Source: UNIVERSITY OF ARIZONA submitted to NRP
MOLECULAR EPIDEMIOLOGY, IN VITRO AND IN VIVO ANALYSES OF VETERINARY CLOSTRIDIUM DIFFICILE STRAINS IN SOUTHERN ARIZONA
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1014237
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Oct 1, 2017
Project End Date
Sep 30, 2022
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
UNIVERSITY OF ARIZONA
888 N EUCLID AVE
TUCSON,AZ 85719-4824
Performing Department
Animal & Comparative Biomedical Sciences
Non Technical Summary
Clostridium difficile is an important pathogen of both human and veterinary populations. In humans, it is the leading healthcare-associated infection in the United States. Clostridium difficile (CD) is a gram-positive, anaerobic, spore-forming bacillus that colonizes the gastrointestinal tract and causes diarrhea which, in some cases, can progress to pseudomembranous colitis, toxic megacolon and death. Risk factors in both human and veterinary populations include age, microbiota status, and prior antibiotic treatment. Disease- causing strains of CD produce 1-3 toxins that enter intestinal epithelial cells and glucosylate or ribosylate Rho family GTPases, leading to cell death. Though it is increasingly appreciated that factors other than the toxins play a role in disease, the identity of such factors, and their functions, remain to be defined.Since the year 2000, new "epidemic-" and outbreak-associated" strains of CD have emerged that cause more severe disease with higher mortality. These strains have been found in many North American communities. CD is also established in food animals, and is a significant problem in the agriculture industry, with non-human neonates (piglets, calves and foals) being particularly affected. These animals are all susceptible to CD infection (CDI) within 1-14 days of birth, and disease manifestation resembles that in humans. Worryingly, the greatest numbers of CD isolates are recovered from suckling piglets inside the farrowing barn. Further, particular molecular types of CD found in pigs have been recovered from human patients. On some farms, up to 75% of all piglets carry CD, and many of these CD strains are resistant to multiple antibiotics. Specifically, since the immune system is un- or under-developed at this time-frame, classic approaches such as vaccination are not used for disease prevention in agriculturally-relevant neonates. Ironically, only antibiotic treatment is considered for suckling piglets [erythromycin, tylosin or tetracycline]; these will further delay the development and establishment of a healthy gastrointestinal microbiota. Neonates are lost in high numbers if symptomatic, and those that survive infection are asymptomatically colonized, and shed CD to further contaminate the environment, and potentially, food sources. Recent findings are suggestive of zoonotic spread, with food-borne transmission of CD spores as a hypothesized route for human infection. Epidemic-associated CD spores, such as those of ribotype 078, may thus be introduced into hospitals by patients infected in the community.In Arizona, the last published CD infection (CDI) surveillance in humans was done 18 years ago. In the past 5 years, and in collaboration with colleagues at multiple Tucson-area hospitals, we have re- initiated robust surveillance efforts; these are currently ongoing. Sampling of the veterinary population in Arizona has also been extremely limited and sporadic, and there have been no standardized surveillance efforts. Therefore, and commencing in early this year (2017), we began tracking and collecting CD isolates from farm-based piglets in Southern Arizona. From this recent (and ongoing) surveillance, we conclude that "hypervirulent" veterinary strains (Ribotype 078) are present in significant levels in piglets the region. Importantly, we have also found the same Ribotype 078 strains in our recent human surveillance; their recovery from human patients is highly suggestive of CD's zoonotic potential. Thus, our current collection of these recent CD isolates of both human and veterinary origin presents a unique opportunity for in-depth, clinically-relevant, molecular analyses.In this proposal, we will therefore perform comparative analyses of CD strains of recent veterinary origin with the goal of understanding the molecular determinants that confer disease and species-specificity.
Animal Health Component
(N/A)
Research Effort Categories
Basic
100%
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
31135101100100%
Knowledge Area
311 - Animal Diseases;

Subject Of Investigation
3510 - Swine, live animal;

Field Of Science
1100 - Bacteriology;
Goals / Objectives
In this project, we will perform comparative analyses of Clostridium difficile (C. difficile; CD) strains of recent veterinary origin with the goal of understanding the molecular determinants that confer disease and species-specificity. This proposal draws on our various strengths and resources. Most importantly, we have a collection of veterinary C. difficile isolates collected in Arizona. We also have extensive expertise in cutting-edge omics approaches, as well as in vitro and in vivo host- pathogen interaction studies.The overarching goal of this project, therefore, is to evaluate the in vitro and in vivo attributes of specific C. difficile (CD) strains of veterinary origin. The Specific Objectives will be to determine if our veterinary clinical samples:• Encode all known CD toxin genes (toxin A, toxin B, and binary toxin)• Express or produce measurable and functional amounts of these toxins• Adhere to human and porcine intestinal epithelial cells• Express antibiotic resistance• Contain unique genetic signatures• Are virulent in animal models of severe C. difficile disease
Project Methods
I. In vitro studies to assess Clostridium difficile (CD) toxin gene presence, toxin production, CD adherence, CD antibiotic susceptibility and genomic signatures:Stool samples will be plated on selective media (TCCFA) to isolate CD. Pure culture of CD in brain-heart infusion will grow for 72 hours, after which supernatant will be collected. Toxin production will be measured using the supernatant on a commercially available toxin A/B ELISA kit as we have previously performed. Detection of CD toxin genes tcdA, tcdB, cdtA, and cdtB will be done using polymerase chain reaction amplification of the genes, also as we have previously performed. Crude template will be prepared from pure colonies using a standard colony lyse solution. Amplicons will be separated on 1% agarose. Adherence will be measured as previously described; both human (C2BBE) and neonatal porcine intestinal epithelial (IEC) cell lines will be used. Antibiotic susceptibility testing [erythromycin, tetracycline, ciprofloxacin, vancomycin (human and veterinary antimicrobials)] will be determined through growth media supplemented with antibiotics in serial dilution as we have previously performed, and then confirmed through PCR amplification of suspected resistance genes. Strains that are found to be most virulent from the studies above will be used for genomics. Whole-cell DNA will be extracted from these strains, and sequenced using an Illumina platform at the University of Arizona's Core Genomics facility.II. In vivo studies to assess CD virulence in animal models for severe CDI:CD strains will be tested in the Syrian golden hamster model of C. difficile infection as we have previously performed and published. In brief, animals will be sensitized to CD infection with a single oral administration of clindamycin (30mg/kg; similar to humans). 3-5 days post-antibiotic, animals will be challenged with 100 spores of veterinary CD. This is a lethal infection model, and death usually occurs within 48-96 hours post-challenge. CDI symptoms will be monitored (diarrhea, inappetence, weight loss), and CD burden quantitated in fecal material, and in cecal contents upon necropsy. We will also perform neonatal piglet infections with at least two recent veterinary-origin (Ribotype 078) CD strains. Studies will involve CD challenges of ~5-day-old piglets obtained from a high health-status herd housed south of Tucson; we currently work with this farm as part of our regular veterinary CD surveillance. CD challenge will include 103-5 spore administrations with two well-described veterinary-associated strains (Ribotype 078). Disease symptoms will be monitored and time-to- death or recovery documented similar to parameters measured in Syrian hamsters. Piglets will be housed at the UA Central Animal Facility according to Dr. Vedantam's current and approved IACUC Protocol.

Progress 10/01/19 to 09/30/20

Outputs
Target Audience:The target audience is the scientific community at the local, state and national level. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?A laboratory scientist and a graduate student were fully trained in all aspects of bacterial whole genome sequencing as well as rodent models of C.difficile infection. How have the results been disseminated to communities of interest?Local seminars, student poster session and invited presentation by the PD. What do you plan to do during the next reporting period to accomplish the goals?We will ramp up our efforts to begin neonatal piglet infections with C.difficile isolatesof relevantmolecular types, and we will also complete whole genome sequencingandanalyses of additional, contemporary C. difficile strains of different ribotypes.

Impacts
What was accomplished under these goals? We completed the whole genome sequencing and phylogenetic analysis of >70 Clostridioides difficile strains of diverse origin. Specifically, we obtained isolates of C. difficile, performed molecular fingerprinting on all of these (Ribotyping) and also quantitated total toxin production and biofilm formation for a subset of them. We then subjected diverse ribotypes (multiple isolates in each) to Illumina platform-based genome sequencing. Data analysis was performed in house. We identified unique genetic signatures on Ribotype 106, and other, strains. These are currently being intensively characterized. Prior to moving on to the neonatal piglet studies of this proposal, we performed enabling studies to characterize the isolates in a rodent model so that we could optimize parameters for larger animal studies. Therefore, we performed Golden Syrian hamster studies of acute C.difficile infection, and established LD50 as well as kinetics of infection for a subset of the new isolates we obtained - and those which we anticipate will be used as challenge strains for piglets in the coming year.We have also completed all required in vitro studies such that we can now transition to the final phase of intensive in vivo interrogation of these strains in our neonatal piglet model. For these latter studies, we have also established a relationship with a local, high-herd-health, non-GMO swine farm outside Tucson, and have completed an agreement wherein newborn piglets will be provided as required to our newly-remodeled, BSL-2 vivarium space that has been dedicated for neonatal swine infection studies.

Publications


    Progress 10/01/18 to 09/30/19

    Outputs
    Target Audience:1. Research communities engaging in bacteriology/molecular microbiology projects 2. Clinicians and veterinarians assessing Clostridium difficile infection in their respective practices Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?An undergraduate and a graduate student were both trained in all aspects of C. difficile recovery, antibiotic testing, DNA sequencing, and molecular fingerprinting (ribotyping). How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals?Aim 1 studies are largely complete. We will wrap up the full in vitro characterization of relevant veterinary-origin C. difficile isolates by testing adherence to host cells, and performing intoxication studies. We will also commence some pilot in vivo studies (hamster model of C. difficile infection) using a subset of the isolates that we whole genome-sequenced.

    Impacts
    What was accomplished under these goals? We undertook a major genome sequencing project in 2019 to begin assessment of unique genetic signatures of clinical isolates of Clostridioides difficile. In concert, we also performed fully-quantitative proteomics for a subset of the isolates, so as to correlate genome and expressed molecules, specifically the toxins as well as other known virulence factors of this pathogen. The data are still being analyzed at the time of submission of this report given COVID-related constraints. However, the actual sequencing of >100 unique strains is complete, as is all the proteomics experimental setup. In summary, we have observed that C. difficile strains known to be associated with clinical outbreaks harbor 1-3 large genetic islands, all of which contain mobile elements. Each island ranges in size from 29-49 kb, and contains genes known to be involved, or modulate, virulence, antibiotic resistance or conjugation-based gene transfer. Some of these genes are also robustly expressed as demonstrated in partner proteomics studies. In addition to the above, we also completed antibiotic resistance testing for 21 unique isolates of C. difficile. Each isolate was tested against a panel of 16 clinically-utilized antibiotics using standard (CLSI-approved) MIC testing. We observed that many of the isolates exhibited a multidrug-resistant phenotype, with some displaying high levels of resistance to erythroromycin, tetracycline, cephamycin and three different fluoroquinolones (levofloxacin, moxifloxacin and ciprofloxacin). Specifically, for one drug - tigecycline - we also observed an inducible resistance, which we conformed experimentally.

    Publications


      Progress 10/01/17 to 09/30/18

      Outputs
      Target Audience:1. Bacteriology-focused research communities 2. Clinicians and veterinarians assessing Clostridium difficile infection in their respective practices Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?An undergraduate and a graduate student were both trained in all aspects of CD recovery, propagation and molecular fingerprinting (ribotyping). These individuals also compiled data for the Biobank and for our internal ribotyping databases. How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals?We will complete AIm 1 studies, i.e. the full in vitro characterization of relevant veterinary-origin CD isolates by testing adherence to host cells, intoxication studies, antibiotic susceptibility testing and whole genome sequencing.

      Impacts
      What was accomplished under these goals? Aim 1 of the current project was focused on enabling in vitro tests in this past year. Specifically, we studied multiple environmentally-relevant isolates of Clostridium difficile (CD) obtained from various geographic locations in Southern Arizona in order to optimize testing protocols, develop a biobank of typed isolates as reference strains, and expand our in-house databases so that all enabling information required for the project would be in place as we ramp up in Year 2. For these isolates, we performed multiple in vitro studies to assess toxin gene presence, toxin production, and CD phylogenetic typing. Samples were plated on selective media (TCCFA) to isolate CD. Pure culture of CD were futher propagated in Brain-Heart Infusion medium Supplemented with yeast extraxt (BHIS) for 72 hours, after which supernatant were harvested, and total toxin determined using a ToxA/ToxB ELISA kit. Detection of CD toxin genes tcdA, tcdB, cdtA, and cdtB was done using polymerase chain reaction amplification of the genes. For these studies, crude template was prepared from pure colonies using a standard colony lyse solution, and toxin genes amplified using the primers: tcdA - YT28/YT29; tcdB - YT17/YT18, cdtA - cdtApos/cdt-Arev, cdtB - cdtBpos/cdtBrev. Amplicons were separated on 1% agarose and visualized by SYBR-Green staining. For phylogenetic typing, and PCR method was used, and primers amplified the intergenic region between the 16s and 23s rDNA genes in CD. Amplicons result in a characteroistic banding pattern when electrophoresed; these represent various phylogenetic clades (Ribotypes) of CD. Using these methods, we studied all CD isolates recovered during the past reporting period. Of these, we showed that approximately 40% were toxigenic; i.e. they contained the toxin genes tcdA and tcdB. Based on ribotyping, the dominant ribotype in our study was the virulent NAP1/RT027 clade, followed by the NAP11/RT106 clade. Importantly, we have also completed all setup and testing of a whole genome sequencing pipeline, including platforms for rapid annotation of sequences. This will greatly facilitate the genome sequencing studies proposed for this project.

      Publications