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Food Microbiology | Spotlight

Coadministration of the Campylobacter jejuni N-Glycan-Based Vaccine with Probiotics Improves Vaccine Performance in Broiler Chickens

H. Nothaft, M. E. Perez-Muñoz, G. J. Gouveia, R. M. Duar, J. J. Wanford, L. Lango-Scholey, C. G. Panagos, V. Srithayakumar, G. S. Plastow, C. Coros, C. D. Bayliss, A. S. Edison, J. Walter, C. M. Szymanski
Johanna Björkroth, Editor
H. Nothaft
aDepartment of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada
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M. E. Perez-Muñoz
bDepartment of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, Canada
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G. J. Gouveia
cDepartments of Genetics and Biochemistry and Molecular Biology, University of Georgia, Athens, Georgia, USA
dComplex Carbohydrate Research Center, University of Georgia, Athens, Georgia, USA
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R. M. Duar
bDepartment of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, Canada
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  • ORCID record for R. M. Duar
J. J. Wanford
eDepartment of Genetics and Genome Biology, University of Leicester, Leicester, United Kingdom
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L. Lango-Scholey
eDepartment of Genetics and Genome Biology, University of Leicester, Leicester, United Kingdom
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C. G. Panagos
dComplex Carbohydrate Research Center, University of Georgia, Athens, Georgia, USA
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V. Srithayakumar
bDepartment of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, Canada
fLivestock Gentec, Edmonton, Alberta, Canada
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G. S. Plastow
bDepartment of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, Canada
fLivestock Gentec, Edmonton, Alberta, Canada
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C. Coros
gDelta Genomics, Edmonton, Alberta, Canada
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C. D. Bayliss
eDepartment of Genetics and Genome Biology, University of Leicester, Leicester, United Kingdom
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A. S. Edison
cDepartments of Genetics and Biochemistry and Molecular Biology, University of Georgia, Athens, Georgia, USA
dComplex Carbohydrate Research Center, University of Georgia, Athens, Georgia, USA
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J. Walter
aDepartment of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada
bDepartment of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, Alberta, Canada
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C. M. Szymanski
aDepartment of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada
dComplex Carbohydrate Research Center, University of Georgia, Athens, Georgia, USA
hDepartment of Microbiology, University of Georgia, Athens, Georgia, USA
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Johanna Björkroth
University of Helsinki
Roles: Editor
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DOI: 10.1128/AEM.01523-17
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  • FIG 1
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    FIG 1

    Comparison of responder and nonresponder groups of SPF leghorn and broiler chickens after vaccination. (A) Colonization levels of C. jejuni 81-176. Birds in the negative-control group (PBS) were nonvaccinated and nonchallenged; birds in the positive-control groups (Cj) were nonvaccinated but challenged with either 1 × 102 CFU (in leghorn chickens) or 1 × 106 CFU (in broiler chickens) of C. jejuni 81-176 on day 28. Birds in the treatment groups (n = 6 for leghorn and broiler chickens) were given 1 × 108 cells of the E. coli vaccine (Ec) by oral gavage on days 7 and 21 and challenged with either 1 × 102 CFU (leghorn chickens) or 1 × 106 CFU (broiler chickens) C. jejuni 81-176 on day 28. Lines represent the median levels of colonization. (B) The gut microbiota in cecal samples of leghorn (top) and broiler (bottom) chickens obtained on the day of euthanasia were compared at the family level. Although both strains share taxonomic groups, their abundances differ between the strains. Members of Clostridiaceae family 1 dominate the gut microbiome of leghorn chickens, while Enterobacteriaceae dominate the gut microbiome of broiler chickens. (C) Analysis of alpha diversity indexes between the indicated (circled in panel A) responder groups (n = 4 leghorn chickens and n = 2 broiler chickens) and nonresponder groups (n = 2 leghorn chickens and n = 4 broiler chickens) in each experiment shows that both leghorn (top) and broiler (bottom) responders have higher alpha diversity indexes. Statistics were analyzed by an unpaired t test with Welch's correction. Lines and bars represent means and standard deviations.

  • FIG 2
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    FIG 2

    Vaccination and challenge experiments with broiler chickens. (A) Colonization levels of C. jejuni 81-176. Birds in the negative-control group (PBS) (n = 4) were nonvaccinated and nonchallenged; birds in the positive-control groups (Cj) (n = 9) were nonvaccinated but challenged with 1 × 106 CFU of C. jejuni 81-176 on day 28. Treatment groups (n = 9) included birds that were given 1 × 108 cells of the E. coli vaccine (Ec) or 1 × 108 cells of the E. coli vaccine in combination with 1 × 108 CFU of A. mobilis (EcAm) or 1 × 108 CFU L. reuteri CSF8 (EcLr) by oral gavage on days 7 and 21. (B) Additional control experiment demonstrating colonization levels of C. jejuni 81-176 in birds given 1 × 108 CFU of A. mobilis (Am) or 1 × 108 CFU of L. reuteri CSF8 alone (Lr) by oral gavage on days 7 and 21. (C) E. coli vaccine persistence in broiler chickens. E. coli fecal shedding was inspected by using cloacal swabs taken prior to the first and second vaccine feedings (days 6 and 13) as well as on the indicated days after vaccination for the following treatment groups: Ec (black bars), EcAm (white bars), and EcLr (gray bars). The PBS, Cj, Am, and Lr groups were all negative for the E. coli vaccine strain (not shown). Vaccine persistence is expressed as a percentage of positive birds within each group with detectable colonies on selective plates. (D) Weight gain of broilers. The average weight gain of the birds in the indicated groups during the vaccination and challenge experiments is shown. Black bars indicate weight gain (percent) over 23 days (day 8 to day 31); white bars show weight gain (percent) over 27 days (day 8 to day 35). Error bars represent the standard deviations within each group. Actual weights are listed in Table S2 in the supplemental material. (E and F) N-glycan-specific antibody responses. ELISA results comparing chicken sera from bleeds performed prior to C. jejuni challenge (day 28) (E) and at day 35 (F) are shown. Each point represents the antibody response measured as the optical density at 450 nm (OD450) for each individual chicken from the indicated groups. Gray bars represent the medians for each group. No N-glycan-specific antibodies were detected in sera from blood samples taken on day 1 and in sera of groups that received A. mobilis or L. reuteri alone (not shown). Statistically significant differences (if present) between groups with P values of <0.05 are indicated by an asterisk.

  • FIG 3
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    FIG 3

    Effect of the vaccine and the selected probiotics, L reuteri and A. mobilis, on the microbial communities in broiler ceca. (A) NMDS analysis based on the Bray-Curtis distance for the standard vaccine (Ec group) compared to controls for broilers shows that, as previously shown for leghorn birds (36), microbial communities from Ec broilers cluster with those from negative controls (PBS). (B and C) Likewise, analysis of beta diversity measured by both Bray-Curtis dissimilarity and unweighted UniFrac distances confirms that coadministration of the probiotics (A. mobilis and L. reuteri) with the vaccine, although significantly different from the Cj group, does not cause significant changes in the overall composition of the chicken gut microbiota compared to the PBS (not vaccinated, not challenged) group. (D) Administration of the E. coli vaccine with and without the probiotics significantly decreases the abundance of C. jejuni. (E, top) Analysis of alpha diversity indexes for the Ec group shows higher alpha diversity indexes in responders (n = 4) than in nonresponders (n = 5). (Bottom) This trend was also seen in the combined analysis of all responders (n = 16) and nonresponders (n = 11) for all treatments under investigation. (F) Analysis of families in the gut microbiome of responders and nonresponders from all treatment groups shows that members of the order Clostridiales (Peptostreptococcaceae and Lachnospiraceae) are affected by vaccine treatment. (G) Reductions in the abundances of C. jejuni occur in parallel with increases in the abundances of Clostridium species for the responder group; specifically, the abundances of OTU25 (Clostridium glycolicum-C. bartlettii-C. metallolevans) and OTU8 (Clostridium difficile) are higher in responders than in nonresponders. Statistics were analyzed by an Adonis test (A and B), one-way ANOVA with multiple comparisons using Benjamini-Hochberg FDR correction (C and D), and Grubbs' test for the removal of outliers followed by an unpaired t test with Welch's correction (E to G). Lines represent means and standard deviations. For panels C and D, the top P value is the P value for overall ANOVA, and letters represent P values for individual comparisons, as specified by the bars.

  • FIG 4
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    FIG 4

    Hierarchical clustering analysis of phase-variable expression states in C. jejuni 81-176 isolates from control and nonresponder broiler chickens. The expression states of each gene (CJJ81176 [gene numbers as indicated]) were determined by analysis of the poly(G) repeat tracts of 28 to 30 colonies per cecal sample and utilized for calculation of the fraction of colonies in an “on” state (color-coded as indicated by the sliding bar on the right). Hierarchical clustering was performed using the percent “on” states for 19 genes and 21 samples. The phylogenetic trees are shown for the genes (top) and samples (left). There are 7 chicken samples that cluster reasonably closely to the gavage samples (orange lines in the tree). These samples are a mix of control (n = 3) and vaccine (n = 4) samples. The other samples are dispersed, with no obvious clustering of control or vaccine samples. This suggests that no specific pattern of phase-variable gene expression is associated with the persisters in the vaccine group and that variation in the vaccinated birds is not different from that in the controls. The hierarchical clustering analysis for the genes indicates three clusters. On the left are the genes that are off (low percent “on”) in most samples (red), and on the right are the genes that are on (high percent “on”) in most samples. In the middle are genes that show a more variable pattern across the samples. Within the latter set are 5 genes in 81-176 (homologs in C. jejuni NCTC11168 are in parentheses): CJJ81176_0086 (no homolog), CJJ81176_1160 (Cj1143), CJJ81176_1312 (Cj1295), CJJ81176_1419 (Cj1420c), and CJJ81176_1421 (Cj1422c) (GenBank accession number CP000538.1 ).

  • FIG 5
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    FIG 5

    NMR metabolomics. (A) PCA plot of aligned, normalized, and scaled data showing high overlap, large intragroup variability, and little separation across principal component 1 (PC1) and PC2. (B) Spectral overlay of averaged spectra within each group indicating a metabolite-rich spectrum with an expanded region of interest between 2.5 and 5 ppm. The C. jejuni posttreatment count has been integrated into the spectra at 10 ppm. (C) STOCSY output displaying correlation as color and covariance as peak height. Asterisks denote negative correlations with the C. jejuni count Driver peak (correlations, −0.60, −0.68, −0.68, −0.70, and −0.60, respectively, from left to right). (D) Expansion of 5 ppm denoting the different study groups as labeled in panel E. (E) Integral distribution of the 5-ppm feature and ANOVA indicating a significant difference between the nonvaccinated but challenged Cj group and the vaccinated and challenged EcAm group (P = 0.025). There were no significant differences between the other groups.

Tables

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  • TABLE 1

    Increases in relative abundances of operational taxonomic units between responders and nonresponders observed in both SPF leghorn and broiler chickens

    OTUOrganismFold increase in relative abundance
    Leghorn chickensBroiler chickens
    RespondersNonrespondersRespondersNonresponders
    13 Anaerosporobacter mobilis IMSNU 400116.57423.12742.31230.0013
    8 Clostridium tertium DSM 24857.19882.48872.65011.1177
    10 Klebsiella pneumoniae DSM 301045.99752.774522.381018.3039
  • TABLE 2

    Decreases in relative abundances of operational taxonomic units between responders and nonresponders observed in both SPF leghorn and broiler chickens

    OTUOrganismFold decrease in relative abundance
    Leghorn chickensBroiler chickens
    RespondersNonrespondersRespondersNonresponders
    7 Anaerostipes caccae L1-921.253419.04571.78584.4762
    29 Bifidobacterium pseudolongum JCM 58200.07830.29220.05550.1021
    2 Escherichia-Shigella flexneri X969635.72139.433512.750418.4703
    14 Lactobacillus fermentum-Lactobacillus mucosae CCUG 431790.09830.21541.12041.4731
    9 Lactobacillus reuteri L235070.18970.66023.06255.5524
  • TABLE 3

    Differences in the relative abundances of significant OTUs between controls and vaccinated broilers

    OTUOrganism(s)% identityFold change in relative abundance for groupP value
    PBSCjEcEcLrEcAm
    OTU_11 Campylobacter jejuni subsp. jejuni-Campylobacter subantarcticus1000.21443.61701.10090.73572.22920.0075
    OTU_13 Proteus mirabilis 1000.00060.09434.07374.95390.6917<0.0001
    OTU_15 Enterococcus casseliflavus-Enterococcus faecium-Enterococcusgallinarum-Enterococcusdispar-Enterococcus canintestini1002.41720.99821.31401.41331.32260.0389
    OTU_16 Enterococcus cecorum 1004.64692.82681.71851.87451.10140.0008
    OTU_20 Ruminococcus sp.-Blautia sp.98.70.15620.53810.29190.75080.54640.0157
    OTU_21 Clostridium paraputrificum 1000.56220.50250.05240.36060.05480.0410
    OTU_24 Weissella paramesenteroides 1000.64530.17610.38110.23470.05840.0304
    OTU_33 Escherichia coli-Shigella dysenteriae99.572.82631.85721.96892.13613.89450.0311
    OTU_34 Corynebacterium variabile 1000.04090.06580.02590.01240.00710.0147
    OTU_37 Corynebacterium sp.1000.01380.01750.00920.01250.00390.0258
    OTU_4 Blautia hydrogenotrophica-Ruminococcus hydrogenotrophicus94.644.923511.643211.520820.971016.13440.0064
    OTU_47 Achromobacter spanius-Achromobacter xylosoxidans-Achromobacterpiechaudii-Achromobacter marplatensis-Alcaligenes faecalis-Collimonas sp.1000.00000.00030.00130.00110.00030.0462
    OTU_56 Clostridium clostridioforme 95.710.00060.00080.00000.00080.00200.0139
    OTU_57 Sanguibacter inulinus 1000.00400.00020.00020.00030.00000.0012
    OTU_59 Pseudomonas geniculata-Stenotrophomonas maltophilia-Xanthomonas sp.-Pectobacterium carotovorum subsp. carotovorum1000.00170.00420.00600.00030.00000.0076
    OTU_61 Brevibacterium stationis-Corynebacterium sp.1000.00000.00000.00030.00220.00000.0268
    OTU_7 Weissella cibaria-Weissellaconfusa1008.53463.52793.28512.87293.23140.0411
    OTU_80 Clostridium aldenense 98.070.71100.63453.10514.04954.39840.0040
  • TABLE 4

    Primers for 81-176 poly(G)-containing genes

    GeneNCTC11168 homologaPrimerPrimer sequence
    CJJ81176_0082Cj0044c81176-0082-fwdGGTTTTACACTAGAACACAGAAG
    81176-0082-fwd-FAMFAM-GGTTTTACACTAGAACACAGAAG
    81176-0082-revCCATACACGAAGAACTTGTTAGCAA
    CJJ81176_0086NA81176-0086-fwdGCACAAGCTACAAATTTAGAAGTG
    81176-0086-fwd-FAMFAM-GCACAAGCTACAAATTTAGAAGTG
    81176-0086-revAAGTAGAAGCATTAGGCGTGGAT
    CJJ81176_0206Cj017181176-0206-fwdTGTTGTGGAAATGGAGTGCATTC
    81176-0206-fwd-NEDTGGTTGTGGAAATGGAGTGCATTC
    81176-0206-revAATAGCTCCTTCATTGCATAGTTC
    CJJ81176_0590Cj056581176-0590-fwdGCTATAGTGTTGATGTGTAGTTTGT
    81176-0590-fwd-FAMFAM-GCTATAGTGTTGATGTGTAGTTTGT
    81176-0590-revCCTTTATCAATTTCTATTCTTAGAC
    CJJ81176_0646Cj061781176-0646-fwdTGGTATAATGCAAGCTATGG
    81176-0646-fwd-VICTGGTATAATGCAAGCTATGG
    81176-0646-revAAATCAATACTCCAAGGAGC
    CJJ81176_0708Cj068581176-0708-fwdGATAGCGAATATAACCTCTAAATTC
    81176-0708-fwd-FAMFAM-GATAGCGAATATAACCTCTAAATTC
    81176-0708-revGAAGAAATCCGCCAATCAAAGGCC
    CJJ81176_0758Cj073581176-0758-fwdGCAAACCAAGCATAGGGGATTGTGG
    81176-0758-fwd-FAMFAM-GCAAACCAAGCATAGGGGATTGTGG
    81176-0758-revTTCACCATCAAAAGCTACAGATCCTG
    CJJ81176_0765NA81176-0765-fwdTGCAAGAGCTGTTCATCGGTTTAAAC
    81176-0765-fwd-NEDTGCAAGAGCTGTTCATCGGTTTAAAC
    81176-0765-revCTTAAAAGGGGATTAAATAAAGGAT
    CJJ81176_1160Cj114381176-1160-fwdCGATGCCAAGAAGCTTTATAAGAGTT
    81176-1160-fwd-FAMFAM-CGATGCCAAGAAGCTTTATAAGAGTT
    81176-1160-revGCTTGTAGTATTTTCACTCCTTGAGAT
    CJJ81176_1312Cj129581176-1312-fwdTTCCTATCCCTAGGAGTATC
    81176-1312-fwd-NEDTTCCTATCCCTAGGAGTATC
    81176-1312-revATAGGCTTCTTTAGCGTTCC
    CJJ81176_1321Cj1305c81176-1321-27-fwdCAACTTTTATCCCACCTAATGGAG
    81176-1321-27-fwd-VICCAACTTTTATCCCACCTAATGGAG
    81176-1321-revGTGGAAAATCTTCATAATATTCACTG
    CJJ81176_1325NA81176-1325-fwdGCTTGATGATAATTTTACCGCCTTAAG
    81176-1325-revCAATCTAGCCTTAGGCACTCCGATT
    CJJ81176_1327NA81176-1325-fwd-FAMFAM-GCTTGATGATAATTTTACCGCCTTAAG
    81176-1327-revTCTCAATAACGGCAAAACAGTTCCC
    CJJ81176_1341Cj134281176-1341-fwdGGTAATCGTCCTCAAACAGG
    81176-1341-fwd-FAMFAM-GGTAATCGTCCTCAAACAGG
    81176-1341-revGCCAAATGCGCTAAATATCC
    CJJ81176_1419Cj1420c81176-1419-fwdGCTAGTTCTTTCCATTGGAC
    81176-1419-fwd-FAMFAM-GCTAGTTCTTTCCATTGGAC
    81176-1419-revTGCCACTGCTTACACGAGCAAG
    CJJ81176_1421Cj1422c81176-1421-35-revTTGAGCTGAGGAAAGATTTGTATAG
    81176-1421-fwdTATTGGTGTGCCTGAGGATTATTAT
    81176-1421-fwd-VICTATTGGTGTGCCTGAGGATTATTAT
    CJJ81176_1429Cj1429c81176-1429-fwdCTCCTATTCTTTCAGAACGTGATAT
    81176-1429-fwd-FAMFAM-CTCCTATTCTTTCAGAACGTGATAT
    81176-1429-revCTATGCTAGCATCATATTCAATTACC
    CJJ81176_1432Cj113881176-1432-fwdCTAGGACAGGCTTTGATTATAAATTC
    81176-1432-fwd-VICCTAGGACAGGCTTTGATTATAAATTC
    81176-1432-revCACCATCATCTCTAACAGATATAAAT
    CJJ81176_1435NA81176-1435-fwdATCTTAATACCTGATTTTATCAAAAC
    81176-1435-fwd-NEDATCTTAATACCTGATTTTATCAAAAC
    • ↵a NA, not applicable (no homolog in NCTC11168).

Additional Files

  • Figures
  • Tables
  • Supplemental material

    • Supplemental file 1 -

      Cloacal swab cell counts on L. reuteri isolation medium (Fig. S1); relative abundances of bacteria of interest for all treatments and for responders and nonresponders (Fig. S2); correlations to the driver peak at 5 ppm (Fig. S3); strains used in in vivo probiotic selection experiments (Table S1); weight gain in broilers (Table S2); multiplex primer mix (Table S3); distribution of five gene phasotypes between control and vaccinated challenge groups (Table S4); multivariate analysis parameters, list of PCs for PCA and PLS-DA, and classification and fit measurements Q2 and R2 (Table S5); metabolite database matching using COLMARm and ASSURE NMR (Table S6).

      PDF, 288K

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Coadministration of the Campylobacter jejuni N-Glycan-Based Vaccine with Probiotics Improves Vaccine Performance in Broiler Chickens
H. Nothaft, M. E. Perez-Muñoz, G. J. Gouveia, R. M. Duar, J. J. Wanford, L. Lango-Scholey, C. G. Panagos, V. Srithayakumar, G. S. Plastow, C. Coros, C. D. Bayliss, A. S. Edison, J. Walter, C. M. Szymanski
Applied and Environmental Microbiology Nov 2017, 83 (23) e01523-17; DOI: 10.1128/AEM.01523-17

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Coadministration of the Campylobacter jejuni N-Glycan-Based Vaccine with Probiotics Improves Vaccine Performance in Broiler Chickens
H. Nothaft, M. E. Perez-Muñoz, G. J. Gouveia, R. M. Duar, J. J. Wanford, L. Lango-Scholey, C. G. Panagos, V. Srithayakumar, G. S. Plastow, C. Coros, C. D. Bayliss, A. S. Edison, J. Walter, C. M. Szymanski
Applied and Environmental Microbiology Nov 2017, 83 (23) e01523-17; DOI: 10.1128/AEM.01523-17
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KEYWORDS

Bacterial Vaccines
Campylobacter Infections
Campylobacter jejuni
chickens
polysaccharides
Poultry Diseases
probiotics
Campylobacter
poultry
probiotics
vaccine
glycoengineering
metabolomics

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Print ISSN: 0099-2240; Online ISSN: 1098-5336