Letter to the Editor
Preganglionic or postganglionic efferent pupillary defect? Clinical versus neuroimaging diagnosis
Defecto pupilar eferente, ¿preganglionar o posganglionar? Diagnóstico clínico vs neuroimagen
C.A. Arciniegas-Perasso
, R.A. Díaz-Cespedes, L. Manfreda-Domínguez, D. Toro-Giraldo
Corresponding author
Servicio de Oftalmología, Sección de Neuro-Oftalmología, Hospital Clínico Universitario de Valencia, Valencia, Spain
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Diagnóstico clínico vs. neuroimagen" "tienePdf" => "es" "tieneTextoCompleto" => "es" "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "66" "paginaFinal" => "68" ] ] "titulosAlternativos" => array:1 [ "en" => array:1 [ "titulo" => "Preganglionic or postganglionic efferent pupillary defect? Clinical versus neuroimaging diagnosis" ] ] "contieneTextoCompleto" => array:1 [ "es" => true ] "contienePdf" => array:1 [ "es" => true ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figura 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 593 "Ancho" => 1300 "Tamanyo" => 186937 ] ] "descripcion" => array:1 [ "es" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Exploración clínica: disociación luz-aproximación. a) Anisocoria por midriasis OD. b) Respuesta de aproximación conservada (y tónica en OD). c) Respuesta a la instilación de pilocarpina 0,125% (OD, miosis por hipersensibilidad colinérgica por denervación; OI, indiferente). d) Ausencia de miosis a la aducción del OD (se descarta reinervación aberrante del MOC).</p>" ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "C.A. 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Frontal ventricles (dotted arrow) are small, and the frontal parenchyma features small hyperintense images (arrow) that could be associated with arterial hypertension. The third ventricle and occipital horns are dilated (CC). b) Axial FLAIR sequence. The third ventricle appears dilated (arrow) and the upper part of the corpus callosum is very thin. c) T1-weighted sagittal slice: the genu and trunk of the corpus callosum (arrow) seem faint. The fourth ventricle is normal-sized. d) T2-weighted axial slice. Frontal sulci are much smaller than cortical sulci on the posterior part of the brain.</p>" ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "E.L. Bartolomé, J.C. Cottura, R. Britos Frescia, R.O. Domínguez" "autores" => array:4 [ 0 => array:2 [ "nombre" => "E.L." "apellidos" => "Bartolomé" ] 1 => array:2 [ "nombre" => "J.C." "apellidos" => "Cottura" ] 2 => array:2 [ "nombre" => "R." "apellidos" => "Britos Frescia" ] 3 => array:2 [ "nombre" => "R.O." 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The dividing line shown in the picture was added intentionally to this figure; it is not visible during the test. (b) Our patient's performance 127 days after head trauma. The image shows a marked tendency to place the cubes on the right side of the board. (c) Performance 10 days after the previous testing session.</p>" ] ] ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "A. García-Molina, J. García-Férnandez, C. Aparicio-López, T. Roig-Rovira" "autores" => array:4 [ 0 => array:2 [ "nombre" => "A." "apellidos" => "García-Molina" ] 1 => array:2 [ "nombre" => "J." "apellidos" => "García-Férnandez" ] 2 => array:2 [ "nombre" => "C." "apellidos" => "Aparicio-López" ] 3 => array:2 [ "nombre" => "T." 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Clinical versus neuroimaging diagnosis" "tieneTextoCompleto" => true "saludo" => "Dear Editor:" "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "66" "paginaFinal" => "68" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "C.A. Arciniegas-Perasso, R.A. Díaz-Cespedes, L. Manfreda-Domínguez, D. Toro-Giraldo" "autores" => array:4 [ 0 => array:4 [ "nombre" => "C.A." "apellidos" => "Arciniegas-Perasso" "email" => array:1 [ 0 => "drcalarpe@gmail.com" ] "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0005" ] ] ] 1 => array:2 [ "nombre" => "R.A." "apellidos" => "Díaz-Cespedes" ] 2 => array:2 [ "nombre" => "L." "apellidos" => "Manfreda-Domínguez" ] 3 => array:2 [ "nombre" => "D." "apellidos" => "Toro-Giraldo" ] ] "afiliaciones" => array:1 [ 0 => array:2 [ "entidad" => "Servicio de Oftalmología, Sección de Neuro-Oftalmología, Hospital Clínico Universitario de Valencia, Valencia, Spain" "identificador" => "aff0005" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Defecto pupilar eferente, ¿preganglionar o posganglionar? Diagnóstico clínico vs neuroimagen" ] ] "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" => 593 "Ancho" => 1300 "Tamanyo" => 202324 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Clinical examination: light-near dissociation. a) Anisocoria due to mydriatic right eye. b) Intact near-response (tonic response in the RE). c) Response to instillation of 0.125% pilocarpine (RE, mydriasis caused by cholinergic denervation supersensitivity; LE, intact). d) No miosis with RE adduction (aberrant reinnervation of the OMN is ruled out).</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><p id="par0005" class="elsevierStylePara elsevierViewall">Tonic pupil syndrome is a disorder secondary to lesion to the parasympathetic pathway at the ganglionic or postganglionic level.<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">1</span></a> Manifestations include mydriasis with abolished or minimal pupillary reflex (with vermiform movements of the iris due to contraction of normally innervated segments of the iris sphincter, only visible with a slit lamp). Constriction with near effort is present (light-near dissociation) and results from subsequent aberrant reinnervation of the iris sphincter by fibres which were originally destined for the ciliary muscle. This reaction is tonic, that is, slow and sustained. Furthermore, the syndrome also manifests with cholinergic supersensitivity due to postganglionic denervation.<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">2</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">The origin of the injury may be local (viral ciliary ganglionitis, open or closed trauma, or orbital tumours), or systemic-neuropathic (syphilis, alcohol abuse, diabetes, amyloidosis, or paraneoplastic alterations). However, its most frequent variant is idiopathic tonic pupil or Adie syndrome,<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">1</span></a> which predominantly affects women (70%) in the third to the fifth decades of life. It is caused by a painless degeneration of the ciliary ganglion and posterior funiculi, sometimes associated with a slow viral infection.<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">3</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">We present the case of a 44-year-old woman with flash blindness and a 7-year history of anisocoria. She reported having suffered head trauma 20 years previously and migraine-like headache that was being treated with flunarizine. The brain magnetic resonance imaging (MRI) ordered by her neurologist showed a kink at the ostium of the right posterior cerebral artery, originating from the carotid system. Since the kink was touching the superior branch of the ipsilateral oculomotor nerve (OMN), doctors suspected compression of the parasympathetic fibres and referred the patient to our department. We examined her and observed anisocoria due to right mydriasis that was more pronounced under photopic conditions. Direct photomotor reflex and consensual response were abolished in the right eye (RE) but remained intact in the left eye (LE). The near response was normal with a tonic reaction. Extrinsic eye movements were normal with no pupillary response to isolated RE adduction. Biomicroscopy results showed an irregular right pupil with minimal sectoral movements in response to light. Instillation of 0.125% pilocarpine into the conjunctival sac provoked miosis in the RE and no response in the LE (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). Bilateral osteotendinous hyporeflexia was also observed. In view of these findings, we proposed the diagnosis of Adie syndrome. Neurologists requested a new gadolinium contrast MRI with thinner slices which revealed displacement of the right OMN without compression (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>). We therefore opted for watchful waiting.</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0020" class="elsevierStylePara elsevierViewall">Pupil abnormalities are examined relatively frequently in neuro-ophthalmology clinics. Finding the lesion location and cause is necessary to assign an accurate diagnosis and subsequently, an appropriate treatment approach. Non-reactive mydriasis may be caused by lesion to the parasympathetic pathway, which can be located at one of several levels: nuclear, preganglionic, ganglionic, and postganglionic.<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">1</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">In this case, differential diagnosis includes lesion to the OMN (preganglionic) and Adie's tonic pupil (ganglionic/postganglionic). Furthermore, differential diagnosis was complicated in this case by results of an imaging scan showing an anatomical variant of the origin of the posterior cerebral artery which might compress parasympathetic fibres of the right OMN. A compression injury to this nerve at the point where it leaves the midbrain may affect parasympathetic fibres, causing mydriasis on the affected side due to a preganglionic defect.<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">3</span></a></p><p id="par0030" class="elsevierStylePara elsevierViewall">However, clinical signs do not indicate compression injury to the OMN at that level. Light-near dissociation, tonic near-response, and vermiform movements of the iris may indicate tonic pupil. Although the supersensitivity test with pilocarpine has traditionally been used to diagnose tonic pupil, positive results are not exclusive to postganglionic parasympathetic lesions but may also be seen with preganglionic lesions.<a class="elsevierStyleCrossRefs" href="#bib0045"><span class="elsevierStyleSup">4,5</span></a></p><p id="par0035" class="elsevierStylePara elsevierViewall">Aberrant reinnervation of the pupil by parasympathetic fibres originally destined for the ciliary muscle depends on the axonal distribution of the ciliary muscle and pupillary sphincter (typically a 30:1 ratio). An abnormal distribution causes light-near dissociation. A similar phenomenon occurs with compressive lesions to the OMN with aberrant reinnervation of the pupillary sphincter by fibres originally destined for the medial rectus muscle. This produces a false light-near dissociation because the pupil responds not only to near objects but also to any eye adduction movement.<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">1</span></a></p><p id="par0040" class="elsevierStylePara elsevierViewall">Clinical findings associated with bilateral osteotendinous hyporeflexia suggest Holmes-Adie syndrome as a diagnosis for our young female patient, after reconsidering the initial diagnosis suggested by MRI findings. Adopting a multidisciplinary approach to these patients helps determine the diagnosis and an appropriate treatment strategy.</p><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0005">Conflicts of interest</span><p id="par0045" class="elsevierStylePara elsevierViewall">The authors have no commercial interests nor have they received any financial support.</p><p id="par0050" class="elsevierStylePara elsevierViewall">The authors declare that this article has not been published or submitted to another journal for publication. They also confirm transfer of the copyright of this article to the Spanish Society of Neurology.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:2 [ 0 => array:2 [ "identificador" => "sec0005" "titulo" => "Conflicts of interest" ] 1 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as: Arciniegas-Perasso CA, Díaz-Cespedes RA, Manfreda-Domínguez L, Toro-Giraldo D. Defecto pupilar eferente, ¿preganglionar o posganglionar? Diagnóstico clínico vs neuroimagen. Neurología. 2016;31:66–68.</p>" ] ] "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" => 593 "Ancho" => 1300 "Tamanyo" => 202324 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Clinical examination: light-near dissociation. a) Anisocoria due to mydriatic right eye. b) Intact near-response (tonic response in the RE). c) Response to instillation of 0.125% pilocarpine (RE, mydriasis caused by cholinergic denervation supersensitivity; LE, intact). d) No miosis with RE adduction (aberrant reinnervation of the OMN is ruled out).</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" => 811 "Ancho" => 1300 "Tamanyo" => 123756 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Brain MRI. a) Zoomed view of coronal slice: we observe oculomotor nerve (OMN) in contact with the right posterior cerebral artery (PCA). b) Zoomed coronal slice: OMN (arrowhead), PCA (arrow).</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:5 [ 0 => array:3 [ "identificador" => "bib0030" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Neuro-ophtalmology" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:1 [ 0 => "J.S. Glaser" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Libro" => array:5 [ "fecha" => "1999" "paginaInicial" => "537" "paginaFinal" => "542" "editorial" => "Raven Press" "editorialLocalizacion" => "Nueva York" ] ] ] ] ] ] 1 => array:3 [ "identificador" => "bib0035" "etiqueta" => "2" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Disorders of pupillary function, accommodation, and lacrimation" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:1 [ 0 => "Aki Kawasaki" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "LibroEditado" => array:4 [ "titulo" => "Walsh & Hoyt's clinical neuro-ophthalmology" "paginaInicial" => "761" "paginaFinal" => "765" "serieFecha" => "2005" ] ] ] ] ] ] 2 => array:3 [ "identificador" => "bib0040" "etiqueta" => "3" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Neuro-ophthalmology. Diagnosis and management" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:3 [ 0 => "G.T. Liu" 1 => "N.J. Volpe" 2 => "S.L. Galleta" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Libro" => array:5 [ "fecha" => "2010" "paginaInicial" => "426" "paginaFinal" => "430" "editorial" => "Saunders-Elsevier" "editorialLocalizacion" => "Philadelphia" ] ] ] ] ] ] 3 => array:3 [ "identificador" => "bib0045" "etiqueta" => "4" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Comparison of cholinergic supersensitivity in third nerve palsy and Adie's syndrome" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "D.M. Jacobson" 1 => "R.A. Vierkant" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:6 [ "tituloSerie" => "J Neuroophthalmol" "fecha" => "1998" "volumen" => "18" "paginaInicial" => "171" "paginaFinal" => "175" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/9736199" "web" => "Medline" ] ] ] ] ] ] ] ] 4 => array:3 [ "identificador" => "bib0050" "etiqueta" => "5" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "A prospective evaluation of cholinergic supersensitivity of the iris sphincter in patients with oculomotor nerve palsies" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:1 [ 0 => "D.M. Jacobson" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:6 [ "tituloSerie" => "Am J Ophthalmol" "fecha" => "1994" "volumen" => "118" "paginaInicial" => "377" "paginaFinal" => "383" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/8085595" "web" => "Medline" ] ] ] ] ] ] ] ] ] ] ] ] ] "idiomaDefecto" => "en" "url" => "/21735808/0000003100000001/v1_201601210907/S2173580815001558/v1_201601210907/en/main.assets" "Apartado" => array:4 [ "identificador" => "9409" "tipo" => "SECCION" "en" => array:2 [ "titulo" => "Letters to the editor" "idiomaDefecto" => true ] "idiomaDefecto" => "en" ] "PDF" => "https://static.elsevier.es/multimedia/21735808/0000003100000001/v1_201601210907/S2173580815001558/v1_201601210907/en/main.pdf?idApp=UINPBA00004N&text.app=https://www.elsevier.es/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S2173580815001558?idApp=UINPBA00004N" ]
| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 6 | 0 | 6 |
| 2024 October | 30 | 7 | 37 |
| 2024 September | 65 | 16 | 81 |
| 2024 August | 32 | 5 | 37 |
| 2024 July | 40 | 3 | 43 |
| 2024 June | 28 | 5 | 33 |
| 2024 May | 15 | 5 | 20 |
| 2024 April | 38 | 8 | 46 |
| 2024 March | 50 | 4 | 54 |
| 2024 February | 75 | 5 | 80 |
| 2024 January | 61 | 4 | 65 |
| 2023 December | 52 | 12 | 64 |
| 2023 November | 62 | 17 | 79 |
| 2023 October | 83 | 22 | 105 |
| 2023 September | 35 | 0 | 35 |
| 2023 August | 49 | 3 | 52 |
| 2023 July | 79 | 11 | 90 |
| 2023 June | 73 | 4 | 77 |
| 2023 May | 109 | 11 | 120 |
| 2023 April | 85 | 4 | 89 |
| 2023 March | 88 | 7 | 95 |
| 2023 February | 72 | 4 | 76 |
| 2023 January | 77 | 7 | 84 |
| 2022 December | 80 | 5 | 85 |
| 2022 November | 85 | 11 | 96 |
| 2022 October | 90 | 52 | 142 |
| 2022 September | 80 | 13 | 93 |
| 2022 August | 54 | 10 | 64 |
| 2022 July | 43 | 11 | 54 |
| 2022 June | 58 | 19 | 77 |
| 2022 May | 49 | 6 | 55 |
| 2022 April | 66 | 7 | 73 |
| 2022 March | 67 | 4 | 71 |
| 2022 February | 93 | 14 | 107 |
| 2022 January | 118 | 10 | 128 |
| 2021 December | 69 | 12 | 81 |
| 2021 November | 68 | 10 | 78 |
| 2021 October | 82 | 13 | 95 |
| 2021 September | 67 | 11 | 78 |
| 2021 August | 42 | 8 | 50 |
| 2021 July | 30 | 12 | 42 |
| 2021 June | 26 | 5 | 31 |
| 2021 May | 42 | 10 | 52 |
| 2021 April | 93 | 9 | 102 |
| 2021 March | 52 | 7 | 59 |
| 2021 February | 26 | 8 | 34 |
| 2021 January | 39 | 13 | 52 |
| 2020 December | 47 | 13 | 60 |
| 2020 November | 43 | 8 | 51 |
| 2020 October | 27 | 4 | 31 |
| 2020 September | 23 | 12 | 35 |
| 2020 August | 28 | 13 | 41 |
| 2020 July | 29 | 6 | 35 |
| 2020 June | 16 | 4 | 20 |
| 2020 May | 36 | 15 | 51 |
| 2020 April | 24 | 4 | 28 |
| 2020 March | 29 | 2 | 31 |
| 2020 February | 31 | 2 | 33 |
| 2020 January | 37 | 3 | 40 |
| 2019 December | 45 | 3 | 48 |
| 2019 November | 27 | 7 | 34 |
| 2019 October | 31 | 5 | 36 |
| 2019 September | 35 | 4 | 39 |
| 2019 August | 18 | 7 | 25 |
| 2019 July | 33 | 17 | 50 |
| 2019 June | 69 | 31 | 100 |
| 2019 May | 168 | 42 | 210 |
| 2019 April | 78 | 24 | 102 |
| 2019 March | 18 | 8 | 26 |
| 2019 February | 25 | 10 | 35 |
| 2019 January | 17 | 7 | 24 |
| 2018 December | 19 | 5 | 24 |
| 2018 November | 28 | 2 | 30 |
| 2018 October | 50 | 1 | 51 |
| 2018 September | 43 | 5 | 48 |
| 2018 August | 12 | 8 | 20 |
| 2018 July | 9 | 4 | 13 |
| 2018 June | 16 | 3 | 19 |
| 2018 May | 19 | 13 | 32 |
| 2018 April | 14 | 3 | 17 |
| 2018 March | 13 | 3 | 16 |
| 2018 February | 16 | 0 | 16 |
| 2018 January | 23 | 0 | 23 |
| 2017 December | 16 | 3 | 19 |
| 2017 November | 14 | 1 | 15 |
| 2017 October | 16 | 0 | 16 |
| 2017 September | 18 | 5 | 23 |
| 2017 August | 26 | 9 | 35 |
| 2017 July | 19 | 6 | 25 |
| 2017 June | 37 | 6 | 43 |
| 2017 May | 31 | 9 | 40 |
| 2017 April | 30 | 4 | 34 |
| 2017 March | 16 | 10 | 26 |
| 2017 February | 49 | 3 | 52 |
| 2017 January | 25 | 2 | 27 |
| 2016 December | 24 | 7 | 31 |
| 2016 November | 21 | 2 | 23 |
| 2016 October | 34 | 4 | 38 |
| 2016 September | 73 | 5 | 78 |
| 2016 August | 56 | 7 | 63 |
| 2016 July | 14 | 1 | 15 |
| 2016 June | 39 | 6 | 45 |
| 2016 May | 50 | 26 | 76 |
| 2016 April | 68 | 29 | 97 |
| 2016 March | 77 | 37 | 114 |
| 2016 February | 70 | 37 | 107 |
| 2016 January | 28 | 9 | 37 |
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