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1. Prolonged indoleamine 2,3-dioxygenase-2 activity and associated cellular stress in post-acute sequelae of SARS-CoV-2 infectionResearch in context

Author

Lihui Guo, Brent Appelman, Kirsten Mooij-Kalverda, Riekelt H. Houtkooper, Michel van Weeghel, Frédéric M. Vaz, Annemiek Dijkhuis, Tamara Dekker, Barbara S. Smids, Jan Willem Duitman, Marianna Bugiani, Paul Brinkman, Jonne J. Sikkens, H.A. Ayesha Lavell, Rob C.I. Wüst, Michèle van Vugt, René Lutter, M.A. van Agtmael, A.G. Algera, B. Appelman, F.E.H.P. van Baarle, M. Beudel, H.J. Bogaard, M. Bomers, P.I. Bonta, L.D.J. Bos, M. Botta, J. de Brabander, G.J. de Bree, S. de Bruin, M. Bugiani, E.B. Bulle, O. Chouchane, A.P.M. Cloherty, D. Buis, M.C.F.J. de Rotte, M. Dijkstra, D.A. Dongelmans, R.W.G. Dujardin, P.E. Elbers, L.M. Fleuren, S.E. Geerlings, T.B.H. Geijtenbeek, A.R.J. Girbes, A. Goorhuis, M.P. Grobusch, L.A. Hagens, J. Hamann, V.C. Harris, R. Hemke, S.M. Hermans, L.M.A. Heunks, M.W. Hollmann, J. Horn, J.W. Hovius, M.D. de Jong, R. Koing, E.H.T. Lim, N. van Mourik, J.F. Nellen, E.J. Nossent, F. Paulus, E. Peters, D. Piña-Fuentes, T. van der Poll, B. Preckel, J.M. Prins, S.J. Raasveld, T.D.Y. Reijnders, M. Schinkel, F.A.P. Schrauwen, M.J. Schultz, A.R. Schuurman, J. Schuurmans, K. Sigaloff, M.A. Slim, P. Smeele, M.R. Smit, C. Stijnis, W. Stilma, C.E. Teunissen, P. Thoral, A.M. Tsonas, P.R. Tuinman, M. van der Valk, D.P. Veelo, C. Volleman, H. de Vries, L.A. van Vught, M. van Vugt, D. Wouters, A.H. Zwinderman, M.C. Brouwer, W.J. Wiersinga, A.P.J. Vlaar, and D. van de Beek

Subjects
IDO2, PASC, Autophagy, Apoptosis, Kynurenine, Mitochondrial_activity, Medicine, Medicine (General), R5-920
Abstract

Summary: Background: Post-acute sequela of SARS-CoV-2 infection (PASC) encompass fatigue, post-exertional malaise and cognitive problems. The abundant expression of the tryptophan-catabolizing enzyme indoleamine 2,3-dioxygenase-2 (IDO2) in fatal/severe COVID-19, led us to determine, in an exploratory observational study, whether IDO2 is expressed and active in PASC, and may correlate with pathophysiology. Methods: Plasma or serum, and peripheral blood mononuclear cells (PBMC) were obtained from well-characterized PASC patients and SARS-CoV-2-infected individuals without PASC. We assessed tryptophan and its degradation products by UPLC-MS/MS. IDO2 activity, its potential consequences, and the involvement of the aryl hydrocarbon receptor (AHR) in IDO2 expression were determined in PBMC from another PASC cohort by immunohistochemistry (IHC) for IDO2, IDO1, AHR, kynurenine metabolites, autophagy, and apoptosis. These PBMC were also analyzed by metabolomics and for mitochondrial functioning by respirometry. IHC was also performed on autopsy brain material from two PASC patients. Findings: IDO2 is expressed and active in PBMC from PASC patients, as well as in brain tissue, long after SARS-CoV-2 infection. This is paralleled by autophagy, and in blood cells by reduced mitochondrial functioning, reduced intracellular levels of amino acids and Krebs cycle-related compounds. IDO2 expression and activity is triggered by SARS-CoV-2-infection, but the severity of SARS-CoV-2-induced pathology appears related to the generated specific kynurenine metabolites. Ex vivo, IDO2 expression and autophagy can be halted by an AHR antagonist. Interpretation: SARS-CoV-2 infection triggers long-lasting IDO2 expression, which can be halted by an AHR antagonist. The specific kynurenine catabolites may relate to SARS-CoV-2-induced symptoms and pathology. Funding: None.

Published
2023
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2. Improving indicator-condition guided testing for HIV in the hospital setting (PROTEST 2·0): A multicenter, interrupted time-series analysis

Author

Saskia J. Bogers, Maarten F. Schim van der Loeff, Anders Boyd, Udi Davidovich, Marc van der Valk, Kees Brinkman, Kim Sigaloff, Judith Branger, Nejma Bokhizzou, Godelieve J. de Bree, Peter Reiss, Jan E.A.M. van Bergen, Suzanne E. Geerlings, T. van Benthem, D. Bons, G.J. de Bree, P. Brokx, U. Davidovich, F. Deug, S.E. Geerlings, M. Heidenrijk, E. Hoornenborg, M. Prins, P. Reiss, A. van Sighem, M. van der Valk, J. de Wit, W. Zuilhof, N. Schat, D. Smith, M. van Agtmael, J. Ananworanich, D. Van de Beek, G.E.L. van den Berk, D. Bezemer, A. van Bijnen, J.P. Bil, W.L. Blok, S.J. Bogers, M. Bomers, A. Boyd, W. Brokking, D. Burger, K. Brinkman, N. Brinkman, M. de Bruin, S. Bruisten, L. Coyer, R. van Crevel, M. Dijkstra, Y.T. van Duijnhoven, A. van Eeden, L. Elsenburg, M.A.M. van den Elshout, E. Ersan, P.E.V. Felipa, T.B.H. Geijtenbeek, J. van Gool, A. Goorhuis, M. Groot, C.A. Hankins, A. Heijnen, M.M.J Hillebregt, M. Hommenga, J.W. Hovius, Y. Janssen, K. de Jong, V. Jongen, N.A. Kootstra, R.A. Koup, F.P. Kroon, T.J.W. van de Laar, F. Lauw, M.M. van Leeuwen, K. Lettinga, I. Linde, D.S.E. Loomans, I.M. van der Lubben, J.T. van der Meer, T. Mouhebati, B.J. Mulder, J. Mulder, F.J. Nellen, A. Nijsters, H. Nobel, E.L.M. Op de Coul, E. Peters, I.S. Peters, T. van der Poll, O. Ratmann, C. Rokx, M.F. Schim van der Loeff, W.E.M. Schouten, J. Schouten, J. Veenstra, A. Verbon, F. Verdult, J. de Vocht, H.J. de Vries, S. Vrouenraets, M. van Vugt, W.J. Wiersinga, F.W. Wit, L.R. Woittiez, S. Zaheri, P. Zantkuijl, A. Żakowicz, M.C. van Zelm, and H.M.L. Zimmermann

Subjects
HIV, HIV testing, Indicator condition, Tuberculosis, Cervical carcinoma, Cervical dysplasia, Public aspects of medicine, RA1-1270
Abstract

Summary: Background: Indicator-condition (IC) guided HIV testing is a feasible and cost-effective strategy to identify undiagnosed people living with HIV (PLHIV), but remains insufficiently implemented. We aimed to promote IC-guided HIV testing in seven ICs. Methods: Relevant departments in five hospitals of the Amsterdam region participated. HIV testing among adult patients without known HIV infection but with an IC was assessed using electronic health records during pre-intervention (January 2015–June 2020) and intervention (July 2020–June 2021) periods. The multifaceted intervention included audit and feedback. The primary endpoint was HIV testing ≤3 months before or after IC diagnosis and the effect of the intervention was evaluated using segmented Poisson regression. Findings: Data from 7986 patients were included, of whom 6730 (84·3%) were diagnosed with an IC in the pre-intervention period and 1256 (15·7%) in the intervention period. The proportion HIV tested ≤3 months before or after IC diagnosis increased from 36.8% to 47.0% (adjusted risk ratio [RR]= 1.16, 95% CI=1.03–1.30, p=0.02). For individual ICs, we observed significant increases in HIV testing among patients with cervical cancer or intraepithelial neoplasia grade 3 (adjusted RR=3.62, 95% CI=1.93–6.79) and peripheral neuropathy (adjusted RR=2.27 95% CI=1.48–3.49), but not the other ICs. Eighteen of 3068 tested patients were HIV positive (0.6%). Interpretation: Overall IC-guided testing improved after the intervention, but not for all ICs. Variations in effect by IC may have been due to variations in implemented developments, but the effect of separate elements could not be assessed. Funding: HIV Transmission Elimination Amsterdam (H-TEAM) initiative, Aidsfonds (grant number: P-42702).

Published
2022
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3. Current evidence on the adoption of indicator condition guided testing for HIV in western countries: A systematic review and meta-analysis

Author

S.J. Bogers, S.H. Hulstein, M.F. Schim van der Loeff, G.J. de Bree, P. Reiss, J.E.A.M van Bergen, and S.E. Geerlings

Subjects
Medicine (General), R5-920
Abstract

Background: Indicator condition (IC) guided testing for HIV is an effective way to identify undiagnosed people living with HIV, but studies suggest its implementation is lacking. This systematic review provides an overview of the adoption of IC-guided testing in Western countries. Methods: Seven ICs were selected: tuberculosis (TB), malignant lymphoma, hepatitis B, hepatitis C, cervical/vulvar carcinoma/intraepithelial neoplasia grade 2+ (CC/CIN2+, VC/VIN2+), and peripheral neuropathy (PN). Embase and Ovid MEDLINE were searched up to November 20th, 2020. Publications of all types, using data from ≥2009, reporting on HIV test ratios in patients ≥18 years in all settings in Western countries were eligible. HIV test ratios and positivity were reported per IC. A random effects-model for proportions was used to calculate estimated proportions (ES) with 95% CIs. This study was registered at PROSPERO, registration number CRD42020160243. Findings: Fifty-seven references, including 23 full-text articles and 34 other publications were included. Most (28/57) reported on HIV testing in TB. No reports on HIV testing in VC/VIN2+ or PN patients were eligible for inclusion. Large variation in HIV test ratios was observed between and within ICs, resulting from different testing approaches. Highest HIV test ratios (pooled ratio: 0·72, 95%CI 0·63–0·80) and positivity (0·05, 95% CI 0·03–0·06) were observed among TB patients, and lowest among CC/CIN2+ patients (pooled ES test ratio: 0·12, 95%CI 0·01–0·31, positivity: 0·00, 95%CI 0·00–0·00). Interpretation: IC-guided HIV testing is insufficiently implemented in Western countries. The large variation in test ratios provides insight into priority areas for implementing routine IC-guided HIV testing in the future. Funding: HIV Transmission Elimination in Amsterdam (H-TEAM) consortium and Aidsfonds (grant number P-42,702).

Published
2021
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4. Lung Microbiota of Critically Ill Patients with COVID-19 Are Associated with Nonresolving Acute Respiratory Distress Syndrome

Author

Robert F. J. Kullberg, Justin de Brabander, Leonoor S. Boers, Jason J. Biemond, Esther J. Nossent, Leo M. A. Heunks, Alexander P. J. Vlaar, Peter I. Bonta, Tom van der Poll, JanWillem Duitman, Lieuwe D. J. Bos, W. Joost Wiersinga, Anno Saris, Heder De Vries, Lilian J. Meijboom, Siebe G. Blok, Alex R. Schuurman, Tom D.Y. Reijnders, Juan J. Garcia Vallejo, Hetty Bontkes, René Lutter, Harm Jan Bogaard, S. de Bruin, R. Koning, M.A. van Agtmael, A.G. Algera, F.E.H.P. van Baarle, D.J.C. Bax, M. Beudel, M. Bomers, M. Botta, G.J. de Bree, M. Bugiani, E.B. Bulle, O. Chouchane, A.P.M. Cloherty, P.E. Elbers, L.M. Fleuren, S.E. Geerlings, B.F. Geerts, T.B.H. Geijtenbeek, A.R.J. Girbes, A. Goorhuis, M.P. Grobusch, F.M.J. Hafkamp, L.A. Hagens, J. Hamann, V.C. Harris, R. Hemke, S.M. Hermans, M.W. Hollmann, J. Horn, J.W. Hovius, M.D. de Jong, N. van Mourik, J.F Nellen, F. Paulus, E. Peters, B. Preckel, S.J. Raasveld, M. Schinkel, M.J. Schultz, K. Sigaloff, M.R. Smit, C. Stijnis, W. Stilma, C.E. Teunissen, P. Thoral, A.M. Tsonas, M. van der Valk, D.P. Veelo, M. van Vugt, D. Wouters, A.H. Zwinderman, M.C. Brouwer, D. van de Beek, Internal medicine, Pulmonary medicine, CCA - Cancer Treatment and quality of life, VU University medical center, ACS - Heart failure & arrhythmias, ACS - Pulmonary hypertension & thrombosis, Center of Experimental and Molecular Medicine, Graduate School, Intensive Care Medicine, ACS - Microcirculation, AII - Inflammatory diseases, Pulmonology, Infectious diseases, and 01 Internal and external specialisms

Subjects
Pulmonary and Respiratory Medicine, Respiratory Distress Syndrome, Tumor Necrosis Factor-alpha, Critical Illness, Microbiota, host–microbial interactions, COVID-19, Critical Care and Intensive Care Medicine, Respiration, Artificial, RNA, Ribosomal, 16S, Humans, artificial respiration, lung microbiome, Lung
Abstract

Rationale: Bacterial lung microbiota are correlated with lung inflammation and acute respiratory distress syndrome (ARDS) and altered in severe coronavirus disease (COVID-19). However, the association between lung microbiota (including fungi) and resolution of ARDS in COVID-19 remains unclear. We hypothesized that increased lung bacterial and fungal burdens are related to nonresolving ARDS and mortality in COVID-19. Objectives: To determine the relation between lung microbiota and clinical outcomes of COVID-19-related ARDS. Methods: This observational cohort study enrolled mechanically ventilated patients with COVID-19. All patients had ARDS and underwent bronchoscopy with BAL. Lung microbiota were profiled using 16S rRNA gene sequencing and quantitative PCR targeting the 16S and 18S rRNA genes. Key features of lung microbiota (bacterial and fungal burden, α-diversity, and community composition) served as predictors. Our primary outcome was successful extubation adjudicated 60 days after intubation, analyzed using a competing risk regression model with mortality as competing risk. Measurements and Main Results: BAL samples of 114 unique patients with COVID-19 were analyzed. Patients with increased lung bacterial and fungal burden were less likely to be extubated (subdistribution hazard ratio, 0.64 [95% confidence interval, 0.42-0.97]; P = 0.034 and 0.59 [95% confidence interval, 0.42-0.83]; P = 0.0027 per log10 increase in bacterial and fungal burden, respectively) and had higher mortality (bacterial burden, P = 0.012; fungal burden, P = 0.0498). Lung microbiota composition was associated with successful extubation (P = 0.0045). Proinflammatory cytokines (e.g., tumor necrosis factor-α) were associated with the microbial burdens. Conclusions: Bacterial and fungal lung microbiota are related to nonresolving ARDS in COVID-19 and represent an important contributor to heterogeneity in COVID-19-related ARDS.

Published
2022
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6. High incidence of HCV in HIV-negative men who have sex with men using pre-exposure prophylaxis

Author

Elske Hoornenborg, Liza Coyer, Anders Boyd, Roel Christiaan Alfons Achterbergh, Maarten Franciscus Schim van der Loeff, Sylvia Bruisten, Henry John Christiaan de Vries, Jelle Koopsen, Thijs J.W. van de Laar, Maria Prins, J.E.A.M. van Bergen, G.J. de Bree, P. Brokx, F. Deug, M. Heidenrijk, M. Prins, P. Reiss, M. van der Valk, U. Davidovich, S.E. Geerlings, E. Hoornenborg, A. Oomen, A. van Sighem, W. Zuilhof, M.L. Groot Bruinderink, R.C.A. Achterbergh, M. van Agtmael, J. Ananworanich, D. Van de Beek, G.E.L. van den Berk, D. Bezemer, A. van Bijnen, W.L. Blok, S. Bogers, M. Bomers, C.A.B. Boucher, W. Brokking, D. Burger, K. Brinkman, N. Brinkman, M. de Bruin, S. Bruisten, L. Coyer, R. van Crevel, C.G. Daans, L. Dellemann, M. Dijkstra, Y.T. van Duijnhoven, A. van Eeden, L. Elsenburg, M.A.M. van den Elshout, C. Ester, E. Ersan, P.E.V. Felipa, P.H.J. Frissen, T.B.H. Geijtenbeek, M.H. Godfried, J. van Gool, A. Goorhuis, M. Groot, C.A. Hankins, A. Heijnen, M.M.J. Hillebregt, A. Hogewoning, M. Hommenga, J.W. Hovius, Y. Janssen, K. de Jong, V. Jongen, N.A. Kootstra, R.A. Koup, F.P. Kroon, T.J.W. van de Laar, F. Lauw, M.M. van Leeuwen, K. Lettinga, I. Linde, D.S.E. Loomans, J.T. van der Meer, T. Mouhebati, B.J. Mulder, J. Mulder, F.J. Nellen, A. Nijsters, H. Nobel, P. Oostvogel, E.L.M. Op de Coul, E. Peters, I.S. Peters, T. van der Poll, O. Ratmann, C. Rokx, M.S. van Rooijen, M.F. Schim van der Loeff, W.E.M. Schoute, G.J. Sonder, J. Veenstra, A. Verbon, F. Verdult, J. de Vocht, H.J. de Vries, S. Vrouenraets, M. van Vugt, W.J. Wiersinga, F.W. Wit, L.R. Woittiez, S. Zaheri, P. Zantkuijl, M.C. van Zelm, A. Żakowicz, H.M.L. Zimmermann, Anatomy and neurosciences, Internal medicine, AII - Infectious diseases, ACS - Diabetes & metabolism, Medical psychology, Molecular cell biology and Immunology, Amsterdam Movement Sciences - Rehabilitation & Development, Amsterdam Movement Sciences, AMS - Rehabilitation & Development, APH - Quality of Care, APH - Health Behaviors & Chronic Diseases, APH - Methodology, APH - Global Health, Graduate School, Infectious diseases, Medical Microbiology and Infection Prevention, Dermatology, General practice, ACS - Heart failure & arrhythmias, APH - Personalized Medicine, APH - Aging & Later Life, Global Health, Neurology, Experimental Immunology, Center of Experimental and Molecular Medicine, APH - Digital Health, Internal Medicine, Medical Microbiology & Infectious Diseases, and Virology

Subjects
Adult, Male, medicine.medical_specialty, Genotype, Hepatitis C virus, Sexual Behavior, Hepacivirus, medicine.disease_cause, Transgender Persons, Men who have sex with men, Pre-exposure prophylaxis, SDG 3 - Good Health and Well-being, Internal medicine, medicine, Humans, Homosexuality, Male, Survival analysis, Phylogeny, Hepatology, AIDS-Related Opportunistic Infections, Unsafe Sex, business.industry, Transmission (medicine), Incidence (epidemiology), Incidence, Hazard ratio, virus diseases, HIV, Hepatitis C, Homosexuality, Middle Aged, medicine.disease, Risk factors, Reinfection, Molecular epidemiology, RNA, Viral, Female, business, Follow-Up Studies
Abstract

Background & Aims: HCV has emerged as a sexually transmitted infection (STI) among HIV-positive men who have sex with men (MSM). We evaluated HCV incidence and its risk factors among HIV-negative MSM using HIV pre-exposure prophylaxis (PrEP). Methods: Participants of the Amsterdam PrEP project were tested for HCV antibodies or HCV-RNA every 6 months. Participants used daily or event-driven PrEP and could switch regimens during follow-up. We calculated incidence rates (IRs) for overall HCV infection and separately for primary and re-infection. A univariable Bayesian exponential survival model was used to identify risk factors associated with incident HCV infection. The HCV NS5B gene fragment (709 bp) was sequenced and compared to HCV isolates from HIV-positive MSM and other risk groups (n = 419) using phylogenetic analysis. Results: Among 350 participants contributing 653.6 person-years (PYs), we detected 15 HCV infections in 14 participants (IR = 2.30/100PY). There were 8 primary infections (IR = 1.27/100PY) and 7 re-infections (IR = 27.8/100PY). IR was 2.71/100PY in daily and 1.15/100PY in event-driven PrEP users. Factors associated with incident HCV infection were higher number of receptive condomless anal sex acts with casual partners (posterior hazard ratio [HR] 1.57 per ln increase; 95% credibility interval [CrI] 1.09–2.20), anal STI (posterior HR 2.93; 95% CrI 1.24–7.13), injecting drug use (posterior HR 4.69; 95% CrI 1.61–12.09) and sharing straws when snorting drugs (posterior HR 2.62; 95% CrI 1.09–6.02). We identified robust MSM-specific HCV clusters of subtypes 1a, 4d, 2b and 3a, which included MSM with and without HIV. Conclusions: HIV-negative MSM using PrEP are at risk of incident HCV infection, while identified risk factors are similar to those in HIV-positive MSM. Regular HCV testing is needed, especially for those with a previous HCV infection and those reporting risk factors. Lay summary: We report that hepatitis C virus infections are frequently acquired among HIV-negative men who have sex with men (MSM) using pre-exposure prophylaxis to prevent HIV infection. New infections occurred more frequently in those reporting receptive anal sex without using condoms, having an anal sexually transmitted infection, injecting drugs, and sharing straws when snorting drugs. The viruses found in HIV-negative men using pre-exposure prophylaxis are genetically similar to those in HIV-positive men, but not in other hepatitis C risk groups, suggesting that (sexual) transmission is occurring between HIV-positive MSM and HIV-negative MSM using pre-exposure prophylaxis. Clinical Trial number: Dutch trial registration number NTR5411.

Published
2020
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