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Surgical management of a strangulated inguinal hernia in a Cynomolgus Monkey (Macaca fascicularis): a case report with discussion of diagnosis, and review of literature

Traitement chirurgical d’une hernie inguinale étranglée chez un macaque cynomolgus (Macaca fascicularis) : cas clinique et discussion de la démarche diagnostique avec revue de la littérature
Baptiste Sadoughi, Manon Dirheimer, Pierrick Regnard et Fanélie Wanert

Résumés

Nous présentons un cas de hernie inguinale étranglée traité chirurgicalement chez un macaque cynomolgus mâle. Le patient présentait un choc sévère associé à un gonflement de l’aine et du scrotum à droite. Une laparoscopie a permis de mettre en évidence une hernie inguinale indirecte, réduite par hernioplastie suivie d’une castration unilatérale et de la suture de l’anneau inguinal. Après évaluation de l’intégrité de l’intestin, il a été décidé de ne pas réaliser d’entérectomie. Le patient a récupéré de l’intervention sans présenter de complications. Bien que la hernie inguinale soit une affection bénigne, la strangulation et la nécrose des anses engagent le pronostic vital. Nous discutons en dernière partie des symptômes évocateurs d’une strangulation lors de hernie inguinale et des options thérapeutiques.

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Notes de la rédaction

Submitted February 19, 2019, accepted after minor revisions April 16, 2019, published online April 26, 2019.

Texte intégral

1 Introduction

1An inguinal hernia is the protrusion of an abdominal organ through a defect in the abdominal wall in the groin region. The adipose tissue, the omentum and the intestinal loops are the most frequently involved organs (Abee et al., 2012; Bali et al., 2011). The protrusion occurs above the inguinal ligament as direct or indirect hernia. Direct inguinal hernias occur through the Hesselback’s triangle, a zone of muscular weakness in the abdominal posterior wall (Figure 1); indirect inguinal hernias develop laterally to the Hesselback’s triangle, from the deep inguinal ring down the inguinal canal. Indirect inguinal hernias are most commonly found in males because of the incomplete obliteration of the processus vaginalis at the time of testicular descent into the scrotum (Ohene-Yeboah et al., 2009; Ruhl and Everhart, 2007; Veen et al., 2007). Repair of inguinal hernias in humans is one of the most performed surgery worldwide (Kassam et al., 2014; Ohene-Yeboah et al., 2009) and only represents an emergency in about 1-3% (Kingsnorth and LeBlanc, 2003; Luijendijk et al., 2000) of patients with strangulation (Simons et al., 2009). Strangulation occurs when blood supply to the herniated structure is compromised leading to severe pain, swelling of the groin region, and eventually life-threatening ischemia, hypovolemic shock, and necrosis leading to perforation, peritonitis and sepsis. In humans, strangulated hernias leads to a tenfold increased risk of death compared to simple inguinal hernias (Harouna et al., 2000; Kingsnorth and LeBlanc, 2003; Waters et al., 1993). Compression of the vascular system may also result in testicular atrophy and ischemic orchitis in males (Kingsnorth and LeBlanc, 2003).

Figure 1

Figure 1

Schematic anatomy of the inguinal region. Adapted from Drake et al. 2010 : p. 289.

Représentation schématique de la région inguinale. A partir de Drake et al. 2010 : p. 289.

2The pathogenesis of inguinal hernias is similar in humans and non-human animals, with reports of inguinal hernias found in both small and large domestic animals (Al-Sobayil and Ahmed, 2007; Waters et al., 1993). Inguinal hernias have been described in several monkey species (Carpenter and Riddle, 1980; Chaffee and Shehan, 1973; Fox, 1971; Graham-Jones, 1960; Rawlings et al., 1971; Starzynski, 1965; Warren and Piccolie, 1979) and at least two ape species (Graham‐Jones, 1962; Pizarro et al., 2019; Taylor et al., 1989). Although they are considered common in macaques (Abee et al., 2012), published information is scarce with, to the authors’ knowledge, only two full text available (Graham-Jones, 1960; Starzynski, 1965). This report presents a new case of strangulated inguinal hernia in a macaque and its emergency surgical management.

2 Case report

3The patient, a fourteen-year-old adult male cynomolgus macaque (Macaca fascicularis), arrived at the Primate Center Silabe® (Fort Foch, 67207 Niederhausbergen, France) at the end of July 2016. It was housed in an individual cage (2.07 m high, 2.13 m wide, 1.76 m deep) with ad libitum food and water for a fifteen-day acclimatization. At mid-term, a routine clinical examination under ketamine sedation (Ketamine 1000 Virbac®, Virbac, France ; 10 mg/kg) revealed a reducible inguinal hernia without any associated symptoms. In accordance with internal standard procedures, the macaque received ivermectin (IVOMEC®, Merial, France ; 1 mg/3 kg) subcutaneously and intradermal tuberculination (old mammalian tuberculin, MOT) in the upper eyelid.

4Two days later, the patient was found lethargic and anorexic during the morning round although no physical alterations had been reported the previous evening. Clinical examination under anaesthesia (Ketamine 1000 Virbac®, Virbac, France ; 10 mg/kg) revealed a swelling of the right inguinal region, from the lower groin extending to the scrotum, and a mildly congested abdominal wall. The swelling was hard, non-reducible and measured 4 cm in diameter. Hypothermia (35.6°C), mild haematochezia and a weight loss of 8.5 % (660 g) since arrival were also reported.

5The history of reducible inguinal hernia associated with gastro-intestinal and general symptoms were indicative of a strangulated inguinal hernia (Harouna et al., 2000 ; Vallicelli et al., 2011). Immediately, the macaque was placed legs stretched in dorsal recumbency on a surgical table, and general anaesthesia was maintained with isoflurane (Vetflurane®, Virbac, France) vaporised in oxygen following endotracheal intubation. The right groin region was prepared aseptically for surgical procedures. Local anaesthesia was provided using lidocaïne (Xylovet®, CEVA santé animale, France ; 21,33 mg i.e. 1 mL per injection), and the patient received prophylactic antibiotics (Cobactan®, Intervet MSD Animal Health, United States ; cefquinome 2.2 mg/kg) and analgesia (tolfenamic acid, Tolfédine®, Vetoquinol, France ; 4 mg/kg, and buprenorphine, Buprécare®, Axience, France ; 0.01-0.02 mg/kg) intramuscularly. A vertical skin incision was made using scalpel blade from the lower groin to the mid scrotum medially to the swelling, and the hernial sac exposed by blunt dissection. Its incision revealed a congested intestinal loop and omentum partially engaged in the scrotum through the hernial ring which confirmed the diagnosis of indirect inguinal hernia. As our attempts at manually reducing the hernia failed, the incision was enlarged to pull out the hernial content (Figure 2). No adherences or rupture of the intestine were found under visual inspection, and although the bowel was dark red, no sign of necrosis was found, and vascular supply appeared maintained.

6The inguinal ring had to be enlarged by incising the musculature to reduce the hernia. The right spermatic vessels and ductus deferens were ligated at the level of the inguinal canal and the right testicle removed. Removal of all testicular structures allowed the hermetic closure of the inguinal ring with the cremaster muscle by an uninterrupted suture using non-absorbable size 3 polyamide monofilament (Dafilon®, B.Braun, Germany). Subcutaneous and skin edges were sutured respectively by simple continuous and “U” upright interrupted mattress sutures with absorbable polyglactin size 3.0 (Vicryl®, Ethicon, United-States). Aluminium was then applied to the wound (Aluspray®, Vetoquinol, France) to prevent infection.

Figure 2

Figure 2

Exposure of the hernial sac content by laparotomy. The intestinal loop (on the left) has a dark red colour consistent with acute inflammation due to entrapment. Adipose tissue on the omentum (on the right) was also externalized. Spermatic vessels and vascular structures are visible through the surgical opening.

Structures anatomiques herniées visibles après laparotomie. La couleur de l’anse intestinale (sur la gauche de l’image) révèle un processus inflammatoire aigu lié à la strangulation). Une partie de l’omentum (sur la droite de l’image) est externalisée, alors que le canal déférent et la vascularisation spermatique sont visibles par au site d’incision.

7Following surgery, the macaque was placed under a heat lamp for awakening. Mild hemorrhagic diarrhea was noticed for a few hours although the animal was alert. Soft food was provided four hours after the surgery and mixed with a gradually increasing portion of the usual diet over the next four days, while the macaque was kept in a squeeze cage. The patient received a second acid tolfenamic injection (Tolfédine®, Vetoquinol, France; 4 mg/kg) forty-eight hours postoperative, and buprenorphine (Buprécare®, Axience, France; 10-20 µg/kg) and cefquinome (Cobactan®, Intervet MSD Animal Health, United States; 2.2 mg/kg) were administered intramuscularly once daily for five days. The macaque experienced mild diarrhea for a week postoperative but exhibited normal behaviour and made an uninterrupted recovery. Two months later, the macaque was euthanized for research purposes. At necropsy, sutures of the inguinal ring were still holding, and the bowel had totally recovered without formation of adherences.

3 Discussion

8The diagnosis of inguinal hernia is first clinical and relies on suggestive history and presence of a bulge in the groin region during examination. The real challenge to veterinarians is to diagnose strangulation and evaluate its severity. Plain or contrast radio-imaging, ultrasonography and Computed Tomography may provide information on the content of the hernial sac and the integrity of the anatomical structure (Towfigh and Shafik, 2017). However, when no imaging device is available as in the present case, veterinarians need to rely on signs and symptoms for diagnosis (Figure 3). Abdominal pain, absence of flatus or stools, and abdominal distension are symptoms preceding shock that may orientate towards strangulation (Vallicelli et al., 2011). Occurrence of vomiting is strongly predictive of nonviable small bowels in dogs affected with inguinal hernias (Waters et al., 1993) and should therefore be closely monitored. Oedema and inflammation of the tegument at the hernial site are associated with bowel necrosis (Harouna et al., 2000), whereas swelling of the scrotum may suggest testicular inflammation or presence of an intestinal loop through the inguinal ring, both requiring early surgical care (Kingsnorth and LeBlanc, 2003). These symptoms should orientate towards surgical treatment instead of conservative therapy for asymptomatic inguinal hernias (Freeman, 2005 ; Simons et al., 2009). Intra-operative inflammation of the hernial sac and oedema of the bowel’s wall also indicate strangulation (Vallicelli et al., 2011). Adequate exposure of the hernial content is essential to visually assess its integrity. In presence of dark purple intestines, it is vital to check for the presence of a mesenteric pulse and intestinal motility. Reduction of the hernia restores blood supply which may lead to reperfusion injuries after liberation of free radicals. Intravenous bolus of alpha1-agonist drugs (bolus of ephedrine, 0.1-0.2 mg/kg every 10-20 min) can be administered to restore mesenteric pulse and prevent vasoplegia following the liberation of free radicals (Pr. Jack-Yves Deschamps, personal communication). Absence of motility, poor peripheral pulse or increased capillary refill time following hernia reduction and adrenergic drugs’ injections suggest nonviable small bowel segments requiring enterectomy. Enterectomy, meaning bowel resection, is a septic surgery that requires two sets of surgical instruments and is associated with increased risk of wound dehiscence postoperatively (Vallicelli et al., 2011). It is thus essential for veterinarians to accurately evaluate the severity of the strangulation as early as possible, to anticipate the surgical instruments and the manual skills mandatory to manage the needed surgery – simple hernia reduction or hernia reduction coupled with enterectomy.

Figure 3

Figure 3

Algorithm for clinical diagnosis of inguinal hernia nature and severity.

Algorithme décisionnel pour le diagnostic clinique et l’estimation de la sévérité d’une hernie inguinale.

9Surgical treatment of inguinal hernias is performed using either suture-repair or mesh-repair techniques. In veterinary medicine, suture repairs are applied regardless of body size (Al-Sobayil and Ahmed, 2007; Whitfield-Cargile et al., 2011), whereas meshes are usually used for large animals (Haupt et al., 2015; Kassam et al., 2014) and recently for the repair of an aseptic umbilical hernia in a chimpanzee (Pizarro et al., 2019). Comparisons of suture- and mesh-repair treatments reveal that, in humans, mesh lead to fewer recurrences and quicker return to normal activity for patients (Luijendijk et al., 2000; Nordin et al., 2002). However, their use is not recommended in the context of infected wounds or violated bowels (Kassam et al., 2014; Kingsnorth and LeBlanc, 2003; Breuing et al., 2010; Whitfield-Cargile et al., 2011). In the present case, suture-repair was successful as revealed by inspection at necropsy. Postoperative movements must be limited to reduce mechanical constraints applied to the groin region and prevent wound dehiscence, although minimal mobility is important to prevent adhesions at the surgical site. Both objectives were met in this case by placing the macaque in a restriction cage allowing horizontal movements only.

10Complications following abdomino-pelvic surgeries are wound infection, rupture of sutures, evisceration, intestinal fistula, and peritonitis in case of bowel strangulation leading to toxins and bacteria transudation (Harouna et al., 2000; Waters et al., 1993). In the current case, no complication except a mild sub-chronic diarrhea was observed. Recurrence is a common issue following indirect inguinal hernia repair. Despite an allegedly reduced recurrence rate in dogs following unilateral castration (Kingsnorth and LeBlanc, 2003; Waters et al., 1993), there is to date no strong data to recommend the ablation of the testis during inguinal hernia repair (Kassam et al., 2014). Although unilateral castration does not impair fertility, laboratory protocols may require unneutered or intact males. If so, the testis on the side of the hernia may be preserved and monitored for swelling or atrophy. In the present case, it was possible to unilaterally neuter the macaque without impairing its inclusion in future research protocol. Contralateral inspection of the inguinal ring is routinely performed in dogs, although unilateral hernias are more common than bilateral hernias (Jahromi et al., 2009). In the present case, the incision over the inguinal ring was made too lateral to allow direct inspection of the contralateral ring and, although bilateral inguinal hernia has never been officially reported in primates, it would have been appropriate to at least perform a careful palpation of the contralateral groin region.

11There is a lack of studies regarding inguinal hernias in primates. Although considered common in monkeys (Abee et al., 2012), no epidemiological data on hernias in macaques or even in primates are available to the authors’ knowledge. Retrospective data of quarantine health checks at arrival at Silabe from November 2015 to December 2017 show that 20.9 ± SE1.4% (n=845) of macaque males exhibited at least one scar suggestive of inguinal hernia surgery (Silabe’s unpublished data). Although it is neither possible to confirm the cause of these scars nor to explain why such a high proportion of cynomolgus monkeys may have undergone hernia surgery at the breeder, these preliminary results should draw attention to either lineage predisposition or prophylactic surgical procedures. Both congenital and acquired elements are suspected in the aetiology of inguinal hernia in both humans and domestic animals (Burcharth et al., 2013; Slatter, 2003). Inguinal hernias are known to be more common among males than among females (Al-Sobayil and Ahmed, 2007; Ohene-Yeboah et al., 2009; Ruhl and Everhart, 2007; Waters et al., 1993), and other factors such as race, age and obesity are also considered to predispose to inguinal hernia (Ruhl and Everhart, 2007). As inguinal hernia severity can vary from benign to extreme emergency in case of bowel strangulation (Ruhl and Everhart, 2007), the total absence of studies on the prevalence of inguinal hernia in macaques may therefore be of concern for laboratories and zoological institutions. Necropsy reports from Silabe since 2009 show that three acute deaths were attributed to strangulated inguinal hernia (unpublished data).

4 Conclusion

12A strangulated inguinal hernia is an emergency that needs to be quickly diagnosed and treated to avoid necrosis of the intestine that could lead to death. Although frequently encountered in macaques, the literature available on inguinal hernias is scarce, probably due to most inguinal hernias being benign. It may therefore be difficult for veterinary surgeons to objectively assess the severity of the strangulation. General and local symptoms can be monitored preoperatively and intraoperatively to assess the integrity of the intestine and help choose whether to perform enterectomy. Although no long-term follow-up was available, short and mid-term follow-up confirmed the validity of the care provided to the macaque. Epidemiologic studies on inguinal hernias in primates would be interesting to provide a perspective on the significance of the condition and to assess specific risk factors in primates.

Acknowledgments

13We thank Silabe and the Primate Centre of Strasbourg University for sharing scientific data and animal history. We are grateful to the animal care keepers especially Christelle Gandon, and to Helen Beyer, Animal Welfare Officer, for their assistance. We would also like to thank Gillian Hilburn for the English proofreading.

Competing interests

14The Authors declare that there is no conflict of interest.

Ethical considerations

15Silabe is licensed to house and use Non-Human Primates for scientific purposes by the French authorities (agreement n° A67-326-36). The animal was identified by both tattoo and electronic microchip according to European legislation and was imported in accordance with international regulations (CITES). The experiment in which the macaque was involved was approved by an ethical committee and received the authorization of the French Research Ministry referenced under n° APAFIS#5716-2016061714424948.

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Table des illustrations

Titre Figure 1
Légende Schematic anatomy of the inguinal region. Adapted from Drake et al. 2010 : p. 289.
URL http://journals.openedition.org/primatologie/docannexe/image/3372/img-1.png
Fichier image/png, 543k
Titre Figure 2
Légende Exposure of the hernial sac content by laparotomy. The intestinal loop (on the left) has a dark red colour consistent with acute inflammation due to entrapment. Adipose tissue on the omentum (on the right) was also externalized. Spermatic vessels and vascular structures are visible through the surgical opening.
URL http://journals.openedition.org/primatologie/docannexe/image/3372/img-2.jpg
Fichier image/jpeg, 332k
Titre Figure 3
Légende Algorithm for clinical diagnosis of inguinal hernia nature and severity.
URL http://journals.openedition.org/primatologie/docannexe/image/3372/img-3.png
Fichier image/png, 31k
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Référence électronique

Baptiste Sadoughi, Manon Dirheimer, Pierrick Regnard et Fanélie Wanert, « Surgical management of a strangulated inguinal hernia in a Cynomolgus Monkey (Macaca fascicularis): a case report with discussion of diagnosis, and review of literature », Revue de primatologie [En ligne], 9 | 2018, mis en ligne le 26 avril 2019, consulté le 23 octobre 2019. URL : http://journals.openedition.org/primatologie/3372 ; DOI : 10.4000/primatologie.3372

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Auteurs

Baptiste Sadoughi

Oniris - Ecole Nationale Vétérinaire, de l’Agroalimentaire et de l’Alimentation Nantes-Atlantique, La Chantrerie - CS 40307 Nantes cedex 3, France
Corresponding author : baptistesadoughi@gmail.com

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Manon Dirheimer

Plateforme Silabe ADUEIS, Centre de Primatologie Université de Strasbourg, Fort Foch, 67207 Niederhausbergen, France
Inserm, 16 avenue du Doyen Lépine, 69500 Bron

Pierrick Regnard

Plateforme Silabe ADUEIS, Centre de Primatologie Université de Strasbourg, Fort Foch, 67207 Niederhausbergen, France

Fanélie Wanert

Plateforme Silabe ADUEIS, Centre de Primatologie Université de Strasbourg, Fort Foch, 67207 Niederhausbergen, France
IHU Strasbourg Institut de Chirurgie Guidée par l’Image, 1 Place de l’Hôpital 67091 Strasbourg – France

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