Antibacterial effects of mangrove ethanolic leaf extract against zoonotic fish pathogen Salmonella arizonae

Jomel S Limbago; Josette Sosas; Angelie A Gente; Parif Maderse; Marjorie M Rocamora; Dennis K Gomez

doi:10.17017/j.fish.260

Jomel S Limbago Fisheries and Aquatic Sciences Department, Cavite State University – Naic, Bucana Malake, Naic, Cavite, Philippines; College of Fisheries and Aquatic Sciences, Iloilo State College of Fisheries, Tiwi, Barotac Nuevo, Iloilo, Philippines https://orcid.org/0000-0002-6425-5892
Josette Sosas College of Fisheries and Aquatic Sciences, Iloilo State College of Fisheries, Tiwi, Barotac Nuevo, Iloilo, Philippines; Bureau of Fisheries and Aquatic Sciences, Regional Office VI, Department of Agriculture, Iloilo City, Philippines
Angelie A Gente College of Fisheries and Aquatic Sciences, Iloilo State College of Fisheries, Tiwi, Barotac Nuevo, Iloilo, Philippines https://orcid.org/0000-0001-8907-0299
Parif Maderse College of Fisheries and Aquatic Sciences, Iloilo State College of Fisheries, Tiwi, Barotac Nuevo, Iloilo, Philippines; National Marine Fisheries Development Center, MCS and Fishing Technology Station, Bureau of Fisheries and Aquatic Resources, Navotas City, Philippines
Marjorie M Rocamora College of Fisheries and Aquatic Sciences, Iloilo State College of Fisheries, Tiwi, Barotac Nuevo, Iloilo, Philippines; Aquaculture Department, Southeast Asian Fisheries Development Center, Tigbauan, Iloilo, Philippines https://orcid.org/0000-0002-9261-1671
Dennis K Gomez College of Fisheries and Aquatic Sciences, Iloilo State College of Fisheries, Tiwi, Barotac Nuevo, Iloilo, Philippines; Fish Health Laboratory, College of Fisheries and Aquatic Sciences, Iloilo State College of Fisheries, Tiwi, Barotac Nuevo, Iloilo, Philippines https://orcid.org/0000-0003-3663-4841

DOI: https://doi.org/10.17017/j.fish.260

Keywords: Antibacterial, In vitro, In vivo, mangroves, phytochemicals, zone of inhibition

Abstract

The emergence of multiple drug-resistant pathogens, affecting aquaculture and public health, has put the spotlight on alternative medicine research. This study was conducted to evaluate the In vitro and In vivo antibacterial activity of mangrove ethanolic leaf extract (MLEE) against Salmonella arizonae isolated from Carassius auratus. In vitro, antimicrobial activity of 10 mangrove species and 13 commercial antibiotics were determined using the agar diffusion method. MLEE with the highest antimicrobial activity were subjected to qualitative phytochemical tests and bioassay experiments. In vivo antibacterial activity of MLEE was assessed using C. auratus intraperitoneally injected with S. arizonae. Results showed that Sonneratia alba has the highest antimicrobial activity against S. arizonae followed by Avicennia marina, A. officinalis, Sonneratia ovata, Rhizophora mucronata, Excoecaria agallocha, and Bruguiera cylindrica. However, bacterial isolate was resistant to A. rhumpiana, Scyphiphora hydrophyllacea, and Laguncularia racemosa. Interestingly, S. alba has comparable antimicrobial activity with amoxicillin, trimethoprim, novobiocin, and cefixime. The activity of S. alba could be attributed to the presence of flavonoids, saponin, sterols, tannin, and terpenoids. Moreover, S. alba has reduced and delayed the onset of goldfish mortality infected with S. arizonae. Based on these findings, the S. alba MLEE, is a potential antimicrobial resource against S. arizonae.

References

Abeysinghe PD (2010) Antibacterial activity of some medicinal mangroves against antibiotic resistant pathogenic bacteria. Indian Journal of Pharmaceutical Sciences 72(2): 167–172.

Ahmed BS, Mostafa AA, Darwesd, OM, Abdel-Rahim EA (2020) Development of specific nano-antibody for application in selective and rapid environmental diagnoses of Salmonella arizonae. Biointerface Research in Applied Chemistry 10(6): 7198–7208.

Audah KA, Amsyir J, Almasyhur F, Hapsari AM, Sutanto H (2018) Development of extract library from Indonesian biodiversity: exploration of antibacterial activity of mangrove Bruguiera cylindrica leaf extracts. IOP Conference Series: Earth and Environmental Science 130(1): 012025.

Avenido P, Serrano AE Jr (2012) Effects of the apple mangrove (Sonneratia caseolaris) on antimicrobial, immunostimulatory and histological responses in black tiger shrimp postlarvae fed at varying feeding frequency. Aquaculture, Aquarium, Conservation & Legislation International Journal of the Biofluc Society 5(3): 112–123.

Bandaranayake WM (2002) Bioactivities, bioactive compounds and chemical constituents of mangrove plants. Wetlands Ecology and Management 10(6): 421–452.

Behbahani BA, Yazdi FT, Shahidi F, Noorbakhsh H, Vasiee A, Alghooneh A (2018) Phytochemical analysis and antibacterial activities extracts of mangrove leaf against the growth of some pathogenic bacteria. Microbial Pathogenesis 114(1): 225–232.

Caldwell ME, Ryerson DL (1939) Salmonellosis in certain reptiles. The Journal of Infectious Diseases 65(3): 242–245.

Cameron-Veas K, Fraile L, Napp S, Garrido V, Grilló MJ, Migura-Garcia L (2018) Multidrug resistant Salmonella enterica isolated from conventional pig farms using antimicrobial agents in preventative medicine programmes. Veterinary Journal 234(1): 36–42.

Caravalho J Jr, McMillan VM, Ellis RB, Betancourt A (1990) Endogenous endophthalmitis due to Salmonella arizonae and Hafnia alvei. Southern Medical Journal 83(3): 325–327.

Casner PR, Zuckerman MJ (1990) Salmonella arizonae in patients with AIDS along the U.S.-Mexican border. The New England Journal of Medicine 323(3): 198–199.

Chandrasekaran M, Kannathasan K, Venkatesalu V, Prabhakar K (2009) Antibacterial activity of some salt marsh halophytes and mangrove plants against methicillin resistant Staphylococcus aureus. World Journal of Microbiology and Biotechnology 25(1): 155–160.

Chapin KC and Lauderdale TL (2007) Reagents, stains, and media: bacteriology. In: Murray PR, Baron EJ, Jorgensen JH, Landry ML, Pfaller MA (Eds) Manual of clinical microbiology. ASM Press, USA.

Cortes E, Zuckerman MJ and Ho H (1992) Recurrent Salmonella arizona infection after treatment for metastatic carcinoma. Journal of Clinical Gastroenterology 14(2): 157–159.

Di Bella S, Capone A, Bordi E, Johnson E, Musso M, ... Petrosillo N (2011) Salmonella enterica ssp. arizonae infection in a 43-year-old Italian man with hypoglobulinemia: a case report and review of the literature. Journal of Medical Case Reports 5: 323.

Djouossi MG, Tamokou JD, Ngnokam D, Kuiate JR, Tapondjou LA, ... Voutquenne-Nazabadioko L (2015) Antimicrobial and antioxidant flavonoids from the leaves of Oncoba spinosa Forssk (Salicaceae). BMC Complementary and Alternative Medicine 15: 134.

dos Santos RR, Xavier RGC, de Oliveira TF, Leite RC, Figueiredo HCP, Leal CAG (2019) Occurrence, genetic diversity, and control of Salmonella enterica in native Brazilian farmed fish. Aquaculture 501: 304–312.

Eswaraiah G, Peele KA, Krupanidhi S, Kumar RB, Venkateswarulua TC (2019) Studies on phytochemical, antioxidant, antimicrobial analysis and separation of bioactive leads of leaf extract from the selected mangroves. Journal of King Saud University - Science 32(1): 842–847.

Galib SM, Mohsin ABM (2010) Exotic ornamental fishes of Bangladesh. Bangladesh Journal of Progressive Science and Technology 8(2): 255–258.

Harizon, Pujiastuti B, Kurnia D, Sumiarsa D, Shiono Y, Supratman U (2015) Antibacterial triterpenoids from the bark of Sonneratia alba (Lythraceae). Natural Products Communications 10(2): 277–280.

Hoag JB, Sessler CN (2005) A comprehensive review of disseminated Salmonella arizona infection with an illustrative case presentation. Southern Medical Journal 98(11): 1123–1129.

Jortner BS, Larsen C (1984) Granulomatous ventriculitis of the brain in arizonosis of turkeys. Veterinary Pathology 21(1): 114–115.

Kathiresan K, Bingham BL (2001) Biology of mangroves and mangrove ecosystems. Advances in Marine Biology 40: 81–251.

Khlif I, Jellali K, Michel T, Halabalaki M, Skaltsounis LA, Allouche N (2015) Characteristics, phytochemical analysis and biological activities of extracts from Tunisian Chetoui olea europaea variety. Journal of Chemistry 2015: 418731.

Kodama H, Nakanishi Y, Yamamoto F, Mikama T, Izawa H, ... Kudo N (1987). Salmonella arizonae isolated from a pirarucu, Arapaima gigas Cuvier, with septicaemia. Journal of Fish Diseases 10(6): 509–512.

Kolker S, Itsekzon T, Yinnon AM, Lachish T (2012) Osteomyelitis due to Salmonella enterica subsp. arizonae: the price of exotic pets. Clinical Microbiology and Infection 18(2): 167–170.

Kumar S, Pandey AK (2013) Chemistry and biological activities of flavonoids: an overview. The Scientific World Journal 2013: 162750.

Lee YC, Hung MC, Hung SC, Wang HP, Cho HL, ... Wang JT (2016) Salmonella enterica subspecies arizonae infection of adult patients in Southern Taiwan: a case series in a non-endemic area and literature review. BMC Infectious Diseases 16: 746.

Lopez D, Cherigo L, de Sedas A, Spadafora C, Martinez-Luis S (2018) Evaluation of antiparasitic, anticancer, antimicrobial and hypoglycemic propertis of organic extracts from Panamanian mangrove plants. Asian Pacific Journal of Tropical Medicine 11(1): 32–39.

Mahajan RK, Khan SA, Chandel DS, Kumar N, Hans C, Chaudhry R (2003) Fatal case of Salmonella enterica subsp. arizonae gastroenteritis in an infant with microcephaly. Journal of Clinical Microbiology 41(12): 5830–5832.

Mierziak J, Kostyn K, Kulma A (2014) Flavonoids as important molecules of plant interactions with the environment. Molecules 19(10): 16240–16265.

Miranda CD, Godoy FA, Lee MR (2018) Current status of the use of antibiotics and the antimicrobial resistance in the Chilean Salmon farms. Frontiers in Microbiology 9: 1284.

Mishra MP, Rath S, Swain SS, Ghosh G, Das D, Padhy RN (2017) In vitro antibacterial activity of crude extracts of 9 selected medicinal plants against UTI causing MDR bacteria. Journal of King Saud University-Science 29(1): 84–95.

Musa WJA, Bialangi N, Situmeang B, Silaban S (2019) Triterpenoid compound from metanol extract of mangrove leaves (Sonneratia alba) and anti-cholesterol activity test. Jurnal Pendidikan Kimia 11(1): 18–23.

Muyot FB, Mutia MTM, Manejar AJA,Guihem GL, Muñez MJ (2019) Status of ornamental fish industry in the Philippines: prospects for development. The Philippine Journal of Fisheries 26(2): 12–32.

Nabeelah BS, Fawzi MM, Gokhan Z, Rajesh J, Nadeem N, ... Pandian SK (2019) Ethnopharmacology, phytochemistry, and global distribution of mangroves- a comprehensive review. Marine Drugs 17(4): 231.

Nishioka H, Doi A, Takegawa H (2017) Pyelonephritis in Japan caused by Salmonella enterica subspecies arizonae. Journal of Infection and Chemothererapy 23(12): 841–843.

Nowinski RJ, Albert MC (2000) Salmonella osteomyelitis secondary to iguana exposure. Clinical Orthopaedics and Related Research 372(1): 250–253.

Nuhu T, Olayinka BO, Bolaju RO, Adabara N (2017) Salmonella arizonae: an uncommon uropathogen? Gulf Medical Journal 6(1): 22–26.

Okla MK, Alamri SA, Alatar AA, Hegazy AK, Al-Ghamdi AA, ... Abdel-Maksoud MA (2019) Antioxidant, hypoglycemic, and neurobehavioral effects of a leaf extract of Avicennia marina on autoimmune diabetic mice. Evidence-Based Complementary and Alternative Medicine 19: 1263260.

Primavera JH, Sadaba RS, Lebara MJHL, Altamirano JP (2004) Handbook of mangroves in the Philippines- Panay. SEAFDEC Aquaculture Department, Iloilo.

Ravikumar S, Inbaneson SJ, Suganthi P, Gnanadesigan M (2011) In vitro antiplasmodial activity of ethanolic extracts of mangrove plants from South East coast of India against chloroquine-sensitive Plasmodium falciparum. Parasitology Research 108(4): 873–878.

Ruangpan L Tendencia EA (2004) Laboratory manual of standardized methods for antimicrobial sensitivity tests for bacteria isolated from aquaculture. SEAFDEC Aquaculture Department, Iloilo, Philippines.

Saad S, Taher M, Susanti D, Qaralleh H, Awang AF (2012) In vitro antimicrobial activity of mangrove plant Sonneratia alba. Asian Pacific Journal of Tropical Biomedicine 2(6): 427–429.

Sachithanandam V, Lalitha P, Parthiban A, Mageswaran T, Manmadhan K, Sridhar R (2019) A Review on antidiabetic properties of Indian mangrove plants with reference to island ecosystem. Evidence-Based Complementary Alternative Medicine 19: 4305148.

Sahoo G, Mulla NS, Ansari ZA, Mohandass C (2012) Antibacterial activity of mangrove leaf extracts against human pathogens. Indian Journal of Pharmaceutical Sciences 74(4): 348–351.

Santos L, Ramos F (2018) Antimicrobial resistance in aquaculture: current knowledge and alternatives to tackle the problem. International Journal of Antimicrobial Agents 52: 135–143.

Seligmann E, Saphra L, Wassermann M (1944) Occurrence of some unusual Salmonella types in man including a new type, Salmonella georgia. American Journal of Hygiene 40(3): 227–231.

Smilack JD, Goldberg MA (1975) Bone and joint infection with Arizona hinshawii: report of a case and a review of the literature. The American Journal of Medical Sciences 270(3): 503–507.

Smith KF, Schmidt V, Rosen GE, Amaral-Zettler L (2012) Microbial diversity and potential pathogens in ornamental fish aquarium water. PloS one 7(9): e39971.

Thatoi H, Samantaray D, Das SK (2016) The genus Avicennia, a pioneer group of dominant mangrove plant species with potential medicinal values: a review. Frontiers in Life Science 9(4): 267–291.

Tonguthai K, Chinabut S, Somsiri T, Chanratchakol P, Kanchanakhan S (1999) Diagnostic procedures for finfish diseases. Aquatic Animal Health Research Institute, Bangkok, Thailand.

Walczak N, Puk K, Guz L (2017) Bacterial flora associated with diseased freshwater ornamental fish. Journal of Veterinary Research 61(4): 445–449.

Wang J, Li Y, Xu X, Liang B, Wu F, ... Song H (2017) Antimicrobial resistance of Salmonella enterica serovar typhimurium in Shanghai, China. Frontiers in Microbiology 8(1): 510.

Watts JEM, Schreier HJ, Lanska L, Hale MS (2017) The rising tide of antimicrobial resistance in aquaculture: sources, sinks and solutions. Marine Drugs 15(6): 158.

Xie Y, Yang W, Tang F, Chen X, Ren L (2015) Antibacterial activities of flavonoids: structure-activity relationship and mechanism. Current Medicinal Chemistry 22(1): 132–149.