검색
검색 팝업 닫기

Ex) Article Title, Author, Keywords

Article

J Vet Clin 2023; 40(6): 457-463

https://doi.org/10.17555/jvc.2023.40.6.457

Published online December 31, 2023

Calcified Dirofilaria immitis Mimicking Thoracic Foreign Body in a Dog

Yeongseok Jeong , Seungjo Park*

College of Veterinary Medicine, Chonnam National University, Gwangju 61186, Korea

Correspondence to:*psc1237@jnu.ac.kr

Received: September 25, 2023; Revised: October 24, 2023; Accepted: November 7, 2023

Copyright © The Korean Society of Veterinary Clinics.

A 13-year-old neutered male Pomeranian, weighting 3 kg, presented with respiratory distress and depression. Radiographic examination revealed calcified ring-like opacities in the main pulmonary artery, mimicking thoracic foreign bodies. Additionally, right heart and main pulmonary artery enlargement and notable lung infiltrations were also observed. Echocardiography showed coil shaped structures in the main pulmonary artery with increased echogenicity compared to other nearby heartworms, which is consistent with calcified Dirofilaria immitis (heartworms). The dog was diagnosed with caval syndrome, which is the advanced and severe manifestation of heartworm infection. This report presents a rare case of calcified heartworm infection observed during a radiological examination, which resemble foreign bodies. Therefore, chronic heartworm disease should be considered as a differential diagnosis when radiopaque ringlike opacities are observed in the pulmonary artery on thoracic radiographs.

Keywords: heartworm (Dirofilaria immitis), calcification, radiography, echocardiography, dog

Heartworm disease is a common parasitic disease in dogs, which is transmitted by mosquitoes and mainly colonizes the main pulmonary and lobar arteries. The worms can migrate to the right ventricle, right atrium, and vena cava in high burden cases (24). The clinical presentation of heartworm infection varies, ranging from asymptomatic to potentially life-threatening conditions, depending on the duration and severity of infection. Mild cases may present as weight loss, reduced exercise tolerance, and mild lethargy. In contrast, chronic infections can lead to more pronounced symptoms, including coughing, dyspnea, and syncope (1,5,12).

The life cycle of D. immitis is long, typically spanning 7 to 9 months, which is relatively longer compared to the majority of parasitic nematodes (15). Inside the mosquitoes, the microfilariae develop from the first larval stage (L1) to the third larval stage (L3). The L3 infective larvae then enter the bloodstream of dogs when the mosquitos bite the dogs and molt into the fourth larval stage (L4). Subsequently, these develop into immature adults. Approximately 6-7 months post-infection, the adults reach maturity and become capable of producing microfilariae. The adult worms have a lifespan of 5-7 years, while the microfilariae can survive for approximately 1-2 years (15).

Antigen testing is the most sensitive diagnostic method for both screening and diagnosis of suspected heartworm infections (5). According to the published data reported, there are various heartworm antigen tests with a weighted average sensitivity of 78.2% and specificity of 97.3% (19). Currently, microfilaria testing concurrently with antigen testing is recommended to enhance diagnostic accuracy and comprehensiveness (5).

Heartworm disease cannot be identified through radiography and sometimes missed during the initial assessment. Although many patients undergo immunodiagnostic antigen tests for screening of heartworm, not all patients are tested, resulting in missed case, which are only identified through radiological evaluation. Therefore, a comprehensive understanding of the diagnostic imaging manifestations of heartworm disease in veterinary medicine is of paramount importance. Thoracic radiography is sometimes highly useful for the assessment of heartworm disease, helping determine its severity, evaluate pulmonary changes, and confirm differential diagnosis (7). According to the American Heartworm Society, one or more radiographic abnormalities are evident in approximately 85% of cases, including right ventricular enlargement (60%), increased prominence of the main pulmonary artery segment (70%), enlargement and increased density of pulmonary arteries (50%), and pulmonary artery tortuosity with a ’pruning sign’ (50%). Right-sided heart failure signs may include caudal vena cava, liver, and/or spleen enlargement; pleural effusion; and ascites (1). Pleural effusion is less common in heartworm disease-related heart failure, as marked enlargement of the cranial lobar pulmonary artery is a more sensitive indicator of heartworm disease compared to caudal vena cava enlargement (25).

Caval syndrome is a life-threatening complication of chronic heartworm disease characterized by acute anorexia, dyspnea, lethargy, systolic murmur, jugular vein distention, weak femoral pulses, pale mucous membranes, anemia, hemoglobinemia, hemoglobinuria, hepatic and renal dysfunction, disseminated intravascular coagulation, and both forward and backward heart failure. Caval syndrome is associated with the migration of large quantities of heartworms from the pulmonary arteries to the right atrium, right ventricle, and/or venae cava, resulting in tricuspid valve regurgitation, which is exacerbated by pulmonary hypertension, leading to right-sided heart failure and reduced ventricular output (21).

Herein, we present a compelling case of a dog demonstrating radiographic features of calcified heartworm parasites inside the heart. Remarkably, the radiographic appearance of the calcified heartworm closely resembled thoracic foreign bodies, adding complexity to the diagnostic process. This distinct observation highlights the importance of considering calcified heartworms as a differential diagnosis for thoracic radiographic abnormalities in clinical practice.

A 13-year-old male-neutered Pomeranian (weight = 3 kg) presented with a recent onset of respiratory distress and depression of 5 days duration. The owner reported that the dog had a normal appetite and had no coughing symptoms. Except for castration, medical and surgical history was unremarkable. The patient had received routine vaccinations in earlier years, and monthly distinct heartworm preventive medication including Ivermectin and Pyrantel (Diroheart, Diroheart-ss) had only been initiated three months prior. The dog was walked once or twice a week and was not on any chronic medications or over-the counter supplements. The patient had a body condition score of 4/5. The heart rate was measured at 140 beats per minute, blood pressure was 108 mmHg, and an average respiratory rate of 37 breaths per minute. Auscultation of the cardiac and respiratory systems was unremarkable.

Laboratory investigations revealed several abnormal findings. The patient had moderate to severe hyperlactatemia (6.0 mmol/L, reference range [RR]: 0.5-2.5 mmol/L), mild leukocytosis (29,110/μL, RR: 5,050-16,760 μL), and mild anemia of 36.2% (RR: 37.3-61.7%) on hematocrit. The patient also had severe azotemia, with blood urea nitrogen levels of 130 mg/dL (RR: 7-27 mg/dL), and moderately increased creatinine (2.0 mg/dL, RR: 0.5-1.8 mg/dL), phosphate (9.1 mg/dL, RR: 2.5-6.8 mg/dL), and symmetric dimethylarginine (29 μg/dL, RR: 0-14.0 μg/dL). Mild elevations were also noted in aspartate aminotransferase (75 U/L, RR: 0-50 U/L) and creatine kinase (277 U/L, RR: 10-200 U/L), which were unremarkable. Notably, there were substantial increases in D-dimer (5156.26 ng/mL, RR: 0-250 ng/mL), C-reactive protein (70.5 mg/L, RR: 10-20 mg/L), and canine pro brain natriuretic peptide (6320 mmol/L, RR: 0-900 mmol/L).

The initial suspicion by the clinicians was that the dog may have ingested or aspirated a foreign body.

Thoracic radiography revealed a mineral opacity (0.6 mm wide) on the ventral and left aspects of the thoracic trachea summating with the cardiac silhouette. The lesion was tortuous and appeared as three coiled figures. Additionally, the right heart and the main pulmonary artery were enlarged. A small amount of pleural effusion, alveolar pattern, and broncho-interstitial pattern was also observed (Fig. 1A, B). These radiographic findings led to the inclusion of heartworm infection as a differential, with the coiled mineral opacity of the lesion being strongly suggestive of calcified heartworms. Abdominal radiography showed a diffuse mild decrease in serosal detail of the abdominal cavity, which was indicative of a small amount of ascites.

Figure 1.Right lateral (A) and ventrodorsal (B) thoracic radiographs of the patient. Mineral opacity (arrows) observed at the 4th to 5th thoracic vertebrae, which was summated with the heart on the ventral and left aspects of the trachea, possibly representing the main pulmonary artery, which is not visualized as an individual structure but courses posteriorly to the ascending aorta and the aortic arch. The main pulmonary artery thus occupies the left aspect of the trachea and the esophagus at the 1 o’clock position in the ventrodorsal (VD) or dorsoventral (DV) views. The lesion was tortuous, resembling three coiled shapes. Additionally, enlargement of the right heart and main pulmonary artery was also observed on the ventrodorsal view (between 5 to 11 o’clock and 1 to 2 o’clock positions of the heart, respectively). The thoracic trachea was dorsally elevated (asterisk) on the lateral view. There was a small amount of pleural effusion (arrowheads). Alveolar infiltration in the mid lobe of the right lung and the anterior aspect of the left cranial lung, along with diffuse broncho-interstitial infiltration, were also observed. Diagram (C, D) of the thoracic radiograph demonstrating the observed opacities (coiled thick lines) probably in the main pulmonary artery.

Echocardiography showed numerous heartworms in the enlarged main pulmonary artery and right ventricle (Fig. 2). The heartworms found in the main pulmonary artery exhibited a higher degree of echogenicity compared to the parasites in other locations. Additionally, severe tricuspid regurgitant flow with a peak jet velocity of 4.5 m/s (peak pressure gradient = 80.6 mmHg) was also observed. Mild pulmonic regurgitant flow was also observed. In motion mode, left ventricular diastolic dimension was significantly lower level (10.2 mm, RR: 18.3-23.6 mm). There were numerous heartworms in the dilated caudal vena cava. The mean percentage of collapse in the diameter of the caudal vena cava was lower than 20%, indicating the systolic pressure of pulmonary artery was expected to be over 90-95 mmHg (severely high).

Figure 2.Echocardiogram (right parasternal short and long-axis transventricular view) showing the heartworm infestation on two- dimensional (2D) mode (A, B, short-axis view; C, D, long-axis view). (A, B) Multiple heartworms (arrow) observed in the dilated main pulmonary artery (MPA/AO = 1.7) and right ventricle. Compared to others heartworms, the heart worms located in the main pulmonary artery showed notably higher echogenicity, and exhibited a coiled appearance, resembling the patterns observed in previous radiographs. (C, D) Heartworms (arrow) observed in the right atrium. (E) Several heartworms (arrow) observed in the caudal vena cava. HW, heartworm; CVC, caudal vena cava; FF, free fluid.

Following the comprehensive diagnostic imaging evaluation, the IDEXX SNAP® 4Dx® Plus test was conducted and provided a definitive diagnosis of heartworm infection. The patient was hospitalized for 4 days for stabilization, and administered medications including sildenafil, anticoagulants, antibiotics, steroids. But the respiratory condition progressively deteriorated. Consequently, emergency surgery for the removal of heartworms was undertaken, however, the patient died during anesthesia. No postmortem examination of the patient was conducted.

Heartworm disease remains a prevalent and serious parasitic infection in dogs, for which early detection is crucial for effective management and treatment. Radiography is a valuable tool for the assessing the severity of heartworm infections, evaluating pulmonary changes, and identifying potential differential diagnosis (7). This case is distinguished by the presence of calcified heartworms on the radiograph, which mimicked thoracic foreign bodies. To the best of the author’s knowledge, no previous reports have documented the detection of calcified heartworms on radiography. Heartworms could potentially exhibit superimposition with the cardiac structures or blood vessels, thereby leading to constrained visibility during observation. However, in a specific case of human infection caused by Dirofilaria immitis, the heartworm exhibited degenerative changes with calcification upon histopathological examination (2). There also have been a few reported cases observed with calcification of parasites on radiographs or computed tomography in human (8,17,18). In the most of cases, the calcification of parasites after the parasites migrate into muscles or subcutaneous tissue and die (17,18). Similarly, heartworms in cases with chronic infection could undergo calcification within the cardiac chambers leading to their death, and later identified through radiographic examinations. In a case report concerning heartworm infection in ferrets, a post-mortem examination revealed the presence of coiled adult female worms within the right atrium and right ventricle. Additionally, three male adult worms were observed in the right atrium, cranial vena cava, and caudal vena cava. Histopathological examination confirmed the presence of dead calcified heartworms (20). In the present case, the lesions observed at the 4th to 5th thoracic vertebrae are likely within the main pulmonary artery, leading to the likelihood of heartworm infection (Fig. 1). This suspicion was further supported by the enlargement of the main pulmonary artery, right heart, and the presence of pleural effusion in the abdominal cavities.

Despite obtaining accurate history, diagnosis of a mineral opacity in heart silhouette such as calcified heartworms, may be difficult to diagnose due to its rare occurrence. The potential differential diagnosis for a mineral opacity in heart silhouette may include cardiovascular system implants and foreign bodies in other thoracic organs including the bronchus, trachea, and cardiovascular system (3,4,9-11,14,16). The implant in cardiovascular can be ruled out by history taking and comparing a figure of the implant with the radiological findings (6). In human studies, extensive research has been conducted on cases of tracheal and bronchial foreign bodies. Majority of foreign bodies found in the airway tend to be in the bronchus, owing to their size and shape (4). Symptoms induced by foreign bodies in the airway include acute respiratory distress, coughing, gagging, and continued breathing difficulty. Only a few asymptomatic cases have been reported (11,16).

Airway foreign bodies lesions can present in diverse range of forms and opacities depending on their types and sizes, including radiopaque lesions, as seen in the present case. The absence of cough and the size of the lesion compared to the patient, which seemed incongruent with typical bronchial foreign bodies, led to the exclusion of foreign body aspiration as a differential. Therefore, the differential diagnoses for foreign body opacities observed on radiology should be based on the patient’s history, signalment, lesions anatomical position, and clinical signs. A computed tomography should be considered in cases where the presence of a foreign body cannot be confirmed on radiography (3).

There are a few case reports detailing intravascular foreign bodies in the cardiovascular system (10). These can be confirmed by radiography, fluoroscopy and computed tomography. In a case series, IV catheters were located in the main pulmonary artery (one dog) and a branch of the pulmonary artery (four dogs). On lateral thoracic radiographic views, a radiopaque foreign body located in a distal branch of the right pulmonary artery was observed. Due to the close anatomical relationship between the bronchi and the main pulmonary artery, distinguishing between these two anatomical regions on radiographic examinations can be challenging (25). However, several distinguishing features enable the differentiation between catheter foreign bodies and calcified heartworm shadowing. Typically, catheter foreign bodies exhibit a non-coiled configuration, while calcified heartworms can be observed in both coiled and linear forms. Additionally, the calcified heartworms are generally longer when compared to catheter foreign bodies, facilitating their differentiation. The adult male D. immitis is approximately 15-18 cm long and has a diameter ranging from 0.7-0.9 mm, while the adult female can grow 25-30 cm long with a diameter of 1.0-1.3 mm (1,13). Nevertheless, meticulous attention to detailed history taking is essential for accurate diagnosis.

The distinctions in comparison to other calcified structures that may be observed radiographically vary according to the anatomical location of the respective opacities. For instance, in the case of bronchial calcification, it involves the calcification of the bronchial walls, leading to the presence of radiolucent areas between the walls where air is contained. Also, bronchial wall is generally thin (bronchus: 0.5 mm/heartworm: 1 mm-1.2 mm) compared to calcified heartworm. Additionally, while bronchial structures are typically observed to run parallel to adjacent blood vessels, in this case, the opacity was seen in a coil-shaped configuration, distinguishing it from bronchial structures. The calcification of pulmonary artery typically exhibits connectivity with adjacent pulmonary arteries and follow a straight course, thereby can be distinguished them from the opacity of present case. Similarly, in the case of valvular calcifications, they do not manifest in a coil-like configuration, allowing for differentiation.

Echocardiography showed a coiled structure with increased echogenicity in the main pulmonary artery, which was consistent with the findings observed on radiograph. This coiled lesion had higher echogenicity compared to typical heartworm echoes, suggesting calcification of the heartworms. The presence of calcified heartworms can facilitate better visualization on radiographs and echocardiograms, as it enhances diagnostic specificity for heartworm disease and serves as a valuable indicator for the monitoring of therapeutic intervention efficacy and the patient’s clinical progression. The observed structure maintained its morphological integrity without discernible mobility and presented a distinctive configuration, lacking any connection with bronchial walls, vascular elements, or valvular structures. As a result, it was diagnosed as calcification of deceased heartworms.

A case report detailing the radiographic features of calcified heartworms and the associated echocardiographic features has not been previously reported. The shape of infected parasites observed are usually observed as worm-like thick linear and/or coiled structures (17,22). The parasitic cyst can also be also calcified and looked like a nodule (17). Further morphological studies may help elucidate and improve detection of the radiographic features associated with dead internal parasites.

Caval syndrome is an uncommon but severe complication of heartworm infection characterized by a heavy worm burden and poor prognosis (21). This condition can be regarded as chronic due to the typical migration of the infecting parasite into the vena cava and right atrium, a process that usually takes approximately 7-17 months. In the present case, the patient was diagnosed with caval syndrome, suggesting a potential association between calcified heartworms and chronic infection. When calcified heartworms are identified on radiographic examinations, a chronic infection is suspected, suggesting the necessity for prompt diagnosis and treatment. In addition to heartworms, other parasites can also infiltrate the cardiovascular system of canines including Angiostrongylus vasorum, which has a unique life cycle involving frogs or chickens as intermediate hosts and red foxes as definitive hosts. There have been documented cases of A. vasorum infections in canines originating from the definitive hosts in various Europe regions, including Romania. Interestingly, the distribution of A. vasorum seems to be associated with the presence of red foxes in the local environment. As a result, differentiating between heartworm infection and A. vasorum infestation may be required. This can be achieved by considering regional factors and employing appropriate diagnostic techniques, such as polymerase chain reaction or antibody testing, which offer distinct features for each type of cardiac parasitic infestation (23).

This case report has some limitations. Firstly, no surgical procedure or postmortem examination of the patient was conducted. Additionally, this report is based on a single case, which should be supported by additional reports and future studies.

Herein, we discuss the radiographic features of the calcified heartworms observed on thoracic radiographs. This emphasis the importance of making a differential diagnoses lists based on patient history and radiographic findings. In conclusion, chronic heartworm disease should be considered as a differential diagnoses when the radiopaque ring-like opacities are observed within the pulmonary artery on thoracic radiographs.

This research was supported by the Animal Medical Institute of Chonnam National University.

  1. American Heartworm Society. Current canine guidelines for the prevention, diagnosis, and management of heartworm (Dirofilaria immitis) infection in dogs. . Holly Springs: American Heartworm Society. 2018: 1-29.
  2. Atsumi E, Matsumoto H, Taira N, Yohena T, Kawasaki H, Kawabata T, et al. Thirteen cases of pulmonary dirofilariasis in a single institution in Okinawa Island. Virchows Arch. 2019; 475: 335-340.
    Pubmed KoreaMed CrossRef
  3. Bajaj D, Sachdeva A, Deepak D. Foreign body aspiration. J Thorac Dis. 2021; 13: 5159-5175.
    Pubmed KoreaMed CrossRef
  4. Banjar AA, Al-Shamani MR, Al-Harbi J. Long standing tracheal foreign body in children: a case report. Egypt J Ear Nose Throat Allied Sci. 2014; 15: 57-59.
    CrossRef
  5. Bowman DD, Atkins CE. Heartworm biology, treatment, and control. Vet Clin North Am Small Anim Pract. 2009; 39: 1127-1158; vii.
    Pubmed CrossRef
  6. Bussadori C, Domenech O, Longo A, Pradelli D, Bussadori R. Percutaneous catheter-based treatment of pulmonic stenosis and patent ductus arteriosus in a dog. J Vet Cardiol. 2002; 4: 29-34.
    Pubmed CrossRef
  7. Carlisle CH. Canine dirofilariasis: its radiographic appearance. Vet Radiol. 1980; 21: 123-130.
    CrossRef
  8. Carranza-Rodríguez C, Pérez-Arellano JL. Radiological detection of Dracunculus medinensis. Am J Trop Med Hyg. 2018; 98: 1218-1219.
    Pubmed KoreaMed CrossRef
  9. Choi YD, Han HJ. Pyothorax induced by an intrathoracic foreign body in a miniature dachshund: migration of a popsicle stick from the stomach. J Vet Med Sci. 2017; 79: 1398-1403.
    Pubmed KoreaMed CrossRef
  10. Culp WT, Weisse C, Berent AC, Getman LM, Schaer TP, Solomon JA. Percutaneous endovascular retrieval of an intravascular foreign body in five dogs, a goat, and a horse. J Am Vet Med Assoc. 2008; 232: 1850-1856.
    Pubmed CrossRef
  11. Davis SJ, Madden G, Carapiet D, Nixon M, Dennis S, Pringle M. Delayed presentation of paediatric tracheal foreign body. Eur Arch Otorhinolaryngol. 2007; 264: 833-835.
    Pubmed CrossRef
  12. Ettinger S, Feldman E. Canine heartworm disease. In: Ettinger S, Feldman E, editors. Textbook of veterinary internal medicine: diseases of the dog and cat. St. Louis: Elsevier/Saunders. 2005: 1118-1144.
  13. Hoch H, Strickland K. Canine and feline dirofilariasis: life cycle, pathophysiology, and diagnosis. Compend Contin Educ Vet. 2008; 30: 133-140; quiz 141.
  14. Iqbal I, Lateef M, Wani AA, Rafiq S. A rare case of foreign body bronchus: a case report. Indian J Otolaryngol Head Neck Surg. 2011; 63(Suppl 1): 81-82.
    Pubmed KoreaMed CrossRef
  15. Kotani T, Powers KG. Developmental stages of Dirofilaria immitis in the dog. Am J Vet Res. 1982; 43: 2199-2206.
  16. Mathiasen RA, Cruz RM. Asymptomatic near-total airway obstruction by a cylindrical tracheal foreign body. Laryngoscope. 2005; 115: 274-277.
    Pubmed CrossRef
  17. Novak R. Calcifications in the breast in Filaria loa infection. Acta Radiol. 1989; 30: 507-508.
    Pubmed CrossRef
  18. Rodríguez Carnero P, Hernández Mateo P, Martín-Garre S, García Pérez Á, Del Campo L. Unexpected hosts: imaging parasitic diseases. Insights Imaging. 2017; 8: 101-125.
    Pubmed KoreaMed CrossRef
  19. Rohrbach BW, Patton S. Effects of diagnostic test accuracy and treatment efficacy on the occurrence of suspected failure of heartworm prophylaxis in dogs. J Vet Intern Med. 2013; 27: 791-797; Erratum in: J Vet Intern Med 2013; 27: 1289.
    Pubmed CrossRef
  20. Sasai H, Kato K, Sasaki T, Koyama S, Kotani T, Fukata T. Echocardiographic diagnosis of dirofilariasis in a ferret. J Small Anim Pract. 2000; 41: 172-174.
    Pubmed CrossRef
  21. Strickland KN. Canine and feline caval syndrome. Clin Tech Small Anim Pract. 1998; 13: 88-95.
    Pubmed CrossRef
  22. Tappe D, Büttner DW. Diagnosis of human visceral pentastomiasis. PLoS Negl Trop Dis. 2009; 3: e320.
    Pubmed KoreaMed CrossRef
  23. Taulescu MA, Negoescu A, Ungur A, Toma C, Ionică AM, Gal C, et al. Is the Angiostrongylus vasorum infection in domestic dogs underestimated or misdiagnosed? A comprehensive presentation of four lethal cases. Front Vet Sci. 2023; 10: 1146713.
    Pubmed KoreaMed CrossRef
  24. Taylor AE. The development of Dirofilaria immitis in the mosquito Aedes aegypti. J Helminthol. 1960; 34: 27-38.
    Pubmed CrossRef
  25. Thrall DE. Textbook of veterinary diagnostic radiology. . St. Louis: Elsevier Health Sciences. 2018: 684-709.

Article

Case Report

J Vet Clin 2023; 40(6): 457-463

Published online December 31, 2023 https://doi.org/10.17555/jvc.2023.40.6.457

Copyright © The Korean Society of Veterinary Clinics.

Calcified Dirofilaria immitis Mimicking Thoracic Foreign Body in a Dog

Yeongseok Jeong , Seungjo Park*

College of Veterinary Medicine, Chonnam National University, Gwangju 61186, Korea

Correspondence to:*psc1237@jnu.ac.kr

Received: September 25, 2023; Revised: October 24, 2023; Accepted: November 7, 2023

This is an open access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

A 13-year-old neutered male Pomeranian, weighting 3 kg, presented with respiratory distress and depression. Radiographic examination revealed calcified ring-like opacities in the main pulmonary artery, mimicking thoracic foreign bodies. Additionally, right heart and main pulmonary artery enlargement and notable lung infiltrations were also observed. Echocardiography showed coil shaped structures in the main pulmonary artery with increased echogenicity compared to other nearby heartworms, which is consistent with calcified Dirofilaria immitis (heartworms). The dog was diagnosed with caval syndrome, which is the advanced and severe manifestation of heartworm infection. This report presents a rare case of calcified heartworm infection observed during a radiological examination, which resemble foreign bodies. Therefore, chronic heartworm disease should be considered as a differential diagnosis when radiopaque ringlike opacities are observed in the pulmonary artery on thoracic radiographs.

Keywords: heartworm (Dirofilaria immitis), calcification, radiography, echocardiography, dog

Introduction

Heartworm disease is a common parasitic disease in dogs, which is transmitted by mosquitoes and mainly colonizes the main pulmonary and lobar arteries. The worms can migrate to the right ventricle, right atrium, and vena cava in high burden cases (24). The clinical presentation of heartworm infection varies, ranging from asymptomatic to potentially life-threatening conditions, depending on the duration and severity of infection. Mild cases may present as weight loss, reduced exercise tolerance, and mild lethargy. In contrast, chronic infections can lead to more pronounced symptoms, including coughing, dyspnea, and syncope (1,5,12).

The life cycle of D. immitis is long, typically spanning 7 to 9 months, which is relatively longer compared to the majority of parasitic nematodes (15). Inside the mosquitoes, the microfilariae develop from the first larval stage (L1) to the third larval stage (L3). The L3 infective larvae then enter the bloodstream of dogs when the mosquitos bite the dogs and molt into the fourth larval stage (L4). Subsequently, these develop into immature adults. Approximately 6-7 months post-infection, the adults reach maturity and become capable of producing microfilariae. The adult worms have a lifespan of 5-7 years, while the microfilariae can survive for approximately 1-2 years (15).

Antigen testing is the most sensitive diagnostic method for both screening and diagnosis of suspected heartworm infections (5). According to the published data reported, there are various heartworm antigen tests with a weighted average sensitivity of 78.2% and specificity of 97.3% (19). Currently, microfilaria testing concurrently with antigen testing is recommended to enhance diagnostic accuracy and comprehensiveness (5).

Heartworm disease cannot be identified through radiography and sometimes missed during the initial assessment. Although many patients undergo immunodiagnostic antigen tests for screening of heartworm, not all patients are tested, resulting in missed case, which are only identified through radiological evaluation. Therefore, a comprehensive understanding of the diagnostic imaging manifestations of heartworm disease in veterinary medicine is of paramount importance. Thoracic radiography is sometimes highly useful for the assessment of heartworm disease, helping determine its severity, evaluate pulmonary changes, and confirm differential diagnosis (7). According to the American Heartworm Society, one or more radiographic abnormalities are evident in approximately 85% of cases, including right ventricular enlargement (60%), increased prominence of the main pulmonary artery segment (70%), enlargement and increased density of pulmonary arteries (50%), and pulmonary artery tortuosity with a ’pruning sign’ (50%). Right-sided heart failure signs may include caudal vena cava, liver, and/or spleen enlargement; pleural effusion; and ascites (1). Pleural effusion is less common in heartworm disease-related heart failure, as marked enlargement of the cranial lobar pulmonary artery is a more sensitive indicator of heartworm disease compared to caudal vena cava enlargement (25).

Caval syndrome is a life-threatening complication of chronic heartworm disease characterized by acute anorexia, dyspnea, lethargy, systolic murmur, jugular vein distention, weak femoral pulses, pale mucous membranes, anemia, hemoglobinemia, hemoglobinuria, hepatic and renal dysfunction, disseminated intravascular coagulation, and both forward and backward heart failure. Caval syndrome is associated with the migration of large quantities of heartworms from the pulmonary arteries to the right atrium, right ventricle, and/or venae cava, resulting in tricuspid valve regurgitation, which is exacerbated by pulmonary hypertension, leading to right-sided heart failure and reduced ventricular output (21).

Herein, we present a compelling case of a dog demonstrating radiographic features of calcified heartworm parasites inside the heart. Remarkably, the radiographic appearance of the calcified heartworm closely resembled thoracic foreign bodies, adding complexity to the diagnostic process. This distinct observation highlights the importance of considering calcified heartworms as a differential diagnosis for thoracic radiographic abnormalities in clinical practice.

Case Report

A 13-year-old male-neutered Pomeranian (weight = 3 kg) presented with a recent onset of respiratory distress and depression of 5 days duration. The owner reported that the dog had a normal appetite and had no coughing symptoms. Except for castration, medical and surgical history was unremarkable. The patient had received routine vaccinations in earlier years, and monthly distinct heartworm preventive medication including Ivermectin and Pyrantel (Diroheart, Diroheart-ss) had only been initiated three months prior. The dog was walked once or twice a week and was not on any chronic medications or over-the counter supplements. The patient had a body condition score of 4/5. The heart rate was measured at 140 beats per minute, blood pressure was 108 mmHg, and an average respiratory rate of 37 breaths per minute. Auscultation of the cardiac and respiratory systems was unremarkable.

Laboratory investigations revealed several abnormal findings. The patient had moderate to severe hyperlactatemia (6.0 mmol/L, reference range [RR]: 0.5-2.5 mmol/L), mild leukocytosis (29,110/μL, RR: 5,050-16,760 μL), and mild anemia of 36.2% (RR: 37.3-61.7%) on hematocrit. The patient also had severe azotemia, with blood urea nitrogen levels of 130 mg/dL (RR: 7-27 mg/dL), and moderately increased creatinine (2.0 mg/dL, RR: 0.5-1.8 mg/dL), phosphate (9.1 mg/dL, RR: 2.5-6.8 mg/dL), and symmetric dimethylarginine (29 μg/dL, RR: 0-14.0 μg/dL). Mild elevations were also noted in aspartate aminotransferase (75 U/L, RR: 0-50 U/L) and creatine kinase (277 U/L, RR: 10-200 U/L), which were unremarkable. Notably, there were substantial increases in D-dimer (5156.26 ng/mL, RR: 0-250 ng/mL), C-reactive protein (70.5 mg/L, RR: 10-20 mg/L), and canine pro brain natriuretic peptide (6320 mmol/L, RR: 0-900 mmol/L).

The initial suspicion by the clinicians was that the dog may have ingested or aspirated a foreign body.

Thoracic radiography revealed a mineral opacity (0.6 mm wide) on the ventral and left aspects of the thoracic trachea summating with the cardiac silhouette. The lesion was tortuous and appeared as three coiled figures. Additionally, the right heart and the main pulmonary artery were enlarged. A small amount of pleural effusion, alveolar pattern, and broncho-interstitial pattern was also observed (Fig. 1A, B). These radiographic findings led to the inclusion of heartworm infection as a differential, with the coiled mineral opacity of the lesion being strongly suggestive of calcified heartworms. Abdominal radiography showed a diffuse mild decrease in serosal detail of the abdominal cavity, which was indicative of a small amount of ascites.

Figure 1. Right lateral (A) and ventrodorsal (B) thoracic radiographs of the patient. Mineral opacity (arrows) observed at the 4th to 5th thoracic vertebrae, which was summated with the heart on the ventral and left aspects of the trachea, possibly representing the main pulmonary artery, which is not visualized as an individual structure but courses posteriorly to the ascending aorta and the aortic arch. The main pulmonary artery thus occupies the left aspect of the trachea and the esophagus at the 1 o’clock position in the ventrodorsal (VD) or dorsoventral (DV) views. The lesion was tortuous, resembling three coiled shapes. Additionally, enlargement of the right heart and main pulmonary artery was also observed on the ventrodorsal view (between 5 to 11 o’clock and 1 to 2 o’clock positions of the heart, respectively). The thoracic trachea was dorsally elevated (asterisk) on the lateral view. There was a small amount of pleural effusion (arrowheads). Alveolar infiltration in the mid lobe of the right lung and the anterior aspect of the left cranial lung, along with diffuse broncho-interstitial infiltration, were also observed. Diagram (C, D) of the thoracic radiograph demonstrating the observed opacities (coiled thick lines) probably in the main pulmonary artery.

Echocardiography showed numerous heartworms in the enlarged main pulmonary artery and right ventricle (Fig. 2). The heartworms found in the main pulmonary artery exhibited a higher degree of echogenicity compared to the parasites in other locations. Additionally, severe tricuspid regurgitant flow with a peak jet velocity of 4.5 m/s (peak pressure gradient = 80.6 mmHg) was also observed. Mild pulmonic regurgitant flow was also observed. In motion mode, left ventricular diastolic dimension was significantly lower level (10.2 mm, RR: 18.3-23.6 mm). There were numerous heartworms in the dilated caudal vena cava. The mean percentage of collapse in the diameter of the caudal vena cava was lower than 20%, indicating the systolic pressure of pulmonary artery was expected to be over 90-95 mmHg (severely high).

Figure 2. Echocardiogram (right parasternal short and long-axis transventricular view) showing the heartworm infestation on two- dimensional (2D) mode (A, B, short-axis view; C, D, long-axis view). (A, B) Multiple heartworms (arrow) observed in the dilated main pulmonary artery (MPA/AO = 1.7) and right ventricle. Compared to others heartworms, the heart worms located in the main pulmonary artery showed notably higher echogenicity, and exhibited a coiled appearance, resembling the patterns observed in previous radiographs. (C, D) Heartworms (arrow) observed in the right atrium. (E) Several heartworms (arrow) observed in the caudal vena cava. HW, heartworm; CVC, caudal vena cava; FF, free fluid.

Following the comprehensive diagnostic imaging evaluation, the IDEXX SNAP® 4Dx® Plus test was conducted and provided a definitive diagnosis of heartworm infection. The patient was hospitalized for 4 days for stabilization, and administered medications including sildenafil, anticoagulants, antibiotics, steroids. But the respiratory condition progressively deteriorated. Consequently, emergency surgery for the removal of heartworms was undertaken, however, the patient died during anesthesia. No postmortem examination of the patient was conducted.

Discussion

Heartworm disease remains a prevalent and serious parasitic infection in dogs, for which early detection is crucial for effective management and treatment. Radiography is a valuable tool for the assessing the severity of heartworm infections, evaluating pulmonary changes, and identifying potential differential diagnosis (7). This case is distinguished by the presence of calcified heartworms on the radiograph, which mimicked thoracic foreign bodies. To the best of the author’s knowledge, no previous reports have documented the detection of calcified heartworms on radiography. Heartworms could potentially exhibit superimposition with the cardiac structures or blood vessels, thereby leading to constrained visibility during observation. However, in a specific case of human infection caused by Dirofilaria immitis, the heartworm exhibited degenerative changes with calcification upon histopathological examination (2). There also have been a few reported cases observed with calcification of parasites on radiographs or computed tomography in human (8,17,18). In the most of cases, the calcification of parasites after the parasites migrate into muscles or subcutaneous tissue and die (17,18). Similarly, heartworms in cases with chronic infection could undergo calcification within the cardiac chambers leading to their death, and later identified through radiographic examinations. In a case report concerning heartworm infection in ferrets, a post-mortem examination revealed the presence of coiled adult female worms within the right atrium and right ventricle. Additionally, three male adult worms were observed in the right atrium, cranial vena cava, and caudal vena cava. Histopathological examination confirmed the presence of dead calcified heartworms (20). In the present case, the lesions observed at the 4th to 5th thoracic vertebrae are likely within the main pulmonary artery, leading to the likelihood of heartworm infection (Fig. 1). This suspicion was further supported by the enlargement of the main pulmonary artery, right heart, and the presence of pleural effusion in the abdominal cavities.

Despite obtaining accurate history, diagnosis of a mineral opacity in heart silhouette such as calcified heartworms, may be difficult to diagnose due to its rare occurrence. The potential differential diagnosis for a mineral opacity in heart silhouette may include cardiovascular system implants and foreign bodies in other thoracic organs including the bronchus, trachea, and cardiovascular system (3,4,9-11,14,16). The implant in cardiovascular can be ruled out by history taking and comparing a figure of the implant with the radiological findings (6). In human studies, extensive research has been conducted on cases of tracheal and bronchial foreign bodies. Majority of foreign bodies found in the airway tend to be in the bronchus, owing to their size and shape (4). Symptoms induced by foreign bodies in the airway include acute respiratory distress, coughing, gagging, and continued breathing difficulty. Only a few asymptomatic cases have been reported (11,16).

Airway foreign bodies lesions can present in diverse range of forms and opacities depending on their types and sizes, including radiopaque lesions, as seen in the present case. The absence of cough and the size of the lesion compared to the patient, which seemed incongruent with typical bronchial foreign bodies, led to the exclusion of foreign body aspiration as a differential. Therefore, the differential diagnoses for foreign body opacities observed on radiology should be based on the patient’s history, signalment, lesions anatomical position, and clinical signs. A computed tomography should be considered in cases where the presence of a foreign body cannot be confirmed on radiography (3).

There are a few case reports detailing intravascular foreign bodies in the cardiovascular system (10). These can be confirmed by radiography, fluoroscopy and computed tomography. In a case series, IV catheters were located in the main pulmonary artery (one dog) and a branch of the pulmonary artery (four dogs). On lateral thoracic radiographic views, a radiopaque foreign body located in a distal branch of the right pulmonary artery was observed. Due to the close anatomical relationship between the bronchi and the main pulmonary artery, distinguishing between these two anatomical regions on radiographic examinations can be challenging (25). However, several distinguishing features enable the differentiation between catheter foreign bodies and calcified heartworm shadowing. Typically, catheter foreign bodies exhibit a non-coiled configuration, while calcified heartworms can be observed in both coiled and linear forms. Additionally, the calcified heartworms are generally longer when compared to catheter foreign bodies, facilitating their differentiation. The adult male D. immitis is approximately 15-18 cm long and has a diameter ranging from 0.7-0.9 mm, while the adult female can grow 25-30 cm long with a diameter of 1.0-1.3 mm (1,13). Nevertheless, meticulous attention to detailed history taking is essential for accurate diagnosis.

The distinctions in comparison to other calcified structures that may be observed radiographically vary according to the anatomical location of the respective opacities. For instance, in the case of bronchial calcification, it involves the calcification of the bronchial walls, leading to the presence of radiolucent areas between the walls where air is contained. Also, bronchial wall is generally thin (bronchus: 0.5 mm/heartworm: 1 mm-1.2 mm) compared to calcified heartworm. Additionally, while bronchial structures are typically observed to run parallel to adjacent blood vessels, in this case, the opacity was seen in a coil-shaped configuration, distinguishing it from bronchial structures. The calcification of pulmonary artery typically exhibits connectivity with adjacent pulmonary arteries and follow a straight course, thereby can be distinguished them from the opacity of present case. Similarly, in the case of valvular calcifications, they do not manifest in a coil-like configuration, allowing for differentiation.

Echocardiography showed a coiled structure with increased echogenicity in the main pulmonary artery, which was consistent with the findings observed on radiograph. This coiled lesion had higher echogenicity compared to typical heartworm echoes, suggesting calcification of the heartworms. The presence of calcified heartworms can facilitate better visualization on radiographs and echocardiograms, as it enhances diagnostic specificity for heartworm disease and serves as a valuable indicator for the monitoring of therapeutic intervention efficacy and the patient’s clinical progression. The observed structure maintained its morphological integrity without discernible mobility and presented a distinctive configuration, lacking any connection with bronchial walls, vascular elements, or valvular structures. As a result, it was diagnosed as calcification of deceased heartworms.

A case report detailing the radiographic features of calcified heartworms and the associated echocardiographic features has not been previously reported. The shape of infected parasites observed are usually observed as worm-like thick linear and/or coiled structures (17,22). The parasitic cyst can also be also calcified and looked like a nodule (17). Further morphological studies may help elucidate and improve detection of the radiographic features associated with dead internal parasites.

Caval syndrome is an uncommon but severe complication of heartworm infection characterized by a heavy worm burden and poor prognosis (21). This condition can be regarded as chronic due to the typical migration of the infecting parasite into the vena cava and right atrium, a process that usually takes approximately 7-17 months. In the present case, the patient was diagnosed with caval syndrome, suggesting a potential association between calcified heartworms and chronic infection. When calcified heartworms are identified on radiographic examinations, a chronic infection is suspected, suggesting the necessity for prompt diagnosis and treatment. In addition to heartworms, other parasites can also infiltrate the cardiovascular system of canines including Angiostrongylus vasorum, which has a unique life cycle involving frogs or chickens as intermediate hosts and red foxes as definitive hosts. There have been documented cases of A. vasorum infections in canines originating from the definitive hosts in various Europe regions, including Romania. Interestingly, the distribution of A. vasorum seems to be associated with the presence of red foxes in the local environment. As a result, differentiating between heartworm infection and A. vasorum infestation may be required. This can be achieved by considering regional factors and employing appropriate diagnostic techniques, such as polymerase chain reaction or antibody testing, which offer distinct features for each type of cardiac parasitic infestation (23).

This case report has some limitations. Firstly, no surgical procedure or postmortem examination of the patient was conducted. Additionally, this report is based on a single case, which should be supported by additional reports and future studies.

Conclusions

Herein, we discuss the radiographic features of the calcified heartworms observed on thoracic radiographs. This emphasis the importance of making a differential diagnoses lists based on patient history and radiographic findings. In conclusion, chronic heartworm disease should be considered as a differential diagnoses when the radiopaque ring-like opacities are observed within the pulmonary artery on thoracic radiographs.

Source of Funding

This research was supported by the Animal Medical Institute of Chonnam National University.

Conflicts of Interest

The authors have no conflicting interests.

Fig 1.

Figure 1.Right lateral (A) and ventrodorsal (B) thoracic radiographs of the patient. Mineral opacity (arrows) observed at the 4th to 5th thoracic vertebrae, which was summated with the heart on the ventral and left aspects of the trachea, possibly representing the main pulmonary artery, which is not visualized as an individual structure but courses posteriorly to the ascending aorta and the aortic arch. The main pulmonary artery thus occupies the left aspect of the trachea and the esophagus at the 1 o’clock position in the ventrodorsal (VD) or dorsoventral (DV) views. The lesion was tortuous, resembling three coiled shapes. Additionally, enlargement of the right heart and main pulmonary artery was also observed on the ventrodorsal view (between 5 to 11 o’clock and 1 to 2 o’clock positions of the heart, respectively). The thoracic trachea was dorsally elevated (asterisk) on the lateral view. There was a small amount of pleural effusion (arrowheads). Alveolar infiltration in the mid lobe of the right lung and the anterior aspect of the left cranial lung, along with diffuse broncho-interstitial infiltration, were also observed. Diagram (C, D) of the thoracic radiograph demonstrating the observed opacities (coiled thick lines) probably in the main pulmonary artery.
Journal of Veterinary Clinics 2023; 40: 457-463https://doi.org/10.17555/jvc.2023.40.6.457

Fig 2.

Figure 2.Echocardiogram (right parasternal short and long-axis transventricular view) showing the heartworm infestation on two- dimensional (2D) mode (A, B, short-axis view; C, D, long-axis view). (A, B) Multiple heartworms (arrow) observed in the dilated main pulmonary artery (MPA/AO = 1.7) and right ventricle. Compared to others heartworms, the heart worms located in the main pulmonary artery showed notably higher echogenicity, and exhibited a coiled appearance, resembling the patterns observed in previous radiographs. (C, D) Heartworms (arrow) observed in the right atrium. (E) Several heartworms (arrow) observed in the caudal vena cava. HW, heartworm; CVC, caudal vena cava; FF, free fluid.
Journal of Veterinary Clinics 2023; 40: 457-463https://doi.org/10.17555/jvc.2023.40.6.457

References

  1. American Heartworm Society. Current canine guidelines for the prevention, diagnosis, and management of heartworm (Dirofilaria immitis) infection in dogs. . Holly Springs: American Heartworm Society. 2018: 1-29.
  2. Atsumi E, Matsumoto H, Taira N, Yohena T, Kawasaki H, Kawabata T, et al. Thirteen cases of pulmonary dirofilariasis in a single institution in Okinawa Island. Virchows Arch. 2019; 475: 335-340.
    Pubmed KoreaMed CrossRef
  3. Bajaj D, Sachdeva A, Deepak D. Foreign body aspiration. J Thorac Dis. 2021; 13: 5159-5175.
    Pubmed KoreaMed CrossRef
  4. Banjar AA, Al-Shamani MR, Al-Harbi J. Long standing tracheal foreign body in children: a case report. Egypt J Ear Nose Throat Allied Sci. 2014; 15: 57-59.
    CrossRef
  5. Bowman DD, Atkins CE. Heartworm biology, treatment, and control. Vet Clin North Am Small Anim Pract. 2009; 39: 1127-1158; vii.
    Pubmed CrossRef
  6. Bussadori C, Domenech O, Longo A, Pradelli D, Bussadori R. Percutaneous catheter-based treatment of pulmonic stenosis and patent ductus arteriosus in a dog. J Vet Cardiol. 2002; 4: 29-34.
    Pubmed CrossRef
  7. Carlisle CH. Canine dirofilariasis: its radiographic appearance. Vet Radiol. 1980; 21: 123-130.
    CrossRef
  8. Carranza-Rodríguez C, Pérez-Arellano JL. Radiological detection of Dracunculus medinensis. Am J Trop Med Hyg. 2018; 98: 1218-1219.
    Pubmed KoreaMed CrossRef
  9. Choi YD, Han HJ. Pyothorax induced by an intrathoracic foreign body in a miniature dachshund: migration of a popsicle stick from the stomach. J Vet Med Sci. 2017; 79: 1398-1403.
    Pubmed KoreaMed CrossRef
  10. Culp WT, Weisse C, Berent AC, Getman LM, Schaer TP, Solomon JA. Percutaneous endovascular retrieval of an intravascular foreign body in five dogs, a goat, and a horse. J Am Vet Med Assoc. 2008; 232: 1850-1856.
    Pubmed CrossRef
  11. Davis SJ, Madden G, Carapiet D, Nixon M, Dennis S, Pringle M. Delayed presentation of paediatric tracheal foreign body. Eur Arch Otorhinolaryngol. 2007; 264: 833-835.
    Pubmed CrossRef
  12. Ettinger S, Feldman E. Canine heartworm disease. In: Ettinger S, Feldman E, editors. Textbook of veterinary internal medicine: diseases of the dog and cat. St. Louis: Elsevier/Saunders. 2005: 1118-1144.
  13. Hoch H, Strickland K. Canine and feline dirofilariasis: life cycle, pathophysiology, and diagnosis. Compend Contin Educ Vet. 2008; 30: 133-140; quiz 141.
  14. Iqbal I, Lateef M, Wani AA, Rafiq S. A rare case of foreign body bronchus: a case report. Indian J Otolaryngol Head Neck Surg. 2011; 63(Suppl 1): 81-82.
    Pubmed KoreaMed CrossRef
  15. Kotani T, Powers KG. Developmental stages of Dirofilaria immitis in the dog. Am J Vet Res. 1982; 43: 2199-2206.
  16. Mathiasen RA, Cruz RM. Asymptomatic near-total airway obstruction by a cylindrical tracheal foreign body. Laryngoscope. 2005; 115: 274-277.
    Pubmed CrossRef
  17. Novak R. Calcifications in the breast in Filaria loa infection. Acta Radiol. 1989; 30: 507-508.
    Pubmed CrossRef
  18. Rodríguez Carnero P, Hernández Mateo P, Martín-Garre S, García Pérez Á, Del Campo L. Unexpected hosts: imaging parasitic diseases. Insights Imaging. 2017; 8: 101-125.
    Pubmed KoreaMed CrossRef
  19. Rohrbach BW, Patton S. Effects of diagnostic test accuracy and treatment efficacy on the occurrence of suspected failure of heartworm prophylaxis in dogs. J Vet Intern Med. 2013; 27: 791-797; Erratum in: J Vet Intern Med 2013; 27: 1289.
    Pubmed CrossRef
  20. Sasai H, Kato K, Sasaki T, Koyama S, Kotani T, Fukata T. Echocardiographic diagnosis of dirofilariasis in a ferret. J Small Anim Pract. 2000; 41: 172-174.
    Pubmed CrossRef
  21. Strickland KN. Canine and feline caval syndrome. Clin Tech Small Anim Pract. 1998; 13: 88-95.
    Pubmed CrossRef
  22. Tappe D, Büttner DW. Diagnosis of human visceral pentastomiasis. PLoS Negl Trop Dis. 2009; 3: e320.
    Pubmed KoreaMed CrossRef
  23. Taulescu MA, Negoescu A, Ungur A, Toma C, Ionică AM, Gal C, et al. Is the Angiostrongylus vasorum infection in domestic dogs underestimated or misdiagnosed? A comprehensive presentation of four lethal cases. Front Vet Sci. 2023; 10: 1146713.
    Pubmed KoreaMed CrossRef
  24. Taylor AE. The development of Dirofilaria immitis in the mosquito Aedes aegypti. J Helminthol. 1960; 34: 27-38.
    Pubmed CrossRef
  25. Thrall DE. Textbook of veterinary diagnostic radiology. . St. Louis: Elsevier Health Sciences. 2018: 684-709.

Vol.41 No.1 February 2024

qrcode
qrcode
The Korean Society of Veterinary Clinics

pISSN 1598-298X
eISSN 2384-0749

Stats or Metrics

Share this article on :

  • line