Increased levels of reactive oxygen species in platelets and platelet-derived microparticles and the risk of respiratory failure in HIV/AIDS patients

Gama, Wellington Mota; Oliveira, Lucas Barbosa; Chaves, Yury Oliveira; Ribeiro, Flavio; Almeida, Taynná Vernalha Rocha; Baptista, Barbara Jose Antunes; Santana, Monique Freire; Ferreira, Luis Carlos; Lacerda, Marcus Vinicius Guimaraes; Nogueira, Paulo Afonso

doi:10.1590/0074-02760200082

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SHORT COMMUNICATION • Mem. Inst. Oswaldo Cruz 115 • 2020 • https://doi.org/10.1590/0074-02760200082 linkcopy

Increased levels of reactive oxygen species in platelets and platelet-derived microparticles and the risk of respiratory failure in HIV/AIDS patients

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Respiratory failure (RF) is the main cause of hospital admission in HIV/AIDS patients. This study assessed comorbidities and laboratory parameters in HIV/AIDS inpatients with RF (N = 58) in relation to those without RF (N = 36). Tuberculosis showed a huge relative risk and platelet counts were slightly higher in HIV/AIDS inpatients with RF. A flow cytometry assay for reactive oxygen species (ROS) showed lower levels in platelets of these patients in relation to the healthy subjects. However, when stimulated with adrenaline, ROS levels increased in platelets and platelet-derived microparticles of HIV/AIDS inpatients, which may increase the risk of RF during HIV and tuberculosis (HIV-TB) coinfection.

Key words:
HIV/AIDS; respiratory failure; reactive oxygen species; platelets and platelet-derived microparticles

Authorship

person Wellington Mota Gama

person Lucas Barbosa Oliveira

person Yury Oliveira Chaves

schoolFundação Oswaldo Cruz-Fiocruz, Instituto Oswaldo Cruz, Programa de Pós-Graduação em Biologia Parasitária, Rio de Janeiro, RJ, BrasilFundação Oswaldo Cruz-FiocruzBrazilRio de Janeiro, RJ, BrazilFundação Oswaldo Cruz-Fiocruz, Instituto Oswaldo Cruz, Programa de Pós-Graduação em Biologia Parasitária, Rio de Janeiro, RJ, BrasilschoolFundação de Medicina Tropical Heitor Vieira Dourado, Instituto de Pesquisa Clínica Carlos Borborema, Manaus, AM, BrasilFundação de Medicina Tropical Heitor Vieira DouradoBrazilManaus, AM, BrazilFundação de Medicina Tropical Heitor Vieira Dourado, Instituto de Pesquisa Clínica Carlos Borborema, Manaus, AM, Brasil

person Flavio Ribeiro

person Taynná Vernalha Rocha Almeida

schoolFundação de Medicina Tropical Heitor Vieira Dourado, Instituto de Pesquisa Clínica Carlos Borborema, Manaus, AM, BrasilFundação de Medicina Tropical Heitor Vieira DouradoBrazilManaus, AM, BrazilFundação de Medicina Tropical Heitor Vieira Dourado, Instituto de Pesquisa Clínica Carlos Borborema, Manaus, AM, BrasilschoolUniversidade Federal do Amazonas, Programa de Pós-Graduação em Ciências da Saúde, Manaus, AM, BrasilUniversidade Federal do AmazonasBrazilManaus, AM, BrazilUniversidade Federal do Amazonas, Programa de Pós-Graduação em Ciências da Saúde, Manaus, AM, Brasil

person Barbara Jose Antunes Baptista

schoolFundação Oswaldo Cruz-Fiocruz, Instituto Leônidas e Maria Deane, Programa de Pós-Graduação em Biologia da Relação Patógeno-Hospedeiro, Manaus, AM, BrasilFundação Oswaldo Cruz-FiocruzBrazilManaus, AM, BrazilFundação Oswaldo Cruz-Fiocruz, Instituto Leônidas e Maria Deane, Programa de Pós-Graduação em Biologia da Relação Patógeno-Hospedeiro, Manaus, AM, BrasilschoolFundação de Medicina Tropical Heitor Vieira Dourado, Instituto de Pesquisa Clínica Carlos Borborema, Manaus, AM, BrasilFundação de Medicina Tropical Heitor Vieira DouradoBrazilManaus, AM, BrazilFundação de Medicina Tropical Heitor Vieira Dourado, Instituto de Pesquisa Clínica Carlos Borborema, Manaus, AM, Brasil

person Monique Freire Santana

schoolUniversidade do Estado do Amazonas, Programa de Pós-Graduação em Medicina Tropical, Manaus, AM, BrasilUniversidade do Estado do AmazonasBrasilManaus, AM, BrasilUniversidade do Estado do Amazonas, Programa de Pós-Graduação em Medicina Tropical, Manaus, AM, Brasil

person Luis Carlos Ferreira

person Marcus Vinicius Guimaraes Lacerda

person Paulo Afonso Nogueira +

schoolUniversidade Federal do Amazonas, Programa de Pós-Graduação em Imunologia Básica e Aplicada, Manaus, AM, BrasilUniversidade Federal do AmazonasBrazilManaus, AM, BrazilUniversidade Federal do Amazonas, Programa de Pós-Graduação em Imunologia Básica e Aplicada, Manaus, AM, BrasilschoolFundação Oswaldo Cruz-Fiocruz, Instituto Leônidas e Maria Deane, Programa de Pós-Graduação em Biologia da Relação Patógeno-Hospedeiro, Manaus, AM, BrasilFundação Oswaldo Cruz-FiocruzBrazilManaus, AM, BrazilFundação Oswaldo Cruz-Fiocruz, Instituto Leônidas e Maria Deane, Programa de Pós-Graduação em Biologia da Relação Patógeno-Hospedeiro, Manaus, AM, BrasilschoolFundação de Medicina Tropical Heitor Vieira Dourado, Instituto de Pesquisa Clínica Carlos Borborema, Manaus, AM, BrasilFundação de Medicina Tropical Heitor Vieira DouradoBrazilManaus, AM, BrazilFundação de Medicina Tropical Heitor Vieira Dourado, Instituto de Pesquisa Clínica Carlos Borborema, Manaus, AM, Brasil

0000-0003-3015-1021

+ Corresponding author:
emailpaulo.nogueira@fiocruz.br

WMG, LBO and YOC performed immunoassays (platelet and microparticles isolation; cytometry); FR, BJAB and MFS performed screening patients; TVRA, LCF, MVGL and PAN coordinated the study and prepared the manuscript.

SCIMAGO INSTITUTIONS RANKINGS

Universidade Federal do Amazonas, Programa de Pós-Graduação em Imunologia Básica e Aplicada, Manaus, AM, BrasilUniversidade Federal do AmazonasBrazilManaus, AM, BrazilUniversidade Federal do Amazonas, Programa de Pós-Graduação em Imunologia Básica e Aplicada, Manaus, AM, Brasil

Fundação Oswaldo Cruz-Fiocruz, Instituto Leônidas e Maria Deane, Programa de Pós-Graduação em Biologia da Relação Patógeno-Hospedeiro, Manaus, AM, BrasilFundação Oswaldo Cruz-FiocruzBrazilManaus, AM, BrazilFundação Oswaldo Cruz-Fiocruz, Instituto Leônidas e Maria Deane, Programa de Pós-Graduação em Biologia da Relação Patógeno-Hospedeiro, Manaus, AM, Brasil

Fundação Oswaldo Cruz-Fiocruz, Instituto Oswaldo Cruz, Programa de Pós-Graduação em Biologia Parasitária, Rio de Janeiro, RJ, BrasilFundação Oswaldo Cruz-FiocruzBrazilRio de Janeiro, RJ, BrazilFundação Oswaldo Cruz-Fiocruz, Instituto Oswaldo Cruz, Programa de Pós-Graduação em Biologia Parasitária, Rio de Janeiro, RJ, Brasil

Fundação de Medicina Tropical Heitor Vieira Dourado, Instituto de Pesquisa Clínica Carlos Borborema, Manaus, AM, BrasilFundação de Medicina Tropical Heitor Vieira DouradoBrazilManaus, AM, BrazilFundação de Medicina Tropical Heitor Vieira Dourado, Instituto de Pesquisa Clínica Carlos Borborema, Manaus, AM, Brasil

Universidade Federal do Amazonas, Programa de Pós-Graduação em Ciências da Saúde, Manaus, AM, BrasilUniversidade Federal do AmazonasBrazilManaus, AM, BrazilUniversidade Federal do Amazonas, Programa de Pós-Graduação em Ciências da Saúde, Manaus, AM, Brasil

Universidade do Estado do Amazonas, Programa de Pós-Graduação em Medicina Tropical, Manaus, AM, BrasilUniversidade do Estado do AmazonasBrasilManaus, AM, BrasilUniversidade do Estado do Amazonas, Programa de Pós-Graduação em Medicina Tropical, Manaus, AM, Brasil

Figures | Tables

Figures (1)
Tables (1)

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Characterisation of platelets and platelet-derived microparticles by double labeling with anti CD41 and dihydroethidium (DHE). (A) The CD41b and DHE double positive platelets selected from Forward and Size scatter graph (small graph in the upper right corner), distributed in the shape of a comet, which is characteristic of the heterogeneous size distribution (selection). (B) Comparison of the total number of CD41+DHE+ platelets between HIV/AIDS patients and healthy subjects. (C) reactive oxygen species (ROS) levels in platelets before and after stimulation with 200 μg/mL adrenaline determined by the median fluorescence intensity (MFI). Platelets of HIV/AIDS patients increased the level of ROS compared to the control platelets. (D) The CD41b and DHE double positive microplatelets selected from Forward and Size scatter graph. The region below the comet-shaped platelet population were selected for determination of CD41+DHE+ microplatelets (small graph in the lower right corner). The CD41 and DHE double microplatelet populations were defined by lateral and frontal dispersion characteristics and for the expression of double labeling on CD41+ (the FL-1 channel panel) and DHE labeling in FL2 channel panel. Red dot plots indicate CD41+DHE+ microplatelets among events below the comet-shaped platelet population. (E) Comparison of the total number of CD41+DHE+ microplatelets between HIV/AIDS patients and healthy subjects. (F) ROS levels in microplatelets of HIV/AIDS patients before and after adrenaline stimulation with 200 μg/mL of adrenaline for 30 minutes.

Thumbnail

TABLE Comparison of comorbidities and clinical data of HIV/AIDS patients with or without respiratory failure

image Characterisation of platelets and platelet-derived microparticles by double labeling with anti CD41 and dihydroethidium (DHE). (A) The CD41b and DHE double positive platelets selected from Forward and Size scatter graph (small graph in the upper right corner), distributed in the shape of a comet, which is characteristic of the heterogeneous size distribution (selection). (B) Comparison of the total number of CD41+DHE+ platelets between HIV/AIDS patients and healthy subjects. (C) reactive oxygen species (ROS) levels in platelets before and after stimulation with 200 μg/mL adrenaline determined by the median fluorescence intensity (MFI). Platelets of HIV/AIDS patients increased the level of ROS compared to the control platelets. (D) The CD41b and DHE double positive microplatelets selected from Forward and Size scatter graph. The region below the comet-shaped platelet population were selected for determination of CD41+DHE+ microplatelets (small graph in the lower right corner). The CD41 and DHE double microplatelet populations were defined by lateral and frontal dispersion characteristics and for the expression of double labeling on CD41+ (the FL-1 channel panel) and DHE labeling in FL2 channel panel. Red dot plots indicate CD41+DHE+ microplatelets among events below the comet-shaped platelet population. (E) Comparison of the total number of CD41+DHE+ microplatelets between HIV/AIDS patients and healthy subjects. (F) ROS levels in microplatelets of HIV/AIDS patients before and after adrenaline stimulation with 200 μg/mL of adrenaline for 30 minutes. open_in_new

table_chartTABLE Comparison of comorbidities and clinical data of HIV/AIDS patients with or without respiratory failure

Comorbidities	RF	No RF	RR	95%CI	p
Comorbidities	n (%)	n (%)	RR	95%CI	p
Gender	44(75.8)	27(75)	1.011	0.8025 to 1.325	0.9999
HAART	46(79.3)	24(66.7)	1.19	0.9302 to 1.61	0.2247
Death	16(27.5)	5(13.9)	1.986	0.8473 to 4.931	0.1361
TB	38(65.5)	1(2.7)	23.59	4.571 to 134	<0.0001
Neurological syndromes	25(43.1)	15(41.6)	1.034	0.6475 to 1.716	0.9999
Cardiovascular comorbidities	2(3.4)	3(8.3)	0.4138	0.0858 to 1.998	0.3676
Digestive syndromes	14(24.1)	10(27.7)	0.869	0.4431 to 1.751	0.8086
Weight loss	29(50)	18(50)	1	0.6691 to 1.549	0.9999
Diarrhea	18(31)	11(30.5)	1.016	0.5571 to 1.918	0.9999
Vomiting	18(31)	17(47.2)	0.6572	0.3942 to 1.108	0.1296
Clinical parameters^*	Median (IQ25;IQ75)	Median (IQ25;IQ75)			p
Age	37(28.75;43)	34.5(29;41.75)			0.6111
HIV-RNA copies/mL	35397(397;173958)	34884(180;498626)			0.5577
CD4-T cells/µL (600 to 1;500/mm3)	60(18.75;234)	84(28;169.8)			0.9826
CD8-T cells/µL (200 to 800/mm3)	544.5(338;1124)	519(292;1041)			0.8519
CD4/CD8 ratio (1.0 and 4.0)	0.15(0.06;0.405)	0.15(0.0575;0.3025)			0.5353
Hemoglobin, g/dL (13.0-18.0 g/dL)	10.5(8765;12.89)	9.7(8.16;12.29)			0.1360
Leukocytes/mL (4;500-11;000/mL)	4180(3290;7200)	4995(3888;7405)			0.3191
Lymphocyte (%)	23.01(17;36)	24(12.75;34.05)			0.8209
Neutrophils/mL (1,800-7,700/mL)	2756(1711;4347)	3552(2542;5021)			0.0543
Monocytes/mL (80-1;100/mL)	295(148.8;418.5)	395.5(209.8;519.8)			0.1493
Eosinophils/mL (40-550/mL)	3(2;6.4)	3.6(2;9.75)			0.5924
Platelets ×10³/mL (150;000-4000;000×10³/mL)	297000(209750;415000)	263000(123500;319750)			0.0344
MPV (8.8 fL a 12.5 fL)	8.06(7.36;8.96)	8.32(7825;8.58)			0.3543
PDW ( 9.3 fL a 16.0 fL)	13.5(11.63;16.75)	14.13(12.25;17.38)			0.4495
Bilirubin, mg/dL (<1.0 mg/dL)	0.39(0.28;0.73)	0.59(0.36;1.55)			0.0270
Creatinine, mg/dL (0.6-1.35 mg/dL)	0.8(0.6;1)	0.8(0.6;1.2)			0.5041
DHL, U/uL (120 e 246 U/uL)	384.5(306.5;487.3)	343(285.8;485.3)			0.3875
Gamma-glutamyltransferase, U/uL^**	91(58.75;217)	89.5(42.25;413.8)			0.7336
Albumin, g/dL (3.5-5.0g/dL)	3.9(3.35;4.5)	3.7(2.59;4.1)			0.1044
Alkaline phosphatase, U/uL (65.0-330.0 U/uL)	287(202.5;403)	296(204;496)			0.8218
Aspartate aminotransferase, U/uL (2-38.0U/uL)	32(25;59)	39(25.25;60.75)			0.4931
Alanine aminotransferase, U/uL (2-44.0U/uL)	41(23.5;74.5)	37(23.25;80.25)			0.7640

*: for some parameters, parenthesis indicate normal range values; **: references values of Gamma-glutamyltransferase (men: 10 to 50 U/uL and women: 7 to 32 U/uL).

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