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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Headache medication and the COVID-19 pandemic</title><author><name sortKey="Maassenvandenbrink, Antoinette" sort="Maassenvandenbrink, Antoinette" uniqKey="Maassenvandenbrink A" first="Antoinette" last="Maassenvandenbrink">Antoinette Maassenvandenbrink</name><affiliation><nlm:aff id="Aff1"></nlm:aff></affiliation></author><author><name sortKey="De Vries, Tessa" sort="De Vries, Tessa" uniqKey="De Vries T" first="Tessa" last="De Vries">Tessa De Vries</name><affiliation><nlm:aff id="Aff1"></nlm:aff></affiliation></author><author><name sortKey="Danser, A H Jan" sort="Danser, A H Jan" uniqKey="Danser A" first="A. H. Jan" last="Danser">A. H. Jan Danser</name><affiliation><nlm:aff id="Aff1"></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">32334535</idno><idno type="pmc">7183387</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7183387</idno><idno type="RBID">PMC:7183387</idno><idno type="doi">10.1186/s10194-020-01106-5</idno><date when="2020">2020</date><idno type="wicri:Area/Pmc/Corpus">000091</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000091</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Headache medication and the COVID-19 pandemic</title><author><name sortKey="Maassenvandenbrink, Antoinette" sort="Maassenvandenbrink, Antoinette" uniqKey="Maassenvandenbrink A" first="Antoinette" last="Maassenvandenbrink">Antoinette Maassenvandenbrink</name><affiliation><nlm:aff id="Aff1"></nlm:aff></affiliation></author><author><name sortKey="De Vries, Tessa" sort="De Vries, Tessa" uniqKey="De Vries T" first="Tessa" last="De Vries">Tessa De Vries</name><affiliation><nlm:aff id="Aff1"></nlm:aff></affiliation></author><author><name sortKey="Danser, A H Jan" sort="Danser, A H Jan" uniqKey="Danser A" first="A. H. Jan" last="Danser">A. H. Jan Danser</name><affiliation><nlm:aff id="Aff1"></nlm:aff></affiliation></author></analytic><series><title level="j">The Journal of Headache and Pain</title><idno type="ISSN">1129-2369</idno><idno type="eISSN">1129-2377</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p id="Par1">The world is currently dominated by the Corona Virus Disease 2019 (COVID-19) pandemic. Besides the obvious concerns about limitation of virus spread and providing the best possible care to infected patients, a concomitant concern has now arisen in view of a putative link between the use of certain drugs, such as Renin-Angiotensin System (RAS) inhibitors and ibuprofen, and an increased risk for COVID-19 infection. We here discuss this concern in relation to headache treatment and conclude that, based on current evidence, there is no reason to abandon treatment of headache patients with RAS inhibitors or ibuprofen.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Fang, L" uniqKey="Fang L">L Fang</name></author><author><name sortKey="Karakiulakis, G" uniqKey="Karakiulakis G">G Karakiulakis</name></author><author><name sortKey="Roth, M" uniqKey="Roth M">M Roth</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Li, W" uniqKey="Li W">W Li</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Loder, E" uniqKey="Loder E">E Loder</name></author><author><name sortKey="Rizzoli, P" uniqKey="Rizzoli P">P Rizzoli</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Shamliyan, Ta" uniqKey="Shamliyan T">TA Shamliyan</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pomes, Lm" uniqKey="Pomes L">LM Pomes</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Serfozo, P" uniqKey="Serfozo P">P Serfozo</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Arendse, Lb" uniqKey="Arendse L">LB Arendse</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ferrario, Cm" uniqKey="Ferrario C">CM Ferrario</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Wang, X" uniqKey="Wang X">X Wang</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kurth, T" uniqKey="Kurth T">T Kurth</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Qiao, W" uniqKey="Qiao W">W Qiao</name></author></analytic></biblStruct></listBibl></div1></back></TEI><pmc article-type="letter"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Headache Pain</journal-id><journal-id journal-id-type="iso-abbrev">J Headache Pain</journal-id><journal-title-group><journal-title>The Journal of Headache and Pain</journal-title></journal-title-group><issn pub-type="ppub">1129-2369</issn><issn pub-type="epub">1129-2377</issn><publisher><publisher-name>Springer Milan</publisher-name><publisher-loc>Milan</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">32334535</article-id><article-id pub-id-type="pmc">7183387</article-id><article-id pub-id-type="publisher-id">1106</article-id><article-id pub-id-type="doi">10.1186/s10194-020-01106-5</article-id><article-categories><subj-group subj-group-type="heading"><subject>Commentary</subject></subj-group></article-categories><title-group><article-title>Headache medication and the COVID-19 pandemic</article-title></title-group><contrib-group><contrib contrib-type="author" corresp="yes"><name><surname>MaassenVanDenBrink</surname><given-names>Antoinette</given-names></name><address><email>a.vanharen-maassenvandenbrink@erasmusmc.nl</email></address><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author"><name><surname>de Vries</surname><given-names>Tessa</given-names></name><xref ref-type="aff" rid="Aff1"></xref></contrib><contrib contrib-type="author"><name><surname>Danser</surname><given-names>A. H. Jan</given-names></name><xref ref-type="aff" rid="Aff1"></xref></contrib><aff id="Aff1"><institution-wrap><institution-id institution-id-type="GRID">grid.5645.2</institution-id><institution-id institution-id-type="ISNI">000000040459992X</institution-id><institution>Dept. of Internal Medicine, Division of Pharmacology and Vascular Medicine,</institution><institution>Erasmus MC University Medical Center Rotterdam,</institution></institution-wrap>P.O. Box 2040, 3000 CA Rotterdam, The Netherlands</aff></contrib-group><pub-date pub-type="epub"><day>25</day><month>4</month><year>2020</year></pub-date><pub-date pub-type="pmc-release"><day>25</day><month>4</month><year>2020</year></pub-date><pub-date pub-type="collection"><year>2020</year></pub-date><volume>21</volume><issue>1</issue><elocation-id>38</elocation-id><history><date date-type="received"><day>2</day><month>4</month><year>2020</year></date><date date-type="accepted"><day>13</day><month>4</month><year>2020</year></date></history><permissions><copyright-statement>© The Author(s) 2020</copyright-statement><license license-type="OpenAccess"><license-p><bold>Open Access</bold>This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>. The Creative Commons Public Domain Dedication waiver (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>) applies to the data made available in this article, unless otherwise stated in a credit line to the data.</license-p></license></permissions><abstract id="Abs1"><p id="Par1">The world is currently dominated by the Corona Virus Disease 2019 (COVID-19) pandemic. Besides the obvious concerns about limitation of virus spread and providing the best possible care to infected patients, a concomitant concern has now arisen in view of a putative link between the use of certain drugs, such as Renin-Angiotensin System (RAS) inhibitors and ibuprofen, and an increased risk for COVID-19 infection. We here discuss this concern in relation to headache treatment and conclude that, based on current evidence, there is no reason to abandon treatment of headache patients with RAS inhibitors or ibuprofen.</p></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd>COVID-19</kwd><kwd>Corona virus</kwd><kwd>Headache</kwd><kwd>Migraine</kwd><kwd>RAS inhibitors</kwd><kwd>Candesartan</kwd><kwd>Ibuprofen</kwd></kwd-group><funding-group><award-group><funding-source><institution>Dutch Research Council (NWO)</institution></funding-source><award-id>Vici grant 09150181910040</award-id><principal-award-recipient><name><surname>MaassenVanDenBrink</surname><given-names>Antoinette</given-names></name></principal-award-recipient></award-group></funding-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© The Author(s) 2020</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec id="Sec1"><title>Background</title><p id="Par14">The world is currently dominated by the pandemic spread of the severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2), which has already infected almost 2,000,000 people worldwide, leading to more than 120,000 deaths (for actual number, see <ext-link ext-link-type="uri" xlink:href="https://who.sprinklr.com/">https://who.sprinklr.com/</ext-link>). Whereas the priority of health authorities is to limit the spread of this virus and to provide the best possible care for patients [<xref ref-type="bibr" rid="CR1">1</xref>], this pandemic also has consequences for the treatment of other diseases, such as headache. A statement from the European Headache Federation on how to currently treat headache patients (often from a distance) has recently been published (<ext-link ext-link-type="uri" xlink:href="https://twitter.com/EMHAlliance/status/1243096347731001344">https://twitter.com/EMHAlliance/status/1243096347731001344</ext-link>). A concomitant concern has now arisen in view of a putative link between the use of certain drugs and an increased risk for COVID-19 infection [<xref ref-type="bibr" rid="CR2">2</xref>]. This particularly applies to renin-angiotensin system (RAS) blockers and the non-steroid anti-inflammatory drug (NSAID) ibuprofen, and is based on the idea that these drugs upregulate the expression of Angiotensin-Converting Enzyme (ACE) 2, the receptor which facilitates SARS-CoV-2 entry [<xref ref-type="bibr" rid="CR3">3</xref>]. Such entry depends on priming by the serine protease transmembrane protease, serine 2 (TMPRSS2) (Fig. <xref rid="Fig1" ref-type="fig">1</xref>).
<fig id="Fig1"><label>Fig. 1</label><caption><p>The carboxypeptidase angiotensin-converting enzyme 2 (ACE2) converts angiotensin (Ang) I into Ang-(1–9) and Ang II into Ang-(1–7) and (panel <bold>a</bold>), yet is not blocked by ACE inhibitors, which prevent the conversion of Ang I to Ang II. As depicted in (panel <bold>b</bold>), ACE2 also binds and internalizes SARS-Cov-2, after priming by the serine protease transmembrane protease, serine 2 (TMPRSS2). Shedding of membrane-bound ACE2 by a disintegrin and metalloprotease 17 (ADAM17) results in the occurrence of soluble (s) ACE2, which can no longer mediate SARS-Cov-2 entry, and which might even prevent such entry by keeping the virus in solution. Ang II, via its type 1 receptor (AT<sub>1</sub>R), upregulates ADAM17, and AT<sub>1</sub>R blockers (ARBs) would prevent this. Ibuprofen has been suggested to increase ACE2, possibly via inhibition of cyclooxygenases (COXs) and activation of Peroxisome Proliferator-Activated Receptor gamma (PPAR-γ). Redrawn after [<xref ref-type="bibr" rid="CR4">4</xref>]</p></caption><graphic xlink:href="10194_2020_1106_Fig1_HTML" id="MO1"></graphic></fig></p><p id="Par15">RAS blockers are currently widely used as off-label drugs in the prophylactic treatment of migraine [<xref ref-type="bibr" rid="CR5">5</xref>]. This mainly concerns the angiotensin-converting enzyme (ACE) inhibitors captopril and lisonopril and the angiotensin II type 1 receptor (AT1R) blocker (ARB) candesartan [<xref ref-type="bibr" rid="CR6">6</xref>]. Ibuprofen is also widely used in the treatment of migraine [<xref ref-type="bibr" rid="CR6">6</xref>], as well as in other types of headache or pain in general, because of its strong analgesic properties.</p><p id="Par16">Apart from the usual considerations, such as drug-drug interactions or gastrointestinal safety the NSAIDs [<xref ref-type="bibr" rid="CR7">7</xref>], in view of the suggested increased risk for COVID-19 infection by RAS inhibitors and ibuprofen, many clinicians now need to know what to advice their patients: continue treatment or not. The relation between RAS blockade and the COVID-19 pandemic in hypertensive patients has recently been discussed, and the advice was to continue RAS blocker treatment in such patients [<xref ref-type="bibr" rid="CR4">4</xref>]. In this short communication, we discuss this concern in relation to headache treatment. We conclude that, based on current evidence, there is no reason to abandon treatment of headache patients with RAS inhibitors or ibuprofen.</p></sec><sec id="Sec2"><title>Renin-angiotensin system (RAS) blockers and ACE2</title><p id="Par17">The renin-angiotensin system is pivotal in the regulation of blood pressure. One of its main components is ACE, which converts angiotensin I (Ang I) into angiotensin II (Ang II). Ang II exerts its hypertensive effects via AT<sub>1</sub>R activation. Apart from ACE, there are multiple other enzymes that metabolize angiotensin (the so-called “angiotensinases”), and one of these is the carboxypeptidase angiotensin-converting enzyme 2 (ACE2). ACE2 converts the octapeptide Ang II (=Ang-(1–8)) into Ang-(1–7), and the decapeptide Ang I (=Ang-(1–10)) into Ang-(1–9) (Fig. <xref rid="Fig1" ref-type="fig">1</xref>). Yet, it additionally hydrolyzes multiple other peptides beyond the angiotensins. It is important to note that ACE2 does not convert Ang I into Ang II, and that its activity is not blocked by ACE inhibitors. This is not surprising, since ACE2 and ACE are different enzymes, and ACE inhibitors have been designed specifically for ACE only. ACE2 is a membrane-bound enzyme, with very low (soluble) levels in blood [<xref ref-type="bibr" rid="CR8">8</xref>, <xref ref-type="bibr" rid="CR9">9</xref>]. The occurrence of sACE2 depends on cleavage of its membrane-anchor by A Disintegrin And Metalloprotease 17 (ADAM17) (Fig. <xref rid="Fig1" ref-type="fig">1</xref>). Interestingly, Ang II upregulates ADAM17. Yet, given that the vast majority of ACE2 is membrane-bound, fluctuations in the percentage of sACE by pathological conditions or drug use are unlikely to have major effects on the amount of membrane-bound ACE2. Obviously, SARS-CoV-2 entry relies exclusively on membrane-bound ACE2. sACE2 cannot mediate such entry, and, if anything, might even prevent it by keeping the virus in solution.</p><p id="Par18">The concern related to the use of RAS blockers in COVID-19 patients is based on the idea that these drugs upregulate ACE2. Indeed, animal studies support such ACE2 upregulation after ARB treatment [<xref ref-type="bibr" rid="CR10">10</xref>–<xref ref-type="bibr" rid="CR12">12</xref>]. However, this generally required high doses, while effects differed per organ and per ARB. If true, this phenomenon should also be observed for ACE inhibitors. Yet, this has hardly been studied. Most importantly, we do not know whether the increase concerned membrane-bound ACE2 in pulmonary cells (relevant in SARS patients), nor whether a rise in membrane-bound ACE2, if occurring, truly facilitates virus entry. We do know that stopping RAS blocker treatment, particular in cardiovascular patients, has major serious consequences, including an increase in mortality.</p><p id="Par19">Migraine patients using RAS blockers for the prevention of migraine often additionally suffer from hypertension. Normalizing increased blood pressure protects against cardiovascular disease, while migraine, especially in women, is associated with an increased cardiovascular risk [<xref ref-type="bibr" rid="CR13">13</xref>]. Hence, suddenly aborting preventive treatment with RAS blockers is likely to impose an increased cardiovascular risk in migraine patients, similar to that in hypertensive patients.</p></sec><sec id="Sec3"><title>Ibuprofen and ACE2</title><p id="Par20">Like RAS inhibitors, ibuprofen has been suggested to increase ACE2 [<xref ref-type="bibr" rid="CR14">14</xref>]. This conclusion is based on a study in diabetic rats exposed to one high dose of ibuprofen (40 mg/kg, corresponding with almost 3 g in a human being of 70 k). The increase in ACE2 was shown in the heart only, and no distinction was made between membrane-bound ACE2 and sACE2. Without providing evidence, the authors speculated that the ACE2 rise was due to inhibition of cyclo-oxygenase and/or activation of peroxisome proliferator-activated receptor γ [<xref ref-type="bibr" rid="CR14">14</xref>]. Clearly, this is an exceptionally weak basis to draw a far-reaching conclusion on the use of ibuprofen in headache patients during the COVID-19 pandemic. Irrespective of this observation, we stress that paracetamol (acetaminophen) should be used as a first choice in headache treatment before starting with NSAIDs, given its better tolerability.</p></sec><sec id="Sec4"><title>Conclusion</title><p id="Par21">Summarizing, there is no convincing evidence that either RAS blockers or ibuprofen facilitate or worsen SARS-CoV-2 infection in any type of patient, including headache patients. In agreement with the advice of the main cardiovascular societies (American Heart Association, <ext-link ext-link-type="uri" xlink:href="https://newsroom.heart.org/news/patients-taking-ace-i-and-arbs-who-contract-covid-19-should-continue-treatment-unless-otherwise-advised-by-their-physician">https://newsroom.heart.org/news/patients-taking-ace-i-and-arbs-who-contract-covid-19-should-continue-treatment-unless-otherwise-advised-by-their-physician</ext-link>, European Society of Hypertension, <ext-link ext-link-type="uri" xlink:href="https://www.eshonline.org/spotlights/esh-stabtement-on-covid-19/">https://www.eshonline.org/spotlights/esh-stabtement-on-covid-19/</ext-link>, International Society of Hypertension, <ext-link ext-link-type="uri" xlink:href="https://ish-world.com/news/a/A-statement-from-the-International-Society-of-Hypertension-on-COVID-19/">https://ish-world.com/news/a/A-statement-from-the-International-Society-of-Hypertension-on-COVID-19/</ext-link>), the World Health Organization (<ext-link ext-link-type="uri" xlink:href="https://twitter.com/WHO/status/1240409217997189128">https://twitter.com/WHO/status/1240409217997189128</ext-link>) and European Medicines Agency (<ext-link ext-link-type="uri" xlink:href="https://www.ema.europa.eu/en/news/ema-gives-advice-use-non-steroidal-anti-inflammatories-covid-19">https://www.ema.europa.eu/en/news/ema-gives-advice-use-non-steroidal-anti-inflammatories-covid-19</ext-link>), we see no rationale to panic and to alter the prescription of these drugs that have an important role in the treatment of headache.</p></sec></body><back><glossary><title>Abbreviations</title><def-list><def-item><term>ACE</term><def><p id="Par2">Angiotensin-Converting Enzyme</p></def></def-item><def-item><term>ADAM17</term><def><p id="Par3">A Disintegrin And Metalloprotease 17</p></def></def-item><def-item><term>Ang I</term><def><p id="Par4">Angiotensin I</p></def></def-item><def-item><term>Ang II</term><def><p id="Par5">Angiotensin II</p></def></def-item><def-item><term>ARB</term><def><p id="Par6">Angiotensin II type 1 receptor blocker</p></def></def-item><def-item><term>AT<sub>1</sub>R</term><def><p id="Par7">Angiotensin II type 1 receptor</p></def></def-item><def-item><term>COVID-19</term><def><p id="Par8">Corona Virus Disease 2019</p></def></def-item><def-item><term>NSAID</term><def><p id="Par9">Non-Steroid Anti-Inflammatory Drug</p></def></def-item><def-item><term>RAS</term><def><p id="Par10">Renin-Angiotensin-System</p></def></def-item><def-item><term>SARS</term><def><p id="Par11">Severe acute respiratory syndrome</p></def></def-item><def-item><term>SARS-CoV-2</term><def><p id="Par12">Severe acute respiratory syndrome coronavirus-2</p></def></def-item><def-item><term>TMPRSS2</term><def><p id="Par13">Serine protease transmembrane protease, serine 2</p></def></def-item></def-list></glossary><fn-group><fn><p><bold>Publisher’s Note</bold></p><p>Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.</p></fn></fn-group><ack><title>Acknowledgements</title><p>The authors wish to thank Estrellita Uijl for her help in preparing the Figure.</p></ack><notes notes-type="author-contribution"><title>Authors’ contributions</title><p>All authors contributed to this manuscript, which reflects our common opinion. The author(s) read and approved the final manuscript.</p></notes><notes notes-type="funding-information"><title>Funding</title><p>Dr. Maassen van den Brink is funded by the Dutch Research Council (NWO, Vici grant 09150181910040).</p></notes><notes notes-type="data-availability"><title>Availability of data and materials</title><p>NA</p></notes><notes><title>Ethics approval and consent to participate</title><p id="Par22">NA</p></notes><notes><title>Consent for publication</title><p id="Par23">All authors have seen and approved the final version of this manuscript.</p></notes><notes notes-type="COI-statement"><title>Competing interests</title><p id="Par24">NA</p></notes><ref-list id="Bib1"><title>References</title><ref id="CR1"><label>1.</label><mixed-citation publication-type="other">Panati K, Narala VR (2020) COVID-19 outbreak: an update on therapeutic options. 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