scholarly journals Occurrence, Antimicrobial Resistance Pattern and Plasmid Profile of Salmonella spp. Isolated from Raw Beef Meat in Dhaka City

2016 ◽  
Vol 29 (1) ◽  
pp. 17-22
Author(s):  
Abul Kalam Azad ◽  
Sahana Parveen ◽  
Md Shakir Uddin Ahmed ◽  
Md Abdul Malek
Keyword(s):  
Drug Resistance ◽  
Nalidixic Acid ◽  
Plasmid Profile ◽  
Dhaka City ◽  
Chromosomal Dna ◽  
Salmonella Spp ◽  
Beef Meat ◽  
Salmonella Infections ◽  
Food Borne ◽  
Sensitivity Reaction

Salmonella is motile enterobacterium that causes diseases like typhoid fever, paratyphoid fever and food borne illnesses. Salmonella infections are due to the consumption of contaminated foods. The objective of the present study was to observe the sanitary and hygienic conditions of the retail areas and to isolate pathogenic Salmonella spp from raw beef, to observe antimicrobial sensitivity pattern of Salmonella spp from the raw beef. A total of forty (40) raw beef samples were collected from the sixteen different butcher shops of the four different markets namely Bazaar-1, Bazaar-2, Bazaar-3 and Bazaar-4 of Dhaka City to determine the presence of the significant enteric pathogen Salmonella. From the colony characteristic and biochemical properties, it was found that out of forty samples Salmonella were found in thirty four (85%) samples. The prevalence of drug resistance bacteria were also assayed by antibiotic susceptibility testing. Among thirty four isolates, nearly 6% (2), 32% (11), 76% (26), 6%(2) and 32% (12) isolates showed resistance to Nitrofurantoin, Nalidixic acid, Ampicillin , Gentamycin and Trimethoprim-sulfamethoxazole respectively. Almost 85%(29), 62%(21), 24% (8), 91% (31), 91% (31)and 68% (23) isolates showed sensitivity to Nitrofurantoin, Nalidixic acid, Ampicillin,Ciprofloxacin,Gentamycin and Trimethoprim-sulfamethoxazole respectively Some isolates also showed intermediate in sensitivity reaction for example 3% (1), 6% (2), 3% (1) and 9% (3) isolates showed intermediate in sensitivity reaction to Nitrofurantoin, Ampicillin, Ciprofloxacin, Gentamycin and Nitrofurantoin respectively. Twenty four isolates were investigated for the plasmid profile analysis where thirteen isolates (about 54%) were found to carry plasmids of different sizes ranging from small (2.3 kb) to large sizes (>10kb and also greater than the chromosomal DNA). The presence of large plasmids may be a possible source of drug resistance. The results of this study demonstrate the unhygienic quality of beef meat and their risk of contracting food borne infections to the consumers.Bangladesh J Microbiol, Volume 29, Number 1, June 2012, pp 17-22

scholarly journals Antibiotic Resistance, Plasmids and Integron Profile of Salmonella Species Isolated from Poultry Farm and Patients

2017 ◽  
Vol 15 (2) ◽  
pp. 209-214 ◽  
Author(s):  
Kohinur Begum ◽  
Sultana Juhara Mannan ◽  
Aliza Ahmed
Keyword(s):  
Drug Resistance ◽  
Nalidixic Acid ◽  
Plasmid Profile ◽  
Class I ◽  
Diffusion Method ◽  
Resistance Pattern ◽  
Poultry Farm ◽  
Serological Tests ◽  
Clinical Strains ◽  
Drug Resistance Pattern

A total of ten selected strains of Salmonella species, five from the environment of poultry farm and five from patients were included in this study. All strains were isolated and identified by using selective media, standard biochemical and serological tests. Antimicrobial susceptibility tests were performed by disc diffusion method using twelve commercial antibiotic discs of aztreonam, ceftriaxone, kanamycin, ciprofloxacin, gentamycin, chloramphenicol, ampicillin, erythromycin, cephalexin, tetracycline, cotrimoxazole and nalidixic acid. Plasmid profile and integron gene detection were conducted by Kado-Liu method and PCR, respectively. Only aztreonam, ceftriaxone, kanamycin and gentamycin were shown to be inhibitory to all strains. However, ciprofloxacin, chloramphenicol, amoxicilin, erythromycin, cephalexin, tetracycline, cotrimoxazole and nalidixic acid revealed different degrees of resistance pattern against environmental and clinical strains. Analysis of plasmid demonstrated that three environmental strains contained both plasmids of 140 Mda and 62 Mda. On the other hand, another three strains, one environmental and two clinical isolate only contained 140 Mda plasmid. All the plasmid containing strains (140 Mda and 62 Mda) exhibited same type of drug resistance pattern, whereas strains containing the 140 Mda plasmid only did not show similar type of resistance pattern. Therefore, no correlation was found between plasmid containing strains and drug resistance. Four environmental strains were also found to be positive for the class I integron and one clinical isolated was positive for class I integron gene conferring resistance to common antibiotics. However, none of the strains were found to contain class II integron. Therefore, the present study demonstrated that both environmental and clinical strains contain both large to middle size plasmids and integron I but not integron II. The plasmid and integron I containing strains experienced resistance to different antibiotics, used in the experiments.Dhaka Univ. J. Pharm. Sci. 15(2): 209-214, 2016 (December)

scholarly journals Prevalence and Antibiogram Profiling of Rotten Fruits from Different Areas of Dhaka City, Bangladesh

2020 ◽  
pp. 1-9
Author(s):  
Mahmuda Akhter Akhi ◽  
Avijit Banik ◽  
Oshin Ghurnee ◽  
Nantu Chandra Das ◽  
Showmitro Nondi ◽  
...  
Keyword(s):  
Drug Resistance ◽  
Vibrio Parahaemolyticus ◽  
Pathogenic Microorganisms ◽  
Dhaka City ◽  
Salmonella Spp ◽  
Street Vendors ◽  
E Coli ◽  
Daily Diet ◽  
Acinetobacter Spp ◽  
Klebsiella Spp

Fruits are highly nutritious, sources of vitamins, minerals, fibers etc. and these are part of our daily diet. However, during cultivation, harvesting, transportation, handling fruits get contaminated with pathogenic microorganisms which leads to severe problems to community. Owning to this point, in current research, bacteriological analysis was performed on Sofeda, Pineapple, Grape, Banana, Apple, Orange, Guava, papaya, Jujube and Starfruit. Total 50 samples were randomly collected from market and street vendors of Dhaka city. Higher numbers of rotten fruits were present in wholesale markets. 35 strains were isolated which included Salmonella spp., Acinetobacter spp., Klebsiella spp., Vibrio cholerae, Vibrio parahaemolyticus, Staphylocoous aureus and E. coli. They were identified using biochemical test and antibiogram for selective isolates. In case of drug resistance of isolates, majority exhibited resistance against Erythromycin, Vancomycin and Amoxycillin and showing sensitivity against Ciprofloxacin and Ceftriaxone. It was observed in the current study that 100% isolates were resistant against Erythromycin, followed by Amoxycillin 90.63% and vancomycin 86.25%, where only 35.27% isolates were resistant against Ciprofloxacin. In case of sensitivity 64.73% isolates were sensitive against Ciprofloxacin followed by Ceftriaxone 66.25%. 

scholarly journals Antimicrobial Susceptibility Pattern of Salmonella spp. Isolated from Enteric Fever Patients in Nepal

2021 ◽  
Vol 13 (2) ◽  
pp. 388-400
Author(s):  
Anu Maharjan ◽  
Binod Dhungel ◽  
Anup Bastola ◽  
Upendra Thapa Shrestha ◽  
Nabaraj Adhikari ◽  
...  
Keyword(s):  
Drug Resistance ◽  
Minimum Inhibitory Concentration ◽  
Nalidixic Acid ◽  
Antimicrobial Susceptibility ◽  
Enteric Fever ◽  
Inhibitory Concentration ◽  
Diffusion Method ◽  
Susceptibility Pattern ◽  
Salmonella Spp ◽  
Blood Samples

Introduction: Enteric fever, a systemic infection caused by Salmonella enterica Typhi and S. enterica Paratyphi is one of the most common infections in developing countries such as Nepal. Aside from irrational practices of antibiotic use, mutations in chromosomal genes encoding DNA gyrase and Topoisomerase IV and by plasmid mediated quinolone resistant (PMQR) genes are suggested mechanisms for the development of resistance to nalidixic acid and reduced susceptibility to ciprofloxacin. Regardless of high endemicity of enteric fever in Nepal, there is paucity of studies on prevalence and drug-resistance of the pathogen. Therefore, this study aimed to assess the antibiotic susceptibility pattern of Salmonella isolates and determine the minimum inhibitory concentration of ciprofloxacin. Methods: A total of 1298 blood samples were obtained from patients with suspected enteric fever, attending Sukraraj Tropical and Infectious Disease Hospital (STIDH) during March–August, 2019. Blood samples were inoculated immediately into BACTEC culture bottles and further processed for isolation and identification of Salmonella Typhi and S. Paratyphi. Axenic cultures of the isolates were further subjected to antimicrobial susceptibility testing (AST) by using the modified Kirby–Bauer disc diffusion method based on the guidelines by CLSI. The minimum inhibitory concentration (MIC) of ciprofloxacin was determined by agar-dilution method. Results: Out of 1298 blood cultures, 40 (3.1%) were positive for Salmonella spp. among which 29 (72.5%) isolates were S. Typhi and 11 (27.5%) isolates were S. Paratyphi A. In AST, 12.5% (5/40), 15% (6/40) and 20% (8/40) of the Salmonella isolates were susceptible to nalidixic acid, ofloxacin and levofloxacin, respectively, whereas none of the isolates were susceptible to ciprofloxacin. The MIC value for ciprofloxacin ranged from 0.06-16 µg/mL in which, respectively, 5% (2/40) and 52.5% (21/40) of the isolates were susceptible and resistant to ciprofloxacin. None of the isolates showed multidrug-resistance (MDR) in this study. Conclusion: This study showed high prevalence of quinolone-resistant Salmonella spp., while there was marked re-emergence of susceptibilities to traditional first option drugs. Hence, conventional first-line-drugs and third-generation cephalosporins may find potential usage as the empirical drugs for enteric fever. Although our reporting was free of MDR strains, extensive surveillance, augmentation of diagnostic facilities and treatment protocol aided by AST report are recommended for addressing the escalating drug-resistance in the country.

Simultaneous occurrence of selected food-borne bacterial pathogens on bovine hides, carcasses and beef meat

2010 ◽  
Vol 13 (4) ◽  
pp. 645-651 ◽  
Author(s):  
K. Wieczorek ◽  
J. Osek
Keyword(s):  
Bacterial Pathogens ◽  
Bacterial Pathogen ◽  
Pcr Analysis ◽  
Simultaneous Occurrence ◽  
Marker Genes ◽  
Human Consumption ◽  
Salmonella Spp ◽  
Beef Meat ◽  
Food Borne ◽  
Meat Samples

Simultaneous occurrence of selected food-borne bacterial pathogens on bovine hides, carcasses and beef meat The aim of this study was to determine the simultaneous occurence of Salmonella spp., L. monocytogenes, verotoxigenic E. coli (VTEC), and Campylobacter spp. in slaughtered cattle and in beef meat subjected for human consumption. A total of 406 bovine hides and 406 corresponding carcasses were used to collect the samples with a swab method after exsanguination and evisceration of animals, respectively. Furthermore, 362 beef meat samples were purchased in local retail shops over the same period of time as for the bovine samples. Food-borne bacterial pathogens were identified with standard ISO methods with some modification by the use of PCR for VTEC. The isolated bacteria were then molecularly speciated (Campylobacter), serotyped (L. monocytogenes) and characterized for the presence of several virulence marker genes (VTEC and Campylobacter). It was found that 49 hide (12.1%) and 3 (0.7%) carcass samples were contaminated with more than one bacterial pathogen tested. Most of the hides were positive for Campylobacter spp. and VTEC (27 samples) and Campylobacter spp. together with L. monocytogenes (12 samples). Eight bovine hides contained L. monocytogenes and VTEC while L. monocytogenes and Salmonella spp. were detected in one sample. Furthermore, 3 pathogens (Campylobacter spp., L. monocytogenes and VTEC) were simultaneously identified in one bovine hide tested. In case of bovine carcasses 2 samples contained Campylobacter spp. and VTEC whereas one carcass was positive for L. monocytogenes and VTEC. On the other hand, 10 out of 362 (2.8%) minced beef samples were contaminated with at least two pathogens tested. The majority of these samples were contaminated with L. monocytogenes and Salmonella spp. (6 samples). It was noticed that equal number of C. jejuni and C. coli were found, irrespective of the origin of the samples. Most of the strains possessed more than one pathogenic factor as identified by PCR. Molecular serotyping of L. monocytogenes revealed that the majority of the isolates (27 out of 31; 87.1%) belonged to 1/2a serogroup. It was found that most of the VTEC isolates possessed the Shiga toxin stx2 gene (12 strains) whereas only 2 strains were stx1-positive. The eneterohemolysin and intimin markers were identified only in 7 and 2 isolates, respectively. PCR analysis revealed that 4 VTEC belonged to O91 serogroup, 2 strains were O145 and 1 isolate was identified as O113. None of the VTEC detected in the study was O157 serogroup.

scholarly journals Salmonella in food products – a vector for distribution of antibiotic resistance

2010 ◽  
Vol 31 (2) ◽  
pp. 89 ◽  
Author(s):  
Thi Thu Hao Van ◽  
Emily Teck Fong Gan ◽  
Peter M Smooker ◽  
Peter J Coloe
Keyword(s):  
Developing Countries ◽  
Antibiotic Resistance ◽  
Production Systems ◽  
Antibiotic Resistance Genes ◽  
Cost Effective ◽  
Salmonella Spp ◽  
Salmonella Infections ◽  
Food Borne ◽  
Common Causes ◽  
Production Animals

Non-typhoidal Salmonella spp. are common food-associated pathogens, and Salmonella infections are one of the most common causes of death associated with food-associated illness, especially in developing countries. As in many other developing countries, raw food hygiene and antimicrobial resistance epidemiology are in their infancy in Vietnam. In addition, the lack of stringent controls on antimicrobial usage in human health and particularly in animal production systems increases the risk of food-borne pathogens harbouring and disseminating antibiotic resistance genes. For countries such as Vietnam, Thailand and other Asian countries, Salmonella vaccination is a more cost-effective way of controlling Salmonella in food production animals than the use of antibiotic therapy.

Inhibition of Bacterial Biofilm Formation by Phytotherapeutics with Focus on Overcoming Antimicrobial Resistance

2020 ◽  
Vol 26 (24) ◽  
pp. 2807-2816 ◽  
Author(s):  
Yun Su Jang ◽  
Tímea Mosolygó
Keyword(s):  
Antimicrobial Resistance ◽  
Biofilm Formation ◽  
Antimicrobial Agents ◽  
Bacterial Biofilm ◽  
Experimental Investigations ◽  
Resistant Bacteria ◽  
Salmonella Spp ◽  
Food Borne ◽  
High Prevalence ◽  
Scientific Attention

: Bacteria within biofilms are more resistant to antibiotics and chemical agents than planktonic bacteria in suspension. Treatment of biofilm-associated infections inevitably involves high dosages and prolonged courses of antimicrobial agents; therefore, there is a potential risk of the development of antimicrobial resistance (AMR). Due to the high prevalence of AMR and its association with biofilm formation, investigation of more effective anti-biofilm agents is required. : From ancient times, herbs and spices have been used to preserve foods, and their antimicrobial, anti-biofilm and anti-quorum sensing properties are well known. Moreover, phytochemicals exert their anti-biofilm properties at sub-inhibitory concentrations without providing the opportunity for the emergence of resistant bacteria or harming the host microbiota. : With increasing scientific attention to natural phytotherapeutic agents, numerous experimental investigations have been conducted in recent years. The present paper aims to review the articles published in the last decade in order to summarize a) our current understanding of AMR in correlation with biofilm formation and b) the evidence of phytotherapeutic agents against bacterial biofilms and their mechanisms of action. The main focus has been put on herbal anti-biofilm compounds tested to date in association with Staphylococcus aureus, Pseudomonas aeruginosa and food-borne pathogens (Salmonella spp., Campylobacter spp., Listeria monocytogenes and Escherichia coli).

Antimicrobial Resistance and Presence of Class 1 Integrons Among Different Serotypes of Salmonella spp. Recovered From Children with Diarrhea in Tehran, Iran

2020 ◽  
Vol 20 (2) ◽  
pp. 160-166
Author(s):  
Seyedeh Hanieh Eshaghi Zadeh ◽  
Hossein Fahimi ◽  
Fatemeh Fardsanei ◽  
Mohammad Mehdi Soltan Dallal
Keyword(s):  
Antibiotic Resistance ◽  
Antimicrobial Resistance ◽  
Multidrug Resistant ◽  
Salmonella Spp ◽  
Class 1 Integron ◽  
Class 1 Integrons ◽  
Food Borne ◽  
Class 1 ◽  
Resistance Patterns ◽  
C 30

Background: Salmonellosis is a major food-borne disease worldwide. The increasing prevalence of antimicrobial resistance among food-borne pathogens such as Salmonella spp. is concerning. Objective: The main objective of this study is to identify class 1 integron genes and to determine antibiotic resistance patterns among Salmonella isolates from children with diarrhea. Methods: A total of 30 Salmonella isolates were recovered from children with diarrhea. The isolates were characterized for antimicrobial susceptibility and screened for the presence of class 1 integron genes (i.e. intI1, sulI1, and qacEΔ1). Results: The most prevalent serotype was Enteritidis 36.7%, followed by Paratyphi C (30%), and Typhimurium (16.7%). The highest rates of antibiotic resistance were obtained for nalidixic acid (53.3%), followed by streptomycin (40%), and tetracycline (36.7%). Regarding class 1 integrons, 36.7%, 26.7%, and 33.3% of the isolates carried intI1, SulI, and qacEΔ1, respectively, most of which (81.8%) were multidrug-resistant (MDR). Statistical analysis revealed that the presence of class 1 integron was significantly associated with resistance to streptomycin and tetracycline (p = 0.042). However, there was no association between class 1 integron and other antibiotics used in this study (p > 0.05). Conclusion: The high frequency of integron class 1 gene in MDR Salmonella strains indicates that these mobile genetic elements are versatile among different Salmonella serotypes, and associated with reduced susceptibility to many antimicrobials.

scholarly journals Animal and Human Multidrug-Resistant, Cephalosporin-ResistantSalmonella Isolates Expressing a Plasmid-Mediated CMY-2 AmpC β-Lactamase

2000 ◽  
Vol 44 (10) ◽  
pp. 2777-2783 ◽  
Author(s):  
P. L. Winokur ◽  
A. Brueggemann ◽  
D. L. DeSalvo ◽  
L. Hoffmann ◽  
M. D. Apley ◽  
...  
Keyword(s):  
Antimicrobial Resistance ◽  
Plasmid Dna ◽  
Antibiotic Use ◽  
Multidrug Resistant ◽  
Geographic Region ◽  
Chromosomal Dna ◽  
Important Food ◽  
Food Borne ◽  
Clonal Spread ◽  
Resistance Rates

ABSTRACT Salmonella spp. are important food-borne pathogens that are demonstrating increasing antimicrobial resistance rates in isolates obtained from food animals and humans. In this study, 10 multidrug-resistant, cephalosporin-resistant Salmonellaisolates from bovine, porcine, and human sources from a single geographic region were identified. All isolates demonstrated resistance to cephamycins and extended-spectrum cephalosporins as well as tetracycline, chloramphenicol, streptomycin, and sulfisoxazole. Molecular epidemiological analyses revealed eight distinct chromosomal DNA patterns, suggesting that clonal spread could not entirely explain the distribution of this antimicrobial resistance phenotype. However, all isolates encoded an AmpC-like β-lactamase, CMY-2. Eight isolates contained a large nonconjugative plasmid that could transformEscherichia coli. Transformants coexpressed cephalosporin, tetracycline, chloramphenicol, streptomycin, and sulfisoxazole resistances. Plasmid DNA revealed highly related restriction fragments though plasmids appeared to have undergone some evolution over time. Multidrug-resistant, cephalosporin-resistant Salmonellaspp. present significant therapeutic problems in animal and human health care and raise further questions about the association between antimicrobial resistance, antibiotic use in animals, and transfer of multidrug-resistant Salmonella spp. between animals and man.

scholarly journals Isolation and Characterization of Bacteriophage ZCSE6 against Salmonella spp.: Phage Application in Milk

Biologics ◽  
2021 ◽  
Vol 1 (2) ◽  
pp. 164-176
Author(s):  
Abdallah S. Abdelsattar ◽  
Anan Safwat ◽  
Rana Nofal ◽  
Amera Elsayed ◽  
Salsabil Makky ◽  
...  
Keyword(s):  
Pathogenic Bacteria ◽  
Raw Milk ◽  
Salmonella Spp ◽  
Isolation And Characterization ◽  
Food Borne ◽  
Wide Range ◽  
Almost All ◽  
And Control ◽  
Milk And Dairy Products

Food safety is very important in the food industry as most pathogenic bacteria can cause food-borne diseases and negatively affect public health. In the milk industry, contamination with Salmonella has always been a challenge, but the risks have dramatically increased as almost all bacteria now show resistance to a wide range of commercial antibiotics. This study aimed to isolate a bacteriophage to be used as a bactericidal agent against Salmonella in milk and dairy products. Here, phage ZCSE6 has been isolated from raw milk sample sand molecularly and chemically characterized. At different multiplicities of infection (MOIs) of 0.1, 0.01, and 0.001, the phage–Salmonella interaction was studied for 6 h at 37 °C and 24 h at 8 °C. In addition, ZCSE6 was tested against Salmonella contamination in milk to examine its lytic activity for 3 h at 37 °C. The results showed that ZCSE6 has a small genome size (<48.5 kbp) and belongs to the Siphovirus family. Phage ZCSE6 revealed a high thermal and pH stability at various conditions that mimic milk manufacturing and supply chain conditions. It also demonstrated a significant reduction in Salmonella concentration in media at various MOIs, with higher bacterial eradication at higher MOI. Moreover, it significantly reduced Salmonella growth (MOI 1) in milk, manifesting a 1000-fold decrease in bacteria concentration following 3 h incubation at 37 °C. The results highlighted the strong ability of ZCSE6 to kill Salmonella and control its growth in milk. Thus, ZCSE6 is recommended as a biocontrol agent in milk to limit bacterial growth and increase the milk shelf-life.

Inactivation of Salmonella Species and Other Food-Borne Pathogens with Salmide®, a Sodium Chlorite–Based Oxyhalogen Disinfectant†

1995 ◽  
Vol 58 (5) ◽  
pp. 535-540 ◽  
Author(s):  
JAIME MULLERAT ◽  
BRIAN W. SHELDON ◽  
N. ARLENE KLAPES
Keyword(s):  
Sodium Chlorite ◽  
Escherichia Coli O157 ◽  
Gram Negative Bacteria ◽  
Disodium Edta ◽  
Biocidal Activity ◽  
Salmonella Spp ◽  
Gram Positive ◽  
Gram Negative ◽  
Food Borne ◽  
Salmonella Hadar

The biocidal activity of Salmide®, a sodium chlorite–based oxyhalogen disinfectant, was tested alone or in combination with disodium ethylenediaminetetraacetate (EDTA) or trisodium phosphate (Na3PO4) against nine Salmonella spp. (choleraesuis, enteritidis, hadar, heidelberg, infantis, montevideo, indiana, typhimurium, worthington) and other selected gram-positive (Bacillus cereus, Listeria monocytogenes, Staphylococcus aureus) and gram-negative bacteria (Escherichia coli O157:H7, Pseudomonas aeruginosa). After a 15-min exposure to 10 mM Salmide® in distilled deionized water at 37°C, a 2.5-to 6.6-log-cycle reduction in population was observed for all of the 16 strains tested, with the exception of L. monocytogenes ATCC 19111, which appeared to be resistant (&lt;1-log-cycle reduction). When Salmonella hadar was simultaneously exposed to 10 mM Salmide® and 5 or 10 mM disodium EDTA at 37°C for 4 min, the biocidal activity of Salmide® was enhanced twofold (6-log-cycle reduction) compared to that observed with 10 mM Salmide® alone. Treatment with 10 mM disodium EDTA alone produced no significant inactivation &lt;1-log-cycle reduction). Exposure of Salmonella hadar to 55 mM Na3PO4 alone or in combination with 10 mM Salmide® yielded a greater than 6-log-cycle reduction, whereas treatment with 10 mM Salmide® alone yielded a4.1-log-cycle reduction. The presence of protein (as bovine serum albumin) in treatments containing Salmide® significantly reduced the biocidal activity. These results demonstrate that Salmide® has a rapid and concentration-dependent biocidal activity against both gram-positive and gram-negative food-borne bacterial pathogens and spoilage organisms.

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