Case and Research Letter
Concomitant Pyoderma Gangrenosum and Erythema Nodosum in a Patient With Ulcerative Colitis
Pioderma gangrenoso concomitante y eritema nudoso en paciente con colitis ulcerosa
N. Kikuchi
, N. Matsumura, T. Hiraiwa, Y. Kato, M. Satoh, T. Yamamoto
Corresponding author
Department of Dermatology, Fukushima Medical University, Fukushima, Japan
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Kikuchi, N. Matsumura, T. Hiraiwa, Y. Kato, M. Satoh, T. Yamamoto" "autores" => array:6 [ 0 => array:4 [ "nombre" => "N." "apellidos" => "Kikuchi" "email" => array:1 [ 0 => "nobuyuk@fmu.ac.jp" ] "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0005" ] ] ] 1 => array:2 [ "nombre" => "N." "apellidos" => "Matsumura" ] 2 => array:2 [ "nombre" => "T." "apellidos" => "Hiraiwa" ] 3 => array:2 [ "nombre" => "Y." "apellidos" => "Kato" ] 4 => array:2 [ "nombre" => "M." "apellidos" => "Satoh" ] 5 => array:2 [ "nombre" => "T." "apellidos" => "Yamamoto" ] ] "afiliaciones" => array:1 [ 0 => array:2 [ "entidad" => "Department of Dermatology, Fukushima Medical University, Fukushima, Japan" "identificador" => "aff0005" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Pioderma gangrenoso concomitante y eritema nudoso en paciente con colitis ulcerosa" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 2242 "Ancho" => 2995 "Tamanyo" => 814785 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">(A) Deep ulcerative lesions on the lower leg. (B) Histological features showing a dense neutrophil infiltrate in the upper to mid-dermis. Hematoxylin and eosin (H&E), original magnification ×40. (C) Higher magnification reveals prominent neutrophil infiltration and extravasation of red blood cells. H&E, original magnification ×400. (D) Painful, subcutaneous erythematous nodules on the knee. (E) Histology shows cellular infiltrates most intense in the subcutaneous septa. H&E, original magnification ×40.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">A 40-year-old woman was admitted to our hospital with a painful ulcer on her leg and fever of over 38<span class="elsevierStyleHsp" style=""></span>°C. She had been diagnosed with ulcerative colitis (UC) 14 years earlier and was on treatment with mesalazine, 3600<span class="elsevierStyleHsp" style=""></span>mg/d, and prednisolone at doses of up to 40<span class="elsevierStyleHsp" style=""></span>mg/d. Infliximab, 5<span class="elsevierStyleHsp" style=""></span>mg/kg, plus azathioprine, 50<span class="elsevierStyleHsp" style=""></span>mg/d, had been added to her treatment a year prior to admission and had been administered 8 times in total. The patient also reported atopic dermatitis since childhood. One week prior to admission she experienced painful erythema of sudden onset on the lower leg; the lesion became ulcerated 4 days later. She denied any history of trauma or bruising.</p><p id="par0010" class="elsevierStylePara elsevierViewall">Physical examination revealed a very tender ulcer measuring 3<span class="elsevierStyleHsp" style=""></span>cm<span class="elsevierStyleHsp" style=""></span>×<span class="elsevierStyleHsp" style=""></span>1.5<span class="elsevierStyleHsp" style=""></span>cm on the left lower leg (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>A). The ulcer had irregular, elevated borders with edema. Laboratory tests revealed a white blood cell count of 7100<span class="elsevierStyleHsp" style=""></span>cells/μL, with 67% neutrophils, and elevation of C-reactive protein levels (9.15<span class="elsevierStyleHsp" style=""></span>mg/dL) and of the erythrocyte sedimentation rate (39<span class="elsevierStyleHsp" style=""></span>mm/h). Serum levels of interleukin (IL) 8 were extremely high (1860<span class="elsevierStyleHsp" style=""></span>pg/mL). Bacterial culture was sterile. A biopsy taken from the border of the ulcer showed a diffuse neutrophil infiltrate in the dermis and subcutaneous adipose tissue (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>B and C). On the second day of hospitalization, the patient developed tender erythema on both her lower legs and on her right thigh. Physical examination revealed a number of poorly defined, indurated, pale pink-erythematous papules measuring 1<span class="elsevierStyleHsp" style=""></span>cm<span class="elsevierStyleHsp" style=""></span>×<span class="elsevierStyleHsp" style=""></span>1<span class="elsevierStyleHsp" style=""></span>cm on the right knee (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>D) and on both lower legs. On histology, a neutrophilic infiltrate was observed in the subcutaneous adipose tissue (most intense in the septa) (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>E). The ulcer had reepithelialized completely 2 months after starting treatment with systemic prednisolone, 25<span class="elsevierStyleHsp" style=""></span>mg/d. The prednisolone dose was then gradually tapered to complete withdrawal 5 months later, with no relapse of the pyoderma gangrenosum (PG). Both infliximab and azathioprine were continued throughout the course of steroid treatment.</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0015" class="elsevierStylePara elsevierViewall">PG and erythema nodosum (EN) are skin lesions associated with UC.<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">1</span></a> In general, such manifestations appear to be related to activity of the intestinal disease; however, some patients develop skin lesions despite remission of their bowel condition. Our patient developed a deep ulcer on her lower leg, followed by painful erythematous subcutaneous nodules at an interval of several days, despite control of her intestinal disease. To date, counting our patient, only 5 five cases of concomitant PG and EN have been reported.<a class="elsevierStyleCrossRefs" href="#bib0055"><span class="elsevierStyleSup">2,3</span></a> The details of these patients, all women aged between 19 and 49 years, are summarized in <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>. One patient had Crohn disease, the other 4 had UC. Skin symptoms appeared simultaneously with an exacerbation of the intestinal disease in all cases except in our patient. Arthritis was observed in 1 case. Systemic steroids were used in 4 cases, with an adequate response, and 1 case was successfully treated using tacrolimus and granulocytapheresis.<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">3</span></a> Very rarely, PG can be induced by tumor necrosis factor (TNF) inhibitors<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">4</span></a>; however, we ruled out the possibility of biologics-induced PG in our patient because the administration of infliximab to control her intestinal symptoms after the onset of her PG and EN did not exacerbate either the skin or the joint manifestations. Furthermore, azathioprine was continued throughout the course of steroid treatment, indicating that PG and EN were not related to azathioprine.</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0020" class="elsevierStylePara elsevierViewall">Our patient complained of flu-like symptoms, such as rhinitis and fever, which may have triggered neutrophil activation and recruitment to the skin via chemokines such as IL-8, a potent neutrophil chemoattractant. Neutrophil priming can occur in response to a number of stimuli, including TNF-α, IL-8, and granulocyte macrophage-colony stimulating factor. In the present case, serum IL-8 was very significantly elevated; this interleukin is also able to induce the production of reactive oxygen species, leading to skin damage.<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">5</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">A further factor to be taken into account in our patient was that she had had atopic dermatitis since childhood. Previous studies have shown an association between atopic dermatitis and UC,<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">6</span></a> and an increased risk of inflammatory bowel disease among patients with atopic dermatitis.<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">7</span></a> However, other studies have not observed a statistically significant increase in the prevalence of atopic dermatitis among patients with UC compared with healthy controls.<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">8</span></a> Possible mechanisms may include an impaired barrier function, potential sharing of type 2 T-helper cell cytokines, and thymic stromal lymphopoietin (TSLP).<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">9</span></a></p><p id="par0030" class="elsevierStylePara elsevierViewall">In summary, we have described the rare case of a patient with UC who developed concurrent PG and EN not related to the activity of her intestinal disease. Reporting of similar cases will help to clarify the mechanisms of the aseptic neutrophilic disorders, such as the so-called aseptic abscess syndrome.</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">Conflict of interests</span><p id="par0035" class="elsevierStylePara elsevierViewall">The authors declare no conflict of interests.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:2 [ 0 => array:2 [ "identificador" => "sec0005" "titulo" => "Conflict of interests" ] 1 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "multimedia" => array:2 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 2242 "Ancho" => 2995 "Tamanyo" => 814785 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">(A) Deep ulcerative lesions on the lower leg. (B) Histological features showing a dense neutrophil infiltrate in the upper to mid-dermis. Hematoxylin and eosin (H&E), original magnification ×40. (C) Higher magnification reveals prominent neutrophil infiltration and extravasation of red blood cells. H&E, original magnification ×400. (D) Painful, subcutaneous erythematous nodules on the knee. (E) Histology shows cellular infiltrates most intense in the subcutaneous septa. H&E, original magnification ×40.</p>" ] ] 1 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "leyenda" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleItalic">Abbreviations</span>: CD, Crohn disease; EN, erythema nodosum; F, female; IBD, inflammatory bowel disease; M, male; PG, pyoderma gangrenosum; UC, ulcerative colitis.</p>" "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Case \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Age/sex \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">IBD \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Duration of IBD, y \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Control of IBD \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Arthritis \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">PG \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">EN \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Time lag \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Therapy \t\t\t\t\t\t\n \t\t\t\t</th><th class="td" title="table-head " align="left" valign="top" scope="col" style="border-bottom: 2px solid black">Reference \t\t\t\t\t\t\n \t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="table-entry " align="char" valign="top">1 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">19/F \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">CD \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Exacerbation \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">No \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Scalp, face, trunk, extremities \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Calf \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Simultaneous \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Hydrocortisone, azathioprine \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top"><a class="elsevierStyleCrossRef" href="#bib0055">2</a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">20/F \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">UC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">2 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Exacerbation \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">No \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Popliteal fossa \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lower leg \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Simultaneous \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Hydrocortisone, ciclosporin \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top"><a class="elsevierStyleCrossRef" href="#bib0055">2</a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="char" valign="top">3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">49/F \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">UC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">25 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Exacerbation \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Yes \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Calf \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Extremities \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Simultaneous \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Hydrocortisone \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top"><a class="elsevierStyleCrossRef" href="#bib0055">2</a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="char" valign="top">4 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">44/F \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">UC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">3 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Exacerbation \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">No \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Back, thigh \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lower leg \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">3 days \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Tacrolimus, granulocytapheresis \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top"><a class="elsevierStyleCrossRef" href="#bib0060">3</a> \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="table-entry " align="char" valign="top">5 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">40/F \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">UC \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="char" valign="top">14 \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Stable \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">No \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lower leg \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Lower leg, thigh \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">7 days \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Prednisolone \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="table-entry " align="left" valign="top">Present case \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab1260384.png" ] ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Clinical features of patients with inflammatory bowel disease and concomitant pyoderma gangrenosum and erythema nodosum.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:9 [ 0 => array:3 [ "identificador" => "bib0050" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Skin manifestations of inflammatory bowel disease" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 9 | 4 | 13 |
| 2024 October | 92 | 32 | 124 |
| 2024 September | 98 | 29 | 127 |
| 2024 August | 162 | 44 | 206 |
| 2024 July | 144 | 37 | 181 |
| 2024 June | 165 | 28 | 193 |
| 2024 May | 117 | 32 | 149 |
| 2024 April | 122 | 19 | 141 |
| 2024 March | 116 | 34 | 150 |
| 2024 February | 107 | 30 | 137 |
| 2024 January | 114 | 32 | 146 |
| 2023 December | 98 | 16 | 114 |
| 2023 November | 125 | 24 | 149 |
| 2023 October | 102 | 12 | 114 |
| 2023 September | 96 | 28 | 124 |
| 2023 August | 50 | 13 | 63 |
| 2023 July | 57 | 19 | 76 |
| 2023 June | 48 | 22 | 70 |
| 2023 May | 58 | 23 | 81 |
| 2023 April | 33 | 14 | 47 |
| 2023 March | 43 | 27 | 70 |
| 2023 February | 37 | 20 | 57 |
| 2023 January | 25 | 21 | 46 |
| 2022 December | 31 | 32 | 63 |
| 2022 November | 22 | 23 | 45 |
| 2022 October | 24 | 26 | 50 |
| 2022 September | 23 | 28 | 51 |
| 2022 August | 15 | 21 | 36 |
| 2022 July | 19 | 27 | 46 |
| 2022 June | 19 | 21 | 40 |
| 2022 May | 50 | 26 | 76 |
| 2022 April | 47 | 21 | 68 |
| 2022 March | 66 | 33 | 99 |
| 2022 February | 69 | 23 | 92 |
| 2022 January | 73 | 24 | 97 |
| 2021 December | 29 | 29 | 58 |
| 2021 November | 55 | 40 | 95 |
| 2021 October | 49 | 65 | 114 |
| 2021 September | 55 | 44 | 99 |
| 2021 August | 77 | 30 | 107 |
| 2021 July | 58 | 14 | 72 |
| 2021 June | 46 | 24 | 70 |
| 2021 May | 61 | 36 | 97 |
| 2021 April | 66 | 46 | 112 |
| 2021 March | 55 | 32 | 87 |
| 2021 February | 38 | 32 | 70 |
| 2021 January | 43 | 13 | 56 |
| 2020 December | 48 | 29 | 77 |
| 2020 November | 17 | 15 | 32 |
| 2020 October | 18 | 6 | 24 |
| 2020 September | 27 | 10 | 37 |
| 2020 August | 22 | 15 | 37 |
| 2020 July | 18 | 14 | 32 |
| 2020 June | 27 | 32 | 59 |
| 2020 May | 18 | 15 | 33 |
| 2020 April | 27 | 16 | 43 |
| 2020 March | 17 | 14 | 31 |
| 2020 February | 4 | 0 | 4 |
| 2020 January | 3 | 0 | 3 |
| 2019 December | 8 | 0 | 8 |
| 2019 November | 4 | 0 | 4 |
| 2019 September | 7 | 0 | 7 |
| 2019 August | 6 | 0 | 6 |
| 2019 July | 8 | 0 | 8 |
| 2019 June | 4 | 0 | 4 |
| 2019 May | 6 | 0 | 6 |
| 2019 April | 2 | 4 | 6 |
| 2019 February | 5 | 0 | 5 |
| 2019 January | 4 | 0 | 4 |
| 2018 November | 6 | 0 | 6 |
| 2018 October | 2 | 0 | 2 |
| 2018 September | 1 | 0 | 1 |
| 2018 February | 17 | 1 | 18 |
| 2018 January | 28 | 13 | 41 |
| 2017 December | 36 | 8 | 44 |
| 2017 November | 31 | 9 | 40 |
| 2017 October | 27 | 6 | 33 |
| 2017 September | 20 | 3 | 23 |
| 2017 August | 23 | 6 | 29 |
| 2017 July | 15 | 5 | 20 |
| 2017 June | 23 | 12 | 35 |
| 2017 May | 21 | 5 | 26 |
| 2017 April | 19 | 10 | 29 |
| 2017 March | 18 | 19 | 37 |
| 2017 February | 14 | 10 | 24 |
| 2017 January | 7 | 9 | 16 |
| 2016 December | 48 | 33 | 81 |
| 2016 November | 11 | 10 | 21 |
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