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9. Banks M. The modern investigation and management of gastrooesophageal reux disease (GORD). Clin Med. 2009;9(6):600–4. Epub
2010/01/26.
10. Shaheen NJ, Weinberg DS, Denberg TD, Chou R, Qaseem A, et al.;
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Physicians. Ann Intern Med. 2012;157:808–16.
11. Martinez SD, Malagon IB, Garewal HS, Cui H, Fass R. Non-erosive
reux disease (NERD)--acid reux and symptom patterns. Aliment
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12. Lundell LR, Dent J, Bennett JR, etal. Endoscopic assessment of oesophagitis: clinical and functional correlates and further validation of the Los
Angeles Classication. Gut. 1999;45:172–80.
13. Hartono JL, Qua CS, Goh KL. Non-erosive reux disease (NERD),
symptomatic and asymptomatic erosive reux disease (ERD): from
hypersensitive to hyposensitive esophagus. Dig Dis Sci. 2011;56(1):90–
6. Epub 2010/05/15.
14. Dean BB, Gano AD Jr, Knight K, et al. Effectiveness of proton pump
inhibitors in nonerosive reux disease. Clin Gastroenterol Hepatol.
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15. Vaezi MF.Laryngeal manifestations of gastroesophageal reux disease.
Curr Gastroenterol Rep. 2008;10(3):271–7. Epub 2008/07/16.
16. Mathus-Vliegen EMH, Smit CF, Devriese PP.Artifacts in 24-h pharyngeal and oesophageal pH monitoring: is simplication of pH data analysis feasible? Scand J Gastroenterol. 2004;39(1):14–9.
17. Adhami T, Goldblum JR, Richter JE, Vaezi MF.The role of gastric and
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18. Ahmed T, Vaezi MF.The role of pH monitoring in extraesophageal gastroesophageal reux disease. Gastrointest Endosc Clin N Am.
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19. Lim PL, Gibbons MJ, Crawford EJ, Watson RGP, Johnston BT. The
effect of lifestyle changes on results of 24-h ambulatory oesophageal pH
monitoring. Eur J Gastroenterol Hepatol. 2000;12(6):655–6.
20. Jamieson JR, Stein HJ, DeMeester TR, etal. Ambulatory 24-h esophageal
pH monitoring: normal values, optimal thresholds, specicity, sensitivity,
and reproducibility. Am J Gastroenterol. 1992;87:1102–11.
21. Schwameis K, Lin B, Roman J, Olengue K, Siegal S, DeMeester SR.Is
pH testing necessary before Antireux surgery in patients with endoscopic erosive esophagitis? J Gastrointest Surg. 2018;22(1):8–12.
22. Hong S-KS, Vaezi MF.Gastroesophageal reux monitoring: pH (catheter
and capsule) and impedance. Gastrointest Endosc Clin N Am.
2009;19(1):1–22.
F. Fontan et al.
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23. Kavanagh R, Smith J, Bashir U, etal. Optimizing bariatric surgery outcomes: a novel preoperative protocol in a bariatric population with gastroesophageal reux disease. Surg Endosc. 2020;34:1812–8.
24. Charbel S, Khandwala F, Vaezi MF.The role of esophageal pH monitoring in symptomatic patients on PPI therapy. Am J Gastroenterol.
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25. Gyawali CP, Kahrilas PJ, Savarino E, etal. Modern diagnosis of GERD:
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gutjnl- 2017- 314722.
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14
JennwoodChen andKyleA.Perry
While gastroesophageal reux disease (GERD) is a common disorder, making the diagnosis can be challenging because symptoms are often vague. Symptom presentations can be variable
between patients, and manifestations of GERD overlap with other
foregut pathologies including functional dyspepsia, esophagitis,
and gastroparesis [1–4]. Consequently, identifying GERD based
on symptoms alone leads to the wrong diagnosis in 30–50% of
patients [5–7]. Similarly, esophageal acid exposure alone is insufcient to predict the presence of GERD symptoms or their severity; however, it can help predict response to anti-reux surgery [8,
9]. Therefore, it is imperative to document objective pathologic
reux in GERD patients, especially for those being considered for
anti-reux surgery (ARS) [6, 10].
J. Chen
Division of Gastroesophageal and Bariatric Surgery, University of Utah,
Salt Lake City, UT, USA
e-mail: Jennwood.Chen@hsc.utah.edu
K. A. Perry (*)
Division of General and Gastrointestinal Surgery, Ohio State University,
Columbus, OH, USA
e-mail: Kyle.Perry@osumc.edu
© Society of American Gastrointestinal and Endoscopic Surgeons
(SAGES) 2023
A. D. Patel et al. (eds.), The SAGES Manual of Physiologic
Evaluation of Foregut Diseases,
https://doi.org/10.1007/978-3-031-39199-6_14
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In the absence of clear endoscopic evidence, the current gold
standard test to diagnose GERD is the 24-h ambulatory esophageal
pH metry or alternatively, the wireless esophageal pH monitoring
probe (Bravo™, Medtronic, Shoreview, MN) which most consider an equivalent option [11]. In fact, the recent GERD consensus panel in Lyon recommends that the optimal diagnostic for
initial proton pump inhibitor (PPI) non-responders without prior
endoscopic demonstration of GERD is pH monitoring done while
withholding anti-secretory therapy [12]. In this chapter, we will
discuss the evolution, interpretation, and utility of wireless pH
monitoring.
J. Chen and K. A. Perry
A Brief History of pH Monitoring
The diagnosis of gastroesophageal reux has been evolving for
over a century since 1884, when Reichmann lowered a sponge in
the esophagus of patient with heartburn and showed that it contained acid [13]. In 1958, using a modied manometry probe,
Tuttle and Grossman measured the in situ pH of the esophagus
2cm above the “respiratory inection point” [14]. Based on their
work, pH would eventually become the standard metric to quantify gastroesophageal reux.
Designed to measure the hydrogen-ion concentration throughout the gastrointestinal tract, the rst wireless pH capsule was created by Jacobson and Mackay in 1957 [15]. Although not
specically geared toward detecting esophageal reux, its creation provided the fundamentals for what would later become the
ambulatory wireless pH monitoring device [16]. In 1974,
DeMeester and Johnson studied gastroesophageal reux in normal individuals and patients with GERD symptoms. Their landmark study established the modern parameters of pH monitoring
to diagnose GERD. In particular, they established the location at
which the pH sensor is to be placed (5cm above the lower esophageal sphincter), dened the threshold pH (≤4) for acid reux,
and created a composite score (Johnson- DeMeester Score) to categorize patients as having pathologic acid reux [17–19].
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197
Catheter-Based pH Monitoring
Until the early 2000s, the primary options for ambulatory esophageal pH monitoring were catheter-based systems. First introduced
in the 1970s, these require passage of a nasopharyngeal catheter
placed 5cm above the endoscopically or manometrically identied lower esophageal sphincter (LES) [20]. The catheter runs
over and behind the ear and is taped securely to the nose. The
catheter connects to a portable digital data recorder that the patient
wears around the waist or over the shoulder. The patient is
instructed to refrain from changing their daily routine, abstain
from bathing, and remain upright until bedtime. Using the digital
data recorder, a virtual diary of events is kept which includes
symptom events (e.g., heartburn, regurgitation, cough, and sore
throat), beginning and end of mealtimes, each time the patient
lays down and gets up, and duration of events.
Interpreting the output of the digital recorder involves analyzing
both graphical and numerical data. The graphical output comprises
a pH tracing that shows acid reux episodes (drops in pH to a level
below pH of 4) over time. The recording system is calibrated to a
sampling rate (usually 4s) at which the pH data are recorded [21].
The numerical data include the percent time of reux over the monitoring period, percent time of reux in the upright and supine positions, total number of reux episodes, number of episodes that last
longer than 5min, duration of the longest episode, and a composite
score [22]. The composite score, commonly referred to as the
DeMeester score, is based on the standard deviation of the mean of
each of the six components measured in normal subjects [23].
Finally, the data also include three measures of symptom correlation: symptom index (SI) dened as the percentage of reux-related
symptom episodes, symptom-sensitivity index (SSI), dened as the
percentage of symptom-associated reux episodes, and symptom
association probability (SAP) which is a measure of correlation
between symptoms and reux episodes [21]. Of the three symptom
correlation schemes, the SAP and the SI, interpreted in conjunction,
are the most statistically valid for symptom-reux association [24].
The normative thresholds for diagnosing pathologic reux, as
agreed upon by professional consensus groups, are as follows: (1)
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24-h total % time pH < 4 greater than 4–5.5% (2) DeMeester
score≥14.7 (3) SAP>95% for primary symptom, SI>50% for
primary symptom [25].
The total duration of the catheter-based ambulatory pH study is
typically 24h. This allows for measurements to be characterized
over a complete circadian cycle and captures the effect of physical
activity and body position on esophageal acid exposure [26].
It should be apparent from the above description that the ability of ambulatory pH monitors to accurately detect abnormal
reux is largely dependent on patient’s tolerance of the test,
adherence to a “normal routine,” and adequate duration of monitoring. It is these areas which catheter-based systems tend to be
most problematic.
Patient discomfort and social embarrassment from the passage
and xation of the nasoesophageal pH catheter are ubiquitous [27,
28]. In fact, up to 10% of patients fail to complete the 24-h moni-
toring period due to intolerance [29, 30]. For those that are able to
endure the duration of the test, studies have shown that patients do
signicantly alter their daily routine [31, 32]. In particular,
patients are more sedentary and spend less time eating, drinking,
and being physically active [33]. Unfortunately, these compensatory behaviors may alter the reliability of the test [27, 32]. Finally,
it has been suggested that limiting the test to 24h decreases the
diagnostic yield due to the high day-to-day variability in acid
exposure and symptom reporting [29, 34, 35]. Studies comparing
repeated 24-h monitoring estimated the reproducibility to be
77–83% which may explain why a signicant portion of patients
with erosive reux have a normal ambulatory 24-h pH study [28,
36, 37]. Furthermore, studies reporting on the detection perfor-
mance of catheter-based systems vary widely with reported sensitivities ranging between 73 and 96% [28, 38, 39].
J. Chen and K. A. Perry
Wireless pH Monitoring
In response to these limitations, the Bravo™ wireless pH monitoring device was developed in 2001 and approved by the US
Food and Drug Administration in 2005 for the evaluation of
patients with GERD [40].
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199
The Bravo™ wireless pH monitoring system utilizes a radiotelemetry pH sensing capsule that is attached to the mucosa of the
distal esophagus. The capsule measures 6mm×5.5mm×25mm
and contains an antimony pH electrode, a reference electrode, a
battery, and a radio-transmitter [40]. The capsule is mounted onto
the end of a delivery catheter for oral or nasal insertion, with the
former being the preferred method [41].
Prior to insertion, an upper endoscopy is generally performed
and the squamocolumnar junction (SCJ) is identied and measured from the incisors. Ideally, the capsule is deployed 6 cm
proximal to the SCJ [42]. This is due to the fact that the SCJ is
approximately 1cm distal to the proximal border of the LES [43].
Therefore, endoscopic placement of the Bravo™ capsule 6cm
proximal to the SCJ corresponds to manometric placement of the
traditional pH catheter 5cm proximal to the LES.Transoral placement of the capsule based on manometric landmarks is an alternative option. However, the positioning requires a correction factor
to account for the longer pathway of the transnasal manometry
catheter [44].
Once the device is activated and calibrated, the delivery catheter is
inserted with or without direct endoscopic guidance. With the catheter in its desired location, a vacuum pump is used to apply suction to
the wall of the capsule. A pressure between 510 and 700mmHg is
applied for approximately 10–30 s, after which time an activation
button is pressed to deploy a spring-loaded pin that attaches the
Bravo™ capsule to the mucosa [40, 45, 46]. If placed without direct
endoscopic guidance, a repeat endoscopy may be performed to conrm placement. The capsule measures pH and transmits data to a
pager-sized receiver that can be worn on the patient’s belt [47]. As
long patients stay within signal detection range of the receiver
(approximately 1m or 3ft.), patients are encouraged to follow their
daily routine, including bathing. Patients keep a virtual diary of their
reux-related symptoms and events.
The parameters measured during wireless pH monitoring are
similar to catheter-based systems [19, 48]. However, in contrast to
the 4s sampling rate of catheter-based systems, the Bravo™ capsule samples esophageal pH every 6s [27]. Another important
difference is that the duration of wireless pH monitoring can be
extended to 96h.
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J. Chen and K. A. Perry
Wireless Versus Catheter-Based pH Monitoring
The clear advantage of wireless pH monitoring over traditional
catheter-based systems is patient comfort and ability to adhere to
routine activities. In a randomized cross-over trial, Wenner etal.
showed that 87% of patients undergoing esophageal pH monitoring preferred the wireless pH capsule over the catheter-based
technique, citing less interference with normal activities and
social embarrassment [32]. In a study of 133 patients who underwent pH monitoring (78 catheter-based; 55 wireless), Grigolon
etal. found that the wireless technique was far better tolerated
than the catheter-based, with minor impact on daily activities
including food intake [31]. Sweis et al. showed that 96% of
patients, who were previously unable to tolerate 24-h catheterbased monitoring, successfully completed 48h of wireless testing
and due to less restriction in activities of daily living, nasopharyngeal discomfort, dysphagia, and chest pain [30]. Finally, in a
meta-analysis of randomized control trials that included 167
patients, authors concluded that the Bravo™ wireless pH monitor
interfered less with daily activities compared to the cathetersystem system [49].
Second, proponents of wireless pH monitoring often discuss
the potential increased sensitivity for detecting reux events due
to the prolonged monitoring capability. While catheter-based
monitoring is carried out over a 24-h cycle, which typically provides 20–22h of interpretable data, the Bravo™ capsule captures
pH levels for up to 96h [25]. In a study of 186 patients undergoing
wireless pH monitoring, extended monitoring for 48h identied
22% more patients with abnormal esophageal acid exposure [50].
Sweis etal. found that 96-h monitoring using the Bravo™ capsule
diagnosed GERD in 76% of patients with typical reux symptoms
but with previously negative 24-h catheter-based pH studies [51].
Authors comparing 48 to 96-h wireless pH monitoring reported a
23.5% increase in GERD diagnosis when the test was extended by
2 days [52]. Similarly, in a study of 99 patients undergoing 96-h
wireless pH testing, Capovilla etal. found an increase in diagnostic yield of 12% when the wireless testing interval was extended
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to 96 h. However, at long-term follow-up, only 25% of these
patients, who would have otherwise had negative tests at 48h,
reported good outcomes post-fundoplication. The authors concluded that while prolonged testing does increase diagnostic
yield, it comes at the expense of potentially recruiting complex
patients who may not respond to surgical therapy [53]. Currently,
the most widely adopted duration for wireless testing is 48h.
Head-to-head studies comparing performance of wireless versus catheter-based pH monitoring are intriguing. Pandolno etal.
subjected 25 asymptomatic patients to simultaneous 24-h catheterbased and 48-h wireless pH monitoring [54]. Digitized uoroscopic images were employed to ensure proper and equivalent
positioning of the pH electrodes. A pH reference was established
using swallows of orange juice (pH= 3.88). The result of the
study showed that the catheter-based system over-reported the
number of acid exposure events by nearly three times (117.0 vs.
41.8). Forty percent of this discrepancy was attributable to awed
software calibration while the majority of the remainder were
brief events with poor reproducibility between systems. In an
almost identical study, Pandolno etal. again noted a signicant
discrepancy between the two systems [55]. In terms of percent
time, the pH was less than 4; Pandolno found that the catheterbased system reported acid exposure values twice those reported
by the Bravo™ capsule. The tendency of catheter-based systems
to over-report esophageal acid exposure has been a consistent
nding in additional studies [48, 56]. Further examination reveals
that the majority of the reux episodes missed by the Bravo™
capsule are short-duration events that are attributable to the longer
sampling rate of the wireless system (6 vs. 4s), the signicance of
which, is questionable [20]. Moreover, unlike the Bravo™ capsule which moves with the esophageal mucosa, catheter-based
probes can “dip down” toward the stomach with each swallow
[26]. Therefore, what is perceived to be an increase in reux
events is simply artifact [57].
Wireless pH monitoring does have limitations. Despite the
overall comfort of the Bravo™ capsule, chest pain can be signicant and is reported much more often when compared to catheterbased systems [49, 58]. Unintended and early detachment of the
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J. Chen and K. A. Perry
capsule can be as high as 10% [59]. Furthermore, when positioned
endoscopically, misplacement is common. In a retrospective study
of 161 patients, investigators reported that nearly 30% of Bravo™
capsules placed were mal-positioned. The majority of which were
>3 cm proximal to the ideal location [42]. Interestingly, upon
reanalysis, the authors concluded that even misplacement of 5cm
did not affect the frequency of positive pH studies. Finally, compared to catheter-based systems, the Bravo™ wireless capsule is
considerably more expensive [40, 45].
Conclusion
Ambulatory pH monitoring is an invaluable tool in the diagnosis
of GERD. The primary end points of pH monitoring are esophageal acid exposure time, number of reux events, and, to a lesser
extent, the association between symptoms and episodes. Wireless
pH monitoring is particularly useful for those patients who are
unable to tolerate catheter-based testing. Extending the duration
of monitoring time to 48 or 96h may increase diagnostic yield
and reproducibility. However, wireless pH monitoring is considerably more expensive and thus may be cost-prohibitive in some
instances.
References
1. Johnson LF, DeMeester TR.Development of the 24-hour intraesophageal
pH monitoring composite scoring system. J Clin Gastroenterol.
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2. Penagini R, Sweis R, Mauro A, etal. Inconsistency in the diagnosis of
functional heartburn: usefulness of prolonged wireless pH monitoring in
patients with proton pump inhibitor refractory gastroesophageal reux
disease. J Neurogastroenterol Motil. 2015;21:265–72.
3. Clayton S, Emerson JF.Eosinophilic esophagitis: a mimic of gastroesophageal reux disease. Am Fam Physician. 2018;97:628–9.
4. Savarino E, de Bortoli N, De Cassan C, et al. The natural history of
gastro- esophageal reux disease: a comprehensive review. Dis Esophagus.
2016;22:331–9.
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