Hernia (2011) 15:23–30 DOI 10.1007/s10029-010-0699-3

ORIGINAL ARTICLE

Bochdalek in the adult: demographics, presentation, and surgical management

S. R. Brown • J. D. Horton • E. Trivette • L. J. Hofmann • J. M. Johnson

Received: 21 December 2009 / Accepted: 12 June 2010 / Published online: 8 July 2010 Ó U.S. Government 2010

Abstract Conclusions Using modern surgical techniques to include Background Bochdalek are a very rare form of laparoscopy, repair can be performed safely, with a short diaphragmatic hernias. There are no robust studies that hospital stay, and with minimal morbidity or mortality. reveal the true natural history of this disease process. The aim of this study was to summarize clinically relevant data Keywords Diaphragmatic hernias Á Bochdalek hernias Á for the purpose of assisting surgeons with the work-up, Laparoscopic repair Á Congenital Á diagnosis, and treatment of adult patients with Bochdalek Posterolateral hernia hernia. Methods A literature search was performed using Pub- Med, Google scholar, EMBASE and the following key- Introduction words: Bochdalek hernia, congenital diaphragmatic hernia, and posterolateral hernia. All case reports and series after Bochdalek hernia (BH) is usually thought of as a perinatal 1955 that pertained to adults were included in the review. pathology associated with significant morbidity and mor- The following data points were queried: age, sex, presen- tality [1]. However, the surgical literature is stippled with tation, studies utilized during work-up, laterality, surgical case reports and small series of BH presenting in adults. In approach, hernia sac management, specific minimally the adult patient, there have been no large retrospective or invasive surgical techniques, and follow-up. prospective studies on BH. Due in part to the exotic nature Results A total of 124 articles comprising 173 patients of this hernia in the adult patient population, there are no met the inclusion criteria. Based on the data provided, well established indications for elective surgical repair. In several conclusions regarding this disease process can be addition, the clinical presentation may be confusing. made. Most patients present with symptoms related to their With the evolution of modern surgical technology, new hernia (86%). Pain is the most common complaint (69%). techniques for repairing these defects have been developed. While laparotomy is the most widely used surgical This review attempts to provide the clinician with an outline approach (38%), minimally invasive surgical techniques for the presentation, work-up, and surgical management of have gained popularity since their first report in 1995. BH. This analysis represents the most comprehensive Laparoscopic repair can be performed with a low compli- review to date on the topic of BH in adults. cation rate (7%) and short hospital stay (4 days).

Materials and methods

We conducted an English language literature search using S. R. Brown (&) Á J. D. Horton Á E. Trivette Á PubMed, EMBASE, and Google Scholar for every case L. J. Hofmann Á J. M. Johnson report, series, and literature review relating to BH in adults. Department of Surgery, William Beaumont Army Medical Center, 5005 North Piedras St, El Paso, TX 79920, USA Keywords included ‘‘Bochdalek hernia’’, ‘‘congenital dia- e-mail: [email protected] phragmatic hernia’’, and ‘‘posterolateral hernia’’. For the 123 24 Hernia (2011) 15:23–30 purposes of this review, all individuals 15 years of age and included: obesity, exertion, trauma, pregnancy, laughter, older were considered adults. All articles from November amusement park ride, recent weight gain, large meal, scuba 1955 until April 2010 were included in this study. Articles diving, diving from diving board, gymnastics, sexual inter- pertaining to the evaluation of BH in pediatric and or course, large meal, prior surgical repair (congenital), neonatal patients were excluded, as well as those studies retching, coughing, constipation secondary to medication that included the incidental discovery of BH on autopsy. effect, and COPD. More than one precipitating factor or Two authors extracted data from each article in a stan- inciting event was present in five cases. The most common dardized manner. Included in the analysis was the patient’s precipitating factor was pregnancy and the most common age, sex, laterality, presence of congenital abnormalities, inciting event was exertion, found in 13 and 7% patients, presenting symptoms, preoperative diagnostic studies, respectively. presence of precipitating factors, surgical approach, time of Only 14% of patients were asymptomatic at the time of diagnosis, additional surgical procedures, placement of presentation. Our analysis categorized the symptomatic chest tube, requirement for emergency surgery, defect size, patients according to the following manifestations: stran- presence of hernia sac, resection of the hernia sac, method gulation, obstruction, pulmonary symptoms, and pain, of hernia repair, recurrence, hernia sac contents, compli- bleeding, dysphagia, or GERD/dyspepsia; the percent of cations, postoperative stay, 30-day mortality, and follow patients presenting with each symptom is listed in Table 2. up. Due to the large numbers of small reports, only Pulmonary symptoms were defined as dyspnea, cough, and descriptive statistics were performed. . The pain/pressure category included patients with chest or abdominal discomfort that was not related to a . Results Several diagnostic modalities were used to evaluate patients with a BH. Many patients had multiple studies. Our search of the literature yielded 141 articles containing The most common study was chest X-ray (88%); followed 173 cases from 31 countries. Despite an English-language- by CT scan (39%), UGI/barium (33%), contrast enema only search strategy, we included authors from around the (10%), EGD (6%) and MRI (4%). world, including six Middle Eastern and six Asian coun- Authors reported surgical repair via five approaches: tries. The disciplines of general surgery, minimally inva- laparotomy, thoracotomy, laparoscopy, thoracoscopy, or sive surgery, thoracic surgery, internal medicine, and combined approach (Table 3). The review identified 17 radiology contributed articles for analysis. Of the 173 cases of laparoscopy in the literature. In nine of these cases, cases, 55% of patients were male and 45% were female the presence or absence of a hernia sac was not recorded. (Table 1). The mean age of men and women was 39 years Three laparoscopic cases identified the presence of a hernia and 41 years, respectively, with a range of 15–88 years. sac [2–4], while the remaining six cases stated there was no The hernia defect was located on the left side in 78% of hernia sac. The hernia sac was not resected in these cases. patients, on the right side in 20%, with bilateral hernias found in 2% of the patients. The size of the defect was not Table 2 Presenting symptoms and the percentage of patients with related to laterality. those symptoms Factors precipitating symptoms or an inciting event were Presenting symptoms defined as any factor or event that the article’s author felt contributed to the patient’s presentation. A precipitating Asymptomatic 14% factor or an inciting event was present in 25% of cases and Pain/pressurea 69% Obstruction 39% Pulmonary symptoms 37% Table 1 Demographic information for the patients included in this Strangulated 28% review Dysphagia 3% Demographics and laterality (N = 173) Results Bleeding 4% Average age (years) 40 GERD 4% Female 45% Other (HTN, fatigue, indigestion) 9% Precipitating factor/inciting event 25% Symptoms for less than 1 month 47% Congenital anomalies 12% The majority of patients were symptomatic at presentation and the Right sided 20% symptom of pain was specific for pain not related to obstruction or Left sided 78% strangulation a Bilateral 2% Located in chest or abdomen, not related to obstruction/ strangulation 123 Hernia (2011) 15:23–30 25

Table 3 Comparison of surgical approaches Laparotomy Thoracotomy Laparoscopy Thoracoscopy Combined

Choice of surgical approach 38% (53/141) 32% (45/141) 12% (17/141) 3% (4/141) 16% (22/141) Diagnosis prior to surgery 65% (30/46) 51% (23/45) 65% (11/17) 100% (4/4) 67% (10/15) Emergency surgery 42% (19/45) 13% (6/45) 19% (3/16) 0% (0/4) 56% (10/18) Size of defect (cm2)42(n = 20) 38 (n = 15) 45 (n = 11) NS 36 (n = 9) Resection of hernia sac 20% (1/5) 50% (4/8) 0% (0/3) 0% (0/2) NS Primary repair 95% (40/42) 82% (31/38) 53% (8/15) 100% (4/4) 67% (12/18) Interposition mesh graft 7% (3/42)a 21% (8/38)a 60% (9/15)b 25% (1/4)a 39% (7/18) Complications 18% (9/51) 16% (6/36) 6% (1/16) 0% (0/3) 38% (6/16) 30 Day mortality 2% (1/50) 5% (2/43) 0% (0/15) 0% (0/4) 0% (0/20) Hospital stay, days (mean) 10 (n = 24) 20 (n = 16) 4 (n = 11) 5 (n = 4) 13 (n = 11) Recurrence 0% (0/48) 0% (0/42) 0% (0/16) 0% (0/4) 0% (0/22) Follow-up, months (mean) 22 (n = 21) 38 (n = 14) 26 (n = 11) 8 (n = 1) 8 (n = 11) a One was combined primary repair reinforced with mesh b Two with combined primary repair reinforced with mesh

Primary closure was performed in 53% of laparoscopic diaphragm, where a BH develops. Complete closure occurs cases, with 60% of cases incorporating mesh into the on the right side before it is complete on the left side—a repair. One case resulted in a stated complication, which fact that may contribute to the left sided BH being more was a pneumothorax immediately postoperatively requiring common than right sided hernias. a chest tube [5]. Only four cases using the thoracoscopic approach have been reported in the English literature [6–9]. Incidence and presentation

The incidence of asymptomatic BH in the adult population Discussion has been well characterized. The best data regarding the incidence of BH comes from Mullins and colleagues, who History reviewed 13,138 CT scans. This study revealed an inci- dence of 0.17%, with 68% being right-sided defects and Clinicians are perhaps most familiar with BH as a serious 77% of the patients being female [11, 12]. It is important to neonatal pathology. First described in 1754 by McCauley, note that the demographics of asymptomatic BH differ who described the clinical course and postmortem anatomy from those with symptomatic defects. Data included in our of an infant, the defect was further characterized and study from primarily symptomatic patients had different popularized by Vincent Alexander Bochdalek in 1848, for results than the Mullins study. These differences may which the condition is eponymous [10]. suggest that BH that occurs in females or on the right side may yield clinically silent disease. Previous reports have Embryology speculated that left-sided defects may be more likely to produce symptoms than right-sided defects [1], which is Embryologically, the development of the diaphragm occurs supported by this data. during the 4th week of gestation. At the inferior portion of The majority of patients (86%) present with symptoms the pericardial cavity, the central tendinous area of the attributed to their hernias, of which pain (66%) and diaphragm develops from the septum transversum, which obstruction (38%) are the most common. Almost one-half separates the thoracic and abdominal cavities. By the present acutely, with 47% presenting with symptoms 6th week, the pleuroperitoneal folds on the lateral body present for 1 month or less. wall grow medially and fuse with the septum transversum. The diagnosis of BH is often difficult to make, due to the During the 8th week of development, the canal between the wide variation in presenting symptoms and the rarity of this septum transversarum and the esophagus closes. The fusion hernia defect. Thomas reported a 38% rate of misdiagnosis of these two muscle groups occurs only in the final stages in his review published in 1991 [13]. In this review, 65% of of development and, as such, are anatomically vulnerable BH cases were diagnosed preoperatively. It must be noted loci. It is at this fibrous lumbocostal trigone, the junction of that misdiagnosis or a delay in diagnosis is not without the lumbar and costal muscle groups in the posterolateral consequence to the patient. Physical exam findings can

123 26 Hernia (2011) 15:23–30 include diminished ipsilateral breath sounds and/or bowel factor, or 8% of cases overall. Pregnancy was also over- sounds within the chest [14]. Misdiagnosis can lead to represented with respect to cases requiring emergency inappropriate interventions such as chest tube placement surgery, with 12% of all such cases being pregnant. Of [15–18]. Failure to promptly diagnose and treat a symp- note, in 1988, Kurzel reported the first successful (survival tomatic BH may lead to strangulation and death [19]. of mother and infant) repair of an acutely symptomatic BH Fingerhut et al. [20] provide additional clinical clues to during pregnancy [45]. consider when evaluating patients with suspected BH: (1) Adult patients presenting with BH may have associated postprandial respiratory symptoms, (2) abdominal or tho- congenital defects. Twelve percent of patients in our study racic symptoms aggravated by the supine position, (3) had an associated abnormality. Associated congenital radiographic abnormalities while supine, and (4) abdomi- anomalies included malrotation [22, 46–48], incomplete nal symptoms aggravated by physical effort. attachment of the cecum [49], hepatic hypoplasia [10, 34, Some authors have suggested that right-sided defects are 42, 50], bifid liver [51], [34], Chi- larger and less likely to produce symptoms [21]. While this laiditi’s syndrome [29], Marfan’s syndrome [52], mitral/ difference in defect size is a logical explanation, our data tricuspid valve prolapse [53], patent ductus arteriosus, demonstrated no appreciable difference in the size when pulmonary sequestration [54], Down’s syndrome [55], comparing left-sided vs right-sided defects (39 cm2 vs accessory lung lobe [56], congenital pulmonary blebs [57], 37 cm2). For BH, the defect usually contains several organs asplenia, deafness [58], accessory diaphragm, aberrant with the following frequencies noted in our study: colon systemic artery to right lower lobe, and anomalous pul- 63%, stomach 40%, omentum 39%, small bowel 28% monary vein [59]. (Fig. 1). Radiographic evaluation Precipitating factors Radiologic studies should be utilized during the evaluation A precipitating factor was found in 25% of cases. The of a patient with a suspected BH. The diagnosis of BH underlying feature common to all of the precipitating fac- should be considered any time an air meniscus sign is tors is an increase in intra-abdominal pressure These fac- present on a chest X-ray [60]. However, BH may be dif- tors or inciting events included pregnancy [2, 3, 22–28], ficult to appreciate on chest X-ray (Fig. 2), and a previ- chronic constipation [29], vigorous physical activity [30– ously normal film does not preclude this diagnosis [61, 62]. 33], severe coughing/COPD [34, 35], fits of laughter [36, Use of CT represents an excellent diagnostic modality. BH 37], hanging upside down on an amusement park ride [38], can be diagnosed readily on CT scan (Figs. 3, 4)[63]. diving from a diving board [39], retching [40], heavy meals Three-dimensional reconstruction of CT scans may [41], and trauma [42, 43]. Late recurrence after BH repair enhance a clinician’s ability to visualize a defect [64]. MRI as a neonate has also been reported [44]. is also a suitable approach. Sagittal and coronal MRI can Pregnancy was the most common precipitating factor, accounting for 34% of cases with at least one precipitating

Fig. 1 Laparoscopic view of a Bochdalek hernia (BH) with herni- Fig. 2 Chest X-ray of a patient with a left sided BH, demonstrating ation of omentum and small bowel into the thorax the difficulty in appreciating a hernia defect in some patients 123 Hernia (2011) 15:23–30 27

[9]. Clinicians should take great care during upper endos- copy of patients suspected of having a BH, as sudden car- diovascular collapse has been reported in this setting [66]. Ultrasound features of BH include a fragmented dia- phragm, accordion-like spleen, and inability to view the spleen and kidney within the same plane [67]. Other modalities used to evaluate a patients with BH include fluoroscopy, bronchograms, and pulmonary angiography [59].

Surgical intervention

The first successful repair of a BH was performed in 1901 by Aue [22]. With the advancement of modern surgical techniques, less invasive means of repair are available. The first reported repair of BH using thoracoscopic technique was performed by Silen in 1995 [8], and the first reported laparoscopic repair in adults was performed by Al-Emadi in 1998 [68]. Based on the wide variation in presenting symptoms it is Fig. 3 CT-scan is a useful imaging modality in patients with a suspected BH unknown if any BH is truly asymptomatic. Most authors recommend hernia repair for all fit surgical candidates regardless of symptoms [49, 54, 62, 69–73] and, while we agree, we also feel this should include those patients diagnosed incidentally on abdominal imaging. For emer- gent cases, laparotomy was the most common approach (Table 3) Trans-abdominal surgical approaches have included midline, paramedian [74], and subcostal incisions [72]. Some surgeons place chest tubes after the abdominal approach [28, 33, 75–79], while others prefer to evacuate the thorax through a transabdominal suction catheter prior to closing the abdomen. For the laparoscopic approach, we agree with other surgeons [69, 71] and recommend placing the patient in a lateral decubitus, reverse trendelenburg position. Repair of strangulated hernias have been reported using minimally invasive techniques [17, 76, 80]. When hernia contents are incarcerated, the diaphragm may need to be opened radi- ally in order to reduce associated viscera. Patients with strangulated hernias may require extensive resection of hernia contents and reconstruction [81]. For primary repair, BH defects are typically closed along their transverse axis Fig. 4 This image reveals a left sided herniation of abdominal in a medial to lateral fashion [33] (Figs. 5, 6). contents into the thorax In contrast to Morgagni hernias, BH rarely contains a hernia sac. Only 18 patients in this study had a hernia sac. Previous reports state that a non-muscularized hernia sac reveal discontinuity of the soft tissue lines of the dia- will be present in 10–15% of patients with CDH. Some phragm [65]. authors propose that rupture of the hernia sac may be the Patients being considered for thoracic repair should first event in the stepwise progression from asymptomatic undergo an upper gastrointestinal series to rule out the to symptomatic presentation [13, 82]. When a hernia sac is presence of malrotation. Identification of malrotation dic- present, some authors recommend sac excision [83], while tates repair through an abdominal approach [8, 61]. Upper others report placing a closed suction drain within the gastrointestinal series may show an ‘‘upside-down stomach’’ hernias sac postoperatively [3]. Conversely, the absence of 123 28 Hernia (2011) 15:23–30

and the frequency of mesh usage did not differ substan- tially with respect to laterality or size of defect. Patient undergoing both open and laparoscopic repair have had excellent outcomes. Due to the small cohort, conclusions regarding the superiority of primary repair vs interposition mesh graft vs primary repair with mesh reinforcement cannot be substantiated. No recurrences were identified in this review. Ahrend was the last author to report a mortality after a BH repair, which occurred in 1947 [88]. After repair, patients may experience improve- ment in pulmonary function tests [89, 90]. Several authors report prolonged gastric ileus and gastroesophageal reflux following repair [45].

Fig. 5 Laparoscopic image of a BH defect after the hernia contents Conclusion have been reduced, and prior to primary repair Bochdalek hernias in the adult commonly present with symptoms, usually pain or obstruction. These hernias have a propensity to occur on the left side and are more fre- quently diagnosed in males. The differential diagnosis can be quite large and advanced imaging technology may prove helpful. Most individuals with BH have precipitating fac- tors that increase intra-abdominal pressure—the most common and most dangerous of which is pregnancy. Misdiagnosis of BH is common, and failure to diagnose and treat promptly resulted in additional procedures, increased morbidity, and a higher complication rate. The use of laparoscopy and thoracoscopy are safe surgical approaches with low morbidity and shorter hospital stay, and the application of mesh appears well tolerated. Sur- geons familiar with these techniques should consider one Fig. 6 Laparoscopic image captured after the primary repair of a of these approaches when treating patients with BH. hernia defect a hernia sac in a BH allows for the pleural and peritoneal References space to communicate directly. Hence, surgeons choosing a laparoscopic technique should be aware that intraoperative 1. Kocakusak A, Arikan S, Senturk O, Yucel AF (2005) Boch- dalek’s hernia in an adult with colon necrosis. Hernia 9(3):284– and postoperative pneumothorax can occur with pneumo- 287 peritoneum [5]. Placing a cannula or trocar through the 2. Palanivelu C, Rangarajan M, Maheshkumaar GS, Parthasarathi R chest wall during laparoscopic repair can provide a release (2008) Laparoscopic mesh repair of a Bochdalek diaphragmatic valve in the event that tension physiology develops. hernia with acute gastric volvulus in a pregnant patient. Singa- pore Med J 49(1):e26–e28 In 1975, Christiansen reported the first repair of a BH in 3. Senkyrik M, Lata J, Husova L, Dite P, Husa P, Horalek F et al an adult using synthetic mesh [73]. Since then, surgeons (2003) Unusual Bochdalek hernia in puerperium. Hepatogastro- have used a variety of different types of mesh including enterology 50(53):1449–1451 Dacron [73, 84], Prolene (Ethicon, Somerville, NJ) [70], 4. Wadhwa A, Surendra JB, Sharma A, Khullar R, Soni V, Baijal M et al (2005) Laparoscopic repair of diaphragmatic hernias: Parietex (Sofradim, Trevoux, France) [2, 24], Gore-Tex experience of six cases. Asian J Surg 28(2):145–150 Dual Mesh (Gore Medical, Flagstaff, AZ) [85, 86], Marlex 5. Takeyama K, Nakahara Y, Ando S, Hasegawa K, Suzuki T [6, 32, 45, 87], and Surgisis (Cook Urological, Fort Worth, (2005) Anesthetic management for repair of adult Bochdalek TX) [71]. However, some authors [71] discourage the use hernia by laparoscopic surgery. J Anesth 19(1):78–80 6. Mousa A, Sanusi M, Lowery RC, Genovesi MH, Burack JH of polypropylene mesh, as it can become adherent to (2006) Hand-assisted thoracoscopic repair of a Bochdalek hernia abdominal viscera. In this review, the surgical approach in an adult. J Laparoendosc Adv Surg Tech A 16(1):54–58

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