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Like Illness in an Otherwise Healthy Adult Outpatient Cohort Original research Effects of human immunodeficiency virus status J Investig Med: first published as 10.1136/jim-2020-001694 on 23 April 2021. Downloaded from on symptom severity in influenza- like illness in an otherwise healthy adult outpatient cohort Rhonda E Colombo ,1,2,3 Christina Schofield,1,2 Stephanie A Richard,2,3 Mary Fairchok,1,2,3 Wei- Ju Chen,2,3 Patrick J Danaher,4 Tahaniyat N Lalani,2,3,5 Michelande Ridoré,2,3 Ryan C Maves,6 John C Arnold,7 Anuradha Ganesan,2,3,8 Brian Agan,2,3 Eugene V Millar,2,3 Christian Coles,2,3 Timothy H Burgess2 ► Additional supplemental ABSTRACT Significance of this study material is published online The impact of HIV on influenza- like illness (ILI) only. To view, please visit has been incompletely described in the era of the journal online (http:// dx. What is already known about this subject? doi. org/ 10. 1136/ jim- 2020- combination antiretroviral therapy, particularly in the 001694). post- H1N1 pandemic period. This analysis informs ► The relative contribution of specific on ILI in an otherwise healthy, predominantly respiratory viruses to acute respiratory For numbered affiliations see illness is likely to vary by season and end of article. outpatient cohort of adults with HIV in the USA. From September 2010 to March 2015, this multisite patient population. Correspondence to observational cohort study enrolled otherwise ► HIV has been described as a risk factor Dr Rhonda E Colombo healthy adults presenting to a participating US for both acquisition and severity of acute and Dr Christina Schofield, military medical center with ILI, a subset of whom respiratory infections in low- income and Department of Medicine, middle- income countries. Madigan Army Medical were HIV positive. Demographics, clinical data, and The impact of HIV status on influenza and Center, Tacoma, WA 98431- self-reported symptom severity were ascertained, ► 5000, USA; and enrollees completed a daily symptom diary influenza-lik e illness (ILI) in the USA and rhonda. e. colombo. ctr@ for up to 10 days. 510 men were included in the other high- income countries is less clear mail. mil, particularly in the post-H1N1 pandemic analysis; 50 (9.8%) were HIV positive. Subjects christina. m. schofield2. civ@ period. mail. mil with HIV were older and less likely to be on active duty. Rhinovirus and influenza A were the most What are the new findings? Accepted 31 March 2021 commonly identified pathogens. Moderate–severe Published Online First ► In this predominantly outpatient cohort of 23 April 2021 diarrhea (p<0.001) and fatigue (p=0.01) were men presenting with ILI, HIV positivity was http://jim.bmj.com/ more frequently reported by HIV- positive men. HIV independently associated with a higher positivity was associated with higher gastrointestinal composite gastrointestinal score, but not scores, but not other measures of ILI symptom other measures of ILI symptom severity, severity, after controlling for age, race, military after controlling for age, race, military status, and influenza season. Few were hospitalized. status, and influenza season. HIV-positive subjects had more influenza B (p=0.04) ► Rhinovirus was the most common and were more likely to receive antivirals (32% vs pathogen detected in both HIV-positive on October 2, 2021 by guest. Protected copyright. 6%, p<0.01). Antiviral use was not significantly and HIV- negative subjects, followed by associated with symptom scores when accounting influenza A virus. for potential confounders. In this predominantly ► Influenza B was more frequently identified outpatient cohort of adult men, HIV had minimal in subjects with HIV (p=0.04); however, the impact on ILI symptom severity. Despite similar absolute number of influenza B cases was illness severity, a higher percentage of subjects with small. HIV reported undergoing antiviral treatment for ILI, ► Despite similar illness severity and likely reflecting differences in prescribing practices. excellent HIV control, a higher percentage Trial registration number: NCT01021098. of subjects with HIV reported undergoing antiviral treatment for ILI, suggesting that prescribing practices favor more cautious © American Federation for treatment of ILI in individuals with HIV. Medical Research 2021. Re- use permitted under INTRODUCTION CC BY- NC. No commercial The effects of HIV infection on influenza-like re- use. Published by BMJ. illness (ILI) in the era of effective combination methodology used, thus limiting the applica- To cite: Colombo RE, antiretroviral therapy (cART), particularly in bility to the broader population. Schofield C, Richard SA, the post-2009 H1N1 influenza pandemic era, In Africa, several studies have been performed et al. J Investig Med have not been well established. Available results suggesting that HIV is a risk factor for both 2021;69:1230–1237. vary, depending on the population studied and acquisition and severity of acute respiratory 1230 Colombo RE, et al. J Investig Med 2021;69:1230–1237. doi:10.1136/jim-2020-001694 Original research outcomes from influenza in HIC versus low- income and J Investig Med: first published as 10.1136/jim-2020-001694 on 23 April 2021. Downloaded from Significance of this study middle-income countries (LMICs) attempted to assess the impact of HIV/AIDS, including data through March 2016.12 How might these results change the focus of research However, only approximately 10% of included studies or clinical practice? collected postpandemic data, and few studies specifically ► These results may help to better inform the clinical risk addressed HIV as a separate comorbidity. For those that assessment and management decisions for a man with did, HIV/AIDS was associated with increased risk of ICU well- controlled HIV who presents with an ILI. admission and/or death in LMIC but not in HIC.12 To our knowledge, there has been no analysis of ILI severity and outcomes in the postpandemic period among a predomi- infections (ARIs). A recent study from Malawi showed that nantly outpatient cohort of otherwise healthy adults living the risk of influenza was >2.5- fold higher among HIV- with HIV in an HIC. Thus, the purpose of this analysis was infected adults as compared with HIV-uninfected adults to compare the prevalence and severity of symptoms as well after adjusting for demographic and socioeconomic factors.1 as clinical outcomes associated with ILI in a US cohort of HIV was also independently associated with a nearly five- adult men with well- controlled HIV with otherwise healthy fold increased risk of severe disease (OR 4.98, 95% CI 2.09 adult men who were HIV negative. to 11.88).1 A meta- analysis of case fatality rates among 36 studies of ARI in Africa found an increased risk of death METHODS in HIV- infected as compared with HIV- uninfected (pooled Overview of the Acute Respiratory Infection Consortium OR 4.10, 95% CI 2.63 to 6.27), with the highest risk of (ARIC) study death occurring among HIV- infected children under the age Established in July 2009, the ARIC is a multisite, multidis- of 5 years.2 ciplinary clinical research network for the study of ILI in The impact of HIV status on influenza and ILI in the US Department of Defense healthcare facilities. At the core USA and other high- income countries (HICs) is less of the ARIC is the Natural History Study, an observational, clear. US studies performed earlier in the HIV epidemic longitudinal cohort study to determine the etiology, epide- identified HIV as a risk factor for increased influenza miology, and clinical characteristics of ILI among otherwise severity3 4; however, whether this association persists in healthy military personnel and beneficiaries.13 Five military the era of cART has been questioned. In a 2011 review, treatment facilities across the continental USA are partic- Sheth et al suggested that HIV infection does not appear ipating: (1) Naval Medical Center Portsmouth, Virginia; to increase susceptibility to influenza in the USA, although (2) Naval Medical Center, San Diego, California; (3) available data were limited regarding the 2009 pandemic Madigan Army Medical Center, Tacoma, Washington; (4) strain H1N1pdm09.5 Serological studies focusing on influ- Brooke Army Medical Center, San Antonio, Texas; and (5) enza incidence in the USA and Australia during the H1N1 Walter Reed National Military Medical Center, Bethesda, pandemic did not detect any evidence of increased risk of Maryland. influenza acquisition among HIV- infected individuals.6 A 2010–2011 multicenter prospective US cohort study found http://jim.bmj.com/ that the duration of influenza virus shedding among HIV- Patient population and procedures infected adults diagnosed with influenza, 95% of whom Between September 2010 and March 2015, 1457 patients were on cART, was similar to durations previously reported aged 0–65 years and presenting within 72 hours after onset for HIV- uninfected individuals with influenza.7 Specifically of ILI, defined as having a temperature of ≥100.4°F and with regard to pandemic influenza, several studies from sore throat or one of the following respiratory symptoms: HIC reported disproportionate rates of HIV among individ- cough, sputum production, shortness of breath, or chest on October 2, 2021 by guest. Protected copyright. uals hospitalized with H1N1pdm09 influenza infection as pain, were recruited. Both inpatient and outpatient subjects compared with the prevalence of HIV in the general popu- were eligible for participation. Subjects with a serious lation.8 However, in a 2009 study of hospitalized patients comorbidity other than HIV (diabetes, active malignan- in the USA with H1N1pdm09, clinical outcomes, including cies, chronic obstructive pulmonary disease, severe asthma, rates of intensive care unit (ICU) admission, mechanical a medical condition requiring immune modulating agents ventilation, and death, did not differ by HIV status.9 A for >5 days within the last month, chronic neuromuscular similar study of patients hospitalized with influenza in Spain disease, chronic kidney disease, or chronic heart disease), as in 2009 also reported similar clinical outcomes between well as individuals under the age of 18 years, were excluded HIV- uninfected and HIV-infected individuals.10 However, from this analysis.
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