Sternal Cleft Associated with Cantrell's Pentalogy in a German Shepherd Dog

Introduction

The sternum is an unpaired segmental series of eight bones (sternebrae) united by cartilaginous joints (synchondroses sternales) that form the floor of the thorax. The first and last sternebrae are known as the manubrium and xiphoid process, respectively.¹ Sternal cleft or bifid sternum is a congenital malformations caused by the failure of fusion in the midline of the sternebrae and xyphoid process.² Congenital sternal defects have been reported in dogs, most of them related to either the absence or incomplete development of sternebrae and xiphoid process.^3–5 There is only one published report of a congenital sternal cleft (bifid sternum) in dogs with a limited description of surgical therapy.⁶

In human medicine, Cantrell's pentalogy is defined as the presence of (1) a defect of the inferior sternum; (2) a midline supraumbilical abdominal wall defect; (3) a congenital intracardiac anomaly; (4) a deficit of the anterior diaphragm; and (5) a defect in the diaphragmatic pericardium.⁷ The association of those anomalies corresponds to a variant of thoracoabdominal ectopia cordis with an estimated incidence of 5.5 cases for q 1 million live human births.^8,9

The individual or collective association of cranial abdominal wall, caudal sternal, diaphragmatic, and pericardial congenital defects has been described previously in dogs.^{3–5,10–12} In one article, ventricular septal defect accompanied the pericardial and pleural lesions.¹¹ To the authors' knowledge, the concurrent association of all five congenital anomalies has only been reported in a litter of cocker spaniels.^3,12

The incidence of cases with congenital midline lesions is difficult to determine. It may be that affected dogs either die or are euthanized without veterinary attention contributing to a substantial lack of information regarding the association of these anomalies in small animals.¹⁰ In contrast to veterinary literature, approximately 100 human cases of Cantrell's pentalogy have been reported since Cantrell et al. first described the condition in 1958.^{7–9,12–14} This has resulted in not only a better understanding of the etiology and classification of the different variants of this syndrome but also improved surgical treatment.

This case report is the first to describe a sternal cleft associated with Cantrell's pentalogy in a German shepherd dog with successful surgical management. The etiology and diagnostic and therapeutic criteria with reference to the human literature has also been reviewed.

Case Report

A 5 mo old male German shepherd dog weighing 15.5 kg was referred for the evaluation of an abdominal wall hernia and exercise intolerance. Physical examination revealed a midline abdominal wall defect extending from the caudal segment of the sternum to the umbilicus, measuring 10 cm. Pulsations of the heart and the ventral aspect of the liver lobes were palpable through the thin skin covering the defect. A grade II/VI systolic murmur was appreciated on cardiac auscultation. Thoracic radiographs revealed a sternal cleft, abnormal position of the diaphragmatic cupola, and left-sided cardiomegaly (Figures 1A, B). Cardiac ultrasound revealed dilatation of the pulmonary artery, descending aorta, and subvalvular portion of the right ventricular outflow tract. The cardiac dimensions, valves, and function were otherwise normal. Ultrasonography using color-flow Doppler revealed high-velocity retrograde turbulent flow emerging from the descending aorta towards the pulmonary artery, consistent with a left-to-right shunting patent ductus arteriosus (PDA). Thoracic computed tomography (CT) showed a caudal sternal cleft with a normal manubrium but incomplete development of the seventh sternebra and agenesis of the xiphoid process (Figure 2). Hematologic, electrolyte, and serum biochemical profiles were within normal limits. To prevent the risk of traumatic injury to the lungs, heart, and liver, reconstructive surgery was proposed.

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The dog was premedicated with morphine^a (0.2 mg/kg subcutaneously) and diazepam^b (0.25 mg/kg IV). Anesthesia was induced with propofol^c (4 mg/kg IV) and maintained with 2% isoflurane^d in O₂ (1.5 L/min). Antibiotic prophylaxis with cephalexin^e (30 mg/kg IV) was administered 30 min before surgery then q 90 min during surgery. The thorax and abdomen were clipped and aseptically prepared, and the dog positioned in dorsal recumbency.

The skin overlying the sternum was incised on the ventral midline, and the incision was extended around the supraumbilical cutaneous atrophy, which was excised. The two halves of the sternebrae were identified and freed from surrounding fibrous tissue to the level of the manubrium. The insertion of the pectoralis muscles was mobilized using blunt dissection, and a retractor was applied between the sternal halves. Surgical exploration revealed a peritoneopericardial diaphragmatic communication with no evidence of adhesions or evisceration. The diaphragmatic defect was a large V-shaped lesion resulting from failure of the pars sternalis of the diaphragm to fuse along its midline and the absence of the last two sternebrae, which prevented proper ventral insertion of the diaphragm. The pericardial sac was attached to the dorsal aspect of both sternal halves and was continuous with each side of the V-shaped diaphragmatic defect. A caudoventral defect was observed in the pericardial sac after blunt dissection of its ventral insertion.

The PDA was approached through the median sternal defect. A persistent left cranial vena cava was incidentally noted, dissected, and retracted dorsally with the vagus nerve to improve exposure of the PDA. The PDA was ligated through the median sternal defect with a double 12 mm titanium clip^f. Subsequently, both flaps of the pericardial sac were mobilized over the apex of the heart and apposed, without tension, using a simple continuous suture pattern with 3-0 absorbable glycomer 631^g.

Reconstruction of the diaphragmatic defect necessitated partial dissection on either side of the paracostal insertion to enable cranial mobilization to the last sternebrae. A simple, continuous suture pattern with 3-0 absorbable glycomer 631 was used to appose the right and left borders of the diaphragm from the dorsal-most aspect of the defect, continuing ventrally until a small defect remained between the diaphragm and sternum. Mattress sutures with 2-0 absorbable glycomer 631 were placed from the diaphragm to the abdominal fascia of the adjacent costal arch and the two halves of the seventh sternebra. To avoid excessive tension when closing the remaining defect of the diaphragm, the mattress sutures were tightened after the sternal cleft had been repaired.

Primary closure of the sternal defect was performed by juxtaposing the internal margins of the two halves of the sternebrae in the midline. A stainless steel monofilament suture^h was passed in a figure eight pattern around the bodies of the two respective halves of two adjacent sternebrae, including the costosternal junction. That procedure was performed from the cranial-most sternebra proceeding in a caudal direction. The deep and superficial pectoral muscles were returned to their normal location and sutured over the midline using a simple continuous suture pattern with 2-0 absorbable glycomer 631. Neither circulatory nor respiratory distress was observed during the procedure.

The diastasis rectus (separation of the rectus abdominis muscle into right and left halves) was repaired by suturing the fascia of the trimmed edges of the rectus abdominis muscles with an appositional simple continuous pattern using 2-0 absorbable glycomer 631. The subcutaneous and intradermal layers were sutured using a simple continuous pattern with 3-0 and 4-0 absorbable glycomer 631, respectively. A thoracic drainⁱ was placed for chest vacuum between the left eighth and ninth ribs. Immediate postoperative radiography showed satisfactory apposition of the two sternal bars and a mild residual pneumothorax.

Prophylactic O₂ was administered postoperatively via an intranasal tube as the new chest conformation might have resulted in decreased volume of the thoracic cavity that could have led to increased pressure and potential risk of lung and mediastinal compression. Anesthetic recovery was uneventful, and O₂ therapy was discontinued 6 hr after surgery. Pain was managed with a continuous rate infusion of fentanyl^j (5 μg/kg/min for 12 hr), morphine (0.2 mg/kg subcutaneously q 4 hr for 36 hr), and carprofen^k (4 mg/kg per os q 24 hr for 10 days). The dog was hospitalized for 7 days, during which time respiratory and cardiovascular parameters remained normal. The fluid collected from the chest tube was regularly quantified, and production progressively increased between 18 and 42 hr postoperatively, coinciding with the onset of lethargy and pyrexia. Cytological examination of the pleural effusion revealed increased polynucleated neutrophil and macrophage counts with intracellular bacteria. Bacterial culture was positive for Streptococcus spp. The pyrexia resolved definitely after initiation of enrofloxacin^l (5 mg/kg either IV or per os q 24 hr for 8 days). Daily cytology showed a progressive clearing of the pleural effusion, and the chest drain was removed 114 hr postoperatively when the fluid production decreased to 2 mL/kg/day. Ten months after surgery, the dog was growing normally and enjoying normal activity. No audible heart murmur was identified on thoracic auscultation, and no complications were observed on thoracic radiographs.

Discussion

Caudal sternal cleft (with incomplete development of the seventh sternebra and agenesis of the xiphoid process), supraumbilical cutaneous atrophy, supraumbilical diastasis rectus, congenital cardiovascular anomalies (PDA and persistent left cranial vena cava), and defects of the pars sternalis of the diaphragm and caudoventral pericardium are compatible with Cantrell's pentalogy in this dog.

As suspected in humans, the association of those anomalies in small animals may result from a failure in early embryonic life during the development of the transverse septum of the diaphragm and the ventromedial migration of the paired mesodermal folds of the upper abdomen.⁷ By analogy to humans, the study authors believe that the association of those congenital midline anomalies in small animals could be defined as Cantrell's pentalogy. In dogs, the concurrent association of those anomalies is thought to occur from an accident in the uterus between the 24th and 28th day of gestation, resulting in a series of errors in the conformational fusion process as follows (1) an error during the migration of the sternal bars towards the midline and their fusion, which would normally nearly meet the manubrium on the 25th day of gestation, but are still widely separated caudally and may explain the sternal cleft; (2) failure of the pleuropericardial folds and the septum transversarum to fuse properly during celomic division into abdominal and thoracic body cavities that may explain the pericardial and diaphragmatic communication; and (3) failure of cardiac septation, which develops simultaneously with the septum transversarum and may explain the development of both diaphragmatic and cardiac defects.^1,3,4,11

Diagnosis of the complete syndrome requires the presence of all five criteria described by Cantrell, but incomplete forms have been reported in humans.^8,14 Toyama (1972) suggested the following classification of the syndrome (1) class 1, a definitive diagnosis with all five defects present; (2) class 2, a probable diagnosis with four defects, including intracardiac and ventral abdominal wall abnormalities; and (3) class 3, an incomplete expression with various combinations of defects, including the presence of a sternal abnormality.¹³ Based on Toyama's classification, the dog described in this case may be considered a class 3 expression of the syndrome because an intracardiac defect was not identified.

Specific reported lesions in humans related to Cantrell's pentalogy include sternal defects (such as lower sternal cleft, irregularities in the shape of the xiphoid, or absence of the entire sternum) and intracardiac defects (such as ventricular septal defect, atrial septal defect, pulmonary stenosis, tetralogy of Fallot, and left ventricular diverticulum).¹⁵ Diastasis rectus, omphalocele, and deformities involving other abdominal organ systems have also been reported.^8,14

Preoperative assessment in affected patients should include thoracic radiographs and CT to map the sternal and diaphragmatic abnormalities, echocardiography and electrocardiogram examinations to evaluate the heart for the presence of any cardiac anomalies, and abdominal ultrasound to characterize any abdominal wall or visceral anomalies.⁸ In the dog described herein, the supraumbilical cutaneous atrophy and the diastasis rectus were easily recognized on physical examination. Thoracic radiographs, CT, and ultrasonography enabled definitive diagnosis of the sternal deformity as well as the abdominal wall and cardiac congenital anomalies before attempting the surgical repair. Because the diaphragmatic defect was difficult to assess and the pericardial defect was not identified on imaging, the definitive diagnosis was determined at the time of surgery. MRI may have proved useful in this dog because it has been reported as an accurate means of diagnosing small defects of the ventral diaphragm and pericardium in humans.¹⁶

The best treatment strategy for Cantrell's pentalogy depends on the size of the thoracic and abdominal wall defect, type of associated heart anomalies, cardiovascular stability, and age of the patient.^9,14,15 In this case, a single-stage surgical correction was implemented based on the absence of intracardiac defects and the fact that PDA ligation presents a low potential for postoperative cardiac failure. In addition, the pericardial, diaphragmatic, sternal, and abdominal wall defects could be repaired relatively quickly. Human patients with cardiac defects routinely undergo two different procedures focused on either corrective or palliative cardiovascular surgery and repair of the diaphragmatic and associated body wall anomalies.⁹ The decision to treat Cantrell's pentalogy is controversial. Intact skin coverage has been documented as an important prognostic indicator for the viability of patients with this syndrome.⁹ Some authors therefore believe that the first step should be to repair wall defects overlying the heart and abdominal cavity to provide visceral protection and prevent infection.^9,14 Conversely, others believe that the limited cardiac output associated with the intracardiac defects would not enable patients to tolerate reconstruction of the body wall before such defects have been repaired.^14,15 Although every case should be evaluated individually, the study authors believe that cardiac surgery should be attempted first as intracardiac defects have a major influence on postnatal and postsurgical survival and, if possible, surgery should be delayed until optimal patient age and weight have been attained to achieve successful correction.¹⁵

The management of specific cardiovascular anomalies in this dog was focused on the closure of the PDA and repair of the pericardial defect. In contrast to the traditional approach in dogs (through a left, fourth intercostal space thoracotomy), the PDA was approached through the sternal cleft, which enabled excellent exposure and a routine occlusion after isolation of the persistent left cranial vena cava and dorsal retraction with the vagus nerve.¹⁷ The study authors chose to perform pericardial reconstruction in this dog because apposition of the unfused (but intact) pleuropericardial membranes represented a straightforward procedure that prevented direct contact of the heart with the adjacent sternal and diaphragmatic tissues thus limiting the potential risk of subsequent adhesions. That approach could be controversial because moderate-sized pericardial defects are rarely clinically significant and incidental defects are generally left untreated.¹⁸ Although not reported in dogs, in human cases where pericardial defects are incidentally diagnosed during interventional surgery for other reasons, subsequent adhesions have been shown to restrict cardiac mobility and, in some cases, induce chronic chest pain and nonspecific symptoms requiring subsequent surgical intervention.^16,18

Surgical correction of the sternal cleft is highly recommended to avoid the potentially increased risk of trauma-related injury to the heart, lungs, and major vessels. If left untreated, patients with sternal clefts might have impaired gas exchange, respiratory symptoms such as dyspnea and coughing, or recurrent pulmonary infections.² The repair of the sternal cleft in this 5 mo old patient was achieved by primary closure. During the first few months of life, the sternum can be easily closed surgically due to the elasticity and relative expandability of young cartilage compared to the adult bony chest wall.² The manner of approximation varies from primary suture closure, removing an inferior wedge of cartilage, or converting a partial sternal defect into a complete defect to enable suture approximation.¹⁵ Trial juxtaposition of the two halves of the sternebrae while observing physiologic parameters is mandatory before finalizing the apposition. Partial thymectomy has been reported in people as a simple procedure to reduce the risk of mediastinal compression to achieve primary closure.² In the event of further patient decompensation, autologous free grafts using either costal cartilage or iliac crest, myocutaneous flaps, or prosthetic repairs may be the only alternative.^2,20,21 Primary and autologous tissue repair provides an excellent functional and cosmetic outcome, in addition to the normal growth and development of the sternum. Its use may be preferable to prosthetic materials such as stainless steel mesh, Marlex acrylic, silicone elastomer, and Teflon, which have been associated with tissue reactions that result in bradycardia and/or hypotension and an increased risk of infection.^19,21 More recent studies reporting the use of new prostheses made from absorbable lactosorb copolymer^m or nonabsorbable^n,o biomaterials or calcium phosphate cement show encouraging results with no difference in the outcome compared to groups treated with primary closure.²

Pyothorax was the main postoperative complication reported in this dog. Duration of surgery (198 min) and/or eventual errors during management of the thoracic drain were critical factors that could be at the origin of this nosocomial infection. In a recent study, 6.5% of patients developed pyothorax following thoracic surgery.²² Surgical time was identified as one potential risk factor for this complication in dogs that required procedures with a similar timing as reported in this case.²² Infection has been previously stated as a drain-related complication.²³ In one study evaluating the short-term outcome of thoracic surgery in dogs, 22% of patients with a postoperative thoracic drain developed complications associated with the drain.²⁴ The duration of thoracic drainage was significantly longer in patients that developed drain-related complications (mean, 87. 2 hr; range, 8–164 hr) than in those that developed no complications (mean, 46.2 hr; range, 4–240 hr). Time of drainage in this case (114 hr) was long but consistent with previous results.²⁴

The prognosis for Cantrell's pentalogy in humans is poor.^8,13,14 Cases with incomplete expression have a better outcome (50% success rate) compared to the those with complete expression.^8,13 Nevertheless, there has been progressive improvement in the survival rate of complete expression variants from 5.5% in the first cases reported by Toyama in 1972 to 14.8 and 32% in more recent reviews.^8,13,14 Intracardiac defects have a major influence on postsurgical survival.¹⁴ The upgrade of definitive repair of the intrinsic cardiac defects has contributed to the improved survival in more recent human patients.^8,9,14 The case presented here and previous reports of dogs suffering from either a mild expression of complete or incomplete Cantrell's pentalogy had a favorable prognosis after single-stage surgical treatment.³ The prognosis in affected dogs may have been directly influenced by the conservative treatment implemented in three puppies presenting with ventricular septal defects and the absence of intracardiac defects in the rest of the patients.^3,12 Nevertheless, in cases presenting with ventricular septal defects, cardiac surgery might have been beneficial due to the development of cardiomegaly in the 6 mo postoperative period.¹²

Most common congenital heart diseases that are related to Cantrell's pentalogy have been treated successfully in dogs with either palliative procedures (such as the modified Blalock-Taussig technique for tetralogy of Fallot) or definitive corrective surgeries (such as open heart techniques requiring cardiopulmonary bypass for closure of atrial and ventricular septal defects and valvulectomy and patching in cases of failed interventional radiology balloon valvuloplasty for pulmonary stenosis).¹⁷ Results obtained in cases treated with those techniques show improved quality of life and satisfactory long-term follow up.¹⁷ These results represent an encouraging step for the definitive treatment of dogs suffering from the complete expression of this syndrome. Meticulous and systematic therapeutic management by a specialized team and financial constraints are the main disadvantages facing this line of management in newborn puppies.

Conclusion

This is the first case reporting a sternal cleft associated with an incomplete Cantrell's pentalogy with successful surgical repair. This case demonstrates that any midline ventral cranial abdominal wall, pericardial, diaphragmatic, or sternal defect requires a thorough physical examination and complementary exams to rule out any possible associated syndromes. Advances in cardiac surgery and results obtained in reported cases are encouraging for the surgical treatment of dogs with class 3 (incomplete) Cantrell's pentalogy. Nevertheless, more case studies are needed to determine the best management strategies and prognostic factors for this syndrome in dogs. It is the hope of the study authors that this report will increase clinical awareness and appropriate management of this condition.