Sánchez Salguero et al. Irish Veterinary Journal (2019) 72:14 https://doi.org/10.1186/s13620-019-0152-6 SHORT REPORT Open Access Heart to spine measurements to detect left atrial enlargement in dogs with mitral insufficiency Xavier Sánchez Salguero1, David Prandi2,3, Francisco Llabrés-Díaz4, Edgar G. Manzanilla5,6* , Llorenç Badiella7 and Claudio Bussadori8 Abstract Background: Radiography is useful to determine left atrial (LA) size when echocardiography is not available. Recently, the authors have described Radiographic Left Atrial Dimension (RLAD) as a new radiographic measurement to assess LA size. The objective of this study was to assess the clinical usefulness of 2 new radiographic measurements to detect and quantify left atrial enlargement (LAE) compared to RLAD and using left atrium to aortic root (LA/Ao) ratio as gold standard. These new measurements, bronchus-to-spine (Br-Spine) and RLAD-to-spine (RLAD-Spine) may be more precise in cases were LA boundaries are not well defined. Fifty dogs, 25 with and 25 without LAE were recruited. Reference LA/Ao ratio was assessed by 2D echocardiography and LAE was considered if LA/Ao > 1.6. Br-spine was measured as a straight vertical line from the main stem bronchus to the ventral border of the vertebra situated immediately dorsal to the heart base. RLAD-Spine was measured from RLAD endpoint perpendicularly to spine. The correlation of RLAD, Br-Spine and RLAD-Spine methods with LA/Ao and their sensitivity and specificity for detecting LAE were calculated. Receiver Operating Characteristic (ROC) curves were used to estimate the optimal cut-off for each method. Results: Correlations between Br-Spine, RLAD-Spine, RLAD and LA/Ao ratio were − 0.66, − 0.76 and 0.89 respectively (P < 0.001). Sensitivity at the optimal cut-off values for detecting LAE were 32.0, 64.0 and 96.0%, respectively. Specificity was 96.0% in all cases. Conclusion: Br-Spine and RLAD-Spine were less sensitive radiographic measurements than RLAD in detecting LAE in dogs. Both Br-Spine and RLAD-Spine may not be good alternatives to RLAD. Keywords: Dog, Left atrial size, Mitral valve disease, Radiographic measurement, RLAD Background clinicians and offers additional information such as pres- Several echocardiographic methods have been published ence of pulmonary oedema. The most frequently used to measure left atrial (LA) dimension [1–4] and the most radiographic sign of LAE is a bulging soft tissue opacity commonly used is the left atrium-to-aorta ratio (LA/Ao) located dorso-caudally to the carina on the latero-lateral [1, 4, 5]. However, echocardiography is technically chal- view [10]. A new measurement to evaluate radiographic lenging and not universally available. Radiography is a left atrial dimension (RLAD) has been recently described simple and useful tool to detect left atrial enlargement [9]. RLAD demonstrated good correlation with LA/Ao (LAE) [6–9]; it is available virtually to all veterinary ratio as well as high sensitivity and specificity to detect LAE [9] in dogs affected by mitral insufficiency. * Correspondence: egmanzanilla@gmail.com; Identifying the exact location of the LA roof, which is edgar.garciamanzanilla@teagasc.ie needed for RLAD, is straightforward in cases with mod- 5 Animal and Grassland Research Centre, Teagasc, Moorepark, Fermoy, erate to severe LAE. However, it is difficult in some nor- Republic of Ireland 6 School of Veterinary Medicine, University College Dublin, Belfield, Republic mal dogs as left and right main stem bronchi, main of Ireland pulmonary veins and the bronchial and vascular trees Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Sánchez Salguero et al. Irish Veterinary Journal (2019) 72:14 Page 2 of 4 are superimposed to each other in this area [11]. New radiographic measurements of LAE free of this superim- position should be explored. In this study we hypothe- sized that bronchus-to-spine (Br-Spine) measurement could help in evaluating heart enlargement and measur- ing the distance between RLAD endpoint and the neigh- bouring vertebrae (RLAD-Spine) could help in evaluating the presence of LAE. Thus, the objective of the study was to test the clinical value of these two radiographic measurements in cases with LAE using LA/ Ao ratio as a reference. Methods A total of 50 client-owned dogs were prospectively in- cluded in this study in 2 groups: Group A (control group) composed of 25 healthy dogs without LAE and Fig. 1 Right lateral thoracic view. The vertebral Heart Size (VHS), Group B, composed of 25 dogs diagnosed with mitral in- long (L) and short (S) cardiac axes are shown. VHS is expressed as total units of vertebral length: 10.2v in this particular case. Bronchus- sufficiency and LAE. Dogs were assigned to one of two to-spine measurement (dark blue line) and the distance between groups according to the absence (Group A) or presence the cranio-ventral and caudo-ventral surface of the vertebrae dorsal (Group B) of LAE defined as La/Ao ratio > 1.6 [4, 6, 8]. All to the heart base (red line) were shown. (L), (S) and Br-Spine dogs had a complete radiographic and echocardiographic measurements were repositioned parallel to the long axis of the examination, complete clinical evaluation including phys- thoracic vertebrae from the cranial edge of the fourth thoracic vertebra (T4). Br-Spine was thus expressed as total units of vertebral ical exam, complete blood count and biochemistry panel length: 1.0v within the same day. Normal dogs were those considered so according to the history, physical, radiographic and echocardiographic examinations. A mitral valve disease The RLAD was measured as previously described [9]. (MVD) diagnosis was based on the presence of a typical The RLAD-Spine was measured perpendicularly to the systolic mitral regurgitation murmur and alterations on vertebrae in a straight line from the endpoint of RLAD the echocardiographic examination (LA and left ventricu- to the ventral aspect of the vertebral column. The dorsal lar enlargement, diffuse nodular thickening of the mitral reference point was defined as the intersection point be- leaflets and Doppler evidence of disturbed flow within the tween the vertical measurement from the left atrial roof LA during systole). Any dog with cardiac disease either and an imaginary line between the cranio-ventral and with a sole diagnosis different from MVD or any disease caudo-ventral surface of the vertebrae dorsal to LA, usu- complex including MVD and another condition were ex- ally T6 (Fig. 2). Br-Spine, RLAD and RLAD-Spine mea- cluded from the study. Dogs with pulmonary hypertension surements were repositioned parallel to the long axis of or radiographic changes compatible with left sided con- the thoracic vertebrae from the cranial edge of T4 and gestive failure were also excluded. expressed as total units of vertebral length to the nearest All radiographic measurements were obtained by the 0.1 vertebra (v). For consistency, a value of one included same observer (XS) using Microsoft Office Power point the length of a vertebral body and the width of the caud- 2007 (Microsoft Corporation, USA) in a digital latero-lateral ally positioned intervertebral disc. thoracic radiograph with the dog in right lateral recum- A complete transthoracic echocardiographic examin- bency. The observer was blinded to all patient details and all ation was performed in all dogs by the same board- measurements were performed in a randomised fashion. certified veterinary cardiologist according to the Ameri- The Br-Spine was measured as the distance measured can Society of Echocardiography standards and guide- in a straight vertical line from the ventral border of the lines and other published recommendations [12] as left cranial lung lobe bronchus (main stem bronchus), described in earlier reports [9]. from the same location as VHS (vertebral heart size), to the Statistical analysis was performed using SAS 9.4 (Cary, ventral border of the vertebra situated immediately dorsal NC, USA). Normality of data was tested using Shapiro to the heart base. The dorsal reference point was defined as Wilk test and visual methods. Means between groups the intersection point between the vertical measurement were compared using t-test. The association between from the heart base and an imaginary line between the measurements was obtained by means of Spearman’s cranio-ventral and caudo-ventral surface of the vertebrae correlation. The accuracy of each test was measured by dorsal to the heart base [5], usually T5 (Fig. 1). means of empirical Receiver Operating Characteristic (ROC) Sánchez Salguero et al. Irish Veterinary Journal (2019) 72:14 Page 3 of 4 The ROC curves showed that RLAD optimal cut-off value was 1.8v, whereas Br-Spine and RLAD-Spine opti- mal cut-off values were 1.0v and 0.8v, respectively. Thus, using these reference values could decrease the overlap between normal dogs and dogs with LAE. Sensitivity and specificity were calculated based on these optimal cut-off values. Sensitivity to detect LAE was higher for RLAD (96%) than for Br-Spine (32%) and RLAD-Spine (64%). A possible explanation could be a greater effect that the dog’s thoracic conformation could have on these 2 new radiographic measurements when compared heart-based measures like RLAD. In addition, several technical factors can affect these 2 new radiographic measurements; the respiratory phase, variations in the Fig. 2 Right lateral thoracic radiograph. Vertebral Heart Size (VHS), conformation of individual dogs of the same breed and long (L) and short (S) cardiac axes are shown. VHS is expressed as slight inconsistencies in positioning for radiography can total units of vertebral length: 12.2v. Radiographic left atrial all decrease or increase the heart-to-spine distance. Both, dimension (RLAD) is shown (white line). RLAD to spine RLAD, Br-Spine and RLAD-Spine showed the same speci- measurement (yellow line) and the distance between the cranio- ficity to detect LAE (96%). These results would likely not ventral and caudo-ventral surface of the vertebrae dorsal to the heart base (blue line) are shown. (L), (S) and RLAD-Spine were be so high in a clinical population of dogs with causes of repositioned parallel to the long axis of the thoracic vertebrae from cardiomegaly other than left atrial enlargement. the cranial edge of the fourth thoracic vertebra (T4). RLAD-Spine was Although differences between AUC for the different thus expressed as total units of vertebral length: 1.1v in this case measurements were not significant, the AUCs were 0.85 (95% CI = 0.744, 0.957) for Br-Spine, 0.91 (95% CI = 0.834, curve, the area under the curve (AUC) and their confidence 0.995) for RLAD-Spine and 0.99 (95% CI = 0.954, 1.000) for intervals. AUC curves were compared using Delong’s RLAD. This higher AUC for RLAD indicates a superior diag- method. The optimal cut-off value that jointly maximized nostic value compared to Br-Spine and RLAD-spine. sensitivity and specificity for each test was determined using The number of patients, the applicability of the the Youden index. Sensitivity and specificity and their confi- methods on different thoracic conformations and the ex- dence intervals were computed at the optimal cut-off point. clusion of dogs with congestive heart failure are the Alpha level for determination of significance was 0.05. main limitations of this study. Conclusion Results and discussion Br-Spine and RLAD-Spine, new radiographic measure- A total of 50 dogs were prospectively included in this ments, are less sensitive than RLAD in detecting LAE in study, 25 dogs in the group of healthy dogs (18 males, 7 dogs. When LA boundaries are radiographically well vi- females; aged 1–7 years; weighing 4–20 kg) and 25 dogs sualized (in most cases, especially in dogs with moderate in the group with LAE (14 males, 11 females; aged 6–10 or severe LAE) we still propose RLAD as the best years; weighing 4.8–21.4 kg). Breeds included mainly method of detecting and quantifying LAE based on its mixed breed dogs (n = 46) and pure breeds included: high sensitivity and sensibility in detecting LAE, as well French Bulldog, Pug, Cavalier King Charles Spaniel and as its high correlation with LA/Ao ratio and high AUC. Pekingese (n = 1 each). Group B showed greater values Abbreviations (mean ± SD) for RLAD (A = 1.4 ± 0.23, B = 2.62 ± 0.55) AUC: Area under the curve; Br-Spine: Bronchus-to-spine; LA: Left atrial; LA/ and LA/Ao (A = 1.33 ± 0.13, B = 2.52 ± 0.56) and lower for Ao: Left atrium-to-aorta ratio; LAE: Left atrial enlargement; MVD: Mitral valve Br-Spine (A = 1.58 ± 0.32, B = 1.10 ± 0.34), RLAD-Spine disease; RLAD: Radiographic left atrial dimension; RLAD-Spine: RLAD-to-spine; ROC: Receiver operating characteristic; v: Vertebrae (unit of length); (A = 1.44 ± 0.35, B = 0.57 ± 0.48; P < 0.05 in all cases). VHS: Vertebral heart size Correlation between RLAD and LA/Ao ratio was good (r = 0.89; P < 0.001) as shown in a previous study [9]. For Acknowledgements The authors thank Oriol Domènech for his collaboration and involvement Br-Spine and RLAD-Spine the correlation coefficient performing the Transthoracic Echocardiogaphies. Yvonne Espada Gerlach with LA/Ao ratio (r = − 0.66 and − 0.76 respectively; P < from the UAB Veterinary Teaching Hospital for her help in obtaining the 0.001) was lower than for RLAD. Br-Spine could become radiographs. a clinically relevant alternative when RLAD is difficult to Authors’ contributions measure, however, based on this data it should not be DP, XSS, FLD and CB designed the study and collaborated in the collection used as diagnostic index in a general population. of data. XSS and DP analyzed and interpreted the patient data. LB and EGM Sánchez Salguero et al. Irish Veterinary Journal (2019) 72:14 Page 4 of 4 carried out the statistical analysis. FLD, CB, XSS, DP, LB and EGM wrote the manuscript. All authors participated in reviewing the manuscript, and read, and approved, the final manuscript. Funding This work did not have any other funding than the author’s own work. Availability of data and materials The datasets used and/or analysed during the current study available from the corresponding author on reasonable request. Ethics approval and consent to participate The study was approved by the Universitat Autònoma de Barcelona ethics committee (CEEAH 1160). Owner consent was obtained for all dogs enrolled. Consent for publication Not applicable. Competing interests The authors declare that they have no competing interests. Author details 1 Animal Science Department, Escola Tècnica Superior d’Enginyeria Agrària, Universitat de Lleida, Lleida, Spain. 2Betulia Veterinary Clinic, Barcelona, Spain. 3 Universitat Autònoma de Barcelona, Bellaterra, Barcelona, Spain. 4Royal Veterinary College, Hawkshead Lane, Hatfield, Hertfordshire, UK. 5Animal and Grassland Research Centre, Teagasc, Moorepark, Fermoy, Republic of Ireland. 6 School of Veterinary Medicine, University College Dublin, Belfield, Republic of Ireland. 7Servei d’Estadística Aplicada, Universitat Autònoma de Barcelona, Bellaterra, Barcelona, Spain. 8Clínica Veterinaria Gran Sasso, Milano, Italy. Received: 17 June 2019 Accepted: 15 November 2019 References 1. Hansson K, Häggström J, Kvart C, et al. Left atrial to aortic root indices using two- dimensional and M-mode echocardiography in Cavalier King Charles spaniels with and without left atrial enlargement. Vet Radiol Ultrasound. 2002;43:568–75. 2. Boon J, Wingfield WE, Miller CW. Echocardiographic indices in the normal dog. Vet Radiol. 1983;24:214–21. 3. Lombard CW. Normal values of the canine M-mode echocardiogram. Am J Vet Res. 1984;45:2015–8. 4. Rishniw M, Erb HN. Evaluation of four 2-dimensional echocardiographic methods of assessing left artrial size in dogs. J Vet Intern Med. 2000;14:429–35. 5. O’Grady MR, Bonagura JD, Powers JD, et al. Quantitative cross-sectional echocardiography in the normal dog. Vet Radiol. 1986;27:34–49. 6. Kittleson MD. Radiography of the cardiovascular system. In: Kittleson MD, Kienle RD, editors. Small animal cardiovascular medicine. St. Louis: Mosby; 1998. p. 47–71. 7. Malcolm EL, Visser LC, Phillips KL, et al. Diagnostic value of vertebral left atrial size as determined from thoracic radiographs for assessment of left atrial size in dogs with myxomatous mitral valve disease. J Am Vet Med Assoc. 2018;253:1038–45. 8. Buchanan JW. Vertebral scale system to measure heart size in radiographs. Vet Clin North Am Small Anim Pract. 2000;30:379–93. 9. Sánchez X, Prandi D, Llabrés-Díaz F, et al. A radiographic measurement of left atrial size in dogs. Ir Vet J. 2018;71:25. 10. Hansson K, Häggström J, Kvart C, et al. Reader performance in radiographic diagnosis of signs of mitral regurgitation in cavalier King Charles spaniels. J Small Anim Pract. 2009;50:44–53. 11. Johnson V, Hansson K, Maï W, et al. The heart and major vessels. In: Schwarz T, Johnson V, editors. BSAVA manual of canine and feline thoracic imaging. 1st ed. Quedgeley: British Small Animal Veterinary Association; 2008. p. 86–176. 12. Thomas WP, Gaber CE, Jacobs GJ, et al. Recommendations for standards in transthoracic two-dimensional echocardiography in the dog and cat. Echocardiography Committee of the Specialty of Cardiology, American College of Veterinary Internal Medicine. J Vet Intern Med. 1993;7:247–52. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.