Guidelines for indicating, obtaining, processing, and evaluating kidney transplant biopsies
Recomendaciones para la indicación, obtención, procesamiento y evaluación de biopsias en el trasplante renal.
Daniel Seróna, Fernando Anayab, Roberto Marcénc, Raimundo García del Morald, Eduardo Vázquez Martule, Antonio Alarcónf, Amado Andrésg, Dolores Burgosh, Miguel González Molinah, Luis Capdevilai, Carlos Jiménezj, Federico Oppenheimerk, José María Moralesg, Luis Pallardól, Ana Sánchez Fructuosom
a Servicio de Nefrología, Hospital Universitari de Bellvitge, Barcelona, Barcelona, España,
b Servicio de Nefrología, Hospital Gregorio Marañón, Madrid, Madrid, España,
c Servicio de Nefrología, Hospital Ramón y Cajal, Madrid, Madrid, España,
d Servicio de Nefrología, Hospital Universitario de Granada, Granada, Granada, España,
e Servicio de Nefrología, Complejo Hospitalario Universitario Juan Canalejo, A Coruña, A Coruña, España,
f Servicio de Nefrología, Hospital Universitario Son Dureta, Palma de Mallorca, Islas Baleares, España,
g Servicio de Nefrología, Hospital 12 de Octubre, Madrid, Madrid, España,
h Servicio de Nefrología, Regional Universitario Carlos Haya, Málaga, Málaga, España,
i Servicio de Nefrología, Hospital de la Vall d¿Hebron, Barcelona, Barcelona, España,
j Servicio de Nefrología, Hospital Universitario La Paz, Madrid, Madrid, España,
k Servicio de Nefrología, Hospital Clínic, Barcelona, Barcelona, España,
l Servicio de Nefrología, Hospital Doctor Peset, Valencia, Valencia, España,
m Servicio de Nefrología, Hospital Clínico San Carlos, Madrid, Madrid, España,
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Nefrología, Hospital Universitario Son Dureta, Palma de Mallorca, Islas Baleares, España, " "etiqueta" => "<span class="elsevierStyleSup">f</span>" "identificador" => "afff" ] 6 => array:3 [ "entidad" => "Servicio de Nefrología, Hospital 12 de Octubre, Madrid, Madrid, España, " "etiqueta" => "<span class="elsevierStyleSup">g</span>" "identificador" => "affg" ] 7 => array:3 [ "entidad" => "Servicio de Nefrología, Regional Universitario Carlos Haya, Málaga, Málaga, España, " "etiqueta" => "<span class="elsevierStyleSup">h</span>" "identificador" => "affh" ] 8 => array:3 [ "entidad" => "Servicio de Nefrología, Hospital de la Vall d¿Hebron, Barcelona, Barcelona, España, " "etiqueta" => "<span class="elsevierStyleSup">i</span>" "identificador" => "affi" ] 9 => array:3 [ "entidad" => "Servicio de Nefrología, Hospital Universitario La Paz, Madrid, Madrid, España, " "etiqueta" => "<span class="elsevierStyleSup">j</span>" "identificador" => "affj" ] 10 => array:3 [ "entidad" => "Servicio de Nefrología, Hospital Clínic, Barcelona, Barcelona, España, " "etiqueta" => "<span class="elsevierStyleSup">k</span>" "identificador" => "affk" ] 11 => array:3 [ "entidad" => "Servicio de Nefrología, Hospital Doctor Peset, Valencia, Valencia, España, " "etiqueta" => "<span class="elsevierStyleSup">l</span>" "identificador" => "affl" ] 12 => array:3 [ "entidad" => "Servicio de Nefrología, Hospital Clínico San Carlos, Madrid, Madrid, España, " "etiqueta" => "<span class="elsevierStyleSup">m</span>" "identificador" => "affm" ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Recomendaciones para la indicación, obtención, procesamiento y evaluación de biopsias en el trasplante renal." ] ] "textoCompleto" => "<p class="elsevierStylePara">INTRODUCTIÓN<br /><br />Despite the significant transplant activity in Spain,1 no consensus has been reached yet in our country about the clinical situations in which a diagnostic biopsy would be recommended, or about how use of protocol or donor biopsies may be improved in clinical practice. Thus, an overall view detects a high heterogeneity between the different centres and even certain practices that may be considered inadequate. For instance, despite the significant<br />evidence advising performance of biopsies in certain donor types or use of protocol biopsies,2,3 a recent epidemiological study demonstrated that the former only account for 3% of all biopsies performed in Spain every year,4 while only two Spanish centres perform serial protocol biopsies. An analysis of diagnostic biopsies also shows significant differences as regards activity in the different centres, with up to 10-fold differences being found in the reported biopsy/transplant ratios in certain cases.4 In addition, no clear agreement appears to exist either about how renal tissue samples should be obtained and processed. There are relevant differences as regards use of different puncture needle gauges, as well as a quite limited use of more specific diagnostic procedures such as immunofluorescence, immunohistochemistry, or electron microscopy.<br /><br />Because of this situation, a group of clinicians and nephropathologists experienced in kidney transplant jointly<br />addressed, in a consensus conference held in Toledo in 2007, the various issues of interest related to the indication,<br />processing, and evaluation of kidney biopsies in transplant patients. The main conclusions and recommendations on<br />the subject of such consensus group are summarised in this document.<br /><br />CLINICAL VALUE OF BIOPSY IN KIDNEY TRANSPLANT<br /><br />Donor biopsy<br />Multiple studies have shown that the presence of pre-existing lesions in the donor biopsy is associated to the occurrence of acute rejection, a poorer function, development of subsequent lesions, and a reduced graft survival.5-20 Despite methodological differences between the different studies and certain disparate results,21 there is currently a fair amount of agreement in that the finding of glomerular, tubulointerstitial, and vascular lesions in the biopsy at the time of implant represents one of the main donor-dependent factors that may condition kidney graft evolution. Indeed, it has been shown in several series that the finding in the donor biopsy of ~20% glomerulosclerosis is associated to the presence of delayed graft function (DGF) immediately after transplant, and also to a reduced kidney function or long-term graft loss.8,13-15,18 The presence of tubulointerstitial damage inherited from the donor, such as interstitial fibrosis, tubular atrophy, or acute tubular necrosis, also has a relevant role and is correlated to subsequent development in the recipient of glomerulosclerosis and chronic interstitial damage. Such events significantly influence kidney function and survival of the implanted organ18-20 and emphasise the importance of indication for performance of this biopsy in the donor using a good analytical methodology.22<br /><br />As regards vascular damage, Nankivell et al found in 2001 that small vessel lesions in the donor predicted for detection of typical chronic nephropathy lesion in biopsies taken at 3 months of transplant,17 whereas in the long term, detection of fibrous intimal thickening in the biopsy at the time of implant has been associated to the occurrence and severity of interstitial fibrosis, as well as to a reduced creatinine clearance.12 Based on all the foregoing, it is understandable that interest in performance of donor biopsies has significantly increased in recent years, in parallel to the increasing use of marginal organs from elderly, diabetic, or hypertensive patients. The presence of these factors is obviously associated to development in the kidney of the abovementioned histological lesions,23,24 which are consistently related to poorer graft evolution outcomes,25,26 as already discussed.<br /><br />Histological evaluation of the potential graft thus represents, together with clinical and laboratory data, a procedure<br />that has been used to decide whether a single or double transplant should be performed or organs from that donor should be discarded.27-29 This is the main current indication for donor biopsy in many centres, but it should not<br />be forgotten that taking a sample at time zero, even in optimum donors, is of great help for adequate interpretation by pathologists of potential subsequent lesions in the recipient. Biopsy should therefore not be limited to the study of graft viability.<br /><br />Finally, it should also be reminded that biopsy performance in donors is of particular interest in the setting of clinical<br />trials in order to have paired morphological data before and after transplant.<br /><br />Recipient biopsy<br />Histological examination of renal biopsy continues to be the test par excellence for diagnostic identification of graft<br />pathology, and its value is shown by the fact that more than 90% of biopsies performed in kidney transplant patients in Spain are indicated for diagnostic reasons.4 The main value of biopsy lies in the possibility of differentiating in detail the presence of lesions suggesting acute rejection, nephrotoxicity induced by calcineurin inhibitors, or chronic lesions, and also of diagnosing not clinically suspected conditions such as de novo glomerulopathies, disease recurrence, or nephropathy associated to polyomavirus type BK. In this regard, introduction in recent years of the Banff criteria and their respective updates30-33 has allowed for having a reproducible tool34 with a high clinical-pathological correlation35 and internationally accepted for description of acute and chronic lesions of the different kidney compartments. In addition, recent incorporation of new histological<br />and marker techniques, such as detection of C4d and donor-specific antibodies, has increased the diagnostic and<br />prognostic capacity of renal biopsy, giving pathologists the possibility of performing increasingly accurate diagnoses. In this regard, the growing volume of evidence accumulated using these procedures recently allowed the Banff conference for proposing introduction of a new concept, late antibody-mediated rejection, as well as criteria required for its diagnosis.33<br /><br />With regard to protocol biopsies, recent studies have been able to establish the natural history of lesions affecting the renal graft,36 as well as the impact of each of them on transplant prognosis. Use of serial biopsies has revealed that prevalence of interstitial infiltrates and tubulitis in stable grafts, the so-called subclinical rejection (SCR), is maximum during the initial months after transplant, after which prevalence gradually decreases (though SCR may persist for longer than one year in some patients).38 Presence of these acute lesion, even in cases with minimal inflammation, is consistently associated to the occurrence of chronic lesions such as interstitial fibrosis and tubular atrophy (IF/TA)36,39-41 and to a decrease in long-term graft survival, as recently seen in patients with SCR lesions two weeks after transplant followed up for 10 years.42 Once established, IF/TA progresses rapidly during the first months, and despite being clinically silent at the start,36,43,44 it is also related to a poorer kidney function and to<br />long-term graft loss45,46 even when detected early at 6 months of transplant.47 In fact, the predictive value of IF/TA is independent from other classical markers such as serum creatinine, proteinuria, or acute rejection.48<br /><br />In this setting, there has been recently an increasing interest in detection of lesion patterns in biopsies that would help predict transplant evolution better and earlier than separate lesion assessment. The combination of IF/TA and vascular damage has been shown to be significantly associated to a poorer 10-year graft survival as compared to IF/AT alone,49 and similar results were seen at 5 years in patients with IF/TA lesions and transplant glomerulopathy.50 Moreover, the combination of acute and chronic lesions also predicts for poorer long-term results, so that IF/TA has a particularly poorer prognosis when it is concomitantly associated to the presence of SCR.41,50,51 In fact, certain lesion patterns found in protocol biopsies within 6 months of transplant, such as the presence of IF/TA plus transplant vasculopathy or IF/TA plus SCR, have shown no less sensitivity and specificity for predicting 7-year graft viability than classical markers such as acute rejection or kidney function.3<br /><br />It is also particular interesting to note that protocol biopsies could have a significant role for improving graft prognosis. There are two reports on this regard that, despite their methodological limitations, support this statement.<br /><br />The first report refers to a study where protocol biopsies were performed 1, 2, 3, 6, and 12 months after transplant.<br />In this study, Rush et al found that detection and early treatment of SCR with corticosteroid boluses resulted in a<br />decreased progression of lesions at 6 months and a better kidney function at 2 years as compared to the control<br />group.52 In the second study, Buehrig et al reported that early detection of nephropathy by the polyomavirus using<br />protocol biopsies within one year of transplant allowed for modifying immunosuppression in early disease stages. At 6 months, graft survival and function in these patients were significantly superior to patients in whom the disease was detected late when a diagnostic biopsy was performed for kidney function impairment.53<br /><br />In conclusion, the biopsy not only represents the best alternative for diagnostic evaluation of renal graft lesions, but is also a good tool for prognostic and viability assessment of the graft. Based on the available evidence, it has been stated that protocol biopsies could be considered as a surrogate marker for graft survival,54 and several groups of<br />researchers are currently focusing their efforts on the search for different lesion patterns, as well as new quantitative parameters for assessing these biopsies, that would improve their predictive value.3 Finally, the significant value of protocol biopsies as secondary endpoint in the setting of clinical trials should not be forgotten. A remarkable experience in this field has already been obtained in several studies intended to describe potential differences in the impact of the different immunosuppressive treatments on renal histology.55-58<br /><br />RECOMMENDATIONS FOR PERFORMING DONOR BIOPSIES (table I)<br /><br />Indications<br /><br />Definite indication<br />In recent years, the growing disparity between the number of patients in a waiting list for receiving a kidney transplant and the number of grafts available has prompted the need for expanding the criteria for considering a kidney adequate to be transplanted (59). In 2001, the UNOS (United Network for Organ Sharing) defined expanded criteria donors (ECD&" "pdfFichero" => "P-E-S-A384-EN.pdf" "tienePdf" => true "PalabrasClave" => array:2 [ "es" => array:3 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec440743" "palabras" => array:1 [ 0 => "aspectos técnicos biopsia" ] ] 1 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec440745" "palabras" => array:1 [ 0 => "Biopsia injerto renal" ] ] 2 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec440747" "palabras" => array:1 [ 0 => "indicaciones de biopsia" ] ] ] "en" => array:3 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec440744" "palabras" => array:1 [ 0 => "technical aspects of graft biopsy" ] ] 1 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec440746" "palabras" => array:1 [ 0 => "kidney graft biopsy" ] ] 2 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec440748" "palabras" => array:1 [ 0 => "indications of graft biopsy" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "es" => array:1 [ "resumen" => "A pesar de la importante actividad trasplantadora en España (1) lo cierto es que todavía no se ha desarrollado en nuestro país un consenso sobre las situaciones clínicas en las que sería recomendable realizar una biopsia diagnóstica, ni sobre cómo mejorar en la práctica clínica el uso de biopsias de protocolo o de biopsias del donante." ] "en" => array:1 [ "resumen" => "Despite the significant transplant activity in Spain,1 no consensus has been reached yet in our country about the clinical situations in which a diagnostic biopsy would be recommended, or about how use of protocol or donor biopsies may be improved in clinical practice. Thus, an overall view detects a high heterogeneity between the different centres and even certain practices that may be considered inadequate." ] ] "bibliografia" => array:2 [ "titulo" => "Bibliography" "seccion" => array:1 [ 0 => array:1 [ "bibliografiaReferencia" => array:87 [ 0 => array:3 [ "identificador" => "bib1" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Valentin MO, Garrido G, Martin Escobar E, de la Rosa G, Mahillo B, Dominguez-Gil B, et al. [Donation and kidney transplantation activity in Spain. 2006]. Nefrologia. 2007;27(4):434-8." "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] 1 => array:3 [ "identificador" => "bib2" "etiqueta" => "2" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "El-Husseini A, Sabry A, Zahran A, Shoker A. Can donor implantation renal biopsy predict long-term renal allograft outcome? 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Am J Transplant. 2007 Dec;7(12):2739-47. <a href="http://www.ncbi.nlm.nih.gov/pubmed/17949456" target="_blank">[Pubmed]</a>" "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] 82 => array:3 [ "identificador" => "bib83" "etiqueta" => "83" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Kayler LK, Lakkis FG, Morgan C, Basu A, Blisard D, Tan HP, et al. Acute cellular rejection with CD20-positive lymphoid clusters in kidney transplant patients following lymphocyte depletion. Am J Transplant. 2007 Apr;7(4):949-54. <a href="http://www.ncbi.nlm.nih.gov/pubmed/17331114" target="_blank">[Pubmed]</a>" "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] 83 => array:3 [ "identificador" => "bib84" "etiqueta" => "84" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Grimbert P, Mansour H, Desvaux D, Roudot-Thoraval F, Audard V, Dahan K, et al. The regulatory/cytotoxic graft-infiltrating T cells differentiate renal allograft borderline change from acute rejection. Transplantation. 2007 Feb 15;83(3):341-6." "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] 84 => array:3 [ "identificador" => "bib85" "etiqueta" => "85" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Aita K, Yamaguchi Y, Horita S, Ohno M, Tanabe K, Fuchinoue S, et al. Thickening of the peritubular capillary basement membrane is a useful diagnostic marker of chronic rejection in renal allografts. Am J Transplant. 2007 Apr;7(4):923-9. <a href="http://www.ncbi.nlm.nih.gov/pubmed/17391134" target="_blank">[Pubmed]</a>" "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] 85 => array:3 [ "identificador" => "bib86" "etiqueta" => "86" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Ivanyi B, Kemeny E, Szederkenyi E, Marofka F, Szenohradszky P. The value of electron microscopy in the diagnosis of chronic renal allograft rejection. Mod Pathol. 2001 Dec;14(12):1200-8. <a href="http://www.ncbi.nlm.nih.gov/pubmed/11743041" target="_blank">[Pubmed]</a>" "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] 86 => array:3 [ "identificador" => "bib87" "etiqueta" => "87" "referencia" => array:1 [ 0 => array:3 [ "referenciaCompleta" => "Oberbauer R, Segoloni G, Campistol JM, Kreis H, Mota A, Lawen J, et al. Early cyclosporine withdrawal from a sirolimus-based regimen results in better renal allograft survival and renal function at 48 months after transplantation. Transpl Int. 2005 Jan;18(1):22-8. <a href="http://www.ncbi.nlm.nih.gov/pubmed/15612979" target="_blank">[Pubmed]</a>" "contribucion" => array:1 [ 0 => null ] "host" => array:1 [ 0 => null ] ] ] ] ] ] ] ] ] "idiomaDefecto" => "en" "url" => "/20132514/0000002800000004/v0_201502091636/X2013251408005392/v0_201502091636/en/main.assets" "Apartado" => array:4 [ "identificador" => "35446" "tipo" => "SECCION" "en" => array:2 [ "titulo" => "Special Originals" "idiomaDefecto" => true ] "idiomaDefecto" => "en" ] "PDF" => "https://static.elsevier.es/multimedia/20132514/0000002800000004/v0_201502091636/X2013251408005392/v0_201502091636/en/P-E-S-A384-EN.pdf?idApp=UINPBA000064&text.app=https://revistanefrologia.com/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/X2013251408005392?idApp=UINPBA000064" ]
| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 10 | 21 | 31 |
| 2024 October | 65 | 104 | 169 |
| 2024 September | 61 | 83 | 144 |
| 2024 August | 71 | 62 | 133 |
| 2024 July | 81 | 60 | 141 |
| 2024 June | 94 | 83 | 177 |
| 2024 May | 97 | 67 | 164 |
| 2024 April | 101 | 54 | 155 |
| 2024 March | 69 | 35 | 104 |
| 2024 February | 63 | 53 | 116 |
| 2024 January | 68 | 33 | 101 |
| 2023 December | 60 | 38 | 98 |
| 2023 November | 82 | 53 | 135 |
| 2023 October | 77 | 52 | 129 |
| 2023 September | 74 | 56 | 130 |
| 2023 August | 77 | 44 | 121 |
| 2023 July | 91 | 45 | 136 |
| 2023 June | 75 | 38 | 113 |
| 2023 May | 83 | 53 | 136 |
| 2023 April | 44 | 24 | 68 |
| 2023 March | 87 | 18 | 105 |
| 2023 February | 53 | 30 | 83 |
| 2023 January | 50 | 35 | 85 |
| 2022 December | 81 | 42 | 123 |
| 2022 November | 41 | 68 | 109 |
| 2022 October | 69 | 56 | 125 |
| 2022 September | 62 | 66 | 128 |
| 2022 August | 53 | 57 | 110 |
| 2022 July | 58 | 60 | 118 |
| 2022 June | 58 | 42 | 100 |
| 2022 May | 78 | 52 | 130 |
| 2022 April | 57 | 59 | 116 |
| 2022 March | 63 | 68 | 131 |
| 2022 February | 48 | 50 | 98 |
| 2022 January | 67 | 48 | 115 |
| 2021 December | 65 | 49 | 114 |
| 2021 November | 71 | 44 | 115 |
| 2021 October | 79 | 50 | 129 |
| 2021 September | 44 | 47 | 91 |
| 2021 August | 58 | 51 | 109 |
| 2021 July | 56 | 48 | 104 |
| 2021 June | 77 | 47 | 124 |
| 2021 May | 68 | 58 | 126 |
| 2021 April | 118 | 112 | 230 |
| 2021 March | 85 | 87 | 172 |
| 2021 February | 114 | 64 | 178 |
| 2021 January | 66 | 40 | 106 |
| 2020 December | 35 | 38 | 73 |
| 2020 November | 45 | 20 | 65 |
| 2020 October | 36 | 29 | 65 |
| 2020 September | 36 | 15 | 51 |
| 2020 August | 43 | 21 | 64 |
| 2020 July | 60 | 27 | 87 |
| 2020 June | 36 | 22 | 58 |
| 2020 May | 45 | 18 | 63 |
| 2020 April | 39 | 24 | 63 |
| 2020 March | 42 | 23 | 65 |
| 2020 February | 65 | 36 | 101 |
| 2020 January | 51 | 35 | 86 |
| 2019 December | 64 | 40 | 104 |
| 2019 November | 60 | 21 | 81 |
| 2019 October | 35 | 17 | 52 |
| 2019 September | 71 | 38 | 109 |
| 2019 August | 40 | 12 | 52 |
| 2019 July | 64 | 29 | 93 |
| 2019 June | 47 | 27 | 74 |
| 2019 May | 57 | 22 | 79 |
| 2019 April | 105 | 57 | 162 |
| 2019 March | 48 | 32 | 80 |
| 2019 February | 23 | 27 | 50 |
| 2019 January | 40 | 27 | 67 |
| 2018 December | 116 | 53 | 169 |
| 2018 November | 236 | 86 | 322 |
| 2018 October | 141 | 84 | 225 |
| 2018 September | 77 | 59 | 136 |
| 2018 August | 62 | 59 | 121 |
| 2018 July | 50 | 47 | 97 |
| 2018 June | 47 | 34 | 81 |
| 2018 May | 43 | 41 | 84 |
| 2018 April | 76 | 39 | 115 |
| 2018 March | 27 | 33 | 60 |
| 2018 February | 36 | 22 | 58 |
| 2018 January | 37 | 36 | 73 |
| 2017 December | 38 | 21 | 59 |
| 2017 November | 39 | 35 | 74 |
| 2017 October | 37 | 14 | 51 |
| 2017 September | 22 | 19 | 41 |
| 2017 August | 25 | 28 | 53 |
| 2017 July | 29 | 41 | 70 |
| 2017 June | 33 | 47 | 80 |
| 2017 May | 37 | 31 | 68 |
| 2017 April | 33 | 23 | 56 |
| 2017 March | 25 | 15 | 40 |
| 2017 February | 16 | 6 | 22 |
| 2017 January | 16 | 27 | 43 |
| 2016 December | 53 | 13 | 66 |
| 2016 November | 46 | 15 | 61 |
| 2016 October | 66 | 12 | 78 |
| 2016 September | 101 | 18 | 119 |
| 2016 August | 167 | 21 | 188 |
| 2016 July | 178 | 9 | 187 |
| 2016 June | 124 | 0 | 124 |
| 2016 May | 134 | 0 | 134 |
| 2016 April | 106 | 0 | 106 |
| 2016 March | 99 | 0 | 99 |
| 2016 February | 125 | 0 | 125 |
| 2016 January | 108 | 0 | 108 |
| 2015 December | 102 | 0 | 102 |
| 2015 November | 101 | 0 | 101 |
| 2015 October | 86 | 0 | 86 |
| 2015 September | 80 | 0 | 80 |
| 2015 August | 85 | 0 | 85 |
| 2015 July | 80 | 0 | 80 |
| 2015 June | 34 | 0 | 34 |
| 2015 May | 55 | 0 | 55 |
| 2015 April | 5 | 0 | 5 |
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