observed 2 months after the multiple viral infection. We cannot explain this phenomenon, given the existing lack of evidence on this particular subject. Such information is crucial to the biologic and clinical understanding of this multiple viral infection, as well as its implications in liver failure progression. Therefore, further studies are required to understand the main role of dengue infection in HIV/HBV coinfected patients treated with HAART.

In regard to HIV-1/DENV coinfection, our results coincide with those previously reported in which no severe complications attributable to dengue infection were observed.811 This behavior is possibly due to the effect of HAART treatment, which could be protecting the patient against dengue; this is according to a previous report that suggests a decrease of hepatitis C disease progression associated with HAART treatment in HIV-1-infected patients in Thailand.19 Even though the effect of HAART treatment during dengue infection remains unknown, the attenuation of certain cytokines in HIV-1-infected patients treated with HAART, such as IL-10 and TNF-α, could play an important role in decreasing dengue disease progression in HIV-1-positive patients.20,21 Both IL-10 and TNF-α are strongly associated with severe dengue infection.22

The HIV-1 viral loads in our patient remained at normal levels (< 40 HIV-1 RNA copies/mL) during DENV-1 infection and 6 months later. Watt and others8 have reported a reduction in the HIV-1 viral load in an HIV-1-positive patient without HAART treatment who presented with dengue infection in Thailand, and demonstrated that HIV-1 replication was suppressed during the acute phase of the infection. The antiviral mechanism involved has not been described, but previous reports2325 have shown that DENV-1 and DENV-2 NS5 protein expression inhibits HIV-1 replication in Jurkat CD4+ T cells. This antiviral effect has been associated with an increase in stromal cell-derived factor 1 (SDF-1) cytokine expression and a decrease in CD4 and CXCR4 expression.24,25 SDF-1 is the principal ligand for the co-receptor CXCR4 and blocks HIV fusion and entry into the CD4+ T cell.26 The fact that DENV NS5 protein expression could induce signaling pathway activation through the cell membrane should not be ruled out. This would produce a transcriptional modification, such as that occurs during SDF-1 cytokine overexpression. There is currently no evidence of such a phenomenon, but the NS3 protein of the hepatitis C virus (HCV) has been reported to have an affinity for a 14-amino acid immunodominant epitope of the CD4+ T cell. This could prevent the immune system attack, enhancing the efficiency of HCV replication and a consequent increase in disease severity.27 The analysis of the effect of DENV protein expression on HIV-1 replication would therefore provide necessary evidence for understanding the mechanism by which the DENV interferes on HIV replication in T lymphocytes.

A limitation of the present study is the fact that the HBV viral load was not determined. We suggest that the viremia of all coinfecting agents should be measured in future studies on patients similar to ours to have a better understanding of the clinical course of the pathology.

In conclusion, our results showed no severe clinical complications during this multiple viral infection. No significant behavior of the HIV-1 viral loads was observed, because the patient was treated with HAART and the viral load remained undetectable. Although previous reports show evidence that tropical diseases can accelerate HIV/AIDS disease progression,4,2830 our results showed that HIV-1 viral load levels apparently remained normal during the follow-up. Similarly, no side effects attributable to HBV infection were observed. However, there was a significant decrease in hepatic enzyme levels 2 months after dengue infection. Further studies with a greater number of patients are required. In addition, experimental studies evaluating the main role of dengue in HIV-1/HBV coinfected patients treated with HAART are needed. They could also explore its possible implications in the development of coadjuvant therapies for HIV/HBV coinfected patients, as well as new models enabling a more detailed study of the biology of these combined RNA viral infections.

ACKNOWLEDGMENTS

We wish to thank the National Council for Science and Technology (Federal Government, Mexico) for its financial assistance under CONACYT grant no. 252229 and FORDECyT-CONACYT grant no. 2009/1-000000117535 and the Institute for Epidemiological Diagnosis and Reference (Department of Health, Mexico) for its participation in the virologic analysis.

  • 1.

    Sun HY, Sheng WH, Tsai MS, Lee KY, Chang SY, Hung CC, 2014. Hepatitis B virus coinfection in human immunodeficiency virus-infected patients: a review. World J Gastroenterol 20: 1459814614.

    • Search Google Scholar
    • Export Citation
  • 2.

    Huang AJ, Núñez M, 2015. Outcomes in HIV/HBV-coinfected patients in the tenofovir era are greatly affected by immune suppression. J Int Assoc Provid AIDS Care 14: 360368.

    • Search Google Scholar
    • Export Citation
  • 3.

    Alemu A, Shiferaw Y, Addis Z, Mathewos B, Birhan W, 2013. Effect of malaria on HIV/AIDS transmission and progression. Parasit Vectors 6: 18.

  • 4.

    Morgado MG, Barcellos C, Pina MF, Bastos FI, 2000. Human immunodeficiency virus/acquired immunodeficiency syndrome and tropical diseases: a Brazilian perspective. Mem Inst Oswaldo Cruz 95 (Suppl 1): 145151.

    • Search Google Scholar
    • Export Citation
  • 5.

    Harms G, Feldmeier H, 2005. The impact of HIV infection on tropical diseases. Infect Dis Clin North Am 19: 121135.

  • 6.

    World Health Organization, 2014. Dengue and Severe Dengue [Internet]. Updated March 2014. Available at: http://www.who.int/mediacentre/factsheets/fs117/en/.

    • Search Google Scholar
    • Export Citation
  • 7.

    Weaver SC, Vasilakis N, 2009. Molecular evolution of dengue viruses: contributions of phylogenetics to understanding the history and epidemiology of the preeminent arboviral disease. Infect Genet Evol 9: 523540.

    • Search Google Scholar
    • Export Citation
  • 8.

    Watt G, Kantipong P, Jongsakul K, 2003. Decrease in human immunodeficiency virus type 1 load during acute dengue fever. Clin Infect Dis 36: 10671069.

    • Search Google Scholar
    • Export Citation
  • 9.

    Gonzalez D, Limonta D, Bandera JF, Perez J, Kouri G, Guzman MG, 2009. Dual infection with dengue virus 3 and human immunodeficiency virus 1 in Havana, Cuba. J Infect Dev Ctries 3: 318320.

    • Search Google Scholar
    • Export Citation
  • 10.

    Siong WC, Ching TH, Jong GC, Pang CS, Vernon LJ, Sin LY, 2008. Dengue infections in HIV patients. Southeast Asian J Trop Med Public 39: 260265.

  • 11.

    Mendes W da S, Branco M dos R, Medeiros MN, 2006. Clinical case report: dengue hemorrhagic fever in a patient with acquired immunodeficiency syndrome. Am J Trop Med Hyg 74: 905907.

    • Search Google Scholar
    • Export Citation
  • 12.

    Pang J, Thein TL, Lye DC, Leo YS, 2015. Differential clinical outcome of dengue infection among patients with and without HIV infection: a matched case-control study. Am J Trop Med Hyg 92: 11561162.

    • Search Google Scholar
    • Export Citation
  • 13.

    Torrentes-Carvalho A, Hottz ED, Marinho CF, da Silva JB, de Oliveira Pinto LM, Fialho LG, Bozza FA, Cunha RV, Damasco PV, Kubelka CF, de Azeredo EL, 2016. Characterization of clinical and immunological features in patients coinfected with dengue virus and HIV. Clin Immunol 164: 95105.

    • Search Google Scholar
    • Export Citation
  • 14.

    Soriano V, Poveda E, Vispo E, Barreiro P, 2013. Hepatitis B in HIV-infected patients. Clin Liver Dis 17: 489501.

  • 15.

    Samanta J, Sharma V, 2015. Dengue and its effects on liver. World J Clin Cases 3: 125131.

  • 16.

    Agarwal MP, Giri S, Sharma V, Roy U, Gharsangi K, 2011. Dengue causing fulminant hepatitis in a hepatitis B virus carrier. Biosci Trends 5: 4445.

  • 17.

    Tang Y, Kou Z, Tang X, Zhang F, Yao X, Liu S, Jin X, 2008. Unique impacts of HBV co-infection on clinical and laboratory findings in a recent dengue outbreak in China. Am J Trop Med Hyg 79: 154158.

    • Search Google Scholar
    • Export Citation
  • 18.

    Wan Z, Xie G, Wu Y, Liu F, Xin S, You S, Liu H, Li C, Li D, 2016. Cytokines elevated in patients with HBV-related acute-on-chronic liver failure promote NK cell mediated cytotoxicity through TRAIL. Dig Liver Dis 48: 528535.

    • Search Google Scholar
    • Export Citation
  • 19.

    Law WP, Duncombe CJ, Mahanontharit A, Boyd MA, Ruxrungtham K, Lange JM, Phanuphak P, Cooper DA, Dore GJ, 2004. Impact of viral hepatitis co-infection on response to antiretroviral therapy and HIV disease progression in the HIV-NAT cohort. AIDS 18: 11691177.

    • Search Google Scholar
    • Export Citation
  • 20.

    Stylianou E, Aukrust P, Kvale D, Müller F, Frøland SS, 1999. IL-10 in HIV infection: increasing serum IL-10 levels with disease progression—down-regulatory effect of potent anti-retroviral therapy. Clin Exp Immunol 116: 115120.

    • Search Google Scholar
    • Export Citation
  • 21.

    Aukrust P, Müller F, Lien E, Nordoy I, Liabakk NB, Kvale D, Espevik T, Frøland SS, 1999. Tumor necrosis factor (TNF) system levels in human immunodeficiency virus-infected patients during highly active antiretroviral therapy: persistent TNF activation is associated with virologic and immunologic treatment failure. J Infect Dis 179: 7482.

    • Search Google Scholar
    • Export Citation
  • 22.

    Malavige GN, Huang LC, Salimi M, Gomes L, Jayaratne SD, Ogg GS, 2012. Cellular and cytokine correlates of severe dengue infection. PLoS One 7: e50387.

  • 23.

    McLinden JH, Stapleton JT, Chang Q, Xiang J, 2008. Expression of the dengue virus type 2 NS5 protein in a CD4+ T cell line inhibits HIV replication. J Infect Dis 198: 860863.

    • Search Google Scholar
    • Export Citation
  • 24.

    Xiang J, McLinden JH, Rydze RA, Chang Q, Kaufman TM, Klinzman D, Stapleton JT, 2009. Viruses within the Flaviviridae decrease CD4 expression and inhibit HIV replication in human CD4+ cells. J Immunol 183: 78607869.

    • Search Google Scholar
    • Export Citation
  • 25.

    López-Lemus UA, Vásquez C, Vázquez-Campuzano R, Valle-Reyes S, Guzmán-Bracho C, Araiza-Garaygordobil D, Rebolledo-Prudencio N, Delgado-Enciso I, Espinoza-Gómez F, 2014. Dengue virus serotype 1 non-structural protein NS5 expression interferes with HIV replication in a CD4+ T-cell line. Am J Trop Med Hyg 90: 418421.

    • Search Google Scholar
    • Export Citation
  • 26.

    De Clercq E, Schols D, 2001. Inhibition of HIV infection by CXCR4 and CCR5 chemokine receptor antagonists. Antivir Chem Chemother 12 (Suppl 1): 1931.

    • Search Google Scholar
    • Export Citation
  • 27.

    Diepolder HM, Gerlach JT, Zachoval R, Hoffmann RM, Jung MC, Wierenga EA, Scholz S, Santantonio T, Houghton M, Southwood S, Sette A, Pape GR, 1997. Immunodominant CD4+ T-cell epitope within nonstructural protein 3 in acute hepatitis C virus infection. J Virol 71: 60116019.

    • Search Google Scholar
    • Export Citation
  • 28.

    González R, Ataíde R, Naniche D, Menéndez C, Mayor A, 2012. HIV and malaria interactions: where do we stand? Expert Rev Anti Infect Ther 10: 153165.

    • Search Google Scholar
    • Export Citation
  • 29.

    Rabello A, Orsini M, Disch J, 2003. Leishmania/HIV co-infection in Brazil: an appraisal. Ann Trop Med Parasitol 97 (Suppl 1): 1728.

  • 30.

    Rocha A, de Meneses AC, da Silva AM, Ferreira MS, Nishioka SA, Burgarelli MK, Almeida E, Turcato Júnior G, Metze K, Lopes ER, 1994. Pathology of patients with Chagas disease and acquired immunodeficiency syndrome. Am J Trop Med Hyg 50: 261268.

    • Search Google Scholar
    • Export Citation

Author Notes

* Address correspondence to Uriel A. López-Lemus, School of Medicine, University of Colima, Avenida Universidad 333, Las Viboras, 28040 Colima, Mexico. E-mail: lemus_a83@yahoo.com

Authors' addresses: Iván Delgado-Enciso, School of Medicine, Public Health, University of Colima, Colima, México and State Cancer Institute, Department of Health, Colima, México, E-mail: ivan_delgado_enciso@ucol.mx. Francisco Espinoza-Gómez, School of Medicine, Public Health, University of Colima, Avenida Universidad 333, Colima, México and Department of Internal Medicine, Regional Hospital of Colima, Department of Health, Colima, México, Email: fespin@ucol.mx. Rodolfo Ochoa-Jiménez, Department of Internal Medicine, Regional Hospital of Colima, Department of Health, Colima, México, E-mail: docochoa@hotmail.com. Salvador Valle-Reyes and Clemente Vásquez, School of Medicine, Public Health, University of Colima, Avenida Universidad 333, Colima, Mexico, E-mails: juanchavador@hotmail.com and clemvas@ucol.mx. Uriel A. López-Lemus, School of Medicine, Public Health, University of Colima, Avenida Universidad 333, Colima, Mexico and Biomedical Sciences, University of Colima, Colima, Mexico, E-mail: lemus_a83@yahoo.com.

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