PARASITES OF PUBLIC HEALTH IMPORTANCE IN LIZARD FISH COLLECTED FROM SHARKIA GOVERNORATE, EGYPT

Document Type : Original Article

Abstract

ABSTRACT
Foodborne infections due to parasites have been well known since time and continue to be of great importance in many regions of the world. A total of one hundred specimens of Sauridaundosqamis (lizard fish) were collected from fish markets at sharkiagovernate from October 2018 till the end of May 2019. Samples were investigated parasitologically for anisakid nematode larvae. The results showed that the total prevalence of anisakid nematode was 58%.The sites of infection were pyloric caeca, peritoneal cavity, stomach, large intestine and liver. Anisakis spp., Phocanema spp. and Hystyrothylacium larvae were isolated.

Highlights

195                                                     Egypt. J. of Appl. Sci., 34 (9) 2019                     

الطفیلیات ذات الاهمیة الصحیة فی أسماک المکرونة المجمعة من محافظة الشرقیة، مصر

أمانی محمد عبدالغنی ، عبدالله فکری عبدالله محمود ، سلوی محمد عبدالغنی

قسم مراقبة الأغذیة کلیة الطب البیطری جامعة الزقازیق مصر

إن العدوى التی تنقلها الأغذیة بسبب الطفیلیات معروفة منذ قدم ولاتزال ذات أهمیة کبیرة فی العدید من مناطق العالم. تم جمع100من سمکة المکرونة البلدی من اسواق السمک بمحافظة الشرقیة. من أکتوبر 2018 حتى نهایة مایو 2019. تم التحقیق فی عینات من الطفیلیات لیرقات أنیماتودا الأنیساکید. أظهرت النتائج أن معدل الانتشار الکلی للدیدان الخیطیةanisakid کان 58 ٪. وکانت مواقع العدوى عبارة عن  caecaالبابی،وتجویف البریتونی،والمعدة،والأمعاء الغلیظة والکبد.وتم عزل یرقات الانیساکیس والفوکانیما ویرقات هستییروثیلاسیوم.

 


Egypt. J. of Appl. Sci., 34 (9) 2019                                                186-195

PARASITES OF PUBLIC HEALTH IMPORTANCE IN LIZARD FISH COLLECTED FROM SHARKIA GOVERNORATE, EGYPT

Amany M. Abd El-Ghany ; A.F.A. Mahmoud

And Salwa M. Abd El-Ghany

Department of Food control, Faculty of Veterinary Medicine, Zagazig University, Egypt

ABSTRACT

Foodborne infections due to parasites have been well known since time and continue to be of great importance in many regions of the world. A total of one hundred specimens of Sauridaundosqamis (lizard fish) were collected from fish markets at sharkiagovernate from October 2018 till the end of May 2019. Samples were investigated parasitologically for anisakid nematode larvae. The results showed that the total prevalence of anisakid nematode was 58%.The sites of infection were pyloric caeca, peritoneal cavity, stomach, large intestine and liver. Anisakis spp., Phocanema spp. and Hystyrothylacium larvae were isolated.

INTRODUCTION

Marine fishes play an important economic role in providing increasing source of protein especially in the developing countries. There is no doubt that parasites that found in fishery product is a hazard to human health and reduce its value. Roberts, (2001).Fish-borne larval nematodes belonging to the family Anisakidae are widespread in fish populations worldwide. Some genera of Anisakidae, vital for public health, embrace Anisakis, Pseudoterranova, Contracaecum, and Hysterothylacium(Berland, 2006).Nematodes are considered as the most economically important helminth parasites infecting fishes in the world (Dick and Choudhury1995). The nematodes are one of the most vital agents for money losses in the marketing value of fish. Therefore, these infections ought to be taken into serious thought for wild and cultivated marine fish.

Anisakiasis in human can be occurred through eating of raw or undercooked fish harbouring the infective third larval stage of parasite. The risk and clinical manifestations of the infection in human  was reported frequently where diarrhea can be occur fewhours after ingestion of infected fish (Ugenti et al., 2004 and Gonzálezet al., 2005 ).The main nematodes known to have caused disease in humans are Anisakis simplex and Pseudo terranovadecipiens. In humans, these nematodes can migrate from the gastrointestinal tract, becoming embedded in the gastrointestinal mucosa and causing tissue reaction and discomfort Beldsoe, andOria,  (2001).

187                                                     Egypt. J. of Appl. Sci., 34 (9) 2019                                             

MATERIALS AND METHODS

One hundred of lizard fishSauridaundosquamis were collected from October 2018 till the end of May 2019 from fish markets, Sharkiagovernate. Skin surface, fins, and gills of fish were examined by the naked eye and dissecting microscope for any attached parasites, lesions, or external changes (Inoue et al. 2000). After dissection, nematode worms as larvae were collected from the surface of visceral organs as the stomach, intestine, and muscles; subsequently rinsed in phosphate-buffered saline (PBS); fixed in 70 % ethanol at 60 °C; and stored in the same solution. For light microscopy, fresh and fixed worms were cleared in lactophenol. Identification was based on the comparison between the morphological characteristics of larval types including the morphology of the digestive tract, the shape and the presence of the boring tooth or the lips at the anterior end, the position of the excretory pore, and the shape of the postanal tail and its terminal mucron(Hafesteinsson and Rizvi1987; Olson et al. 1983; Smith 1983; Køie1993; Anderson 2000; Shih and Jeng2002).

RESULTS

I-Prevalence and distribution of anisakid nematode in lizard fish (S. undosquamis):

Larval anisakids were found in 58 out of 100 examined lizard fish (58%) (Table, 1). The prevalence of Anisakis spp., Pseudoterranova spp. and Hysterothylacium spp. L3 was 11%, 46% and 14%, respectively. Single infection with one anisakid nematode recorded 45% while, mixed infection with two anisakid species was 13% (Table, 2). The mean intensity was 1.45, 11.78 and 1.79 for Anisakis spp., Pseudoterranova spp. and Hysterothylacium spp. larvae, respectively.

The distribution of anisakid larvae in different body parts was as follows; 47 (8.06%), 14 (2.40%), 447 (76.67%), 69 (11.84%), 3 (0.51%) and 3,(0.51%) from body cavity stomach, pyloric caeca, large intestine, liver surface and gonads, respectively.

Of 583 anisakid nematodes recovered; 16 were Anisakis spp. L3, 542 Pseudoterranova spp. L3 and 25 were Hysterothylacium spp. L3. The total number of Anisakis spp. L3 recovered was 16; 15 (93.75%) and one (6.25%) from body cavity and stomach, respectively while, the total number of Pseudoterranova spp. L3 was 542; 32 (5.90%), 11 (2.03%), 438 (89.81%), 56 (10.33%), 2 (0.37%) and 3 (0.55%) from body cavity, stomach, pyloric caeca, large intestine, liver surface and gonads, respectively. Moreover, the total number of Hysterothylacium spp. L3 recovered was 25; 3 (12%), 9 (36%) and 13 (52%) from stomach, pyloric caeca and large intestine, respectively (Table, 3,4).

Egypt. J. of Appl. Sci., 34 (9) 2019                        188

Egypt. J. of Appl. Sci., 34 (9) 2019                                                186-195

Egypt. J. of Appl. Sci., 34 (9) 2019                                                186-195

Egypt. J. of Appl. Sci., 34 (9) 2019                                                186-195

II- Prevalence of anisakid nematode in relation to host size:

The host length was divided into five classes (13-14.9, 15-17.9, 18-20.9, 21-23.9 and ≥24 cm). The prevalence of total anisakid infection was observed in relation to host size in the examined fish(Fig, 1).

Table (1): Prevalence and distribution of anisakid nematodes (n = 100)

No. infected

(%)

Infected With Anisakis (%)

Infected With Phocanema (%)

Infected With Hysterothylacium larvae (%)

59 (59%)

11 fishes

 

46 fishes

 

14 fishes

 

 

Peritoneal cavity,

liver surface

Peritoneal cavity,

pyloric aeca,

large intestine, liver surface, stomach

pyloric aeca,

large intestine,

stomach

Table (2): Single and mixed infection of anisakid nematode in S. undosquamisin relation to host size.

Host size class (cm)

A. l

P.  l

H.  l

H. a

A. +  P.  l

P.  l+ H.  l

13-14.9

-

1

-

-

-

-

15-17.9

-

13

-

-

-

6

18-20.9

-

4

1

-

-

2

21-23.9

-

5

2

-

-

2

≥ 24

9

10

-

-

2

1

Total

9

33

3

-

2

11

  1. Anisakis, P. Pseudoterranova, H. Hysterothylacium, l larval stage, a adult stage.

Table (3): Spearman’s rank correlation coefficient (rs) used to evaluate possible relationships among the total length of S. undosquamis, and prevalence and number of anisakid nematodes.

Parameters

rs

P-value

Length and presence of Anisakisl

0.39

< 0.01**

Length and presence ofPseudoterranoval

-0.41

< 0.01**

Length and presence of Hysterothylaciuml

0.30

< 0.05*

Length and number of anisakid larvae

-0.39

< 0.05*

l larval stage.

Table (4): Single and mixed infection of anisakid nematode in S. undosquamis:

Total examined

Inf

Anisakis

Phocanema

Hysterothylacium

A.+Ph.

Ph.+H.

100

58

9

34

3

2

11

P%

58%

15.5%

58.6%

5.1%

3.4%

18.9%

189Egypt. J. of Appl. Sci., 34 (9) 2019                                             

Fig. (1): Single and mixed infection of anisakid nematode in S. undosquamis:

III-Distribution of anisakid larvae in marine fishes:

The third-stage larvae of Anisakisspp. were isolated from peritoneal cavity, mesenteries, liver surface of Lizardfish (Sauridaundosquamis).The third-stage larvae of Phocanemadecipienswere isolated from body cavity, pyloric caeca, large intestine and liver surface of Lizardfish (Sauridaundosquamis). The third-stage larvae of Hysterothylaciumaduncumwere isolated from body cavity and mesenteries of of Lizardfish (Sauridaundosquamis). 

DISCUSSION

The European Food Safety Authority (EFSA) states that all wild-caught marine and freshwater fish must be considered as potentially containing pathogenic parasites(EFSA, 2010). The nematodes are one of the most important agents for financial losses in the marketing value of fish (Shih et al., 2010).

I-The prevalence of anisakid nematodes in examined fish:

This study revealed that the total prevalence of anisakid nematode in lizard fish was 58%. In contrast, Morsyet al. (2015) observed that the prevalence of anisakid larvae in the same fish species was 75%. Comparatively, anisakid nematode were detected at lower incidencebyAbd al-Aal et al. (2008), Abd El-Ghany (2011), Nada and Abd El-Ghany (2011) and Ahmed et al. (2010) which was 41.86%, 48.76%, 43.43% and 48.76%, respectively.This may be due to differences in the number of samples analysed. The high prevalence of these nematode in commercially important fish species indicates that damage to the fishing industry could occur by considerably reducing the quality of fish, leading to a loss in marketing values (Dornyet al., 2009 and Shih et al., 2010).

Egypt. J. of Appl. Sci., 34 (9) 2019                        190

The current study found that the infection rate of Anisakis sp. larvae in S. undosquamis was 11%with intensity of (1-2) and larvae were found in body cavity and stomach while higher prevalence was reported by Abd El-Ghany (2011) andMorsy et al. (2015) as 24.79% and 35%, respectively. Moreover, Pseudoterranova sp. larvae were detected in body cavity and different visceral organs with a prevalence of 46% and intensity (1-72).This result was different than that mentioned byAbd El-Ghany (2011) andMorsy et al. (2015). Additionally,Hysterothylacium spp. larvae were isolated from stomach, pyloric caeca and large intestine of 14 fishes.

II-Relationship between length of examined fish and prevalence of anisakid nematodes:

The fish length was an influent factor for parasitation by anisakid nematodes in the examined fish species, suggesting that larger specimens may involve a higher risk of infection. In this study,the fish length was weak but significantly correlated with number of the recovered anisakid nematodes (rs= -0.39, P < 0.05). Similarly, Karpiej et al. (2013) found that the number of parasites increased with the fish length (rs= 0.300; P <0.005). As well as,Pulleiro-Potel et al. (2015), Barcala et al. (2018) reported that there was an affirmative association between standard length and prevalence in examined fish samples (p < 0.05). Our results revealed that there was a significant Anisakis L3 prevalence-length relationship (rs= 0.39, p < 0.001). This was in accordance with Young's (1972) hypothesis; A. simplex L3 distributions in fish are expected to be primarily influenced by fish size.Similarly,a recent study considers fish host body size as a major predictor of Anisakissp. occurrence in most fish species (Levsen et al. 2018).The host size is directly related to the age of the host and therefore, the high level of parasitation in older specimens may be due to the accumulation of larvae along time and the higher probabilities of infection, leading to a higher level of abundance and prevalence (Strømnes and Andersen, 2000). On the other hand, there was no relationship between length of fish and occurrence of PseudoterranovaL3 (rs =0.039, P > 0.05), Hysterothylacium L3 (rs =0.099, P > 0.05), and Hysterothylacium adult (rs =- 0.056, P > 0.05) in P. pagrus, which is perhaps unexpected.

III-Morphometric characteristics of detected anisakid nematode:

   Morphological and morphometric studies of the recovered anisakid nematodes revealed that they were third-stage larvae of the genera Anisakis, Pseudoterranova and Hysterothylacium and adult of genus Hysterothylacium of family Anisakidae. This study provides essential information on specific identification and differentiation of infective stages of zoonotic nematode in edible fish. The anterior end of Anisakis and Pseudoterranova larvaehad a boring tooth, long esophagus and ventriculus. However, the ventriculus in Pseudoterranovahad intestinal caeca. The posterior end of Anisakisspp. larvae had a mucron distinguishing it fromPseudoterranova. Morphometric characteristics of larvae were in accordance with Shih (2004), Abd al-Aal et al. (2008), Ahmed et al. (2010), Abd El-Ghany (2011) and Nada and Abd El-Ghany (2011).

191Egypt. J. of Appl. Sci., 34 (9) 2019                                             

Hysterothylaciumlarvae as well as adult worms were characterized by presence of ventriculus, intestinal caeca and ventricular appendix. Also, the excretory pore located at or near the level of nerve ring and the typical cactus tail, which agree with many authors (Deardorff and Overstreet, 1981;Felizardo et al., 2009; Morsy et al., 2013 andMorsy et al., 2015). Specimens of Hysterothylacium larva identified in this study show the same morphological criteria as those observed by Shih and Jeng (2002) in Taiwanese coast of the Northwest Pacific and Morsy et al. (2013) in the Red Sea. However, the morphometric criteria of our specimens show a slight difference compared to those reported by the same authors. Such morphometric differences could be associated with some geographical factors of environment. On the other hand, Knoff et al. (2012) described Hysterothylacium larva that the tail was conical and had a mucron but our study revealed that the tail had multiple spines give it the appearance of a cactus tail.

References

Abd-Al-Aal, Z.; O.H.Amer; A.A. El-Ashram and W.T. El-Ekiaby (2008): Light and electron microscopic studies on some larvae in marine fishes. Zag. Vet. J., 36(5): 110-118.

Abd El-Ghany, A.M. (2011): Parasitological and immunological studies on anisakid parasites. Ph.D. Thesis(Parasitology), Fac. Vet. Med., Zagazig University.

Ahmed, B.A.; E.A.Desoky; O.H. Amer and Amany M. Abd El-Ghany (2010): Larval anisakids (Nematoda: Ascaridoidea)inlizardfish(Sauridaundosquamis)at Sharkia province, Egypt. Zag. Vet. J., 38(1): 168-175.

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Barcala, E.; A.Ramilo; N.Ortega; G.Picó; E.Abollo; S. Pascual and P. Muñoz (2018): Occurrence of AnisakisandHysterothylaciumlarvae in commercial fish from Balearic sea (Western Mediterranean Sea). Parasitol. Res., 117(12): 4003-4012.

Beldsoe, G.E.andM.P. Oria, (2001). Potential Hazards in Cold‐Smoked Fish: Parasites. Journal of Food Science66: S1100-S1103.

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Deardorff, T.L. and R.M. Overstreet (1981): Review of Hysterothylacium, and Iheringascaris (both previously: Thynnascaris) (Nematoda: Anisakidae) from the northern Gulf of Mexico. Proc. Biolog Soc. Wash., 93: 1035-1079.

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Dorny, P.; N.Praet;N. Deckers and S. Gabriel (2009): Emerging food-borne parasites. Vet. Parasitol., 163(3): 196-206.

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González, S.Q. ;R.E.González ;L.G.Arias ;A.M. Gil ;J.S. Vicente and E.F. Corral (2005): Anisakiasis gastrointestinal manifestations: description of 42 cases. RevistaClinica Espanola205(7): 311-315.

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195                                                     Egypt. J. of Appl. Sci., 34 (9) 2019                     

الطفیلیات ذات الاهمیة الصحیة فی أسماک المکرونة المجمعة من محافظة الشرقیة، مصر

أمانی محمد عبدالغنی ، عبدالله فکری عبدالله محمود ، سلوی محمد عبدالغنی

قسم مراقبة الأغذیة کلیة الطب البیطری جامعة الزقازیق مصر

إنالعدوىالتیتنقلهاالأغذیةبسببالطفیلیاتمعروفةمنذقدم ولاتزالذاتأهمیةکبیرةفیالعدیدمنمناطقالعالم. تمجمع100من سمکة المکرونة البلدی من اسواق السمک بمحافظة الشرقیة. منأکتوبر 2018 حتىنهایةمایو 2019. تمالتحقیقفیعیناتمنالطفیلیاتلیرقاتأنیماتوداالأنیساکید. أظهرتالنتائجأنمعدلالانتشارالکلیللدیدانالخیطیةanisakidکان 58 ٪. وکانتمواقعالعدوىعبارةعنcaecaالبابی،وتجویفالبریتونی،والمعدة،والأمعاءالغلیظةوالکبد.وتمعزلیرقاتالانیساکیس والفوکانیما ویرقات هستییروثیلاسیوم.

 

 

 

 

 

 

 

 

 

References

Abd-Al-Aal, Z.; O.H.Amer; A.A. El-Ashram and W.T. El-Ekiaby (2008): Light and electron microscopic studies on some larvae in marine fishes. Zag. Vet. J., 36(5): 110-118.
Abd El-Ghany, A.M. (2011): Parasitological and immunological studies on anisakid parasites. Ph.D. Thesis(Parasitology), Fac. Vet. Med., Zagazig University.
Ahmed, B.A.; E.A.Desoky; O.H. Amer and Amany M. Abd El-Ghany (2010): Larval anisakids (Nematoda: Ascaridoidea)inlizardfish(Sauridaundosquamis)at Sharkia province, Egypt. Zag. Vet. J., 38(1): 168-175.
Egypt. J. of Appl. Sci., 34 (9) 2019                        192
Anderson, R.C. (2000): Nematode Parasites of Vertebrates. Their Development and Transmission.2nd edition.CABI Publishing, Wallingford and New York.
Barcala, E.; A.Ramilo; N.Ortega; G.Picó; E.Abollo; S. Pascual and P. Muñoz (2018): Occurrence of AnisakisandHysterothylaciumlarvae in commercial fish from Balearic sea (Western Mediterranean Sea). Parasitol. Res., 117(12): 4003-4012.
Beldsoe, G.E.andM.P. Oria, (2001). Potential Hazards in Cold‐Smoked Fish: Parasites. Journal of Food Science66: S1100-S1103.
Berland, B. (2006): Musings on nematode parasites. Havforskningsinstituttet (Institute of Marine Research, Bergen), ISSN 0071-5638.
Deardorff, T.L. and R.M. Overstreet (1981): Review of Hysterothylacium, and Iheringascaris (both previously: Thynnascaris) (Nematoda: Anisakidae) from the northern Gulf of Mexico. Proc. Biolog Soc. Wash., 93: 1035-1079.
Dick, T.A. andA.Choudhury (1995): Phylum Nematoda. In: Woo PTK (ed) Fish diseases and disorders, volume I protozoan and metazoan infection. Cambridge University Press, Cambridge, UK, pp: 415– 446.
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