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Phaeohyphomycosis caused by Alternaria infectoria presenting as multiple vegetating lesions in a renal transplant patient
Feohifomicosis producida por Alternaria infectoria con presentación clínica de múltiples lesiones vegetantes en un paciente sometido a un trasplante renal
Daniela Cunhaa,
, Cristina Amaroa, María Raquel Vieiraa, María da Luz Martinsb, Ana Paula Madurob, João Inácioc, Ana Afonsod, Gabriela Marques Pintoa, Jorge Cardosoa
Corresponding author
a Dermatology Department, Hospital de Curry Cabral, Lisbon, Portugal
b Mycology Laboratory, Instituto de Higiene e Medicina Tropical/CREM, Universidade Nova de Lisboa, Lisbon, Portugal
c Laboratório Nacional de Investigação Veterinária, Instituto Nacional de Recursos Biológicos, Lisbon, Portugal
d Histopathology Department, Hospital de Curry Cabral, Lisbon, Portugal
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"Mycology Laboratory, Instituto de Higiene e Medicina Tropical/CREM, Universidade Nova de Lisboa, Lisbon, Portugal" "etiqueta" => "<span class="elsevierStyleSup">b</span>" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Laboratório Nacional de Investigação Veterinária, Instituto Nacional de Recursos Biológicos, Lisbon, Portugal" "etiqueta" => "<span class="elsevierStyleSup">c</span>" "identificador" => "aff0015" ] 3 => array:3 [ "entidad" => "Histopathology Department, Hospital de Curry Cabral, Lisbon, Portugal" "etiqueta" => "<span class="elsevierStyleSup">d</span>" "identificador" => "aff0020" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Feohifomicosis producida por <span class="elsevierStyleItalic">Alternaria infectoria</span> con presentación clínica de múltiples lesiones vegetantes en un paciente sometido a un trasplante renal" ] ] "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" => 713 "Ancho" => 950 "Tamanyo" => 207707 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Microscopic examination following lactophenol blue staining (magnification ×1500).</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">Subcutaneous phaeohyphomycosis is an infection caused by an heterogeneous group of dematiaceous fungi.<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> Infections by species of <span class="elsevierStyleItalic">Alternaria</span> accounted for a significant number of cases reported in recent years.<a class="elsevierStyleCrossRefs" href="#bib0010"><span class="elsevierStyleSup">2,3,5,6,9,11,12,14,16,18</span></a> Members of this genus are generally found in aerosols, in soil, or on plants, and are typically pathogenic only to immunocompromised hosts.<a class="elsevierStyleCrossRefs" href="#bib0010"><span class="elsevierStyleSup">2,3,5,6,8–16,18</span></a> Nevertheless, a few reports describing cutaneous infections among immunocompetent individuals have also been described.<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">The development and refinement of modern molecular biologic techniques have lead to a better genotypic characterization of dematiaceous species associated with phaeohyphomycosis, resulting in a better understanding of these infections over the past decade.</p><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Case report</span><p id="par0015" class="elsevierStylePara elsevierViewall">A 53-year-old male gardener presented with multiple asymptomatic vegetating hyperkeratotic lesions and nodules on the distal extremities that had evolved over the past two months. There was no previous history of skin lesions or trauma. The patient had undergone kidney transplantation 16 months previously, due to end-stage renal disease of unknown etiology. Since transplantation, the patient was treated with tacrolimus plus mofetil mycophenolate and prednisolone and, at presentation, the dosages were 6<span class="elsevierStyleHsp" style=""></span>mg bid, 750<span class="elsevierStyleHsp" style=""></span>mg bid and 10<span class="elsevierStyleHsp" style=""></span>mg o.d., respectively.</p><p id="par0020" class="elsevierStylePara elsevierViewall">On examination, there were widespread, multiple keratotic and vegetating tumours, as well as several purplish non-painful nodules on the forearms, dorsum of the hands and shins. Lesions varied in size but a few reached 3.0<span class="elsevierStyleHsp" style=""></span>cm in diameter (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). There was no edema or lymphadenopathy and vital signs were normal. The patient was treated with itraconazole 400<span class="elsevierStyleHsp" style=""></span>mg o.d. for 10 months and the tacrolimus dose was adjusted accordingly. Complete resolution of skin lesions was achieved 9 months after treatment and itraconazole was administered for 4 weeks more. There was no recurrence 15 months after completion of the treatment.</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0025" class="elsevierStylePara elsevierViewall">Routine laboratory tests, including renal function and chest radiography, were unremarkable. Histopathology of the skin biopsy showed a granulomatous infiltrate with septate hyphae and oval-shaped structures following periodic acid-Schiff and Grocott's staining (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>). Direct examination of portions of the biopsy performed with 20% potassium hydroxide solution revealed several hyaline septate hyphae. For isolation, the remainder of the biopsy was inoculated onto Sabouraud dextrose agar, Brain–heart-infusion agar and Malt agar (DIFCO<span class="elsevierStyleSup">®</span>, Detroit, USA) and incubated at 24<span class="elsevierStyleHsp" style=""></span>°C and 37<span class="elsevierStyleHsp" style=""></span>°C. After seven days incubation, fungal colonies were discernable on the respective media. By day 21, the surface of the colonies was gray-white and cottony and the reverse was dark-brown. Microscopic examination revealed septate, brown hyphae with simple or branched conidiophores and multiple conidia. Conidia were mainly ovoid but some were muriform, smooth walled or verrucous, and a few ended with apical beaks, most forming acropetal chains (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>). After DNA extraction, the ITS (internal transcribed spacer) region of rDNA was PCR-amplified and sequencing of the ITS region was carried out using forward primer ITS1 and reverse primer ITS4 following standard protocols (STAB Vida Lda, Caparica, Portugal). The nucleotide sequence was deposited in GenBank with the accession number HM467255. Standard BLAST searches at GenBank database revealed a high similarity between this sequence and others representing <span class="elsevierStyleItalic">Alternaria</span> species (which are assigned in GenBank as <span class="elsevierStyleItalic">Lewia</span>, the designation of the respective teleomorphs). A phylogenetic tree was computed using PAUP software (Sinauer Associates, Inc., Sunderland, MA), including ITS sequences belonging to reference strains of <span class="elsevierStyleItalic">Alternaria</span> species, and to other closely related fungi, retrieved from GenBank (data not shown). This phylogenetic analysis placed our fungal isolate in the <span class="elsevierStyleItalic">Alternaria infectoria</span> species-group<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> and the 99.6% nucleotide identity with the type strain of <span class="elsevierStyleItalic">A. infectoria</span>, CBS 112250<span class="elsevierStyleSup">T</span>, further classified the isolate as this species.</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Discussion</span><p id="par0030" class="elsevierStylePara elsevierViewall">Cutaneous infections caused by <span class="elsevierStyleItalic">Alternaria</span> spp. were rarely reported prior to the use of highly potent immunosuppressive drugs in solid organ transplantation. These types of infections, however, are likely to become more frequent as the number of patients on these drug therapies and their survival time increase. Infections in patients with underlying immunosuppressive disease, such as diabetes mellitus, Cushing's syndrome, or haematological cancers have also been reported.<a class="elsevierStyleCrossRefs" href="#bib0040"><span class="elsevierStyleSup">8,10,13</span></a> Among the <span class="elsevierStyleItalic">Alternaria</span> species responsible for opportunistic infections in organ recipient patients, <span class="elsevierStyleItalic">A. infectoria</span> accounts for only a minority of cases reported over the past decade.<a class="elsevierStyleCrossRefs" href="#bib0010"><span class="elsevierStyleSup">2,3,5,6,9,11,12,14,16,18</span></a></p><p id="par0035" class="elsevierStylePara elsevierViewall">The spectrum of cutaneous manifestations resulting from alternariosis is broad and includes papules, tumours, and ulcerating lesions. There is no correlation between any given presentation and a specific causal agent among <span class="elsevierStyleItalic">Alternaria</span> species. Nevertheless, the great majority of the reported cutaneous infections caused by <span class="elsevierStyleItalic">A. infectoria</span> presented as asymptomatic nodules distributed at the extremities.<a class="elsevierStyleCrossRefs" href="#bib0010"><span class="elsevierStyleSup">2,3,5,6,12,18</span></a> The anatomic distribution of the lesions seems to result from direct inoculation of the fungus into damaged skin following contact with a contaminated fomite or plant.<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a></p><p id="par0040" class="elsevierStylePara elsevierViewall">As <span class="elsevierStyleItalic">A. infectoria</span> is a common saprophyte prevalent in the environment inhabiting primarily leaves and kernels of grasses and cereals,<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> fungi may be present at the superficial epidermal layers of human skin, representing environmental contaminants. Therefore, when phaeohyphomycosis is suspected, a deep tissue sample should be obtained for isolation and identification of the fungus.<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> The morphological findings of cutaneous alternariosis include dermal granulomatous infiltrates with variable epidermal changes. Fungal elements are usually seen within these infiltrates, presenting as spheroidal chlamydospore-like structures and hyphae, with and without pigmentation.<a class="elsevierStyleCrossRefs" href="#bib0030"><span class="elsevierStyleSup">6,7</span></a> Fungal culture on Sabouraud agar without cycloheximide yields “greyish”, “green, powdery” or “felty” colonies. By lactophenol cotton blue staining, the microscopic observation of pigmented conidiophores giving rise to dictyospores is highly suggestive of <span class="elsevierStyleItalic">A. infectoria.</span> The apical growth of long geniculate secondary conidiophores is a typical feature of the <span class="elsevierStyleItalic">A. infectoria</span> species-group.</p><p id="par0045" class="elsevierStylePara elsevierViewall">Molecular studies may provide additional time-efficient diagnostic information. Comparative analysis of rDNA ITS nucleotide sequences is commonly used for the identification of fungal species,<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> including <span class="elsevierStyleItalic">Alternaria</span> spp.<a class="elsevierStyleCrossRefs" href="#bib0060"><span class="elsevierStyleSup">12,14,16</span></a> This approach led to a rapid and accurate identification of the isolate described in this report that was otherwise difficult to identify using traditional culture-based mycologic methods.</p><p id="par0050" class="elsevierStylePara elsevierViewall">Different treatment options for this infection are available since no standard treatment has been defined. Small, isolated lesions may be successfully treated by simple surgical excision<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> or cryosurgery.<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> Multiple and larger lesions usually require systemic antimycotic therapy. On occasion, a combination of surgical and systemic antinfungal agents has proved efficacious.<a class="elsevierStyleCrossRefs" href="#bib0035"><span class="elsevierStyleSup">7,16</span></a> Itraconazole is the most commonly used drug, followed by amphotericin B.<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3–5,9</span></a> Itraconazole doses used range between 100 and 400<span class="elsevierStyleHsp" style=""></span>mg for 2–8 months in monotherapy regimens.<a class="elsevierStyleCrossRefs" href="#bib0015"><span class="elsevierStyleSup">3,6,7</span></a></p><p id="par0055" class="elsevierStylePara elsevierViewall">This case report is remarkable due to its clinical presentation with multiple nodules and vegetating tumours as well as the slow but successful response to monotherapy with high-dose itraconazole. Furthermore, it illustrated the efficacy of molecular techniques in <span class="elsevierStyleItalic">Alternaria</span> species identification.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle">Conflict of interest</span><p id="par0060" class="elsevierStylePara elsevierViewall">The authors have nothing to declare.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:8 [ 0 => array:2 [ "identificador" => "xres121171" "titulo" => "Abstract" ] 1 => array:2 [ "identificador" => "xpalclavsec108458" "titulo" => "Keywords" ] 2 => array:2 [ "identificador" => "xres121172" "titulo" => "Resumen" ] 3 => array:2 [ "identificador" => "xpalclavsec108457" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0010" "titulo" => "Case report" ] 5 => array:2 [ "identificador" => "sec0015" "titulo" => "Discussion" ] 6 => array:2 [ "identificador" => "sec0020" "titulo" => "Conflict of interest" ] 7 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2010-12-01" "fechaAceptado" => "2011-06-22" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec108458" "palabras" => array:4 [ 0 => "Mycosis" 1 => "Kidney transplantation" 2 => "Itraconazole" 3 => "Immunocompromised patient" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec108457" "palabras" => array:4 [ 0 => "Micosis" 1 => "Trasplante renal" 2 => "Itraconazol" 3 => "Paciente inmunocomprometido" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">The genus <span class="elsevierStyleItalic">Alternaria</span> is one of the most common black moulds and appears to be increasing as a causative agent of subcutaneous phaeohyphomycosis, particularly among immunosuppressed patients.</p><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">A 53-year-old patient who had received a kidney transplant presented with multiple verrucous lesions on the distal extremities. Positive histopathology and cultures, in addition to rDNA ITS region sequencing, identified the fungal isolate as <span class="elsevierStyleItalic">Alternaria infectoria</span>. Oral itraconazole was administered for 10 months. A follow-up at 15 months demonstrated no signs of infection.</p><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Clinical manifestations of cutaneous alternariosis vary significantly and only a few cases have been described in the literature. Although optimal treatment options remain controversial, this case of phaeohyphomycosis was successfully treated with itraconazole monotherapy.</p>" ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Las especies del género <span class="elsevierStyleItalic">Alternaria</span> son mohos ubicuos que se caracterizan por presentar colonias de color gris; parecen ser cada vez más frecuentes como agente causal de las feohifomicosis subcutáneas, en especial entre pacientes inmunocomprometidos.</p><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Un paciente de 53 años de edad, que se había sometido a un trasplante renal, consultó por presentar tumores verrugosos en el tercio distal de las extremidades. La histopatología y cultivo positivos, además de la secuenciación de la región de transcripción interna ITS del rDNA, permitieron la identificación del aislamiento fúngico como <span class="elsevierStyleItalic">Alternaria infectoria</span>. Se instauró tratamiento con itraconazol oral durante 10 meses y, a los 15 meses de seguimiento, se demostró la ausencia de signos de infección.</p><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Las manifestaciones clínicas de la alternariosis cutánea son muy variables y tan sólo se han descrito unos pocos casos en los que se presenta en forma de tumoraciones verrugosas. Aunque el tratamiento de elección sigue siendo motivo de controversia, el paciente presentado en este estudio fue tratado satisfactoriamente con itraconazol.</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" => 716 "Ancho" => 950 "Tamanyo" => 138435 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Widespread verrucous hyperkeratotic tumours.</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" => 704 "Ancho" => 950 "Tamanyo" => 175029 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Histopathological examination with Grocott's stain (magnification ×400).</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" => 713 "Ancho" => 950 "Tamanyo" => 207707 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Microscopic examination following lactophenol blue staining (magnification ×1500).</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:18 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "A polyphasic approach to the taxonomy of the <span class="elsevierStyleItalic">Alternaria infectoria</span> species–group" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:5 [ 0 => "B. 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 October | 14 | 9 | 23 |
| 2024 September | 24 | 6 | 30 |
| 2024 August | 22 | 4 | 26 |
| 2024 July | 13 | 4 | 17 |
| 2024 June | 22 | 2 | 24 |
| 2024 May | 21 | 6 | 27 |
| 2024 April | 16 | 12 | 28 |
| 2024 March | 33 | 5 | 38 |
| 2024 February | 24 | 1 | 25 |
| 2024 January | 30 | 2 | 32 |
| 2023 December | 33 | 6 | 39 |
| 2023 November | 32 | 7 | 39 |
| 2023 October | 37 | 4 | 41 |
| 2023 September | 33 | 1 | 34 |
| 2023 August | 19 | 2 | 21 |
| 2023 July | 44 | 8 | 52 |
| 2023 June | 38 | 4 | 42 |
| 2023 May | 80 | 9 | 89 |
| 2023 April | 65 | 13 | 78 |
| 2023 March | 52 | 0 | 52 |
| 2023 February | 44 | 4 | 48 |
| 2023 January | 40 | 9 | 49 |
| 2022 December | 33 | 14 | 47 |
| 2022 November | 45 | 13 | 58 |
| 2022 October | 32 | 14 | 46 |
| 2022 September | 31 | 18 | 49 |
| 2022 August | 29 | 21 | 50 |
| 2022 July | 28 | 12 | 40 |
| 2022 June | 19 | 5 | 24 |
| 2022 May | 17 | 15 | 32 |
| 2022 April | 26 | 19 | 45 |
| 2022 March | 33 | 7 | 40 |
| 2022 February | 50 | 13 | 63 |
| 2022 January | 85 | 33 | 118 |
| 2021 December | 48 | 6 | 54 |
| 2021 November | 48 | 9 | 57 |
| 2021 October | 70 | 15 | 85 |
| 2021 September | 40 | 13 | 53 |
| 2021 August | 45 | 18 | 63 |
| 2021 July | 23 | 14 | 37 |
| 2021 June | 28 | 10 | 38 |
| 2021 May | 45 | 13 | 58 |
| 2021 April | 113 | 21 | 134 |
| 2021 March | 47 | 9 | 56 |
| 2021 February | 16 | 13 | 29 |
| 2021 January | 25 | 16 | 41 |
| 2020 December | 17 | 15 | 32 |
| 2020 November | 12 | 16 | 28 |
| 2020 October | 6 | 5 | 11 |
| 2020 September | 15 | 10 | 25 |
| 2020 August | 12 | 9 | 21 |
| 2020 July | 18 | 12 | 30 |
| 2020 June | 18 | 15 | 33 |
| 2020 May | 19 | 6 | 25 |
| 2020 April | 12 | 6 | 18 |
| 2020 March | 13 | 2 | 15 |
| 2020 February | 14 | 4 | 18 |
| 2020 January | 22 | 9 | 31 |
| 2019 December | 10 | 10 | 20 |
| 2019 November | 10 | 3 | 13 |
| 2019 October | 9 | 2 | 11 |
| 2019 September | 18 | 2 | 20 |
| 2019 August | 13 | 4 | 17 |
| 2019 July | 14 | 14 | 28 |
| 2019 June | 59 | 12 | 71 |
| 2019 May | 114 | 28 | 142 |
| 2019 April | 69 | 22 | 91 |
| 2019 March | 12 | 4 | 16 |
| 2019 February | 13 | 2 | 15 |
| 2019 January | 9 | 3 | 12 |
| 2018 December | 12 | 5 | 17 |
| 2018 November | 15 | 2 | 17 |
| 2018 October | 20 | 12 | 32 |
| 2018 September | 14 | 6 | 20 |
| 2018 August | 14 | 2 | 16 |
| 2018 July | 8 | 2 | 10 |
| 2018 June | 7 | 1 | 8 |
| 2018 May | 11 | 1 | 12 |
| 2018 April | 9 | 0 | 9 |
| 2018 March | 13 | 0 | 13 |
| 2018 February | 19 | 1 | 20 |
| 2018 January | 20 | 1 | 21 |
| 2017 December | 8 | 0 | 8 |
| 2017 November | 16 | 1 | 17 |
| 2017 October | 16 | 0 | 16 |
| 2017 September | 18 | 0 | 18 |
| 2017 August | 17 | 6 | 23 |
| 2017 July | 13 | 2 | 15 |
| 2017 June | 18 | 2 | 20 |
| 2017 May | 34 | 3 | 37 |
| 2017 April | 27 | 2 | 29 |
| 2017 March | 29 | 37 | 66 |
| 2017 February | 31 | 4 | 35 |
| 2017 January | 18 | 2 | 20 |
| 2016 December | 59 | 3 | 62 |
| 2016 November | 62 | 7 | 69 |
| 2016 October | 74 | 1 | 75 |
| 2016 September | 46 | 2 | 48 |
| 2016 August | 39 | 3 | 42 |
| 2016 July | 50 | 1 | 51 |
| 2016 June | 55 | 6 | 61 |
| 2016 May | 41 | 11 | 52 |
| 2016 April | 35 | 1 | 36 |
| 2016 March | 23 | 6 | 29 |
| 2016 February | 20 | 9 | 29 |
| 2016 January | 37 | 9 | 46 |
| 2015 December | 70 | 5 | 75 |
| 2015 November | 53 | 1 | 54 |
| 2015 October | 45 | 5 | 50 |
| 2015 September | 56 | 2 | 58 |
| 2015 August | 69 | 2 | 71 |
| 2015 July | 33 | 5 | 38 |
| 2015 June | 45 | 1 | 46 |
| 2015 May | 56 | 2 | 58 |
| 2015 April | 31 | 4 | 35 |
| 2015 March | 26 | 5 | 31 |
| 2015 February | 38 | 6 | 44 |
| 2015 January | 36 | 10 | 46 |
| 2014 December | 30 | 8 | 38 |
| 2014 November | 50 | 3 | 53 |
| 2014 October | 42 | 2 | 44 |
| 2014 September | 28 | 1 | 29 |
| 2014 August | 35 | 2 | 37 |
| 2014 July | 32 | 2 | 34 |
| 2014 June | 47 | 6 | 53 |
| 2014 May | 41 | 6 | 47 |
| 2014 April | 37 | 7 | 44 |
| 2014 March | 97 | 17 | 114 |
| 2014 February | 67 | 10 | 77 |
| 2014 January | 82 | 7 | 89 |
| 2013 December | 92 | 7 | 99 |
| 2013 November | 71 | 14 | 85 |
| 2013 October | 29 | 4 | 33 |
| 2013 September | 42 | 10 | 52 |
| 2013 August | 55 | 8 | 63 |
| 2013 July | 69 | 8 | 77 |
| 2013 June | 123 | 5 | 128 |
| 2013 May | 126 | 9 | 135 |
| 2013 April | 363 | 10 | 373 |
| 2013 March | 725 | 11 | 736 |
| 2013 February | 176 | 8 | 184 |
| 2013 January | 61 | 6 | 67 |
| 2012 December | 21 | 10 | 31 |
| 2012 November | 20 | 4 | 24 |
| 2012 October | 4 | 2 | 6 |
| 2012 January | 1050 | 0 | 1050 |
Show all
