Diaphragmatic Hernia of the Stomach with Gastric Rupture in a Domestic Pig

Case Study Diaphragmatic Hernia of the Stomach with Gastric Rupture in a Domestic Pig

Lori R Hill,1,* Steven Y Huang,2 and Mihai Gagea1

A 5.5-mo-old castrated, male Red Duroc pig presented acutely with depression and abdominal pain 9 d after an altercation with another pig. A CT examination indicated right pneumothorax and herniation of the stomach into the thoracic cavity. Due to a poor prognosis, the pig was euthanized. A necropsy and gross examination revealed a tear of the diaphragmatic muscle in the region of the esophageal hiatus through which the stomach was displaced into the right side of the thoracic cavity. In addition, the herniated stomach had a rupture of the stomach wall through which the gastric mucosa was everted and exposed into the right thoracic cavity. The right thoracic cavity had acute fibrinous pleuritis, and the right lung was collapsed. CT scans performed every 1 to 2 wk for 2 mo prior to the pig’s death did not reveal any abnormalities in the diaphragm. Trauma was considered the most likely cause of the diaphragmatic tear and subsequent herniation and rupture of the stomach.

Abbreviation: DH, diaphragmatic hernia

Hernias involving the diaphragm comprise 3 main types: peri- strenuous activity or dystocia can be contributing factors. In cattle toneopericardial, in which abdominal organs extend into the and water buffalo, trauma can lead to herniation of the reticu- pericardial sac; pleuroperitoneal, in which abdominal organs lum.21 DH in conjunction with intrathoracic gastric rupture has are found within the pleural cavity; and hiatal, in which the ab- been described in humans; contributing factors include pregnan- dominal esophagus, gastroesophageal junction, or portions of cy, 22 gastric ulceration,23 strangulation,6 gastroplasty,30 bariatric the stomach protrude through the esophageal hiatus of the dia- surgery39 and volvulus.33 phragm into the thoracic cavity.21 DH is uncommon in swine. There have been a few reports of The esophageal hiatus lies in the muscular part of the dia- fatal epizootics of DH in growing swine (birth to 4 mo of age), phragm between the 2 medial divisions of the right crus. The but a conclusive etiology could not be determined in any of the esophagus with its supplying vessels and the vagal nerve cases.14,15,26,31,40,42 We here report a unique case of a pig with a dia- trunks pass through this opening.11 Of the 3 openings in the phragmatic hiatal tear and herniation of the stomach into the tho- diaphragm (caval, aortic, and esophageal), the esophageal hia- racic cavity with subsequent rupture of the herniated stomach tus is the weakest because it is formed by pliable muscle, in wall. contrast to the fibrous tendons of the other 2 hiatuses, and is therefore more susceptible to herniation. Hiatal hernias are Case Report usually characterized by protrusion of the stomach into the History and clinical observations. The 5.5-mo-old castrated thoracic cavity through a widening of the right crus of the dia- male Red Duroc pig had been purchased for a research project phragm.7 from a producer whose primary business purpose is to sell pure- Diaphragmatic hernia (DH) occurs in humans25 and in numer- bred boars, gilts, show pigs, and semen. All new sows added to ous other species including ,ruminants,5,8,10,35 horses,27 wild16 and the herd are isolated for 45 d and tested for pseudorabies, brucel- domestic canids and cats,19 NHP,29 swine,14,15,26,31,40,42 and rabbits.12 losis, and porcine reproductive and respiratory syndrome. Sows In dogs, DH has been associated with muscular dystrophy3 and and boars are routinely vaccinated against porcine parvovirus, reported as a complication of tetanus.1 More specifically, hiatal leptospirosis, erysipelas, porcine reproductive and respiratory DH has been reported in cattle,2 dogs,28,36 marine mammals,4,13,34 syndrome, and swine influenza. At 5 and 2 wk prior to farrowing, wild17 and domestic cats,24 and the maned wolf.16 In small ani- sows are vaccinated with Clostridium perfringens type C, Esch- mals, such as dogs and cats, automobile-related trauma is a com- erichia coli bacterin–toxoid, Bordetella bronchiseptica, erysipelas, mon cause of DH, although congenital defects of the diaphragm and Pasteurella multocida bacterin–toxoid. At 2 wk after farrowing, also can result in herniation. In horses, in addition to trauma, sows are vaccinated against leptospirosis and erysipelas. Piglets and adult animals are routinely dewormed. Neonates are injected Received: 14 Dec 2015. Revision requested: 01 Feb 2016. Accepted: 03 Feb 2016. with iron, penicillin, and tulathromycin (Draxxin, Pfizer Animal 1Department of Veterinary Medicine and Surgery, Division of Basic Science Research, and 2Department of Interventional Radiology, Division of Diagnostic Imaging, The University Health, New York, NY) and are vaccinated against Mycoplasma of Texas MD Anderson Cancer Center, Houston, Texas hyopneumoniae. At 3 to 4 wk of age, pigs are vaccinated against M. *Corresponding author. Email: [email protected] 399 Vol 66, No 5 Comparative Medicine October 2016

hyopneumoniae, erysipelas, circovirus, swine influenza, M. hyorhi- nis, M. hyosynoviae, and Streptococcus parasuis. The University of Texas MD Anderson Cancer Center is an AAALAC-accredited institution, and all experimental manipula- tions were approved by the Center’s IACUC. Swine are housed and cared for in accordance with the Guide for the Care and Use of Laboratory Animals,20 Public Health Service policy,38 and the Ani- mal Welfare Act and Animal Welfare Regulations.37 The health of all animals is monitored daily. The pig arrived at our animal facility at the age of 3 mo. He was pair-housed in an indoor run on elevated, plastic-coated, wire- mesh flooring. A fecal examination performed on intake was neg- ative for pathogenic parasites. At 15 d after arrival, the pig was entered into a study investigating a novel absorbable filter that was placed in the inferior vena cava for the prevention of pulmonary embolism. On the day of surgery, the pig was anesthetized, and blood was collected for baseline measurements (CBC, serum chemistry profile, and arterial blood gases). CT and a digital subtraction venacavagram were performed to determine the geometry of the inferior vena cava. Under ultrasound guidance, a 21-gauge needle was used to access the right common femoral vein. A 16-French sheath was advanced into the inferior vena cava to allow deployment of the resorbable filter. After filter deployment, inferior vena cava pressure was measured cephalad (cranial) and caudal to the inferior vena cava filter. Digital subtraction and CT venography were performed to evaluate filter positioning and detect potential filter-related complications. Blood was again collected to assess changes in hematology, serum chemistry, and arterial blood gas values. At 4 d after filter deployment, an autologous thrombus Figure 1. A coronal image taken 11 d prior to symptom onset demon- was introduced into the filter by using the same method of access. strates a normally positioned stomach (thick arrows) below the dia- Pre- and postprocedural bloodwork, pressure measurements, CT phragm. The expected position of the gastroesophageal junction is in- imaging, and digital subtraction venacavagrams were performed. dicated (thin arrow). Bloodwork, pressure measurements, and imaging were repeated 5 times at intervals of 7 to 14 d. No abnormalities were detected in the majority of the stomach was herniated into the right lower any of the diagnostic tests or imaging studies performed through- thorax. In addition, a tension pneumothorax was present in the out the study, and the pig was clinically normal until the 61st day right thoracic cavity, with a small amount of extraluminal air be- of the experiment, when he presented with a spontaneous, acute low the diaphragm (Figure 2) . illness and was euthanized on the same day. Necropsy findings. The pig was euthanized by exsanguination Social housing of social species is the default method at our in- under general anesthesia, which was followed by a complete stitution. The subject pig’s social partner was euthanized in the necropsy and gross examination of internal organs. Body weight course of the study. The next day (2 d after the subject’s most recent at the time of necropsy was 59 kg. After opening the abdominal CT scan, which was normal), an attempt was made to house the cavity, we observed that approximately 80% of the stomach was subject (54.4 kg) with another pig of similar size. It became evident displaced into the thoracic cavity through a 5-cm linear tear or immediately that the animals were incompatible, because they en- rupture of the diaphragmatic muscle in the region of the esopha- gaged in an aggressive altercation. Therefore, a decision was made geal hiatus. The stomach was twisted and strangulated at the site to house the 2 pigs separately for the remainder of the study. The of herniation through the diaphragmatic rupture (Figure 3 A) . only abnormality observed on examination of the subject after the The abdominal surface of the diaphragm had a red area in the fight was a shallow laceration of the pinna. At 9 d after the fight, the central portion of the ventral region, consistent with acute or sub- subject presented spontaneously with acute depression, anorexia, acute hemorrhage and trauma. The abdominal cavity contained a and reluctance to stand. On physical examination, palpation of the large amount of clear and pale-yellow proteinaceous fluid, which abdomen resulted in splinting of the abdominal musculature. The clotted within 10 min after exposure to room temperature air. The pig was anesthetized, and CT was performed. The constellation of gallbladder was markedly distended with bile content, likely due CT imaging findings in combination with the pig’s acute clinical to extension of the ductus choledochus which, combined with the presentation were consistent with a rupture of the diaphragm with displacement of stomach, impaired the normal flow of bile into intrathoracic displacement of the stomach. In light of these results the duodenum. and the poor prognosis, the pig was euthanized. The stomach was herniated through the diaphragmatic rupture Images acquired 2 d prior to the fight demonstrated a normal only into the right side of the thoracic cavity. The herniated part thorax and a normally positioned stomach lying below the dia- of the stomach had diffuse, marked congestion and edema and phragm, with the gastroesophageal junction in the expected posi- a 4-cm tear of the stomach wall through which the gastric mu- tion (Figure 1). CT imaging on the day of necropsy showed that cosa was everted (Figure 3 B and D). The right side of the thoracic

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Figure 2. CT images on the day of necropsy. (A) A scout image demonstrates a tension pneumothorax on the right (arrowheads). (B) Axial, (C) coronal, and (D) sagittal images demonstrate displacement of the stomach into the right lower chest (arrows). The tension pneumothorax is located anteriorly (ventrally) on the axial image (**).

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Figure 3. DH and intrathoracic rupture of the stomach, gross lesions. (A) Abdominal cavity image showing the normal part of the stomach (ns) that remained in the abdominal cavity, the site of stomach herniation with twisting and strangulation of the stomach (white arrow), the area of diaphragmatic hemorrhage (black arrow), and the markedly distended gallbladder (gb). (B) Mucosal surface of the stomach with the site of gastric cardia (gc), an area of normal stomach (ns), and an area of herniated stomach (hs) with the site of the rupture of the stomach wall (rs). (C and D) Thoracic cavity images showing the atelectatic right lung (arl), abundant fluid and fibrin (f) in the pleural cavity, and herniated stomach (hs), with everted and exposed edematous gastric mucosa. cavity contained a large amount of yellow to pale-red fluid and swine. One report42 involved 3 families of swine in which DH copious yellow fibrinous material attached to the pleural surface was observed from birth to 4 mo of age. Bilateral and right- or of the lung and thoracic wall, which were mixed with a small left-sided defects were observed. An autosomal recessive mode amount of gastric ingesta (Figure 3 C and D). The right lung was of inheritance was suspected but not verified.42 There have been a collapsed and diffusely red. These lesions confirmed the diag- few reports of fatal epizootics of DH in growing swine (birth to 4 nosis of acute hiatal hernia of the stomach into the right thoracic mo of age), but a conclusive etiology could not be determined in cavity through a diaphragmatic tear, with subsequent rupture of any of the cases.14,15,31,33,40 The nature of the diaphragmatic defects the herniated stomach wall, acute fibrinous pleuritis, and diffuse varied. A report of DH in a commercial production herd involved atelectasis of the right lung. The tear of the diaphragmatic muscle animals between 21 and 70 d of age.14 Diaphragmatic defects with was longitudinal or parallel to the muscle fibers and had rough smooth, rounded edges (indicating chronicity) involved the right margins, with a small amount of blood on the surface. midportion of the diaphragm (with herniation of the large and small intestines), the right and left fibrous portions, or the central Discussion part of the diaphragm in the area of the esophageal hiatus (resulting in herniation of abdominal organs into the pericardial sac). Inguinal and umbilical hernias are the most prevalent congeni- The anomalies were so prevalent that elimination of the entire tal disorders in pigs,9 and the heritability of these abnormalities herd was necessary. No etiology could be determined.14 Epizo- has been confirmed.32,41 Conversely, DH is uncommon in pigs. otics in 4 different herds in another report involved swine be- Although many studies suggest that genetic factors are involved tween 3 and 16 wk of age.31 Defects involved the right, tendinous in development of congenital DH in humans,18,25 heritability of portion of the diaphragm with herniation of the right lobe of the DH has been proposed but not conclusively demonstrated in

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liver, intestine, cecum, and colon. A genetic predisposition was 3. Bedu AS, Labruyere JJ, Thibaud JL, Barthelemy I, Leperlier D, not confirmed by the evidence, nor was trauma. An association Saunders JH, Blot S. 2012. Age-related thoracic radiographic changes with injectable combinations of vitamin E and sodium selenite in golden and labrador retriever muscular dystrophy. Vet Radiol was proposed but could not be verified.31 Ultrasound 53:492–500. 4. Biancani B, Field CL, Dennison S, Pulver R, Tuttle AD. 2012. Possible predisposing factors to DH in pigs include congenital Hiatal hernia in a harbor seal (Phoca vitulina) pup. J Zoo Wildl Med malformation, abnormal weakness of the diaphragmatic muscle, 43:355–359. 32 vitamin E or selenium deficiency, and trauma. In our case, con- 5. Black-Schultz LL, Hanson PD, Wilson DG, Markel MD. 1993. genital malformation was ruled out because there was no his- Diaphragmatic hernia in a llama. J Am Vet Med Assoc 202:410–412. tory of DH in the herd of origin. The serial CT images obtained 6. Brume J, Driscoll P, Meehan SE, Pringle R. 1986. Strangulated until 2 d prior to the fight did not reveal any abnormalities in the para-oesophageal hiatus hernia with gangrene and perforation of diaphragm, and the gross examination of the diaphragm did not stomach. Br J Clin Pract 40:127–128. reveal any developmental abnormalities. Rather, the red area of 7. Dean C, Etienne D, Carpentier B, Gielecki J, Tubbs RS, Loukas M. 2011. Hiatal hernias. Surg Radiol Anat 34:291–299. the tendinous diaphragm in the midventral region, distant from 8. DeVilbiss B, Ziegler J, Righter D, Allen A, Barrington G, Haldorson the area of diaphragmatic tear (Figure 3 A), was consistent with G. 2011. Diaphragmatic hernia in a 2-y-old alpaca (Vicugna pacos). J hemorrhage and trauma of the diaphragm. The lesion could have Zoo Wildl Med 42:513–517. been the result of trauma to the sternal region, although the ribs, 9. Ding NS, Mao HR, Guo YM, Ren J, Xiao SJ, Wu GZ, Shen HQ, sternum, and other surrounding tissues were normal grossly. Wu LH, Ruan GF, Brenig B, Huang LS. 2009. A genome-wide scan The experimental manipulation of the pig had no identifi- reveals candidate susceptibility loci for pig hernias in an intercross able association with the diaphragmatic tear and intrathoracic between white duroc and erhualian. J Anim Sci 87:2469–2474. herniation of the stomach. The accumulation of large amounts 10. Divers TJ, Smith BP. 1979. Diaphragmatic hernia in a cow. J Am Vet Med Assoc 175:1099–1100. of proteinaceous, clear fluid in the abdominal cavity was likely 11. Dyce KM, Sack WO, Wensing CJG. 1987. Textbook of veterinary unrelated to the experimental implantation of the intravascular anatomy. 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Institute for Laboratory Animal Research. 2011. Guide for the care and use of laboratory animals. Washington (DC): National Academies edema that weakened the stomach wall. Press. In conclusion, diaphragmatic trauma was the most likely cause 21. Kahn CM, Line S. 2011. The Merck veterinary manual. Whitehouse of this unusual case of DH of the stomach with intrathoracic rup- Station (NY): Merck. ture of the gastric wall in a domestic pig. DH should be consid- 22. Luu TD, Reddy VS, Miller DL, Force SD. 2006. Gastric rupture as- ered as part of the differential diagnosis for swine that develop sociated with diaphragmatic hernia during pregnancy. Ann Thorac acute abdominal pain or respiratory distress secondary to a trau- Surg 82:1908–1910. matic event. To our knowledge, this report is the first description 23. Maa J, Lubbock C, Harrison M, Corvera C. 2009. 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