Phytotherapy in Lactococcosis in Aquaculture: History
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Lactococcosis, particularly that caused by Lactococcus garvieae, is a major re-emerging bacterial disease seriously affecting the sustainability of aquaculture industry. Medicinal herbs and plants do not have very much in vitro antagonism and in vivo disease resistance towards lactococcosis agents in aquaculture. Most in vitro studies with herbal extractives were performed against L. garvieae with no strong antibacterial activity, but essential oils, especially those that contain thymol or carvacrol, are more effective. 

  • lactococcosis
  • Lactococcus garvieae
  • phytotherapy
  • aquaculture

1. Introduction

Among the species of Lactococcus genus, L. garvieae has been highlighted as one of the most serious global bacterial pathogens in the aquaculture sector, both in freshwater and marine fish, especially at water temperatures of >15 °C, but L. lactis and L. piscium seem to be limited to some highly valuable aquaculture species, such as salmonids and sturgeons, at various water temperatures [1][2][3]. Due to the widespread sources of the bacterial agents and disease spreading, as well as the heterogenicity of the bacterial stains implicated in the disease outbreaks, both vaccination and chemotherapy require more attention in future. The application of co-friendly environmental substances, such as medicinal herbs and probiotics, are nowadays a potential best alternative to antibiotic therapy and an immune enhancer against such bacterial diseases.

2. Diseases Caused by Lactococcus Members in Aquaculture

2.1. Disease Caused by L. garvieae

Lactococcosis, caused by L. garvieae, is a systemic hyperacute bacterial disease causing general hemorrhagic symptoms in susceptible aquatic organisms [4][5]. Based on their ability to agglutinate serum raised against L. garvieae, there are two groups of bacterial serotypes: non-agglutinating (KG−) and agglutinating (KG+) phenotypes [6]. The affected fish first become relatively anorexic, with a visible darkening of skin color, showing sluggish movement and abnormal behaviors, such as erratic and spiral swimming [1][4]. In the later stages of the disease the affected fish display signs of swollen abdomen, anal prolapsus, lateral or bilateral exophthalmia (Figure 1A,B), cataracts (Figure 1C), congestion of the internal organs, spleen and liver enlargement, accumulation of turbid ascitic fluid in the peritoneal cavity, and the presence of exudates in the brain [1][2][7][8]. Acute hyperemia and or extensive hemorrhage and petechiae of the organs, including the mucosal layers of the intestine, can also be seen in the diseased fish (Figure 1F), and in some cases the diseased fish show signs of explosion in the eyes prior to the loss of their eyes (Figure 1D,E) [1][2][9]. In advanced forms of the disease, a Gram stain preparation of hematopoietic tissue imprints, including spleen and kidney, can exhibit huge numbers of Gram-positive coccoid cells in single or chain forms (Figure 1G).
Vetsci 08 00181 g001 550
Figure 1. Rainbow trout growing in race ways and affected by L. garvieae showing: (A) typical bilateral exophthalmia and no change in the color skin, (B) typical bilateral exophthalmia and beginning of skin color change, (C) typical cataract and dark color, (D) bilateral exophthalmia and a complete loss of the eye, (E) darkening of body and an explosion of the eye, (F) hemorrhage of intestine, (G) direct Gram stain preparation of spleen of diseased fish showing huge numbers of Gram-positive coccoid cells confirmed as L. garvieae by phenotyping and molecular works. (photos by Professor Mehdi Soltani).
Pericarditis, peritonitis and meningitis, diffuse hemorrhage in the sclera of the eye, focal necrosis in the spleen and clumps of bacteria, hemorrhage in serosa of the swim bladder and in the interstitium of the skeletal muscles, degeneration and necrosis in epithelia of the stomach glands and their lumens full of necrotic material are among the identified histopathological findings in lactococcosis infection caused by L. garvieae [10][11][12]. Vascular changes in spleen and kidneys [13] and degenerations in the tubular epithelium with an increase in the melano-macrophage centers, hemorrhage in the form of a hematoma covering the myocardium and the bulbus arteriosa, petechial hemorrhage, vascular change, degeneration and necrosis are major histopathological findings. Lipid and ell infiltration in the liver, hemorrhage and vascular change in muscles, and petechial hemorrhage and edema in the gills are further microscopic changes reported in the infected fish by L. garvieae [11]. The severity of such pathological changes is, however, varied and depended on various factors, including level of virulent of bacterial strain, fish species and size and level of health management criteria, such as water temperature.
Evidence of bacterial cells in fish macrophage in tissues of spleen, kidney, heart (endothelial), and peritoneum are evidence of a septicemic condition, suggesting that macrophages play a key role in the host immune response to L. garvieae infection. However, intra-macrophage resistance of the bacteria can cause a spread of the pathogen to all tissues of fish by macrophages. Further, as in the young fish phagocytosis by macrophage activation may not be sufficient, thus, pathogenesis is a determinant factor, and the disease can progress.
Several factors play roles in the virulence of L. garvieae. Polysaccharide capsule is the major virulence factor in L. garvieae infection [9]. The capsulated strains resist to phagocytosis, but some non-capsulated strains are pathogenic in fish causing high mortality in rainbow trout [14], thus, the bacterial capsule may not the sole determinant of the bacterial pathogenicity. Haemolytic toxin is known to cause mortality in fish via intramuscular injection and an intracellular toxin with a low leukocidal activity reported by the bacterial isolates recovered from the diseased fish [15]. Plasmids of the virulent isolates contain a protein with an enzymatic domain corresponding to the family of actin-ADP-ribosyltransferases [16] that can kill eukaryotic cells by transferring ADP-ribose to essential proteins [17]. The toxicity of this protein in fish however, warranted future research works. The presence of a putative set of virulence factor genes (hly1, hly2, hly3, nox, sod, pavA, psaA), and proteins of enolase, lactate dehydrogenase phosphoenolpyruvate-protein phosphotransferase with roles in adhesion, cytolytic activity, oxidative stress tolerance, and metal homeostasis have been detected in strains of L. garvieae, including the avirulent reference strains ATCC® 49156 and ATCC® 4392, isolates from diseased rainbow trout in Turkey, France, Iran, Spain, and Italy [18], and fish pathogenic non-capsulated strains in South Africa [19]. These virulence lifestyle factors can indirectly contribute to host tissue damage through aiding in the infection process by evasion of the host’s innate immunity, systemic invasion, cofactor homeostasis, and spreading in the host and adhesion to host tissues. Further research works need to be directed studying the differential expression of virulence lifestyle and true virulence genes during growth in the host environment. Additionally, more studies need to assess the specific virulence factors responsible for the pathogenicity of L. garvieae, as putative virulence factor genes are present in both the fish pathogenic isolates and the avirulent isolates.

2.2. Diseases Caused by Other Species of Lactococcus Genus

L. lactis strains are genetically classified into four subspecies of lactis, cremoris, tractae, and hordniae [20]. It is not a common veterinary pathogen, although it can cause cattle mastitis and be involved in septic arthritis of the neonatal calf. For example, several variants of L. lactis have been associated with bovine mastitis [21]. In humans, it has been reported as a cause of endocarditis, arthritis, and septicemia in patients, although this requires more clarification [22][23][24][25][26].

Up to date, there are only four reports of lactococcosis by L. lactis in an aquatic organisms. The first report was an outbreak of white tail disease in cultured giant freshwater prawn (Macrobrachium rosenbergii) in Taiwan [27]. The affected prawns were cloudy and whitish in the muscles, showing remarkable edema and necrosis and inflammation in the muscles and hepatopancreas. In subsequent report by Chen et al. [3] L. lactis subsp. Lactis was isolated from affected hybrid sturgeon, Bester (Huso huso x Acipenser ruthenus) with signs of anorexia, pale body color, reddish spots on the abdomen, enteritis, enlarged abdomen, rapid respiration rate ascites, and 70%–100% mortality. Microscopically, the affected sturgeons demonstrated extensive haemorrhagic multifocal necrotic foci of spleen and liver with degeneration of hepatic cells, lipid droplets and glycogen granules, necrosis and renal tubule epithelial swelling and hydropic degeneration in kidney, skin ulcers deep in underling muscles, appearance of present of immunocompetent cells in the stomach, and small focus on tips of gills and on the myocardium [3]. No histopathological changes were, however seen in the eyeball, cerebrum and meninges of affected fish. The third report was from silver carp (Hypophthalmichthys molitrix) with extensive skin lesions near the caudal peduncle and musculoskeletal lesion in the USA [28]. The fourth outbreak of infection by L. lactis has been reported as the cause of endocarditis valvularis, parientalis thromboticans in mature allis shad (Alosa alosa) in Europe in 2018 that could be associated with the stressors, such as capturing, transport, breeding, and low oxygen level [29]. Although, in some cases the disease was reproduced experimentally, the mechanisms of pathogenesis by L. lactis in aquatic animals warranted future research works.

3. Phytotherapy of Lactococcosis in Aquaculture

3.1. In Vitro Studies

Almost all in vitro studies with vegetable and lichens extractives were performed against L. garvieae. For convenience, details of in vitro and in vivo studies have been included in Table 1 and Table 2. Overall, extracts do not show strong antibacterial activity against L. garvieae, but essential oils are more effective, mainly those that contain thymol or carvacrol. There are some differences on minimum inhibitory and bactericidal concentrations for the same extractive in different studies (Table 1).
Table 1. Minimum inhibitory concentration (MIC) (μg mL−1 or μL mL−1) and minimum bactericidal concentration (MBC) (μg mL−1 or μL mL−1) of plant and lichen extractives against Lactococcus garvieae. The portion of the plant used to prepare the extractives were cited only if stated in the studies. Note: The MIC50 and MIC90 of 15 antibiotics against 146 strains of L. garvieae isolated from diseased fish are also given at the end of the table.
Origin/
Source of L. garvieae
Plant Extractive Major Compounds MIC MBC Reference
Rainbow trout Camellia sinensis (green tea-leaves) Methanolic extract Unknown 800 1100 Akbary, 2014
Rainbow trout Thymus vulgaris (thyme), Origanum vulgare (oregano) and Eucalyptus sp. Mix-oil® (essential oils from leaves) Citraconic anhydride, 1, 8-cineole, thymol 6.25 12.5 Amiri et al., 2020
Unknown Glycyrrhiza glabra L. (black sugar-root) n-hexane extract Unknown Unknown 5630 Asan-Ozusaglam et al., 2014
Unknown Glycyrrhiza glabra L. (root) Dichloromethane extract Unknown Unknown 1410 Asan-Ozusaglam et al., 2014
Type culture collection Lavandula angustifolia (lavender) Essential oil Unknown 500 Unknown Baba, 2020
Type culture collection Eugenia caryophyllus Essential oil Unknown 250 Unknown Baba, 2020
Rainbow trout Mentha piperitae (pepper mint) Essential oil Unknown 500 Unknown Baba, 2020
Rainbow trout Rosmarinus officinalis (rosemary) Essential oil Unknown 500 Unknown Baba, 2020
Rainbow trout Cinnamomum zeylanicum (cinnamon) Essential oil Unknown 250 Unknown Baba, 2020
Rainbow trout Nigella sativa (black cumin) Essential oil Unknown 250 Unknown Baba, 2020
Strain O41 Lavandula officinalis (true lavender-flowers) Ethanolic extract Essential oil (linalyl acetate), tannins,
coumarins, flavonoids, and phytosterols
4200 8400 Bulfon et al., 2014
Strain O41 Melissa officinalis (lemon balm-leaves) Ethanolic extract Rosmarinic acid, essential oil (citral,
citronellal, β-caryophyllen), caffeic acid, and chlorogenic acidderivatives
8400 33,600 Bulfon et al., 2014
Strain O41 Ocimum basilicum (sweet basil-flowering plant) Ethanolic extract Essential oil (linalool, estragol, camphor, eugenol, ocimene, cineol, sesquiterpenes), tannins, favonoids, caffeic acid, and esculoside 16,800 Unknown Bulfon et al., 2014
Strain O41 Origanum vulgare (oregano-inflorescence) Ethanolic extract Carvacrol, thymol, γ-terpinene, p-cymene, limonene, linolool, and borneol 4200 33,600 Bulfon et al., 2014
Strain O41 Orthosiphon stamineus (Java tea-leaves) Ethanolic extract Essential oil (sesquiterpenes), flavones, triterpenoid, saponins, vitamins, and organic salts 33,600 Unknown Bulfon et al., 2014
Strain O41 Rosmarinus officinalis (leaves) Ethanolic extract Essential oil (eucalyptol, α-pinene, camphor, borneol), flavonoids, rosmarinic acid, and terpenes 8400 Unknown Bulfon et al., 2014
Strain O41 Salvia officinalis (sage-leaves) Ethanolic extract Essential oil (thujone, monoterpenes, and sesquiterpenes), tannins, bitter substances, and flavonoids 4200 33,600 Bulfon et al., 2014
Strain O41 Thymus vulgaris (leaves) Ethanolic extract Essential oil (thymol, carvacrol, p-cimol, and terpinene), tannins, flavonoids and triterpenes Unknown Unknown Bulfon et al., 2014
Strain O41 Vaccinium vitis-idaea (lingonberry-leaves) Ethanolic extract Phenolic glycosides (arbutin and hydroquinone), tannins, flavonoids (iperoside, avicularin, isoquercitrin), terpenic acids (ursolic and oleanolic acids), organic acids, and mineral salts 4200 Unknown Bulfon et al., 2014
Rainbow trout Glycyrrhiza glabra L. (root) Ethanolic extract Unknown 920 Unknown Fereidouni et al., 2013
Rainbow trout Peganum harmala (wild rue-seed) Methanolic extrac Unknown 105 Unknown Fereidouni et al., 2013
Rainbow trout Trachyspermum copticum (carum ajowan-seed) Ethanolic extract Unknown 453 Unknown Fereidouni et al., 2013
Rainbow trout Myrtus communis (myrtle-leaves) Essential oil Unknown 672 Unknown Fereidouni et al., 2013
Rainbow trout Juglans regia (English walnut-leaves) Ethanolic extract Unknown 510 Unknown Fereidouni et al., 2013
Rainbow trout Quercus branti Lindley (Brant’s oak-seed) Ethanolic extract Unknown 978 Unknown Fereidouni et al., 2013
Rainbow trout Tanacetum parthenium (feverfew-leaves) Essential oil Unknown 824 Unknown Fereidouni et al., 2013
Rainbow trout Satureja bachtiarica Bung. (savory-leaves) Essential oil Unknown 126 Unknown Fereidouni et al., 2013
Rainbow trout Glycyrrhiza glabra L.(root) Ethanolic extract Glycyrrhizinic acid >1000 >1000 Goudarzi et al., 2011
Rainbow trout Satureja bachtiarica Bung. (aerial parts) Essential oil Phenols: Carvacrol, thymol 8 16 Goudarzi et al., 2011
Rainbow trout Satureja bachtiarica Bung. (aerial parts) Ethanolic extract Phenols: Carvacrol, thymol >1000 >1000 Goudarzi et al., 2011
Rainbow trout Punica granatum (pomegranate-flowers) Ethanolic extract Polyphenols: pomegranatate >1000 >1000 Goudarzi et al., 2011
Rainbow trout Quercus branti Lindley (seed/flour) Ethanolic extract Tannins >1000 >1000 Goudarzi et al., 2011
Rainbow trout Echinophora platyloba DC. (prickly parsnip-aerial parts) Essential oil Monoterpenes: trans-β-ocimene >1000 >1000 Goudarzi et al., 2011
Rainbow trout Echinophora platyloba DC. (aerial parts) Ethanolic extract Monoterpenes: trans-β-ocimene >1000 >1000 Goudarzi et al., 2011
Rainbow trout Heracleum lasiopetalum Boiss. (fruits) Ethanolic extract Sesquiterpene hydrocarbons: Germacrene-D >1000 >1000 Goudarzi et al., 2011
Rainbow
trout
Kelussia odoratissima Mozaff. (wild celery-leaves) Ethanolic extract Z-ligustilide >1000 >1000 Goudarzi et al., 2011
Rainbow trout Stachys lavandulifolia Vahl (wood betony-flowers) Ethanolic extract Sabinene, α-pinene, β-myrcene >1000 >1000 Goudarzi et al., 2011
Rainbow trout Thymus daenensis Celak. (common thyme-aerial part/inflorescence) Ethanolic extract Phenols: thymol, carvacrol >1000 >1000 Goudarzi et al., 2011
Rainbow trout Thymus daenensis Celak. (Aerial part/inflorescence) Essential oil Phenols: thymol, carvacrol 8 16 Goudarzi et al., 2011
Rainbow trout Myrtus communis (leaves) Ethanolic extract α-pinene, 1,8-cineole, myrtenyl acetate >250 >500 Goudarzi et al., 2011
Rainbow trout Myrtus communis (leaves) Essential oil α-pinene, 1,8-cineole, myrtenyl acetate >1000 >1000 Goudarzi et al., 2011
Rainbow trout Thymbra spicata (spiked thyme-aerial part/inflorescence) Essential oil Phenols: thymol, carvacrol 8 16 Goudarzi et al., 2011
Rainbow trout Bunium persicum (Boiss.) K.-
Pol. (black caraway-fruits)
Essential oil γ-terpinen-7-al, cuminaldehyde, γ terpinene 8 16 Goudarzi et al., 2011
Rainbow trout Teucrium polium (felty germander-aerial parts) Essential oil α-pinene, linalool >1000 >1000 Goudarzi et al., 2011
Rainbow trout Alhagi maurorum (camelthorn-aerial parts) Essential oil Alhagidin, alhagitin, quercetin, catechin >1000 >1000 Goudarzi et al., 2011
Rainbow trout Zataria multifora Boiss. (Shirazi thyme) Essential oil Phenols: thymol, carvacrol 4 8 Goudarzi et al., 2011
Olive flounder (P. olivaceus) Zingiber officinale (ginger) Essential oil   2000 2000 Hossain et al., 2019
L. garvieae GQ850376 Eucalyptus globulus (southern blue gum-aerial parts) Essential oil 1,8-eucalypol, pinene, terpineol acetae, globulol 250 250 Mahmoodi et al., 2012
L. garvieae GQ850376 Eucalyptus globulus (aerial parts) Methanolic extract 1,8-eucalypol, pinene, terpineol acetae, globulol 500 500 Mahmoodi et al., 2012
L. garvieae GQ850376 Zataria multiflora (aerial parts) Essential oil phenolic monoterpene, Carvacrol, alpha-pinene 7.8 15.6 Mahmoodi et al., 2012
L. garvieae GQ850376 Zataria multiflora (aerial parts) Methanolic extract phenolic monoterpene Carvacrol, alpha-pinene 15.6 15.6 Mahmoodi et al., 2012
L. garvieae GQ850376 Anethum graveolens (dill-seed) Essential oil D-carvacrol, limonene, dill apiole, E-dihydrocarvone, Z-dihydrocarvone 62.4 125 Mahmoodi et al., 2012
L. garvieae GQ850376 Anethum graveolens (seed) Methanolic extract D-carvacrol, limonene, dill apiole, E-dihydrocarvone, Z-dihydrocarvone 125 125 Mahmoodi et al., 2012
L. garvieae GQ850376 Rosmarinus officinalis Essential oil 1,8-cineole, alpha-pinene, toluene 15.6 31.2 Mahmoodi et al., 2012
L. garvieae GQ850376 Rosmarinus officinalis Methanolic extract 1,8-cineole, alpha-pinene, toluene 31.2 31.2 Mahmoodi et al., 2012
Rainbow trout Citrus paradisi (grapefruit), Citrus reticulata (tangerine), Citrus aurantium ssp. bergamia (bergamot), Citrus sinensis (sweet orange) Biocitro ® (blend of citrus extracts) Ascorbic acid, citrus bioflavonoids (hesperidin, naringin, quercetin, rutin) and organic acids 2.0 Unknown Mora-Sánchez et al., 2020
Tilapia (O. andersonii) Capsicum annum (Chili pepper) Methanolic extract (capsaicin) Unknown Unknown 196.7 Ndashe et al., 2020
Olive flounder Citrus aurantifolia (key lime-peel) Essential oil Limonene, γ-terpinene, β-pinene 0.125% (v/v) 1% (v/v) Pathirana et al., 2018
Olive flounder Limonene Commercial trans-limonene (>99%) Limonene 0.031% (v/v) 0.025% (v/v) Pathirana et al., 2018
Olive flounder Syzygium aromaticum (clove-buds) Essential oil Eugenol, β-caryophyllene, α-humulen, eugenyl-acetate 0.5% (v/v) 1% (v/v) Pathirana et al., 2019a
Olive flounder Commercial eugenol (>99%) Isolated compound
eugenol
Eugenol 1% (v/v) 1% (v/v) Pathirana et al., 2019a
Olive flounder Cinnamomum zeylanicum Essential oil Cinnamaldehyde, eugenol,
β-Caryophyllene
0.015% (v/v) 0.031% (v/v) Pathirana et al., 2019b
Olive flounder Commercial trans-cinnamaldehyde (>99%) (Sigma-Aldrich) cinnamaldehyde Cinnamaldehyde 0.003% (v/v) 0.015% (v/v) Pathirana et al., 2019b
Rainbow trout Argania spinose L. (argan-oil) Essential oil Oleic acid, linoleic acid, palmitic acid, stearic acid 250 Unknown Öntas et al., 2016
Rainbow trout Citrus limon L. (lemon-peel) Essential oil Limonene, γ-terpinene, β-pinene, α-terpineol, myrecene and terpinolene 500 Unknown Öntas et al., 2016
Strain ATCC43921 Cinnamomum verum (cinnamon-bark) Essential oil Unknown 120 Unknown Rattanachaikunsopon et al., 2009
Strain ATCC43921 Ocimum sanctum (holy basil-leaves) Essential oil Unknown 240 Unknown Rattanachaikunsopon et al., 2009
Strain ATCC43921 Zingiber officinale (roots) Essential oil Unknown 120 Unknown Rattanachaikunsopon et al. 2009
Strain ATCC43921 Syzygium aromaticum (flower buds) Essential oil Unknown 30 Unknown Rattanachaikunsopon et al., 2009
Rainbow trout Zataria multiflora (aerial parts) Essential oil Carvacrol, benzene and phenol 0.12 0.12 Soltani et al., 2014
Rainbow trout Allium sativum (garlic-edible parts) Essential oil trisulfide, di-2-propenyl, disulfide, di-2-propenyl and trisulfide, methyl 2-propenyl 0.5 1 Soltani et al., 2014
Rainbow trout Cinnamomum zeylanicum (bark) Essential oil cinnamic aldehyde, linalool, ortho methoxy cinnamic aldehyde and 1,8-cineole 0.5 0.5 Soltani et al., 2014
S. quinqueradiata Chloramphenicol     0.8 a 1.6 b Maki et al., 2008
S. quinqueradiata Ciprofloxacin     1.6 a 3.13 b Maki et al., 2008
S. quinqueradiata Erythromycin     0.1 a 800 b Maki et al., 2008
S. quinqueradiata Enoxacin     6.25 a 12.5 b Maki et al., 2008
S. quinqueradiata Florfenicol     1.6 a 1.6 b Maki et al., 2008
S. quinqueradiata Floroxacin     12.5 a 12.5 b Maki et al., 2008
S. quinqueradiata Kanamycin     25 a 50 b Maki et al., 2008
S. quinqueradiata Lincomycin     25 a 800 b Maki et al., 2008
S. quinqueradiata Norfloxacin     6.25 a 12.5 b Maki et al., 2008
S. quinqueradiata Oxolinic acid     400 a 800 b Maki et al., 2008
S. quinqueradiata Orbifloxacin     1.6 a 1.6 b Maki et al., 2008
S. quinqueradiata Ofloxacin     3.13 a 6.25 b Maki et al., 2008
S. quinqueradiata Penzylpenicillin     0.8 a 1.6 b Maki et al., 2008
S. quinqueradiata Streptomycin     25 a 50 b Maki et al., 2008
S. quinqueradiata Tetracycline     12.5 a 400 b Maki et al., 2008
Letters a and b showing MIC50 and MIC90, respectively.
Table 2. Efficacy of medicinal herbs and plants on the survival of aquatic animals infected with Lactococcus garvieae. The portion of the plant used to prepare the extractives were cited only if stated in the studies.
Host Plant Extractive Dosage/Duration Survival Increase Compared to Control (%) 2 Reference
Giant freshwater prawn (Macrobrachium
rosenbergii)
Eichhornia crassipes (water hyacinth-leaves) Hot-water extract 1 g kg diet−1, 12 days
2 g kg diet−1, 12 days
3 g kg diet−1, 12 days
↑57.3
↑128.6
↑171.4
Chang et al., 2013
Giant freshwater prawn
(M. rosenbergii)
Eichhornia crassipes (leaves) Powder 20 g kg diet−1, 120 days ↑44.3 Chang et al., 2016
    Hot-water extract 20 g kg diet−1, 120 days ↑89.0  
    Aqueous extract 1 2 g kg diet−1, 120 days ↑89.0  
    Dreg of aqueous extract 1 18 g kg diet−1, 120 days ↑77.7  
Giant freshwater prawn
(M. rosenbergii)
Musa acuminate (banana-peel) Aqueous extract 1 g kg diet−1, 120 days
3 g kg diet−1, 120 days
6 g kg diet−1, 120 days
↑200
↑300
↑467
Rattanavichai et al., 2015
Giant freshwater prawn
(M. rosenbergii)
Morinda cutrifolia (noni) Aqueous extract 0.6 g kg diet−1, 21 days
3 g kg diet−1, 21 days
6 g kg diet−1, 21 days
↑250
↑50.4
NS
Halim et al., 2017
Nile tilapia
(Oreochromis niloticus)
Argania spinosa (argan-seeds) Oil 5 mL kg diet−1, 45 days
10 mL kg diet−1, 45 days
20 mL kg diet−1, 45 days
↑66.7
↑91.7
↑86.1
Baba et al., 2017
Rainbow trout
(Oncorhynchus mykiss)
Lentinula edodes (Shiitake mushroom) Aqueous extract 10 g kg diet−1, 45 days
20 g kg diet−1, 45 days
↑79.0
↑109.7
Baba et al., 2015
Rainbow trout
(O. mykiss)
Pleurotus ostreatus (oyster mushroom) Aqueous extract 10 g kg diet−1, 42 days
20 g kg diet−1, 42 days
↑40.0
↑60.1
Uluköy et al., 2016
Rainbow trout
(O. mykiss)
Usnea barbata (beard lichen) Methanolic extract 230 mg kg fish−1 (a)
460 mg kg fish−1 (a)
690 mg kg fish−1 (a)
↑62.4
↑45.3
NS
Bilen et al., 2019
Three spotted tilapia (Oreochromis andersonii) Capsaicin Isolated compound 1.97 mg kg fish−1 (b) 80% survival vs. 0% survival in control Ndashe et al., 2020
Rainbow trout
(O. mykiss)
Origanum onites (oregano) Essential oil 0.125 mL kg diet−1, 56 days
1.5 mL kg diet−1, 56 days
2.5 mL kg diet−1, 56 days
3.0 mL kg diet−1, 56 days
↑54
↑92
↑84
No mortality
Diler et al. 2017
Nile tilapia
(Oreochromis niloticus)
Syzygium aromaticum (clove-buds) Essential oil 5 mL kg diet−1, 5 days
10 mL kg diet−1, 5 days
20 mL kg diet−1, 5 days
30 mL kg diet−1, 5 days
↑40
↑70
↑80
No mortality
Rattanachaikunsopon et al., 2009
Mullet (Mugil cephalus) * TCM Aqueous extract of the powder 5 g kg fish−1, 28 days
10 g kg fish−1, 28 days
20 g kg fish−1, 28 days
NS
↑230.8
↑184.6
Choi et al., 2014
Rainbow trout
(O. mykiss)
Citrus paradisi (grapefruit), Citrus reticulata (tangerine), Citrus aurantium ssp. bergamia (bergamot), Citrus sinensis (sweet orange) Biocitro ® (blend of these extracts) 0.75 g kg diet−1, 28 days ↑120 Mora-Sánchez et al., 2020
1 Aqueous extract was the supernatant of the hot-water extract filtered and centrifuged. The left filtered product and sediment were the dreg of aqueous extract. 2 survival increase calculated by the equation: (survival treatment × 100)/survival control–100. NS = nonsignificant difference from control. * TCM = traditional Chinese medicine: composed by the plants Rhizoma coptidis, Radix scutellariae, Cortex phellodendri, Fructus gardeniae jasminoidis, Fructus forsythiae, and Flos lonicerae japonicae. (a) = Gavage in infected fish twice a day for 10 days. (b) = Injected in the same day of infection with the bacteria.

3.2. In Vivo Studies

All in vivo studies were related to survival against L. garvieae infection, and, in most cases, the extractives of medicinal herbs and plants were added to the diets for various periods before the treated fish being challenged with L. garvieae infection. Overall, the essential oils that showed the best in vitro antibacterial activity against L. garvieae (Table 1) were not tested for the in vivo bioassays yet. The extractives tested under in vivo conditions presented moderate in vitro antibacterial activity against this bacterium or even were not tested in vitro. However, the dietary supplementation with all tested extractives reduced mortality of infected animals (Table 2), probably because they improved immune parameters before challenging the treated fish with L. garvieae. A 12-day feeding giant freshwater prawn (Macrobrachium rosenbergii) with hot-water extract of water hyacinth (Eichhornia crassipes) leaves at 1, 2, and 3 g kg−1 diet induced significantly higher survival rate after challenge with L. garvieae infection, but higher disease resistance was seen in the prawn treated with higher concentration of the extract [30]. In addition, the treated animals exhibited an enhancement in the immune responses including respiratory burst, phenoloxidase activity, superoxide dismutase activity, glutathione peroxidase, total hemocyte value, differential hemocyte count, transglutaminase activity, and phagocytic activity towards L. garvtieae. In the subsequent research work by Chang and Cheng [31], dietary addition of three tested water hyacinth extracts (Table 2) for 120 days increased survival and immune parameters, i.e., total hemocyte count, semi-granular and granular cells counts of giant freshwater prawn while phenoloxidase activity, respiratory bursts of hemocytes were not observed only with dietary addition of powder of this plant to the diet.

4. Conclusions

Disease outbreaks by Lactococcus species specially L. garvieae is one of the major concerns faced in the aquaculture production worldwide, and various biological and environmental variables, as well as the aquaculture practices and husbandry can affect the quantity and impacts of the morbidity and mortality. Data influencing the economic losses can, thus, assist to develop policies and strategies to reduce the losses by lactococcosis outbreaks in aquaculture industry. Lactococcosis outbreaks especially by L. garvieae are increasingly recognized as a significant and re-emerging bacterial disease in aquaculture, but there is no an estimation of its economic impacts. Data describing antagonistic activity and disease resistance efficacy of potential medicinal herbs and plants towards lactococcosis caused by L. garvieae, L. lactis, L. piscium and L. raffinolactis in finfish are not very much. Almost all in vitro studies with vegetable and lichens extractives were performed against L. garvieae. Despite no strong antibacterial activity by herb extracts against L. garvieae, essential oils especially those that contain thymol and carvacrol are more effective against L. garvieae strains. The exhibited differences on minimum inhibitory and bactericidal values for the same extractive in different studies could be due to the use of different bacterial strains or parts or chemotypes of the same plant. Despite best anti-L. garvieae activity by the essential oils under in vitro assays, the in vivo bioassays need be assessed yet. The extractives tested under in vivo conditions presented moderate antibacterial activity against this bacterium or even were not tested in vitro. However, the dietary supplementation with all tested extractives reduced mortality of infected animals, probably because they improved immune parameters before challenging the treated fish with L. garvieae.

This entry is adapted from the peer-reviewed paper 10.3390/vetsci8090181

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