Symptoms of gastroesophageal reflux disease improve after parathyroidectomy
Primary hyperparathyroidism can be associated with symptoms related to GERD, but it is unclear which symptoms of GERD improve after parathyroidectomy. Our goal was to assess prospectively for changes in specific GERD symptoms after parathyroidectomy using a validated questionnaire. Using the GERD health-related quality of life (GERD-HRQL) questionnaire, symptoms of heartburn were prospectively assessed before and 6 months after treatment of hyperparathyroidism with parathyroidectomy. This validated questionnaire includes 10 items, with a Likert scale of 0-5. Scores range from 0 to 45, a lesser score indicates fewer/less severe symptoms. Pre- and postoperative surveys were available for 51 patients. Parathyroidectomy improved the overall questionnaire score (12.5 ± 1.3 vs 4.5 ± 0.9, P < .0001). Overall scores for each question improved after parathyroidectomy, including symptoms of dysphagia (P = .001) and overall satisfaction with symptoms (P < .0001). However, the number of patients taking antireflux medication before and after parathyroidectomy was not substantially different (34 vs 28 patients, P = .17). All symptoms of GERD improved after parathyroidectomy for hyperparathyroidism. Despite the decrease in symptoms, there was not a change in the number of patients who remained on anti-reflux therapy. For patients with symptoms of GERD, a trial off antireflux medications after parathyroidectomy should be considered.
Symptoms of gastroesophageal
reﬂux disease improve after
Alexandra E. Reiher, MD,
Haggi Mazeh, MD,
Sarah Schaefer, NP,
Jon Gould, MD,
Herbert Chen, MD,
and Rebecca S. Sippel, MD,
Madison and Milwaukee, WI, and Evanston, IL
Background. Primary hyperparathyroidism can be associated with symptoms related to GERD, but it is
unclear which symptoms of GERD improve a fter parathyroidectomy. Our goal was to assess prospectively
for changes in speciﬁc GERD symptoms after parathyroidectomy using a validated questionnaire.
Methods. Using the GERD health-related quality of life (GERD-HRQL) questionnaire, symptoms of
heartburn were prospectively assessed before and 6 months after treatment of hyperparathyroidism with
parathyroidectomy. This validated questionnaire inclu des 10 items, with a Likert scale of 0–5. Scores
range from 0 to 45, a lesser score indicates fewer/less severe symptoms.
Results. Pre- and postoperative surveys were available for 51 patients. Parathyroidectomy improved the
overall questionnaire score (12.5 ± 1.3 vs 4.5 ± 0.9, P < .0001). Overall scores for each question
improved after parathyroidectomy, including symptoms of dysphagia (P = .001) and overall satisfactio n
with symptoms (P < .0001). However, the number of patients taking antireﬂux medication before and
after parathyroidectomy was not substantially different (34 vs 28 patients, P = .17).
Conclusion. All symptoms of GERD improved after parathyroidectomy for hyperparathyroidism. Despite
the decrease in symptoms, there was not a change in the number of patients who remained on anti-reﬂux
therapy. For patients with symptoms of GERD, a trial off antireﬂux medications after parathyroidectomy
should be considered. (Surgery 2012;152:123 2-7.)
From the Section of Endocrine Surgery, Department of Surgery,
University of Wisconsin, Madison, WI;
Division of Endocrinology, Department of Internal Medicine,
Northshore University Healthcare System,
Evanston, IL; and Department of General Surgery,
Medical College of Wisconsin, Milwaukee, WI
CLASSIC SYMPTOMS ASSOCIATED WITH PRIMARY HYPERPARA-
(PHPT) include nephrolithiasis and
bone disease. However, several symptoms can be
related to PHPT, including polydipsia, polyuria,
depression, and decreased appetite. Gastric and
duodenal ulceration, as well as heartburn or gas-
troesophageal reﬂux disease (GERD), also have
been described. The incidence of heartburn in
patients with PHPT is as great as 30%. Other
gastrointestinal (GI) manifestations include consti-
pation (33%), nausea (24%), and decreased appe-
tite (15%). The underlying mechanism remains
Patients with symptomatic PHPT should un-
dergo parathyroid surgery to achieve cure, and
certain asymptomatic patients should undergo
surgical resection of their adenoma. Currently,
symptoms of GERD are not considered an indica-
tion for parathyroidectomy (PTX). Criteria devel-
oped by the NIH Managem ent of Asymptomatic
Primary Hyperparathyroidism for operative inter-
vention include serum calcium concentration of
1.0 mg/dL or more above the upper limit of
normal; creatinine clearance <60 mL/min; bone
density at the hip, lumbar spine, or distal radius
that is more than 2.5 standard deviations less than
peak bone mass (T score <2.5) and/or previous
fragility fracture; or age less than 50 years.
cures PHPT, improves bone mineral density, may
decrease the risk of fracture, decreases the risk
of kidney stones, and improves some quality of
life (QOL) measurements
; however, its effect on
gastrointestinal symptoms have been poorly
GERD is deﬁned by the American College of
Gastroenterology as symptoms or mucosal damage
produced by the abnormal reﬂux of gastric
Presented as an oral presentation at the American Association
of Endocrine Surgeons, Iowa City, IA, May 1, 2012.
Accepted for publication August 23, 2012.
Reprint requests: Rebecca S. Sippel, MD, Department of Sur-
gery, University of Wisconsin, 600 Highland Avenue, Clinical
Science Center J4/703, Madison, WI 53792-3284. E-mail:
0039-6060/$ - see front matter
Ó 2012 Mosby, Inc. All rights reserved.
contents into the esophagus.
The most common
symptoms associated with GERD are heartburn,
dysphagia, and regurgitation. Diagnostic testing
for GERD includes upper endoscopy, ambulatory
esophageal pH monitoring, barium swallow stud-
ies, and assessing response to treatment with anti-
secretory therapy such as proton pump inhibitors
or H2 antagonists.
Treatment of GERD includes antireﬂux medi-
cations or operative intervention for refractory
cases. Standard medical treatment with antireﬂux
medications is safe overall but there are side-effects
and risks associated with taking these medications.
The side-effect proﬁle for proton-pump inhibitors
(PPIs) includes headaches (1–2 %), diarrhea (1.9–
4.1%), nausea (0.02–0.9%), and rash (0.4–1.1%).
Chronic use of PPIs has been associated with
decreased calcium absorption due to decreased
gastric acid, as well as community-acquired pneu-
There have also been conﬂicting studies
regarding a possible increased risk of fractures in
patients using proton pump inhibitors for longer
than 6 months.
Removing such medications
from a patient’s medication list would, therefore,
be of beneﬁt to the patient.
Health-related QOL questionnaires are consid-
ered a standardized instrument to evaluate the
effects of treatment of GERD in clinical trials.
The GERD-HRQL questionnaire was designed to
measure symptomatic outcomes of GERD with
the use of a simple instrument---a questionnaire.
The questionnaire was designed and validated by
Velanovich et al
in 1996 and includes 10 items,
with a Likert scale of 0–5. The GERD-HRQL total
score is the sum of the individual item scores,
with the worse possible score reaching 45 points.
After medical or operative treatment, with an inter-
val of 1 to 6 months, patients were again asked to
complete the G ERD-HRQL questionnaire. The
questionnaire was able to identify the most com-
mon and bothersome symptoms of GERD, as well
as differentiate between satisﬁed and unsatisﬁed
GERD patients. Velanovich et al
evaluated 72 pa-
tients who were asked to complete the GERD-
HRQL at initial assessment.
Although the authors of previous studies have
described symptoms of heartburn improving after
no published studies have investigated spe-
ciﬁc symptoms of GERD before and after PTX.
Our goal was to prospectively assess the changes
in speciﬁc GERD symptoms before and after PTX
by using a validated questionnaire, the GERD
health-related quality of life (GERD-HRQL)
This prospective study wa s performed at a single
academic institution from March 2010 through
June 2011 and approved by its institutional review
board. Patients undergoing PTX were asked to
complete a survey as part of their preoperative
evaluation. PTX was performed by 1 of 2 endo-
crine surgeons at our institution. All patients were
asked whether they had symptoms of heartburn. If
patients answered yes to having heartburn, they
were asked to complete an additional survey, the
GERD-HRQL questionnaire. The questionnaire
was then provided to patients to complete at their
follow-up appointment 6 months after PTX.
The GERD-HRQL validated questionnaire in-
cludes 10 items, with a Likert scale of 0–5. Six items
measure satisfaction with the degree of heartburn
symptoms, 2 with dysphagia/odynophagia, and
1 with the impact of medication on daily life.
One item measures overall satisfaction with the
present condition. Sco res range from 0 to 45, with
a lower score indicating fewer/less severe symp-
toms (Supplementary File 1).
Paired t tests were used to compare individual
data pre and op post-op eratively, and unpaired t
tests and the Fisher exact were used to compare
the responders and nonresponders. Statistical anal-
ysis was performed with Microsoft Excel (2003 for
Microsoft Windows; Microsoft, Redmond, WA). Re-
sults are expressed as the mean ± SEM.
Pre- and postoperative surveys were available for
51 patients. Mean age at time of PTX was 59 ± 2
years, and 78% of patients were female. Mean body
mass index (BMI) was 30.7 ± 6.3 kg/m
). Mean preoperative calcium
was 10.6 ± 0.1 mg/dL, and mean preoperative
PTH was 142 ± 24 pg/mL. Forty-eight patients
had PHPT, 2 patients had secondary hyperparathy-
roidism, and 1 patient had tertiary hyperparathy-
roidism. Thirty-two patients had 1 parathyroid
adenoma (63%), 11 patients had 2 parathyroid ad-
enomas (22%), and 8 patients underwent subtotal
PTX (16%). Follow-up surveys were completed 6
months postoperatively and were available on
100% of patients. Average 6-month postoperative
calcium was 9.4 ± 0.1 mg/dL and average postoper-
ative PTH was 50.7 ± 6.7 pg/mL. All patients were
eucalcemic at 6 months’ follow-up.
Overall score s for each question improved after
PTX, including severity of symptoms (P < .0001),
the presence of heartburn lying down (P = .001)
or standing up (P = .004), symptoms after meals
Volume 152, Number 6
Reiher et al 1233
(P = .002), impact of symptoms on diet (P = .03),
difﬁculty swallowing (P = .002), pain with swallow-
ing (P = .03), and overall satisfaction with symp-
toms (P < .0001). Also, the impact of symptoms
on daily life improved (P = .02). Interestingly, the
overall number of patients on antireﬂux medica-
tion before and after PTX was not signiﬁcantly dif-
ferent (34 vs 28 patients, P = .11; Table I) Patients
with a preoperative score <20 were older than pa-
tients with a pre-operative score $20 (60 ± 2 vs 54 ±
2 years, respectively; P = .02.
Surgery signiﬁcantly improved the overall ques-
tionnaire score (12.5 ± 1.3 vs 4.5 ± 0.9; P < .0001).
BMI did not explain the changes observed. There
was not a signiﬁcant difference in percent change
in score between patients with an average BMI <25
(41 ± 30%) and patients with an average BMI
$25 (63 ± 8%), P = .49. Greater than 50%
improvement in scores was recorded in 67% of pa-
tients after PTX. Only 7 patients (14%) reported
no change in symptoms or worsening of symptoms.
There was no difference in preoperative
PTH levels (P = 1.0) or calcium levels (P = .57)
between patients wh o had >50% improvement (re-
sponders) versus those with <50% improvement
(nonresponders) in symptoms of GERD after sur-
gery (Table II). Interestingly, the nonresponders
had lesser base line scores before surgery than the
responders, but this difference was not signiﬁcant.
In addition, there were fewer responders on antire-
ﬂux medications 6 months after surgery than non-
responders (P = .005).
Patients with a preoperative score of >15 (n =
15) had a 68 ± 9% improvement in their score
post-operatively, while patients with a preoperative
score <15 (n = 36) had a 54 ± 12% improvement in
their score postoperatively. The differences in
score improvement were not substantially different
(P = .35).
This is the ﬁrst study to investigate speciﬁc GERD
symptoms in patients with PHPT before and 6
months after parathyroidectomy. Patients with
symptoms of GERD before parathyroidectomy had
an average score on the GERD-HRQL questionnaire
of 12.5 ± 1.3, which signiﬁcantly improved to 4.5 ±
0.9 after PTX (P < .0001). Overall, each symptom
score improved after PTX. Although symptoms of
GERD have been linked to hyperparathyroidism
and hypercalcemia, the pathophysiology of GERD
symptoms and peptic ulcer disease in these patients
In a study published in 1982,
Mowschenson et al
demonstrated changes in
lower esophageal sphincter pressures before and
after PTX. Patients with heartburn had a lower
esophageal sphincter pressure below normal before
operation, and 4 of the 5 patients had an increase in
lower esophageal pre ssure.
Studies have demon-
strated increased gastric acid secretion and gastrin
levels in the presence of hypercalcemia, but other
studies have found conﬂicting results.
GERD can impact substantially a patient’s QOL
and work productivity. In a study that used surveys,
authors demonstrated that greater 30% of patients
experiencing heartburn reported decreased work
The impact of GERD symptoms on
a patient’s QOL is most important when evaluating
for treatment response.
Despite signiﬁcant improvement in symptoms
of GERD, there was not a substantial change in the
number of patients receiving antireﬂux medica-
tion before and after PTX in our study (P = .11).
Only 6 patients (12%) had been taken off antire-
ﬂux medication after PT X. A study from the Uni-
versity of Pittsburgh demonstrated that 11% of
patients had medications discontinued or de-
creased after PTX. However, only 3 patients were
noted to have proton pump inhibitors discontin-
ued after surgery.
A Swedish study demonstrated
that 27% of 97 long-term PPI users were able to
discontinue PPIs after PTX without recurrence of
Given the ﬁnancial and psychologic
burden for patients to take medications on a daily
basis, patients and their primary care providers
need to be educated that discontinuation of antire-
ﬂux medications after PTX should be considered,
especially in patients with a signiﬁcant improve-
ment or resolution of their GERD symptoms.
Classic symptoms of PHPT---nephrolithiasis,
bone disease, and neuropsychiatric symptoms---are
Table I. Questionnaire scores before and 6
months after PTX
Preoperative Postoperative P value
Overall score 12.5 ± 1.3 4.5 ± 0.9 <.0001
Severity 2.01 ± 0.20 0.84 ± 0.14 <.0001
Present lying down 1.53 ± 0.21 0.76 ± 0.15 .001
Present standing up 1.04 ± 0.18 0.49 ± 0.13 .004
After meals? 1.16 ± 0.18 0.55 ± 0.13 .002
Affects diet 0.71 ± 0.17 0.37 ± 0.11 .03
Wakes you from sleep 1.04 ± 0.18 0.49 ± 0.13 .004
Difﬁculty swallowing 1.03 ± 0.21 0.37 ± 0.12 .002
Pain with swallowing 0.48 ± 0.13 0.18 ± 0.09 .03
Affects daily life 0.55 ± 0.16 0.14 ± 0.07 .02
Satisfaction 2.16 ± 0.25 0.55 ± 0.14 <.0001
No. patients on
34 (67%) 28 (55%) .11
1234 Reiher et al
an indication for curative PTX.
For patients with-
out these symp toms, the indications for PTX are de-
Our study showed subs tantial
improvement in all symptoms of GERD after PTX
for PHPT. Therefore, despite the lack of a clear un-
derstanding behind the mechanism of improved
symptoms, patients with PHPT who have symptoms
of GERD should be considered for curative PTX be-
cause it may decrease symptoms and the need for
long-term medication. The use of a preoperative
survey can help identify such patients.
This is the ﬁrs t study to evaluate speciﬁc symp-
toms of GERD attributable to hyperparathyroidism
and assess for changes in symptoms of GERD after
curative PTX using a validated questionnaire. The
GERD-HRQL questionnaire was used in this study
because it is a validated questionnaire, it is easy for
patients to use, and it is easy for physicians to
interpret the results. Despite our study relatively
small sample size, our results show a fairly impor-
tant improvement in the majority of patients. We
selected patients for this study based upon self-
reporting of heartburn symptoms. We di d not do
formal pH monitoring or radiographic imaging in
our patients; therefore, we do not know if the
symptoms they reported were truly related to
gastroesophageal reﬂux or if the symp toms were
related to another condition. Therefore, we do not
know if the improvement that was seen was truly
due to changes in gastric pH or decreasing reﬂux
time or if they are potentially attributable to other
reasons. The questionnaire that we used has been
well validated and does correlate highly with sen-
sitivity to the effects of GERD treatment.
Although all the patients in this study did
complain of GERD symptoms, this was not the
primary indication for surgery and the deg ree of
symptomatology varied among our cohort. There-
fore, our results are reﬂective of the general
population of patients undergoing parathyroid
surgery and may not be representative of the
subset of patients with more severe or refractory
GERD symptoms. Our ﬁndings will need to be
validated with additional studies in this popula-
tion. Interestingly, we did ﬁnd that those patients
with the greatest symptoms pre-operatively were
the most likely to show improvem ent after PTX.
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Table II. Comparison between patients with >50% improvement in scores versus patients with <50%
improvement in scores after PTX
>50% improvement in
scores (n = 34, 67%)
<50% improvement in
scores (n = 17, 33%) P value
Age, years 60 ± 2 56 ± 3 .34
31.2 ± 1.5 29.5 ± 1.5 .42
Preoperative calcium, mg/dL 10.6 ± 0.1 10.7 ± 0.3 .57
Preoperative PTH, pg/mL 142 ± 32 142 ± 34 1.0
25-hydroxy vitamin D, ng/mL 36 ± 3 36 ± 4 .91
Patients on antireﬂux medications
n = 20 (59%) n = 14 (82%) .09
Patients on antireﬂux medications
6 months postoperatively, %
n = 12 (34%) n = 14 (82%) .005
Average total preoperative score 12.1 ± 1.5 11.9 ± 2.3 .96
Average total postoperative score 1.1 ± 0.3 11.4 ± 1.1 <.0001
Data are presented as mean ± SEM.
BMI, Body mass index; PTH, parathyroid hormone; PTX, parathyroidectomy.
Volume 152, Number 6
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Dr Keith Heller (New York, NY): Did you do any-
thing to control for the placebo effect of surgery?
Could you have used as a control a comparable
group of patients with GERD who had a thyroid lo-
Dr Alexandra Reiher: We did not use thyroid pa-
tients as a control group. We did perform the post-
operative questionnaire 6 month s after PTX to
eliminate any placebo effect from the procedure.
Dr Wen Shen (San Francisco, CA): With Tums
being, obviously, a double agent, working both in
our realm of calcium supplementation, but also
for the symptoms of GERD, did you control for
people taking Tums as calcium supplementation
Dr Alexandra Reiher: You bring up an excellent
point. Again, having it be 6 months postopera-
tively, any treatment for transient hypocalcemia
or as prophylaxis had been resolved. With patients
who were taking more than 1,000 milligrams per
day, that was considered more than just calcium
Dr Wen Shen (San Francisco, CA): Did that
count within your preoperative GERD medication
list, Tums as well?
Dr Alexandra Reiher: Yes. Patients were asked if
they were on medications for heartburn and then
to describe it, and we looked at their doses as well.
Dr Marco Raffaelli (Rome, Italy): I would like to
know if you have any data about the diagnosis of
gastroesophageal reﬂux disease, if it was clinical
or if the patient had undergone an examination
before taking drugs. The second question, do
you have any data about the gastrin level s in this
group of patients that could be affected by their
Dr Alexandra Reiher: If I understand your ﬁrst
question regarding medications, the patients
were asked at the time of preoperative evaluation
if they had symptoms of heartburn. And if they
did, they completed the questionnaire. And then
those patients were followed postoperatively. We
did not perform any other measure of diagnosing
GERD, pre- or postoperatively. Regarding calcium
levels, postoperatively, the average calcium at 6
months was 9.4 in this group. Gastrin levels were
Dr Ashok R. Shaha (New York, NY): One of the
best ways to evaluate the GERD effect is to perform
ﬁberoptic laryngoscopy and observe the laryngo-
pharyngeal changes. Another way is to measure
the pH levels. I know you did not do that, but
that may be something you may want to pursue if
you really feel that the PTX does have an effect
PTX does have an effect on general symptoms
of the patient, and I’m not sure whether the
patients are interpreting the general symptoms of
wellbeing or true GERD. So, in future, you may
want to look more criti cally at the pH value and
Dr Alexandra Reiher: You bring up an excellent
point. And I agree that the next step would be to
use m ore diagnostic studies, such as pH monitor-
ing or endoscopy. But this study did look at speciﬁc
symptoms of GERD rather than just generalized
symptoms. So I think this is the next step towards
a study such as that.
Dr Quan-Yang Duh (San Francisco, CA): Did
any of these patients undergo manometry? The
gold standard of diagnosis would be esophageal
Dr Alexandra Reiher: No, we did not use spe-
ciﬁc diagnostic tests. Although I think it’s
1236 Reiher et al
important to keep in the mind that GERD is re-
lated to how symptomatic it is for the patient,
and that guides management of GERD.
Dr Stuart Wilson (Milwaukee, WI): Quan Duh
stole some of my thunder, but I wanted to make
one comment and ask one question. I think it’s
been 31 year s ago, but right after our ﬁrst annual
meeting, Bill Silen, who is one of our founding
members, was very interested in parathyroid dis-
ease and made really good observations. And he
had a group of about a dozen patients, and I think
he had talked 5 or 6 of them into esophageal
manometry. This was 31 years ago. And I think 4
of the 5 showed clearly that lower esophageal
sphincter (LES) pressure that was decreased be-
forehand had increased afterwards.
Now, of course, you can have a defect in esoph-
ageal hernia so they are not all going to respond,
but I think from a historical point of view that was
interesting. So I was going to ask one question if
you could separate out your responders and non-
responders by measuring LES pressure, because
the effect of calcium on motility of the esophagus
and LES, I think, is clear.
Volume 152, Number 6
Reiher et al 1237