Spatio-temporal disparities of Clonorchis sinensis infection in animal hosts in China: a systematic review and meta-analysis

Liu, Kai; Tan, Jing; Xiao, Lu; Pan, Rui-Tai; Yao, Xiao-Yan; Shi, Fu-Yan; Li, Shi‐Zhu; Li, Lan‐Hua

doi:10.1186/s40249-023-01146-4

	All areas
	No. of data points	Sample size	No. of positive	Pooled prevalence, % (95% CI)	I², % (95% CI)	R², % (QM P value)	QE P value
All second intermediate hosts	927	1,62,568	36,050	14.2 (12.7–15.7)	98.6 (98.6–98.7)
Taxonomic class						35.5 (< 0.0001)	< 0.0001
Cyprinidae: Gobioninae
Pseudorasbora	144	46,390	20,358	48.5 (44.2–52.7)	99.1
Abbottina	40	5926	1800	28.7 (21.6–36.4)	99.0
Saurogobio	12	2396	430	38.9 (24.8–54.0)	98.0
Hemibarbus	3	195	14	4.7 (0.0–25.8)	81.0
Gnathopogon	1	109	9	8.3 (0.0–51.7)	Ne
Paraleucogobio	1	85	5	5.9 (0.0–47.7)	Ne
Mesogobio	1	119	9	7.6 (0.0–50.4)	Ne
Cyprinidae: Cyprininae
Carassius	92	15,014	1267	7.2 (4.6–10.4)	95.5
Cyprinus	55	4736	380	6.1 (2.9–10.2)	83.4
Cyprinidae: Leuciscinae
Ctenopharyngodon	70	12,718	3984	15.2 (10.9–20.1)	98.6
Squaliobarbus	2	859	97	9.1 (0.0–38.2)	44.4
Pseudaspius	1	145	108	74.5 (26.0–100.0)	Ne
Phoxinus	5	608	80	19.2 (4.2–40.8)	93.1
Leuciscus	1	27	4	14.8 (0.0–65.9)	Ne
Cyprinidae: Culterinae
Hemiculter	55	9576	1048	10.9 (6.9–15.7)	95.4
Parabramis	26	1255	143	5.2 (1.2–11.3)	89.4
Erythroculter	5	1200	139	16.7 (3.0–37.5)	92.8
Anabarilius	2	191	89	46.8 (14.5–80.7)	93.7
Pseudolaubuca	8	1502	153	11.8 (2.2–26.6)	81.9
Culter	4	217	87	18.8 (2.5–43.7)	94.5
Megalobrama	2	149	39	19.7 (0.5–54.0)	96.2
Pseudohemiculter	1	2342	396	16.9 (0.0–63.3)	Ne
Cyprinidae: Hypophthaemichthyinae
Aristichthys	41	4821	766	11.6 (6.6–17.5)	90.7
Hypophthalmichthys	31	1864	158	6.1 (2.0–11.9)	84.4
Cyprinidae: Acheilognathinae
Rhodeus	39	5381	880	14.7 (9.2–21.2)	97.9
Gobio	2	41	7	11.6 (0.0–46.9)	91.6
Cyprinidae: Labeoninae
Cirrhinus	29	2748	496	9.8 (4.6–16.6)	94.4
Sinilabeo	1	73	5	6.9 (0.0–49.9)	Ne
Ptychidio	1	72	3	4.2 (0.0–44.3)	Ne
Other fish in Cyprinidae
Xenocypris	3	898	41	2.4 (0.0–21.6)	0.0
Distoechodon	1	21	1	4.7 (0.0–51.5)	Ne
Opsariichthys	4	346	45	8.6 (0.0–28.4)	85.4
Zacco	1	732	130	17.8 (0.0–64.5)	Ne
Onychostoma	1	93	7	7.5 (0.0–50.7)	Ne
Puntius	1	152	5	3.3 (0.0–40.7)	Ne
Spinibarbus	1	82	3	3.7 (0.0–42.9)	0.0
Cypriniformes: Cobitidae
Misgurnus	20	3667	138	3.9 (0.3–10.0)	96.3
Schistura	1	153	44	28.8 (0.2–77.2)	Ne
Perciformes: Cichlidae
Oreochromis	20	2510	156	4.6 (0.7–11.1)	84.1
Cichla	2	119	4	4.7 (0.0–32.4)	80.2
Perciformes: Eleotridae
Perccottus	8	865	261	40.5 (23.4–58.9)	98.6
Micropercops	4	216	28	16.7 (1.6–40.9)	96.1
Bosttychus	4	150	7	5.3 (0.0–24.2)	75.0
Odontobutis	1	58	0	0.0 (0.0–29.4)	Ne
Other fish in Perciformes
Channa	9	459	23	4.7 (0.0–15.6)	80.9
Macropodus	4	187	38	12.4 (0.4–34.8)	88.7
Lateolabrax	5	219	3	0.7 (0.0–12.0)	0.0
Siniperca	4	298	25	13.8 (0.6–36.8)	97.1
Epinephelus	3	146	5	2.2 (0.0–20.5)	35.7
Rhinogobius	8	1045	59	5.6 (0.0–17.7)	82.6
Pampus	2	61	5	7.3 (0.0–38.4)	0.0
Mastacembelus	1	33	33	100.0 (67.7–100.0)	Ne
Caranx	1	31	1	3.2 (0.0–45.4)	Ne
Helostoma	1	26	3	11.5 (0.0–61.6)	Ne
Other fish except Perciformes and Cypriniformes
Pelteobagrus	16	993	37	3.0 (0.0–9.9)	88.4
Silurus	11	411	17	2.8 (0.0–11.5)	58.8
Clarias	1	29	1	3.5 (0.0–46.4)	Ne
Monopterus	10	1767	32	2.0 (0.0–9.8)	90.2
Salmo	4	162	5	1.3 (0.0–15.4)	72.5
Brachymystax	1	791	86	10.9 (0.0–54.9)	Ne
Salanx	1	48	0	0.0 (0.0–30.4)	Ne
Oryzias	3	95	8	7.0 (0.0–31.1)	30.2
Gambusia	2	142	4	2.9 (0.0–26.8)	0.0
Sebastiscus	1	39	5	12.8 (0.0–61.6)	Ne
Sardinella	1	44	0	0.0 (0.0–30.7)	Ne
Unspecified fish	53	15,501	1728	6.8 (3.5–10.8)	98.6
Shellfish	38	9220	108	0.7 (0.0–3.3)	88.1
Period of investigating						1.8 (0.0002)	< 0.0001
Before 1990	224	47,688	14,544	18.2 (14.9–21.6)	99.1
1990–1999	114	19,024	4982	19.0 (14.5–24.0)	98.7
2000–2009	337	56,251	10,831	13.2 (10.9–15.7)	98.2
After 2010	252	39,605	5693	10.2 (7.8–12.8)	97.8
Season of investigating						2.3 (< 0.0001)	< 0.0001
Spring	65	14,199	4775	29.2 (22.4–36.6)	98.9
Summer	93	11,611	2029	13.9 (9.5–18.9)	98.0
Autumn	115	14,358	3815	10.5 (7.0–14.6)	98.4
Winter	13	1076	248	7.6 (0.6–20.0)	98.9
Unspecified	641	1,21,324	25,183	13.7 (12.0–15.5)	98.7
Detecting method						0.0 (0.6348)	< 0.0001
Direct compression	447	74,958	16,766	14.2 (12.1–16.5)	98.7
Artificial digestion	237	34,458	6938	13.0 (10.3–16.0)	97.9
Unspecified	243	53,152	12,346	15.1 (12.2–18.2)	99.0
Pseudorasbora spp.	144	46,390	20,358	48.5 (42.8–54.3)	99.1 (99.0–99.1)
Period of investigating						6.9 (0.0046)	< 0.0001
Before 1990	52	22,357	11,905	58.2 (49.0–67.2)	98.6
1990–1999	23	5226	2474	55.6 (41.6–69.2)	98.5
2000–2009	36	7360	2882	44.8 (33.8–56.0)	98.9
After 2010	33	11,447	3097	32.7 (22.3–44.0)	99.2
Season of investigating						3.6 (0.0562)	< 0.0001
Spring	12	1671	825	68.2 (48.7–85.0)	99.6
Summer	19	3275	1280	38.7 (24.2–54.4)	98.5
Autumn	20	5699	2941	46.6 (31.8–61.8)	98.8
Winter	2	322	244	89.2 (47.0–1.0)	98.8
Unspecified	91	35,423	15,068	47.3 (40.3–54.5)	99.1
Detecting method						0.7 (0.2261)	< 0.0001
Direct compression	80	25,865	10,476	46.0 (38.3–53.7)	99.3
Artificial digestion	20	3291	1540	42.3 (27.3–58.0)	96.9
Unspecified	44	17,234	8342	55.9 (45.5–66.1)	98.6

	Areas with population infection rate ≥ 1.0%
	No. of data points	Sample size	No. of positive	Pooled prevalence, % (95% CI)	I², % (95% CI)	R², % (QM P value)	QE P value
All second intermediate hosts	425	69,593	13,703	13.3 (11.4–15.3)	97.8 (97.7–97.9)
Taxonomic class						29.9 (< 0.0001)	< 0.0001
Cyprinidae: Gobioninae
Pseudorasbora	43	8304	3668	47.3 (40.1–54.7)	97.8
Abbottina	3	301	112	28.8 (8.2–55.6)	97.1
Saurogobio	9	2126	334	35.2 (20.6–51.4)	98.2
Hemibarbus	3	195	14	4.7 (0.0–23.9)	81.0
Gnathopogon	1	109	9	8.3 (0.0–48.1)	Ne
Paraleucogobio
Mesogobio
Cyprinidae: Cyprininae
Carassius	37	5819	688	8.0 (4.1–12.9)	95.8
Cyprinus	30	3510	299	8.1 (3.6–13.8)	80.8
Cyprinidae: Leuciscinae
Ctenopharyngodon	50	10,476	3572	18.6 (13.5–24.3)	98.7
Squaliobarbus	2	859	97	9.1 (0.0–35.7)	44.4
Pseudaspius	1	145	108	74.5 (29.3–99.9)	Ne
Phoxinus	2	484	67	33.0 (6.8–66.6)	97.5
Leuciscus
Cyprinidae: Culterinae
Hemiculter	19	2468	502	16.5 (9.1–25.5)	96.1
Parabramis	17	738	115	6.7 (1.5–14.4)	91.7
Erythroculter	2	1095	122	20.7 (1.6–52.1)	95.5
Anabarilius
Pseudolaubuca	4	1291	139	19.8 (4.1–42.5)	86.7
Culter	1	37	11	29.7 (0.1–77.5)	Ne
Megalobrama	1	57	3	5.3 (0.0–43.8)	Ne
Pseudohemiculter	1	2342	396	16.9 (0.0–59.7)	Ne
Aristichthys	32	4241	670	10.4 (5.5–16.4)	92.3
Hypophthalmichthys	15	1101	109	8.0 (2.0–16.7)	83.3
Cyprinidae: Acheilognathinae
Rhodeus	13	1640	600	26.9 (15.9–39.6)	97.9
Gobio	1	21	0	0 (0–32.29)	Ne
Cyprinidae: Labeoninae
Cirrhinus	26	2578	487	10.6 (5.3–17.4)	94.7
Sinilabeo	1	73	5	6.9 (0.0–46.3)	Ne
Ptychidio	1	72	3	4.2 (0.0–40.7)	Ne
Other fish in Cyprinidae
Xenocypris	2	873	41	4.5 (0.0–29.1)	0.0
Distoechodon
Opsariichthys	1	51	3	5.9 (0.0–45.4)	Ne
Zacco	1	732	130	17.8 (0.0–61.0)	Ne
Onychostoma	1	93	7	7.5 (0.0–47.1)	Ne
Puntius
Spinibarbus	1	82	3	3.7 (0.0–39.2)	Ne
Cypriniformes: Cobitidae
Misgurnus	8	1102	42	1.5 (0.0–9.1)	68.9
Schistura	1	153	44	28.8 (0.7–73.9)	Ne
Perciformes: Cichlidae
Oreochromis	17	2367	151	5.1 (0.9–11.8)	86.1
Cichla
Perciformes: Eleotridae
Perccottus	6	738	167	30.2 (14.1–49.3)	98.6
Micropercops
Bosttychus	1	23	2	8.7 (0–54.5)	Ne
Odontobutis	1	58	0	0.0 (0.0–26.2)	Ne
Other fish in Perciformes
Channa	5	339	19	7.4 (0.0–23.0)	89.4
Macropodus	1	75	27	36.0 (2.4–81.3)	Ne
Lateolabrax	3	168	3	1.6 (0.0–17.2)	44.0
Siniperca	4	298	25	13.6 (1.0–34.8)	97.1
Epinephelus
Rhinogobius	1	619	31	5.0 (0.0–40.3)	Ne
Pampus	1	25	1	4.0 (0.0–45.0)	Ne
Mastacembelus
Caranx
Helostoma
Pelteobagrus	5	598	6	0.7 (0.0–10.0)	59.2
Silurus	7	301	7	1.2 (0.0–9.8)	30.8
Clarias	1	29	1	3.5 (0.0–42.8)	Ne
Monopterus	4	461	32	9.9 (0.3–28.6)	84.6
Salmo	2	99	5	3.8 (0.0–27.5)	89.2
Brachymystax	1	791	86	10.9 (0.0–51.2)	Ne
Salanx	1	48	0	0.0 (0.0–27.0)	Ne
Oryzias
Gambusia
Sebastiscus
Sardinella	1	44	0	0.0 (0.0–27.4)	Ne
Unspecified fish	25	7636	710	3.4 (0.6–7.9)	97.0
Shellfish	8	1708	30	1.7 (0.0–9.2)	92.4
Period of investigating						0.0 (0.6575)	< 0.0001
Before 1990	95	10,354	2169	15.3 (11.2–19.9)	97.7
1990–1999	32	6976	1642	12.8 (6.7–20.4)	98.9
2000–2009	178	35,725	6539	13.3 (10.5–16.5)	97.7
After 2010	120	16,538	3353	11.9 (8.6–15.5)	97.6
Season of investigating						4.7 (< 0.0001)	< 0.0001
Spring	39	9732	3379	26.6 (19.1–34.9)	98.7
Summer	37	4246	426	7.4 (3.1–13.1)	97.1
Autumn	42	5657	1144	8.0 (3.7–13.6)	97.9
Winter	3	164	1	0.1 (0.0–16.0)	0.0
Unspecified	304	49,794	8753	13.6 (11.4–15.9)	97.3
Detecting method						0.1 (0.2996)	< 0.0001
Direct compression	167	30,699	5597	14.3 (11.2–17.6)	98.1
Artificial digestion	181	28,403	6017	11.7 (9.1–14.6)	97.7
Unspecified	77	10,491	2089	15.3 (10.7–20.4)	97.5
Pseudorasbora spp.	43	8304	3668	47.3 (37.7–57.1)	97.8 (97.4; 98.1)
Period of investigating						0.0 (0.8666)	< 0.0001
Before 1990	18	2694	1097	44.8 (29.7–60.3)	97.1
1990–1999	4	605	204	38.3 (11.1–70.1)	97.7
2000–2009	10	1730	684	50.1 (29.8–70.5)	98.8
After 2010	11	3275	1683	52.4 (32.9–71.5)	96.3
Season of investigating						2.4 (0.2716)	< 0.0001
Spring	5	228	164	68.2 (39.5–91.2)	96.3
Summer	7	729	236	31.1 (11.7–54.7)	95.3
Autumn	5	1265	758	47.0 (20.5–74.5)	96.6
Winter
Unspecified	26	6082	2510	47.9 (35.8–60.2)	98.0
Detecting method				0.0 (0.0–0.0)	0.0	6.5 (0.0795)	< 0.0001
Direct compression	21	4469	1926	51.3 (38.0–64.6)	98.3
Artificial digestion	13	2748	1238	32.0 (17.1–48.9)	97.4
Unspecified	9	1087	504	60.6 (39.8–79.7)	96.2

	Areas with population infection rate < 1.0%
	No. of data points	Sample size	No. of positive	Pooled prevalence, % (95% CI)	I², % (95% CI)	R², % (QM P value)	QE P value
All second intermediate hosts	502	92,975	22,347	14.9 (12.7–17.2)	99.0 (98.9–99.0)
Taxonomic class						39.3 (< 0.0001)	< 0.0001
Cyprinidae: Gobioninae
Pseudorasbora	101	38,086	16,690	49.0 (43.7–54.3)	99.3
Abbottina	37	5625	1688	28.7 (20.9–37.1)	99.1
Saurogobio	3	270	96	49.8 (20.1–79.6)	96.1
Hemibarbus
Gnathopogon
Paraleucogobio	1	85	5	5.9 (0.0–50.2)	Ne
Mesogobio	1	119	9	7.7 (0.0–52.9)	Ne
Cyprinidae: Cyprininae
Carassius	55	9195	579	6.8 (3.4–11.1)	94.7
Cyprinus	25	1226	81	3.9 (0.4–9.8)	84.7
Cyprinidae: Leuciscinae
Ctenopharyngodon	20	2242	412	7.8 (2.2–15.9)	97.3
Squaliobarbus
Pseudaspius
Phoxinus	3	124	13	11.1 (0.0–38.4)	87.4
Leuciscus	1	27	4	14.8 (0.0–68.3)	Ne
Cyprinidae: Culterinae
Hemiculter	36	7108	546	8.4 (3.9–14.1)	92.7
Parabramis	9	517	28	3.0 (0.0–13.1)	57.8
Erythroculter	3	105	17	14.1 (0.0–42.8)	93.9
Anabarilius	2	191	89	46.8 (13.3–82.1)	93.7
Pseudolaubuca	4	211	14	5.6 (0.0–25.1)	73.3
Culter	3	180	76	15.3 (0.0–44.9)	96.3
Megalobrama	1	92	36	39.1 (1.6–87.9)	Ne
Pseudohemiculter
Aristichthys	9	580	96	16.3 (4.7–32.3)	64.4
Hypophthalmichthys	16	763	49	4.6 (0.2–12.7)	84.4
Cyprinidae: Acheilognathinae
Rhodeus	26	3741	280	9.8 (4.2–17.2)	94.7
Gobio	1	20	7	35.0 (0.0–89.0)	Ne
Cyprinidae: Labeoninae
Cirrhinus	3	170	9	4.2 (0.0–25.7)	51.9
Sinilabeo
Ptychidio
Other fish in Cyprinidae
Xenocypris	1	25	0	0.0 (0.0–36.6)	Ne
Distoechodon	1	21	1	4.8 (0.0–54.0)	Ne
Opsariichthys	3	295	42	9.6 (0.0–35.0)	89.1
Zacco
Onychostoma
Puntius	1	152	5	3.3 (0.0–43.3)	Ne
Spinibarbus
Cypriniformes: Cobitidae
Misgurnus	12	2565	96	6.0 (0.4–16.1)	97.6
Schistura
Perciformes: Cichlidae
Oreochromis	3	143	5	2.2 (0.0–21.6)	33.8
Cichla	2	119	4	4.8 (0.0–34.1)	80.2
Perciformes: Eleotridae
Perccottus	2	127	94	73.4 (35.1–98.4)	0.0
Micropercops	4	216	28	16.7 (1.2–42.2)	96.1
Bosttychus	3	127	5	4.4 (0.0–27.3)	80.2
Odontobutis
Other fish in Perciformes
Channa	4	120	4	1.8 (0.0–18.6)	26.8
Macropodus	3	112	11	6.3 (0.0–30.8)	69.0
Lateolabrax	2	51	0	0.0 (0.0–21.2)	0.0
Siniperca
Epinephelus	3	146	5	2.2 (0.0–21.7)	35.7
Rhinogobius	7	426	28	5.8 (0.0–19.9)	85.1
Pampus	1	36	4	11.1 (0.0–61.9)	Ne
Mastacembelus	1	33	33	100.0 (65.3–100.0)	Ne
Caranx	1	31	1	3.2 (0.0–47.9)	Ne
Helostoma	1	26	3	11.5 (0.0–64.1)	Ne
Pelteobagrus	11	395	31	4.7 (0.0–15.1)	90.4
Silurus	4	110	10	7.3 (0.0–29.3)	66.8
Clarias
Monopterus	6	1306	0	0.0 (0.0–6.7)	0.0
Salmo	2	63	0	0.0 (0.0–20.3)	0.0
Brachymystax
Salanx
Oryzias	3	95	8	7.0 (0.0–32.4)	30.2
Gambusia	2	142	4	2.9 (0.0–28.4)	0.0
Sebastiscus	1	39	5	12.8 (0.0–64.0)	Ne
Sardinella
Unspecified fish	28	7865	1018	10.5 (5.0–17.5)	99.1
Shellfish	30	7512	78	0.5 (0.0–3.5)	86.6
Period of investigating						3.5 (0.0002)	< 0.0001
Before 1990	129	37,334	12,375	20.3 (15.6–25.3)	99.4
1990–1999	82	12,048	3340	21.7 (15.8–28.2)	98.6
2000–2009	159	20,526	4292	13.0 (9.5–17.0)	98.6
After 2010	132	23,067	2340	8.8 (5.6–12.6)	97.6
Season of investigating						1.8 (0.0103)	< 0.0001
Spring	26	4467	1396	33.2 (21.3–46.2)	99.2
Summer	56	7365	1603	19.2 (12.3–27.0)	98.1
Autumn	73	8701	2671	12.1 (7.2–17.9)	98.5
Winter	10	912	247	11.2 (1.0–28.6)	99.1
Unspecified	337	71,530	16,430	13.7 (11.2–16.5)	99.1
Detecting method						0.0 (0.5954)	< 0.0001
Direct compression	280	44,259	11,169	14.2 (11.4–17.3)	98.9
Artificial digestion	56	6055	921	18.0 (11.2–25.9)	98.0
Unspecified	166	42,661	10,257	15.0 (11.3–19.1)	99.2
Pseudorasbora spp.	101	38,086	16,690	49.0 (41.9–56.2)	99.3 (99.2–99.3)
Period of investigating						18.7 (< 0.0001)	< 0.0001
Before 1990	34	19,663	10,808	65.0 (54.2–75.2)	98.9
1990–1999	19	4621	2270	59.3 (44.4–73.4)	98.6
2000–2009	26	5630	2198	42.7 (30.4–55.5)	99.0
After 2010	22	8172	1414	23.9 (13.2–36.5)	99.0
Season of investigating						1.8 (0.2113)	< 0.0001
Spring	7	1443	661	68.3 (41.9–89.6)	99.7
Summer	12	2546	1044	43.3 (23.9–63.8)	99.0
Autumn	15	4434	2183	46.5 (28.9–64.7)	99.0
Winter	2	322	244	89.2 (44.8–100.0)	98.8
Unspecified	65	29,341	12,558	47.1 (38.4–56.0)	99.3
Detecting method						0.9 (0.2383)	< 0.0001
Direct compression	59	21,396	8550	44.1 (35.0–53.4)	99.4
Artificial digestion	7	543	302	62.5 (35.1–86.3)	95.4
Unspecified	35	16,147	7838	54.8 (42.7–66.5)	98.8

Table 2 Estimates of pooled prevalence and subgroup analysis of Clonorchis sinensis in second intermediate hosts

Infectious Diseases of Poverty

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