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Background: Respiratory troubles have economic impacts in countries where livestock industry is an important segment of the agricultural sector, as well as these problems may cause significant economic losses for bovine producers. Various practical methods are used to assess diseases that affect the bovine respiratory system. Ultrasonography is a noninvasive tool that has been used frequently in diagnosis of various animal diseases. The present study was designed to establish whether thoracic ultrasonography is a diagnostic tool for detection of respiratory troubles in weaned buffalo and cattle calves, as well as to assess its prognostic value in comparison with clinical respiratory scores. Thirty five (15 buffalo and 20 cattle) calves were included. Twelve (6 buffalo and 6 cattle) clinically healthy calves were enrolled as controls. Results: Based on physical examinations, clinical respiratory scores (CRS), ultrasound lung scores (ULS) and postmortem findings, animals were classified into 4 groups as pulmonary emphysema (n = 8), interstitial pulmonary syndrome (n = 7), bronchopneumonia (n = 12), and pleurisy (n = 8). The mean values of CRS and ULS were significantly higher in diseased calves (P < 0.01). In calves with pulmonary emphysema and interstitial syndrome, thoracic ultrasonography revealed numerous comet-tail artifacts, which varied in numbers and imaging features. Furthermore, variable degrees of pulmonary consolidation with alveolograms and bronchograms were noticed in bronchopneumonic calves. In addition, thick irregular or fragmented pleura with pleural effusions and fibrin shreds were imaged in calves with pleurisy. A weak correlation was calculated between CRS and ULS (r = 0.55, P < 0.01). Hematologically, the counts of white blood cells, activities of aspartate aminotransferase and partial tensions of carbon dioxide were significantly increased in all diseased groups. Serum concentrations of total globulins were higher in claves with bronchopneumonia (P < 0.05). The partial tension of oxygen was decreased in all diseased calves (P < 0.05). Conclusions: Thoracic ultrasonography is a diagnostic tool for various lung troubles and assessment the grade and severity of pulmonary diseases, as well as it can be used as a follow-up tool for evaluating the prognosis of respiratory troubles and monitoring the efficacy of therapies. Keywords: Bronchopneumonia, Calves, Emphysema, Interstitial pulmonary syndrome, Prognosis * Correspondence: firstname.lastname@example.org Internal Veterinary Medicine, Department of Animal Medicine, Faculty of Veterinary Medicine, Assiut University, Assiut 71526, Egypt Full list of author information is available at the end of the article © The Author(s). 2018 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. Hussein et al. Journal of Animal Science and Technology (2018) 60:29 Page 2 of 11 Background of the calves examined. All animals were examined clin- Bovine respiratory disease and diarrhea are the most ically as described previously , which included gen- common diseases affecting the health of dairy calves . eral heath condition and auscultation of the heart and Bovine respiratory diseases are multifactorial, being lungs. Furthermore, rectal temperature and respiratory caused by various viruses, bacteria, and mycoplasma and and heart rates were also recorded. After complete are dependent on predisposing factors as well as man- and thorough clinical examinations, 12 calves (6 buf- agement errors . falo and 6 cattle) were included in this study as con- Respiratory troubles have economic impacts in coun- trols. These animals did not have a history of tries where livestock industry is an important segment previous respiratory illness and their physical examin- of the agricultural sector, as well as these problems may ation was within normal ranges. cause significant economic losses for bovine producers. Respiratory diseases cause an estimated $800 million to Clinical respiratory score (CRS) $900 million annually in economic losses from death, re- Each calf was assessed using respiratory scoring chart duced feed efficiency, and treatment costs [3, 4]. In dairy from the University of Wisconsin . This scoring sys- calves, respiratory diseases were associated with a lower tem based on assessment of five clinical signs including body weight , reduced average daily gain  and a po- rectal temperature, cough, eye and nasal discharge, and tential for increased mortality . In beef calves, medical ear position. Information on nasal discharge, ocular dis- costs attributable to the treatment of respiratory diseases charge, ear and head position, rectal temperature, and are substantial, and the economic impacts of respiratory the frequency of induced or spontaneous coughing were problems on carcass merit and meat quality further in- recorded for each calf. Each clinical sign partitioned into crease the economic costs . four levels of severity (from 0 to 3) as 0 indicates the Various practical methods are used to assess diseases lowest risk of being sick and 3 with the highest risk of that affect the bovine respiratory system, including aus- respiratory disease. It is recommended to treat calves be- cultation, percussion, blood ancillary tests, radiography, cause of high respiratory disease if the CRS is ≥5, and to ultrasonography, and more invasive procedures such as observe calves with scores of 4. Calves with ≤3 are con- pulmonary aspirations and biopsies . Ultrasonography sidered clinically healthy. is a noninvasive tool that has been used frequently in diagnosis of cardiac diseases in buffalo . Further- Thoracic ultrasonography more, ultrasonography is a good choice for imaging and Ultrasonographic examination of the pleura and lungs describing suppurative pneumonia in cattle . was carried out as described previously . In prepar- From the clinical point of view, it is of great interest to ation, the area from 3rd to 12th intercostal spaces (ICS) make a precise diagnosis, as it permits rapid evaluation was clipped, shaved, and scrubbed with alcohol to re- and decision making regarding treatment options and move excess oil, and coupling gel was applied. Thoracic avoids wasteful supportive treatments. In comparison ultrasonography was carried out using 4–6 MHz micro with clinical respiratory score, therefore, thoracic ultra- convex ultrasound transducer (MyLab™One VET, Esaote, sonography was used to assign the spread and evaluate Netherlands), where the frequency was changed accord- the prognostic aspects of respiratory diseases in weaned ing to the examination’s requirement. In both sides, each dairy buffalo and cattle calves. The results were com- lung was examined dorsoventrally with the transducer pared with the clinical and postmortem findings. held parallel to the ribs. The lung was considered nor- mal if the characteristic features of well-ventilated lung Methods tissue with a smooth visceral surface was seen and if a Animals, history and clinical examination pleural reflective band and reverberation artifacts were A total of 35 calves (15 buffalo and 20 cattle) aged be- observed . The different abnormalities noted were tween 4 and 7 months were included in the present the presence of comet-tail artifacts, pleural fluid accu- study. Fifteen cattle calves were examined at the Clinic mulation, pleural irregularity and thickening, and con- of Ruminant and Swine, Faculty of Veterinary Medicine, solidated lung. Comet-tails were observed from the Free University of Berlin, Germany. The remaining 20 pleura to the deeper part of the ultrasonogram during calves (15 buffalo and 5 cattle) were examined at the De- the scanning of the site . Pleural effusion was diag- partment of Animal Medicine, Faculty of Veterinary nosed by accumulation of fluid between the parietal and Medicine, Assiut University, Egypt. Based on the owners’ visceral layers of pleura. Pleural irregularity and thicken- complaints, all animals were admitted because of inap- ing was noted if, in contrast to a normal thin smooth petance, nasal discharges, coughing, and variable degrees hyperechoic line, the pleural line was serrated with an ir- of dyspnea. There was no history of previous medica- regular shape and the pleural line thickness higher than tions either by the farmers or field veterinarians in any 1mm . Pulmonary consolidation was noted if the lung Hussein et al. Journal of Animal Science and Technology (2018) 60:29 Page 3 of 11 tissue appeared hypoechoic and its echo texture looked therapy, while the cattle calves euthanased for welfare like liver parenchyma. Based on the degree of lung con- reasons. solidation and the number of lobes involved, ultrasono- graphic lung score (ULS) (0–5) was used to categorize Statistical analyses calves as described previously . Bronchoaerograms The data were statistically analyzed using SPSS (SPSS was defined as hyperechoic spots indicated small bron- analytical program for Windows Version 20; SPSS chi filled with air. GmbH, Munich, Germany). The normality of all vari- ables was tested using Kolmogorov-Smirnov test. All variables were normally distributed. Differences between Blood sampling, hematological and biochemical analyses diseased and control animals were assessed by one-way Two venous blood samples were collected from jugular analysis of variance (ANOVA). Pearson’s correlation co- vein; one placed in tubes containing ethylene diamine efficient (r) was used to determine the relationship tetraacetic acid (EDTA) as anticoagulant and the other between parameters. Post hoc Bonferroni multiple com- in plain tubes. The haematocrit, haemoglobin concentra- parison test was used to assess the possible variation in tion, total red blood cell count (RBCs) and total white variables with the preceding of therapy. For all statistical blood cells count (WBCs) were measured in the samples examinations, results were considered significant at P < containing EDTA using veterinary automated cell coun- 0.05. All data are listed as mean ± SD. ter. After centrifugation of the second blood sample, serum samples were collected and then frozen at − 20 °C Results till biochemical analysis. In the serum samples, commer- Based on clinical examination including, coughing, tach- cial test kits were used to determine the concentrations ypnoea, inspiratory dyspnea, nasal discharges, abnormal of total proteins and albumin. The activities of aspartate lung sounds and CRS as well as ultrasonographic find- aminotransferase (AST) and γ-glutamyl transpeptidase ings and postmortem findings for dead and euthanized (GGT) were also measured in serum samples. The bio- cases, diseased calves were classified into 4 groups: pul- chemical analyses of the parameters were spectro- monary emphysema (n = 8), interstitial pulmonary syn- photometrically measured according to the standard drome (n = 7), bronchopneumonia (n = 12), and pleurisy protocols of the test kits using UV spectrophotome- (n = 8). ters. From each animal, a third blood sample was col- lected from the caudal auricular artery and placed in Clinical presentation and respiratory score a syringe contains heparin as anticoagulant for arterial Clinical presentations were varied according to the re- blood gas analysis. Arterial blood gas indices were es- spiratory disease condition. At admission, the general timated using blood gas analyser (ABL 5, Radiometer, condition of most calves was deteriorated. The most ob- Copenhagen, Denmark). servable clinical presentations were dullness, difficult in- spiration (mouth breathing, widening of nostrils) Postmortem examination (Fig. 1a), and variable degrees of nasal discharges, which Necropsies were performed on 15 calves (7 buffalo and was either unilateral or bilateral, that ranged from 8 cattle). Buffalo calves died 1 day after beginning of mucopurulent to purulent in consistency (Fig. 1b). The Fig. 1 Clinical presentations of calves with respiratory troubles. a Dullness, lacrimation and mouth breathing are signs in a buffalo calf with interstitial pulmonary syndrome (CRS = 5); b ocular secretion (white arrow) and purulent nasal discharges (black arrow) in a cattle calf with bronchopneumonia (CRS = 6). CRS, Clinical respiratory score Hussein et al. Journal of Animal Science and Technology (2018) 60:29 Page 4 of 11 Table 1 Clinical respiratory and ultrasound lung scores in calves with respiratory troubles (n = 35) Buffalo calves Cattle calves Control (n = 6) Emphysema (n = 8) Interstitial pulmonary syndrome (n = 7) Control (n = 6) Bronchopneumonia (n = 12) Pleurisy (n =8) ** ** ** ** CRS 1.5 ± 0.3 4.3 ± 0.3 5.1 ± 0.5 1.7 ± 0.2 5.2 ± 0.2 5 ± 0.4 ** * ** ** ULS 0.0 ± 0.0 2.3 ± 0.3 2.1 ± 0.3 0.0 ± 0.0 3.1 ± 0.2 3.4 ± 0.3 CRS Clinical respiratory score, ULS ultrasound lung score * ** or Means within a row of the same species are significantly different (P < 0.05) or (P < 0.01), respectively from values of the corresponding control animals values of rectal temperature ranged from 38.7 °C to 41 ° real-time examination. Neither lung consolidation nor C. The lowest and highest values of body temperature pleural effusions were visualized in these normal calves. were noticed in calves with emphysema and pleurisy, re- The postmortem examinations of these calves confirmed spectively. In addition, 8 calves with bronchopneumonia these ultrasonographic results. showed pyrexia (mean value of rectal temperature was In calves with pulmonary emphysema, the ultrasono- 40 ± 0.6 °C). The mean value of pulse rate was 92beats/ graphic examination of chest showed numerous min (range, 78–110). The mean respiratory rate was comet-tail artifacts in the form of bright echogenic 43breaths/min (range, 28–52). Upon percussion of the bands extending at the lung surface and running perpen- lungs, 5 cases with pulmonary emphysema showed in- dicular to the pleura. These comet-tail artifacts ranged creased and 4 cases with bronchopneumonia had re- from 3 (Fig. 3a) to 4 (Fig. 3b) in number. The most af- duced resonance. Upon auscultation of lungs, 3 cases fected lung lobes were the intermediate (5 calves), then with interstitial pulmonary syndrome exhibited exagger- the cranial (3 calves) lobes. The Thoracic ultrasonog- ated vesicular sounds, 5 cases with bronchopneumonia raphy of buffalo calves with interstitial pulmonary syn- showed moist ráles and 2 cases with pleurisy had pleur- drome revealed presence of multiple ultrasound lung itic frictional sounds, resembling two sheets of sand- comets fanning out from the pleural line to the edge of paper rubbing against each other. Four cases with the image. These lung comets were broader than that in pulmonary emphysema showed reduced vesicular breath emphysema and the entire ultrasound image appeared sounds. In contrast, six cases (2 with interstitial pulmon- white in colour (Fig. 4a). At postmortem examinations ary syndrome and 4 with bronchopneumonia) exhibited of these calves, their lungs were severely congested and no lung sounds by auscultation. The mean values of edematous (Fig. 4 b). CRS were significantly higher in all diseased groups in In calves with bronchopneumonia, the ultrasono- comparison with their corresponding control ones (P < graphic appearance of diseased lungs varied depending 0.01) (Table 1). on the degree and type of lesions. Four cases showed small hypoechoic circular zones (about 7 mm in diam- Ultrasonographic and postmortem findings eter) at the lung surface, representing a superficial fluid The ultrasonographic appearance of normal aerated lung alveologram with a comet-tail artifact (Fig. 5a). The of control groups was characterized by the uppermost ultrasonographic features of the lung tissue in ten calves white linear echo, representing parietal and visceral with bronchopneumonia appeared hypoechoic and its pleurae, with reverberation artifacts (Fig. 2). During res- echo texture may look like liver parenchyma, represent- piration, the visceral pleura was seen moving with a ing pulmonary consolidation and containing ramified fluid bronchgrams (Fig. 5b). These consolidated areas have a homogenous and echoic basic texture with well defined borders. Lesions of lung consolidation were found on the left side of the thorax in 7 cases and on the right side of the thorax in 3 cases. In three cases, air-filled alveoli were imaged in this hepatized lung tis- sue, appearing as hyperechoic spots in the consolidated parenchyma. Occasionally, hyperechoic reflective bands of an air-filled bronchus were detected in the pulmonary tissue, representing air bronchoaerograms. The most af- fected lobes were the cranial (8 calves) (Fig. 5c), then the cardiac (2 calves) and intermediate (2 calves) lobes. Fig. 2 Ultrasonogram of a normal lung generated using a 5 MHz Thoracic ultrasonographic examination of calves with sector probe: hyperechoic pleural line (P) with less echogenic lines pleurisy revealed presence of thick fragmented visceral parallel to the pleural surface (arrows) represent reverberation pleura and filling of pleural sac with echogenic fibrin artifacts. TW, Thoracic wall; P, Pleura; Ds, Dorsal; Vt, Ventral shreds and anechoic exudates (Fig. 6). Moderate pleural Hussein et al. Journal of Animal Science and Technology (2018) 60:29 Page 5 of 11 Fig. 3 Ultrasonograms of the lung of buffalo calves with pulmonary emphysema. a A mild case of pulmonary emphysema shows few echogenic bands (C) run from the lung surface with reverberation artifacts (arrows); b A severe case of pulmonary emphysema shows multiple echogenic bands (C) originate from the pleural surface. TW, Thoracic wall; P, Pleura; Ds, Dorsal; Vt, Ventral; C, Comet-tail artifacts effusion was seen in 3 cases, while pleural irregularity analysis revealed increased partial tension of carbon was observed in 4 of 8 cattle calves with pleurisy. One dioxide (PCO ) in all diseased. In contrast, the mean case showed roughened texture of the pleural surface values of partial tension of oxygen (PO )werede- causing narrow streaks of comet tails. creased in all diseased groups (P < 0.05). Pearson’s correlation coefficients were calculated to The association between the laboratory parameters find the relationship between ULS and CRS. A weak cor- and various respiratory troubles is summarized in Table 3 relation was noticed between the two variables (r = 0.55, for 26 calves with ultrasound lung score ≥ 1 and clinical P < 0.01) (Fig. 7). respiratory score ≥ 5. It was noticed that only WBCs and PCO were significantly (P = 0.006) and (P = 0.004), re- Hematological and biochemical findings spectively, indicated respiratory troubles in weaned Table 2 summarizes the mean values of hematological calves. However, weak correlations were observed be- and biochemical indices in calves with respiratory tween ULS and WBCs (r = 0.47, P < 0.1) and ULS and troubles. The total white blood cell counts were PCO (r = 0.36, P < 0.05) (Table 4). higher in all diseased groups in comparison with the corresponding controls (P < 0.05). The mean values of Therapy and outcome serum total proteins and globulins were significantly Calves were treated with 8.7 mg/kg amoxicillin trihy- increased only in calves with bronchopneumonia (P < drate, clavulanic acid (Synulox®) injected once daily 0.05). The serum activities of AST were higher in into the muscles of the neck or hindquarters. Brom- buffalo claves with emphysema and interstitial pul- hexine Hydrochloride (Bisolvon) in a dose 0.5 mg/kg monary syndrome in comparison with the corre- per os. 0.5 mg/kg meloxicam (metacam) intravenous sponding control group (P < 0.05). Arterial blood gas injection. The clinical signs including CRS and Fig. 4 Ultrasonogram and postmortem finding of a buffalo calf with interstitial pulmonary syndrome. Image (a) shows multiple ultrasound lung comets fanning out from the pleural line to the edge of the image (arrows), white lung. Image (b) represents postmortem findings of the same calf that shows severely congested and edematous lung. TW, Thoracic wall; P, Pleura; Ds, Dorsal; Vt, Ventral; RS, Rib shadowing Hussein et al. Journal of Animal Science and Technology (2018) 60:29 Page 6 of 11 Fig. 5 Ultrasonograms of cattle calves with bronchopneumonia. a An image for a mild case shows a small hypoechoic zone on the surface of the lung (arrow, diameter: 7 mm), representing fluid alveologram with comet-tail artifact (C). b An image for the cranial lobe of a severely bronchopneumonic calf shows consolidated lung with ramified fluid bronchograms (FG). c This image represents postmortem findings of the same case in image B showing consolidation of the cranial lobe (arrow). TW, Thoracic wall; P, Pleura; Ds, Dorsal; Vt, Ventral; CL, Consolidated lung appetite were improved in most diseased calves, Discussion therefore; they were discharged from the hospital one Clinical findings of deteriorated body condition, cough- or 3 days after beginning of treatment and the im- ing, and variable degrees of nasal discharges, dyspnea portance of completing the therapeutic course was and respiratory noises in all diseased groups were sup- emphasized to the owner and referring veterinarian. ported in a previous study of bovine pulmonary diseases Ten cattle calves with bronchopneumonia were se- . In present study, most of diseased groups showed verely diseased and they kept in the hospital for a increased body temperature except those with emphy- month and examined clinically and ultrasonographi- sema, indicating acute stage of respiratory disease in the cally for assessment of therapy. After 3 days from the pyretic groups. In a previous report , the authors in- beginning of treatment, coughing and nasal discharges dicated fever > 39.7 °C as the most important selection were much reduced. The clinical respiratory score criterion for antibiotic therapy in growing cattle with was improved after 5 days (Table 5). Few crackle acute respiratory illness. sounds were heard over lung lesion. Crackles were Radiography, computed tomography (CT), and ultra- not consistently identified in 6 calves despite the sonography are non-invasive clinical tools for diagnosing presence of lung hepatization noted during ultrasono- respiratory troubles antemortem. Radiology had a good graphic examination. Follow-up ultrasound examin- sensitivity and poor specificity . In a previous study ation of calves revealed gradual improvement and , a high correlation was found between CT and post- tissue healing (Fig. 8). One incurable case was eutha- mortem levels of lung consolidations in young dairy nased and sent for necropsy examination, which re- calves. However, radiography and CT are not practical vealed gross lung pathology and exudation. for diagnosing respiratory diseases in large numbers of Fig. 6 Ultrasonogram of a lung of cattle calf with fibrinous pleurisy exhibits interrupted visceral pleura (VP) with accumulation of fibrin Fig. 7 A scatter plot for the relationship between the clinical (F) and inflammatory exudates forming pleural effusion (PE). TW, respiratory scores (CRS) and ultrasound lung scores (ULS) in calves Thoracic wall; Ds, Dorsal; Vt, Ventral; L, Lung with respiratory troubles Hussein et al. Journal of Animal Science and Technology (2018) 60:29 Page 7 of 11 Table 2 Laboratory findings in calves with respiratory troubles (n = 35) Buffalo calves Cattle calves Control (n = 6) Emphysema (n = 8) Interstitial pulmonary Control (n = 6) Bronchopneumonia Pleurisy (n =8) syndrome (n =7) (n = 12) RBCs (× 10 /L) 7.7 ± 0.2 7.8 ± 0.2 7.5 ± 0.3 7.8 ± 0.2 8.2 ± 0.3 8.5 ± 0.3 PCV (%) 30 ± 1 28 ± 0.9 28 ± 1 27 ± 1 28 ± 0.7 29 ± 0.9 Hemoglobin (g/L) 99 ± 2.2 98 ± 1.6 100 ± 0.9 96 ± 3 94 ± 3 98 ± 2.3 9 ** ** * ** WBCs (× 10 /L) 6.3 ± 0.2 7.8 ± 0.3 11.7 ± 0.5 7.7 ± 0.4 11 ± 1 12.3 ± 0.8 Total proteins (g/L) 60 ± 0.7 59 ± 1.4 60 ± 0.8 58 ± 1.5 64 ± 2.3 63 ± 2.4 Albumin (g/L) 30 ± 0.5 29 ± 1 29 ± 0.6 26 ± 0.9 25 ± 1.1 26 ± 1.3 Globulins (g/L) 30 ± 0.4 30 ± 1 31 ± 1 32 ± 1.2 39 ± 2.5 37 ± 2.6 * ** * * AST (U/L) 45 ± 4 66 ± 6 71 ± 6 58 ± 6 77 ± 5 76 ± 7 GGT (U/L) 19 ± 0.8 22 ± 1.6 20 ± 0.7 24 ± 1.3 24 ± 1.4 23 ± 1.2 Arterial blood gas analysis pH 7.35 ± 0.002 7.34 ± 0.006 7.34 ± 0.004 7.36 ± 0.01 7.33 ± 0.01 7.36 ± 0.01 ** ** * * PCO (mmHg) 50 ± 2.2 62 ± 1.5 69 ± 1.3 48 ± 5 60 ± 3 57 ± 2.2 ** ** ** * PO (mmHg) 85 ± 5 58 ± 3.3 55 ± 2.3 88 ± 8 62 ± 3 66 ± 4 Bicarbonate (mmol/L) 27 ± 0.7 27 ± 1 26 ± 0.8 29 ± 1 30 ± 1.1 29 ± 1.6 BE (mmol/L) 1.3 ± 0.5 0.4 ± 0.9 0.8 ± 0.6 2.2 ± 0.5 −0.1 ± 0.8 1.5 ± 0.6 * ** or Means within a row of the same species are significantly different (P < 0.05) or (P < 0.01) from values of the corresponding control animals calves in a farm setting because of physical equipment Ultrasonographic examination of normal air-filled pul- constraints, expenses, anaesthetic requirements, and the monary tissue appeared as a hyperechoic line represent- hazards of exposure to radiation . In contrast, thor- ing the visceral pleura due to total reflection of acic ultrasonography can be carried out calf-side using ultrasound waves . Furthermore, presence of rever- readily transportable machines without the fear of ex- beration artifacts may be attributed to block the progres- posure to radiation, as well as no special health and sion of the ultrasound waves by the air contained in the safety procedures or restrictions are required. lung tissue . Table 3 Association between laboratory measures and various respiratory troubles in 26 calves with ultrasound lung score ≥ 1 and clinical respiratory score ≥ 5 Variable Emphysema (n = 5) Interstitial pulmonary syndrome (n = 5) Bronchopneumonia (n = 10) Pleurisy (n =6) P-value RBCs (× 10 /L) 7.7 ± 0.23 7.9 ± 0.33 8.4 ± 0.37 8.9 ± 0.32 0.153 PCV (%) 28 ± 0.9 30 ± 1 28 ± 0.8 29 ± 1 0.686 Hemoglobin (g/L) 99 ± 2 101 ± 1.2 97 ± 3 100 ± 2.6 0.772 WBCs (×10 /L) 7.5 ± 0.3 12.2 ± 0.4 11.1 ± 1.1 13.3 ± 0.6 0.006 Total proteins (g/L) 60 ± 1.3 61 ± 0.8 66 ± 2.6 63 ± 3.1 0.366 Albumin (g/L) 29 ± 1.5 29 ± 1.7 25 ± 1.2 26 ± 1.7 0.139 Globulins (g/L) 31 ± 0.9 32 ± 1 41 ± 2.5 37 ± 3.5 0.058 AST (U/L) 62 ± 7.7 72 ± 7 81 ± 5.5 83 ± 6.1 0.175 GGT (U/L) 21 ± 2.1 20 ± 1 23 ± 1.5 21 ± 1 0.578 Arterial blood gas analysis pH 7.34 ± 0.01 7.33 ± 0.01 7.32 ± 0.01 7.35 ± 0.01 0.299 PCO (mmHg) 64 ± 1 72 ± 2 62 ± 2 60 ± 3 0.004 PO (mmHg) 53 ± 3 52 ± 2 55 ± 5 60 ± 4 0.163 Bicarbonate (mmol/L) 27 ± 1.2 27 ± 1 30 ± 1.2 29 ± 1.3 0.322 BE (mmol/L) 0.8 ± 0.9 0.4 ± 1.4 −0.7 ± 1.6 1.5 ± 0.8 0.694 Hussein et al. Journal of Animal Science and Technology (2018) 60:29 Page 8 of 11 Table 4 Pearson correlation coefficients between syndrome showed broad ultrasound lung comets that haematological and biochemical variables and ultrasound lung appeared on the monitor as white images, indicating dif- score in calves with respiratory troubles (n = 35) fuse pulmonary lesions. According to the authors’ know- Variables Ultrasound lung score ledge, no studies in animals reporting the ultrasound NS RBCs r = 0.28 description of interstitial pulmonary syndrome are avail- NS able. Therefore, this report described for the first time PCV r = 0.26 NS the ultrasound imaging of interstitial pulmonary syn- Hb r = − 0.05 drome in calves. Diffuse parenchymal lung disease must ** WBCs r = 0.47 be considered if the multiple comet-tail artifacts are dis- NS Total proteins r = 0.28 tributed over the entire lung surface  In human NS Albumin r = − 0.14 medicine, Lichtenstein and Mezière  attributed these NS Globulins r = 0.32 ultrasound comets to the thickening of subpleural inter- NS lobular septa, which would cause fragmentation of the AST r = 0.26 NS pleural specular reflector at the points of greatest imped- GGT r = 0.21 ance. In the present study, this variation between the NS pH r = 0.04 two types of comets of pulmonary emphysema and PCO r = 0.36 interstitial syndrome may be due to the differences in NS PO r = 0.15 the pathogenesis and lesions of both respiratory diseases. NS Bicarbonate r = 0.13 Furthermore, this ultrasound variation can be used as an NS important item for diagnosis and differential diagnosis of Base excess r = − 0.11 NS ** * the two diseased conditions, especially the physical ex- Not significant; P < 0.01; P < 0.05 aminations of animals in both groups revealed no obvi- Thoracic ultrasonography in buffalo calves with pul- ous sharp differences. monary emphysema revealed narrow comet-tail artifacts Ultrasonographic examinations of cattle calves with extended from the pleural surface and downward. In cat- bronchopneumonia revealed presence of pulmonary con- tle, Flöck  also reported the presence of comet-tail solidations, where the lung tissues appeared hypoechoic artifacts in the presence of pulmonary emphysema. In and their echo texture may look like liver parenchyma addition, buffalo calves with interstitial pulmonary containing bronchoaerograms and/or brochograms in this Table 5 Pre- and post-therapeutic variations of CRS, ULS and laboratory indices in calves with bronchopneumonia (n = 10) Control (n = 6) Pre- and post-therapeutic days At admission (0) 5 10 20 30 a b c d d CRS 1.7 ± 0.2 5.4 ± 0.2 3.8 ± 0.2 2.6 ± 0.2 1.8 ± 0.2 1.5 ± 0.2 a ab abc bc c ULS 0.0 ± 0.0 3.4 ± 0.3 3.2 ± 0.2 2.9 ± 0.3 2.6 ± 0.2 2.3 ± 0.1 RBCs (×10 /L) 7.8 ± 0.2 8.4 ± 0.4 8.1 ± 0.3 7.8 ± 0.2 8.2 ± 0.1 8.0 ± 0.1 PCV (%) 27 ± 1 28 ± 0.8 29 ± 0.6 29 ± 0.7 28 ± 0.3 29 ± 0.4 Hemoglobin (g/L) 96 ± 3 97 ± 3 99 ± 2 98 ± 2 102 ± 1 99 ± 1 9 a ab b b b WBCs (×10 /L) 7.7 ± 0.4 11.7 ± 1 10.5 ± 0.9 9.3 ± 0.4 8.8 ± 0.2 9 ± 0.2 Total proteins (g/L) 58 ± 1.5 66 ± 3 65 ± 2 63 ± 2 62 ± 1 63 ± 1 Albumin (g/L) 26 ± 0.9 25 ± 1 24 ± 0.9 25 ± 0.7 26 ± 1.1 27 ± 0.6 Globulins (g/L) 32 ± 1.2 41 ± 2 41 ± 2 38 ± 2 36 ± 1 36 ± 1 a a a ab b AST (U/L) 62 ± 6 81 ± 5 83 ± 3 81 ± 3 78 ± 3 69 ± 3 GGT (U/L) 24 ± 1.3 23 ± 1.5 21 ± 0.9 20 ± 0.5 22 ± 0.5 21 ± 0.5 Arterial blood gas analysis pH 7.36 ± 0.01 7.33 ± 0.01 7.32 ± 0.01 7.31 ± 0.02 7.32 ± 0.01 7.32 ± 0.01 a ab ab ab b PCO (mmHg) 48 ± 2 56 ± 3 54 ± 3 51 ± 1 50 ± 2 49 ± 1 b ab ab ab a PO (mmHg) 88 ± 2 58 ± 3 66 ± 3 69 ± 2 73 ± 2 75 ± 3 Bicarbonate (mmol/L) 29 ± 1 29 ± 0.8 29 ± 0.7 28 ± 0.6 27 ± 0.6 27 ± 0.5 BE (mmol/L) 2.2 ± 0.5 −0.7 ± 1.6 0.9 ± 0.3 0.6 ± 0.3 0.8 ± 0.1 0.6 ± 0.2 CRS Clinical respiratory score, ULS ultrasound lung score a,b,c,d values of different superscript letters in the same raw differs significantly (P < 0.05) Hussein et al. Journal of Animal Science and Technology (2018) 60:29 Page 9 of 11 Fig. 8 Ultrasonograms of a calf with severe bronchopneumonia show the development of pulmonary lesions during the course of therapy. Image (a), at admission of the calf, reveals consolidated cranial lobe (CL) with hyperechoic bronchoaerogram (BG). Image (b) for the same calf after 5 days of therapy shows consolidated cranial lobe (CL), bronchoaerogram (BG) and fluid bronchogram (FB). Image (c), after 10 days of therapy, exhibits consolidated lung (CL) and few bronchoaerograms (BG). Image (d), after 20 days of therapy, reveals improvement of pulmonary lesions but lung consolidation (CL) and fluid bronchogram (FB) are still present. Image (e), after 30 days of therapy, shows an obvious improvement in the pulmonary tissue in comparison with previous images but a remnant of fluid bronchogram (FB) is still present. TW, Thoracic wall; P, Pleura; Ds, Dorsal; Vt, Ventral region. As reported elsewhere , bronchoaerograms are In addition, white blood cell counts were associated with small bronchi filled with air, which makes them appear various respiratory troubles, indicating active inflamma- hyperechoic, while bornchograms are anechoic tubular tory reactions in the lung tissues. However, many dis- structures, representing fluid filled bronchi. In the current eases may exhibit such increases as a consequence of study, bronchograms resembled the blood vessels in the inflammatory processes like in respiratory diseases . echogenicity. Therefore, Doppler ultrasonography was In calves with bronchopneumonia, increased concentra- used to distinguish between blood vessels and broncho- tions of serum total proteins and globulins could be at- grams. Bronchograms appeared lacking the blood flow. tributed to the acute phase response as a result of Thoracic ultrasonography of calves with pleurisy showed pulmonary infection. As mentioned before , the de- varied images ranged from thickening and irregularity to mand for amino acids for synthesis of the positive acute fragmentation with pleural effusion of pleurae, indicating phase proteins is markedly increased during the acute the degree and severity of illness. As mentioned before phase reaction. In the present study, AST activities were , ultrasonography allows evaluation of pleura and per- significantly increased, which may be due to increased mits pleural effusion to be visualized and quantifies the respiratory rates and consequently increased efforts of nature and extent of the effusion. intercostal muscles with prolonged pulmonary diseases. For evaluation of prognosis, periodical follow-up ultra- This is in agreement with a previous report . How- sonography of bronchopneumonic calves during therapy ever, AST is not a specific parameter to a particular showed gradual improvement of ultrasound lung scores, organ, as it originates from many tissues but muscles indicating healing of the pulmonary tissues. In contrast, and liver are considered to be its major sources . In clinical respiratory scores were weakly correlated with the current study, arterial blood gas analysis showed in- ultrasound lung scores; this may be explained as the clin- creased PCO and decreased PO in diseased calves, in- 2 2 ical signs of respiratory problems diminished or subsided dicating impaired lung function. However, PCO and while the pulmonary lesions were still existed. It may be a PO failed to distinguish among the various respiratory misleading and a false decision about the case prognosis diseases. As mentioned elsewhere , the authors re- may be taken by the bovine veterinarians if they depend ported that disturbed partial tensions of oxygen and car- only on the physical examinations and consequently the bon dioxide may develop as a result of decreased effective disease relapse may occur. Therefore, it may be advisable alveolar ventilation. In contrast, Tharwat and Oikawa  to use thoracic ultrasonography as a follow-up tool for reported no changes in arterial blood gases in cattle with monitoring the efficacy of therapy. As mentioned else- respiratory disorders. Such difference may be attributed to where , the type, severity, and extent of pulmonary the variations in the degree and severity of illness. In this diseases cannot always be determined by clinical examin- study, it was noticed that only white blood cells and PCO ation alone and this may lead to misinterpretation of re- were associated with respiratory troubles. 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