Case report
Mesalamine-induced myocarditis following diagnosis of Crohn's disease: A case report
Miocardite induzida pela mesalamina após o diagnóstico de doença de Crohn – relato de um caso clínico
Carlos Galvão Braga
, Juliana Martins, Carina Arantes, Vítor Ramos, Catarina Vieira, Alberto Salgado, Sónia Magalhães, Adelino Correia
Corresponding author
Serviço de Cardiologia, Hospital de Braga, Braga, Portugal
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disease: A case report" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "717" "paginaFinal" => "720" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Carlos Galvão Braga, Juliana Martins, Carina Arantes, Vítor Ramos, Catarina Vieira, Alberto Salgado, Sónia Magalhães, Adelino Correia" "autores" => array:8 [ 0 => array:4 [ "nombre" => "Carlos" "apellidos" => "Galvão Braga" "email" => array:1 [ 0 => "carlos.galvaobraga@gmail.com" ] "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">¿</span>" "identificador" => "cor0005" ] ] ] 1 => array:2 [ "nombre" => "Juliana" "apellidos" => "Martins" ] 2 => array:2 [ "nombre" => "Carina" "apellidos" => "Arantes" ] 3 => array:2 [ "nombre" => "Vítor" "apellidos" => "Ramos" ] 4 => array:2 [ "nombre" => "Catarina" "apellidos" => "Vieira" ] 5 => array:2 [ "nombre" => "Alberto" "apellidos" => "Salgado" ] 6 => array:2 [ "nombre" => "Sónia" "apellidos" => "Magalhães" ] 7 => array:2 [ "nombre" => "Adelino" "apellidos" => "Correia" ] ] "afiliaciones" => array:1 [ 0 => array:2 [ "entidad" => "Serviço de Cardiologia, Hospital de Braga, Braga, Portugal" "identificador" => "aff0005" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "pt" => array:1 [ "titulo" => "Miocardite induzida pela mesalamina após o diagnóstico de doença de Crohn – relato de um caso clínico" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 1016 "Ancho" => 2334 "Tamanyo" => 201776 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Echocardiogram in parasternal short-axis view showing moderately depressed left ventricular systolic function (ejection fraction of 38%), with global hypocontractility, although more obvious in the posterior, inferior and lateral walls (A – diastole; B – systole).</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Mesalamine (5-aminosalicylic acid) is a well-known treatment for inflammatory bowel disease, often used as the first-line drug. Although rare, adverse cardiac reactions due to mesalamine have been described in the literature, and include pericarditis, myocarditis, coronary vasculitis and left ventricular dysfunction.<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1–4</span></a> We report a case of mesalamine-induced myocarditis in a patient with a recent diagnosis of Crohn's disease.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Case report</span><p id="par0010" class="elsevierStylePara elsevierViewall">A 19-year-old male with no relevant medical history, besides having been diagnosed two weeks previously with Crohn's disease for which he was medicated with mesalamine 1500 mg twice a day and budesonide 9 mg daily, was admitted to the local hospital with retrosternal chest pain radiating to the left arm. He reported no accompanying symptoms and no relieving or aggravating factors were identified. The patient had no reported previous infection. The physical examination was unremarkable and there were no signs of hemodynamic instability or heart failure. The initial 12-lead electrocardiogram revealed sinus rhythm and slight ST-segment elevation with upward concavity in leads I, II, III, aVF and V3–V6 (<a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>). As laboratory tests showed elevated cardiac necrosis biomarkers (troponin I 9.1 ng/ml), he was transferred to our hospital for cardiological evaluation. Following admission to the cardiac care unit, he mentioned some episodes of chest pain which improved after treatment with aspirin. Repeated blood tests demonstrated a further increase in cardiac biomarkers (peak troponin I 27.3 ng/ml and peak total CK 915 IU/l) accompanied by elevation of NT-proBNP (6413 pg/ml) and inflammatory parameters (C-reactive protein 130 mg/l, 15<span class="elsevierStyleHsp" style=""></span>800 leukocytes). Remodeling therapy with ACE inhibitors and beta-blockers was also introduced, due to the moderately depressed left ventricular systolic function (ejection fraction of 38%) seen on the transthoracic echocardiogram, with global hypocontractility, although more noticeable in the posterior, inferior and lateral walls (<a class="elsevierStyleCrossRef" href="#fig0010">Figure 2</a>). Cardiac magnetic resonance imaging (MRI) with delayed gadolinium enhancement revealed multiple areas of myocardial fibrosis, mainly subepicardial, suggesting a non-ischemic pattern (<a class="elsevierStyleCrossRef" href="#fig0015">Figure 3</a>). There was no sign of myocardial infarction and the patient was therefore diagnosed with acute myocarditis.</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia><elsevierMultimedia ident="fig0015"></elsevierMultimedia><p id="par0015" class="elsevierStylePara elsevierViewall">In view of mesalamine's cardiovascular toxicity as described in the literature, this drug was discontinued shortly after admission. The patient remained asymptomatic thereafter and laboratory tests were favorable (NT-proBNP 905 pg/ml and troponin I 0.13 ng/ml at discharge). Electrocardiograms showed progressive resolution of ST-segment elevation and the echocardiogram was repeated one week later, demonstrating improvement in left ventricular systolic function (ejection fraction of 45%).</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Discussion</span><p id="par0020" class="elsevierStylePara elsevierViewall">Classic myocarditis refers to inflammation of the heart muscle as a result of exposure to either discrete external antigen triggers, such as viruses, bacteria, parasites or drugs, or to internal triggers such as autoimmune activation against self-antigens. Drugs can act as a direct toxic agent (anthracyclines and cocaine) or by a hypersensitivity reaction, as is thought to be the case with mesalamine and other medications (clozapine, sulfonamides, cephalosporins, penicillins and tricyclic antidepressants).<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">Cardiac disease can be associated with Crohn's disease as an extraintestinal manifestation of inflammatory bowel disease or as a consequence of drug-induced side effects.<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1–4</span></a> Myocarditis associated with mesalamine is a rare but potentially serious phenomenon, generally occurring 2–4 weeks after the initial exposure to the drug, although presentation may be delayed over years, especially if steroids are used concomitantly.<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> Mesalamine's mechanism of action is not fully understood, but it includes inhibition of the cyclooxygenase pathway, inducing an anti-inflammatory effect in the colon. The exact mechanism for mesalamine-induced myocardial inflammation is not clearly identified, but it is thought to be a hypersensitivity reaction rather than a cytotoxic effect.<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1,2</span></a> One proposed mechanism is humoral-mediated hypersensitivity, in which antibodies formed against mesalamine cross-react with cardiac tissue causing inflammation.<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> The diagnosis of hypersensitivity myocarditis is supported by two facts: inflammation worsens if mesalamine is reintroduced during the acute phase,<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> and resolution of symptoms occurs within one week after drug discontinuation, as has been described in all reported cases.<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1–4</span></a> Eosinophilic infiltration of the myocardium on endomyocardial biopsy has also been described,<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> which seems to confirm the link between mesalamine and hypersensitivity myocarditis.</p><p id="par0030" class="elsevierStylePara elsevierViewall">In our case, the onset and resolution of symptoms were similar to those reported in the literature. Soon after discontinuing mesalamine, our patient evolved well, with progressive falls in cardiac biomarkers and improvement in left ventricular systolic function. Considering this evolution and the fact that there was no previous infection, mesalamine-induced myocarditis was considered to be the most likely diagnosis.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Conclusion</span><p id="par0035" class="elsevierStylePara elsevierViewall">This case illustrates the importance of eliciting a thorough medical history and being aware of the timing when new medications are started. It is imperative that any new onset of chest pain in the setting of inflammatory bowel disease treated with mesalamine should be evaluated via cardiac enzymes, electrocardiogram, echocardiogram and possibly cardiac MRI to rapidly diagnose any complication caused by either the inflammatory bowel disease itself or an adverse drug reaction.</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Ethical disclosures</span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Protection of human and animal subjects</span><p id="par0040" class="elsevierStylePara elsevierViewall">The authors declare that no experiments were performed on humans or animals for this investigation.</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Confidentiality of data</span><p id="par0045" class="elsevierStylePara elsevierViewall">The authors declare that they have followed the protocols of their work center on the publication of patient data and that all the patients included in the study received sufficient information and gave their written informed consent to participate in the study.</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Right to privacy and informed consent</span><p id="par0050" class="elsevierStylePara elsevierViewall">The authors have obtained the written informed consent of the patients or subjects mentioned in the article. The corresponding author is in possession of this document.</p></span></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Conflict of interests</span><p id="par0055" class="elsevierStylePara elsevierViewall">The authors have no conflict of interests to declare.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:11 [ 0 => array:2 [ "identificador" => "xres296952" "titulo" => "Abstract" ] 1 => array:2 [ "identificador" => "xpalclavsec280618" "titulo" => "Keywords" ] 2 => array:2 [ "identificador" => "xres296953" "titulo" => "Resumo" ] 3 => array:2 [ "identificador" => "xpalclavsec280617" "titulo" => "Palavras-chave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:2 [ "identificador" => "sec0010" "titulo" => "Case report" ] 6 => array:2 [ "identificador" => "sec0015" "titulo" => "Discussion" ] 7 => array:2 [ "identificador" => "sec0020" "titulo" => "Conclusion" ] 8 => array:3 [ "identificador" => "sec0025" "titulo" => "Ethical disclosures" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0030" "titulo" => "Protection of human and animal subjects" ] 1 => array:2 [ "identificador" => "sec0035" "titulo" => "Confidentiality of data" ] 2 => array:2 [ "identificador" => "sec0040" "titulo" => "Right to privacy and informed consent" ] ] ] 9 => array:2 [ "identificador" => "sec0045" "titulo" => "Conflict of interests" ] 10 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2012-12-01" "fechaAceptado" => "2012-12-07" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec280618" "palabras" => array:4 [ 0 => "Myocarditis" 1 => "Mesalamine" 2 => "Transthoracic echocardiography" 3 => "Cardiac magnetic resonance imaging" ] ] ] "pt" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palavras-chave" "identificador" => "xpalclavsec280617" "palabras" => array:4 [ 0 => "Miocardite" 1 => "Mesalamina" 2 => "Ecocardiografia transtorácica" 3 => "Ressonância magnética cardíaca" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Mesalamine is a common treatment for Crohn's disease, and can be rarely associated with myocarditis through a mechanism of drug hypersensitivity. We present the case of a 19-year-old male who developed chest pain two weeks after beginning mesalamine therapy. The electrocardiogram showed slight ST-segment elevation with upward concavity in the inferolateral leads; blood tests demonstrated elevated troponin I and the echocardiogram revealed moderately depressed left ventricular systolic function with global hypocontractility. Cardiac magnetic resonance imaging confirmed the diagnosis of myocarditis, revealing multiple areas of subepicardial fibrosis. The onset of symptoms after mesalamine, and improvement of chest pain, cardiac biomarkers and left ventricular systolic function after discontinuing the drug, suggest that our patient suffered from a rare drug-hypersensitivity reaction to mesalamine.</p>" ] "pt" => array:2 [ "titulo" => "Resumo" "resumen" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">A mesalamina é um tratamento comum para a doença de Crohn, associando-se de forma rara à miocardite aguda, através de uma reação de hipersensibilidade ao fármaco. Os autores apresentam o caso clínico de um jovem de 19 anos com aparecimento de dor torácica duas semanas após ter iniciado tratamento com mesalamina para a doença de Crohn. O eletrocardiograma mostrou um discreto supradesnivelamento do segmento ST, de concavidade ascendente, nas derivações infero-laterais; as análises revelaram elevação da troponina I e o ecocardiograma exibiu uma depressão moderada da função sistólica do ventrículo esquerdo, por hipocontractilidade global. A ressonância magnética cardíaca confirmou o diagnóstico de miocardite, evidenciando múltiplas áreas de fibrose subepicárdica. O início dos sintomas após o começo da mesalamina e a melhoria da dor torácica, biomarcadores cardíacos e função sistólica ventricular esquerda após a suspensão do medicamento, sugerem que o nosso paciente teve uma reação rara de hipersensibilidade à mesalamina.</p>" ] ] "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as: Galvão Braga C, Martins J, Arantes C, Ramos V, Vieira C, Salgado A, et al. Miocardite induzida pela mesalamina após o diagnóstico de doença de Crohn – relato de um caso clínico 2012. http://dx.doi.org/.</p>" ] ] "multimedia" => array:3 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1524 "Ancho" => 3170 "Tamanyo" => 1091780 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Electrocardiogram on day of chest pain onset: sinus rhythm and slight ST-segment elevation with upward concavity in leads I, II, III, aVF and V3–V6.</p>" ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 1016 "Ancho" => 2334 "Tamanyo" => 201776 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Echocardiogram in parasternal short-axis view showing moderately depressed left ventricular systolic function (ejection fraction of 38%), with global hypocontractility, although more obvious in the posterior, inferior and lateral walls (A – diastole; B – systole).</p>" ] ] 2 => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 948 "Ancho" => 2334 "Tamanyo" => 194677 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Cardiac magnetic resonance imaging with myocardial suppression after contrast. Late gadolinium enhancement reveals multiple areas of subepicardial myocardial fibrosis, mainly in the inferior and lateral walls, in short-axis (A) and 4-chamber views (B).</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:7 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Mesalamine-induced myocarditis and coronary vasculitis in a pediatric ulcerative colitis patient: a case report" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:3 [ 0 => "E. Perez-Colon" 1 => "G.H. Dadlani" 2 => "I. 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 7 | 7 | 14 |
| 2024 October | 66 | 31 | 97 |
| 2024 September | 70 | 39 | 109 |
| 2024 August | 52 | 38 | 90 |
| 2024 July | 29 | 33 | 62 |
| 2024 June | 41 | 34 | 75 |
| 2024 May | 39 | 18 | 57 |
| 2024 April | 29 | 38 | 67 |
| 2024 March | 27 | 17 | 44 |
| 2024 February | 25 | 23 | 48 |
| 2024 January | 26 | 24 | 50 |
| 2023 December | 24 | 24 | 48 |
| 2023 November | 39 | 23 | 62 |
| 2023 October | 27 | 19 | 46 |
| 2023 September | 30 | 18 | 48 |
| 2023 August | 31 | 23 | 54 |
| 2023 July | 18 | 11 | 29 |
| 2023 June | 29 | 10 | 39 |
| 2023 May | 32 | 34 | 66 |
| 2023 April | 23 | 4 | 27 |
| 2023 March | 34 | 20 | 54 |
| 2023 February | 27 | 23 | 50 |
| 2023 January | 22 | 23 | 45 |
| 2022 December | 33 | 25 | 58 |
| 2022 November | 41 | 24 | 65 |
| 2022 October | 30 | 21 | 51 |
| 2022 September | 19 | 30 | 49 |
| 2022 August | 35 | 31 | 66 |
| 2022 July | 27 | 24 | 51 |
| 2022 June | 28 | 21 | 49 |
| 2022 May | 31 | 35 | 66 |
| 2022 April | 27 | 20 | 47 |
| 2022 March | 26 | 31 | 57 |
| 2022 February | 25 | 20 | 45 |
| 2022 January | 22 | 24 | 46 |
| 2021 December | 23 | 29 | 52 |
| 2021 November | 37 | 37 | 74 |
| 2021 October | 81 | 39 | 120 |
| 2021 September | 48 | 22 | 70 |
| 2021 August | 41 | 24 | 65 |
| 2021 July | 23 | 24 | 47 |
| 2021 June | 33 | 20 | 53 |
| 2021 May | 27 | 36 | 63 |
| 2021 April | 43 | 37 | 80 |
| 2021 March | 58 | 10 | 68 |
| 2021 February | 56 | 16 | 72 |
| 2021 January | 31 | 7 | 38 |
| 2020 December | 31 | 7 | 38 |
| 2020 November | 27 | 8 | 35 |
| 2020 October | 13 | 11 | 24 |
| 2020 September | 60 | 8 | 68 |
| 2020 August | 31 | 13 | 44 |
| 2020 July | 37 | 6 | 43 |
| 2020 June | 47 | 9 | 56 |
| 2020 May | 57 | 4 | 61 |
| 2020 April | 38 | 12 | 50 |
| 2020 March | 58 | 10 | 68 |
| 2020 February | 118 | 12 | 130 |
| 2020 January | 51 | 7 | 58 |
| 2019 December | 61 | 8 | 69 |
| 2019 November | 58 | 3 | 61 |
| 2019 October | 91 | 16 | 107 |
| 2019 September | 71 | 14 | 85 |
| 2019 August | 41 | 5 | 46 |
| 2019 July | 64 | 9 | 73 |
| 2019 June | 36 | 9 | 45 |
| 2019 May | 62 | 12 | 74 |
| 2019 April | 44 | 17 | 61 |
| 2019 March | 133 | 9 | 142 |
| 2019 February | 111 | 16 | 127 |
| 2019 January | 114 | 7 | 121 |
| 2018 December | 114 | 21 | 135 |
| 2018 November | 56 | 5 | 61 |
| 2018 October | 116 | 24 | 140 |
| 2018 September | 66 | 14 | 80 |
| 2018 August | 51 | 5 | 56 |
| 2018 July | 35 | 3 | 38 |
| 2018 June | 45 | 7 | 52 |
| 2018 May | 56 | 6 | 62 |
| 2018 April | 48 | 6 | 54 |
| 2018 March | 66 | 6 | 72 |
| 2018 February | 49 | 8 | 57 |
| 2018 January | 42 | 3 | 45 |
| 2017 December | 86 | 9 | 95 |
| 2017 November | 36 | 9 | 45 |
| 2017 October | 41 | 6 | 47 |
| 2017 September | 46 | 4 | 50 |
| 2017 August | 48 | 10 | 58 |
| 2017 July | 43 | 6 | 49 |
| 2017 June | 71 | 7 | 78 |
| 2017 May | 48 | 3 | 51 |
| 2017 April | 35 | 3 | 38 |
| 2017 March | 37 | 54 | 91 |
| 2017 February | 44 | 8 | 52 |
| 2017 January | 49 | 3 | 52 |
| 2016 December | 45 | 6 | 51 |
| 2016 November | 40 | 2 | 42 |
| 2016 October | 42 | 4 | 46 |
| 2016 September | 42 | 13 | 55 |
| 2016 August | 12 | 1 | 13 |
| 2016 July | 17 | 6 | 23 |
| 2016 June | 13 | 3 | 16 |
| 2016 May | 16 | 5 | 21 |
| 2016 April | 13 | 2 | 15 |
| 2016 March | 43 | 7 | 50 |
| 2016 February | 42 | 13 | 55 |
| 2016 January | 33 | 3 | 36 |
| 2015 December | 28 | 4 | 32 |
| 2015 November | 34 | 8 | 42 |
| 2015 October | 29 | 7 | 36 |
| 2015 September | 21 | 6 | 27 |
| 2015 August | 29 | 10 | 39 |
| 2015 July | 19 | 8 | 27 |
| 2015 June | 10 | 1 | 11 |
| 2015 May | 19 | 5 | 24 |
| 2015 April | 16 | 5 | 21 |
| 2015 March | 23 | 2 | 25 |
| 2015 February | 24 | 2 | 26 |
| 2015 January | 22 | 7 | 29 |
| 2014 December | 28 | 8 | 36 |
| 2014 November | 18 | 2 | 20 |
| 2014 October | 27 | 5 | 32 |
| 2014 September | 24 | 4 | 28 |
| 2014 August | 31 | 4 | 35 |
| 2014 July | 30 | 10 | 40 |
| 2014 June | 16 | 3 | 19 |
| 2014 May | 38 | 5 | 43 |
| 2014 April | 24 | 2 | 26 |
| 2014 March | 39 | 15 | 54 |
| 2014 February | 47 | 8 | 55 |
| 2014 January | 41 | 12 | 53 |
| 2013 December | 29 | 9 | 38 |
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