Coeliac disease and membranous nephropathy
Enfermedad celíaca y nefropatía membranosa
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Soro, M.D. Sánchez de la Nieta, F. Rivera" "autores" => array:3 [ 0 => array:3 [ "Iniciales" => "S." "apellidos" => "Soro" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "affa" ] ] ] 1 => array:3 [ "Iniciales" => "M.D." "apellidos" => "Sánchez de la Nieta" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "affb" ] ] ] 2 => array:4 [ "Iniciales" => "F." "apellidos" => "Rivera" "email" => array:1 [ 0 => "friverahdez@senefro.org" ] "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "affb" ] ] ] ] "afiliaciones" => array:2 [ 0 => array:3 [ "entidad" => "Sección de Reumatología, Hospital General de Ciudad Real, Ciudad Real, Ciudad Real, España, " "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "affa" ] 1 => array:3 [ "entidad" => "Seccion de Nefrología, Hospital General de Ciudad Real, Ciudad Real, Ciudad Real, España, " "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "affb" ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Enfermedad celíaca y nefropatía membranosa" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig1" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "copyright" => "Elsevier España" "figura" => array:1 [ 0 => array:4 [ "imagen" => "41918078_f1_pag480.jpg" "Alto" => 320 "Ancho" => 398 "Tamanyo" => 15886 ] ] ] ] "textoCompleto" => "<p class="elsevierStylePara"><span class="elsevierStyleBold">INTRODUCTION</span></p><p class="elsevierStylePara">Coeliac disease (CD) is a relatively common entity with a prevalence in this country of 1:250 to 1:500, depending on which diagnostic criteria are employed.<span class="elsevierStyleSup">1</span> Genetic factors (HLA-DQ2 and/or DQ8 antigens) are involved in its pathogenesis, as well as environmental factors, and there are changes in humoral and cellular immunity responses to antigens contained in cereals (wheat, barley, rye and oats) which contain a protein called gluten. The peptides derived from gliadin (the alcohol-soluble fraction of gluten) possess many toxic components, which contain various antigens implicated in its pathogenesis.<span class="elsevierStyleSup">2</span> CD can appear at any age, with symptoms of malabsorption, which are more or less evident and may be associated with other autoimmune diseases. An increase in renal diseases,<span class="elsevierStyleSup">3</span> the most prominent of which are forms of glomerulonephritis, especially nephropathies with mesangial IgA deposits, has also been reported.<span class="elsevierStyleSup">4</span></p><p class="elsevierStylePara">We describe a case of classical CD, which appeared after the patient¿s first pregnancy and was associated with nephrotic proteinuria secondary to membranous nephropathy (MN). After receiving treatment based on conservative measures (ACEI, statins) and a gluten-free diet, there was an improvement in the patient¿s digestive symptoms, a disappearance of circulating IgA anti-tissue transglutaminase antibodies and a parallel decrease in proteinuria. We investigated the relationship between CD and MN, as well as the role of a gluten-free diet in its control</p><p class="elsevierStylePara"><span class="elsevierStyleBold">CASE REPORT</span></p><p class="elsevierStylePara">A female patient, aged 35 years, with no relevant medical history, presented symptoms, including abdominal pain, diarrhoea and constitutional syndrome, some weeks after giving birth to her first child; there were no complications during the pregnancy. The patient was examined in the Gastroenterology Department, where she was diagnosed with CD on the basis of the following diagnostic criteria: 1) high anti-transglutaminase antibody levels and 2) an intestinal biopsy which revealed villar atrophy in the duodenum and crypt hyperplasia. Shortly after the onset of these symptoms, she developed polyarthralgias affecting middle joints, predominantly of the wrists and feet, together with paresthesias and cutaneous lesions with pruriginous micropapules. She was referred to the Nephrology Department upon detection of proteinuria (+++). Results of Physical Examination: blood pressure 104/76mm Hg, BMI 27, minimal oedema of the lower limbs and papules on elbows and arms. Analytical findings: normal haemogram and coagulation, creatinine 0.9mg/dl, total cholesterol 238mg/dl, triglycerides 104mg/dl, total protein 6.5g/dl and albumin 3.6g/dl. Immunological assays: ANA, anti-DNA, ANCAs, C3, C4, anti-cardiolipin antibodies, lupic anticoagulant and cryoglobulins negative or normal. Serological tests: HBV, HCV and HIV negative. IgA antitissue transglutaminase antibodies positive: 800U/ml (normal < 7U/ml). Urine: proteins 4.4g/day and sediment with 5 RBC/HPF. The renal echography was normal. Given the persistence of the nephrotic proteinuria over a period of several weeks, a percutaneous renal biopsy was performed, the result of which revealed stage 2 MN with no vascular or interstitial lesions. Treatment consisted of a gluten-free diet and other conservative measures, including statins, aspirin at anti-aggregant doses, enalapril and losartan, to which there was no initial response. However, the follow-up results at 12 months were negative for anti-transglutaminase antibodies and there was complete remission of the proteinuria, as indicated in figure 1. During this time there were no other indications of systemic disease, except an increase in TSH levels to 6.6μU/ml, with a T41 level of 1.1ng/dl, and negative results for anti-thyroglobulin and anti-microsomal antibodies.</p><p class="elsevierStylePara"><span class="elsevierStyleBold">DISCUSSION</span></p><p class="elsevierStylePara">In this case we describe a patient who simultaneously presented CD and MN, an association which has been described very little in the literature. It is very likely that both entities have a common pathogenesis and require similar treatment.</p><p class="elsevierStylePara">CD is an autoimmune disease, which appears after exposure to environmental antigens (the gliadin contained in gluten) in patients with a genetic predisposition. For reasons which are unknown, certain components of gliadin provoke a change in the immune response in the intestinal wall, which is associated with local inflammation and the release of tissue transglutaminase, an enzyme produced by inflammatory and endothelial cells, and fibroblasts. Tissue transglutaminase increases the antigenicity of gluten peptides, stimulating T cells, which leads to villar atrophy and, consequently, malabsorption syndrome.<span class="elsevierStyleSup">1,2</span> CD can appear at any age and, sometimes, there are few symptoms, although it starts off with diarrhoea, abdominal pain and distension, vomiting, flatulence and anorexia. Its non-digestive manifestations include: iron deficiency anaemia, polyarthritis, growth retardation, osteoporosis and neurological symptoms. A biopsy of the duodenum-jejunum junction is indispensable for the diagnosis of CD. Atrophy, shortening of the villi and crypt hypertrophy in the small intestine are not specific to, but are very characteristic of this disease. In addition, the presence of high levels of IgA anti-tissue transglutaminase antibodies is useful for diagnostic purposes and for evaluating the progression of the disease, as their disappearance parallels clinical improvement; it is estimated that their sensitivity and specificity are 93.1 and 93.6%, respectively.<span class="elsevierStyleSup">1,5</span> Therefore, our patient met the three criteria required to confirm a diagnosis of classical CD: villar atrophy, symptoms of malabsorption and the disappearance of symptoms after following a gluten-free diet.</p><p class="elsevierStylePara">CD is associated with other autoimmune diseases, such as dermatitis herpetiformis, IgA deficit, Sjögren¿s syndrome, Addison¿s disease, type I diabetes, thyroid diseases, systemic lupus and hepatitis.<span class="elsevierStyleSup">1,6</span> The patient described in this case study had skin lesions, possibly atopic dermatitis, which is also associated with CD, that were not shown conclusively to be related to the disease. Moreover, its onset was associated with polyarthralgias, with no evidence of systemic lupus, possibly owing to symptoms of osteoarthritis, which has also been reported in CD. Moreover, patients with CD exhibit a greater prevalence of renal diseases. In an epidemiological study conducted in Sweden, Ludvigson et al.<span class="elsevierStyleSup">3</span> described an increase in the number of cases of chronic glomerulonephritis and advanced renal insufficiency in patients with CD and this risk is greater when the diagnosis is made in adults.</p><p class="elsevierStylePara">Although the incidence of renal disease in the CD patient population is low and, vice versa, the presence of CD in patients diagnosed with glomerulonephritis is minimal, this ssociation has pathogenic aspects that are common to both conditions and which can affect treatment. Isolated cases of CD linked to nephrotic syndrome have been documented. Giménez et al.<span class="elsevierStyleSup">7</span> reported a series of five children with nephrotic syndrome, who at some point developed CD; in the renal biopsy, performed on two of them, lesions with minimal changes or mesangial glomerulonephritis with IgM deposits were detected. In our opinion, it is best to rule out CD, which is more or less masked, in patients with glomerular nephropathies, given how easy it is to establish anti-tissue transglutaminase antibody levels and the therapeutic implications this entails. By far the main association between CD and glomerular disease is IgA nephropathy, which occurs in 3% of CD patients. It has also been reported that 22-77% of patients with IgA nephropathy have IgA anti-gliadin antibodies and 3-4% of these have CD.<span class="elsevierStyleSup">8,9</span> It is curious that our patient has an MN without IgA deposits, the co-existence of which with CD is exceptional. We have only come across one case similar to ours,<span class="elsevierStyleSup">10</span> which showed a poor response to treatment that involved blocking the renin-angiotensin system combined with a gluten-free diet, contrary to what we observed in our patient. In another publication a link between CD and MN is described, but the patient was initially diagnosed with MN and, then, 10 years later, with CD, the opposite to what happened in the case we present.<span class="elsevierStyleSup">11</span> In our opinion, the link between CD and MN is not coincidental and we think they share an autoimmune pathogenesis. Firstly, both entities are simultaneous in their onset and it may be the case that the autoimmune changes facilitate both the digestive and renal symptoms. Secondly, the remission of the proteinuria coincides with the disappearance of the IgA anti-tissue transglutaminase antibodies; although the remission may have been spontaneous, the fact that they coincided at the same time means that we can establish some kind of link, as the majority of cases of MN remit when the original cause is addressed. We would like to emphasize that our patient has not received immunosuppressive treatment, as we regarded her MN as a secondary condition and, in addition, she had never had a full nephrotic syndrome.</p><p class="elsevierStylePara">We conclude that the appearance of proteinuria in patients with CD may be due to MN and that a gluten-free diet improves both entities, supporting the view that there are pathogenic mechanisms which are common to both diseases.<br></br></p><p class="elsevierStylePara"><a href="grande/41918078_f1_pag480.jpg" class="elsevierStyleCrossRefs"><img src="41918078_f1_pag480.jpg"></img></a></p><p class="elsevierStylePara">Figure 1. </p>" "pdfFichero" => "P-E-S-A419-EN.pdf" "tienePdf" => true "PalabrasClave" => array:2 [ "es" => array:2 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec439733" "palabras" => array:1 [ 0 => "Nefropatía membranosa" ] ] 1 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec439735" "palabras" => array:1 [ 0 => "Enfermedad celíaca" ] ] ] "en" => array:2 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec439734" "palabras" => array:1 [ 0 => "Membranous nephropathy" ] ] 1 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec439736" "palabras" => array:1 [ 0 => "Celiac disease" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "es" => array:1 [ "resumen" => "<p class="elsevierStylePara">La enfermedad celíaca se produce por la interacción entre el gluten contenido en los cereales y varios factores genéticos y autoinmunes. Aunque las manifestaciones clínicas predominantes son digestivas, se han descrito varias manifestaciones sistémicas. También se ha asociado con varias enfermedades renales, entre las que predominan las glomerulonefritis. Describimos el caso de una paciente con una enfermedad celíaca aparecida tras su primera gestación que de forma simultánea presenta proteinuria nefrótica y microhematuria, con sustrato morfológico de nefropatía membranosa. Tras recibir tratamiento con medidas conservadoras (IECA, estatina) y dieta sin gluten, se aprecia mejoría de la clínica digestiva, y desaparición de los anticuerpos antitransglutaminasa tisular tipo IgA y de la proteinuria. Revisamos la relación entre enfermedad celíaca y nefropatía membranosa y el papel de la dieta libre de gluten en el control de las mismas.</p>" ] "en" => array:1 [ "resumen" => "Celiac disease results from the interaction between gluten and immune, genetic, and environmental factors. Although the main clinical manifestations are derived from gastrointestinal system, it has been described some renal diseases, especially chronic glomerulonephritis. We describe a young female patient with celiac disease which appears after delivery. Moreover, she develops simultaneously nephrotic proteinuria and microhematuria as a result of membranous nephropathy. The treatment with glutenfree diet and other conservative measures (ACEI and statin) is followed by clinical improvement and simultaneous decrease of tissue antitransglutaminase IgA-antibodies and complete remission of proteinuria. We review the relationship between celiac disease and membranous nephropathy and the role of diet in the management of both diseases." ] ] "multimedia" => array:1 [ 0 => array:7 [ "identificador" => "fig1" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "copyright" => "Elsevier España" "figura" => array:1 [ 0 => array:4 [ "imagen" => "41918078_f1_pag480.jpg" "Alto" => 320 "Ancho" => 398 "Tamanyo" => 15886 ] ] ] ] "bibliografia" => array:2 [ "titulo" => "Bibliography" "seccion" => array:1 [ 0 => array:1 [ "bibliografiaReferencia" => array:11 [ 0 => array:3 [ "identificador" => "bib1" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Schuppan D, Dieterich W. Pathogenesis, epidemiology, and clinical manifestations of celiac disease in adults. UpToDate, Basow, DS (Ed), UpToDate, Waltham, MA, 2009." "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] 1 => array:3 [ "identificador" => "bib2" "etiqueta" => "2" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Green PH, Cellier C. Celiac disease. N Engl J Med 2007;357:1731-43. <a href="http://www.ncbi.nlm.nih.gov/pubmed/17960014" target="_blank">[Pubmed]</a>" "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] 2 => array:3 [ "identificador" => "bib3" "etiqueta" => "3" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Ludvigsson JF, Montgomery SM, Olen O, Ekbom A, Ludvigsson J, Fored M. Coeliac disease and risk of renal disease-a general population cohort study. Nephrol Dial Trasnsplant 2006;21:1809-15." "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] 3 => array:3 [ "identificador" => "bib4" "etiqueta" => "4" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Pasternack A, Collin P, Mustonen J, Reunala T, Rantala I, Laurila K, Teppo A M. Glomerular IgA deposits in patients with celiac disease. Clin Nephrol 1990;34:56-60. <a href="http://www.ncbi.nlm.nih.gov/pubmed/2225554" target="_blank">[Pubmed]</a>" "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] 4 => array:3 [ "identificador" => "bib5" "etiqueta" => "5" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Viola L, Lugli L, Melegari A, Marotti E, Amarri S, Balli F. Antitransglutaminase enzyme-linked immune-adsorbed assay in coeliac disease diagnosis: evaluation of a diagnostic algorithm. Pediatr Med Chir 2004;26:126-31. <a href="http://www.ncbi.nlm.nih.gov/pubmed/15700737" target="_blank">[Pubmed]</a>" "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] 5 => array:3 [ "identificador" => "bib6" "etiqueta" => "6" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Collin P, Mäki M. Associated disorders in coeliac disease: clinical aspects. Scand J Gastroenterol 1994;29:769-75. <a href="http://www.ncbi.nlm.nih.gov/pubmed/7824853" target="_blank">[Pubmed]</a>" "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] 6 => array:3 [ "identificador" => "bib7" "etiqueta" => "7" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Giménez A, Vila J, Camacho JA, Vila A, Concheiro A, García L. Nephrotic Syndrome Associated with Celiac Disease. A report of five cases. Nephron 2002;92:950. <a href="http://www.ncbi.nlm.nih.gov/pubmed/12399649" target="_blank">[Pubmed]</a>" "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] 7 => array:3 [ "identificador" => "bib8" "etiqueta" => "8" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Sategna-Guidetti C, Ferfoglia G, Bruno M, Pulitano R, Roccatello D, Amore A, Coppo R. Do IgA antigliadin and IgA antiendomysium antibodies show there is latent coeliac disease in primary IgA nephropathy? Gut 1992;33:476-8. <a href="http://www.ncbi.nlm.nih.gov/pubmed/1582590" target="_blank">[Pubmed]</a>" "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] 8 => array:3 [ "identificador" => "bib9" "etiqueta" => "9" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Almroth G, Axelsson T, Mussener E, Grodzinsky E, Midhagen G, Olcen P. Increased prevalence of anti-gliadin IgA-antibodies with aberrant duodenal histopathological findings in patients with IgA-nephropathy and related disorders. Ups J Med Sci 2006;111:339-52. <a href="http://www.ncbi.nlm.nih.gov/pubmed/17578801" target="_blank">[Pubmed]</a>" "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] 9 => array:3 [ "identificador" => "bib10" "etiqueta" => "10" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Halma C, Ubels F. Celiac sprue-associated membranous nephropathy. Clin Nephrol 2007;68:197. <a href="http://www.ncbi.nlm.nih.gov/pubmed/17915626" target="_blank">[Pubmed]</a>" "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] 10 => array:3 [ "identificador" => "bib11" "etiqueta" => "11" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Casella G, Perego D, Baldini V, Monti C, Crippa S, Buda CA. A rare association between ulcerative colitis (UC), celiac disease (CD), membranous glomerulonephritis, leg venous thrombosis, and heterozygosity for factor V Leiden. J Gastroenterol 2002;37:761-2. <a href="http://www.ncbi.nlm.nih.gov/pubmed/12375154" target="_blank">[Pubmed]</a>" "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] ] ] ] ] ] "idiomaDefecto" => "en" "url" => "/20132514/0000002900000005/v0_201502091625/X2013251409003887/v0_201502091626/en/main.assets" "Apartado" => array:4 [ "identificador" => "35422" "tipo" => "SECCION" "en" => array:2 [ "titulo" => "Case Reports" "idiomaDefecto" => true ] "idiomaDefecto" => "en" ] "PDF" => "https://static.elsevier.es/multimedia/20132514/0000002900000005/v0_201502091625/X2013251409003887/v0_201502091626/en/P-E-S-A419-EN.pdf?idApp=UINPBA000064&text.app=https://revistanefrologia.com/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/X2013251409003887?idApp=UINPBA000064" ]
| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 3 | 8 | 11 |
| 2024 October | 47 | 60 | 107 |
| 2024 September | 38 | 61 | 99 |
| 2024 August | 59 | 65 | 124 |
| 2024 July | 71 | 49 | 120 |
| 2024 June | 69 | 60 | 129 |
| 2024 May | 92 | 37 | 129 |
| 2024 April | 61 | 48 | 109 |
| 2024 March | 56 | 33 | 89 |
| 2024 February | 52 | 34 | 86 |
| 2024 January | 39 | 31 | 70 |
| 2023 December | 32 | 32 | 64 |
| 2023 November | 30 | 40 | 70 |
| 2023 October | 36 | 57 | 93 |
| 2023 September | 42 | 38 | 80 |
| 2023 August | 53 | 29 | 82 |
| 2023 July | 56 | 36 | 92 |
| 2023 June | 36 | 44 | 80 |
| 2023 May | 43 | 48 | 91 |
| 2023 April | 43 | 27 | 70 |
| 2023 March | 46 | 33 | 79 |
| 2023 February | 33 | 22 | 55 |
| 2023 January | 34 | 18 | 52 |
| 2022 December | 38 | 34 | 72 |
| 2022 November | 48 | 20 | 68 |
| 2022 October | 59 | 35 | 94 |
| 2022 September | 41 | 29 | 70 |
| 2022 August | 48 | 57 | 105 |
| 2022 July | 54 | 44 | 98 |
| 2022 June | 31 | 29 | 60 |
| 2022 May | 78 | 46 | 124 |
| 2022 April | 93 | 56 | 149 |
| 2022 March | 63 | 47 | 110 |
| 2022 February | 91 | 45 | 136 |
| 2022 January | 56 | 26 | 82 |
| 2021 December | 44 | 41 | 85 |
| 2021 November | 43 | 43 | 86 |
| 2021 October | 37 | 43 | 80 |
| 2021 September | 55 | 45 | 100 |
| 2021 August | 80 | 32 | 112 |
| 2021 July | 50 | 33 | 83 |
| 2021 June | 29 | 24 | 53 |
| 2021 May | 41 | 29 | 70 |
| 2021 April | 114 | 63 | 177 |
| 2021 March | 79 | 25 | 104 |
| 2021 February | 60 | 20 | 80 |
| 2021 January | 61 | 18 | 79 |
| 2020 December | 45 | 8 | 53 |
| 2020 November | 61 | 18 | 79 |
| 2020 October | 30 | 13 | 43 |
| 2020 September | 74 | 15 | 89 |
| 2020 August | 42 | 10 | 52 |
| 2020 July | 97 | 13 | 110 |
| 2020 June | 53 | 10 | 63 |
| 2020 May | 62 | 19 | 81 |
| 2020 April | 58 | 21 | 79 |
| 2020 March | 53 | 9 | 62 |
| 2020 February | 72 | 21 | 93 |
| 2020 January | 76 | 13 | 89 |
| 2019 December | 86 | 32 | 118 |
| 2019 November | 56 | 29 | 85 |
| 2019 October | 43 | 17 | 60 |
| 2019 September | 54 | 25 | 79 |
| 2019 August | 36 | 9 | 45 |
| 2019 July | 51 | 23 | 74 |
| 2019 June | 40 | 10 | 50 |
| 2019 May | 45 | 15 | 60 |
| 2019 April | 100 | 88 | 188 |
| 2019 March | 74 | 21 | 95 |
| 2019 February | 29 | 9 | 38 |
| 2019 January | 44 | 22 | 66 |
| 2018 December | 95 | 23 | 118 |
| 2018 November | 75 | 11 | 86 |
| 2018 October | 89 | 12 | 101 |
| 2018 September | 75 | 8 | 83 |
| 2018 August | 51 | 14 | 65 |
| 2018 July | 48 | 9 | 57 |
| 2018 June | 58 | 8 | 66 |
| 2018 May | 57 | 12 | 69 |
| 2018 April | 31 | 4 | 35 |
| 2018 March | 61 | 9 | 70 |
| 2018 February | 38 | 6 | 44 |
| 2018 January | 32 | 7 | 39 |
| 2017 December | 58 | 10 | 68 |
| 2017 November | 52 | 8 | 60 |
| 2017 October | 36 | 9 | 45 |
| 2017 September | 52 | 15 | 67 |
| 2017 August | 47 | 25 | 72 |
| 2017 July | 35 | 28 | 63 |
| 2017 June | 32 | 28 | 60 |
| 2017 May | 45 | 29 | 74 |
| 2017 April | 35 | 26 | 61 |
| 2017 March | 35 | 27 | 62 |
| 2017 February | 34 | 23 | 57 |
| 2017 January | 25 | 21 | 46 |
| 2016 December | 80 | 10 | 90 |
| 2016 November | 82 | 12 | 94 |
| 2016 October | 90 | 35 | 125 |
| 2016 September | 140 | 8 | 148 |
| 2016 August | 231 | 8 | 239 |
| 2016 July | 194 | 24 | 218 |
| 2016 June | 138 | 0 | 138 |
| 2016 May | 116 | 0 | 116 |
| 2016 April | 74 | 0 | 74 |
| 2016 March | 68 | 0 | 68 |
| 2016 February | 103 | 0 | 103 |
| 2016 January | 105 | 0 | 105 |
| 2015 December | 119 | 0 | 119 |
| 2015 November | 108 | 0 | 108 |
| 2015 October | 68 | 0 | 68 |
| 2015 September | 82 | 0 | 82 |
| 2015 August | 72 | 0 | 72 |
| 2015 July | 58 | 0 | 58 |
| 2015 June | 45 | 0 | 45 |
| 2015 May | 46 | 0 | 46 |
| 2015 April | 6 | 0 | 6 |
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