Situs Inversus Totalis in a Dog With a Chronic Diaphragmatic Hernia

Introduction

Situs inversus totalis (SIT) is a congenital developmental abnormality consisting of complete left-to-right inversion of all thoracic and abdominal viscera, so they lie in a mirror image to their normal orientation. This condition is reported to occur in approximately one in 8000 to one in 10,000 humans.^1,2 Although no epidemiological studies have been done in dogs, the condition is likely a similarly rare occurrence. Situs inversus totalis is a component of Kartagener’s syndrome, a disease complex that is also characterized by bronchiectasis and rhinosinusitis. Situs inversus totalis can also occur alone.

In the veterinary literature, SIT has been reported as an isolated condition in the golden retriever, shih tzu, German shepherd dog, and a domestic shorthaired cat.^3–7 Situs inversus totalis has been seen in association with Kartagener’s syndrome in the Cavalier King Charles spaniel, dachshund, chow chow, border collie, and Doberman pinscher.^8–12 As a majority of human cases of SIT are asymptomatic, the same is possibly true in canine cases.^13–15 This case report describes a Doberman pinscher with asymptomatic SIT that was discovered during correction of a chronic diaphragmatic hernia.

Case Report

A 4-year-old, 28-kg, spayed female Doberman pinscher was presented to the University of Missouri-Columbia Veterinary Medical Teaching Hospital with respiratory distress after being sedated for radiography by the referring veterinarian. Radiographs were being made to assess right forelimb and hind-limb lameness. The dog was adopted 9 months prior and had an intermittent cough and shifting-limb lameness since adoption. No known traumatic incidents had occurred since adoption, and no respiratory difficulties were noted until the dog was sedated. On physical examination, the dog was bright and alert. Body condition score was 3 out of 9. Borborygmus was auscultated in the left ventral thorax. Bronchovesicular lung sounds could be heard over the dorsal thoracic cavity bilaterally. Normal heart sounds could be auscultated on the right but not the left side of the thorax. Abdominal palpation was difficult because of a tense abdomen. No pain was elicited during complete orthopedic examination, and the neurological examination was within normal limits. Repeat physical examination the following day revealed pain on range of motion of the dog’s coxofemoral and scapulohumeral joints bilaterally.

Thoracic and abdominal radiography was performed without sedation. Thoracic radiographs revealed the presence of abdominal organs in the ventral thorax [Figure 1]. The small intestines, spleen, and a portion of the liver could be discerned in the thorax. Abdominal radiographs revealed partial or complete absence of the above organs, but no other abnormalities were noted [Figure 2]. A diagnosis of diaphragmatic hernia was made.

Serum biochemical analysis, complete blood count (CBC), urinalysis, coagulation profile, buccal mucosal bleeding time, and pre- and postprandial serum bile acid levels were performed. Hypoglycemia (73 mg/dL; reference range 81 to 133 mg/dL), low blood urea nitrogen (5 mg/dL; reference range 8 to 28 mg/dL), hypoalbuminemia (2.5 g/dL; reference range 2.9 to 4 g/dL), and hyperglobulinemia (4.3 g/dL; reference range 2.2 to 3.6 g/dL) were noted. The CBC revealed a leukocytosis (25.4 × 10³ leukocytes/μL; reference range 6 to 17 × 10³ leukocytes/μL) with a mature neutrophilia (21.08 × 10³ neutrophils/μL; reference range 3 to 11.5 × 10³ neutrophils/μL) and a mild eosinophilia (1.52 × 10³ eosinophils/μL; reference range 0.1 to 1.25 × 10³ eosinophils/μL). Results of urinalysis and coagulation profile were within reference ranges. Buccal mucosal bleeding time was slightly prolonged (5 minutes; reference range <4 minutes). Pre- and postprandial bile acid levels were determined to further evaluate liver function; levels were within reference ranges.

An Ehrlichia canis immunofluorescent assay was also submitted and was negative. Radiographs were made of both coxofemoral joints and scapulohumeral joints. Pelvic radiographs revealed bony proliferation at the ventral border of the right ilium (consistent with old trauma) but were otherwise within normal limits. Lateral and craniocaudal radiographs of both shoulders were unremarkable. Because of the leukocytosis, history of shifting-limb lameness, periosteal bone proliferation, and a history of travel to the southern United States, infection with Hepatozoon (H.) americanum was considered. However, a rectus abdominus muscle biopsy was performed at the time of surgical correction of the diaphragmatic hernia, and no evidence of H. americanum infection was seen.

Three days after presentation, the dog underwent exploratory celiotomy. The dog was premedicated with fentanyl^a (10 μg/kg intravenously [IV]), induced with ketamine^b (10 mg/kg IV), and maintained with a continuous-rate infusion (CRI) of fentanyl^a (5 μg/kg per minute IV) and isoflurane in oxygen while on a ventilator. Perioperative cefazolin^c (22 mg/kg IV) was administered at the start of anesthesia and every 90 minutes thereafter. Direct blood pressure was monitored with an arterial catheter in the dorsal pedal artery.

Surgical exploration confirmed a diaphragmatic defect with cranial displacement of the liver, spleen, stomach, and proximal small intestine into the thoracic cavity. The defect was in the left ventral quadrant of the diaphragm and extended through the central tendinous portion of the diaphragm to the dorsal body wall and caval foramen. Initial replacement of the abdominal viscera into the peritoneal cavity was difficult, and the viscera became congested and cyanotic. On closer examination, situs inversus was discovered; the dog’s abdominal viscera were oriented in a left-to-right mirror image of the normal orientation [Figure 3]. After realizing the abnormality, the gastrointestinal tract and spleen were returned to the abdominal cavity in their appropriate orientation, and the abdominal viscera regained a normal pink coloration. No additional abnormalities were noted on exploration. Prior to closure of the chest, a thoracostomy tube was placed, and the defect in the diaphragm was closed with a simple continuous pattern of a nonabsorbable suture material.^d The edges of the diaphragmatic tear were not trimmed. The herniorrhaphy was initiated dorsally and continued ventrally, and the celiotomy was closed routinely.

Thoracic radiography performed the day after surgery confirmed dextrocardia (i.e., inversion of the normal position of the heart) [Figure 4]. Eight weeks after surgery, the dog was diagnosed with and treated for immune-mediated polyarthritis. At 13 months postsurgery, the dog was reexamined and considered completely normal based upon owner observation and physical examination. No evidence of rhinosinusitis or bronchiectasis (i.e., coughing) was seen.

Discussion

The normal anatomical orientation of the thoracic and abdominal viscera is termed situs solitus. Situs inversus total-is occurs when the thoracic and abdominal viscera develop in the mirror image position of their normal orientation. Physical examination findings for an animal with SIT are within normal limits except that the palpable apex heartbeat is on the right side of the thoracic cavity. Electrocardiogram (ECG) studies in these animals demonstrate an inversion of the normal ECG pattern.^11,14 Situs inversus totalis is usually an incidental finding that is discovered on radiographic examination.^5,6 Unless SIT is concurrent with bronchiectasis and rhinosinusitis as part of the Kartagener’s triad, it does not appear to be a clinically significant finding. However, a thorough knowledge of the internal anatomy of an animal with this condition is very important when interpreting diagnostic images or performing surgery or other invasive procedures.

This is the first report, to the authors’ knowledge, of SIT as an incidental finding during a diaphragmatic hernia repair. Whether the SIT was related to the development of the diaphragmatic hernia in this case was not known. The hernial edges were thickened and fibrotic, but the diaphragmatic musculature was easily apposed. In addition, a small number of adhesions between the liver and thoracic cavity were manually broken down prior to reduction of the liver. Because of this, the hernia was believed to be chronic. A congenital defect would likely not have thickened edges and could be difficult to close if the musculature had never formed. Therefore, trauma was suspected as the cause of the rupture. However, since trauma was never witnessed, a congenital diaphragmatic hernia could not be ruled out. In humans, SIT has been reported to occur concurrently with congenital diaphragmatic hernias.¹⁶ A retrospective study evaluating the prevalence of gastrointestinal abnormalities in human patients with situs anomalies found that out of 67 patients, 58% to 88% had one or more intraabdominal or intrathoracic lesion.¹⁷ Diaphragmatic herniation was reported as one of these lesions, but it occurred only in patients with right isomerism (bilateral right-sidedness) and not in those with SIT.

Correction of the diaphragmatic hernia was performed in an effort to establish normal respiratory function and to prevent occurrence of life-threatening gastric dilatation. In addition, a left-sided gastropexy was performed at the pyloric antrum. Repair of the chronic diaphragmatic hernia was more difficult because of the abnormal orientation of the thoracic and abdominal viscera. Once the abnormality was noted, reduction of the viscera and closure of the defect were routine.

Situs inversus totalis is one of three components of Kartagener’s syndrome, along with bronchiectasis and rhinosinusitis. In humans, approximately 25% of those affected with SIT are believed to also have Kartagener’s syndrome.² While bronchiectasis and rhinosinusitus are thought to be caused by primary ciliary dysfunction (or ciliary dyskinesia), the cause of SIT is not completely under-stood. ¹⁸ In veterinary medicine, SIT alone has been reported in a golden retriever, a shih tzu, a German shepherd dog, and a domestic shorthaired cat.^3–7 Kartagener’s syndrome (which includes SIT) has been reported in a Cavalier King Charles spaniel, a dachshund, a chow chow, a border collie, and a Doberman pinscher.^8–12

Ciliary dyskinesia is a disruption of the normal 9:2 structure of the microtubules comprising the individual cilia, resulting in ciliary malfunction and abnormal ciliary motility. ^18,19 One theory proposes that the normal orientation of the thoracic and abdominal viscera can then be disrupted, where-by abnormal ciliary motility of embryonic epithelial cells results in chance positioning of the viscera.^18,19 This has been evaluated in both dogs²⁰ and humans;²¹ approximately 50% of humans with primary ciliary dyskinesia also have SIT. Cilia in the rest of the body can also be affected, leading to bronchiolar ciliary disruption and bronchiectasis, upper respiratory ciliary dysfunction and chronic rhinosinusitis, as well as sperm motility disorders and infertility.^18–20

In the case reported here, no evidence of bronchiectasis or rhinosinusitis was seen, making a primary ciliary problem unlikely. No bronchogram or ciliary biopsies were obtained, however, so ciliary dysfunction cannot be ruled out. No upper respiratory problems (i.e., nasal discharge, sneezing) were noted or reported by the owner, and no bronchiectasis was seen on thoracic radiographs. As in this case, in most reports of animals with SIT (without Kartagener’s syndrome), the abnormality was diagnosed as an incidental finding either at the time of surgery or necropsy.^5–7,14

Conclusion

A 4-year-old Doberman pinscher with no known history of trauma since adoption 9 months prior was diagnosed with a chronic diaphragmatic hernia. At surgery, an incidental diagnosis of SIT was made. After realizing the abnormality, the diaphragmatic hernia was repaired routinely. If the situs anomaly had not been recognized and the viscera were left in their “normal” orientation, the ischemic injury would have been catastrophic and resulted in certain death.

Acknowledgments

The authors thank Dr. Sharon Kerwin for her critical review of the manuscript.