Anisakis infection in marine fishes and resident awareness of anisakiasis in Qingdao in 2021

doi:10.12140/j.issn.1000-7423.2023.01.008

Abstract

Abstract:

Objective To investigate the Anisakis infection in marine fishes in the Yellow Sea and local resident awareness of anisakiasis in Qingdao. Methods In October 2021, marine fishes were purchased from Fisherman’s Wharf in Qingdao and Taixi Wharf in Langya. The viscera and muscle of the marine fishes were disected to search for Anisakis larvae. The Anisakis infection in different fish species, and different organs were examined to anlyze the correlation between the infection intensity and body length and weight of the marine fishes. Five villages were randomly selected in the West Coast New District to conduct a questionnaire survey on anisakiasis knowledge among residents who were willing to participate in the survey. The knowledge awareness rate and behavior habits of the residents on Anisakis were analyzed. Surveillance for anisakiasis was conducted in local sentinel hospital. The Fisher exact test was used to compare the infection rate and the responders proportion; Spearman rank correlation analysis was performed; Chi-square test was used for analyzing the knowledge awareness rate. Results A total of 196 fish from 22 species were collected, of which 70 were infected with Anisakis. The infection rate was 35.7% (70/196). Total 13 species of marine fishes were found infected with Anisakis, accounting for 59.1% (13/22), among which Muraenesox cinereus, Pleuronichthys cornutus, Gadous macrocephaius, Scomber japonicas (all 10/10) and Nibea albiflora (9/9) were all infected with Anisakis larvae. The infection rate of Anisakis was significantly different between different species (χ² = 147.93, P < 0.01). The average infection intensity was 34.8 larvae/fish (2 439/70). The highest infection intensity was found in Gadous macrocephaius (189.3 larvae/fish), followed by Scomberomorus niphonius (25.7 larvae/fish). In Larimichthys polyactis and Pennahia argentata, Anisakis larvae were only found in mesentery and intestinal wall, accounting for 4/4 and 5/5, respectively. In Esox reicherti and Sebastiscus marmoratus, Anisakis larvae were only found in the body cavity, accounting for 13/13 and 2/2, respectively. Rank correlation analysis show that the infection intensities of Anisakis in L. polyactis and E. reicherti were positively correlated with body length (r = 0.71, 0.81, all P < 0.05) and body weight (r = 0.64, 0.80, all P < 0.05), while the infection intensity of Anisakis in Lophiomus litulon was negatively correlated with body weight (r = -0.98, P < 0.01). The infection intensity of other infected fishes was not correlated with body length and body weight. A total of 387 local residents were surveyed, 8.5% (33/387) of which had heard of anisakiasis, 4.9% (19/387) had knowledge on the harm of anisakiasis, and 7.0% (27/387) preferred to eat raw or semi-raw marine fishes, 17.8% (69/387) of residents processed raw and cooked food with shared cutting boards. The knowledge awareness rates of male and female were 11.2% (18/160) and 6.6% (15/227), respectively (χ² = 7.69, P < 0.05). The knowledge awareness rate of residents in Zhuangjiatong Village [36.7% (26/71)] was higher than that of other villages (χ² = 81.15, P < 0.01). The knowledge awareness rate in ≥ 60 years old residents was the highest, which was 11.8% (16/136), but there was no significant difference among age groups (χ² = 10.89, P > 0.05). Sentinel hospitals monitor did not find any patient infected with Anisakis. Conclusion The infection rate of Anisakis in marine fishes in Qingdao is comparatively high. The knowledge awareness rate on preventrion and control of anisakiasis in resident is low. The locals comsume raw or semi-cooked marine fishes, and process raw and cooked food with shared cutting boards.

Key words: Anisakis, Marine fishes, Infection, Questionnaire investigation

CLC Number:

R383.19

LI Dan, JI Fengying, WANG Longjiang, WANG Yongbin, LI Yuejin, YAN Ge, XU Yan, BU Xiuqin, ZHANG Benguang. Anisakis infection in marine fishes and resident awareness of anisakiasis in Qingdao in 2021[J]. CHINESE JOURNAL OF PARASITOLOGY AND PARASITIC DISEASES, 2023, 41(1): 52-58.

Figures/Tables 5

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References 20

[1]	?opieńska-Biernat E, Stryiński R, Dmitryjuk M, et al. Infective larvae of Anisakis simplex (Nematoda) accumulate trehalose and glycogen in response to starvation and temperature stress[J]. Biol Open, 2019, 8(3): bio040014.
[2]	Adroher-Auroux FJ, Benítez-Rodríguez R. Anisakiasis and Anisakis: an underdiagnosed emerging disease and its main etiological agents[J]. Res Vet Sci, 2020, 132: 535-545.
[3]	Zhang HM, Ye B, Lin SX, et al. Research of Anisakis infection in marine fish and awareness rate of Anisakis knowledge in Laoshan district of Qingdao[J]. Chin Prim Health Care, 2020, 34(10): 81-82. (in Chinese)
	(张洪梅, 叶兵, 林思夏, 等. 青岛市崂山区部分海鱼异尖线虫感染状况及居民知晓率调查[J]. 中国初级卫生保健, 2020, 34(10): 81-82.)
[4]	Zhang WQ, Ren XT, Zhao YQ, et al. Investigation of Anisakis spp. larva infection in marine fish for sale in Yantai City[J]. Chin J Parasitol Parasit Dis, 2017, 35(5): 472-477. (in Chinese)
	(张雯倩, 任晓彤, 赵玉绮, 等. 烟台市市售海鱼异尖线虫幼虫感染现况调查[J]. 中国寄生虫学与寄生虫病杂志, 2017, 35(5): 472-477.)
[5]	Gong CB, Wang ZX, Dong FG, et al. Investigationon infection of Anisakis sp. 3rd stage larvae in fresh marine fish for sale in Yantai from 2016 to 2017[J]. Mod Prev Med, 2018, 45(10): 1766-1768. (in Chinese)
	(宫春波, 王朝霞, 董峰光, 等. 2016—2017年烟台市售140份鲜活海鱼异尖线虫Ⅲ期幼虫感染状况[J]. 现代预防医学, 2018, 45(10): 1766-1768.)
[6]	Qin YH, Zhao YF, Ren YX, et al. Anisakiasis in China: the first clinical case report[J]. Foodborne Pathog Dis, 2013, 10(5): 472-474.
[7]	Administration of Quality Supervision, Inspection and Quarantine. Protocol of diagnosis for anisakiasis: SN/T 1509—2005[S]. Beijing: Administration of Quality Supervision, Inspection and Quarantine, 2005. (in Chinese)
	(中华人民共和国国家质量监督检验检疫总局. 异尖线虫病诊断规程: SN/T 1509—2005[S]. 北京: 中华人民共和国国家质量监督检验检疫总局, 2005.)
[8]	Li D, Yue LM. Research progress of human infection with anisakiasis[J]. J Pathog Biol, 2021, 16(9): 1107-1112. (in Chinese)
	(李丹, 岳林明. 人异尖线虫病的研究进展[J]. 中国病原生物学杂志, 2021, 16(9): 1107-1112.)
[9]	Zhou JY, Lin Q, Zhang H, et al. Investigation and molecular identification of Anisakis infection in marine fish in Zhoushan fishing ground[J]. Prev Med, 2017, 29(7): 694-697, 701. (in Chinese)
	(周晶耀, 林启, 张辉, 等. 舟山渔场海洋鱼类异尖线虫感染调查及分子鉴定[J]. 预防医学, 2017, 29(7): 694-697, 701.)
[10]	Tang ZL, Huang Y, Yu XB. Current status and perspectives of Clonorchis sinensis and clonorchiasis: epidemiology, pathogenesis, omics, prevention and control[J]. Infect Dis Poverty, 2016, 5: 71.
[11]	Wang ZY, Wu HY, Jiang L, et al. Surveillance and analysis of parasitic infection in food on market in Shanghai during 2015—2019[J]. Chin J Parasitol Parasit Dis, 2021, 39(3): 347-351. (in Chinese)
	(王真瑜, 吴寰宇, 江莉, 等. 2015—2019年上海市市售食品寄生虫感染监测分析[J]. 中国寄生虫学与寄生虫病杂志, 2021, 39(3): 347-351.)
[12]	Xu Y, Zeng QY, Sun ZH, et al. Preliminary investigation of Anisakis infection in commercial marine fish in Lianyungang City[J]. Chin J Vet Sci, 2018, 38(12): 2343-2347. (in Chinese)
	(徐杨, 曾巧英, 孙志华, 等. 连云港市售海鱼异尖线虫感染情况的初步调查[J]. 中国兽医学报, 2018, 38(12): 2343-2347.)
[13]	Tang YZ, Sun QS, Peng P, et al. Research advances of anisakiasis in China[J]. J Anhui Agric Sci, 2012, 40(24): 12079-12081. (in Chinese)
	(唐艺芝, 孙青松, 彭鹏, 等. 我国异尖线虫病研究进展[J]. 安徽农业科学, 2012, 40(24): 12079-12081.)
[14]	Miu F, Zhang BG, Liu X, et al. Infection status of Anisakis in aquatic product in the Yellow Sea waters of Shandong[J]. Parasitoses Infect Dis, 2014, 12(4): 189-190. (in Chinese)
	(缪峰, 张本光, 刘新, 等. 山东黄海海域水产品异尖线虫感染情况调查[J]. 寄生虫病与感染性疾病, 2014, 12(4): 189-190.)
[15]	Du XT, Zhou QY. The third-stage larvae of Anisakis infection in partial marine fish in Dandong[J]. Chin Trop Med, 2019, 19(1): 40-42. (in Chinese)
	(杜学婷, 周秋颖. 丹东市部分海鱼异尖线虫第Ⅲ期幼虫感染情况[J]. 中国热带医学, 2019, 19(1): 40-42.)
[16]	Ye B, Sun ZQ, Song XY, et al. Research of Anisakis infecting in marine fish in Shandong Qingdao[J]. J Med Pest Control, 2017, 33(9): 985-986. (in Chinese)
	(叶兵, 孙忠清, 宋旭岩, 等. 山东青岛市市售海鱼异尖线虫幼虫感染调查[J]. 医学动物防制, 2017, 33(9): 985-986.)
[17]	Wei ZC, Zhang W, Deng XL. Investigation of Anisakis larvae infection in marine fish in markets of Anshan City, Liaoning Province[J]. Chin J Parasitol Parasit Dis, 2020, 38(6): 789-791. (in Chinese)
	(魏卓超, 张巍, 邓晓丽. 辽宁省鞍山市市售海鱼异尖线虫幼虫感染情况调查[J]. 中国寄生虫学与寄生虫病杂志, 2020, 38(6): 789-791.)
[18]	Zhang XY, Yu M, Zhao QQ, et al. Investigation of Anisakis infections in market-available marine fish in Dongtai City[J]. Chin J Schisto Control, 2020, 32(4): 426-427, 440. (in Chinese)
	(张学艳, 俞敏, 赵青青, 等. 东台市市售海鱼中异尖线虫感染调查[J]. 中国血吸虫病防治杂志, 2020, 32(4): 426-427, 440.)
[19]	Ma HW, Jiang TJ, Quan FS, et al. Investigation for infection status of Anisakis larvae in marine fish and cephalopods from the Bohai Sea, China[J]. J Med Sciecnce Yanbian Univ, 2001, 24(2): 105-114. (in Chinese)
	(马宏伟, 姜泰京, 全福实, 等. 渤海鱼类和头足类异尖科线虫幼虫感染情况调查[J]. 延边大学医学学报, 2001, 24(2): 105-114.)
[20]	Zhang JH, Lin Q, Xu X, et al. Survey of infection of Anisakis(L3) in marine fishes caught in the sea around Zhoushan, Zhejiang Province[J]. Dis Surveillance, 2010, 25(6): 469-473. (in Chinese)
	(张均和, 林启, 徐徐, 等. 浙江省舟山渔场鱼类异尖线虫感染现况调查[J]. 疾病监测, 2010, 25(6): 469-473.)

海产种类 Marine species	检查数 No. exam’d	感染数 No. infected	感染率/% Infection rate/%	检获虫数 No. Anisakis found	平均感染度/条·尾^-1 Average infection intensity/larvae·fish^-1
小黄鱼 Larimichthys polyactis	10	2	2/10	4	2.0
白姑鱼 Pennahia argentata	10	1	1/10	5	5.0
鳗鲡鱼 Anguilla japonica	10	10	10/10	20	2.0
偏口鱼 Pleuronichthys cornutus	10	10	10/10	197	19.7
蓝点马鲛 Scomberomorus niphonius	10	3	1/30	77	25.7
太平洋真鳕 Gadous macrocephaius	10	10	10/30	1 893	189.3
石鲽鱼 Pleuronichthys cornutus	6	4	4/6	30	7.5
带鱼 Trichiurus lepturus	10	3	3/30	5	1.7
鲐鱼 Scomber japonicus	10	10	10/30	134	13.4
狗鱼 Esox reicherti	7	2	2/7	13	6.5
褐菖鮋 Sebastiscus marmoratus	10	2	2/30	2	1.0
鮟鱇鱼 Lophiomus litulon	5	4	4/5	36	9.0
黄姑鱼 Nibea albiflora	9	9	9/9	23	2.6
鲻鱼、舌鳎鱼等8种鱼 Eight species of fishes including Mugil cephalus, Cynoglossus robustus, etc.	79	0	0	0	0
总计 Total	196	70	35.7	2 439	34.8

海产种类 Marine products	检获虫数 No. Anisakis found	异尖线虫的构成比/% Constituent ratio of Anisakis/%						χ²	P值 P value
海产种类 Marine products	检获虫数 No. Anisakis found	肠系膜和肠壁 Mesentery and intestinal wall	体腔 Coelom	胃壁 Gastric wall	肝 Liver	泄殖腔 Cloaca	生殖器 Genitals	χ²	P值 P value
小黄鱼 Larimichthys polyactis	4	4/4	0	0	0	0	0	5.61	> 0.05
白姑鱼 Pennahia argentata	5	5/5	0	0	0	0	0	5.23	> 0.05
鳗鲡鱼 Anguilla japonica	20	16/20	0	3/20	0	1/20	0	24.39	< 0.01
偏口鱼 Pleuronichthys cornutus	197	7.6	60.9	5.6	21.8	3.1	1.0	20.88	< 0.01
蓝点马鲛 Scomberomorus niphonius	77	18.2	0	5.2	0	74.0	2.6	4.15	> 0.05
太平洋真鳕 Gadous macrocephaius	1 893	24.1	35.9	31.3	8.6	0	0	29.66	< 0.01
石鲽鱼 Pleuronichthys cornutus	30	0	0	0	96.7	0	3.3	10.94	< 0.01
带鱼 Trichiurus lepturus	5	1/5	0	0	0	4/5	0	4.99	> 0.05
鲐鱼 Scomber japonicus	134	0.8	82.1	0	1.5	15.7	0	21.47	< 0.01
狗鱼 Esox reicherti	13	0	13/13	0	0	0	0	5.77	> 0.05
褐菖鮋 Sebastiscus marmoratus	2	0	2/2	0	0	0	0	5.61	> 0.05
鮟鱇鱼 Lophiomus litulon	36	75.0	22.2	2.78	0	0	0	7.12	> 0.05
黄姑鱼 Nibea albiflora	23	73.9	17.4	8.7	0	0	0	12.27	< 0.01

海产种类 Marine products	体长 Body length			体质量 Body mass
海产种类 Marine products	平均体长[M（Q）] /cm Average length [M (Q)]/cm	秩相关系数 Rank correlation coefficient	P值 P value	平均质量 [M（Q）]/kg Average mass [M (Q)]/kg	秩相关系数 Rank correlation coefficient	P值 P value
小黄鱼 Larimichthys polyactis	16.00（3.00）	0.71	< 0.05	0.13（0.02）	0.64	< 0.05
白姑鱼 Pennahia argentata	23.00（3.00）	0.18	> 0.05	0.15（0.02）	0.36	> 0.05
鳗鲡鱼 Anguilla japonica	47.00（5.00）	0.03	> 0.05	0.15（0.01）	-0.29	> 0.05
偏口鱼 Pleuronichthys cornutus	27.50（2.00）	0.57	> 0.05	0.23（0.03）	0.45	> 0.05
蓝点马鲛 Scomberomorus niphonius	54.50（4.00）	-0.01	> 0.05	1.00（0.25）	-0.35	> 0.05
太平洋真鳕 Gadous macrocephaius	48.00（3.00）	0.47	> 0.05	1.36（0.29）	0.59	> 0.05
石鲽鱼 Pleuronichthys cornutus	37.00（3.00）	-0.09	> 0.05	0.48（0.03）	-0.02	> 0.05
带鱼 Trichiurus lepturus	69.50（10.00）	0.05	> 0.05	0.19（0.04）	-0.17	> 0.05
鲐鱼 Scomber japonicus	30.50（1.00）	0.05	> 0.05	0.28（0.02）	-0.22	> 0.05
狗鱼 Esox reicherti	70.00（11.00）	0.81	< 0.05	0.70（0.37）	0.80	< 0.05
褐菖鮋 Sebastiscus marmoratus	17.00（1.00）	-0.28	> 0.05	0.20（0.01）	-0.20	> 0.05
鮟鱇鱼 Lophiomus litulon	31.00（5.00）	-0.39	> 0.05	0.52（0.14）	-0.98	< 0.01
黄姑鱼 Nibea albiflora	30.00（8.00）	-0.05	> 0.05	0.25（0.08）	0.40	> 0.05

特征 Feature	知识了解情况占比/% Proportion of knowledge of anisakiasis/%				行为习惯占比/% Proportion of behavior habits/%
特征 Feature	知道异尖线虫病 Know of anisakiasis	知道如何引起感染Know how to cause infection	知道预防感染方法 Know how to prevent infection	知道感染症状 Know infection symptoms	有食生或半生海鱼习惯 Have the habit of eating raw or semi-raw sea fish/%	生、熟食砧板不分 Raw and cooked food handled with not separated cutting boards
性别 Gender
男 Male	11.2（18/160）	8.8（14/160）	10.0（16/160）	8.1（13/160）	20.6（33/160）	15.6（25/160）
女 Female	6.6（15/227）	4.0（9/227）	4.9（11/227）	2.6（6/227）	11.5（26/227）	19.4（44/227）
年龄组 Age
1~19	0/5	0/5	0/5	0/5	1/5	0/5
20~39	2.1（2/96）	0（0/96）	2.1（2/96）	0（0/96）	39.6（38/96）	4.2（4/96）
40~59	10.0（15/150）	7.3（11/150）	9.3（14/150）	6.7（10/150）	11.3（17/150）	14.0（21/150）
≥ 60	11.8（16/136）	8.8（12/136）	8.1（11/136）	6.6（9/136）	2.2（3/136）	32.4（44/136）
村 Village
积米崖 Jimiya	0（0/69）	0（0/69）	0（0/69）	0（0/69）	0.0（0/69）	2.9（2/69）
高峪 Gaoyu	9.2（7/76）	0（0/76）	9.2（7/76）	0（0/76）	7.9（6/76）	0（0/76）
刘家崖 Liujiaya	0（0/101）	0（0/101）	0（0/101）	0（0/101）	2.0（2/101）	58.4（59/101）
庄家瞳 Zhuangjiatong	36.6（26/71）	32.4（23/71）	28.2（20/71）	26.8（19/71）	1.4（1/71）	9.9（7/71）
陈家贡 Chenjiagong	0（0/70）	0（0/70）	0（0/70）	0（0/70）	71.4（50/70）	1.4（1/70）
总计Total	8.5（33/387）	5.9（23/387）	7.0（27/387）	4.9（19/387）	15.3（59/387）	17.8（69/387）

特征 Feature	疾病知识知晓率/% Understanding of disease knowledge/%			χ²	P值 P values
特征 Feature	非常了解 Very well	基本了解 Basic understanding	不了解 Do not understand	χ²	P值 P values
性别 Gender
男 Male	8.1（13/160）	3.1（5/160）	88.8（142/160）	7.69	< 0.05
女 Female	2.2（5/227）	4.4（10/227）	93.4（212/227）
年龄组/岁 Age group/Year
1~19	0/5	0/5	5/5	10.89	> 0.05
20~39	0.0（0/96）	2.1（2/96）	97.9（94/96）
40~59	6.7（10/150）	3.3（5/150）	90.0（135/150）
≥ 60	5.9（8/136）	5.9（8/136）	88.2（120/136）
村 Village
积米崖 Jimiya	0（0/69）	0（0/69）	100（69/69）	81.15	< 0.01
高峪 Gaoyu	0（0/76）	9.2（7/76）	90.8（69/76）
刘家崖 Liujiaya	0（0/101）	0（0/101）	100（101/101）
庄家瞳 Zhuangjiatong	25.4（18/71）	1 1.3（8/71）	63.3（45/71）
陈家贡 Chenjiagong	0（0/70）	0（0/70）	100（70/70）