Blood glucose profile as a rapid method for observing Koi carp (Cyprinus carpio) health status - case study of ectoparasites in Blitar, Indonesia

Perfil de glicose no sangue como um método rápido para observar o estado de saúde de carpa Koi (Cyprinus carpio) - estudo de caso de ectoparasitos em Blitar, Indonésia

Abstract

Assessment of fish health is one of the efforts of farmers in minimizing losses due to disease. Rapid tests on fish health can be done through blood observations. This study aimed to determine the blood glucose profile of koi carp due to ectoparasite infestation from the level of blood glucose. The results showed that reported parasites from Blitar’s koi carp were Trichodina, Dactylogyrus, Gyrodactylus, Myxobolus, Thelohanellus, Ichthyophthirius, and Argulus. Trichodina showed the highest prevalence (100%) in this case while Thelohanellus was the highest intensity level (93.8±16.3). The results of blood glucose level measurement based on parasite infestation levels showed no significant difference (p>0.05) though the health problems caused by parasites in light, medium or heavy infestation. This research also indicated that the blood glucose profile could be used as a rapid method to detect fish health caused by parasites. We suggest that other variables such as nutritional status, life stage or feeding must be conducted to ensure the glucose role in parasite identification as a rapid method for the future work.

Keywords:
Blood identification method; fish disease; glucose; Koi carp

Resumo

A avaliação da saúde dos peixes é um dos esforços dos produtores para minimizar as perdas por doenças. Testes rápidos de saúde de peixes podem ser feitos por meio de observações de sangue. Este estudo teve como objetivo determinar o perfil glicêmico de peixes “koi”, devido à infestação de ectoparasitos a partir do nível de glicemia. Os resultados mostraram que os parasitas relatados de peixes “koi” de Blitar foram Trichodina, Dactylogyrus, Gyrodactylus, Myxobolus, Thelohanellus, Ichthyophthirius e Argulus. Trichodina apresentou a maior prevalência (100%) neste caso, enquanto Thelohanellus foi o maior em nível de intensidade (93,8±16,3). Os resultados da medição do nível de glicose no sangue, com base nos níveis de infestação parasitária, não mostraram diferença significativa (p>0,05), apesar dos problemas de saúde causados ​​por parasitas em infestação leve, média ou pesada. Esta pesquisa também indicou que o perfil de glicose no sangue pode ser usado como um método rápido, para detectar a saúde dos peixes causada por parasitas. Este estudo também sugere que outras variáveis, como estado nutricional, estágio de vida ou alimentação, devem ser conduzidas para garantir o papel da glicose na identificação do parasita como um método rápido para trabalhos futuros.

Palavras-chave:
Método de identificação de sangue; doença de peixe; glicose; carpa Koi

Introduction

Koi carp (Cyprinus carpio) is one of the commercial aquaculture species in Indonesia. Data from The Ministry of Maritime Affairs and Fisheries in 2020 showed that the export value of koi carp reached 2,775 kg with nominal 34,881 USD. Study Domasevich et al. (2022) has already stated that koi is a favorite fish among aquarists for all qualitative attributes. Therefore, many koi carp cultivation businesses are carried out in Indonesia, especially Blitar. Blitar is one of the cities with the largest koi carp production in Indonesia. Previous data stated that Blitar produces 40 million koi carp per year and the government has designed Blitar as a minapolitan area for ornamental koi carp (Abidin et al., 2019).

Unfortunately, koi carp farming activities in Blitar still have problems. In June 2020, the koi production area in Blitar was attacked by a fish disease. Many studies reported that extreme parasites attacked the koi carp in Blitar (Maftuch et al., 2018; Soelistyoadi et al., 2020; Yanuhar et al., 2021). Furthermore, the parasite case in Blitar caused mortality reaching 90% (Yanuhar et al., 2021). The infected fish became weak, experienced less motion, pale color, decreased appetite, and mortality occurred. The parasites that caused the case in Blitar recently were Myxobolus, Argulus, Trichodina, Dactylogyrus, Gyrodactylus, and Ichthyophthirius multifiliis (Kismiyati et al., 2015; Azmi et al., 2013; Mahasri et al., 2011).

One way to prevent this case is to understand the condition of the fish's blood. When fish are infected by parasites, the body's defense mechanism becomes weak so that fish become stressed. Stress levels can be determined by increasing blood glucose levels in fish (Jiang et al., 2017). Stress causes an increase in glucocorticoids which results in an increase in blood glucose levels to cope with high energy requirements (Suarez-Bregua et al., 2018). If the fish's blood glucose condition is not normal, the fish's life will be disrupted and can even cause death. Measurement of blood glucose levels can be used to diagnose stressed fish simply, effectively, and rapidly for a variety of stressors (Sulmartiwi et al., 2013; Makaras et al., 2020). Based on the description above, we conducted a study in Blitar to determine the type and number of parasites and also blood glucose levels in koi carp. This study aimed to re-introduce the method of blood glucose profile determination of koi carp due to ectoparasite infestation from the level of blood glucose.

Materials and Methods

Sample collection

Koi carp samples with a size of 5-10 cm were collected in June 2021 from Blitar, East Java, Indonesia (112°14'-112°28' East Longitude and 8°2'-8°8' South Latitude) (Figure 1).

Figure 1
Geographical location of the sampling station.

Fish and blood collection

The fish samples (n=60) were collected and transported by using a styrofoam box filled with ice from the field to the Laboratory of the Livestock and Fisheries Service of Blitar Regency as described in a previous study for ectoparasite examination (Morey et al., 2022). Before being packed in styrofoam, koi carp were anesthetized using clove oil and directly measured for blood glucose levels using an EasyTouch^™, then packed per fish and labeled. Blood was drawn using a 1 mL syringe filled with 2% EDTA (Ethylene Diamine Tetra Acid) solution which was used as an anticoagulant. Koi carp blood sampling was done through the caudal vein. The caudal vein is under the vertebrae. A minimum of 0.1 ml of blood is taken and then inserted at the end of the test script that has been inserted into the digital blood glucose test kit. The results of blood glucose levels will appear on the screen of a digital blood glucose device in the form of numbers with units of mg/dL. The fish samples used in this study have found animal welfare based on Guidelines for the Use of Fishes in Research (AFS, 2014) and approved by Fisheries and Marine Faculty of Universitas Airlangga according to protocol number 1231, 2021.

Examination of study parameter

The main parameters observed were blood glucose levels, ectoparasite prevalence, infestation, intensity, and water quality. Examination of ectoparasites in koi carp (n=60) was carried out using the native method by scraping on the surface of the body and gills (Yusni & Rambe, 2019). The scrapping results were observed using a binocular microscope (OLYMPUS Cx21) with a magnification of 100x. The degree of infestation was determined as the severity of the damage caused by the parasite to the host. Formula of the degree of ectoparasite infestation determination according to (Williams & Bunkley-Williams, 1996) was shown in Table 1.

Table 1
Formula of degree of parasite infestation determination.

Level of infestation (parasites)	Categories
<1	Very light
1-5	Light
6-10	Moderate
11-50	Medium
51-100	Heavy
101-999	Superheavy
>1000	Superinfection

The prevalence and intensity of ectoparasites were observed according to Bush et al. (1997), while blood measurement was conducted according to previous research methods (Eames et al., 2010). Prevalence is the total number of cases of a disease occurring at a certain time (Ayanful-Torgby et al., 2018). The prevalence was calculated using the following formula (Pawar, 2022):

$\text{Prevalence =}\frac{\text{Number of infected fish}}{\text{Number of fish samples}}\text{x 100\%}$ (1)

The ectoparasite intensity was calculated to determine the number of parasites in individuals or populations which was indicated by the average parasite value per host (Shaw et al., 2018). Intensity was calculated using the following formula (Hakim et al., 2019):

$\text{Intensity =}\frac{\text{Number of parasites found}}{\text{Number of fish infested with parasites}}$ (2)

The results of the examination of blood glucose levels with units of mg/dL and the degree of ectoparasite infestation are presented in the form of tables and figures to provide a descriptive picture.

Water quality

Water quality measurement data follows the procedures from previous studies (Wiyoto & Effendi, 2020). The results of the water quality measurement in the koi carp pond soil obtained a temperature of 28^oC, dissolved oxygen 4.71 mg/L, pH 8.6, and ammonia 0.05 mg/L.

Statistical analysis

This study used an ANOVA test at 5% significance to determine differences in blood glucose values ​​of koi carp in each category of the degree of ectoparasite infestation to evaluate the rapid method. Prior to the ANOVA test, the normality test was carried out by Kolmogorov Smirnov and the homogeneity test was carried out by Levene's Test.

Results

Fish parasite examination

The results of the examination of ectoparasites found are Trichodina, Dactylogyrus, Gyrodactylus, Myxobolus, Thelohanellus, Ichthyophthirius, and Argulus (Figure 2). Trichodina showed the highest prevalence (100%) in this case while Ichtyophthirius was the lowest (13.3%) (Figure 2). Heavy levels of infestation showed in Myxobolus and Thelohanellus. In intensity level, Thelohanellus was the highest (93.8±16.3) while Argulus showed the lowest value (2.1±0.7) (Table 2).

Figure 2
A. Cyprinus carpio; B. Dactylogyrus sp. (a. Opisthaptor; b. Eye spot; c. Hook), 100x; C. Gyrodactylus sp. (a. Opisthaptor; b. Haptor), 100x; D. Myxobolus sp., 100x; E. Thelohanellus sp., 100x; F. Ichthyophthirius (a. Micronucleus; b. Macronucleus; c. Cilia; d. Membrant), 100x; G. Argulus sp. (a. Testes; b. Maxilla; c. Stylet; d. Leg; e. Proboscis), 40x; H. Skin infested by Gyrodactylus sp.; I. Trichodina sp. (a. Adhesive disc; b. Denticle ray; c. Denticle), 100x.

Table 2
Fish parasite observation in this study.

Species Fish	Ectoparasite	Predilection	Prevalence (%)	Mean Intensity	Degree of infestation
Cyprinus carpio (n=60)	Trichodina sp.	Gills, skin	100	23.9±6.03	Medium
	Dactylogyrus sp.	Gills, skin	95	21.8±0.25	Medium
	Gyrodactylus sp.	Gills, skin	46.7	4.9±3.61	Light
	Myxobolus sp.	Gills, skin	31.7	75±25.03	Heavy
	Thelohanellus sp.	Gills, skin	13.3	93.8±16.3	Heavy
	Ichthyophthirius	Gills	6.7	2.3±2.5	Light
	Argulus sp.	Skin	15	2.1±0.7	Light

Koi carp blood glucose profile

Measurement of blood glucose levels showed a different value in fish infested with parasites. The result showed that koi carp with light, medium, and heavy infestation of ectoparasites had blood glucose levels that were not significantly different (p = 0.715 > 0.05) (Table 3).

Table 3
Results of blood glucose level measurement based on the degree of parasite infestation. There was no significant difference in blood glucose for the three degrees of ectoparasitic infestation (p = 0.715 > 0.05).

Fish Samples	Degree of infestation	Blood glucose level
		Mean ± SE (mg/dL)	F-value	p-value
Cyprinus carpio (n=60)	Light	99.242±6.592	0.337	NS
	Medium	86.333±26.168		NS
	Heavy	106.791±10.819		NS

• SE: standard error; NS: not significant.

Discussion

Ectoparasite investigation and blood glucose response

The parasites found in this study were indeed ectoparasites in koi carp. Trichodina, Dactylogyrus, Gyrodactylus, Myxobolus, and Thelohanellus were infested in the gills and skin of koi carp (Elisafitri et al., 2021; Yanuhar et al., 2019; Zhang et al., 2022). Another study stated that Ichthyophthirius attaches to gills while Argulus is found in koi carp skin (Firdausi et al., 2020; Koyuncu, 2020). Gills are a favorite part for parasites to attach to. This is because the parasite uses the host molecule on the gills as a receptor and tries to avoid the host’s immune system (Scheifler et al., 2022). The presence of parasites in fish gills reduces the gill surface area, causes disturbances of hydromineral balance, increases ATP-ase expression and induces apoptosis in mitochondria-rich cells (Oğuz & Oğuz, 2020). This mechanism causes reduced oxygen entering the fish, the color of the gills becomes pale, uncertain movement, fade color, stress, and even mortality (Suliman et al., 2021). Besides gills, skin is a favorite place for parasites to attach. This is because the parasite attaches to the skin and gills of the host to get nutrients in the form of epidermal cells or even blood to develop (Faruk, 2018). The skin-infested parasite is the most abundant, diverse, and pathogenic group of parasites in both freshwater and seawater fish (Zhang et al., 2017).

Infestation level of koi carp

This study also showed that the infestation of light, medium, and heavy were found in koi carp from Blitar. Previously, extreme parasite cases were reported in the Koi carp from Blitar which caused mortality of up to 90% (Maftuch et al., 2018; Soelistyoadi et al., 2020; Yanuhar et al., 2021). The presence of ectoparasite infestations on the body surface of fish could change the normal physiological function of host cells in infested organs and symptoms including lethargy, gill or skin lesions and increased mucus production (Jiang et al., 2017). If two or more parasites infest the same host or organ, there will be competition with each other for nutrients from the host which can affect the immunity and physiology of the host's body (Poulin, 2013). Fish will experience stress and overcoming this requires more energy sources than glucose. Fish divert energy normally used for growth to other physiological processes to maintain homeostasis (McNamara et al., 2013).

The cause of parasitism

The phenomenon of parasitic attack in Blitar was probably caused by environmental factors such as water quality. The results of the water quality measurement in the koi carp pond were temperature 28^oC, dissolved oxygen 4.71 mg/L, pH 8.6, and ammonia 0.05 mg/L. According to a previous study, the optimal water quality parameters for the survival of fish were having an oxygen content of more than 5 mg/L, pH of 6.5-8.5, and ammonia content of less than 0.05 mg/L (Noga, 2010). It was indicated that the water quality in the koi carp pond was not optimal for the growth of koi carp. Low dissolved oxygen and high temperature could be the main factors that caused the high infestation parasite in the soil pond where the koi carp are cultivated. In water conditions with warm temperatures (25-32^oC), acidic pH, and low dissolved oxygen will encourage the proliferation of the parasite group (Saha et al., 2013). The poor water quality in Blitar for koi cultivation may be caused by the origin of the water source. Another study stated that koi cultivation in Blitar used springs, rainwater, river and irrigation water (Kilawati et al., 2020; Kartikasari et al., 2021). This water source had been polluted due to the activity of factory, household and livestock waste so its quality decreased (Sabila et al., 2022; Khopsoh et al., 2021; Hertika et al., 2021; Izzati & Retnaningdyah, 2022).

Blood glucose profile as fish health indicator

This study showed the infestation of ectoparasites with light, medium, and heavy categories increases the blood glucose levels of koi carp. It was indicated that blood glucose profile could be used as a rapid method to determine the fish’s health. This finding is also the same as a previous study that found no change in haemotological parameters in fish infected with parasites (Fallah et al., 2015). Glucose is a monosaccharide of the aldohexose group and a necessary source of energy and carbon for most vertebrates including fish. Blood glucose concentration is widely used as key physiological indicator expressing the general health condition of fish (Endo & Wu, 2019). Glucose is the primary carbohydrate energy source of vertebrates and is stored as glycogen, an a-linked polymer, predominantly in the liver and muscles (‘animal starch’) (Shendurse & Khedkar, 2016). The average blood glucose level in this study indicated the value exceeds the limit. According to previous studies, the normal blood glucose level in fish is 40-90 mg/dL (Patriche, 2009). Several studies have shown the role of glucose as an indicator of the state of stress in fish due to ectoparasites such as Trichodina, Cryptocaryon, Lernaea cyprinacea, Argulus foliaceus, Ceratothoa oestroides (Mahasri et al., 2020; Fallah et al., 2015; Özdemir et al., 2016). In spite of the extended use of glucose as a common stress indicator, undefined and uncontrolled variables which may alter the response in the secretion of glucose must be considered, such as nutritional status, life stage, time since the last feeding, maturation or effects of swimming. Most of those factors are not directly considered stressors but have an effect on the glucose level which makes them a source of error (Martínez-Porchas et al., 2009; Malik et al., 2020).

Conclusion

The result of this study provides information regarding the use of glucose as an indicator of fish health status regarding fish ectoparasite infestation. Changes in blood glucose values ​​can be used as an early indicator of impaired fish health due to parasites. This study also suggests that other variables such as nutritional status, life stage or feeding must be conducted to ensure the glucose role in parasite identification as a rapid method.

Acknowledgements

This research was supported by Faculty of Fisheries and Marine, Universitas Airlangga. Special thanks to Department of Animal Husbandry and Fisheries, Blitar, East Java, Indonesia for their helps during the sampling and laboratory services. This research was funded by Faculty of Fisheries and Marine Universitas Airlangga (Grant Number: 212/UN3/2021).

• How to cite: Afiyah, Fira MD, Santanumurti MB, Jamal MT, Muttaqin A, Subekti S, et al. Blood glucose profile as a rapid method for observing Koi carp (Cyprinus carpio) health status - case study of ectoparasites in Blitar, Indonesia. Braz J Vet Parasitol 2023; 32(2): e014622. https://doi.org/10.1590/S1984-29612023019

References

• Abidin Z, Setiawan B, Soemarno, Primyastanto M, Sulong A. Ecological and socio-economic sustainability of ornamental fish business in minapolitan area of Blitar Regency, East Java, Indonesia. IOP Conf Ser Earth Environ Sci 2019; 239: 012039. http://dx.doi.org/10.1088/1755-1315/239/1/012039
  » http://dx.doi.org/10.1088/1755-1315/239/1/012039
• American Fisheries Society - AFS. Guidelines for the use of fishes in research [online]. Bethesda; 2014 [cited 2022 Jan 22]. Available from: https://fisheries.org/policy-media/science-guidelines/guidelines-for-the-use-of-fishes-in-research/
  » https://fisheries.org/policy-media/science-guidelines/guidelines-for-the-use-of-fishes-in-research/
• Ayanful-Torgby R, Quashie NB, Boampong JN, Williamson KC, Amoah LE. Seasonal variations in Plasmodium falciparum parasite prevalence assessed by varying diagnostic tests in asymptomatic children in Southern Ghana. PLoS One 2018; 13(6): e0199172. http://dx.doi.org/10.1371/journal.pone.0199172 PMid:29906275.
  » http://dx.doi.org/10.1371/journal.pone.0199172
• Azmi H, Indriyanti DR, Kariada N. Identifikasi ektoparasit pada ikan koi (Cyprinus carpio L) di pasar ikan hias Jurnatan Semarang. Life Sci [online] 2013 [cited 2023 Mar 1]; 2(2): 64-70. Available from: https://journal.unnes.ac.id/sju/index.php/UnnesJLifeSci/article/view/2906
  » https://journal.unnes.ac.id/sju/index.php/UnnesJLifeSci/article/view/2906
• Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. http://dx.doi.org/10.2307/3284227 PMid:9267395.
  » http://dx.doi.org/10.2307/3284227
• Domasevich MA, Hasegawa H, Yamazaki T. Quality evaluation of Kohaku Koi (Cyprinus rubrofuscus) using image analysis. Fishes 2022; 7(4): 158. http://dx.doi.org/10.3390/fishes7040158
  » http://dx.doi.org/10.3390/fishes7040158
• Eames SC, Philipson LH, Prince VE, Kinkel MD. Blood sugar measurement in Zebrafish reveals dynamics of glucose homeostatis. Zebrafish 2010; 7(2): 205-213. http://dx.doi.org/10.1089/zeb.2009.0640 PMid:20515318.
  » http://dx.doi.org/10.1089/zeb.2009.0640
• Elisafitri M, Satyantini WH, Arief M, Sulmartiwi L. Parasitic disease in Koi fish (Cyprinus carpio) in freshwater ponds with different densities in Sukabumi, West Java. IOP Conf Ser Earth Environ Sci 2021; 718(1): 012050. http://dx.doi.org/10.1088/1755-1315/718/1/012050
  » http://dx.doi.org/10.1088/1755-1315/718/1/012050
• Endo H, Wu H. Biosensors for the assessment of fish health: a review. Fish Sci 2019; 85(4): 641-654. http://dx.doi.org/10.1007/s12562-019-01318-y
  » http://dx.doi.org/10.1007/s12562-019-01318-y
• Fallah FJ, Khara H, Rohi JD, Sayadborani M. Hematological parameters associated with parasitism in pike, Esox lucius caught from Anzali wetland. J Parasit Dis 2015; 39(2): 245-248. http://dx.doi.org/10.1007/s12639-013-0329-y PMid:26064009.
  » http://dx.doi.org/10.1007/s12639-013-0329-y
• Faruk MAR. Fish parasite: infectious diseases associated with fish parasite Boca Raton: CRC Press; 2018.
• Firdausi AP, Rahman R, Mahadhika R, Sumadikarta A. The ectoparasitic protozoa of koi fish (Cyprinus carpio) in Sukabumi. J Akuakultur Rawa Indones 2020; 8: 50-57. http://dx.doi.org/10.36706/jari.v8i1.11640
  » http://dx.doi.org/10.36706/jari.v8i1.11640
• Hakim LN, Irawan H, Wulandari R. Identification, intensity and prevalence of endoparasites in Silver Pompano Tachinotus Bloch at Plantation City Tanjungpinang. Intek Akuakultur 2019; 3(1): 45-55.
• Hertika AMS, Supriatna S, Darmawan A, Nugroho BA, Handoko AD, Qurniawatri AY, et al. The hematological profile of Barbonymus altus to evaluate water quality in the Badher bank conservation area, Blitar, East Java, Indonesia. Biodiversitas J 2021; 22(5): 2532-2541. http://dx.doi.org/10.13057/biodiv/d220510
  » http://dx.doi.org/10.13057/biodiv/d220510
• Izzati FN, Retnaningdyah C. Evaluation of river water quality based on biotic index of benthic macroinvertebrate as bioindicator (case study in Genjong River Wlingi Blitar East Java, Indonesia). Biotropika J Trop Biol 2022; 10(2): 117-125. http://dx.doi.org/10.21776/ub.biotropika.2022.010.02.05
  » http://dx.doi.org/10.21776/ub.biotropika.2022.010.02.05
• Jiang D, Wu Y, Huang D, Ren X, Wang Y. Effect of blood glucose level on acute stress response of grass carp Ctenopharyngodon idella. Fish Physiol Biochem 2017; 43(5): 1433-1442. http://dx.doi.org/10.1007/s10695-017-0383-y PMid:28589315.
  » http://dx.doi.org/10.1007/s10695-017-0383-y
• Kartikasari DPP, Bhawiyuga A, Kilawati Y, Maimunah Y, Muttaqin A. Memanfaatkan internet of aquaculture dalam meningkatkan kualitas produksi pada kelompok pembudidaya ikan koi di Blitar. J Innov Appl Technol [online] 2021 [cited 2023 Mar 1]; 7(2): 1321-1325. Available from: https://jiat.ub.ac.id/index.php/jiat/article/view/331
  » https://jiat.ub.ac.id/index.php/jiat/article/view/331
• Khopsoh B, Faradila R, Lidiyawati A, Haryuni N, Lestariningsih L, Afrilia T. Identifikasi bakteri Escherichia coli dari air minum unggas di Peternakan Layer. Musamus J Sci [online] 2021 [cited 2023 Mar 1]; 4(2): 41-45. Available from: http://ejournal.unmus.ac.id/index.php/live/article/view/3956
  » http://ejournal.unmus.ac.id/index.php/live/article/view/3956
• Kilawati Y, Maimunah Y, Muttaqin A, Kartikasari DP, Bhawiyuga A, Amrillah A. Implementasi internet of aquaculture (IoA) untuk deteksi kualitas lingkungan secara cepat dalam upaya pemberdayaan kelompok pembudidaya ikan koi di Blitar. J Innov Appl Technol 2020; 6(2): 1104-1110. http://dx.doi.org/10.21776/ub.jiat.2020.006.02.14
  » http://dx.doi.org/10.21776/ub.jiat.2020.006.02.14
• Kismiyati K, Subekti S, Inaya AFN. The influence of papaya seed (Carica papaya) toward the damage eggs of Argulus japonicus. J Ilm Perikan Kelaut 2015; 7(2): 159-164. http://dx.doi.org/10.20473/jipk.v7i2.11200
  » http://dx.doi.org/10.20473/jipk.v7i2.11200
• Koyuncu C. Koi balığı (Cyprinus carpio, Linnaeus, 1758) yetiştiriciliğinde Argulus japonicus (Thiele, 1900) enfestasyonu. Acta Aquat Turc 2020; 16(1): 66-70. http://dx.doi.org/10.22392/actaquatr.587691
  » http://dx.doi.org/10.22392/actaquatr.587691
• Maftuch M, Sanoesi E, Farichin I, Saputra BA, Ramdhani L, Hidayati S, et al. Histopathology of gill, muscle, intestine, kidney, and liver on Myxobolus sp. infected Koi carp (Cyprinus carpio). J Parasit Dis 2018; 42(1): 137-143. http://dx.doi.org/10.1007/s12639-017-0955-x PMid:29491573.
  » http://dx.doi.org/10.1007/s12639-017-0955-x
• Mahasri G, Widyastuti P, Sulmartiwi L. Leucocyte profil of Koi fish (Cyprinus carpio) which infested by Ichthyophthirius multifiliis on the different infestation degree with cohabitation methode. J Ilm Perikan Kelaut 2011; 3(1): 91-96. http://dx.doi.org/10.20473/jipk.v3i1.11629
  » http://dx.doi.org/10.20473/jipk.v3i1.11629
• Mahasri G, Yodharta IND, Novalisa D, Mukti AT. Correlation between glucose level and protozoan ectoparasite infestation level of Humpback Grouper (Cromileptes altivelis) nursery in UPBL Situbondo, East Java. IOP Conf Ser Earth Environ Sci 2020; 441(1): 012022. http://dx.doi.org/10.1088/1755-1315/441/1/012022
  » http://dx.doi.org/10.1088/1755-1315/441/1/012022
• Makaras T, Razumienė J, Gurevičienė V, Šakinytė I, Stankevičiūtė M, Kazlauskienė N. A new approach of stress evaluation in fish using β-d-Glucose measurement in fish holding-water. Ecol Indic 2020; 109: 105829. http://dx.doi.org/10.1016/j.ecolind.2019.105829
  » http://dx.doi.org/10.1016/j.ecolind.2019.105829
• Malik MA, Komarewar S, Dar SA. Why fish is a natural diabetic animal? World J Aquac Res Develop 2020; 2: 1010.
• Martínez-Porchas M, Martínez-Córdova LR, Ramos-Enriquez R. Cortisol and glucose: reliable indicators of fish stress? Pan-Am J Aquat Sci 2009; 4(2): 158-178.
• McNamara KB, Van Lieshout E, Jones TM, Simmons LW. Age‐dependent trade‐offs between immunity and male, but not female, reproduction. J Anim Ecol 2013; 82(1): 235-244. http://dx.doi.org/10.1111/j.1365-2656.2012.02018.x PMid:22849327.
  » http://dx.doi.org/10.1111/j.1365-2656.2012.02018.x
• Morey GAM, Rojas CAT, Marin GAR, Guardia CTC. Occurrence of Eustrongylides sp. (Nematoda: Dioctophymatidae) in fish species collected in the Peruvian Amazonia and its implications for public health. Acta Parasitol 2022; 67(3): 1432-1439. http://dx.doi.org/10.1007/s11686-022-00574-w PMid:35639231.
  » http://dx.doi.org/10.1007/s11686-022-00574-w
• Noga EJ. Fish disease: diagnosis and treatment 2nd ed. Hoboken: Wiley Balckwell; 2010. http://dx.doi.org/10.1002/9781118786758
  » http://dx.doi.org/10.1002/9781118786758
• Oğuz AR, Oğuz EK. Histopathology and immunohistochemistry of gills of Van fish (Alburnus tarichi Güldenstädt, 1814) infected with myxosporean parasites. J Histotechnol 2020; 43(2): 76-82. http://dx.doi.org/10.1080/01478885.2019.1686848 PMid:31783723.
  » http://dx.doi.org/10.1080/01478885.2019.1686848
• Özdemir G, Çelik EŞ, Yilmaz S, Gürkan M, Kaya H. Histopathology and blood parameters of Bogue Fish (Boops boops, Linnaeus 1758) parasitized by Ceratothoa oestroides (Isopoda: cymothoidae). Turk J Fish Aquat Sci 2016; 16(3): 585-596. http://dx.doi.org/10.4194/1303-2712-v16_3_28
  » http://dx.doi.org/10.4194/1303-2712-v16_3_28
• Patriche T. The importance of glucose determination in the blood of the cyprinids. Lucr Stiint Zooteh Biotehnol 2009; 42: 102-106.
• Pawar RT. Studies on the prevalence and seasonal variation of Gangesia (Gangesia) ramkai (Pawar, 2008) from freshwater fish, Wallago attu (Bleeker). Int J Fauna Biol Stud 2022; 9(1): 26-29.
• Poulin R. Explaining variability in parasite aggregation levels among host samples. Parasitology 2013; 140(4): 541-546. http://dx.doi.org/10.1017/S0031182012002053 PMid:23343821.
  » http://dx.doi.org/10.1017/S0031182012002053
• Sabila AT, Highall AR, Purbasari A, Perwiro D, Sulistywati E, Widianto AA. Analisis pengaruh limbah Pabrik Gula Rejoso Manis Indo terhadap pencemaran lingkungan masyarakat Rejoso dan Umbuldamar. JIHI3S [online] 2022 [cited 2023 Mar 1]; 2(4): 322-332. Available from: http://journal3.um.ac.id/index.php/fis/article/view/2096
  » http://journal3.um.ac.id/index.php/fis/article/view/2096
• Saha H, Saha RK, Kamilya D, Kumar P. Low pH, dissolved oxygen and high temperature induces Thelohanellus rohita (myxozoan) infestation in tropical fish, Labeo rohita (Hamilton). J Parasit Dis 2013; 37(2): 264-270. http://dx.doi.org/10.1007/s12639-012-0177-1 PMid:24431581.
  » http://dx.doi.org/10.1007/s12639-012-0177-1
• Scheifler M, Magnanou E, Sanchez-Brosseau S, Desdevises Y. Host specificity of monogenean ectoparasites on fish skin and gills assessed by a metabarcoding approach. Int J Parasitol 2022; 52(8): 559-567. http://dx.doi.org/10.1016/j.ijpara.2022.02.001 PMid:35358503.
  » http://dx.doi.org/10.1016/j.ijpara.2022.02.001
• Shaw AK, Sherman J, Barker FK, Zuk M. Metrics matter: the effect of parasite richness, intensity and prevalence on the evolution of host migration. Proc Biol Sci 2018; 285(1891): 20182147. http://dx.doi.org/10.1098/rspb.2018.2147 PMid:30429312.
  » http://dx.doi.org/10.1098/rspb.2018.2147
• Shendurse AM, Khedkar CD. Glucose: properties and analysis. In: Caballero B, Finglas PM, Toldrá F, editors. Encyclopedia of food and health Burlington: Elsevier; 2016. p. 239-247. http://dx.doi.org/10.1016/B978-0-12-384947-2.00353-6
  » http://dx.doi.org/10.1016/B978-0-12-384947-2.00353-6
• Soelistyoadi RN, Nurekawati AD, Setyawati D. Morphology and sequencing of Myxobolus koi DNA that infects Koi fish (Cyprinus carpio) in Blitar Regency. J Aquac Sci 2020; 5(1): 38-53. http://dx.doi.org/10.31093/joas.v5i1.89
  » http://dx.doi.org/10.31093/joas.v5i1.89
• Suarez-Bregua P, Guerreiro PM, Rotllant J. Stress, glucocorticoids and bone: a review from mammals and fish. Front Endocrinol 2018; 9: 526. http://dx.doi.org/10.3389/fendo.2018.00526 PMid:30250453.
  » http://dx.doi.org/10.3389/fendo.2018.00526
• Suliman EAM, Osman HA, Al-Deghayem WAA. Histopathological changes induced by ectoparasites on gills and skin of Oreochromis niloticus (Burchell 1822) in fish ponds. J Appl Biol Biotechnol 2021; 9(1): 68-74. http://dx.doi.org/10.7324/JABB.2021.9109
  » http://dx.doi.org/10.7324/JABB.2021.9109
• Sulmartiwi L, Harweni S, Mukti AT, Triastuti J. Influence use of bandotan (Ageratum conyzoides) to rate Koi fish (Cyprinus carpio) blood glucose after transportation. J Ilm Perikan Kelaut 2013; 5(1): 73-76. http://dx.doi.org/10.20473/jipk.v5i1.11428
  » http://dx.doi.org/10.20473/jipk.v5i1.11428
• Williams EH, Bunkley-Williams L. Parasites of offshore big game fishes of Puerto Rico and the western Atlantic San Juan: Puerto Rico Department of Natural and Environmental Resources; Mayaguez: University of Puerto Rico; 1996.
• Wiyoto W, Effendi I. Analysis of water quality for mariculture in Moro, Karimun, Riau Islands with principal component analysis. J Aquac Fish Health 2020; 9(2): 143-154. http://dx.doi.org/10.20473/jafh.v9i2.17192
  » http://dx.doi.org/10.20473/jafh.v9i2.17192
• Yanuhar U, Hardiono SA, Junirahma NS, Caesar NR. Profile of Myxobolus infection in koi fish (Cyprinus carpio) gill tissue from Land Pond, Nglegok, Blitar Regency. IOP Conf Ser Earth Environ Sci 2021; 674(1): 012016. http://dx.doi.org/10.1088/1755-1315/674/1/012016
  » http://dx.doi.org/10.1088/1755-1315/674/1/012016
• Yanuhar U, Junirahma NS, Susilowati K, Caesar NR, Musa M. Effects of probiotic treatment on histopathology of koi carp (Cyprinus carpio) infected by Myxobolus sp. J Phys Conf Ser 2019; 1374(1): 012051. http://dx.doi.org/10.1088/1742-6596/1374/1/012051
  » http://dx.doi.org/10.1088/1742-6596/1374/1/012051
• Yusni E, Rambe E. Identification of ectoparasites in fry Tilapia (Oreochromis niloticus) in aquaculture pond. IOP Conf Ser Earth Environ Sci 2019; 260(1): 012110. http://dx.doi.org/10.1088/1755-1315/260/1/012110
  » http://dx.doi.org/10.1088/1755-1315/260/1/012110
• Zhang B, Zhai Y, Liu Y, Gu Z. Myxobolus pseudowulii sp. n. (Myxozoa: Myxosporea), a new skin parasites of yellow catfish Tachysurus fulvidraco (Richardson) and redescription of Myxobolus voremkhai (Akhmerov, 1960). Folia Parasitol (Praha) 2017; 64: 030. http://dx.doi.org/10.14411/fp.2017.030 PMid:28980972.
  » http://dx.doi.org/10.14411/fp.2017.030
• Zhang XY, Yao X, Zhou F, Yang CZ, Liu Y. Identification of Thelohanellus pseudonikolskii n. sp. and Myxobolus koi Kudo, 1920 from goldfish Carassius auratus. Aquacult Rep 2022; 24: 101167. http://dx.doi.org/10.1016/j.aqrep.2022.101167
  » http://dx.doi.org/10.1016/j.aqrep.2022.101167

Publication Dates

• Publication in this collection
  07 Apr 2023
• Date of issue
  2023

History

• Received
  29 Nov 2022
• Accepted
  01 Mar 2023