Case report
Primary cardiac lymphoma in a patient with concomitant renal cancerPrimary cardiac lymphoma in a patient with concomitant renal cancer
Linfoma primário do coração em doente com neoplasia renal síncrona
Davide Severino
, Beatriz Santos, Cátia Costa, David Durão, Miguel Alves, Isabel Monteiro, Luz Pitta, Margarida Leal
Corresponding author
Serviço de Cardiologia, Hospital de Santarém, Santarém, Portugal
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"paginaFinal" => "773.e5" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Davide Severino, Beatriz Santos, Cátia Costa, David Durão, Miguel Alves, Isabel Monteiro, Luz Pitta, Margarida Leal" "autores" => array:8 [ 0 => array:4 [ "nombre" => "Davide" "apellidos" => "Severino" "email" => array:1 [ 0 => "davideseverino8@gmail.com" ] "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0005" ] ] ] 1 => array:2 [ "nombre" => "Beatriz" "apellidos" => "Santos" ] 2 => array:2 [ "nombre" => "Cátia" "apellidos" => "Costa" ] 3 => array:2 [ "nombre" => "David" "apellidos" => "Durão" ] 4 => array:2 [ "nombre" => "Miguel" "apellidos" => "Alves" ] 5 => array:2 [ "nombre" => "Isabel" "apellidos" => "Monteiro" ] 6 => array:2 [ "nombre" => "Luz" "apellidos" => "Pitta" ] 7 => array:2 [ "nombre" => "Margarida" "apellidos" => "Leal" ] ] "afiliaciones" => array:1 [ 0 => array:2 [ "entidad" => "Serviço de Cardiologia, Hospital de Santarém, Santarém, Portugal" "identificador" => "aff0005" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "pt" => array:1 [ "titulo" => "Linfoma primário do coração em doente com neoplasia renal síncrona" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 2752 "Ancho" => 2500 "Tamanyo" => 393484 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Thoracic-abdominal-pelvic computed tomography showing a lesion with contrast uptake at the level of the right atrium (A) and a solid, nodular lesion in the right kidney (B).</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Non-Hodgkin lymphoma (NHL) is associated with a higher incidence of other cancers, both solid tumors and other blood cancers. Studies by Travis et al.<a class="elsevierStyleCrossRefs" href="#bib0110"><span class="elsevierStyleSup">1,2</span></a> showed a high probability of a second cancer in NHL patients, increasing over time. The incidence of renal cell carcinoma (RCC) appears to be particularly high in these patients, with a reported observed-to-expected ratio of 1.47–2.07.<a class="elsevierStyleCrossRefs" href="#bib0110"><span class="elsevierStyleSup">1,2</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">The explanations initially proposed for this association were the late effects of chemotherapy and radiation therapy used in cancer treatment or immunosuppression caused by the disease itself. While this may be true of certain cancers such as leukemia and bladder cancers, which are frequently associated with previous use of alkylating agents, it does not explain why some of these cancers precede lymphoma or develop in patients who have not undergone treatment with these agents.<a class="elsevierStyleCrossRefs" href="#bib0110"><span class="elsevierStyleSup">1,2</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">However, other studies have found a higher than expected incidence of RCC in NHL patients based on the incidence of each disease in the general population. A study by Anderson et al.<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">3</span></a> found concomitant RCC and NHL in 41 patients. The data from this study showed that NHL patients have a relative risk of 1.86 of developing RCC, while RCC patients have a relative risk of 2.67 of developing NHL, similarly to other studies.<a class="elsevierStyleCrossRefs" href="#bib0120"><span class="elsevierStyleSup">3–5</span></a> We present a case report of primary cardiac lymphoma in a patient with concomitant RCC, which highlights the importance of this association.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Case report</span><p id="par0020" class="elsevierStylePara elsevierViewall">A 67-year-old man, white, with a history of hypertension and dyslipidemia, went to the emergency department due to increasing fatigue over the previous two weeks, epigastric discomfort radiating to the retrosternal region, and weight loss (around 3 kg in two weeks). He denied fever, cough, expectoration, dyspnea or limb edema. On physical examination, he was hemodynamically stable and apyretic but became short of breath on minimal exertion (28 cpm). Heart sounds were muffled but there was no peripheral edema. The electrocardiogram (ECG) showed sinus tachycardia with low voltage QRS in the limb leads (<a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a>). Laboratory tests revealed slightly elevated creatinine (1.5 mg/dl) and markedly elevated BNP (3462 pg/dl), no increase in inflammatory markers (leukocytes 4.9×10<span class="elsevierStyleSup">9</span>/l and C-reactive protein 3.9 mg/dl), hemoglobin 13.9 g/dl, and negative markers of myocardial necrosis. The echocardiogram showed a large circumferential pericardial effusion and an oval, heterogeneous mass at the level of the right atrioventricular groove, together with thickening of the right ventricular free wall (<a class="elsevierStyleCrossRef" href="#fig0010">Figure 2</a>).</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0025" class="elsevierStylePara elsevierViewall">Thoracic-abdominal-pelvic computed tomography (CT) was performed to characterize the pericardial effusion and cardiac mass and to exclude associated cancer. This confirmed a lesion with contrast uptake in the vicinity of the right atrium (<a class="elsevierStyleCrossRef" href="#fig0015">Figure 3</a>A), together with a solid, nodular lesion in the right kidney suggestive of RCC (<a class="elsevierStyleCrossRef" href="#fig0015">Figure 3</a>B). Cardiac and abdominal magnetic resonance imaging (MRI) was also performed, which was inconclusive as to whether the cardiac lesion was primary or secondary but which confirmed the suspicion of primary renal cancer.</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><p id="par0030" class="elsevierStylePara elsevierViewall">The patient underwent right nephrectomy and anatomopathological study confirmed that the kidney lesion was conventional RCC, Fuhrman grade 2, with no evidence of extrarenal involvement.</p><p id="par0035" class="elsevierStylePara elsevierViewall">Given the discrepancy between the absence of local involvement of the kidney lesion and the presence of a cardiac mass that could be a secondary lesion, it was decided to refer the patient for heart biopsy; the result of anatomopathological study was consistent with diffuse CD20+ large B cell NHL.</p><p id="par0040" class="elsevierStylePara elsevierViewall">Following confirmation of the diagnosis, the patient was referred to the hematology clinic, where he began chemotherapy, with partial clinical response and stabilization of the disease after the second treatment cycle.</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Discussion</span><p id="par0045" class="elsevierStylePara elsevierViewall">Primary cardiac lymphoma is defined as NHL involving the heart and/or the pericardium. In contrast to cardiac involvement in diffuse NHL, which occurs in up to 20% of patients, primary cardiac lymphoma is a rare entity, accounting for 1.3% of all primary cardiac tumors and 0.5% of all extranodal lymphomas.<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">6</span></a></p><p id="par0050" class="elsevierStylePara elsevierViewall">There is no pathognomonic clinical presentation, symptoms depending on the site of the cancer. Primary cardiac lymphoma primarily affects the right heart and in particular the right atrium, as was the case in our patient.<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">6</span></a></p><p id="par0055" class="elsevierStylePara elsevierViewall">The ECG in most cases, including the one presented, shows nonspecific alterations in ventricular repolarization and low voltage QRS complexes, the most common arrhythmia being complete atrioventricular block.<a class="elsevierStyleCrossRefs" href="#bib0140"><span class="elsevierStyleSup">7,8</span></a></p><p id="par0060" class="elsevierStylePara elsevierViewall">Transthoracic echocardiography is the first-line diagnostic exam as it provides the best images of the right heart, while newer imaging techniques such as CT and MRI are increasingly used to assess these patients due to their excellent spatial resolution.<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">7</span></a> As in the case presented, primary cardiac lymphoma tends to present as an isodense or hypodense image, with slow and heterogeneous contrast uptake.<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">9</span></a> Pericardial effusion and thickening are also frequent findings.<a class="elsevierStyleCrossRefs" href="#bib0150"><span class="elsevierStyleSup">9,10</span></a></p><p id="par0065" class="elsevierStylePara elsevierViewall">Approximately 45% of patients with RCC present with localized tumors, as in the case presented, while 30% may have metastases at the time of diagnosis.<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">11</span></a> Although the heart may be one of the organs affected, the most common metastatic sites are, in descending order, the lungs, bone, soft tissues, liver and central nervous system.<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">11</span></a></p><p id="par0070" class="elsevierStylePara elsevierViewall">Cardiac metastization of neoplasms is rare. A study of 266 cases of neoplasms involving the heart among 11<span class="elsevierStyleHsp" style=""></span>432 autopsies showed that only three originated from renal cancer.<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">12</span></a> When it does occur, it tends to present two distinct patterns: isolated involvement of the right heart, often through hematogenous dissemination via the inferior vena cava; or concomitant involvement of the left heart through a lymphatic pathway involving the carinal lymph nodes and parasternal lymph vessels.<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">13</span></a> Cardiac involvement in the absence of inferior vena cava thrombi is even rarer.<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">14</span></a> The combination of all these findings led us to request a biopsy of the cardiac mass, since there was a high probability of it being a different neoplasm.</p><p id="par0075" class="elsevierStylePara elsevierViewall">As previously mentioned, NHL patients appear to have a higher incidence of RCC. To date no specific mechanism has been established to explain this association, although a number of factors have been proposed, including previous therapy, immune dysfunction, genetic predisposition and environmental factors. Among the most widely discussed are immune dysfunction, a possible viral etiology and genetic predisposition.<a class="elsevierStyleCrossRefs" href="#bib0110"><span class="elsevierStyleSup">1,2</span></a></p><p id="par0080" class="elsevierStylePara elsevierViewall">According to the hypothesis of immune dysfunction, the immune dysregulation induced by the primary neoplasm predisposes the patient to a second cancer. A study by Yagisawa et al.<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">15</span></a> showed the presence of multiple immunological disorders (asthma, idiopathic thrombocytopenic purpura and mesangial proliferative glomerulonephritis) in a patient with NHL and RCC, suggesting an abnormal immunological mechanism. There is also a higher incidence of NHL in patients with melanoma, and the fact that melanoma and RCC respond to immunotherapy suggests immune dysfunction as a possible mechanism.<a class="elsevierStyleCrossRefs" href="#bib0120"><span class="elsevierStyleSup">3,16</span></a></p><p id="par0085" class="elsevierStylePara elsevierViewall">Certain viruses are now known to be potentially carcinogenic, notably Epstein-Barr virus and human T-lymphotropic virus type 1,<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">17</span></a> and a possible viral etiology for certain types of lymphoma has been reported in various studies. Etkind et al.<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">18</span></a> detected mouse mammary tumor virus-like DNA sequences in a T-cell lymphoma of a breast cancer patient who was simultaneously diagnosed with both diseases. Subsequent studies by the same group isolated similar viral sequences in lymphomas and breast cancer cells from patients with both diseases.<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">19</span></a> Basombrio et al.<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">20</span></a> obtained data in an animal model that were consistent with a common viral etiology between NHL and certain solid organ cancers.</p><p id="par0090" class="elsevierStylePara elsevierViewall">The available evidence shows common chromosome abnormalities between RCC and NHL, the most frequent being chromosome 17p deletions and p53 mutations. However, it has yet to be determined whether the same genes are involved in both cancers.<a class="elsevierStyleCrossRefs" href="#bib0205"><span class="elsevierStyleSup">21,22</span></a></p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Conclusion</span><p id="par0095" class="elsevierStylePara elsevierViewall">Primary tumors of the heart are rare. Many patients are asymptomatic or present only vague and nonspecific symptoms. Cardiac lymphomas are particularly rapid growing and have a poor short-term prognosis, so early detection is essential.</p><p id="par0100" class="elsevierStylePara elsevierViewall">There has been a steady increase in the number of cases reported of concomitant RCC and NHL, and the association appears to be multifactorial. Genetic predisposition, common immune diseases and environmental factors may all contribute to this association. However, further studies are required to clarify the common etiology of these two cancers.</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="par0105" 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="par0110" class="elsevierStylePara elsevierViewall">The authors declare that no patient data appear in this article.</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Right to privacy and informed consent</span><p id="par0115" class="elsevierStylePara elsevierViewall">The authors declare that no patient data appear in this article.</p></span></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Conflicts of interest</span><p id="par0120" class="elsevierStylePara elsevierViewall">The authors have no conflicts of interest to declare.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:11 [ 0 => array:3 [ "identificador" => "xres823915" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec820505" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres823914" "titulo" => "Resumo" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec820504" "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" => "Conflicts of interest" ] 10 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2015-02-25" "fechaAceptado" => "2015-03-21" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec820505" "palabras" => array:5 [ 0 => "Primary cardiac lymphoma" 1 => "Renal cancer" 2 => "Echocardiography" 3 => "Heart biopsy" 4 => "Pericardial effusion" ] ] ] "pt" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palavras-chave" "identificador" => "xpalclavsec820504" "palabras" => array:5 [ 0 => "Linfoma primário do coração" 1 => "Neoplasia renal" 2 => "Ecocardiografia" 3 => "Biópsia cardíaca" 4 => "Derrame pericárdico" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Primary cardiac lymphoma is defined as non-Hodgkin lymphoma involving the heart and/or pericardium. It is a rare cancer that primarily affects the right heart and in particular the right atrium. By contrast, renal cell carcinoma is a relatively common cancer, which in rare circumstances can metastasize to the heart. It is now known that there is an association between non-Hodgkin lymphoma and renal cell carcinoma, although the underlying mechanisms are not fully understood. The authors present a case of primary cardiac non-Hodgkin lymphoma in a patient with concomitant renal cell carcinoma and explore the possible reasons for this association.</p></span>" ] "pt" => array:2 [ "titulo" => "Resumo" "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">O linfoma primário do coração é definido como um linfoma não Hodgkin que envolve o coração e/ou o pericárdio. Trata-se de uma neoplasia rara que envolve principalmente as cavidades direitas e, em especial, a aurícula direita. Por sua vez, o carcinoma das células renais é uma neoplasia relativamente comum que, em situações mais raras, pode metastizar para o coração. Atualmente, é conhecida uma associação entre a ocorrência de linfomas não Hodgkin e de carcinomas das células renais, apesar dos mecanismos a ela subjacentes não serem claramente conhecidos. Com este artigo, os autores apresentam um caso de um linfoma não Hodgkin primário do coração num doente com uma neoplasia renal síncrona e exploram as bases admitidas para esta associação.</p></span>" ] ] "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as: Severino D, Santos B, Costa C, Durão D, Alves M, Monteiro I, et al. Linfoma primário do coração em doente com neoplasia renal síncrona. Rev Port Cardiol. 2015;34:773.</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" => 1896 "Ancho" => 3174 "Tamanyo" => 732275 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Admission electrocardiogram showing sinus tachycardia with low voltage in the limb leads and nonspecific alterations in ventricular repolarization.</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" => 1517 "Ancho" => 3038 "Tamanyo" => 310555 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Two-dimensional transthoracic echocardiography in subcostal view showing large circumferential pericardial effusion and an oval, heterogeneous mass measuring 54 mm×39 mm at the level of the right atrioventricular groove, together with thickening of the right ventricular free wall.</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" => 2752 "Ancho" => 2500 "Tamanyo" => 393484 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Thoracic-abdominal-pelvic computed tomography showing a lesion with contrast uptake at the level of the right atrium (A) and a solid, nodular lesion in the right kidney (B).</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:22 [ 0 => array:3 [ "identificador" => "bib0110" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Second cancers among long-term survivors of non-Hodgkin's lymphoma" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:3 [ 0 => "L.B. 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 7 | 3 | 10 |
| 2024 October | 35 | 36 | 71 |
| 2024 September | 48 | 29 | 77 |
| 2024 August | 45 | 33 | 78 |
| 2024 July | 37 | 30 | 67 |
| 2024 June | 32 | 25 | 57 |
| 2024 May | 42 | 18 | 60 |
| 2024 April | 38 | 27 | 65 |
| 2024 March | 35 | 18 | 53 |
| 2024 February | 36 | 29 | 65 |
| 2024 January | 24 | 22 | 46 |
| 2023 December | 29 | 31 | 60 |
| 2023 November | 37 | 17 | 54 |
| 2023 October | 24 | 12 | 36 |
| 2023 September | 28 | 20 | 48 |
| 2023 August | 24 | 19 | 43 |
| 2023 July | 22 | 14 | 36 |
| 2023 June | 24 | 17 | 41 |
| 2023 May | 34 | 24 | 58 |
| 2023 April | 21 | 15 | 36 |
| 2023 March | 32 | 29 | 61 |
| 2023 February | 26 | 23 | 49 |
| 2023 January | 25 | 25 | 50 |
| 2022 December | 28 | 28 | 56 |
| 2022 November | 35 | 11 | 46 |
| 2022 October | 33 | 24 | 57 |
| 2022 September | 28 | 48 | 76 |
| 2022 August | 22 | 46 | 68 |
| 2022 July | 27 | 35 | 62 |
| 2022 June | 20 | 21 | 41 |
| 2022 May | 24 | 28 | 52 |
| 2022 April | 28 | 27 | 55 |
| 2022 March | 25 | 36 | 61 |
| 2022 February | 24 | 13 | 37 |
| 2022 January | 24 | 22 | 46 |
| 2021 December | 24 | 27 | 51 |
| 2021 November | 22 | 34 | 56 |
| 2021 October | 21 | 45 | 66 |
| 2021 September | 20 | 28 | 48 |
| 2021 August | 19 | 36 | 55 |
| 2021 July | 17 | 30 | 47 |
| 2021 June | 19 | 20 | 39 |
| 2021 May | 20 | 31 | 51 |
| 2021 April | 80 | 27 | 107 |
| 2021 March | 42 | 24 | 66 |
| 2021 February | 54 | 15 | 69 |
| 2021 January | 24 | 23 | 47 |
| 2020 December | 38 | 13 | 51 |
| 2020 November | 25 | 17 | 42 |
| 2020 October | 33 | 15 | 48 |
| 2020 September | 49 | 13 | 62 |
| 2020 August | 19 | 14 | 33 |
| 2020 July | 45 | 9 | 54 |
| 2020 June | 46 | 6 | 52 |
| 2020 May | 41 | 5 | 46 |
| 2020 April | 54 | 16 | 70 |
| 2020 March | 37 | 8 | 45 |
| 2020 February | 61 | 31 | 92 |
| 2020 January | 27 | 8 | 35 |
| 2019 December | 32 | 5 | 37 |
| 2019 November | 32 | 11 | 43 |
| 2019 October | 22 | 2 | 24 |
| 2019 September | 46 | 10 | 56 |
| 2019 August | 30 | 5 | 35 |
| 2019 July | 43 | 16 | 59 |
| 2019 June | 35 | 8 | 43 |
| 2019 May | 28 | 12 | 40 |
| 2019 April | 33 | 22 | 55 |
| 2019 March | 167 | 11 | 178 |
| 2019 February | 122 | 8 | 130 |
| 2019 January | 118 | 7 | 125 |
| 2018 December | 125 | 10 | 135 |
| 2018 November | 153 | 13 | 166 |
| 2018 October | 241 | 14 | 255 |
| 2018 September | 50 | 15 | 65 |
| 2018 August | 37 | 9 | 46 |
| 2018 July | 35 | 7 | 42 |
| 2018 June | 57 | 12 | 69 |
| 2018 May | 62 | 7 | 69 |
| 2018 April | 59 | 4 | 63 |
| 2018 March | 106 | 11 | 117 |
| 2018 February | 28 | 5 | 33 |
| 2018 January | 48 | 6 | 54 |
| 2017 December | 66 | 8 | 74 |
| 2017 November | 36 | 8 | 44 |
| 2017 October | 37 | 16 | 53 |
| 2017 September | 23 | 4 | 27 |
| 2017 August | 34 | 13 | 47 |
| 2017 July | 30 | 9 | 39 |
| 2017 June | 37 | 17 | 54 |
| 2017 May | 39 | 7 | 46 |
| 2017 April | 38 | 10 | 48 |
| 2017 March | 38 | 6 | 44 |
| 2017 February | 38 | 6 | 44 |
| 2017 January | 30 | 8 | 38 |
| 2016 December | 27 | 13 | 40 |
| 2016 November | 17 | 4 | 21 |
| 2016 October | 37 | 8 | 45 |
| 2016 September | 19 | 3 | 22 |
| 2016 August | 18 | 1 | 19 |
| 2016 July | 8 | 9 | 17 |
| 2016 June | 8 | 7 | 15 |
| 2016 May | 16 | 3 | 19 |
| 2016 April | 29 | 2 | 31 |
| 2016 March | 26 | 19 | 45 |
| 2016 February | 48 | 35 | 83 |
| 2016 January | 101 | 40 | 141 |
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