Literature DB >> 32657527

SARS-CoV-2 and HIV coinfection: clinical experience from Rhode Island, United States.

Katrina M Byrd1, Curt G Beckwith1, Joseph M Garland1, Jennie E Johnson1, Su Aung1, Susan Cu-Uvin1, Dimitrios Farmakiotis1, Timothy Flanigan1, Fizza S Gillani1, Raul Macias-Gil1, Maria Mileno1, Bharat Ramratnam1, Natasha R Rybak1, Martha Sanchez1, Karen Tashima1, Eleftherios Mylonakis1, Rami Kantor1.   

Abstract

INTRODUCTION: Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) has infected >6 million people worldwide since December 2019. Global reports of HIV/SARS-CoV-2 coinfection are limited. To better understand the impact of the coronavirus disease 2019 (COVID-19) pandemic on persons with HIV and improve their care, we present an outpatient and inpatient clinical experience of HIV/SARS-CoV-2 coinfection from Rhode Island, US.
METHODS: We describe outpatient and inpatient preparedness for the COVID-19 pandemic, and present a case series of all known patients with HIV/SARS-CoV-2 coinfection at The Miriam Hospital and Rhode Island Hospital, and The Miriam Hospital Infectious Diseases and Immunology Center, in Providence, Rhode Island, US. RESULTS AND DISCUSSION: The Infectious Diseases and Immunology Center rapidly prepared for outpatient and inpatient care of persons with HIV and SARS-CoV-2. Between 30 March and 20 May 2020, 27 patients with HIV were diagnosed with SARS-CoV-2. Twenty were male, six female and one transgender female; average age was 49 years; 13/27 were Hispanic and 6/27 were African American. All had HIV viral load <200 copies/mL and were on antiretroviral therapy with CD4 count range 87 to 1441 cells/µL. Twenty-six of the 27 had common COVID-19 symptoms for one to twenty-eight days and most had other co-morbidities and/or risk factors. Nine of the 27 were hospitalized for one to thirteen days; of those, three lived in a nursing home, six received remdesivir through a clinical trial or emergency use authorization and tolerated it well; eight recovered and one died. Overall, 17% of known Center people had HIV/SARS-CoV-2 coinfection, whereas the comparable state-wide prevalence was 9%.
CONCLUSIONS: We highlight challenges of outpatient and inpatient HIV care in the setting of the COVID-19 pandemic and present the largest detailed case series to date from the United States on HIV/SARS-CoV-2 coinfection, adding to limited global reports. The aggregated clinical findings suggest that the clinical presentation and outcomes of COVID-19 appear consistent with those without HIV. Whether SARS-CoV-2 infection is more frequent among persons with HIV remains to be determined. More data are needed as we develop our understanding of how HIV and antiretroviral therapy are affected by or have an impact on this pandemic.
© 2020 The Authors. Journal of the International AIDS Society published by John Wiley & Sons Ltd on behalf of International AIDS Society.

Entities:  

Keywords:  COVID-19; HIV; SARS-CoV-2; coinfection; preparedness

Mesh:

Year:  2020        PMID: 32657527      PMCID: PMC7357287          DOI: 10.1002/jia2.25573

Source DB:  PubMed          Journal:  J Int AIDS Soc        ISSN: 1758-2652            Impact factor:   5.396


INTRODUCTION

The first case of coronavirus disease 2019 (COVID‐19), caused by Severe Acute Respiratory Syndrome Coronavirus 2 (SARS‐CoV‐2) was reported in Wuhan, China in December 2019 [1]. Within months, the virus infected more than six million people, causing over 350,000 deaths worldwide. The first COVID‐19 case in the US was diagnosed on January 20, 2020, and as of June 02, the US leads the world in both COVID‐19 cases (1,857,872) and deaths (107,911) [2, 3]. There are 37.9 million persons with HIV (PWH) globally, and 1.1 million in the US [4]. PWH may be considered vulnerable to infections due to CD4 cell depletion. However, despite the large scale of the COVID‐19 pandemic, little is known about its characteristics in PWH. To date, there are only 158 confirmed HIV/SARS‐CoV‐2 coinfections reported in detail in the literature, nine from China [5, 6, 7, 8], 56 from Spain [9, 10], 33 from Germany [11], 47 from Italy [12] and 13 from the US [13, 14] with diverse clinical severity and host characteristics including HIV‐related immunosuppression. The first Rhode Island (RI) COVID‐19 case was diagnosed on 1 March, and as of 2 June, there were 15,441 cases (1.4% of the RI population) and 772 fatalities (4.9% of cases) [15]. Of 1.06 million people in RI, approximately 2800 (0.3%) had HIV in 2018 [16]. Uniquely, the Miriam Hospital Infectious Diseases and Immunology Center (the Center) cares for more than 80% of PWH who are in care in the state. Given limited knowledge of HIV/SARS‐CoV‐2 coinfection, in RI or elsewhere, and to better understand the impact of the COVID‐19 pandemic on PWH and improve their care, we present our outpatient and inpatient clinical experience.

METHODS

We first describe processes undertaken to achieve appropriate outpatient and inpatient preparedness for the COVID‐19 pandemic at The Miriam Hospital and RI Hospital, primary hospitals for the largest academic medical center in the state, and the Miriam Hospital Infectious Diseases and Immunology Center, in Providence, RI, US. We then present a case series of all known outpatients and inpatients with HIV/SARS‐CoV‐2 coinfection until the time of this writing. Medical records were reviewed for demographic, clinical, laboratory and outcomes data. The study was approved by, and a consent waiver was obtained from the Institutional Review Board at The Miriam Hospital in Providence, RI.

RESULTS AND DISCUSSION

Outpatient preparedness

The Center is a large, Ryan White‐funded HIV clinic, caring for more than 1800 patients; 98% meeting statewide income eligibility for financial assistance, and 76% reporting incomes below the federal poverty line. In 2019, 99% of Center patients were prescribed ART and 91% had HIV viral load (VL) <200 copies/mL. After the first COVID‐19 case in RI, the Center rapidly converted most patient visits to telehealth and deferred nonurgent laboratory testing. Understanding challenges PWH might face during social distancing, and realizing potential health consequences of changing insurance status due to job loss and furloughs, outreach‐worker staff proactively assist patients with insurance and medication access; the hospital pharmacy offers no‐charge home medication delivery; pharmacy liaisons assist with co‐pays; behavioral therapists use telehealth; and social workers address community challenges and evaluate and help to address food insecurities. In regards to COVID‐19 testing and evaluation, the Center implemented a health‐system‐wide telehealth programme to evaluate suspected ambulatory COVID‐19 cases; completed construction of a negative‐pressure exam room to evaluate suspected walk‐in cases; streamlined testing access; provided post‐hospitalization telehealth visits to patients discharged with COVID‐19 (both with and without HIV); and served as an active site for COVID‐19 clinical trials.

Inpatient preparedness

The Center operates a dedicated inpatient teaching “Immunology Service” (the Service) for admitted Center patients, staffed by Center faculty, with multidisciplinary Center staff coordination. With COVID‐19 hospitalizations, the Service was made aware of all COVID‐19 cases and provided an important link between admitted PWH and available COVID‐19 clinical trials. The Infectious Diseases Division, which encompasses the Service, enrolled COVID‐19 patients into two Phase 3 remdesivir clinical trials (ClinicalTrials.gov, NCT04292730, NCT04292899) and a convalescent plasma therapy study. The Center is also a site for an ambulatory study of azithromycin and hydroxychloroquine. Importantly, PWH were not excluded from these trials and the Service actively referred PWH to them. It is crucial that PWH enroll in such trials, as we offer potential life‐saving treatments, and learn whether HIV itself or HIV‐related immunosuppression predispose PWH to different clinical presentations, courses, or outcomes compared to persons without HIV, and whether ART provides protection from SARS‐CoV‐2.

Case series

Between 30 March and 20 May, 27 RI PWH were diagnosed with COVID‐19 using nucleic acid‐based testing; 0.18% of COVID‐19 diagnoses in the state during that time period. Nine were hospitalized (Table 1) and 18 were outpatients (Table 2). Overall, patientsHIV was diagnosed between 1980 and 2019; 20 were male, six female and one transgender female, ages 30 to 71 years; 13/27 Hispanic and 6/27 African American; most were diagnosed with COVID‐19 in the outpatient or emergency department setting; and all had HIV VL < 200 copies/mL and were on antiretroviral therapy with a CD4 count range 87 to 1441 cells/µL. Twenty‐six of the 27 had common COVID‐19 symptoms for one to twenty‐eight days and most had other co‐morbidities and/or risk factors, with no apparent differences between hospitalized and non‐hospitalized patients. Chest imaging, if obtained, ranged from normal X‐rays to computerized tomography multifocal airspace disease with ground glass infiltrates. Abnormal imaging findings were more common among hospitalized patients. The nine hospitalized patients (Table 1) were admitted for one to thirteen (average 8) days. Of those, three lived in nursing‐homes, three had O2 saturations < 94% at presentation, six received remdesivir through a clinical trial or emergency use authorization, and none required intensive care unit admission. Most had COVID‐19‐associated laboratory abnormalities, reflecting lymphopenia and inflammation. Of the hospitalized patients, eight were discharged and one died. This patient had advanced metastatic renal cell carcinoma and goals of care focused on his comfort. Eighteen of the 27 were followed in the outpatient setting and did not require hospitalization (Table 2).
Table 1

Inpatient HIV and SARS‐CoV‐2 coinfection in Rhode Island

Patient 1Patient 2Patient 3Patient 4Patient 5Patient 6Patient 7Patient 8Patient 9
General
Sex (gender)MaleMaleMaleMaleMaleMaleMale (female)MaleFemale
Age (years)635263435945397160
Race/ethnicityAAHispanicHispanicHispanicAAHispanicHispanicWhite (non‐Hispanic)White (non‐Hispanic
HIV
Dx year198920052011201020022009200519991980’s
Current ARTABC/DTG/3TCEVG/c/FTC/TAFEVG/c/FTC/TAFEVG/c/FTC/TAFEFV, ABCEFV/FTC/TDFBTG/FTC/TAFABC/DTG/3TCBTG/FTC/TAF
VL (copies/mL) a <20<20<20<20<20<20<20<20<20
CD4 count a (cells/µL)442567877009363348353611189
CD4% a 13319424223334556
Time CD4> 200Since 2011Since 2005NeverSince 2011Since 2002Since 2010Since 2008Since 2003At least since 2008
COVID‐19
Risk factorsNursing home with + casesNoneNoneRecent travelNursing home with + casesContact with + casesContact with + casesNursing home with + casesRecent hospitalization
Other Co‐morbiditiesDementia, CVAObesity, HTNDM, HLDNoneCancer, ESRDNoneObesityAlcoholismCOPD, Cocaine use, DM
Active tobacco useNo (former smoker)NoNo (former smoker)YesNoNoNoYesYes
SymptomsSOB, lethargySOB, fever, HASOBSOB, cough, sore throat, chest painSOBSOB, HASOB, fever, HALethargy, decreased appetiteSOB, fever, chills
Symptoms pre‐testing1 day8 days28 days14 days1 day8 days7 days7 days2 days
Min RA O2%70%86%79%95%94%94%94%95%85%
ALC (109/L) b 300600130013705005001000600600
CRP (mg/L) c 202102254N/A276296209134
Ferritin (ng/mL) c 1633179500321N/A10951600804159
D‐dimer(ng/mL) c N/A514245252N/A255189747N/A
ALT (IU/L) c 721026229N/A113116321
AST IU/L) c 81764531N/A103501825
LDH (IU/L) c 154337236252N/A468367147250
HCV statusCuredNegNegNegNegClearedNegNegCured
ImagingCXR: bibasilar asdCXR: bilateral asdCXR: bilateral asdCT mf ground glass infiltratesCXR: diffuse BL asdCXR: mf BL asdCXR: BL asdCXR: right asdCXR: emphysematous changes
COVID‐19 therapyRDV (10 days)RDV (8 days)RDV (10 days)NoNoNoRDV (4 days)RDV (2 days)RDV (5 days)
Time in hospital13 days8 days13 days6 days8 days1 day8 days4 days8 days
OutcomeDCDCDCDCDiedDCDCDCDC

/c, cobicistat; +, positive; 3TC, lamivudine; AA, African American; ABC, abacavir; ALC, absolute lymphocyte count; ART, antiretroviral therapy; asd, air space disease; BL, bilateral; BTG, bictegravir; CD4 count/VL are prior to SARS‐CoV‐2 infection; cong, congestion; CT, computerized tomography; CVA, cerebrovascular accident; CXR, chest X‐ray; DC, discharge; DM, diabetes mellitus, DRV, darunavir; DTG, dolutegravir; dx, diagnosis; ED, emergency department; EFV, efavirenz; ESRD, end stage renal disease; EVG, elvitegravir; FTC, emtricitabine; HA, headache; HCV, hepatitis C virus; HLD, hyperlipidaemia; HTN, hypertension; ICU, intensive care unit; IST, interstitial; mf, multifocal; Min, minimal; N/A, not available; Neg, negative; O2, oxygen; RA, room air; RDV, remdesivir; RPV, rilpivirine; RUL, right upper lobe; Sat, saturation; SOB, shortness of breath; TAF, tenofovir alafenamide; TDF, tenofovir disoproxil fumarate, VL, viral load.

Before COVID‐19

lowest recorded

highest recorded.

Table 2

Outpatient HIV and SARS‐CoV‐2 coinfection in Rhode Island

Pt 1Pt 2Pt 3Pt 4Pt 5Pt 6Pt 7Pt 8Pt 9Pt 10Pt 11Pt 12Pt 13Pt 14Pt 15Pt 16Pt 17Pt 18
General
SexMaleMaleFemaleFemaleMaleMaleMaleMaleFemaleMaleMaleMaleMaleMaleMaleMaleFemaleFemale
Age (years)623757513253483837575644543730424751
Race/ethnicityWhite; non‐HispanicWhite; non‐HispanicOtherHispanicHispanicWhite; non‐HispanicAAWhite; non‐HispanicAAHispanicHispanicHispanicHispanicHispanicWhite; non‐HispanicHispanicAAAA
HIV
Dx year201520122015200120122009200220132015201720012014201020102019200520092017
Current ARTBTG/FTC/TAFBTG/FTC/TAFBTG/FTC/TAFDTG/RPVBTG/FTC/TAFEVG/c/FTC/TAFEVG/c/FTC/TAFEVG/c/FTC/TAFEVG/c/FTC/TAFBTG/FTC/TAFBTG/FTC/TAFBTG/FTC/TAFBTG/FTC/TAFBTG/FTC/TAFBTG/FTC/TAFBTG/FTC/TAFDVR/c/FTC/TAFBTG/FTC/TAF
VL (copies/mL) a <2069<20<20<20<2046<20<20<20<2046<20<20<20<20<20<20
CD4 count a (cells/µL)74678921674634668313757606441441444357813638459743347239
CD4% a 233516211934353027532714363236183216
Time CD4> 200Since 2015Since 2017Since 2015Since 2012Since 2016Since 2010Since 2003Since 2016Since 2015Since 2017Since 2002Since 2016Since 2010Since 2011Since 2019Since 2006Since 2009Since 2017
COVID‐19
Risk factorsWorks in homeless ShelterContact with + casesContact with + casesNoneContact with + casesContact with + cases; travelContact with + casesHealthcare workerNoneNoneContact with + casesHealthcare workerContact with + casesContact with + casesNoneNoneWorks in group homeHealthcare worker
Other Co‐morbiditiesHTNObesityDMDM, asthmaHLH in remission, Histo‐plasmosisHTNHTNObesityNoneNoneHTN, obesityObesityHTN, CADAlcoholism, cirrhosisNoneNoneNoneObesity
Active tobacco useNoNo (former smoker)NoNo (former smoker)No (former smoker)YesNoNo (former smoker)NoNoNoNo (former smoker)NoNo (former smoker)YesNoNoNo
SymptomsCough, fever, low appetiteCough, fever, myalgiaNoneFever, myalgia, HA, chillsFever, cough, sore throatAnosmia, nasal congFatigue, nasal cong, HAMyalgia, back painHAHA, myalgia, anosmiaHA, myalgia, anosmiaMyalgia, back painLethargy, anosmiaSOB, fever, myalgiaAnosmiaCough, myalgiaFever, coughHA, back pain
Symptoms pre‐testing14 days2 daysN/A1 day3 daysweeks4 days3 daysUnknown7 daysUnknown5 daysUnknownUnknownUnknown9 daysUnknown4 days
Min RA O2%96%98%N/A98%N/AN/AN/AN/AN/A97%N/A95%N/A95%N/AN/AN/A99%
ALC (109/L) b 2200800N/A1800N/AN/AN/AN/AN/A1400N/A2200N/A2100N/AN/AN/A1600
CRP (mg/L) c N/AN/AN/AN/AN/AN/AN/AN/AN/A180N/AN/AN/AN/AN/AN/AN/AN/A
Ferritin (ng/mL) c N/AN/AN/AN/AN/AN/AN/AN/AN/A412N/AN/AN/AN/AN/AN/AN/AN/A
D‐dimer (ng/mL) c N/AN/AN/AN/AN/AN/AN/AN/AN/A142N/AN/AN/AN/AN/AN/AN/AN/A
ALT (IU/L) c N/A14N/A25N/AN/AN/AN/AN/A24N/AN/AN/A61N/AN/AN/A10
AST IU/L) c N/A31N/A21N/AN/AN/AN/AN/A30N/AN/AN/A71N/AN/AN/A18
LDH (IU/L) c N/AN/AN/AN/AN/AN/AN/AN/AN/A245N/AN/AN/AN/AN/AN/AN/AN/A
HCV statusNegNegNegNegNegNegNegNegNegNegNegNegNegNegNegNegCuredNeg
ImagingCXR: mild ist asdCXR: clear lungsN/ACXR: RUL asdN/AN/AN/AN/AN/ACXR: BL asdN/ACXR: BL asdN/ACXR: ist asdN/AN/AN/ANeg
COVID‐19 therapyNoNoNoNoNoNoNoNoNoNoNoNoNoNoNoNoNoNo
OutcomeDC from EDDC from EDHomeDC from EDHomeHomeHomeHomeHomeHomeHomeDC from EDHomeHomeHomeHomeHomeHome

/c, cobicistat; +, positive; 3TC, lamivudine; AA, African American; ABC, abacavir; ALC, absolute lymphocyte count; ART, antiretroviral therapy; asd, air space disease; BL, bilateral; BTG, bictegravir; CD4 count/ VL are prior to COVID‐19 infection; cong, congestion; CT, computerized tomography; CVA, cerebrovascular accident; CXR, chest X‐ray; DC, discharge; DM, diabetes mellitus, DRV, darunavir; DTG, dolutegravir; dx, diagnosis; ED, emergency department; EFV, efavirenz; ESRD, end stage renal disease; EVG, elvitegravir; FTC, emtricitabine; HA, headache; HCV, hepatitis C virus; HLD, hyperlipidaemia; HLH, haemophagocytic lymphohistiocytosis; HTN, hypertension; ICU, intensive care unit; IST, interstitial; mf, multifocal; Min, minimal; N/A, not available; Neg, negative; O2, oxygen; Pt, patient; RA, room air; RDV, remdesivir; RPV, rilpivirine; RUL, right upper lobe; Sat, saturation; SOB, shortness of breath; TAF, tenofovir alafenamide; TDF, tenofovir disoproxil fumarate, VL, viral load.

Before COVID‐19

lowest recorded

highest recorded.

Inpatient HIV and SARS‐CoV‐2 coinfection in Rhode Island /c, cobicistat; +, positive; 3TC, lamivudine; AA, African American; ABC, abacavir; ALC, absolute lymphocyte count; ART, antiretroviral therapy; asd, air space disease; BL, bilateral; BTG, bictegravir; CD4 count/VL are prior to SARS‐CoV‐2 infection; cong, congestion; CT, computerized tomography; CVA, cerebrovascular accident; CXR, chest X‐ray; DC, discharge; DM, diabetes mellitus, DRV, darunavir; DTG, dolutegravir; dx, diagnosis; ED, emergency department; EFV, efavirenz; ESRD, end stage renal disease; EVG, elvitegravir; FTC, emtricitabine; HA, headache; HCV, hepatitis C virus; HLD, hyperlipidaemia; HTN, hypertension; ICU, intensive care unit; IST, interstitial; mf, multifocal; Min, minimal; N/A, not available; Neg, negative; O2, oxygen; RA, room air; RDV, remdesivir; RPV, rilpivirine; RUL, right upper lobe; Sat, saturation; SOB, shortness of breath; TAF, tenofovir alafenamide; TDF, tenofovir disoproxil fumarate, VL, viral load. Before COVID‐19 lowest recorded highest recorded. Outpatient HIV and SARS‐CoV‐2 coinfection in Rhode Island /c, cobicistat; +, positive; 3TC, lamivudine; AA, African American; ABC, abacavir; ALC, absolute lymphocyte count; ART, antiretroviral therapy; asd, air space disease; BL, bilateral; BTG, bictegravir; CD4 count/ VL are prior to COVID‐19 infection; cong, congestion; CT, computerized tomography; CVA, cerebrovascular accident; CXR, chest X‐ray; DC, discharge; DM, diabetes mellitus, DRV, darunavir; DTG, dolutegravir; dx, diagnosis; ED, emergency department; EFV, efavirenz; ESRD, end stage renal disease; EVG, elvitegravir; FTC, emtricitabine; HA, headache; HCV, hepatitis C virus; HLD, hyperlipidaemia; HLH, haemophagocytic lymphohistiocytosis; HTN, hypertension; ICU, intensive care unit; IST, interstitial; mf, multifocal; Min, minimal; N/A, not available; Neg, negative; O2, oxygen; Pt, patient; RA, room air; RDV, remdesivir; RPV, rilpivirine; RUL, right upper lobe; Sat, saturation; SOB, shortness of breath; TAF, tenofovir alafenamide; TDF, tenofovir disoproxil fumarate, VL, viral load. Before COVID‐19 lowest recorded highest recorded.

Case series highlights

We highlight several unique points related to these 27 PWH and COVID‐19. First, the detailed description of the 27 RI patients adds to the limited HIV/SARS‐CoV‐2 coinfection literature. Patients had typical COVID‐19 symptoms like cough, shortness of breath, lethargy, fever, headache, sore throat, chest pain, myalgia and anosmia. Twenty were male, six female and one transgender female, most Hispanic or African American (including the one patient who died), with an average age 49 years. More than half recovered at home without requiring hospitalization. HIV VL was <200 copies/mL for all, and with the exception of hospitalized patient #3, all had CD4 count >200 cells/µL. Taken together, despite concerns for higher COVID‐19 prevalence in PWH with CD4 counts <200 or potentially poorer overall clinical outcomes in PWH, our data are consistent with reports from outside the US, suggesting that COVID‐19 is not more frequent among virologically suppressed PWH on ART. Additionally, clinical presentations, course and outcomes appear consistent with persons without HIV. It is still too early to draw any definitive conclusions from these few cases, and additional larger studies are needed. Second, three patients, all hospitalized, lived in nursing‐homes with other residents with COVID‐19. All were initially asymptomatic; patient #1 became acutely confused and hypoxic leading to hospitalization; patient #5 was admitted for pain control in the setting of metastatic cancer, developed hypoxia and tachypnoea on hospital day 8, when he opted for comfort care and subsequently died; and patient #8 was admitted for the complication of decreased oral intake and altered mental status. These cases highlight that nursing‐home residents were vulnerable to COVID‐19, likely because they were typically older, have co‐morbidities, live in close proximity to other at‐risk persons, and have prolonged interactions with caregivers, as described [17]. Many reported individuals in these settings were asymptomatic at testing, as were our three patients, suggesting asymptomatic infection, with or without HIV [17]. Third, we report the first six PWH and COVID‐19 in RI, adding to the two reported cases from Italy [12] and Spain [10], who received remdesivir. All six tolerated it well, including two with history of hepatitis C virus. In a preliminary report of a double‐blind, randomized, placebo‐controlled trial, remdesivir was recently shown to be superior to placebo in shortening the time to recovery in adults hospitalized with COVID‐19 and evidence of lower respiratory tract infection [18]. We eagerly await the final results of ongoing clinical trials evaluating the safety and efficacy of remdesivir for COVID‐19, and it is essential and encouraging that PWH were included in these trials. Fourth, whether and how HIV antiretrovirals impact acquisition or treatment of COVID‐19 remains unknown. Clinical trials to explore these possibilities are ongoing, for drugs such as tenofovir/emtricitabine, lopinavir/ritonavir and darunavir/cobicistat [19, 20, 21]. A randomized, controlled, open‐label trial involving hospitalized adult patients with severe COVID‐19 showed no benefit of lopinavir‐ritonavir treatment beyond standard of care [22]. All 27 PWH in this series were on antiretroviral therapy; 25/27 on emtricitabine or lamivudine; and 17/18 (94%) of outpatients and 6/9 (67%) of inpatients (p = 0.09; Fisher’s Exact Test) on tenofovir formulations; suggesting that these antiretrovirals were not completely protective against SARS‐CoV‐2 infection. Whether ART medications have any impact on infection or outcomes remains to be determined. Fifth, one RI patient with a CD4 count of 87 cells/µL presented with four weeks of progressive dyspnoea. He underwent bronchoscopy that ruled out Pneumocystis jirovecii pneumonia during a separate hospitalization four weeks before his COVID‐19 diagnosis. At that time, COVID‐19 was uncommon and he was not tested. Interestingly, a specimen from that bronchoscopy, subsequently tested, was positive for SARS‐CoV‐2. The patient had a prolonged 28‐day period before re‐hospitalization with respiratory symptoms and O2 saturations down to 79%, and his nasopharyngeal PCR testing remained positive at 38 days, which is on the longer end of the reported SARS‐CoV‐2 shedding range of eight to thirty‐seven days [1]. Whether this prolonged symptomatology and PCR positivity is related to HIV infection, low CD4 count, ART, and/or other factors remains to be determined. Lastly, with RIs aggressive rollout of ambulatory SARS‐CoV‐2 diagnostic testing, 162 Center patients were tested at the time data collection was completed, of whom the above 27 (17%) were found to be positive; Although this is currently higher than the statewide positivity rate (15,441 /170,739; 9%; p = 0.00002 chi square test) [15], these numbers are subject to bias and should be interpreted cautiously, and broader testing, including of asymptomatic individuals and antibody testing, is still urgently needed.

CONCLUSIONS

We present a RI perspective, to our knowledge the largest detailed case series to date from the US, on HIV/SARS‐CoV‐2 coinfection. Despite being limited by a retrospective study design, small number of cases, limited testing early on and some unavailable data in times of telemedicine, this case series adds to limited global reports. Data are as yet inconclusive on the effect of the COVID‐19 pandemic on PWH [9, 10, 11, 12, 13, 14, 23, 24]. More data on prevalence, clinical characteristics and outcomes of HIV/SARS‐CoV‐2 coinfection are needed to understand the existence of any differences between PWH and persons without HIV. Current guidance advises HIV providers on follow‐up (e.g. telehealth), practice management (e.g. staff support and triage) and medication needs (e.g. 90‐day supply) [25]. These, as well as increased surveillance, testing and continued clinical follow‐up are critical as we develop our understanding of how HIV and antiretroviral therapy are affected by or have an impact on the COVID‐19 pandemic.

COMPETING INTEREST

All authors declare we have no competing interests.

AUTHORS’ CONTRIBUTIONS

RK conceived the study and was involved in all its aspects. KB, JMG, EM, FSG and RK compiled the case series. KMB collected all data and wrote the first draft of the manuscript with RK, with contributions from CGB and JMG. All authors read, critically revised and approved the final manuscript.
  13 in total

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2.  A Case Series of Five People Living with HIV Hospitalized with COVID-19 in Chicago, Illinois.

Authors:  Jessica P Ridgway; Brianna Farley; Jean-Luc Benoit; Christopher Frohne; Aniruddha Hazra; Natasha Pettit; Mai Pho; Kenneth Pursell; Jina Saltzman; Jessica Schmitt; Arno Ziggy Uvin; David Pitrak; Moira McNulty
Journal:  AIDS Patient Care STDS       Date:  2020-05-29       Impact factor: 5.078

3.  Description of COVID-19 in HIV-infected individuals: a single-centre, prospective cohort.

Authors:  Pilar Vizcarra; María J Pérez-Elías; Carmen Quereda; Ana Moreno; María J Vivancos; Fernando Dronda; José L Casado
Journal:  Lancet HIV       Date:  2020-05-28       Impact factor: 12.767

4.  Remdesivir for the Treatment of Covid-19 - Final Report.

Authors:  John H Beigel; Kay M Tomashek; Lori E Dodd; Aneesh K Mehta; Barry S Zingman; Andre C Kalil; Elizabeth Hohmann; Helen Y Chu; Annie Luetkemeyer; Susan Kline; Diego Lopez de Castilla; Robert W Finberg; Kerry Dierberg; Victor Tapson; Lanny Hsieh; Thomas F Patterson; Roger Paredes; Daniel A Sweeney; William R Short; Giota Touloumi; David Chien Lye; Norio Ohmagari; Myoung-Don Oh; Guillermo M Ruiz-Palacios; Thomas Benfield; Gerd Fätkenheuer; Mark G Kortepeter; Robert L Atmar; C Buddy Creech; Jens Lundgren; Abdel G Babiker; Sarah Pett; James D Neaton; Timothy H Burgess; Tyler Bonnett; Michelle Green; Mat Makowski; Anu Osinusi; Seema Nayak; H Clifford Lane
Journal:  N Engl J Med       Date:  2020-10-08       Impact factor: 91.245

5.  Early Virus Clearance and Delayed Antibody Response in a Case of Coronavirus Disease 2019 (COVID-19) With a History of Coinfection With Human Immunodeficiency Virus Type 1 and Hepatitis C Virus.

Authors:  Juanjuan Zhao; Xuejiao Liao; Haiyan Wang; Lanlan Wei; Mingzhao Xing; Lei Liu; Zheng Zhang
Journal:  Clin Infect Dis       Date:  2020-11-19       Impact factor: 9.079

6.  Co-infection of SARS-CoV-2 and HIV in a patient in Wuhan city, China.

Authors:  Feng Zhu; Yang Cao; Shuyun Xu; Min Zhou
Journal:  J Med Virol       Date:  2020-03-11       Impact factor: 2.327

7.  A Trial of Lopinavir-Ritonavir in Adults Hospitalized with Severe Covid-19.

Authors:  Bin Cao; Yeming Wang; Danning Wen; Wen Liu; Jingli Wang; Guohui Fan; Lianguo Ruan; Bin Song; Yanping Cai; Ming Wei; Xingwang Li; Jiaan Xia; Nanshan Chen; Jie Xiang; Ting Yu; Tao Bai; Xuelei Xie; Li Zhang; Caihong Li; Ye Yuan; Hua Chen; Huadong Li; Hanping Huang; Shengjing Tu; Fengyun Gong; Ying Liu; Yuan Wei; Chongya Dong; Fei Zhou; Xiaoying Gu; Jiuyang Xu; Zhibo Liu; Yi Zhang; Hui Li; Lianhan Shang; Ke Wang; Kunxia Li; Xia Zhou; Xuan Dong; Zhaohui Qu; Sixia Lu; Xujuan Hu; Shunan Ruan; Shanshan Luo; Jing Wu; Lu Peng; Fang Cheng; Lihong Pan; Jun Zou; Chunmin Jia; Juan Wang; Xia Liu; Shuzhen Wang; Xudong Wu; Qin Ge; Jing He; Haiyan Zhan; Fang Qiu; Li Guo; Chaolin Huang; Thomas Jaki; Frederick G Hayden; Peter W Horby; Dingyu Zhang; Chen Wang
Journal:  N Engl J Med       Date:  2020-03-18       Impact factor: 91.245

8.  Asymptomatic and Presymptomatic SARS-CoV-2 Infections in Residents of a Long-Term Care Skilled Nursing Facility - King County, Washington, March 2020.

Authors:  Anne Kimball; Kelly M Hatfield; Melissa Arons; Allison James; Joanne Taylor; Kevin Spicer; Ana C Bardossy; Lisa P Oakley; Sukarma Tanwar; Zeshan Chisty; Jeneita M Bell; Mark Methner; Josh Harney; Jesica R Jacobs; Christina M Carlson; Heather P McLaughlin; Nimalie Stone; Shauna Clark; Claire Brostrom-Smith; Libby C Page; Meagan Kay; James Lewis; Denny Russell; Brian Hiatt; Jessica Gant; Jeffrey S Duchin; Thomas A Clark; Margaret A Honein; Sujan C Reddy; John A Jernigan
Journal:  MMWR Morb Mortal Wkly Rep       Date:  2020-04-03       Impact factor: 17.586

9.  Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study.

Authors:  Fei Zhou; Ting Yu; Ronghui Du; Guohui Fan; Ying Liu; Zhibo Liu; Jie Xiang; Yeming Wang; Bin Song; Xiaoying Gu; Lulu Guan; Yuan Wei; Hui Li; Xudong Wu; Jiuyang Xu; Shengjin Tu; Yi Zhang; Hua Chen; Bin Cao
Journal:  Lancet       Date:  2020-03-11       Impact factor: 79.321

10.  Computed tomography imaging of an HIV-infected patient with coronavirus disease 2019.

Authors:  Jiaxiang Chen; Xinge Cheng; Rongpin Wang; Xianchun Zeng
Journal:  J Med Virol       Date:  2020-06-12       Impact factor: 20.693

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  24 in total

1.  Overview of the Haematological Effects of COVID-19 Infection.

Authors:  T M Wiggill; E S Mayne; J L Vaughan; S Louw
Journal:  Adv Exp Med Biol       Date:  2021       Impact factor: 2.622

2.  Characteristics and Outcomes of SARS-CoV-2 Infection Among Adults Living With HIV In Delaware:: The Story of a Syndemic During the First 12 Months of the SARS-CoV-2 Pandemic.

Authors:  Adam K Skrzynski; Brooke L Darmstadter; Sharon P Miner; Keshab Subedi; Deborah Kahal
Journal:  Dela J Public Health       Date:  2021-12-15

3.  Enigma of the high prevalence of anti-SARS-CoV-2 antibodies in HIV-positive people with no symptoms of COVID-19 in Burkina Faso.

Authors:  Tani Sagna; Paul Ouedraogo; Lassina Traore; Dorcas Obiri-Yeboah; Albert Yonli; Aristide Tapsoba; Frida Tovo; Abel Sorgho; Laetitia Zongo; Ouégo Nikiema; Dénise Ilboudo; Marius Belemgnegre; Christelle W Nadembega; Djeneba Ouermi; Florencia W Djigma; Théodora M Zohoncon; Henriette Poaty; Vittorio Colizzi; Jacques Simpore
Journal:  J Public Health Afr       Date:  2022-05-25

Review 4.  The interplay between HIV and COVID-19: summary of the data and responses to date.

Authors:  Lillian B Brown; Matthew A Spinelli; Monica Gandhi
Journal:  Curr Opin HIV AIDS       Date:  2021-01       Impact factor: 4.283

5.  Human Immunodeficiency Virus and Severe Acute Respiratory Syndrome Coronavirus 2 Coinfection: A Systematic Review of the Literature and Challenges.

Authors:  Raj H Patel; Arpan Acharya; Hitendra S Chand; Mahesh Mohan; Siddappa N Byrareddy
Journal:  AIDS Res Hum Retroviruses       Date:  2021-03-23       Impact factor: 2.205

6.  Antiretroviral drug activity and potential for pre-exposure prophylaxis against COVID-19 and HIV infection.

Authors:  Dennis C Copertino; Bruno C Casado Lima; Rodrigo R R Duarte; Timothy R Powell; Christopher E Ormsby; Timothy Wilkin; Roy M Gulick; Miguel de Mulder Rougvie; Douglas F Nixon
Journal:  J Biomol Struct Dyn       Date:  2021-03-18       Impact factor: 5.235

7.  HIV-1 Infection Does Not Change Disease Course or Inflammatory Pattern of SARS-CoV-2-Infected Patients Presenting at a Large Urban Medical Center in New York City.

Authors:  Justin Laracy; Jason Zucker; Delivette Castor; Donald J McMahon; Tai Wei Guo; Michael Yan; Noga Shalev; Matthew Scherer; Peter Gordon; Magdalena Sobieszczyk; Michael T Yin
Journal:  Open Forum Infect Dis       Date:  2021-01-28       Impact factor: 3.835

Review 8.  Tenofovir, Another Inexpensive, Well-Known and Widely Available Old Drug Repurposed for SARS-COV-2 Infection.

Authors:  Isabella Zanella; Daniela Zizioli; Francesco Castelli; Eugenia Quiros-Roldan
Journal:  Pharmaceuticals (Basel)       Date:  2021-05-11

9.  SARS-CoV-2 percent positivity and risk factors among people with HIV at an urban academic medical center.

Authors:  Eleanor E Friedman; Samantha A Devlin; Moira C McNulty; Jessica P Ridgway
Journal:  PLoS One       Date:  2021-07-21       Impact factor: 3.240

Review 10.  Prevalence and factors associated with SARS-CoV-2 seropositivity in the Spanish HIV Research Network Cohort.

Authors:  Juan Berenguer; Cristina Díez; María Martín-Vicente; Rafael Micán; María J Pérez-Elías; Lucio J García-Fraile; Francisco Vidal; Inés Suárez-García; Daniel Podzamczer; Jorge Del Romero; Federico Pulido; José A Iribarren; Félix Gutiérrez; Eva Poveda; Carlos Galera; Rebeca Izquierdo; Víctor Asensi; Joaquín Portilla; Juan C López; José R Arribas; Santiago Moreno; Juan González-García; Salvador Resino; Inmaculada Jarrín
Journal:  Clin Microbiol Infect       Date:  2021-06-26       Impact factor: 8.067

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