Cholecystectomy and the risk of alimentary tract cancers: A systematic review

Table 1 Descriptive characteristics of studies on the association between cholecystectomy and oesophageal adenocarcinoma

Ref.	Period of study	Study design	No. of cases	No. of controls	Exposure ascertainment	Outcome ascertainment	Follow-up (yr)	Effect estimate	Adjustments	Quality of publication
Freedman et al[20], 2000	1994-1997	Case-control	189	820	Self report	Pathology records	-	RR = 1.03 (0.63-1.69)	Age, gender, alcohol, smoking, BMI, physical activity, education, diet	37
Nogueira et al[21], 2014	1992-2005	Case-control	132/5488	2572/1000000	Medicare database	Cancer registry	> 6	OR = 0.95 (0.80-1.14)	Age, gender, diabetes	49
Freedman et al[23], 2001	1965-1997	Cohort	53/268312		National registry	Cancer registry	> 10	SIR = 1.3 (1.0-1.8)	Age, gender	38
Goldacre et al[22], 2005	1963-1999	Cohort	91/39245	803/334813	NHS database	Cancer registry	NA	RR = 0.98 (0.79-1.21)	Age, gender, calendar year, residence	36
Lagergren and Mattsson[24], 2011	1965-2008	Cohort	126	345251	NA	Cancer registry	15	RR = 1.29 (1.07-1.53)	Age, gender, calendar Year	40

NA: Not available; BMI: Body mass index.

Table 2 Descriptive characteristics of studies on the association between cholecystectomy and oesophageal squamous cell cancer

Ref.	Period of study	Study design	No. of cases	No. of controls	Exposure ascertainment	Outcome ascertainment	Follow-up (yr)	Effect estimate	Adjustments	Quality of publication
Freedman et al[20], 2000	1994-1997	Case-control	167	820	Self-report	Pathology records		OR = 0.82 (0.43-1.54)	Age, gender, alcohol, smoking, BMI, physical activity, education, diet	37
Nogueira et al[21], 2014	1992-2005	Case-control	100/4732	2572/100000	Medicare database	Cancer registry	> 6	OR = 0.85 (0.69-1.04)	Age, gender, diabetes	49
Ichimiya et al[26], 1986	1953-1984	Cohort	29	1238	Self report	Death registry	< 31	0.59 (0.26-1.36	Age, gender	48
Freedman et al[23], 2001	1965-1997	Cohort	129/268312	NA	National registry	Cancer registry	> 10	SIR = 0.9 (0.7-1.1)	Age, gender	38
Lagergren and Mattsson[24], 2011	1965-2008	Cohort	193/345251		NA	Cancer registry	15	SIR 0.93 (0.81-1.08)	Age, gender, calendar year	40

Ichimiya et al[26], 1986, reported on oesophageal cancer without specifying pathology of cancer. NA: Not available; BMI: Body mass index.

Table 3 Descriptive characteristics of studies on the association between cholecystectomy and gastric cardia cancer

Ref.	Period of study	Study design	No. of cases	No. of controls	Exposure ascertainment	Outcome ascertainment	Follow-up (yr)	Effect estimate	Adjustments	Quality of publication
Freedman et al[20], 2000	1994-1997	Case-control	262	820	Self-report	Pathology	-	RR = 0.67 (0.39-1.13)	Age, gender, alcohol, smoking, BMI, physical activity, education, diet	37
Nogueira et al[21], 2014	1992-2005	Case-control	122/5579	2572/100000	Medicare database	Cancer registry	> 6	OR = 0.88 (0.73-1.06)	Age, gender, diabetes	49
Fall et al[28], 2007	1970-1997	Cohort	94/251672	NA	National registry	Cancer registry	11.5	RR = 0.95 (0.76-1.16)	Age, gender, surgical procedure	42

NA: Not available; BMI: Body mass index.

Table 4 Descriptive characteristics of studies on the association between cholecystectomy and gastric cancer

Ref.	Period of study	Study design	No. of cases	No. of controls	Exposure ascertainment	Outcome ascertainment	Follow-up (yr)	Effect estimate	Adjustments	Quality of publication
Sarli et al[27], 1986	1980-1984	Case control	157	157	Surgical and database	Pathology	NA	0.77 (0.09-6.40)	Age, gender	26
Ichimiya et al[26], 1986	1953-1984	Cohort	29	1238	Self report	Death registry	NA	0.92 (0.66-1.28)	Age, gender	33
Nogueira et al[21], 2014	1992-2005	Case-control	429/12925	2572/100000	Medicare database	Cancer registry	> 6	OR = 1.26 (1.13-1.40)	Age, gender, diabetes	49
Goldacre et al[22], 2005	1963-1999	Cohort	177/39254	1354/334813	NHS database	Cancer registry	NA	1.06 (0.88-1.26)	Age, gender, calendar year, residence	36
Fall et al[28], 2007	1970-1997	Cohort	854/251672	NA	National registry	Cancer registry	11.5	1.11 (1.04-1.19)	Age, gender, surgical procedure	42
Chen et al[29], 2014	2000-2010	Cohort	31/5850		National database	Cancer registry	10	1.81 (1.09-3.02)	Age, gender, comorbidities	53

NA: Not available.

Table 5 Descriptive characteristics of studies on the association between cholecystectomy and pancreatic cancer

Ref.	Period of study	Study design	No. of cases	No. of controls	Exposure ascertainment	Outcome ascertainment	Follow-up (yr)	Effect estimate	Adjustments	Quality of publication
Wynder et al[37], 1973	1950-1964	Case-control	11/142	16/307	Hospital records	NA	> 2	1.57 (0.76-3.24)1	Age, gender, race, hospital	28
Haines et al[38], 1982	1973-1978	Case-control	8/116	18/232	Hospital records	Medical records	≥ 5	0.89 (0.40-1.98)1	Age, gender, race, year of admission	27
Mack et al[39], 1986	1976-1981	Case-control	38/490	44/490	Hospital records	Pathology records	> 1	0.8 (0.5-1.4)	Age, gender, race	27
Cuzick and Babiker[40] 1989	1983-1986	Case-control	14/216	7/279	Hospital records	Medical records	NA	2.43 (0.91-7.12	Age, gender	29
Farrow and Davis[41] 1990	1982-1986	Case-control	8/218	6/188	Hospital records	Cancer registry	≥ 3	1.1 (0.3-3.4)	Age	29
Bueno de Mesquite et al[42], 1992	1984-1988	Case-control	24/176	44/487	Hospital records	Medical records	> 5	1.15 (0.55-2.40)	Age, response status, smoking	31
Lee et al[43], 1996	1989-1994	Case-control	12/282	6/282	Hospital records	Medical records	NA	2.04 (0.76-6.21)	Age, gender	43
Gullo et al[45], 1996	1987-1992	Case-Control	93/720	71/720	Hospital records	Medical records	> 1	1.00 (0.70-1.43)	Age, gender	34
Silverman et al[30], 2001	1986-1989	Case-Control	132/484	150/2099	Hospital records	Pathology records	> 2	1.77 (1.26-2.48)1	Age, race, gender, smoking, alcohol consumption, BMI, Calorie intake.	31
Ko et al[32], 2007	1995-1999	Case-control	75/532	155/1701	Hospital records	SEER abstracts	NA	1.73 (1.29-2.33)1	Ag, gender, BMI, smoking, diabetes	36
Hassan et al[44], 2007	2000-2006	Case-Control	808	808	Hospital records	Self reported	> 2	OR = 1.1 (0.9-1.8)	Age, gender, smoking, comorbidities	35
Zhang et al[31], 2014	1994-1998	Case-Control	215	676	Self report	Pathology reports	> 2	2.11 (1.32-3.35)	Age, gender, race, smoking, physical activity, diabetes	51
Nogueira et al[21], 2014	1992-2005	Case-control	1106/33280	2572/100000	Medicare database	Cancer registry	> 6	OR = 1.23 (1.15-1.33)	Age, gender, diabetes	49
Ichimiya et al[26], 1986	1953-1984	Cohort	3/1238	NA	National registry	Death registry	NA	SMR = 0.86 (0.33-2.25)1	Age, gender	33
Shibata et al[46], 1994	1981-1990	Cohort	65/13979	NA	Hospital records	NA	> 4	RR = 2.09 (0.99-4.39)	Age, gender, smoking	32
Ekbom et al[33], 1996	1965-1987	Cohort	261/62615	NA	National registry	Cancer registry	> 1	1.20 (1.06-1.36)	Age, gender	28
Chow et al[34], 1999	1977-1993	Cohort	184/42461	NA	National registry	Cancer registry	≥ 4	1.3 (1.1-1.6)	Age, gender, obesity, years of follow-up, other comorbidities	33
Coughlin et al[35], 2000	1982-1996	Cohort	3751/1.2 M	NA	Study database	Cancer registry	14	RR = 1.2 (1.0-1.5)	Age, gender, smoking, race, education, BMI, diet.	31
Ye et al[48], 2001	1965-1997	Cohort	730/268312	NA	National database	Cancer registry	≥ 2	SIR = 1.06 (0.98-1.14)	Age, gender, calendar year	35
Schernhammer et al[47], 2002	1976-1986	Cohort	37/145927	256/1675355	Self-report	Self report and death registry	> 10	1.23 (0.86-1.77)	Age, gender, BMI, Physical activity, diabetes	34
Goldacre et al[22], 2005	1963-1999	Cohort	127/39254	791/334813	NHS database	Cancer registry	≥ 2	1.06 (0.88-1.26)	Age, gender, calendar year, residence.	36
Arnold et al[36], 2009	1984-2004	Cohort	6243/1060389	NA	Hospital records	Death registry	NA	HR = 1.62 (1.02-2.55) blackHR = 1.10 (1.0-1.22) white	Age, gender, BMI, smoking, FH of pancreatic cancer, diabetes.	41
Chen et al[29], 2014	2000-2010	Cohort	16/5850		National database	Cancer registry	10	1.13 (0.60-2.12)	Age, gender, comorbidities	53

¹RR and 95% confidence intervals were calculated from raw data. NA: Not available; BMI: Body mass index.

Table 6 Descriptive characteristics of studies on the association between cholecystectomy and extrahepatic bile duct cancer

Ref.	Period of study	Study design	No. of cases	No. of controls	Exposure ascertainment	Outcome ascertainment	Follow-up (yr)	Effect estimate	Adjustments	Quality of publication
Nogueira et al[21], 2014	1992-2005	Case-control	118/3681	2572/100000	Medicare database	Cancer registry	> 6	OR = 1.19 (0.98-1.43)	Age, gender, diabetes	49
Chow et al[34], 1999	1977-1993	Cohort	16/42461	NA	National registry	Cancer registry	≥ 4	0.7 (0.3-1.4)	Age, gender, obesity, years of follow-up, other comorbidities	33
Chen et al[29], 2014	2000-2010	Cohort	9/5850		National database	Cancer registry	10	2.22 (0.91-5.41)	Age, gender, comorbidities	53

NA: Not available.

Table 7 Descriptive characteristics of studies on the association between cholecystectomy and liver cancer

Ref.	Period of study	Study design	No. of cases	No. of controls	Exposure ascertainment	Outcome ascertainment	Follow-up (yr)	Effect estimate	Adjustments	Quality of publication
Nogueira et al[21], 2014	1992-2005	Case-control	332/10219	2572/100000	Medicare database	Cancer registry	> 6	OR = 1.23 (1.15-1.33)	Age, gender, diabetes	49
Chow et al[34], 1999	1977-1993	Cohort	48/42461	NA	National registry	Cancer registry	≥ 4	1.1 (0.7-1.5)	Age, gender, obesity, years of follow-up, other comorbidities	33
Goldacre et al[22], 2005	1963-1999	Cohort	38/39245	306/334813	NHS database	Cancer registry	NA	0.91 (0.64-1.25)	Age, gender, calendar year, residence	36
Chen et al[29], 2014	2000-2010	Cohort	87/5850	163/5850	National database	Cancer registry	10	1.17 (0.90-1.52)	Age, gender, comorbidities	53

NA: Not available.

Table 8 Descriptive characteristics of studies on the association between cholecystectomy and small intestinal cancer

Ref.	Period of study	Study design	No. of cases	No. of controls	Exposure ascertainment	Outcome ascertainment	Follow-up (yr)	Effect estimate	Adjustments	Quality of publication
Nogueira et al[21], 2014	1992-2005	Case-control	148/3694	2572/100000	Medicare database	Cancer registry	> 6	OR = 1.49 (1.26-1.77)	Age, gender	49
Lagergren et al[51], 2001	1965-1997	Cohort	68/2784601	NA	National registry	National registry	10	1.77 (1.37-2.24)	Age, gender, time aftercholecystectomy	38
Lagergren et al[51], 2001	1965-1997	Cohort	98/2784602	NA	National registry	National registry	10	1.71 (1.39-2.08)	Age, gender, time aftercholecystectomy	38
Goldacre et al[52], 2012	1998-2008	Cohort	NA	327460/3M	HES database	Cancer registry	10	2.47 (0.82-6.28)	Age, gender, period since cholecystectomy	45

¹Proximal small bowel adenocarcinoma;

²Distal small bowel carcinoids. NA: Not available.

Table 9 Descriptive characteristics of studies on the association between cholecystectomy and colorectal cancer

Ref.	Period of study	Study design	No. of cases	No. of controls	Exposure ascertainment	Outcome ascertainment	Follow-up (yr)	Effect estimate	Adjustments	Quality of publication
Nogueira et al[21], 2014	1992-2005	Case-control	3907/150045	2572/100000	Medicare database	Cancer registry	> 6	OR = 0.97 (0.92-1.02)	Age, gender	49
Schmidt et al[60], 2012	1992 -1994	Case-Control	10/254	0/1043	National database	Cancer registry	24	HR = 1.20 (0.85-1.70)	Age, gender	41
Todoroki et al[67], 1999	1991-1994	Case-Control	226/1982	270/2129	Medicare database and self report	Cancer registry	≥ 2	OR = 1.1 (0.9-1.3)	Age, gender, Family history, BMI, diet, NSAIDs	48
Zeng et al[62], 1993	1965-1986	Case-Control	8/503	18/2188	Hospital records	Hospital records	≥ 2.5	OR = 1.95 (0.84-4.51)		26
Neugut et al[66], 1991	1986-1988	Case-Control	11/106	41/507	Hospital Records	Self-report	2	OR = 0.96 (0.46-1.98)	Age, gender	34
Lee et al[54], 1989	1980-1987	Case-Control	40/165	19/165	Hospital Records	Hospital Records	≥ 2	RR = 2.11 (1.19-3.85)		30
Kune et al[65], 1988	1980-1981	Case-Control	35/715	57/727	Hospital Records	Self-reporting and hospital records		RR = 1.10 (0.7-1.1)		36
Neugut et al[58], 1988	1983-1985	Case-Control	11/56	10/84	Hospital records	Self-reporting		OR = 1.8 (0.6-5.4)	Age, socioeconomic status	38
Friedman et al[63], 1987	1971-1984	Case-Control	174/5898	773/27687	Medicare Database	Cancer registry	≥ 2	OR = 1.1 (0.9-1.2)	Age, gender, geographical area, calendar year	47
1Weiss et al[53], 1982	1976-1977	Case-Control	92	687	Cancer Registry	Self-reporting	≥ 1	RR = 1.4 (0.7-2.6)		40
2Turnbull et al[61], 1981	1972-1976	Case-Control	20/305	5	Hospital records	Hospital records	> 5	RR = 2.7		33
Chen et al[29], 2014	2000-2010	Cohort	67/5850	76/5850	National database	Cancer registry	10	HR = 1.56 (1.12-2.17)	Age, gender, comorbidities	53
2Hartz et al[55], 2012	1993-1998	Cohort	1207/150912	NA	National database	Self-report	8	HR = 1.36 (1.13-1.64)	Age, smoking, obesity, Family history, comorbidities	48
Shao et al[56], 2005	1987-2002	Cohort	297/55960	574668	National database	National database		IRR = 1.32 (1.16-1.48	Age, gender	54
2Schernhammer et al[59], 2003	1982-1998	Cohort	133/6669	78515	National database of nurses	Self-report and National death registry	16	RR = 1.21 (1.01-1.46)	Age, smoking, BMI, lifestyle factors, comorbidities	57
1Johansen et al[64], 1996	1977-1989	Cohort	225/42098	NA	Hospital database	Cancer registry	1-16	RR = 1.09 (1.0-1.2)	Age, gender, calendar year	43
Linos et al[57], 1981	1950-1969	Cohort	42/1681		Hospital database	Hospital records and self reporting		2RR = 1.3 (0.9-1.9)3RR = 1.3 (0.7-2.2)		34

¹Excluding rectal cancer;

²Women only;

³Men only; NA: Not available; BMI: Body mass index; NSAIDs: Nonsteroidal anti-inflammatory drugs.

Table 10 Descriptive characteristics of studies on the association between cholecystectomy and proximal colon cancer

Ref.	Period of study	Study design	No. of cases	No. of controls	Exposure ascertainment	Outcome ascertainment	Follow-up (yr)	Effect estimate	Adjustments	Quality of publication
Nogueira et al[21], 2014	1992-2005	Case-control	1963/66740	2,572/100000	Medicare database	Cancer registry	> 6	OR = 1.06 (0.99-1.12)	Age, gender	49
Todoroki et al[67], 1999	1991-1994	Case-control	134/967	270/2129	Medicare database and self report	Cancer registry	≥ 2	OR = 1.3 (1.0-1.6)	Age, gender, family history, BMI, diet, NSAID use	48
Zeng et al[62], 1993	1965-1986	Case-control	5/108	18/2188	Hospital records	Hospital records	≥ 2.5	OR = 5.85 (2.13-16.7)		26
Friedman et al[63], 1987	1971-1984	Case-control	70/1925	773/27687	Medicare Database	Cancer registry	≥ 2	OR = 1.2 (0.9-1.5)	Age, gender, geographical area, calendar year	47
Vernick et al[69], 1981	1975-1978	Case-control	21/150	23/250	National database	Self-report and hospital records		RR = 1.77 (0.95-3.3)		44
1Schernhammer et al[59], 2003	1982-1998	Cohort	46/6669	78515	National database of nurses	Self-report and National death registry	16	RR = 1.35 (0.97-1.88)	Age, smoking, BMI, lifestyle factors, comorbidities	57
Lagergren et al[51], 2001	1965-1997	Cohort	861/278460	NA	National registry	National registry	10	SIR = 1.16 (1.08-1.24)	Age, gender, time after cholecystectomy	35
1Ekbom et al[68], 1993	1965-1983	Cohort	633/62615		National registry	National registry	< 23	SIR = 1.24 (1.03-1.48)	Age	46

¹Women only. NA: Not available; BMI: Body mass index; NSAIDs: Nonsteroidal anti-inflammatory drugs.

Table 11 Descriptive characteristics of studies on the association between cholecystectomy and distal colon cancer

Ref.	Period of study	Study design	No. of cases	No. of controls	Exposure ascertainment	Outcome ascertainment	Follow-up (yr)	Effect estimate	Adjustments	Quality of publication
Nogueira et al[21], 2014	1992-2005	Case-control	986/40996	2572/100000	Medicare database	Cancer registry	> 6	OR = 0.93 (0.86-1.00)	Age, gender	49
Todoroki et al[67], 1999	1991-1994	Case-Control	87/965	270/2129	Medicare database and self report	Cancer registry	≥ 2	OR = 0.8 (0.6-1.1)	Age, gender, Family history, BMI, diet, NSAID use	48
Zeng et al[62], 1993	1965-1986	Case-Control	2/131	18/2188	Hospital records	Hospital records	≥ 2.5	OR = 1.87 (0.43-8.14)		26
Friedman et al[63], 1987	1971-1984	Case-Control	60/1963	773/27687	Medicare database	Cancer registry	≥ 2	OR = 1.2 (0.9-1.6)	Age, gender, geographical area, calendar year	47
Schernhammer et al[59], 2003	1982-1998	Cohort	28/6669	78515	National database of nurses	Self-report and National death registry	16	RR = 0.95 (0.64-1.43)	Age, smoking, BMI, lifestyle factors, comorbidities	57
Lagergren et al[51], 2001	1965-1997	Cohort	2564/278460	NA	National registry	National registry	10	SIR = 0.98 (0.94-1.02)	Age, gender, time after cholecystectomy	35

NA: Not available; BMI: Body mass index; NSAIDs: Nonsteroidal anti-inflammatory drugs.

Table 12 Descriptive characteristics of studies on the association between cholecystectomy and rectal cancer

Ref.	Period of study	Study design	No. of cases	No. of controls	Exposure ascertainment	Outcome ascertainment	Follow-up (yr)	Effect estimate	Adjustments	Quality of publication
Chiong et al[70], 2012	1950-2012	Meta-Analysis	14226/460262	NA	Mixed sources	Mixed sources	Variable	OR = 1.14 (0.92-1.41)	Age, gender	54
Zeng et al[62], 1993	1965-1986	Case-Control	1/264	18/2188	Hospital records	Hospital records	≥ 2.5	OR = 0.46 (0.06-3.45)		26
Kune et al[65], 1988	1980-1981	Case-Control	29/715	57/727	Hospital records	Self-reporting and hospital records		RR = 1.22 (0.7-2.0)		36
Friedman et al[63], 1987	1971-1984	Case-Control	43/1921	773/27687	Medicare database	Cancer registry	≥ 2	OR = 0.9 (0.6-1.2)	Age, gender, geographical area, calendar year	47
Weiss et al[53], 1982	1976-1977	Case-Control	49	687	Cancer registry	Self-reporting	≥ 1	RR = 1.0 (0.4-2.4)	Age	40
Shao et al[56], 2005	1987-2002	Cohort	83/55960	574668	National database	National database		IRR = 1.00 (0.85-1.17)	Age, gender	54
1Schernhammer et al[59], 2003	1982-1998	Cohort	32/6669	78515	National database of nurses	Self-report and National death registry	16	RR = 1.58 (1.05-2.36)	Age, smoking, BMI, lifestyle factors, comorbidities	57
2Johansen et al[64], 1996	1977-1989	Cohort	119/42098	NA	Hospital register	Cancer registry	1-16	RR = 1.07 (0.9-1.3)	Age, gender, calendar year	43
Linos et al[57], 1981	1950-1969	Cohort	17/168134/1681		Hospital database	Hospital records and self reporting		1RR = 0.5 (0.1-1.3)3RR = 2.3 (0.9-4.8)		34

¹Women only;

²Excluding rectal cancer;

³Men only. NA: Not available; BMI: Body mass index.