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Hiatal hernia diagnosis prospectively assessed in obese patients before bariatric surgery: accuracy of high-resolution manometry taking intraoperative diagnosis as reference standard

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https://doi.org/10.1007/s00464-019-06865-0

Hiatal hernia diagnosis prospectively assessed in obese patients

before bariatric surgery: accuracy of high‑resolution manometry

taking intraoperative diagnosis as reference standard

Antonella Santonicola1 · Luigi Angrisani2 · Antonio Vitiello2 · Salvatore Tolone3 · Nigel John Trudgill4 ·

Carolina Ciacci1 · Paola Iovino1

Received: 12 December 2018 / Accepted: 18 May 2019

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Abstract

Background Hiatal hernia (HH) is common in obese patients undergoing bariatric surgery. Preoperative traditional techniques such as upper gastrointestinal endoscopy (UGIE) or barium swallow/esophagram do not always correlate with intraopera-tive findings. High-resolution manometry (HRM) has shown a higher sensitivity and specificity than traditional techniques in non-obese patients in the HH diagnosis, whereas there is a lack of data in the morbidly obese population. We aimed to prospectively assess the diagnostic accuracy of HRM in HH detection, in comparison with barium swallow and UGIE, assuming intraoperative diagnosis as a standard of reference.

Methods Forty-one consecutive morbidly obese patients prospectively recruited from a tertiary-care referral hospital devoted to bariatric and metabolic surgery underwent a preoperative evaluation including standardized GERD questionnaires, barium swallow, UGIE, and HRM. The surgical procedures were performed by a single surgeon who was blinded to the results of other investigations.

Results HH was intraoperatively diagnosed in 11/41 patients (26.8%). In 10/11 patients, the preoperative HRM showed an esophagogastric junction suggestive of HH. When compared to intraoperative evaluation, the sensitivity of the HRM was 90.9% and the specificity 63.3%, with a positive predictive value of 47.6% and a negative predictive value of 95.0%. HRM showed a higher sensitivity and specificity compared to barium swallow and UGIE.

Conclusions HRM has a high accuracy of HH detection in morbidly obese patients assuming an intraoperative diagnosis as reference standard. It could therefore be a very useful tool in the preoperative work-up of obese patients undergoing bariatric surgery.

Keywords Hiatal hernia · High-resolution manometry · Obesity · Barium swallow · Esophagram · Upper gastrointestinal endoscopy · Bariatric surgery

Obese subjects have a three times higher risk of having a hiatal hernia (HH) than non-obese individuals [1–3].

In obese candidates for bariatric surgery, the preva-lence of HH varies across the studies ranging from 23 to 52% [4]. Among the different types of HH, the sliding one is closely associated with GERD [5]. Classically, the diagnosis of a HH relies on the interpretation of an upper gastrointestinal endoscopy (UGIE) or a barium swallow [6, 7]; however, these techniques have several limitations. One is that they are essentially “snapshot techniques.” The presence of a HH is consequently considered an all-or-none phenomenon, despite the fact that the diagnosis of a small HH can be inconsistent due to the subjectivity of the test [8]. High-resolution manometry (HRM) is a novel

Antonella Santonicola and Luigi Angrisani equally contributed to the present manuscript.

* Paola Iovino piovino@unisa.it

1 Department of Medicine, Surgery and Dentistry, “Scuola

Medica Salernitana”, University of Salerno, Via S. Leonardo 1, 84131 Salerno, Italy

2 General and Endoscopic Surgery Unit, S. Giovanni Bosco

Hospital, Naples, Italy

3 Surgery Unit, Department of Surgery, University

of Campania Luigi Vanvitelli, Caserta, Italy

4 Department of Gastroenterology, Sandwell General Hospital,

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technology that provides a more reliable assessment of esophageal motility than conventional manometry. HRM measures pressure events along the entire length of the esophagus simultaneously, from the cricopharyngeus to the Lower Esophageal Sphincter (LES), shortening the procedure time and requiring less catheter manipulation than traditional manometry [9]. HRM has demonstrated a high sensitivity and specificity (92% and 93%, respec-tively) for the detection of a HH in non-obese patients [8] allowing a dynamic evaluation of the esophagogastric junction (EGJ) with a more accurate analysis. The com-bination of an UGIE and a HRM could reach a sensitivity of 98% in the diagnosis of a HH, thereby eliminating the need for a barium swallow for the preoperative diagnosis of a HH [8] in lean individuals. In obese patients under-going bariatric procedures, a recent study demonstrated that the preoperative barium swallow might even be dis-advantageous, because in the case of false-positive results, it prolonged operative time [10]. However, other studies reveal that UGIE often over-diagnoses small HHs that in the majority of cases do not require any repair during bari-atric surgery [11]. To the best of our knowledge, there are only a few studies comparing HRM with traditional tech-niques such as barium swallow and UGIE in the diagnosis of HH in non-obese individuals [8, 12], whereas there is a lack of data in the morbidly obese population.

The aim of this study is to prospectively evaluate the diagnostic accuracy of HRM in HH detection, in compari-son with barium swallow and UGIE, taking an intraopera-tive diagnosis as reference standard [13, 14].

Materials and methods

Subjects

Morbidly obese patients from a high-volume outpatient center dedicated to bariatric and metabolic surgery were prospectively recruited. Adherence to the ethical conduct standards of the Declaration of Helsinki ensured patients’ welfare [15]. The study was approved by the Ethical Com-mittee of the ASL Napoli Centro. Informed consent was obtained from all patients. Exclusion criteria were preg-nancy, presence of a paraesophageal hiatal hernia, and previous esophageal or gastric surgery.

All patients underwent a preoperative evaluation that included a careful medical history, evaluation of comor-bidities, i.e., dyslipidemia, type 2 Diabetes (T2D), Body Mass Index (BMI), an assessment of GERD symptoms [16, 17] using a standardized questionnaire as well as a preoperative and an intraoperative assessment for HH.

Preoperative HH detection

Esophageal high-resolution manometry (HRM) HRM

studies were performed using a solid-state HRM cath-eter consisting of 36 pressure channels spaced at 1-cm intervals (Manoscan™ eso high-resolution manom-etry system, Medtronic, Minneapolis, USA). Patients were asked to discontinue any medication influencing esophageal motor function 5–7 days prior to testing. After an overnight fast, the subjects were intubated and positioned to record esophageal pressure from the hypopharynx to the stomach with approximately two to three sensors in the stomach. The manometric pro-tocol included at least 10 swallows of 5 mL of water and a 2-min period when the patient was asked not to swallow to assess basal sphincter pressure. Data analy-sis was performed by two investigators (AS, ST) who were blinded to pre- and intraoperative findings at the time of analysis. According to Pandolfino et al. [18], the pressure morphology of the EGJ was classified in three types, based on the presence of axial cranial sepa-ration between LES and crural diaphragm (CD): EGJ Type I, no separation between LES and CD; EGJ Type II, minimal separation (> 1 and ≤ 2 cm); EGJ Type III, > 2 cm of separation. EGJ Type III morphology is suggestive of the presence of a sliding HH [19]. HRM preoperative findings were not revealed to the surgeon who operated blindedly.

Upper GI endoscopy (UGIE) HH was diagnosed if

there was a separation between the squamocolumnar junction and the diaphragmatic pinch. Sliding HH is diagnosed when the separation between the squamo-columnar junction and the diaphragmatic impression is greater than 2 cm as measured using the hash marks on the endoscope (spaced 5 cm apart) [20]. The images on the monitor were digitally captured for the purpose of making photographs.

Barium swallow The diagnosis of a HH was made if

there was a herniated B-ring at the level of the squa-mocolumnar junction or when rugal folds traversing the diaphragm were observed [6].

UGIE and barium preoperative findings were not revealed to the surgeon who operated blindedly.

Intraoperative HH detection

The intraoperative diagnosis of HH was considered to be the reference standard [14]. All the surgical proce-dures were performed laparoscopically by a single sur-geon (L.A.) who was blinded to UGIE, HRM, and barium

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swallow results. The presence of a sliding HH was defined according to the following protocol [21]: EGJ and its rela-tionship to the hiatus were carefully inspected without an orogastric tube in the stomach to disclose the presence of sliding HH. If a clear diaphragmatic defect was observed and the EGJ was above the diaphragm, the diagnosis of a HH was obtained. When the diagnosis of a HH was not clear, a standard greater curvature dissection would be per-formed with dissection of the left crus, complete mobili-zation of the gastric fundus, and meticulous dissection of the fat pad to clearly identify the EGJ at the level of the Angle of His.

If the EGJ was in the chest above the level of the dia-phragm, HH was diagnosed. The surgical procedure has been accurately described elsewhere [22, 23].

Statistics

Data were summarized using mean ± standard deviation (M ± SD) unless otherwise indicated. Categorical and continuous data were compared between patients with or without intraoperative HH diagnosis using ANOVA and Chi square, respectively. The correlation between barium swallow, UGIE, and HRM for HH diagnosis was calculated by non-parametric (Spearman rho) correlation. For HRM,

barium swallow, and UGIE, the ability to diagnose a HH was assessed by means of a receiver operating characteristic (ROC) analysis with calculation of the area under the curve (AUC). The sensitivity, specificity, and predictive value of a positive test (PVPT), and predictive value of a negative test (PVNT) were determined (Table 1). The interobserver agreement for determining the presence of a HH on HRM studies was assessed using Cohen’s kappa as appropriate. The significance level was set at < 0.05. The statistical pro-gram used was the Statistical Package for Social Sciences (SPSS) for Windows, version 12.0.

Results

Subjects characteristics

Forty-one obese patients were studied. The presence of a sliding HH was intraoperatively diagnosed in 11/41 patients (26.8%).

Table 2 shows their demographic and clinical characteris-tics as well as the prevalence of the main obesity-associated comorbidities (i.e., hypertension, dyslipidemia, T2D).

Patients with and without HH intraoperatively diag-nosed were similar for sex, age, BMI, and comorbidities. Table 1 Definition and

description of sensitivity, specificity, predictive value of a positive test, predictive value of a negative test used in the article

HH hiatal hernia

Sensitivity Probability of a positive test result if a HH is present (true positive) Specificity Probability of a negative test result if a HH is absent (true negative) Predictive value of a positive test

(PVPT) Probability of having a HH if the test result is positive Predictive value of a negative test

(PVNT) Probability of not having a HH if the test result is negative

Table 2 Demographic characteristics and prevalence of obesity-associated comorbidities in patients with and without hiatal hernia

Data are expressed as percentage (%) or M ± SD, when appropriate HH hiatal hernia

Patients with HH

n = 11 Patients without HHn = 30 Total populationn = 41 p

Sex (M/F) 1/10 4/26 5/36 0.6 Age (years) 35.9 ± 11.3 35.4 ± 9.5 35.5 ± 9.8 0.9 Weight (kg) 114.2 ± 18.6 120.3 ± 16.3 118.9 ± 16.8 0.3 BMI (kg/m2) 44.9 ± 5.9 44.7 ± 5.4 44.8 ± 5.4 0.9 Hypertension n (%) 4 (36.4%) 3 (10%) 7 (17.1%) 0.07 Dyslipidemia n (%) 3 (27.3%) 4 (13.3%) 7 (17.1%) 0.2

Type 2 diabetes mellitus n (%) 0 0 0 –

Typical GERD symptoms n (%) 9 (81.8%) 11(36.7%) 20 (48.8%) 0.01

Esophagitis grade A, B (sec. Los Angeles), n (%) 3 (27.3%) 8 (26.7%) 11 (26.8%) 0.9

Esophagitis grade C, D (sec. Los Angeles), n (%) 0 0 0 –

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The prevalence of typical GERD symptoms was signifi-cantly higher in patients with intraoperative HH compared to patients without HH (p = 0.01); however, the prevalence of esophagitis, defined according to Los Angeles classifica-tion, was similar in the two groups.

Preoperative HH detection

HRM According to EGJ morphology [18], 20/41 (48.8%) patients were classified as type I, 4 (9.8%) as Type II, and 17 (41.5%) as type III. Interobserver agreement for the HH diagnosis by HRM was substantial (Cohen’s Kappa = 0.76).

In the group without intraoperative HH, HRM cor-rectly classified 19/30 (63.3%) patients (true-negative cases). Eleven patients were positive for HH by HRM, but the surgeon did not diagnose any HHs (i.e., false-positive cases).

In the group with intraoperative HH, 10 patients (90.9%) were correctly classified as having a HH on HRM (true-positive cases); however, there was one nega-tive case (9.1%) (false-neganega-tive case).

Table 3 summarizes the sensitivity and specificity, the PVPT, and the PVNT of HRM compared to intraopera-tive findings. The AUC for HRM in detecting an intraop-erative diagnosis of a HH was 0.77 (95% CI 0.61–0.92),

p = 0.009.

Upper GI endoscopy Among patients with HH by

UGIE, 5 (27.8%) had a type I, 2 (11.1%) a type II, and 11 (61.1%) a type III EGJ by HRM. There was a signifi-cant correlation between the three morphological types of EGJ assessed by HRM and the presence of HH by UGIE (R = 0.38, p = 0.01).

In the group without intraoperative HH, UGIE cor-rectly classified 20/30 (66.7%) patients (true-negative cases). Ten patients (33.3%) had a HH diagnosis by UGIE, but the surgeon did not diagnose HHs (i.e., false-positive cases).

In the group with intraoperative HH, 8 patients (72.7%) were correctly classified as positive for HH (true-positive

cases); however, in 3 patients (27.3%) the UGIE was nega-tive for HH (false-neganega-tive cases).

Table 3 summarizes the sensitivity and specificity, the PVPT, and the PVNT of UGIE compared to intraoperative findings. The AUC for UGIE in detecting an intraoperative diagnosis of a HH was 0.69 (95% CI 0.51–0.82), p = 0.056.

Barium swallow Among the patients with HH on barium

swallow, 3 (33.3%) had a type I, and 6 (66.7%) a type III EGJ by HRM. There was no correlation between the three morphological types of EGJ assessed by barium swallow and the presence of HH (R = 0.22, p = 0.16). In the group without intraoperative HH, the barium

swallow correctly classified 26/30 (86.7%) patients (true-negative cases). Four patients (13.3%) had a HH diagnosis, but the surgeon did not diagnose HHs (i.e., false-positive cases).

In the group with intraoperative HH, 5 patients (45.5%) were correctly classified as positive for HH (true-positive cases); however, in 6 patients (54.5%) the barium swal-low was negative for HH (false-negative cases).

Table 3 summarizes the sensitivity and specificity, the PVPT, and the PVNT for the barium swallow compared to intraoperative findings. The AUC for barium swallow in detecting an intraoperative diagnosis of a HH was 0.66 (0.46/0.86) with a 95% CI p = 0.12.

Diagnostic value of HRM

An additional analysis was performed comparing the HRM results with a common diagnostic strategy using only endos-copy or only barium swallow. In the group without intraop-erative HH, HRM did not disclosed a HH in 19/30 (63.3%) patients, while UGIE or barium swallow correctly classified 17/30 (56.7%) patients (true-negative cases).

In the group with intraoperative HH, 10/11 patients (90.9%) were correctly classified as having a HH on HRM, while 8 (72.7%) were correctly identified with UGIE or barium swallow (true-positive cases). In other words, an approach based on barium swallow or UGIE showed a lower sensitivity and specificity than HRM, assuming an intra-operative diagnosis as reference standard. Furthermore, the PVPT and the PVNT of the approach with UGIE or barium swallow were 38% and 85%, respectively, showing a prob-ability of having a HH if the test result is positive and a probability of not having a HH if the test result is negative, lower than HRM.

Discussion

HRM is a novel technology that has been demonstrated to accurately assess EGJ and esophageal body motor function, widely used also in pediatric age [24]. Moreover, there is Table 3 Sensitivity, specificity, predictive value of positive and

nega-tive tests for HRM, UGIE, and barium swallow using intraoperanega-tive assessment as reference standard for HH

HRM high-resolution manometry, UGIE upper gastrointestinal endos-copy, HH hiatal hernia, PVPT predictive value of positive test, PVNT predictive value of negative test

HRM UGIE Barium swallow

Sensitivity (%) 90.9 72.7 45.5

Specificity (%) 63.3 66.7 86.7

PVPT (%) 47.6 44.4 55.5

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consensus on the pivotal role of HRM prior to antireflux surgery [25].

This is the first study that has prospectively evaluated in a morbidly obese population the accuracy of HRM in HH diagnosis assuming an intraoperative diagnosis as a standard of reference. Our results showed that HRM is highly accu-rate for diagnosing HH with high sensitivity and specificity. Moreover, in this study the accuracy of HRM for HH detec-tion exceeded the accuracy of barium swallow or UGIE.

Other authors [8] have demonstrated high sensitivity (92%) and specificity (93%) of HRM in the diagnosis of HH in a cohort of lean individuals, considering the pres-ence of HH during an endoscopy or esophagogram as the gold standard. Another recent study confirmed the high sen-sitivity and specificity (94.3% and 91.5%, respectively) of HRM in a non-obese cohort of patients, using the in vivo evaluation as the reference standard [26]. In our obese popu-lation, we have described a similar sensitivity (90.9%) to that reported in the normal weighted population, but a lower specificity (60.6 vs. 91.5%).

Traditionally, the preoperative work-up of obese candi-dates for bariatric surgery includes a barium swallow and/ or UGIE. However, this approach is currently under debate. Some authors in fact consider barium swallow unnecessary and obsolete [10], while others questioned the accuracy of preoperative UGIE in an obese population undergoing bari-atric surgery [27], especially in asymptomatic patients [28,

29]. The current statement of several prominent international scientific societies (American Society for Metabolic and Bariatric Surgery, the Society of American Gastrointestinal and Endoscopic Surgeons, and the American Society for Gastrointestinal Endoscopy) emphasizes the importance of performing a routine preoperative UGIE [30].

Mohammed et al. [11] evaluated the efficiency of UGIE in a large population of obese bariatric patients and described a similar sensitivity (78%) but a better specificity (82%) com-pared to 66.7% observed in our study.

The diagnostic value of HRM was further enhanced when comparing the HRM with a common diagnostic strategy using only UGIE or only barium swallow demonstrating a better sensitivity and specificity of HRM with a very high negative predictive value.

Because of this very high negative predictive value in the detection of HH, it is unlikely that intraoperative observation will reveal a HH when HRM does not show a HH. Of note in this study we found that the combination of the highly rec-ommended UGIE together with HRM reached a sensitivity of 100%. This demonstrates that the combination of upper GI endoscopy and HRM in obese patient candidates for bari-atric surgery allows the detection of all HHs at preoperative work-up. This indeed might influence the choice of bariatric procedure and the operating room planning. What is the bet-ter management of the HH during bariatric surgery is out

of the aim of the present study. However, there is an ongo-ing debate among bariatric surgeons on this topic, and dur-ing the last few years many studies have been published on more and more patients with continued or acquired GERD symptoms after bariatric procedures, especially the restric-tive ones [31]. Then, further studies should be performed to help address these questions.

This study has some points of strengths and some weak-nesses. Firstly, it is a prospective evaluation of HH in a cohort of consecutively enrolled morbidly obese patients. Secondly, the two physicians who performed the HRM were blinded to the endoscopic, radiologic, and intraoperative findings at the time of analysis. Thirdly, a single surgeon blinded to the presence or absence of a HH diagnosed by barium swallow, UGIE, and/or HRM explored the hiatus intraoperatively to search for a HH using the same technique. However, there are some limitations such as the small sam-ple size and that the intraoperative diagnosis of a HH can be more difficult in morbidly obese than normal weight sub-jects. The hernia defect, in fact, could be masked by a large fat pad, the adipose tissue at the level of the cardias also called Belsey Fat, and/or by large pre-hernia lipoma. This might explain the false-positive results obtained with either HRM or UGIE in our population. Additionally, the laparo-scopic intraoperative diagnosis of HH could differ among surgeons as well as the preoperative endoscopic diagnosis of HH could differ among endoscopists. However, previous studies demonstrated a consistent interobserver agreement by using UGIE for the HH diagnosis [8, 32].

Conclusions

HRM is a very safe and beneficial tool that is able to diag-nose HH in obese patient candidates for bariatric surgery. It might be used routinely in combination with the highly recommended UGIE, avoiding the need for barium swallow with its exposure to radiation. The lack of a preoperative HH diagnosis may influence the choice of procedure or change the operative strategy, prolonging the planned operative time.

Further studies, possibly involving more centers devoted to bariatric and metabolic surgery, are welcomed to confirm the accuracy of HRM in a larger sample size and its useful-ness in routine clinical practice.

Compliance with ethical standards

Disclosures Antonella Santonicola, Luigi Angrisani, Antonio Vitiello, Salvatore Tolone, Nigel John Trudgill, Carolina Ciacci, and Paola Iovino have no conflicts of interest or financial ties to disclose.

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