Angioedema induced by angiotensin-converting enzyme inhibitors: an analysis of hospitalizations during the COVID-19 pandemic

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Abstract

Backgraund: The pathogenesis of angioedema induced by angiotensin-converting enzyme inhibitors is based on the accumulation of bradykinin as a result of angiotensin-converting enzyme blockade. The SARS-CoV-2 virus by binding to the angiotensin-converting enzyme 2 receptor, may inhibit its production, which in turn leads to an increase in bradykinin levels. Thus, infection with SARS-CoV-2 may be a likely trigger for the development of angioedema.

Aims: to analyze the cases of hospitalizations of patients with angioedema associated with the use of angiotensin-converting enzyme inhibitors and angiotensin receptor blockers during the COVID-19 pandemic.

Materials and methods: a retrospective analysis of the medical records of inpatient patients admitted to the Vitebsk Regional Clinical Hospital in May-December 2020 with isolated (without urticaria) angioedema while receiving angiotensin-converting enzyme inhibitors or angiotensin receptor blockers was performed. All patients received smears from the naso- and oropharynx for COVID-19 by polymerase chain reaction.

Results: there were admitted 15 patients (9 men and 6 women) aged 44-72 years for emergency indications, which was 53.6% among all patients with isolated angioedema. In two cases, a concomitant diagnosis of mild COVID-19 infection was established with the predominance symptoms of angioedema in the clinical picture with localization in the face, tongue, sublingual area, soft palate. All patients had a favorable outcome of the disease.

Conclusions: patients with аngiotensin-converting enzyme inhibitor-induced angioedema may need to be hospitalized to monitor upper respiratory tract patency. There were cases of a combination of аngiotensin-converting enzyme inhibitor-induced angioedema and mild COVID-19 infection. Issues requiring additional research: the effect of SARS-CoV-2 infection on the levels of bradykinin and its metabolites; the trigger role of COVID-19 infection in the development of angioedema in patients receiving angiotensin-converting enzyme inhibitors/angiotensin receptor blockers; recommendations for the management of patients with аngiotensin-converting enzyme inhibitor-induced angioedema and a positive result for COVID-19.

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OBOSNOVANIE

Ingibitory angiotenzinprevrashhajushhego fermenta (IAPF) i blokatory angiotenzinovyh receptorov (BAR) zanimajut odno iz vedushhih mest v lechenii arterialnoj gipertenzii (AG) i hronicheskoj serdechnoj nedostatochnosti, pokazany dlja sohranenija pochechnoj funkcii u pacientov s saharnym diabetom i hronicheskoj boleznju pochek. Okolo 40 millionov chelovek v mire primenjajut IAPF. V tozhe vremja, shirokoe ispolzovanie IAPF privelo k uvelicheniju rasprostranennosti pobochnyh reakcij dannoj gruppy lekarstvennyh sredstv (LS) [1, 2].

Angiootek (AO) – harakternyj i potencialno ugrozhajushhij zhizni pobochnyj jeffekt pri prieme IAPF. Dannaja nezhelatelnaja reakcija u lic, poluchajushhih IAPF, razvivaetsja v 0,1-0,7% sluchaev, rezhe (0,1%) AO mozhet voznikat pri prieme BAR [3]. Sredi vseh sluchaev AO, trebujushhih gospitalizacii v otdelenija neotlozhnoj pomoshhi, dolja IAPF-inducirovannyh AO sostavljaet 30-40% [4, 5]. Po nashim dannym, iz 87 pacientov Vitebskoj oblastnoj klinicheskoj bolnicy, gospitalizirovannyh po jekstrennym pokazanijam s izolirovannym AO v 2012 godu, u 44,8% AO byl vyzvan priemom IAPF [6]. Sredi bolnyh, obrativshihsja za neotlozhnoj pomoshhju, do 16% trebujut intubacii i 1% – traheostomii. Bystroe razvitie simptomov; vovlechenie jazyka, mjagkogo neba ili gortani; simptomy sljunotechenija, respiratornogo distressa svjazany s bolee vysokim riskom intubacii [7].

AO, vyzvannye IAPF otnosjatsja k priobretennym bradikinin-oposredovannym AO. Kljuchevuju rol v ih patogeneze igraet sosudorasshirjajushhij peptid bradikinin (BK). IAPF predotvrashhajut prevrashhenie BK v neaktivnye metabolity i privodjat k ego nakopleniju [8]. V razvitii AO pri prieme BAR takzhe predpolagaetsja uchastie BK [9, 10].

IAPF-inducirovannye AO blednye, ne zudjashhie, ne soprovozhdajutsja krapivnicej i chashhe vsego lokalizujutsja v oblasti gub, jazyka, glotki, gortani. K redkoj lokalizacii AO otnosjat organy brjushnoj polosti. Otek mozhet razvivatsja v razlichnye sroki ot nachala primenenija IAPF. Faktory riska: afroamerikanskoe proishozhdenie, zhenskij pol, pozhiloj vozrast, kurenie, sezonnaja allergija. AO mozhet razreshitsja spontanno, no pri prodolzhenii priema IAPF, kak pravilo, voznikaet recidiv [5, 11]. Posle prekrashhenija priema IAPF sohranjaetsja verojatnost recidiva AO v techenie priblizitelno shesti nedel za schet podavlenija tkanevogo APF. V jetot srok pacientam ne rekomenduetsja naznachat LS, snizhajushhie aktivnost renin-angiotenzin-aldosteronovoj sistemy (RAAS) [11]. U pacientov s IAPF-inducirovannymi AO, pri zamene na BAR risk razvitija takoj nezhelatelnoj reakcii sostavljaet <10% (ot 0 do 17%) [12].

Pacienty s IAPF-inducirovannymi AO nuzhdajutsja v svoevremennoj diagnostike i neotlozhnoj pomoshhi s korrekciej terapii dlja predotvrashhenija povtornyh jepizodov. Diagnoz ustanavlivaetsja na osnovanii anamneza, klinicheskoj kartiny, iskljuchenija gistaminovyh i drugih vidov bradikininovyh AO [5]. Odobrennoj targetnoj terapii ostryh pristupov AO, vyzvannyh IAPF v nastojashhee vremja ne sushhestvuet. Dlja lechenija tjazhelyh form obsuzhdaetsja vozmozhnost primenenija ikatibanta [2].

V vozniknovenii AO u pacientov, poluchajushhih IAPF (osobenno dlitelnoe vremja), vazhnoe znachenie prinadlezhit razlichnym triggeram. Sredi LS, kotorye mogut sposobstvovat razvitiju AO na fone priema IAPF, nazyvajutsja nesteroidnye protivovospalitelnye sredstva, antagonisty kalcija, immunodepressanty, ingibitory dipeptidilpeptidazy IV, ingibitory mTOR. Provocirujushhimi faktorami takzhe mogut byt travma, hirurgicheskie manipuljacii v oblasti golovy ili shei [2, 5, 8]. Predpolagaetsja, chto infekcija COVID-19 takzhe mozhet javljatsja triggerom razvitija AO u lic, poluchajushhih IAPF [13]. Virus SARS-CoV-2, svjazyvajas s receptorom angiotenziprevrashhajushhego fermenta 2 (APF2), vozmozhno, podavljaet produkciju APF2, chto v svoju ochered vedet k povysheniju urovnja BK [14]. Opisany sluchai izolirovannyh AO u pacientov, inficirovannyh SARS-CoV-2, poluchajushhih IAPF [13, 15, 16].

CEL

Provesti analiz sluchaev gospitalizacij pacientov s AO, associirovannymi s priemom IAPF ili BAR v period pandemii COVID-19.

METODY

Dizajn issledovanija

Rabota vypolnena v dizajne odnocentrovogo retrospektivnogo sploshnogo nekontroliruemogo issledovanija, kotoroe vkljuchalo analiz medicinskih kart pacientov s AO na fone priema IAPF/BAR, gospitalizirovannyh v period pandemii COVID-19.

Kriterii sootvetstvija

Kriterii vkljuchenija: ustanovlennyj diagnoz AO (T78.3, MKB-10); priem IAPF/BAR; otsutstvie drugih verojatnyh prichin razvitija AO. Kriterii nevkljuchenija: sochetanie AO i krapivnicy; nasledstvennyj AO (D84.1, MKB-10).

Uslovija provedenija

Issledovanie provodiloc na baze UZ «Vitebskaja oblastnaja klinicheskaja bolnica» (VOKB), Respublika Belarus. V issleduemyj period v UZ «VOKB» osushhestvljalas gospitalizacija pacientov v vozraste 18 let i starshe s jekstrennoj allergologicheskoj patologiej.

Prodolzhitelnost issledovanija

Period vkljuchenija v issledovanie – maj-dekabr 2020 g.; smeshhenie zaplanirovannyh vremennyh intervalov ne predstavleno.

Opisanie medicinskogo vmeshatelstva

Issledovanie osushhestvljali metodom sploshnoj vyborki medicinskih kart pacientov, nahodivshihsja na lechenii v reanimacionnom (RAO) i allergologicheskom otdelenijah UZ «VOKB» s izolirovannym (bez krapivnicy) AO s maja po dekabr 2020 g. U vseh pacientov pri postuplenii v stacionar provodilos objazatelnoe laboratornoe issledovanie biomateriala (mazok iz noso- i rotoglotki) na nalichie soputstvujushhej infekcii COVID-19 metodom polimeraznoj cepnoj reakcii (PCR) v rezhime realnogo vremeni. Dlja dalnejshego analiza otobrany medicinskie karty pacientov, kotorye poluchali IAPF/BAR i ne imeli drugih ochevidnyh prichin razvitija AO. Dlja ustanovlenija prichinno-sledstvennoj svjazi razvitija AO s priemom IAPF/BAR primenjali algoritm Naranzho [17].

Osnovnoj ishod issledovanija

Ocenivali kliniko-anamnesticheskie dannye, rezultaty laboratornyh i instrumentalnyh obsledovanij pacientov s AO na fone priema IAPF/BAR.

Dopolnitelnye ishody issledovanija

Analizirovali prichinno-znachimye IAPF/BAR.

Analiz v podgruppah

Sredi gospitalizirovannyh pacientov s izolirovannymi AO, vydelena gruppa bolnyh s IAPF/BAR inducirovannymi AO.

Metody registracii ishodov

Analiz pokazatelej, vnesennyh v bazu dannyh iz medicinskih kart stacionarnyh pacientov: demograficheskie pokazateli (pol, vozrast); osnovnoj klinicheskij diagnoz i soputstvujushhie zabolevanija; lokalizacija AO; gospitalizacija v RAO; prichinno-znachimye IAPF/BAR i soputstvujushhie LS; anamnesticheskie dannye (jepizody AO, atopija v anamneze); dannye osnovnyh laboratornyh (obshhij analiz krovi, biohimicheskij analiz krovi, koagulogramma) i instrumentalnyh (rentgenografija organov grudnoj kletki, JeKG) issledovanij; rezultaty kachestvennogo opredelenija IgG/IgM k SARS-CoV-2 v syvorotke krovi i mazkov iz noso- i rotoglotki na COVID-19 metodom PCR.

Jeticheskaja jekspertiza

Dizajn iccledovanija odobren komitetom po jetike klinicheskih ispytanij UO «Vitebskij gosudarstvennyj ordena Druzhby narodov medicinskij universitet», protokol № 7 ot 02.12.2020 g.

Statisticheskij analiz

Principy rascheta razmera vyborki: razmer vyborki predvaritelno ne rasschityvalsja.

Metody statisticheskogo analiza dannyh: dlja obrabotki dannyh ispolzovali programmnoe obespechenie Statistica 10.0 (StatSoft Inc., SShA) i Microsoft Office Excel 2016 (Microsoft Corporation, SShA); rasschityvalas mediana (25-75% interkvartilnyj razmah) vozrasta pacientov – Me (25;75), dostovernost razlichij kolichestvennyh pokazatelej opredeljali po kriteriju Manna-Uitni, chastoty kachestvennyh priznakov – po 2-h storonnemu tochnomu kriteriju Fishera; rezultaty schitali statisticheski znachimymi pri r<0,05.

REZULTATY

Obekty (uchastniki) issledovanija

V hode issledovanija my retrospektivno ocenili medicinskie karty 28 pacientov, gospitalizirovannyh po jekstrennym pokazanijam v UZ «VOKB» s maja po dekabr 2020 g. s izolirovannymi AO. Dlja dalnejshego analiza vybrany medicinskie karty 15 pacientov (9 muzhchin i 6 zhenshhin), kotorye poluchali lechenie IAPF/BAR i ne imeli drugih ochevidnyh prichin dlja razvitija AO. Dolja AO, vyzvannyh IAPF/BAR sostavila 53,6%. Prichinno-sledstvennaja svjaz s priemom IAPF/BAR soglasno ispolzovannomu algoritmu Naranzho rascenena kak verojatnaja u 12 (80%) bolnyh, vozmozhnaja – u 3 (20%). Vozrast bolnyh s ustanovlennym diagnozom IAPF/BAR-inducirovannogo AO sostavil 59(55;62) let i dostoverno ne otlichalsja ot vozrasta pacientov s izolirovannymi AO ot drugih prichin.

Osnovnye rezultaty issledovanija

Harakteristika pacientov s IAPF/BAR-inducirovannymi AO predstavlena v tablice 1. Lokalizacija oteka otmechena v oblasti lica, jazyka i mjagkogo neba (risunok 1). Gospitalizacija v RAO potrebovalas 3 (20%) pacientam. Povtornye jepizody otmecheny u 9/15 pacientov, v tom chisle 3-h sluchajah svjazannye s povtornym primeneniem IAPF. Chastota gospitalizacii v RAO dostoverno ne otlichalas u pacientov s AO na fone priema IAPF/BAR i pacientov s izolirovannymi AO ne poluchavshih IAPF/BAR (r>0,05). Atopiju/bronhialnuju astmu v anamneze imeli 2 (13,3%) pacienta. Vse bolnye poluchali IAPF/BAR po povodu AG, v 7/15 sluchajah primenjalsja rezhim monoterapii, v 5/15 – kombinirovannoe lechenie, v 3/15 sluchajah IAPF ispolzovalis nereguljarno. Bolshinstvo (13, 86,7%) pacientov imeli soputstvujushhie zabolevanija i v 53,3% sluchaev poluchali sovmestno s antigipertenzivnymi LS preparaty drugih grupp.

Kachestvennoe opredelenie IgG/IgM k SARS-CoV-2 provedeno v 12/15 sluchajah. Polozhitelnye IgG k SARS-CoV-2 vyjavleny v 1 sluchae, IgG i IgM – v 2-h (PCR-test otricatelnyj). U vseh pacientov vzjaty mazki iz noso- i rotoglotki na COVID-19 metodom PCR. V 2-h sluchajah poluchen polozhitelnyj rezultat testa PCR i ustanovlen soputstvujushhij diagnoz infekcii COVID-19. Pacienty s AO i COVID-19 ne imeli povyshenija temperatury tela, izmenenij na rentgenogramme organov grudnoj kletki, snizhenija urovnja kisloroda v krovi, otmechalos povyshenie S-reaktivnogo belka i v odnom sluchae – povyshenie urovnja D-dimera. Lokalizacija AO: lico, jazyk, podjazychnaja oblast, mjagkoe nebo.

Lechenie AO vkljuchalo parenteralnoe vvedenie gljukokortikosteroidov (deksametazon), N1-antigistaminnyh LS (klemastin, hloropiramin) i, v rjade sluchaev, furosemida. Vse pacienty imeli blagoprijatnyj ishod AO.

Dopolnitelnye rezultaty issledovanija

Raspredelenie pacientov v zavisimosti ot vida prichinno-znachimogo IAPF/BAR predstavleno na risunke 2. Naibolee chastoj prichinoj razvitija AO byli jenalapril i kaptopril. V 2-h sluchajah sovmestno s kaptoprilom primenjalis dlitelnodejstvujushhie IAPF/BAR.

OBSUZhDENIE

Rezjume osnovnogo rezultata issledovanija

IAPF-inducirovannye AO mogut imet zhizneugrozhajushhuju lokalizaciju i trebovat gospitalizacii. V kachestve vozmozhnogo triggera razvitija dannogo vida AO obsuzhdaetsja infekcija, vyzvannaja SARS-CoV-2. V nashem issledovanii vyjavleny sluchai sochetanija AO na fone priema IAPF i infekcii COVID-19 legkogo techenija.

Obsuzhdenie osnovnogo rezultata issledovanija

V nastojashhee vremja schitaetsja, chto osnovnuju rol v patogeneze IAPF-inducirovannyh AO igraet snizhenie katabolizma i nakoplenie BK. Blokada APF (kininazy II) ne tolko obespechivaet umenshenie obrazovanija angiotenzina (AT) II, no i prepjatstvuet prevrashheniju BK v neaktivnye peptidy [8]. Pri primenenii BAR takzhe vozmozhno uvelichenie urovnja BK. Tak, soglasno jeksperimentalnym dannym, odnim iz sledstvij blokady AT1-receptorov javljaetsja reaktivnoe usilenie obrazovanija AT II. Vozdejstvie AT II na AT2-receptory privodit k povysheniju urovnja BK [9].

BK predstavljaet soboj nonapeptid, kotoryj otshhepljaetsja ot vysokomolekuljarnogo kininogena pod dejstviem kallikreina plazmy. Ego biologicheskij jeffekt realizuetsja cherez aktivaciju receptorov V2, nahodjashhihsja v membranah jendotelialnyh i gladkomyshechnyh kletok. Obrazovavshijsja BK bystro inaktiviruetsja putem fermentativnogo raspada glavnym obrazom pod dejstviem kininazy II (APF), a takzhe nejtralnoj jendopeptidazy (neprilizina) i dipeptidilpeptidazy IV (DPPIV). Karboksipeptidaza N (kininaza I) i aminopeptidaza P (APP) katabolizirujut BK, obrazuja chastichno aktivnye produkty. V rasshheplenii aktivnogo metabolita BK des-Arg9-bradikinina uchastvuet APF2 [2, 5]. Takzhe bylo pokazano, chto v razvitii AO pri prieme IAPF mozhet imet znachenie polimorfizm genov, kodirujushhih sootvetstvujushhie molekuly, uchastvujushhie v metabolizme i dejstvii BK (APP, DPPIV, receptor V2 i dr.). Povyshennyj lokalnyj uroven BK privodit k usileniju vysvobozhdenija oksida azota, prostaglandinov, chto vyzyvaet usilenie pronicaemosti sosudov v postkapilljarnom i venuljarnom otdelah s jekstravazaciej zhidkosti i razvitiem oteka [2].

V dekabre 2019 g. v Kitae nachalas jepidemija novogo infekcionnogo zabolevanija, poluchivshego nazvanie COVID-19, vyzvannogo predstavitelem semejstva koronavirusov – SARS-CoV-2, kotoraja priobrela mirovoj masshtab. Jendotelialnaja disfunkcija i povyshennaja pronicaemost sosudov – harakternye patologicheskie priznaki COVID-19 [18]. Jeti javlenija mogut privodit k uvelicheniju jekstravazacii zhidkosti i povysheniju riska AO. Schitaetsja, chto zashhitnye jeffekty IAPF/BAR svjazany s uvelicheniem jekspressii APF2 i ingibirovaniem izbytochnoj aktivnosti RAAS cherez umenshenie jeffektov AT II. Cvjazyvanie SARS-CoV-2 s receptorom APF2 mozhet privodit k podavleniju poverhnostnoj reguljacii APF2, snizhaja ego zashhitnye jeffekty i usugubljaja neblagoprijatnye jeffekty AT II. Snizhenie jekspressii APF2 narushaet ego rol v rasshheplenii rjada substratov, vkljuchaja metabolity BK [13, 18].

V opisannyh sluchajah razvitija AO na fone primenenija IAPF i infekcii COVID-19, novaja koronavirusnaja infekcija rassmatrivaetsja kak vozmozhnyj triggernyj faktor. Inficirovanie SARS-CoV-2 mozhet javljatsja «vtorym udarom», kotoryj privodit k razvitiju oteka u pacientov, poluchajushhih dannuju gruppu LS [13, 15, 16]. Techenie infekcii COVID-19 harakterizuetsja znachitelnoj variabelnostju. V analiziruemyh nami sluchajah sochetanija IAPF-inducirovannogo AO i COVID-19, v klinicheskoj kartine preobladali simptomy AO. Vozmozhno, priznaki infekcii verhnih dyhatelnyh putej (rinit, bol v gorle) maskirovalis simptomami oteka slizistoj obolochki rotoglotki.

Ogranichenija issledovanija

Ogranichenijami dannogo issledovanija javilis ego retrospektivnyj harakter i nebolshaja prodolzhitelnost analiziruemogo perioda.

ZAKLJuChENIE

Pacienty s IAPF-inducirovannymi AO mogut nuzhdatsja v gospitalizacii dlja monitoringa prohodimosti verhnih dyhatelnyh putej. Naibolee chastoj prichinoj AO sredi analizirovannyh sluchaev byli jenalapril i kaptopril. U pacientov s AO na fone priema IAPF vyjavleny sluchai infekcii COVID-19 legkogo techenija s preobladaniem v klinicheskoj kartine simptomov AO s lokalizaciej v oblasti lica, jazyka, podjazychnoj oblasti, mjagkogo neba. Pri razvitii AO neobhodim celenapravlennyj sbor anamneza otnositelno priema IAPF/BAR i cimptomov COVID-19, a takzhe obsledovanie na infekciju COVID-19 metodom PCR. Voprosy, trebujushhie dopolnitelnyh issledovanij: vlijanie inficirovanija SARS-CoV-2 na urovni BK i ego metabolitov; triggernaja rol infekcii COVID-19 v razvitija AO u pacientov, poluchajushhih IAPF/BAR; rekomendacii po vedeniju pacientov s IAPF-inducirovannymi AO i polozhitelnym rezultatom na COVID-19.

 

 

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About the authors

Tatsiana М. Sabalenka

Vitebsk State Order of Peoples’ Friendship Medical University

Author for correspondence.
Email: t.sobolen@tut.by
ORCID iD: 0000-0002-8702-6486
SPIN-code: 9309-5550

Аssistant Рrofessor of the Department of Basic and Clinical Pharmacology with Faculty Course of Professional Skills Upgrading and Staff Retraining, Vitebsk State Order of Peoples’ Friendship Medical University

Belarus, 210009, Frunze Av., 27, Vitebsk, Republic of Belarus

Volha V. Zakharava

УЗ "Витебская областная клиническая больница"

Email: zakharovkan@mail.ru
ORCID iD: 0000-0002-6696-0704

Head of the Department of Allergy, Vitebsk Regional Clinical Hospital

Belarus, 210037, Voinov-internacionalistov St., 37, Vitebsk, Republic of Belarus

Natallia R. Prakoshyna

Vitebsk State Order of Peoples’ Friendship Medical University

Email: drnatalipr@gmail.com
ORCID iD: 0000-0002-3471-6977
SPIN-code: 4022-5469

Аssistant Рrofessor of the Department of Basic and Clinical Pharmacology with Faculty Course of Professional Skills Upgrading and Staff Retraining, Vitebsk State Order of Peoples’ Friendship Medical University

Belarus, 210009, Frunze Av., 27, Vitebsk, Republic of Belarus

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