Sociodemographic predictors associated with the spectrum of non-opportunist neuroretinal disease of non-infectious etiology in patients with HIV/AIDS: A scoping review | Archivos de la Sociedad Española de Oftalmología (English Edition)

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15 and 7.1%–10.6%, respectively,<a class="elsevierStyleCrossRefs" href="#bib0020">4–10</a> even prevalences of up to 27% of cases of HIV-related non-infectious retinal vasculopathy with CD4 counts below 200 cells/mm,<a class="elsevierStyleCrossRefs" href="#bib0015">3,11</a> have been reported in different regions of the world such as China, India, Taiwan, Africa and South Korea, age older than 35 years, World Health Organization (WHO) stages III and IV and low CD4 < 200 cells/μL, have been recognized as significant risk factors for the development of HIV/AIDS eye disease.<a class="elsevierStyleCrossRefs" href="#bib0060">12–19</a> In Tokyo, Japan, a study highlighted that the risk of infectious or non-infectious HIV retinopathy for each decrease in CD4 count by values of 100 cells/μL along with the increase for each 1 log/copies in viral load and for each decade of age from the fourth decade were statistically significant factors.<a class="elsevierStyleCrossRef" href="#bib0100">20</a>From a pathophysiological point of view, non-infectious and non-opportunistic neuroretinal disease in patients with HIV/AIDS progresses rapidly in European Americans with the IL-10-5′A variant (RR = 2.09) and in African Americans with the RANTES-In1 chemokine receptor ligand polymorphism 1.1 C<a class="elsevierStyleCrossRef" href="#bib0105">21</a>; in populations with protective mitochondrial haplogroups such as J, H3 and U5a1-15218 of the European mitochondrial macrohaplogroup we investigate the role of HAART or AIDS itself in mitochondrial toxicity that may cause accelerated progression of neuroretinal disorder.<a class="elsevierStyleCrossRef" href="#bib0110">22</a> The existence of a senescence state in HIV/AIDS patients with dilated retinal venular diameters and shorter telomere length associated with increased age-related morbidity has been proposed,<a class="elsevierStyleCrossRef" href="#bib0115">23</a> with a common genetic network between age-related macular degeneration and neurodegenerative disease in HIV patients.<a class="elsevierStyleCrossRef" href="#bib0120">24</a>Studies demonstrate foveal and pericentral neuroretinal thinning with microstructural white matter damage in children<a class="elsevierStyleCrossRef" href="#bib0125">25</a> and cognitive impairment linked to thinning of the retinal ganglion cell layer and inner plexiform layer<a class="elsevierStyleCrossRefs" href="#bib0130">26,26–30</a>; while another study reported, paradoxically, thickening of the inner nuclear and outer plexiform layers as conditions that may coexist,<a class="elsevierStyleCrossRef" href="#bib0155">31</a> it has been suggested that cognitive impairment may also be related to an increased concentration of beta 2-microglobulin as a marker for central nervous system (CNS) immune activation,<a class="elsevierStyleCrossRef" href="#bib0160">32</a> with visual field defects linked to a low CD4 count that on perimetry are located superiorly near the blind spot, implying damage to the inferior retina near the optic disc<a class="elsevierStyleCrossRef" href="#bib0165">33</a>; impaired color vision and contrast sensitivity in HIV patients are mainly linked to increasing age and advanced stages of AIDS.<a class="elsevierStyleCrossRefs" href="#bib0170">34–38</a>TargetThe coexistence of infectious retinitis and non-infectious retinal disease as the most frequent ocular manifestations, even in the HAART era, is what motivates this study, as well as the characterization of sociodemographic variables (age, gender, ethnicity, transmission risk, CD4 count, disease stage, follow-up time since diagnosis and treatment) and their association with the development of non-infectious non-opportunistic neuroretinal disease in patients with HIV/AIDS.Materials and methodsStudy designThe study is designed as an integrative review, according to O’Malley’s methodology.Inclusion and exclusion criteriaInclusion criteria for the selection of articles were defined as those original studies such as clinical trials, cohort studies, case-control studies, systematic reviews or meta-analyses, which established a direct or indirect association between neuroretinal disease and HIV/AIDS; without restrictions regarding the year of publication and in English or Spanish, those limited to establish a link between HIV/AIDS and opportunistic infectious retinal infection without including non-infectious disease among their study variables and non-original articles such as narrative reviews, series or case reports and letters to the editor, as well as those published in languages other than English or Spanish, were excluded. The search period in the databases was between January to March 2020.Literature search strategyBased on the PICO methodology, the selected articles were identified by searching PubMed, PubMed Central, all of Medline, Ovid, Scopus and Virtual Health Library databases; and by using the AND/OR Boolean operators, different combinations of medical subject heading terms (MESH) were performed (Appendix A, Supplementary data): macular degeneration; macular degeneration, age-related; acquired human immunodeficiency syndrome; acquired immunodeficiency syndrome; AIDS; HIV; human immunodeficiency virus, retina, optic nerve, nerve fibers, scanning laser polarimetry, tomography, optical coherence, electroretinography, fluorescein angiography, contrast sensitivity, visual fields, color vision (NOT cytomegalovirus, opportunistic infections, herpes zoster ophthalmicus, cytomegalovirus retinitis, ocular syphilis).<a class="elsevierStyleCrossRef" href="#bib0295">59</a>Study selection and data extractionFrom the initial search, 86,358 records were identified and then multiplied, yielding 43,554 articles. Two researchers, who reviewed the titles and abstract of each paper, resolved any differences by consensus and each variable was tabulated along with the title, author, year of publication and description of sociodemographic variables. The studies that met the eligibility and quality criteria were filtered for a total of 13 texts that were included for qualitative synthesis in the review.<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a> shows the flow chart of the selected articles; the present review follows the recommendations of the PRISMA methodology.<elsevierMultimedia ident="fig0005"></elsevierMultimedia>ResultsFor the presentation of the results, initially a general description of the studies was made, including the type of study, the regions where they were conducted and the years of publication, together with the most important conclusions of each work. Subsequently, the qualitative tabulation of each sociodemographic variable was made and the results were reported around the sociodemographic variables of interest, focusing the analysis on the elements of inferential statistics, measures of association and statistical significance that the different authors proposed in their research.Description of the studiesMortality from age-related causes and chronic noncommunicable diseases tends to increase in patients with HIV and AIDS who have good adherence to HAART. Jabs et al., in their case-control study of participants in the Longitudinal Study of Ocular Complications of AIDS (LSOCA) cohort who were diagnosed with intermediate-stage age-related macular degeneration by analysis of retinal photographs analyzed at the University of Wisconsin-Madison School of Medicine and Public Health Department of Ophthalmology and Visual Sciences Reading Center in 2019, found that macular degeneration in patients with AIDS was associated with increased mortality, hazard ratio (HR): 1.48 95% CI: 1.02–2.15, P-value = .04, in association with increased inflammatory biomarkers such as polymerase chain reaction (PCR) test, interleukin-6 (IL-6) and IP-10 protein.<a class="elsevierStyleCrossRef" href="#bib0195">39</a>Similarly, the accelerated rate of age-related chronic noncommunicable disease presentation in patients with HIV or AIDS was also illustrated by Jabs et al. in their cohort study of LSOCA patients enrolled between September 1, 1998 and July 31, 2011 at 19 clinical centers in the United States, who underwent retinal photography at 5 and 10 years of follow-up, finding an incidence of age-related macular degeneration of 0.65/100 person-years, with smoking as the only significant risk factor for developing this pathology and with a 1.75-fold risk (95% CI 1.16, 2.64; P = .008) relative to the control cohort of the Multi-Ethnic Study of Atherosclerosis (MESA). Even though the mean age in the MESA cohort was 17 years older than in LSOCA (61 ± nine years vs. 44 ± eight years)<a class="elsevierStyleCrossRef" href="#bib0200">40</a>; or in their 2015 cross-sectional study, where Jabs et al. found that of 1.825 participants with AIDS, 9.9% had mid-stage age-related macular degeneration, which, when compared to cases in the uninfected Beaver Deam cohort study, found a fourfold higher prevalence of macular degeneration in LSOCA, with a risk per decade of age OR 1.9 (95% CI 1.6, 2.3, P < .001), with prevalences of 4.0% for those aged 30–39 years and 24.3% for those >60 years, where injection drug use (OR = 2.4, 95% CI 1.5, 3.9, P < .001) and risk from heterosexual contact were significant risk factors (OR = 1.9, 95% CI 1.3, 2.8, P = .001).<a class="elsevierStyleCrossRef" href="#bib0205">41</a>Some associations with sociodemographic variables were explicitly and statistically significantly reported by the work of Jabs et al. in their 2015 cohort study of 1822 AIDS patients diagnosed with neuroretinal disorder, where they found that 16% of participants had neuroretinal disorder at enrollment, with a 20-year cumulative incidence of 51% (95% CI, 46–55), a finding that was more common in women and African Americans, with mortality adjusted for low CD4 counts and detectable viral load in patients with neuroretinal disorder HR, 1.7; 95% CI, 1.3–2.1; P < .0001), with increased risks of bilateral visual impairment HR, 6.5; 95% CI, 2.6–10.6; P < .0001) and blindness HR, 5.9; 95% CI, 2.8–13.7; P = .0.<a class="elsevierStyleCrossRef" href="#bib0210">42</a>The relationship between CD4 count levels and viral loads versus the development of neuroretinal disease qualitatively does not allow us to establish a clear trend towards infectious or non-infectious retinopathy, since both conditions occur indistinctly at high or low CD4 counts and at high or low viral loads. The results are illustrated in Nishijima’s retrospective study of patients examined at the AIDS Clinical Center, Tokyo Japan, HIV-1 infected patients aged 17 years and older and enrolled between January 2004 and December 2013, with 1515 participants. HIV retinopathy was diagnosed in 127 (8%), with CD4 count < .200/μL in all cases of cytomegalovirus retinitis and HIV retinopathy,<a class="elsevierStyleCrossRef" href="#bib0100">20</a> contrasting with Kuppermann’s prospective study of patients examined at the University of California, San Diego, during a period between September 16, 1991, to October 30, 1991, finding that of 132 persons with AIDS, 46 (35%) had HIV-related noninfectious retinal vasculopathy, of which 39 of 87 (45%) patients with CD4 counts of <50 cells/mm3 had HIV-related non-infectious retinal vasculopathy, while seven of 45 (16%) with CD4 counts of >50 cells/mm3 also had these changes.<a class="elsevierStyleCrossRef" href="#bib0055">11</a>Progression to non-infectious neuroretinal disease appears to be positively influenced by adherence to modern HAART, findings illustrated in Accorinti’s retrospective study of patients examined at the Department of Ophthalmological Sciences of the University of Rome from 1997 to 2003, with 735 individuals treated with HAART for at least two months (group 1) and 838 examined untreated from 1988 to 1995 (group 2), finding that, in the group of patients treated with HAART, the prevalence of age-related ocular manifestations was significantly higher.<a class="elsevierStyleCrossRef" href="#bib0215">43</a> Also, Miller’s retrospective study of patients analyzed at the Wills Eye Institute and Thomas Jefferson University Hospitals, where 222 admissions were reviewed for a total of 188 subjects divided into two groups from 1995 to 2003 and the second group between 2003 and 2010, reporting a decrease in opportunistic disease in the second cohort with an increase in retinal disease of non-infectious etiology explained, apparently, by earlier onset and greater adherence to HAART in the second cohort.<a class="elsevierStyleCrossRef" href="#bib0220">44</a>The negative impact on quality of life in HIV patients diagnosed with neuroretinal disorder who suffer alterations in visual function, contrast sensitivity, and color vision has been described in different regions, such as in Ashraf’s 2015 prospective observational cross-sectional study of LSOCA study participants for a total of 813 individuals, which found that those with HIV neuroretinal disorder, unlike controls, had lower scores on the subscales: near activities (77 vs. 86; P = .004), distant activities (85 vs. 91; P = .01), social functioning (89 vs. 96; P = .0005), mental health (75 vs. 87; P = .0001), dependence (81 vs. 94; P < .0001), driving (75 vs. 85; P = .02), color vision (90 vs. 97; P < .0001), and peripheral vision (85 vs. 91; P = .0496).<a class="elsevierStyleCrossRef" href="#bib0135">27</a> Also, Freeman’s prospective, multicenter cohort study of AIDS patients, comprising 1.351 people from 19 clinical trial sites who enrolled in September 1998 in the LSOCA cohort, which observed a significant relationship between low contrast sensitivity and decreased CD4+ T-cell count levels, finding that 39% of eyes had abnormal mean deviation on automated perimetry and 12% had low contrast sensitivity.<a class="elsevierStyleCrossRef" href="#bib0225">45</a> Driving ability was also assessed in Cheng’s case-control study of patients enrolled between June 2009 and October 2009, with individuals cared for at the University of California, San Diego at the Jacobs Retina Center, which aimed to study the association between retinal nerve fiber layer (RNFL) thickness and driving ability in 38 drivers, among 22 HIV-positive participants and 16 HIV-negative controls of the same age, who completed a computer-based driving simulation, it was reported that HIV-seropositive patients showed a significantly higher weighted error score than controls (P = .006), with the highest number of driving errors occurring in people with CD4 < 100 P = .056 and retinal layer thickness <80 µm P = .025.<a class="elsevierStyleCrossRef" href="#bib0140">28</a>Cognitive impairment secondary to HIV neuroretinal disorder has been pathophysiologically and contradictorily explained by changes in retinal nerve fiber layer thickness. Invernizzi’s single-center cross-sectional study at the Luigi Sacco Hospital in Italy between January 2015 and December 2016 compared retinal layer thickness in HIV-infected subjects with and without cognitive impairment, with participants aged 40–70 years for a total of 79 individuals, 34 cognitively impaired and 35 non-cognitively impaired, as well as 70 controls; Among the findings, the ganglion cell layer was found to be significantly thinner in patients with HIV cognitive impairment compared to controls and those without cognitive impairment (P = .01 and P = .02, respectively).<a class="elsevierStyleCrossRef" href="#bib0130">26</a> On the other hand, Demirkaya’s 2016 case-control study involving patients attending the sexual health outpatient clinic of the Academic Medical Center in Amsterdam, The Netherlands, with 92 HIV-positive men with suppressed viremia on HAART for minimum 12 months and 63 uninfected controls with a minimum age of 45 years, assessed contrast sensitivity with the Pelli Robson PR CS test and temporal contrast sensitivity TCS, along with optical coherence tomography analysis, reporting, paradoxically, that the total peripheral retinal thickness in the HIV positive group increased compared to the control group (+4.6 μm, P value = .029), due to an increase in the inner nuclear layer (+1.04 μm, P value = .006) and the outer plexiform layer (+0.95 μm, P value = .006), however, the authors clarify that the decrease in contrast sensitivity in HIV patients was not clinically significant when compared to controls.<a class="elsevierStyleCrossRef" href="#bib0155">31</a>DiscussionAge, gender and ethnicityThe studies by Jabs et al. found a slight trend for the development of age-related macular degeneration and HIV-associated neuroretinal disorder starting in the fourth decade of life and female gender, with non-Hispanic white and African–American races; findings not statistically significant.<a class="elsevierStyleCrossRefs" href="#bib0195">39–42</a> the studies by Ashraf, Demirkaya and Cheng found a trend for the development of HIV-related neuroretinal disorder with median ages starting in the fifth decade of life; Ashraf’s study again observed a higher frequency of neuroretinal disorder in non-Hispanic whites and African Americans, contrasting with a higher rate of presentation in men. However, oversampling is not ruled out, given the higher male participation in the study, not statistically significant findings.<a class="elsevierStyleCrossRefs" href="#bib0135">27,28,31</a> Freeman found the mean age of 42 years as a risk factor for visual disturbances expressed in changes in visual acuity, automated perimetry and contrast sensitivity, with the clearest risk from the age of 50 years OR: 1.6 (1.1–2.5). Paradoxically, the ethnic group that had less tendency to alteration in visual function was the non-Hispanic whites.<a class="elsevierStyleCrossRef" href="#bib0225">45</a> Invernizzi showed that the mean age of 53.1 ± 7.3 years (41–70) was most associated with cognitive impairment in HIV patients related to retinal nerve fiber layer thinning. These results should be interpreted with caution given that the participants’ ages ranged from 40 to 70 years<a class="elsevierStyleCrossRef" href="#bib0130">26</a> (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>).<elsevierMultimedia ident="fig0010"></elsevierMultimedia>Route of transmission, time since diagnosis and stage of diseaseInvernizzi evidenced that mean 14.5 ± 8.6 CI 95%<a class="elsevierStyleCrossRefs" href="#bib0005">1–30</a> years since HIV diagnosis was most frequently associated with cognitive impairment related to retinal nerve fiber layer thinning in a population of participants aged 40–70 years.<a class="elsevierStyleCrossRef" href="#bib0130">26</a> Demirkaya found no statistically significant difference between route of transmission and development of neuroretinal disorder secondary to HIV; however, he reported a mean of 14.5 CI 95%<a class="elsevierStyleCrossRefs" href="#bib0005">1–27</a> years from HIV diagnosis for the development of neuroretinal disorder, The reason for the increased nerve fiber layer thickness in this study is not clearly explained, but there was still a degree of impairment of visual function with respect to impaired contrast sensitivity.<a class="elsevierStyleCrossRef" href="#bib0155">31</a> On the other hand, Ashraf mentions a mean of 11.3 years from AIDS diagnosis for the development of neuroretinal disorder.<a class="elsevierStyleCrossRef" href="#bib0135">27</a> The studies by Jabs and Ashraf suggest a slight non-significant trend towards greater development of age-related macular degeneration and neuroretinal disorder in patients who acquired AIDS through sexual contact. However, the possibility of oversampling of this predictor must be taken into account. They also reported means since diagnosis ranging from 3.9 to 4.7 years, taking into account, as previously stated, that the mean ages in these studies were found to be over the fourth decade of life, being statistically significant findings.<a class="elsevierStyleCrossRefs" href="#bib0135">27,40–42</a> Freeman observed that homosexual men and those using intravenous drugs were most at risk for developing alterations in visual function expressed as changes in visual acuity and impaired visual field; however, these results should be interpreted with caution given that 80% of the participants were men with a high probability of oversampling of this predictor<a class="elsevierStyleCrossRef" href="#bib0225">45</a> (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>).<elsevierMultimedia ident="fig0015"></elsevierMultimedia>CD4 count, viral load, diagnosis and treatmentJabs’ studies report that mean CD4 of 179 CI: (82–325) and mean viral load: 3.2 ± 1.5, P: .07 were most frequently associated with age-related macular degeneration,<a class="elsevierStyleCrossRef" href="#bib0195">39</a> with no significant difference in prevalences between nadir values or peak CD4 counts and viral load, with a slight trend to higher frequency of age-related macular degeneration in those receiving HAART<a class="elsevierStyleCrossRefs" href="#bib0130">26,40</a> and with prevalences of macular degeneration as high as 9.9%.<a class="elsevierStyleCrossRef" href="#bib0205">41</a> Jabs also found a neuroretinal disorder with mean CD4 counts between 40–184 cells/μL and mean viral loads between 2.94 and 5.30 log/copies with a slight tendency to a higher development of neuroretinal disorder among patients who received HAART for a longer time,<a class="elsevierStyleCrossRef" href="#bib0210">42</a> in Accorinti’s study it is noteworthy that in the group of subjects who received HAART, cases of neuroretinal degeneration started to appear in the group of subjects who received HAART, with a higher prevalence of age-related macular degeneration in the group of patients who received HAART, cases of macular degeneration and age-related eye diseases began to appear, findings not statistically significant,<a class="elsevierStyleCrossRef" href="#bib0215">43</a> correlating with the findings of Miller who found that, of 13.9% of patients with non-infectious retinopathy, 18.2% developed it with early HAART and 12% with late HAART in a non-significant way, P-value .4097:, 4097.<a class="elsevierStyleCrossRef" href="#bib0220">44</a> Invernizzi reported mean CD4 counts 171.8 ± 145.9 cells/μL in patients with cognitive impairment secondary to HIV, contrasting with Kuppermann who observed that non-infectious retinopathy was more frequently found with CD4 counts between zero to 50 cells/μL, diagnosing non-infectious retinopathy in 27% of individuals.<a class="elsevierStyleCrossRef" href="#bib0055">11</a> Demirkaya reported neuroretinal disorder in both high CD4 counts (595 cells/μL) of patients receiving HAART and also low nadir CD4 counts (180 cells/μL), with viral loads of 4.9 log/copies before HAART and 1.6 log/copies after starting HAART for a median of 12 years from the beginning of HAART.<a class="elsevierStyleCrossRef" href="#bib0155">31</a> Ashraf reported neuroretinal disorder with mean CD4 counts ranging from 76 to 379 with mean viral loads ranging from 1.7 to 3.4 in a non-statistically significant manner.<a class="elsevierStyleCrossRef" href="#bib0135">27</a> Nishijima observed that the risk of retinopathy per 100 cell decrease in CD4 count was adjusted, OR: 1.7 95% CI: 1.36–2.13, P-value: <.001 and the risk of retinopathy per 1 log10copies/mL increase in viral load was adjusted OR: 1.6 95% CI: 1.20–2.06, P-value: .001; with a non-significant protective trend towards those receiving antiretroviral therapy adjusted OR: 0.8 95% CI: 0.37–1.83, P-value: .63. However, these data should be interpreted with caution as the study does not clearly differentiate between infectious and non-infectious retinopathy.<a class="elsevierStyleCrossRef" href="#bib0100">20</a> Freeman found the following distribution of Snellen visual acuity <20/20, according to the different ranges of CD4 in cells/μL, as follows <50: n = 122 50–99, n = 60 100–199, n = 109 200–349, n = 107 > 350 n = 94 with non-statistically significant differences, P value: .90<a class="elsevierStyleCrossRef" href="#bib0225">45</a> (<a class="elsevierStyleCrossRef" href="#fig0020">Fig. 4</a>).<elsevierMultimedia ident="fig0020"></elsevierMultimedia>Epidemiological impact and paradigm shiftHIV/AIDS neuroretinal disease defined as an abnormality of retinal-optic nerve function, clinically manifested as decreased contrast sensitivity or color vision in the absence of opportunistic infection or media opacity, with abnormalities in automated perimetry and loss of retinal nerve fiber layers even in patients with good visual acuity,<a class="elsevierStyleCrossRefs" href="#bib0135">27,42</a> even in the HAART era, has experienced a progressive increase in prevalence due to different theories such as increased life expectancy, the state of immunosenescence or the metabolic effects of antiretroviral drugs.<a class="elsevierStyleCrossRefs" href="#bib0080">16,39–41,43,44,46</a>,<a class="elsevierStyleCrossRef" href="#bib0235">47</a> Increased rates of mortality and visual disability in patients with neuroretinal disorder and age-related macular degeneration has been suggested, with an apparent inability of antiretroviral therapy to prevent non-infectious neuroretinal disease in patients with HIV/AIDS.<a class="elsevierStyleCrossRefs" href="#bib0020">4,42,48–51</a> Ocular manifestations of any etiology occur from the age of 35 years,<a class="elsevierStyleCrossRefs" href="#bib0065">13,19</a> with a trend towards the development of age-related macular degeneration from the fourth decade of life and neuroretinal disorder from the fifth, with a higher risk of age-related macular degeneration in women, in non-Hispanic white and African-American races, and in those who acquired AIDS through sexual contact, with means from diagnosis between 3.9 and 4.7 years.<a class="elsevierStyleCrossRefs" href="#bib0195">39–42</a> However, the data are contradictory, as the neuroretinal disorder had a higher rate of presentation in men, with a slight trend toward homosexual and intravenous drug-using men, possibly due to oversampling in the studies, while non-Hispanic white and African-American races remained at highest risk. Medians between 11.3–14.5 years since HIV diagnosis were more frequently associated with cognitive impairment,<a class="elsevierStyleCrossRefs" href="#bib0130">26–28,31</a> both high and low CD4 counts and high and low viral loads presented with neuroretinal disease without significant differences, where longer duration and early initiation of HAART had a modest impact on the development of this pathology.<a class="elsevierStyleCrossRefs" href="#bib0055">11,20,26,27</a>,<a class="elsevierStyleCrossRefs" href="#bib0155">31,39–45</a> Some studies recommend immediate comprehensive ophthalmologic examination in those HIV/AIDS patients with CD4 counts <200 and in the first five years of HIV infection and in the first five years of HAART follow-up with emphasis on the prevention of visual impairment and blindness,<a class="elsevierStyleCrossRefs" href="#bib0090">18,20,52–55</a> including the use of tests such as campimetry, coherence tomography and angiography in a focused and cost-effective manner in high-risk patients who present at the ophthalmology clinic with the predictors described in this review since the decrease in visual field has been irreversibly documented, including impaired visual acuity and abnormal color vision in the advanced stages of AIDS,<a class="elsevierStyleCrossRefs" href="#bib0145">29,31,38,56</a>,<a class="elsevierStyleCrossRef" href="#bib0285">57</a> which may well be pathophysiologically related to retinovascular or optic nerve disease<a class="elsevierStyleCrossRefs" href="#bib0150">30,45,58</a> and in the case of ganglion cell layer thinning may be associated with accelerated cognitive decline<a class="elsevierStyleCrossRefs" href="#bib0130">26,27,32</a> and impaired daily living and driving skills<a class="elsevierStyleCrossRef" href="#bib0140">28</a> that will ultimately negatively impact the quality of life of this group of at-risk patients.ConclusionsHAART therapy has reduced opportunistic retinal infection; however, its role is controversial in the development of non-infectious retinopathy, so it is essential to ensure early recognition and detection of high-risk groups that present in the ophthalmological consultation with the sociodemographic predictors described in this study and thus strengthen efforts in research, prevention, diagnosis and development of novel treatments capable of halting the progression of these new diseases.FinancingThis work has not received any funding.Declaration of conflict of interestThe authors declare that they have no conflicts of interest." "textoCompletoSecciones" => array:1 [ "secciones" => array:15 [ 0 => array:3 [ "identificador" => "xres1704070" "titulo" => "Abstract" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Background" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Methods" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Discussion" ] 4 => array:2 [ "identificador" => "abst0025" "titulo" => "Conclusions" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1508572" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres1704071" "titulo" => "Resumen" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "abst0030" "titulo" => "Antecedentes" ] 1 => array:2 [ "identificador" => "abst0035" "titulo" => "Métodos" ] 2 => array:2 [ "identificador" => "abst0040" "titulo" => "Resultados" ] 3 => array:2 [ "identificador" => "abst0045" "titulo" => "Discusión" ] 4 => array:2 [ "identificador" => "abst0050" "titulo" => "Conclusiones" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec1508571" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Background" ] 5 => array:2 [ "identificador" => "sec0010" "titulo" => "Target" ] 6 => array:3 [ "identificador" => "sec0015" "titulo" => "Materials and methods" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "sec0020" "titulo" => "Study design" ] 1 => array:2 [ "identificador" => "sec0025" "titulo" => "Inclusion and exclusion criteria" ] 2 => array:2 [ "identificador" => "sec0030" "titulo" => "Literature search strategy" ] 3 => array:2 [ "identificador" => "sec0035" "titulo" => "Study selection and data extraction" ] ] ] 7 => array:2 [ "identificador" => "sec0040" "titulo" => "Results" ] 8 => array:2 [ "identificador" => "sec0045" "titulo" => "Description of the studies" ] 9 => array:3 [ "identificador" => "sec0050" "titulo" => "Discussion" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "sec0055" "titulo" => "Age, gender and ethnicity" ] 1 => array:2 [ "identificador" => "sec0060" "titulo" => "Route of transmission, time since diagnosis and stage of disease" ] 2 => array:2 [ "identificador" => "sec0065" "titulo" => "CD4 count, viral load, diagnosis and treatment" ] 3 => array:2 [ "identificador" => "sec0070" "titulo" => "Epidemiological impact and paradigm shift" ] ] ] 10 => array:2 [ "identificador" => "sec0075" "titulo" => "Conclusions" ] 11 => array:2 [ "identificador" => "sec0080" "titulo" => "Financing" ] 12 => array:2 [ "identificador" => "sec0085" "titulo" => "Declaration of conflict of interest" ] 13 => array:2 [ "identificador" => "xack600761" "titulo" => "Acknowledgements" ] 14 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2020-08-04" "fechaAceptado" => "2020-11-28" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1508572" "palabras" => array:3 [ 0 => "Age-related macular degeneration (AMD)" 1 => "Neuroretinal disorder (NRD)" 2 => "Highly active antiretroviral therapy (HAART)" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1508571" "palabras" => array:3 [ 0 => "Degeneración macular relacionada con la edad (AMD)" 1 => "Trastorno neurorretiniano (NRD)" 2 => "Tratamiento antirretroviral de gran actividad (TARGA)" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:3 [ "titulo" => "Abstract" "resumen" => "BackgroundNon-infectious retinal disease, even in the HAART era, continues to be one of the most common diagnoses in patients with HIV, with prevalences of up to 27% of cases. This study aims to characterize the association between demographic variables and their role. As a risk factor for the development of non-opportunistic non-infectious retinal disease in patients with HIV/AIDS. MethodsAn integrative review of the literature was carried out according to Arksey O’Malley’s approach, based on the PICO methodology and following the PRISMA recommendations; An exhaustive search was carried out in databases of articles that were filtered using established criteria, with their extraction and analysis carried out qualitatively. ResultsOcular manifestations from any cause develop from 35 years of age in patients with HIV/AIDS, with the highest risk for age-related macular degeneration over the fourth decade of life and for the development of neuroretinal disorder on the fifth decade of life; some studies report a slight tendency to diagnose macular degeneration in women and those who acquired AIDS through sexual contact; data contrasted with increased risk for diagnosing neuroretinal disorder in homosexual men who also use intravenous drugs, possibly due to oversampling in studies; non-Hispanic whites and African Americans were the races most commonly affected by neuroretinal disease; the means between the 11.3–14.5 years elapsed since the HIV diagnosis were more frequently associated with cognitive impairment and both in those with high or low CD4 counts, and in patients with high or low viral loads, neuroretinal disease without Statistically significant differences. Adherence and early initiation of HAART had a modest impact on the development of neuroretinal disease. DiscussionEven in the HAART era, non-infectious neuroretinal disease and cytomegalovirus retinitis remain the most frequent ocular diagnoses, however, different studies argue an increase in age-related non-infectious retinal diseases in patients with HIV, theories that are may explain by the increase in life expectancy, the metabolic effects of HAART itself or the generalized pro-inflammatory state in this group of patients, it is essential to recognize this new diagnostic challenge in order to direct preventive efforts through the use of cost-effective sociodemographic risk predictors towards that technological tools for diagnosis and treatment can be targeted. ConclusionsHIV/AIDS patients who present at the ophthalmological consultation with the suggested sociodemographic predictors have a high risk of visual impairment due to non-infectious retinopathy, therefore prevention, diagnosis and treatment efforts directed at these diseases should be increased." "secciones" => array:5 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Background" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Methods" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Discussion" ] 4 => array:2 [ "identificador" => "abst0025" "titulo" => "Conclusions" ] ] ] "es" => array:3 [ "titulo" => "Resumen" "resumen" => "AntecedentesLa enfermedad retiniana no infecciosa, aún en la era TARGA, continúa siendo uno de los diagnósticos más comunes en pacientes con VIH, con prevalencias hasta del 27% de los casos, este estudio se propone caracterizar la asociación entre unas variables demográficas y su papel como factor de riesgo para el desarrollo de enfermedad retiniana no infecciosa no oportunista en pacientes con VIH/SIDA. MétodosSe realizó una revisión integrativa de la literatura según el planteamiento de Arksey O’Malley, partiendo de la metodología PICO y siguiendo las recomendaciones PRISMA; se realizó una búsqueda exhaustiva en bases de datos de artículos que se filtraron mediante criterios establecidos, con la extracción y análisis de los mismos realizada de forma cualitativa. ResultadosLas manifestaciones oculares por cualquier causa se desarrollan desde los 35 años de edad en los pacientes con VIH/SIDA, con el mayor riesgo para degeneración macular relacionada con la edad sobre la cuarta década de vida y para el desarrollo de trastorno neurorretiniano sobre la quinta década de vida; algunos estudios reportan una ligera tendencia para diagnosticar degeneración macular en mujeres y aquellos que adquirieron el SIDA por contacto sexual; datos contrastados con un mayor riesgo para diagnosticar trastorno neurorretiniano en los hombres homosexuales que tambien usan drogas intravenosas, posiblemente por un sobremuestreo en los estudios; los blancos no hispánicos y los afroamericanos fueron las razas más comúnmente afectadas por la enfermedad neurorretiniana; las medias entre los 11,3 a 14,5 años transcurridos desde el diagnostico de VIH se asociaron más frecuentemente a trastorno cognitivo y tanto en aquellos con recuentos CD4 altos o bajos, como en pacientes con cargas virales altas o bajas se presentó enfermedad neuroretiniana sin diferencias estadisticamente significativas. La adherencia y el inició temprano de TARGA presentaron un modesto impacto en el desarrollo de enfermedad neuroretiniana. DiscusiónAún en la era TARGA, la enfermedad neurorretiniana no infecciosa y la retinitis por citomegalovirus siguen siendo los diagnósticos oculares más frecuentes, sin embargo, diferentes estudios argumentan un aumento de enfermedades retinianas no infecciosas relacionadas con la edad en los pacientes con VIH, teorías que se pueden explicar por el aumento en la expectativa de vida, los efectos metabólicos del propio TARGA o el estado proinflamatorio generalizado en este grupo de pacientes, es esencial reconocer este nuevo reto diagnóstico para dirigir esfuerzos preventivos mediante el empleo de predictores de riesgo sociodemográficos costoefectivos hacia los que se puedan focalizar herramientas tecnológicas de diagnóstico y tratamiento. ConclusionesLos pacientes VIH/SIDA que se presenten en la consulta oftalmológica con los predictores sociodemográficos sugeridos tienen un alto riesgo de discapacidad visual por retinopatía no infecciosa, por tanto se deben incrementar los esfuerzos de prevención, diagnóstico y tratamientos dirigidos a estas enfermedades." "secciones" => array:5 [ 0 => array:2 [ "identificador" => "abst0030" "titulo" => "Antecedentes" ] 1 => array:2 [ "identificador" => "abst0035" "titulo" => "Métodos" ] 2 => array:2 [ "identificador" => "abst0040" "titulo" => "Resultados" ] 3 => array:2 [ "identificador" => "abst0045" "titulo" => "Discusión" ] 4 => array:2 [ "identificador" => "abst0050" "titulo" => "Conclusiones" ] ] ] ] "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "Please cite this article as: Gómez-Gualdrón SA, Sánchez-Uzcátegui MA, Camacho-López PA. Predictores sociodemográficos asociados al espectro de enfermedad neurorretiniana no oportunista de etiología no infecciosa en pacientes con VIH/SIDA: revisión integrativa. Arch Soc Esp Oftalmol. 2021. https://doi.org/10.1016/j.oftal.2020.11.026" ] ] "apendice" => array:1 [ 0 => array:1 [ "seccion" => array:1 [ 0 => array:4 [ "apendice" => "The following is Supplementary data to this article:<elsevierMultimedia ident="upi0005"></elsevierMultimedia>" "etiqueta" => "Appendix A" "titulo" => "Supplementary data" "identificador" => "sec0095" ] ] ] ] "multimedia" => array:5 [ 0 => array:8 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 2675 "Ancho" => 2508 "Tamanyo" => 310862 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0005" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "Flowchart of the literature search." ] ] 1 => array:8 [ "identificador" => "fig0010" "etiqueta" => "Fig. 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 4126 "Ancho" => 2516 "Tamanyo" => 1072074 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0010" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "Age, sex, ethnicity." ] ] 2 => array:8 [ "identificador" => "fig0015" "etiqueta" => "Fig. 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 3474 "Ancho" => 2510 "Tamanyo" => 852782 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0015" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "Transmission pathway, time since diagnostic, stage." ] ] 3 => array:8 [ "identificador" => "fig0020" "etiqueta" => "Fig. 4" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr4.jpeg" "Alto" => 4175 "Ancho" => 2008 "Tamanyo" => 934914 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0020" "detalle" => "Fig. " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "cd4 count, diagnostic, treatment." ] ] 4 => array:5 [ "identificador" => "upi0005" "tipo" => "MULTIMEDIAECOMPONENTE" "mostrarFloat" => false "mostrarDisplay" => true "Ecomponente" => array:2 [ "fichero" => "mmc1.docx" "ficheroTamanyo" => 15213 ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:59 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Manifestations ophtalmologiques du SIDA en milieu africain. 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Sociodemographic predictors associated with the spectrum of non-opportunist neuroretinal disease of non-infectious etiology in patients with HIV/AIDS: A scoping review

Predictores sociodemográficos asociados al espectro de enfermedad neurorretiniana no oportunista de etiología no infecciosa en pacientes con VIH/SIDA: revisión integrativa

S.A. Gómez-Gualdróna,b,

Corresponding author

sergiogomez1995@hotmail.com

Corresponding author.

, M.A. Sánchez-Uzcáteguib,c, P.A. Camacho-Lópezd,e

a Universidad Pedagógica y Tecnológica de Colombia, Boyacá, Colombia

b Hospital Universitario de Santander, Santander, Colombia

c Universidad Autónoma de Bucaramanga, Bucaramanga, Colombia

d Fundación Oftalmológica de Santander – FOSCAL, Santander, Colombia

e Facultad de Ciencias de la Salud, Universidad Autónoma de Bucaramanga, Bucaramanga, Colombia

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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Background</span><p id="par0005" class="elsevierStylePara elsevierViewall">Ocular complications in patients with human immunodeficiency virus &#40;HIV&#41; can be classified into four main categories&#58; retinal vascular lesions&#44; opportunistic infections&#44; neoplasms of the ocular surface and orbit&#44; as well as neuro-ophthalmologic abnormalities&#46;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#44;2</span></a> Potential complications in a population of 40 million HIV cases worldwide&#44; where prevalences of general ocular manifestations have been reported to be between 50&#37;&#8211;75&#37; of patients&#44;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> non-infectious HIV retinopathy and cytomegalovirus retinitis&#44; even in the era of highly active antiretroviral therapy &#40;HAART&#41;&#44; have been reported to be the most frequent with prevalences between 5&#46;7&#59; 15 and 7&#46;1&#37;&#8211;10&#46;6&#37;&#44; respectively&#44;<a class="elsevierStyleCrossRefs" href="#bib0020"><span class="elsevierStyleSup">4&#8211;10</span></a> even prevalences of up to 27&#37; of cases of HIV-related non-infectious retinal vasculopathy with CD4 counts below 200&#8239;cells&#47;mm&#44;<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3&#44;11</span></a> have been reported in different regions of the world such as China&#44; India&#44; Taiwan&#44; Africa and South Korea&#44; age older than 35 years&#44; World Health Organization &#40;WHO&#41; stages III and IV and low CD4&#8239;&#60;&#8239;200&#8239;cells&#47;&#956;L&#44; have been recognized as significant risk factors for the development of HIV&#47;AIDS eye disease&#46;<a class="elsevierStyleCrossRefs" href="#bib0060"><span class="elsevierStyleSup">12&#8211;19</span></a> In Tokyo&#44; Japan&#44; a study highlighted that the risk of infectious or non-infectious HIV retinopathy for each decrease in CD4 count by values of 100&#8239;cells&#47;&#956;L along with the increase for each 1&#8239;log&#47;copies in viral load and for each decade of age from the fourth decade were statistically significant factors&#46;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">From a pathophysiological point of view&#44; non-infectious and non-opportunistic neuroretinal disease in patients with HIV&#47;AIDS progresses rapidly in European Americans with the IL-10-5&#8242;A variant &#40;RR&#8239;&#61;&#8239;2&#46;09&#41; and in African Americans with the RANTES-In1 chemokine receptor ligand polymorphism 1&#46;1 C<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">21</span></a>&#59; in populations with protective mitochondrial haplogroups such as J&#44; H3 and U5a1-15218 of the European mitochondrial macrohaplogroup we investigate the role of HAART or AIDS itself in mitochondrial toxicity that may cause accelerated progression of neuroretinal disorder&#46;<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a> The existence of a senescence state in HIV&#47;AIDS patients with dilated retinal venular diameters and shorter telomere length associated with increased age-related morbidity has been proposed&#44;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">23</span></a> with a common genetic network between age-related macular degeneration and neurodegenerative disease in HIV patients&#46;<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">24</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">Studies demonstrate foveal and pericentral neuroretinal thinning with microstructural white matter damage in children<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">25</span></a> and cognitive impairment linked to thinning of the retinal ganglion cell layer and inner plexiform layer<a class="elsevierStyleCrossRefs" href="#bib0130"><span class="elsevierStyleSup">26&#44;26&#8211;30</span></a>&#59; while another study reported&#44; paradoxically&#44; thickening of the inner nuclear and outer plexiform layers as conditions that may coexist&#44;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">31</span></a> it has been suggested that cognitive impairment may also be related to an increased concentration of beta 2-microglobulin as a marker for central nervous system &#40;CNS&#41; immune activation&#44;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">32</span></a> with visual field defects linked to a low CD4 count that on perimetry are located superiorly near the blind spot&#44; implying damage to the inferior retina near the optic disc<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">33</span></a>&#59; impaired color vision and contrast sensitivity in HIV patients are mainly linked to increasing age and advanced stages of AIDS&#46;<a class="elsevierStyleCrossRefs" href="#bib0170"><span class="elsevierStyleSup">34&#8211;38</span></a></p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Target</span><p id="par0020" class="elsevierStylePara elsevierViewall">The coexistence of infectious retinitis and non-infectious retinal disease as the most frequent ocular manifestations&#44; even in the HAART era&#44; is what motivates this study&#44; as well as the characterization of sociodemographic variables &#40;age&#44; gender&#44; ethnicity&#44; transmission risk&#44; CD4 count&#44; disease stage&#44; follow-up time since diagnosis and treatment&#41; and their association with the development of non-infectious non-opportunistic neuroretinal disease in patients with HIV&#47;AIDS&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Materials and methods</span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Study design</span><p id="par0025" class="elsevierStylePara elsevierViewall">The study is designed as an integrative review&#44; according to O&#8217;Malley&#8217;s methodology&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Inclusion and exclusion criteria</span><p id="par0030" class="elsevierStylePara elsevierViewall">Inclusion criteria for the selection of articles were defined as those original studies such as clinical trials&#44; cohort studies&#44; case-control studies&#44; systematic reviews or meta-analyses&#44; which established a direct or indirect association between neuroretinal disease and HIV&#47;AIDS&#59; without restrictions regarding the year of publication and in English or Spanish&#44; those limited to establish a link between HIV&#47;AIDS and opportunistic infectious retinal infection without including non-infectious disease among their study variables and non-original articles such as narrative reviews&#44; series or case reports and letters to the editor&#44; as well as those published in languages other than English or Spanish&#44; were excluded&#46; The search period in the databases was between January to March 2020&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Literature search strategy</span><p id="par0035" class="elsevierStylePara elsevierViewall">Based on the PICO methodology&#44; the selected articles were identified by searching PubMed&#44; PubMed Central&#44; all of Medline&#44; Ovid&#44; Scopus and Virtual Health Library databases&#59; and by using the AND&#47;OR Boolean operators&#44; different combinations of medical subject heading terms &#40;MESH&#41; were performed &#40;Appendix A&#44; Supplementary data&#41;&#58; <span class="elsevierStyleItalic">macular degeneration&#59; macular degeneration&#44; age-related&#59; acquired human immunodeficiency syndrome&#59; acquired immunodeficiency syndrome&#59; AIDS&#59; HIV&#59; human immunodeficiency virus&#44; retina&#44; optic nerve&#44; nerve fibers&#44; scanning laser polarimetry&#44; tomography&#44; optical coherence&#44; electroretinography&#44; fluorescein angiography&#44; contrast sensitivity&#44; visual fields&#44; color vision &#40;NOT cytomegalovirus&#44; opportunistic infections&#44; herpes zoster ophthalmicus&#44; cytomegalovirus retinitis&#44; ocular syphilis&#41;&#46;</span><a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">59</span></a></p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Study selection and data extraction</span><p id="par0040" class="elsevierStylePara elsevierViewall">From the initial search&#44; 86&#44;358 records were identified and then multiplied&#44; yielding 43&#44;554 articles&#46; Two researchers&#44; who reviewed the titles and abstract of each paper&#44; resolved any differences by consensus and each variable was tabulated along with the title&#44; author&#44; year of publication and description of sociodemographic variables&#46; The studies that met the eligibility and quality criteria were filtered for a total of 13 texts that were included for qualitative synthesis in the review&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a> shows the flow chart of the selected articles&#59; the present review follows the recommendations of the PRISMA methodology&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Results</span><p id="par0050" class="elsevierStylePara elsevierViewall">For the presentation of the results&#44; initially a general description of the studies was made&#44; including the type of study&#44; the regions where they were conducted and the years of publication&#44; together with the most important conclusions of each work&#46; Subsequently&#44; the qualitative tabulation of each sociodemographic variable was made and the results were reported around the sociodemographic variables of interest&#44; focusing the analysis on the elements of inferential statistics&#44; measures of association and statistical significance that the different authors proposed in their research&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0115">Description of the studies</span><p id="par0055" class="elsevierStylePara elsevierViewall">Mortality from age-related causes and chronic noncommunicable diseases tends to increase in patients with HIV and AIDS who have good adherence to HAART&#46; Jabs et al&#46;&#44; in their case-control study of participants in the Longitudinal Study of Ocular Complications of AIDS &#40;LSOCA&#41; cohort who were diagnosed with intermediate-stage age-related macular degeneration by analysis of retinal photographs analyzed at the University of Wisconsin-Madison School of Medicine and Public Health Department of Ophthalmology and Visual Sciences Reading Center in 2019&#44; found that macular degeneration in patients with AIDS was associated with increased mortality&#44; <span class="elsevierStyleItalic">hazard ratio</span> &#40;HR&#41;&#58; 1&#46;48 95&#37; CI&#58; 1&#46;02&#8211;2&#46;15&#44; <span class="elsevierStyleItalic">P</span>-value&#8239;&#61;&#8239;&#46;04&#44; in association with increased inflammatory biomarkers such as polymerase chain reaction &#40;PCR&#41; test&#44; interleukin-6 &#40;IL-6&#41; and IP-10 protein&#46;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">39</span></a></p><p id="par0060" class="elsevierStylePara elsevierViewall">Similarly&#44; the accelerated rate of age-related chronic noncommunicable disease presentation in patients with HIV or AIDS was also illustrated by Jabs et al&#46; in their cohort study of LSOCA patients enrolled between September 1&#44; 1998 and July 31&#44; 2011 at 19 clinical centers in the United States&#44; who underwent retinal photography at 5 and 10 years of follow-up&#44; finding an incidence of age-related macular degeneration of 0&#46;65&#47;100 person-years&#44; with smoking as the only significant risk factor for developing this pathology and with a 1&#46;75-fold risk &#40;95&#37; CI 1&#46;16&#44; 2&#46;64&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;008&#41; relative to the control cohort of the Multi-Ethnic Study of Atherosclerosis &#40;MESA&#41;&#46; Even though the mean age in the MESA cohort was 17 years older than in LSOCA &#40;61&#8239;&#177;&#8239;nine years vs&#46; 44&#8239;&#177;&#8239;eight years&#41;<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">40</span></a>&#59; or in their 2015 cross-sectional study&#44; where Jabs et al&#46; found that of 1&#46;825 participants with AIDS&#44; 9&#46;9&#37; had mid-stage age-related macular degeneration&#44; which&#44; when compared to cases in the uninfected Beaver Deam cohort study&#44; found a fourfold higher prevalence of macular degeneration in LSOCA&#44; with a risk per decade of age OR 1&#46;9 &#40;95&#37; CI 1&#46;6&#44; 2&#46;3&#44; <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;001&#41;&#44; with prevalences of 4&#46;0&#37; for those aged 30&#8211;39 years and 24&#46;3&#37; for those &#62;60 years&#44; where injection drug use &#40;OR&#8239;&#61;&#8239;2&#46;4&#44; 95&#37; CI 1&#46;5&#44; 3&#46;9&#44; <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;001&#41; and risk from heterosexual contact were significant risk factors &#40;OR&#8239;&#61;&#8239;1&#46;9&#44; 95&#37; CI 1&#46;3&#44; 2&#46;8&#44; <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;001&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">41</span></a></p><p id="par0065" class="elsevierStylePara elsevierViewall">Some associations with sociodemographic variables were explicitly and statistically significantly reported by the work of Jabs et al&#46; in their 2015 cohort study of 1822 AIDS patients diagnosed with neuroretinal disorder&#44; where they found that 16&#37; of participants had neuroretinal disorder at enrollment&#44; with a 20-year cumulative incidence of 51&#37; &#40;95&#37; CI&#44; 46&#8211;55&#41;&#44; a finding that was more common in women and African Americans&#44; with mortality adjusted for low CD4 counts and detectable viral load in patients with neuroretinal disorder HR&#44; 1&#46;7&#59; 95&#37; CI&#44; 1&#46;3&#8211;2&#46;1&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;0001&#41;&#44; with increased risks of bilateral visual impairment HR&#44; 6&#46;5&#59; 95&#37; CI&#44; 2&#46;6&#8211;10&#46;6&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;0001&#41; and blindness HR&#44; 5&#46;9&#59; 95&#37; CI&#44; 2&#46;8&#8211;13&#46;7&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;0&#46;<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">42</span></a></p><p id="par0070" class="elsevierStylePara elsevierViewall">The relationship between CD4 count levels and viral loads versus the development of neuroretinal disease qualitatively does not allow us to establish a clear trend towards infectious or non-infectious retinopathy&#44; since both conditions occur indistinctly at high or low CD4 counts and at high or low viral loads&#46; The results are illustrated in Nishijima&#8217;s retrospective study of patients examined at the AIDS Clinical Center&#44; Tokyo Japan&#44; HIV-1 infected patients aged 17 years and older and enrolled between January 2004 and December 2013&#44; with 1515 participants&#46; HIV retinopathy was diagnosed in 127 &#40;8&#37;&#41;&#44; with CD4 count&#8239;&#60;&#8239;&#46;200&#47;&#956;L in all cases of cytomegalovirus retinitis and HIV retinopathy&#44;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a> contrasting with Kuppermann&#8217;s prospective study of patients examined at the University of California&#44; San Diego&#44; during a period between September 16&#44; 1991&#44; to October 30&#44; 1991&#44; finding that of 132 persons with AIDS&#44; 46 &#40;35&#37;&#41; had HIV-related noninfectious retinal vasculopathy&#44; of which 39 of 87 &#40;45&#37;&#41; patients with CD4 counts of &#60;50&#8239;cells&#47;mm<span class="elsevierStyleSup">3</span> had HIV-related non-infectious retinal vasculopathy&#44; while seven of 45 &#40;16&#37;&#41; with CD4 counts of &#62;50&#8239;cells&#47;mm<span class="elsevierStyleSup">3</span> also had these changes&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a></p><p id="par0075" class="elsevierStylePara elsevierViewall">Progression to non-infectious neuroretinal disease appears to be positively influenced by adherence to modern HAART&#44; findings illustrated in Accorinti&#8217;s retrospective study of patients examined at the Department of Ophthalmological Sciences of the University of Rome from 1997 to 2003&#44; with 735 individuals treated with HAART for at least two months &#40;group 1&#41; and 838 examined untreated from 1988 to 1995 &#40;group 2&#41;&#44; finding that&#44; in the group of patients treated with HAART&#44; the prevalence of age-related ocular manifestations was significantly higher&#46;<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">43</span></a> Also&#44; Miller&#8217;s retrospective study of patients analyzed at the <span class="elsevierStyleItalic">Wills Eye Institute</span> and Thomas Jefferson University Hospitals&#44; where 222 admissions were reviewed for a total of 188 subjects divided into two groups from 1995 to 2003 and the second group between 2003 and 2010&#44; reporting a decrease in opportunistic disease in the second cohort with an increase in retinal disease of non-infectious etiology explained&#44; apparently&#44; by earlier onset and greater adherence to HAART in the second cohort&#46;<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">44</span></a></p><p id="par0080" class="elsevierStylePara elsevierViewall">The negative impact on quality of life in HIV patients diagnosed with neuroretinal disorder who suffer alterations in visual function&#44; contrast sensitivity&#44; and color vision has been described in different regions&#44; such as in Ashraf&#8217;s 2015 prospective observational cross-sectional study of LSOCA study participants for a total of 813 individuals&#44; which found that those with HIV neuroretinal disorder&#44; unlike controls&#44; had lower scores on the subscales&#58; near activities &#40;77 vs&#46; 86&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;004&#41;&#44; distant activities &#40;85 vs&#46; 91&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;01&#41;&#44; social functioning &#40;89 vs&#46; 96&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;0005&#41;&#44; mental health &#40;75 vs&#46; 87&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;0001&#41;&#44; dependence &#40;81 vs&#46; 94&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;0001&#41;&#44; driving &#40;75 vs&#46; 85&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;02&#41;&#44; color vision &#40;90 vs&#46; 97&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#60;&#8239;&#46;0001&#41;&#44; and peripheral vision &#40;85 vs&#46; 91&#59; <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;0496&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">27</span></a> Also&#44; Freeman&#8217;s prospective&#44; multicenter cohort study of AIDS patients&#44; comprising 1&#46;351 people from 19 clinical trial sites who enrolled in September 1998 in the LSOCA cohort&#44; which observed a significant relationship between low contrast sensitivity and decreased CD4&#43; T-cell count levels&#44; finding that 39&#37; of eyes had abnormal mean deviation on automated perimetry and 12&#37; had low contrast sensitivity&#46;<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">45</span></a> Driving ability was also assessed in Cheng&#8217;s case-control study of patients enrolled between June 2009 and October 2009&#44; with individuals cared for at the University of California&#44; San Diego at the Jacobs Retina Center&#44; which aimed to study the association between retinal nerve fiber layer &#40;RNFL&#41; thickness and driving ability in 38 drivers&#44; among 22 HIV-positive participants and 16 HIV-negative controls of the same age&#44; who completed a computer-based driving simulation&#44; it was reported that HIV-seropositive patients showed a significantly higher weighted error score than controls &#40;<span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;006&#41;&#44; with the highest number of driving errors occurring in people with CD4&#8239;&#60;&#8239;100 <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;056 and retinal layer thickness &#60;80&#8239;&#181;m <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;025&#46;<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">28</span></a></p><p id="par0085" class="elsevierStylePara elsevierViewall">Cognitive impairment secondary to HIV neuroretinal disorder has been pathophysiologically and contradictorily explained by changes in retinal nerve fiber layer thickness&#46; Invernizzi&#8217;s single-center cross-sectional study at the Luigi Sacco Hospital in Italy between January 2015 and December 2016 compared retinal layer thickness in HIV-infected subjects with and without cognitive impairment&#44; with participants aged 40&#8211;70 years for a total of 79 individuals&#44; 34 cognitively impaired and 35 non-cognitively impaired&#44; as well as 70 controls&#59; Among the findings&#44; the ganglion cell layer was found to be significantly thinner in patients with HIV cognitive impairment compared to controls and those without cognitive impairment &#40;<span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;01 and <span class="elsevierStyleItalic">P</span>&#8239;&#61;&#8239;&#46;02&#44; respectively&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">26</span></a> On the other hand&#44; Demirkaya&#8217;s 2016 case-control study involving patients attending the sexual health outpatient clinic of the Academic Medical Center in Amsterdam&#44; The Netherlands&#44; with 92 HIV-positive men with suppressed viremia on HAART for minimum 12 months and 63 uninfected controls with a minimum age of 45 years&#44; assessed contrast sensitivity with the Pelli Robson PR CS test and temporal contrast sensitivity TCS&#44; along with optical coherence tomography analysis&#44; reporting&#44; paradoxically&#44; that the total peripheral retinal thickness in the HIV positive group increased compared to the control group &#40;&#43;4&#46;6&#8239;&#956;m&#44; <span class="elsevierStyleItalic">P</span> value&#8239;&#61;&#8239;&#46;029&#41;&#44; due to an increase in the inner nuclear layer &#40;&#43;1&#46;04&#8239;&#956;m&#44; <span class="elsevierStyleItalic">P</span> value&#8239;&#61;&#8239;&#46;006&#41; and the outer plexiform layer &#40;&#43;0&#46;95&#8239;&#956;m&#44; <span class="elsevierStyleItalic">P</span> value&#8239;&#61;&#8239;&#46;006&#41;&#44; however&#44; the authors clarify that the decrease in contrast sensitivity in HIV patients was not clinically significant when compared to controls&#46;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">31</span></a></p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0120">Discussion</span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0125">Age&#44; gender and ethnicity</span><p id="par0090" class="elsevierStylePara elsevierViewall">The studies by Jabs et al&#46; found a slight trend for the development of age-related macular degeneration and HIV-associated neuroretinal disorder starting in the fourth decade of life and female gender&#44; with non-Hispanic white and African&#8211;American races&#59; findings not statistically significant&#46;<a class="elsevierStyleCrossRefs" href="#bib0195"><span class="elsevierStyleSup">39&#8211;42</span></a> the studies by Ashraf&#44; Demirkaya and Cheng found a trend for the development of HIV-related neuroretinal disorder with median ages starting in the fifth decade of life&#59; Ashraf&#8217;s study again observed a higher frequency of neuroretinal disorder in non-Hispanic whites and African Americans&#44; contrasting with a higher rate of presentation in men&#46; However&#44; oversampling is not ruled out&#44; given the higher male participation in the study&#44; not statistically significant findings&#46;<a class="elsevierStyleCrossRefs" href="#bib0135"><span class="elsevierStyleSup">27&#44;28&#44;31</span></a> Freeman found the mean age of 42 years as a risk factor for visual disturbances expressed in changes in visual acuity&#44; automated perimetry and contrast sensitivity&#44; with the clearest risk from the age of 50 years OR&#58; 1&#46;6 &#40;1&#46;1&#8211;2&#46;5&#41;&#46; Paradoxically&#44; the ethnic group that had less tendency to alteration in visual function was the non-Hispanic whites&#46;<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">45</span></a> Invernizzi showed that the mean age of 53&#46;1&#8239;&#177;&#8239;7&#46;3 years &#40;41&#8211;70&#41; was most associated with cognitive impairment in HIV patients related to retinal nerve fiber layer thinning&#46; These results should be interpreted with caution given that the participants&#8217; ages ranged from 40 to 70 years<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">26</span></a> &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0130">Route of transmission&#44; time since diagnosis and stage of disease</span><p id="par0095" class="elsevierStylePara elsevierViewall">Invernizzi evidenced that mean 14&#46;5&#8239;&#177;&#8239;8&#46;6 CI 95&#37;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#8211;30</span></a> years since HIV diagnosis was most frequently associated with cognitive impairment related to retinal nerve fiber layer thinning in a population of participants aged 40&#8211;70 years&#46;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">26</span></a> Demirkaya found no statistically significant difference between route of transmission and development of neuroretinal disorder secondary to HIV&#59; however&#44; he reported a mean of 14&#46;5 CI 95&#37;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#8211;27</span></a> years from HIV diagnosis for the development of neuroretinal disorder&#44; The reason for the increased nerve fiber layer thickness in this study is not clearly explained&#44; but there was still a degree of impairment of visual function with respect to impaired contrast sensitivity&#46;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">31</span></a> On the other hand&#44; Ashraf mentions a mean of 11&#46;3 years from AIDS diagnosis for the development of neuroretinal disorder&#46;<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">27</span></a> The studies by Jabs and Ashraf suggest a slight non-significant trend towards greater development of age-related macular degeneration and neuroretinal disorder in patients who acquired AIDS through sexual contact&#46; However&#44; the possibility of oversampling of this predictor must be taken into account&#46; They also reported means since diagnosis ranging from 3&#46;9 to 4&#46;7 years&#44; taking into account&#44; as previously stated&#44; that the mean ages in these studies were found to be over the fourth decade of life&#44; being statistically significant findings&#46;<a class="elsevierStyleCrossRefs" href="#bib0135"><span class="elsevierStyleSup">27&#44;40&#8211;42</span></a> Freeman observed that homosexual men and those using intravenous drugs were most at risk for developing alterations in visual function expressed as changes in visual acuity and impaired visual field&#59; however&#44; these results should be interpreted with caution given that 80&#37; of the participants were men with a high probability of oversampling of this predictor<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">45</span></a> &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0135">CD4 count&#44; viral load&#44; diagnosis and treatment</span><p id="par0100" class="elsevierStylePara elsevierViewall">Jabs&#8217; studies report that mean CD4 of 179 CI&#58; &#40;82&#8211;325&#41; and mean viral load&#58; 3&#46;2&#8239;&#177;&#8239;1&#46;5&#44; <span class="elsevierStyleItalic">P</span>&#58; &#46;07 were most frequently associated with age-related macular degeneration&#44;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">39</span></a> with no significant difference in prevalences between nadir values or peak CD4 counts and viral load&#44; with a slight trend to higher frequency of age-related macular degeneration in those receiving HAART<a class="elsevierStyleCrossRefs" href="#bib0130"><span class="elsevierStyleSup">26&#44;40</span></a> and with prevalences of macular degeneration as high as 9&#46;9&#37;&#46;<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">41</span></a> Jabs also found a neuroretinal disorder with mean CD4 counts between 40&#8211;184&#8239;cells&#47;&#956;L and mean viral loads between 2&#46;94 and 5&#46;30&#8239;log&#47;copies with a slight tendency to a higher development of neuroretinal disorder among patients who received HAART for a longer time&#44;<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">42</span></a> in Accorinti&#8217;s study it is noteworthy that in the group of subjects who received HAART&#44; cases of neuroretinal degeneration started to appear in the group of subjects who received HAART&#44; with a higher prevalence of age-related macular degeneration in the group of patients who received HAART&#44; cases of macular degeneration and age-related eye diseases began to appear&#44; findings not statistically significant&#44;<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">43</span></a> correlating with the findings of Miller who found that&#44; of 13&#46;9&#37; of patients with non-infectious retinopathy&#44; 18&#46;2&#37; developed it with early HAART and 12&#37; with late HAART in a non-significant way&#44; <span class="elsevierStyleItalic">P</span>-value &#46;4097&#58;&#44; 4097&#46;<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">44</span></a> Invernizzi reported mean CD4 counts 171&#46;8&#8239;&#177;&#8239;145&#46;9&#8239;cells&#47;&#956;L in patients with cognitive impairment secondary to HIV&#44; contrasting with Kuppermann who observed that non-infectious retinopathy was more frequently found with CD4 counts between zero to 50&#8239;cells&#47;&#956;L&#44; diagnosing non-infectious retinopathy in 27&#37; of individuals&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> Demirkaya reported neuroretinal disorder in both high CD4 counts &#40;595&#8239;cells&#47;&#956;L&#41; of patients receiving HAART and also low nadir CD4 counts &#40;180&#8239;cells&#47;&#956;L&#41;&#44; with viral loads of 4&#46;9 log&#47;copies before HAART and 1&#46;6 log&#47;copies after starting HAART for a median of 12 years from the beginning of HAART&#46;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">31</span></a> Ashraf reported neuroretinal disorder with mean CD4 counts ranging from 76 to 379 with mean viral loads ranging from 1&#46;7 to 3&#46;4 in a non-statistically significant manner&#46;<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">27</span></a> Nishijima observed that the risk of retinopathy per 100 cell decrease in CD4 count was adjusted&#44; OR&#58; 1&#46;7 95&#37; CI&#58; 1&#46;36&#8211;2&#46;13&#44; <span class="elsevierStyleItalic">P</span>-value&#58; &#60;&#46;001 and the risk of retinopathy per 1 log10copies&#47;mL increase in viral load was adjusted OR&#58; 1&#46;6 95&#37; CI&#58; 1&#46;20&#8211;2&#46;06&#44; <span class="elsevierStyleItalic">P</span>-value&#58; &#46;001&#59; with a non-significant protective trend towards those receiving antiretroviral therapy adjusted OR&#58; 0&#46;8 95&#37; CI&#58; 0&#46;37&#8211;1&#46;83&#44; <span class="elsevierStyleItalic">P</span>-value&#58; &#46;63&#46; However&#44; these data should be interpreted with caution as the study does not clearly differentiate between infectious and non-infectious retinopathy&#46;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a> Freeman found the following distribution of Snellen visual acuity &#60;20&#47;20&#44; according to the different ranges of CD4 in cells&#47;&#956;L&#44; as follows &#60;50&#58; n&#8239;&#61;&#8239;122 50&#8211;99&#44; n&#8239;&#61;&#8239;60 100&#8211;199&#44; n&#8239;&#61;&#8239;109 200&#8211;349&#44; n&#8239;&#61;&#8239;107&#8239;&#62;&#8239;350 n&#8239;&#61;&#8239;94 with non-statistically significant differences&#44; <span class="elsevierStyleItalic">P</span> value&#58; &#46;90<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">45</span></a> &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>&#41;&#46;</p><elsevierMultimedia ident="fig0020"></elsevierMultimedia></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0140">Epidemiological impact and paradigm shift</span><p id="par0105" class="elsevierStylePara elsevierViewall">HIV&#47;AIDS neuroretinal disease defined as an abnormality of retinal-optic nerve function&#44; clinically manifested as decreased contrast sensitivity or color vision in the absence of opportunistic infection or media opacity&#44; with abnormalities in automated perimetry and loss of retinal nerve fiber layers even in patients with good visual acuity&#44;<a class="elsevierStyleCrossRefs" href="#bib0135"><span class="elsevierStyleSup">27&#44;42</span></a> even in the HAART era&#44; has experienced a progressive increase in prevalence due to different theories such as increased life expectancy&#44; the state of immunosenescence or the metabolic effects of antiretroviral drugs&#46;<a class="elsevierStyleCrossRefs" href="#bib0080"><span class="elsevierStyleSup">16&#44;39&#8211;41&#44;43&#44;44&#44;46</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">47</span></a> Increased rates of mortality and visual disability in patients with neuroretinal disorder and age-related macular degeneration has been suggested&#44; with an apparent inability of antiretroviral therapy to prevent non-infectious neuroretinal disease in patients with HIV&#47;AIDS&#46;<a class="elsevierStyleCrossRefs" href="#bib0020"><span class="elsevierStyleSup">4&#44;42&#44;48&#8211;51</span></a> Ocular manifestations of any etiology occur from the age of 35 years&#44;<a class="elsevierStyleCrossRefs" href="#bib0065"><span class="elsevierStyleSup">13&#44;19</span></a> with a trend towards the development of age-related macular degeneration from the fourth decade of life and neuroretinal disorder from the fifth&#44; with a higher risk of age-related macular degeneration in women&#44; in non-Hispanic white and African-American races&#44; and in those who acquired AIDS through sexual contact&#44; with means from diagnosis between 3&#46;9 and 4&#46;7 years&#46;<a class="elsevierStyleCrossRefs" href="#bib0195"><span class="elsevierStyleSup">39&#8211;42</span></a> However&#44; the data are contradictory&#44; as the neuroretinal disorder had a higher rate of presentation in men&#44; with a slight trend toward homosexual and intravenous drug-using men&#44; possibly due to oversampling in the studies&#44; while non-Hispanic white and African-American races remained at highest risk&#46; Medians between 11&#46;3&#8211;14&#46;5 years since HIV diagnosis were more frequently associated with cognitive impairment&#44;<a class="elsevierStyleCrossRefs" href="#bib0130"><span class="elsevierStyleSup">26&#8211;28&#44;31</span></a> both high and low CD4 counts and high and low viral loads presented with neuroretinal disease without significant differences&#44; where longer duration and early initiation of HAART had a modest impact on the development of this pathology&#46;<a class="elsevierStyleCrossRefs" href="#bib0055"><span class="elsevierStyleSup">11&#44;20&#44;26&#44;27</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRefs" href="#bib0155"><span class="elsevierStyleSup">31&#44;39&#8211;45</span></a> Some studies recommend immediate comprehensive ophthalmologic examination in those HIV&#47;AIDS patients with CD4 counts &#60;200 and in the first five years of HIV infection and in the first five years of HAART follow-up with emphasis on the prevention of visual impairment and blindness&#44;<a class="elsevierStyleCrossRefs" href="#bib0090"><span class="elsevierStyleSup">18&#44;20&#44;52&#8211;55</span></a> including the use of tests such as campimetry&#44; coherence tomography and angiography in a focused and cost-effective manner in high-risk patients who present at the ophthalmology clinic with the predictors described in this review since the decrease in visual field has been irreversibly documented&#44; including impaired visual acuity and abnormal color vision in the advanced stages of AIDS&#44;<a class="elsevierStyleCrossRefs" href="#bib0145"><span class="elsevierStyleSup">29&#44;31&#44;38&#44;56</span></a><span class="elsevierStyleSup">&#44;</span><a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">57</span></a> which may well be pathophysiologically related to retinovascular or optic nerve disease<a class="elsevierStyleCrossRefs" href="#bib0150"><span class="elsevierStyleSup">30&#44;45&#44;58</span></a> and in the case of ganglion cell layer thinning may be associated with accelerated cognitive decline<a class="elsevierStyleCrossRefs" href="#bib0130"><span class="elsevierStyleSup">26&#44;27&#44;32</span></a> and impaired daily living and driving skills<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">28</span></a> that will ultimately negatively impact the quality of life of this group of at-risk patients&#46;</p></span></span><span id="sec0075" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0145">Conclusions</span><p id="par0110" class="elsevierStylePara elsevierViewall">HAART therapy has reduced opportunistic retinal infection&#59; however&#44; its role is controversial in the development of non-infectious retinopathy&#44; so it is essential to ensure early recognition and detection of high-risk groups that present in the ophthalmological consultation with the sociodemographic predictors described in this study and thus strengthen efforts in research&#44; prevention&#44; diagnosis and development of novel treatments capable of halting the progression of these new diseases&#46;</p></span><span id="sec0080" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0150">Financing</span><p id="par0115" class="elsevierStylePara elsevierViewall">This work has not received any funding&#46;</p></span><span id="sec0085" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0155">Declaration of conflict of interest</span><p id="par0120" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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          "titulo" => "Financing"
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          "identificador" => "sec0085"
          "titulo" => "Declaration of conflict of interest"
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        13 => array:2 [
          "identificador" => "xack600761"
          "titulo" => "Acknowledgements"
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        14 => array:1 [
          "titulo" => "References"
        ]
      ]
    ]
    "pdfFichero" => "main.pdf"
    "tienePdf" => true
    "fechaRecibido" => "2020-08-04"
    "fechaAceptado" => "2020-11-28"
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        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Keywords"
          "identificador" => "xpalclavsec1508572"
          "palabras" => array:3 [
            0 => "Age-related macular degeneration &#40;AMD&#41;"
            1 => "Neuroretinal disorder &#40;NRD&#41;"
            2 => "Highly active antiretroviral therapy &#40;HAART&#41;"
          ]
        ]
      ]
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          "titulo" => "Palabras clave"
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          "palabras" => array:3 [
            0 => "Degeneraci&#243;n macular relacionada con la edad &#40;AMD&#41;"
            1 => "Trastorno neurorretiniano &#40;NRD&#41;"
            2 => "Tratamiento antirretroviral de gran actividad &#40;TARGA&#41;"
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      "en" => array:3 [
        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Background</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Non-infectious retinal disease&#44; even in the HAART era&#44; continues to be one of the most common diagnoses in patients with HIV&#44; with prevalences of up to 27&#37; of cases&#46; This study aims to characterize the association between demographic variables and their role&#46; As a risk factor for the development of non-opportunistic non-infectious retinal disease in patients with HIV&#47;AIDS&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Methods</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">An integrative review of the literature was carried out according to Arksey O&#8217;Malley&#8217;s approach&#44; based on the PICO methodology and following the PRISMA recommendations&#59; An exhaustive search was carried out in databases of articles that were filtered using established criteria&#44; with their extraction and analysis carried out qualitatively&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Ocular manifestations from any cause develop from 35 years of age in patients with HIV&#47;AIDS&#44; with the highest risk for age-related macular degeneration over the fourth decade of life and for the development of neuroretinal disorder on the fifth decade of life&#59; some studies report a slight tendency to diagnose macular degeneration in women and those who acquired AIDS through sexual contact&#59; data contrasted with increased risk for diagnosing neuroretinal disorder in homosexual men who also use intravenous drugs&#44; possibly due to oversampling in studies&#59; non-Hispanic whites and African Americans were the races most commonly affected by neuroretinal disease&#59; the means between the 11&#46;3&#8211;14&#46;5 years elapsed since the HIV diagnosis were more frequently associated with cognitive impairment and both in those with high or low CD4 counts&#44; and in patients with high or low viral loads&#44; neuroretinal disease without Statistically significant differences&#46; Adherence and early initiation of HAART had a modest impact on the development of neuroretinal disease&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Discussion</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Even in the HAART era&#44; non-infectious neuroretinal disease and cytomegalovirus retinitis remain the most frequent ocular diagnoses&#44; however&#44; different studies argue an increase in age-related non-infectious retinal diseases in patients with HIV&#44; theories that are may explain by the increase in life expectancy&#44; the metabolic effects of HAART itself or the generalized pro-inflammatory state in this group of patients&#44; it is essential to recognize this new diagnostic challenge in order to direct preventive efforts through the use of cost-effective sociodemographic risk predictors towards that technological tools for diagnosis and treatment can be targeted&#46;</p></span> <span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Conclusions</span><p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">HIV&#47;AIDS patients who present at the ophthalmological consultation with the suggested sociodemographic predictors have a high risk of visual impairment due to non-infectious retinopathy&#44; therefore prevention&#44; diagnosis and treatment efforts directed at these diseases should be increased&#46;</p></span>"
        "secciones" => array:5 [
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            "titulo" => "Background"
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            "titulo" => "Methods"
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          2 => array:2 [
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            "titulo" => "Results"
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            "titulo" => "Discussion"
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        "titulo" => "Resumen"
        "resumen" => "<span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Antecedentes</span><p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">La enfermedad retiniana no infecciosa&#44; a&#250;n en la era TARGA&#44; contin&#250;a siendo uno de los diagn&#243;sticos m&#225;s comunes en pacientes con VIH&#44; con prevalencias hasta del 27&#37; de los casos&#44; este estudio se propone caracterizar la asociaci&#243;n entre unas variables demogr&#225;ficas y su papel como factor de riesgo para el desarrollo de enfermedad retiniana no infecciosa no oportunista en pacientes con VIH&#47;SIDA&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">M&#233;todos</span><p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Se realiz&#243; una revisi&#243;n integrativa de la literatura seg&#250;n el planteamiento de Arksey O&#8217;Malley&#44; partiendo de la metodolog&#237;a PICO y siguiendo las recomendaciones PRISMA&#59; se realiz&#243; una b&#250;squeda exhaustiva en bases de datos de art&#237;culos que se filtraron mediante criterios establecidos&#44; con la extracci&#243;n y an&#225;lisis de los mismos realizada de forma cualitativa&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Resultados</span><p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">Las manifestaciones oculares por cualquier causa se desarrollan desde los 35 a&#241;os de edad en los pacientes con VIH&#47;SIDA&#44; con el mayor riesgo para degeneraci&#243;n macular relacionada con la edad sobre la cuarta d&#233;cada de vida y para el desarrollo de trastorno neurorretiniano sobre la quinta d&#233;cada de vida&#59; algunos estudios reportan una ligera tendencia para diagnosticar degeneraci&#243;n macular en mujeres y aquellos que adquirieron el SIDA por contacto sexual&#59; datos contrastados con un mayor riesgo para diagnosticar trastorno neurorretiniano en los hombres homosexuales que tambien usan drogas intravenosas&#44; posiblemente por un sobremuestreo en los estudios&#59; los blancos no hisp&#225;nicos y los afroamericanos fueron las razas m&#225;s com&#250;nmente afectadas por la enfermedad neurorretiniana&#59; las medias entre los 11&#44;3 a 14&#44;5 a&#241;os transcurridos desde el diagnostico de VIH se asociaron m&#225;s frecuentemente a trastorno cognitivo y tanto en aquellos con recuentos CD4 altos o bajos&#44; como en pacientes con cargas virales altas o bajas se present&#243; enfermedad neuroretiniana sin diferencias estadisticamente significativas&#46; La adherencia y el inici&#243; temprano de TARGA presentaron un modesto impacto en el desarrollo de enfermedad neuroretiniana&#46;</p></span> <span id="abst0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Discusi&#243;n</span><p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">A&#250;n en la era TARGA&#44; la enfermedad neurorretiniana no infecciosa y la retinitis por citomegalovirus siguen siendo los diagn&#243;sticos oculares m&#225;s frecuentes&#44; sin embargo&#44; diferentes estudios argumentan un aumento de enfermedades retinianas no infecciosas relacionadas con la edad en los pacientes con VIH&#44; teor&#237;as que se pueden explicar por el aumento en la expectativa de vida&#44; los efectos metab&#243;licos del propio TARGA o el estado proinflamatorio generalizado en este grupo de pacientes&#44; es esencial reconocer este nuevo reto diagn&#243;stico para dirigir esfuerzos preventivos mediante el empleo de predictores de riesgo sociodemogr&#225;ficos costoefectivos hacia los que se puedan focalizar herramientas tecnol&#243;gicas de diagn&#243;stico y tratamiento&#46;</p></span> <span id="abst0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Conclusiones</span><p id="spar0070" class="elsevierStyleSimplePara elsevierViewall">Los pacientes VIH&#47;SIDA que se presenten en la consulta oftalmol&#243;gica con los predictores sociodemogr&#225;ficos sugeridos tienen un alto riesgo de discapacidad visual por retinopat&#237;a no infecciosa&#44; por tanto se deben incrementar los esfuerzos de prevenci&#243;n&#44; diagn&#243;stico y tratamientos dirigidos a estas enfermedades&#46;</p></span>"
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        "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as&#58; G&#243;mez-Gualdr&#243;n SA&#44; S&#225;nchez-Uzc&#225;tegui MA&#44; Camacho-L&#243;pez PA&#46; Predictores sociodemogr&#225;ficos asociados al espectro de enfermedad neurorretiniana no oportunista de etiolog&#237;a no infecciosa en pacientes con VIH&#47;SIDA&#58; revisi&#243;n integrativa&#46; Arch Soc Esp Oftalmol&#46; 2021&#46; <span class="elsevierStyleInterRef" id="intr0005" href="https://doi.org/10.1016/j.oftal.2020.11.026">https&#58;&#47;&#47;doi&#46;org&#47;10&#46;1016&#47;j&#46;oftal&#46;2020&#46;11&#46;026</span></p>"
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