Fate of dyspeptic or colonic symptoms after laparoscopic cholecystectomy.

BACKGROUND/AIMS: Gallbladder diseases can give rise to dyspeptic or colonic symptoms in addition to biliary pain. Although most biliary pain shows improvement after cholecystectomy, the fates of dyspeptic or colonic symptoms still remain controversial. This study as-sessed whether nonspecific gastrointestinal symptoms improved after laparoscopic cholecystectomy (LC) and identified the char-acteristics of patients who experienced continuing or exacerbated symptoms following surgery.
METHODS: Sixty-five patients who underwent LC for uncomplicated gallbladder stones or gallbladder polyps were enrolled. The patients were surveyed on their dyspeptic or colonic symptoms before surgery and again at 3 and 6 months after surgery. Patients' mental sanity was also assessed using a psychological symptom score with the Symptom Checklist-90-Revised questionnaire.
RESULTS: Forty-four (67.7%) patients showed one or more dyspeptic or colonic symptoms before surgery. Among these, 31 (47.7%) and 36 (55.4%) patients showed improvement at 3 and 6 months after surgery, respectively. However, 18.5% of patients showed continuing or exacerbated symptoms at 6 months after surgery. These patients did not differ with respect to gallstone or gall-bladder polyps, but differed in frequency of gastritis. These patients reported lower postoperative satisfaction. Patients with ab-dominal symptoms showed higher psychological symptom scores than others. However, poor mental sanity was not related to the symptom exacerbation.
CONCLUSIONS: Elective LC improves dyspeptic or colonic symptoms. Approximately 19% of patients reported continuing or exacerbated symp-toms following LC. Detailed history-taking regarding gastritis before surgery can be helpful in predicting patients' outcome after LC.

Introduction

The symptoms of gallstones occur in a wide range, from no symptoms to severe abdominal pain.1 In addition to abdominal pain, gallbladder stimulation by gallstones can give rise to gastrointestinal symptoms such as indigestion, nausea, vomiting and food intolerance.2 In almost all patients with gallstones, biliary pain disappears after cholecystectomy.3–5 However, the rates of relief from nonspecific gastrointestinal symptoms tend to be low and heterogeneous in patients who undergo an elective cholecystectomy.3

In contrast to patients with gallstones, most patients with gallbladder polyps are asymptomatic. However, a minority of patients report abdominal symptoms that are similar to those induced by small gallstones that are rarely detached from the mucosa.6

When cholecystectomy is recommended, many patients wondered about the relief of their symptoms and about any occurrence of new symptoms after removing the gallbladder. However, many studies have reported that the changes in abdominal symptoms after laparoscopic cholecystectomy (LC) may differ according to the selection of patients and their preoperative conditions. Variable factors were reported as predictors of poor outcomes in many different studies. The presence of gastrointestinal diseases including irritable bowel syndrome7 or bloating,8 rather than the original gallbladder disease, was also related to the persistence of symptoms after cholecystectomy. Patients with psychiatric medication,8 psychological problems,8 personality disorders9 and neuroticism10 showed poor outcomes. Patients with poor outcomes after cholecystectomy also showed decreased compliance, which complicates the effectiveness of treatment. Therefore, a method for predicting outcomes and factors related to poor outcomes is necessary in the clinical setting.

This study was designed to evaluate the outcomes of non-specific gastrointestinal symptoms after LC and to identify the factors attributable to poor outcomes. We compared symptom scores in patients with gallstones, who had typical biliary pain, and in those with gallbladder polyps, who were typically symptom free or experienced only mild abdominal discomfort. We evaluated the effects of psychological factors on the symptom outcome by scoring mental sanity in all patients with the Symptom Checklist-90 (SCL-90) questionnaire prior to surgery.

Materials and Methods

Subjects

Among 134 patients who received LC at Chungbuk National University Hospital between October 2009 and May 2010. A total 65 patients which include 32 patients with gallstones, 31 patients with gallbladder polyps and 2 patients with both gallstones and gallbladder polyps were enrolled in this study. Two patients with gallstones and gallbladder polyps were included in the gallstone group. All patients experienced relief from abdominal pain at the time of surgery and underwent elective LC. Patients were excluded for the following reasons: 19 who were younger than 15 or older than 65 years of age, 31 with acute cholecystitis, 8 with stenosis or gallstones in the biliary tract, 6 with presence of cancer and 5 with severe comorbidities. Written informed consent was obtained from all subjects prior to LC.

Dyspeptic or Colonic Symptoms at Pre- and Post-operation

Interviews were conducted 1 day before surgery to assess medical history and abdominal symptoms. Abdominal symptoms of indigestion, nausea, vomiting, food intolerance, heartburn, acid regurgitation, loss of appetite, diarrhea and constipation were recorded as 0, 1 and 2 for “none,” “weak” and “severe,” respectively. Additionally, simple psychological diagnoses and examinations using the Symptom Checklist-90-Revised (SCL-90-R) questionnaire were recorded for all patients to evaluate overall mental health prior to surgery. The SCL-90-R records 0 to 4 points for each item by self-evaluation, with measurements consisting of 90 items. Overall, the global severity index, positive symptom distress index, and positive symptom total were measured. The SCL-90-R used internet scoring (testcenter.co.kr) operated by Test Center Inc. (Seoul, South Korea). Total scores for abdominal symptoms were recorded at 3 and 6 months after surgery through phone interviews and compared with preoperative scores. Patients were determined to have an overall improvement when they remained in an asymptomatic state or showed a decrease in total symptom scores.

Pathologic Evaluation of Cholecystectomized Gallbladder

All gallbladder specimens were sent for histopathology. The presence of chronic cholecystitis, gallbladder wall thickening and adenomatous hyperplasia were analyzed as pathological data. Chronic cholecystitis was diagnosed when the mucosa was infiltrated with mononuclear inflammatory cells and the epithelium showed atrophic, hyperplastic or metaplastic changes. A gall-bladder wall ≥ 3 mm in thickness was defined as thickened. Adenomatous hyperplasia was defined by the presence of hyperplasia of the gallbladder wall, limited to the epithelial elements of the mucosa without the involvement of the muscular layer.11

Statistical Methods

Discrete variables, including symptoms and clinical features, were evaluated using the Chi-square test, while the t test or paired t test was used to assess changes in symptom scores before and after surgery. SCL-90-R results were analyzed using the Mann-Whitney U test to assess the relationship between patients’ symptoms before and after surgery. P-values less than 0.05 were considered to be statistically significant. All analyses were performed using the SPSS software (ver. 12; SPSS Inc., Chicago, USA).

Results

Characteristics of Patients With Gallstones or Gallbladder Polyps

Among the 34 patients with gallstones or 31 patients with gallbladder polyps, no differences were noted for gender, ages, history of abdominal surgery, or history of pancreatitis or hepatitis. Two patients with gallstones were currently using a psychiatric medication. Twelve patients were diagnosed with gastritis by an endoscopic exam less than 2 months before surgery. All but 3 patients with gallbladder polyps had chronic cholecystitis. Gallbladder wall thickening more than 3 mm was detected in 67.6% and 54.8% of patients with gallstones and gallbladder polyps, respectively. Adenomatous hyperplasia was detected in seven patients with gallstones and in one patient with gallbladder polyp. Prior to surgery, all patients’ blood and liver function tests were in normal ranges (Table 1).

Table 1.

Clinical Characteristics of 65 Patients With Gallbladder Diseases

Parameters	Gallstones (n = 34)	Gallbladder polyps (n = 31)	P-value
Male:Female	16:18	19:12	NS
Age (mean ± SD, yr)	45.0 ± 7.0	46.0 ± 6.0	NS
Past medical history (n [%])
Abdominal surgery	11 (32.4)	11 (35.5)	NS
Pancreatitis or hepatitis	5 (14.7)	2 (6.5)	NS
Psychiatric drugs	2 (5.9)	0 (0.0)	NS
Gastritis	6 (17.6)	6 (19.4)	NS
Laboratory findings (mean ± SD)
AST (IU/L)	22.5 ± 4.5	23.6 ± 6.6	NS
ALT (IU/L)	32.6 ± 18.5	23.7 ± 12.9	0.030
Alkaline phosphatase (IU/L)	176.2 ± 62.9	154.5 ± 66.8	NS
WBC (/mm3)	6,650 ± 1,388	6,319 ± 1,811	NS
Histopathological findings (n [%])
Chronic cholecystitis	34 (100.0)	28 (90.3)	NS
GB wall thicking (≥ 3 mm)	23 (67.6)	17 (54.8)	NS
Adenomatous hyperplasia	7 (20.6)	1 (3.2)	0.033

AST, aspartate transaminase; ALT, alanine transaminase; WBC, white blood cell; GB, gallbladder; NS, not significant.

Patients’ Dyspeptic or Colonic Symptoms Before and After Elective Laparoscopic Cholecystectomy

One or more abnormalities in abdominal symptoms were recorded in 44 (67.7%) patients, including indigestion (50.8%), nausea (26.2%), heartburn (23%), loss of appetite (21.5%), food intolerance (20%), constipation (18.5%), acid regurgitation (9.2%), diarrhea (7.7%) and vomiting (4.6%) (Table 2). Abdominal symptom score (range, 0–18) before surgery was 1.92. This score decreased to 1.11 and 0.88, at 3 months and 6 months after surgery, respectively (P = 0.006 and P < 0.001 by a paired t test). The number of patients who showed improved symptom scores was 31 (47.7%) and 36 (55.4%) after 3 and 6 months, respectively. Among abdominal symptoms, indigestion, food intolerance, heartburn and constipation were improved after 3 and 6 months. However, nausea, vomiting, loss of appetite and acid regurgitation did not differ before and after surgery. Diarrhea, which was aggravated 3 months after surgery, was restored to the pre-surgical level at 6 months after surgery (Table 2).

Table 2.

Frequencies of Dyspeptic or Colonic Symptoms Before and After Laparoscopic Cholecystectomy

Symptoms	Before	3 months after surgery	6 months after surgery	P1-value	P2-value
Absence	21 (32.3)	42 (64.6)	45 (69.2)	-	-
Overall symptom scores (mean ± SD)	1.92 ± 2.11	1.11 ± 1.78	0.88 ± 1.68	0.006a	< 0.001a
Indigestion				0.035	0.013
None	32 (49.2)	46 (70.8)	50 (76.9)
Weak	20 (30.8)	15 (23.1)	11 (16.9)
Severe	13 (20.0)	4 (6.1)	4 (6.2)
Nausea				NS	NS
None	48 (73.8)	57 (87.7)	57 (87.7)
Weak	15 (23.1)	8 (12.3)	8 (12.3)
Severe	2 (3.1)	0 (0.0)	0 (0.0)
Vomiting				NS	NS
None	62 (95.4)	65 (100.0)	62 (95.4)
Weak	3 (4.6)	0 (0.0)	3 (4.6)
Severe	0 (0.0)	0 (0.0)	0 (0.0)
Food intolerance				0.006	< 0.001
None	52 (80)	51 (78.5)	55 (84.6)
Weak	7 (10.8)	14 (21.5)	8 (12.3)
Severe	6 (9.2)	0 (0.0)	2 (3.1)
Heart burn				0.014	0.024
None	50 (76.9)	55 (84.6)	57 (87.7)
Weak	14 (21.5)	10 (15.4)	8 (12.3)
Severe	1 (1.5)	0 (0.0)	0 (0.0)
Acid regurgitation				NS	NS
None	59 (90.8)	61 (93.8)	62 (95.4)
Weak	5 (7.7)	4 (6.2)	3 (4.6)
Severe	1 (1.5)	0 (0.0)	0 (0.0)
Loss of appetite				NS	NS
None	51 (78.5)	54 (83.1)	61 (93.8)
Weak	13 (20.0)	9 (13.8)	4 (6.2)
Severe	1 (1.5)	2 (3.1)	0 (0.0)
Diarrhea				0.050	NS
None	60 (92.3)	51 (80.0)	59 (86.2)
Weak	5 (7.7)	10 (15.4)	9 (13.8)
Severe	0 (0.0)	3 (4.6)	0 (0.0)
Constipation				< 0.001	< 0.001
None	53 (81.5)	56 (86.2)	57 (87.7)
Weak	9 (13.8)	9 (13.8)	8 (12.3)
Severe	3 (4.6)	0 (0)	0 (0.0)

Paired t test.

P, P-value of before 3 months vs. post 3 months; P, P-value of before 6 months vs. post 6 months; NS, not significant. Data are presented as n (%).

Relation Between Dyspeptic or Colonic Symptoms and Psychological Symptom Scores

A simple psychiatric test before surgery showed great differences between symptom positive and negative group. Specifically, patients with abdominal symptoms had significantly higher values than patients without symptoms regarding somatization, obsessive-compulsion, interpersonal sensitivity, depression, anxiety, and paranoid ideation. Overall group measurements were also higher regarding global severity index, positive symptom distress index, and positive symptom total. However, no differences were noted between the groups for measures of hostility, phobic anxiety, and psychoticism (Table 3).

Table 3.

Comparison of Psychological Symptom Scores Between Symptomatic and Asymptomatic Patients Before Laparoscopic Cholecystectomy

Symptom Checklist-90-Revised	Symptomatic patients (n = 44)	Asymptomatic patients (n = 21)	P-value
Somatization	46.9 ± 6.9	39.0 ± 2.8	< 0.001
Obsessive-compulsion	41.3 ± 8.0	36.1 ± 4.7	< 0.001
Interpersonal sensitivity	42.4 ± 8.7	36.9 ± 3.3	< 0.001
Depression	42.4 ± 7.9	36.4 ± 4.5	< 0.001
Anxiety	44.2 ± 7.0	40.1 ± 4.6	0.015
Hostility	43.6 ± 6.9	40.5 ± 2.2	0.060
Phobic anxiety	45.2 ± 6.8	42.1 ± 1.6	0.148
Paranoid ideation	41.8 ± 6.0	39.4 ± 3.5	0.040
Psychoticism	42.6 ± 7.2	39.8 ± 2.9	0.063
Global severity index	42.3 ± 7.6	36.4 ± 3.6	< 0.001
Positive symptom distress	46.9 ± 8.7	39.9 ± 12.3	0.020
Positive symptom total	39.9 ± 8.2	31.4 ± 6.2	< 0.001

Data are presented as mean ± SD of T score.

Clinical Features of Patients With Continuing or Exacerbated Symptoms After Surgery

At 6 months after cholecystectomy, 12 of 65 (18.5%) patients had either no improvement or an increased total symptom score compared to before surgery. No difference was noted between improved and unimproved patients in regard to gallstones or gallbladder polyps, gender, age, educational levels, economic conditions, marital status, gallbladder pathology or history of abdominal surgery. However, the patients having gastritis showed poor outcomes (P = 0.007, Table 4). The patients without gastritis showed total symptom scores to be decreased at 3 months and 6 months after LC compared to those at the time of enrollment, especially regarding the dyspeptic symptoms. However, the patients with gastritis did not show improvements of dyspeptic or colonic symptoms (Figure). Patients’ surgical satisfaction differed depending on the degree of symptom improvement after surgery (P < 0.001, Table 4). Only 33.3% of patients with unimproved abdominal symptoms were satisfied with their surgery, while 94.3% of patients with symptom improvement were satisfied. No significant difference was detected in SCL-90-R examination values with respect to the patients’ outcomes (Table 5).

Table 4.

Clinical and Epidemiological Characteristics of Patients With Worsened Abdominal Symptoms at 6 Months After Laparoscopic Cholecystectomy

Parameters	n	Improved patients (n = 53)	Unimproved patients (n = 12)	P-value
Male	35	29 (82.9)	6 (17.1)	NS
Age (mean ± SD, yr)	65	45.8 ± 6.7	45.0 ± 6.4	NS
Types of gallbladder diseases				NS
Gallbladder stones	34	26 (76.5)	8 (23.5)
Gallbladder polyps	31	27 (87.1)	4 (12.9)
Education status				NS
Less than college	43	36 (83.7)	7 (16.3)
University graduates	22	17 (77.3)	5 (22.7)
Socioeconomic status				NS
Less than intermediate	14	11 (78.6)	3 (21.4)
Medium or more	51	42 (82.4)	9 (17.6)
Marriage				NS
Unmarried	10	7 (70.0)	3 (30.0)
Married	55	46 (83.6)	9 (16.4)
Past medical history
Abdominal surgery	22	18 (81.8)	4 (18.2)	NS
Pancreatitis or hepatitis	7	7 (100.0)	0 (0.0)	NS
Psychiatric treatment	2	1 (50.0)	1 (50.0)	NS
Gastritis	12	6 (50.0)	6 (50.0)	0.007
Histopathologic findings
Chronic cholecystitis	62	51 (82.3)	11 (17.7)	NS
GB wall thicking (≥ 3 mm)	40	33 (82.5)	7 (17.5)	NS
Adenomatous hyperplasia	8	5 (62.5)	3 (37.5)	NS
Patients’ satisfaction				< 0.001
Very satisfied	38	38 (100.0)	0 (0.0)
Satisfied	16	12 (75.0)	4 (25.0)
Neutral	10	3 (30.0)	7 (70.0)
Dissatisfied	1	0 (0.0)	1 (100.0)

GB, gallbladder; NS, not significant.

Data are presented as n (%).

Figure.

Changes of symptom scores, total, dyspeptic or colonic symptoms, before surgery and at 3 and 6 months after surgery in patients without gastritis (A) and in those with gastritis (B). Dyspeptic symptoms include indigestion, nausea, vomiting, food intolerance, heart burn, acid regurgitation and loss of appetite. Colonic symptoms represent diarrhea and constipation.

Table 5.

Changes in Psychological Symptom Scores According to Gastrointestinal Symptom Improvement at 6 Months After Laparoscopic Cholecystectomy

Symptom Checklist-90-Revised	Improved patients (n = 53)	Unimproved patients (n = 12)	P-value
Somatization	45.3 ± 7.5	44.6 ± 5.2	NS
Obsessive-compulsion	40.2 ± 7.4	39.3 ± 9.3	NS
Interpersonal sensitivity	41.6 ± 8.2	41.8 ± 8.9	NS
Depression	42.2 ± 8.0	41.1 ± 8.2	NS
Anxiety	43.2 ± 6.9	43.0 ± 6.4	NS
Hostility	42.9 ± 5.5	44.2 ± 10.2	NS
Phobic anxiety	44.8 ± 6.7	44.3 ± 4.6	NS
Paranoid ideation	41.4 ± 5.5	41.8 ± 7.7	NS
Psychoticism	42.3 ± 7.2	42.1 ± 4.9	NS
Global severity index	41.1 ± 7.4	40.9 ± 8.2	NS
Positive symptom distress	45.2 ± 10.5	43.2 ± 12.9	NS
Positive symptom total	38.3 ± 9.2	37.6 ± 7.3	NS

NS, not significant.

Data are presented as mean ± SD of T score.

Discussion

This study demonstrated that elective LC improves non-specific gastrointestinal symptoms; the number of patients having abdominal symptoms decreased from 44 (67.7%) before surgery, to 23 (35.4%) and then 20 (30.8%), respectively, at 3 and 6 months after surgery. Scores for symptoms before and after surgery showed the same trend, with the average score of 1.92 before surgery decreasing to 1.11 and 0.88 at 3 and 6 months, respectively. Symptoms were improved in patients with gallstones or gallbladder polyps, regardless of the type of disease.

Previous studies revealed that abdominal symptoms continued in 43–57% even after elective LC in patients with gallstones.2,8,12,13 In contrast, the present study showed a lower rate of continuous symptoms than those of previous studies. The reasons may be that all patients except three had chronic cholecystitis and severe pathologic changes are usually related with a high rate of symptom relief.14 Similar to previous reports,3,8,15,16 our findings showed that indigestion, food intolerance, heartburn, and constipation were improved after surgery. However, nausea, vomiting, and acid regurgitation did not differ before and after surgery. The incidence of diarrhea increased temporarily at 3 months after surgery and then recovered by 6 months. Currently, no studies have reported any variations in symptoms before and after surgery for patients with gallbladder polyps. This study confirmed that more than half of the patients with gallbladder polyps also reported dyspeptic or colonic symptoms before surgery and showed improvements after surgery which is a similar feature presented in patients with gallstones.

Nevertheless, cholecystectomy was not effective in easing the symptoms for every patient, because no symptom improvement or a worsening of symptoms occurred in 12 of 65 (18.5%) patients at 6 months after surgery. Abdominal symptoms may have resulted from diseases in organs other than the gallbladder because many patients with no improvement in symptoms were diagnosed with gastritis before surgery. Sosada et al.17 reported that many symptoms had originated from gastrointestinal tracts and not from the gallbladder. In the present study, twelve patients were diagnosed with gastritis by endoscopy and these patients showed poor outcomes. Other studies revealed that the presence of irritable bowel syndrome7 or bloating8 was also related with persistent symptoms after cholecystectomy.

At present, no obvious correlation can be drawn from the literature regarding psychiatric problems and worsening symptoms after surgery. Previous studies suggested that patients with continuous pain after surgery had increased psychological vulnerability.14,18,19 However, other study reported that psychiatric factors had no special relationship with symptom variation after surgery.11 The current study considered that psychiatric conditions before a surgery did not greatly affect variation in symptoms after surgery, although they showed significant differences when compared with the scores for patients with no symptoms.

Cholecystectomy has been recommended under limited conditions.20,21 Although controversy remains whether cholecystectomy should be performed in gallstone patients with dyspeptic or colonic symptoms, many reports show that atypical symptoms are improved after cholecystectomy in gallstone patients, suggesting the need to offer cholecystectomy to these patients.22 Considering that these studies found chronic cholecystitis in 95% of cases after cholecystectomy, atypical abdominal symptoms are likely to occur as a result of chronic inflammation. However, it is very difficult to identify patients with gallstones or gallbladder polyps for treatment when they report atypical abdominal symptoms, because symptom variation is very subjective. Although the causes of dyspeptic or colonic symptoms in patients with gallbladder polyps or gallstones have not been clarified, the present view is that surgery should be performed when other medical treatments have been tried and after the existence of gastritis is ruled out. In the present study, patient’s satisfaction on surgery differed depending on the degree of symptom improvement after surgery.

Approximately two-thirds of patients who underwent gallbladder surgery showed improvement in their abdominal symptoms irrespective of gallstones or gallbladder polyps. Many patients with no improvement in their symptoms had been diagnosed with gastritis before surgery and their satisfaction with surgery was low. Detailed history-taking regarding gastritis before surgery can be helpful in predicting patients’ outcome after LC.