Urea breath test for Helicobacter pylori infection in adult dyspeptic patients: A meta-analysis of diagnostic test accuracy

Table 1 Characteristics of the included studies that assessed the diagnostic test accuracy of the ¹³C-urea breath test

Ref.	Country	Design	Population, n	Prevalence (%)	Reference standard	Index test (model)	Optimal cut-off	Urea dosing (mg)	Time after administration (min)	Measurement tecnique	TP	FP	TN	FN
Wang et al[29], 2021	China	Cross-sectional	217	65.9	HE	13C-UBT	10.4‰ DOB	50	30	IS	120	14	60	23
Alzoubi et al[33], 2020	Jordan	Cross-sectional	30	56.7	RUT or HE	13C-UBT	4‰ DOB	75	30	IS	16	3	10	1
Nawacki et al[34], 2018	Poland	Cross-sectional	50	36.0	RUT	13C-UBT	9.5‰ DOB	NR	30	IS	16	0	32	2
Som et al[27], 2014	India	Cross-sectional	83	59.0	RUT	13C-UBT	1.47‰	75	Multiple times	ICOS	49	0	34	0
Bruden et al[35], 2011	United States	Cross-sectional	280	53.2	HE or (HpC and RUT)	13C-UBT	7 DOB	NR	NR	NR	139	16	115	10
Peng et al [36], 2009	Taiwan	Cross-sectional	100	53.0	HpC or (HE and RUT)	13C-UBT	4.8‰ DOB	100	15	IS	53	7	40	0
Jordaan et al[37], 2008	South Africa	Cross-sectional	103	58.3	HE	13C-UBT	4.5‰ DOB	75	NR	GCMS	55	3	40	5
Gatta et al[26], 2006	Italy	RCT	100	43.0	HE and RUT	13C-UBT	4.40‰-6.26‰ DOB	25	30	IRMS	43	0	57	0
Peng et al[38], 2005	Taiwan	Cross-sectional	50	36.0	HpC or (HE and RUT)	13C-UBT	5‰ DOB	100	15	IRMS	18	0	32	0
Kato et al[39], 2004	Japan	Cross-sectional	254	51.1	HpC or (HE and RUT)	13C-UBT	2.5‰ DOB	100	20	IRMS	252	5	242	6
Ohara et al[40], 2004	Japan	Cross-sectional	254	51.2	HpC or (HE and RUT)	13C-UBT	2.5‰ DOB	100	Multiple times	IRMS	127	2	122	3
Chen et al[41], 2003	Taiwan	Cross-sectional	554	66.6	HpC or (HE and RUT)	13C-UBT	3.5‰ DOB	100	20	IS	361	6	179	8
Valdepérez et al[42], 2003	Spain	Cross-sectional	85	76.8	HE and RUT	13C-UBT	NR	100	30	NR	61	0	19	2
Gatta et al[43], 2003	Italy	Cross-sectional	200	56.5	HpC or (HE and RUT)	13C-UBT	3.11‰-6.84‰ DOB	75	30	IRMS	113	0	87	0
Wong et al[44], 2003	China	Cross-sectional	200	49.5	HE and RUT	13C-UBT	2.1‰ DOB	50	20	IRMS	99	0	101	0
Ng et al[45], 2002	China	Cross-sectional	213	54.9	HE and RUT	13C-UBT	4.0‰-6.5‰ DOB	75	30	IRMS	112	2	94	5
Wong et al[46], 2001	China	Cross-sectional	101	48.1	HE and RUT	13C-UBT	7.0-8.0‰ DOB	50	20	IRMS	99	4	103	0
Wong et al[47], 2001	China	Cross-sectional	294	55.4	HE, HpC, CLO (RUT), in-house RUT, PCR, UBT (at least four positive)	13C-UBT	5‰ DOB	75	30	IRMS	151	4	127	12
Shirin et al[48], 2001	United States	Cross-sectional	97	47.4	HE and RUT	13C-UBT	Positive: > 6‰ DOB (> 2 points)/negative: < 3‰ DOB (> 2 points)	75	5	MCS	45	2	49	1
Pilotto et al[49], 2000	Italy	Cross-sectional	96	51.0	HE, HpC, and RUT	13C-UBT	5‰ DOB	100	30	IRMS	49	2	45	0
Sheu et al[50], 2000	Taiwan	Cross-sectional	177	47.5	HE or HpC	13C-UBT	3.5 DOB	50	15	IS	81	1	92	3
Wong et al[51], 2000	China	Cross-sectional	202	56.4	HE and RUT	13C-UBT	4.5‰ DOB	75	30	IRMS	108	2	86	6
Hahn et al[52], 2000	United States	Cross-sectional	67	6.0	HE and at least two positives of (definitive presence of H. pylori organisms in HE, UBT, Serology)	13C-UBT	2.4‰ DOB	125	30	IRMS	4	9	54	0
Chen et al[53], 2000	Japan	Cross-sectional	162	83.3	HE and Serology	13C-UBT	2.5‰ DOB	100	20	IRMS	135	1	26	0
Peng et al[54], 2000	Taiwan	Cross-sectional	136	59.6	HpC or (HE and RUT)	13C-UBT	4.8‰ DOB	100	15	IRMS	76	6	49	5
Riepl et al[55], 2000	Germany	Cross-sectional	84	35.7	HE, HpC, and RUT	13C-UBT	6.5‰ DOB	75	15	IS	30	0	54	0
D'Elios et al[56], 2000	Italy	Cross-sectional	256	45.3	HE	13C-UBT	4‰ DOB	75	30	IRMS	113	2	138	3
van der Hulst et al[57], 1999	Italy	Cross-sectional	544	52.2	HE or HpC	13C-UBT	7.5‰ DOB ± 0.8	100	30	LOGES	260	21	239	24
Leodolter et al[58], 1999	Germany	Cross-sectional	320	48.1	HpC or (HE and RUT)	13C-UBT	4‰ DOB	75	30	IRMS	142	2	164	12
Mock et al[59], 1999	Canada	Cross-sectional	98	19.8	HE or (RUT and Serology)	13C-UBT	3‰ DOB	75	30	IRMS	17	2	75	2
Mock et al[59], 1999	Korea	Cross-sectional	107	68.2	HE or (RUT and Serology)	13C-UBT	3‰ DOB	75	30	IRMS	69	1	33	4
Perri et al[60], 1998	Belgium	Cross-sectional	172	73.3	HE or HpC	13C-UBT	1.15‰ DOB	75	60	IRMS	121	1	45	5
Ohara et al[61], 1998	Japan	Cross-sectional	213	77.5	HpC or at least two positives of (HE, RUT, Serology)	13C-UBT	2.5‰ DOB	100	20	IRMS	162	1	47	3
Leodolter et al[62], 1998	Germany	Cross-sectional	40	50.0	HpC or (HE and RUT)	13C-UBT	4‰ DOB	75	10	IRMS	20	0	20	0
Andersen et al[63], 1998	Denmark	Cross-sectional	97	54.6	HE or HpC	13C-UBT	5‰ DOB	100	Multiple times	IRMS	46	4	40	7
Ellenrieder et al[64], 1997	Germany	Cross-sectional	132	43.2	(HE, HpC, RUT) at least two positives	13C-UBT	3.5‰ DOB	NR	30	IS	52	8	67	5
Epple et al[65], 1997	Germany	Cross-sectional	126	61.1	HE	13C-UBT	1.3‰ DOB	75	30	IRMS	74	7	42	3
Labenz et al[66], 1996	Germany	Cross-sectional	70	67.1	HE or HpC	13C-UBT	4‰ DOB	75	30	IRMS	46	0	23	1
Logan et al[67], 1991	England	Cross-sectional	56	68.0	HE	13C-UBT	4.5‰ DOB	125	Multiple times	IRMS	32	1	15	2
Dill et al[68], 1990	Scotland	Cross-sectional	69	49.3	HpC	13C-UBT	3‰ c-PDR	250	20	IRMS	33	0	35	1

CLO: Campylobacter-like organism; GCMS: Gas chromatography-mass spectrometry; HE: Histopathological examination; HpC: Helicobacter pylori culture; ICOS: Integrated Cavity Output Spectrometry; IRMS: Isotope ratio mass spectrometry; IS: Infrared spectrometry; LOGES: Laser opto-galvanic Effect Spectroscopy; MCS: Molecular correlation spectrometry; NR: Not reported; RUT: Rapid urease test; UBT: Urea breath test; DOB: Delta over baseline; RCT: Randomized clinical trial.

Table 2 Characteristics of the included studies that assessed the diagnostic test accuracy of the ¹⁴C-urea breath test

Ref.	Country	Design	Population, n	Prevalence (%)	Reference standard	Index test (model)	Optimal cut-off	Urea dosing (μCi)	Time after administration (min)	Measurement tecnique	TP	TN	FP	FN
Han et al[30], 2023	China	Cross-sectional	205	42.4	HE and RUT	14C-UBT	100 dpm	0.75	20	SC	83	3	115	4
Wang et al[29], 2021	China	Cross-sectional	267	71.9	HE	14C-UBT	238 dpm	0.75	25	NR	158	12	63	34
Miftahussurur[69], 2021	Indonesia	Cross-sectional	55	23.6	HE	14C-UBT	57 cpm	1	10	HA	12	1	41	1
Cosgun et al[70], 2016	Turkey	Cross-sectional	126	92.1	HpC or HE	14C-UBT	NR	1	10	HA	112	7	3	4
Atli et al[71], 2012	Turkey	Cross-sectional	100	35.0	HE	14C-UBT	Positive: > 50 cpm/suspicious: 25-50 cpm /negative: < 25 dpm	1	10	HA	32	4	61	3
Alarcón-Rivera et al[72], 2011	Mexico	Cross-sectional	84	70.2	HE	14C-UBT	Positive: > 50 ppm/indeterminate: 25-50 ppm/negative: < 25 ppm	1	10-15	HA	56	1	24	3
Mansour-Ghanaei et al[73], 2011	Iran	Cross-sectional	125	56.8	HE, RUT, Serology (at least two positive)	14C-UBT	50 cpm	1	15	HA	67	0	54	4
Ozdemir et al[74], 2008	Turkey	Cross-sectional	89	66.3	HE, RUT, PCR (at least two positive)	14C-UBT	Positive: > 50 cpm/equivocal: 25-50 cpm; negative: < 25 dpm	1	10	HA	57	0	30	2
Rasool et al[75], 2007	Pakistan	Cross-sectional	94	64.9	RUT	14C-UBT	50 cpm	1	10	β-SC	60	3	30	1
Gurbuz et al[76], 2005	Turkey	Cross-sectional	65	44.6	HE	14C-UBT	Positive: > 50 cpm/suspicious: 25-50 cpm /negative: < 25 dpm	1	10	HA	26	8	28	3
Gatta et al[31], 2003	Italy	Cross-sectional	117	65.0	HpC or (HE and RUT)	14C-UBT	130-136 dpm (dpm at sample-dpm at T0)	1	12.5	LSC	73	2	39	3
González et al[77], 2003	Chile	Cross-sectional	NR	71.9	Two or more positives	14C-UBT	200 dpm	1	10	LSC	61	14	11	3
Oztürk et al[78], 2009	Turkey	Cross-sectional	75	65.8	HE	14C-UBT	100 dpm	1	10	LSC	48	5	20	0
Gomes et al[79], 2002	Brazil	Cross-sectional	137	83.9	HE and RUT	14C-UBT	1000 cpm	5	15	LSC	114	1	21	1
Desroches et al[80], 1997	Canada	Cross-sectional	56	80.4	HE or HpC	14C-UBT	0.33‰ AS (14CO2 specific activity)	5	20	LSC	44	0	11	1
Allardyce et al[81], 1997	New Zealand	Cross-sectional	63	34.9	HE and RUT	14C-UBT	49 dpm	1	30	β-SC	22	2	39	0
Faigel et al[82], 1996	United States	Cross-sectional	50	42.6	HE or RUT	14C-UBT	Positive: > 200 dpm in any sample/borderline: 100-200 dpm (as the peak count)/negative: < 100 dpm (in all samples)	1	Multiple times	LSC	18	1	26	2
Goh et al[83], 1995	Malaysia	Cross-sectional	63	50.8	HpC or [HE and (RUT or Gram staining)]	14C-UBT	1275 dpm	5	15	LSC	32	0	31	0
Kao et al[84], 1993	China	Cross-sectional	184	53.8	HpC or RUT	14C-UBT	150‰	5	10	LSC	99	14	71	0
Vivas et al[85], 1993	Venezuela	Cross-sectional	15	53.3	HE	14C-UBT	100 dpm	1	20	β-SC	8	1	6	0
Novis et al[28], 1991	Israel	Cross-sectional	64	80.3	HE	14C-UBT	4,7‰	10	Multiple times	LSC	59	3	12	2

CLO: Campylobacter-like organism; HA: Heliprobe Analyser; HE: histopathological examination; HpC: Helicobacter pylori culture; LSC: Liquid scintillation counting; NR: Not reported; RUT: Rapid urease test; SC: Solid scintillation counting; UBT: Urea breath test; β-SC: Beta-scintillation counting.