Submitted Successfully!
Thank you for your contribution! You can also upload a video entry or images related to this topic.
Ver. Summary Created by Modification Content Size Created at Operation
1 + 2477 word(s) 2477 2021-11-15 05:24:16 |
2 Format change Meta information modification 2477 2021-11-16 04:26:47 |

Video Upload Options

Do you have a full video?


Are you sure to Delete?
If you have any further questions, please contact Encyclopedia Editorial Office.
Elgamoudi, B. Campylobacter Biofilms. Encyclopedia. Available online: (accessed on 28 November 2023).
Elgamoudi B. Campylobacter Biofilms. Encyclopedia. Available at: Accessed November 28, 2023.
Elgamoudi, Bassam. "Campylobacter Biofilms" Encyclopedia, (accessed November 28, 2023).
Elgamoudi, B.(2021, November 16). Campylobacter Biofilms. In Encyclopedia.
Elgamoudi, Bassam. "Campylobacter Biofilms." Encyclopedia. Web. 16 November, 2021.
Campylobacter Biofilms

Microbial biofilms occur naturally in many environmental niches and can be a significant reservoir of infectious microbes in zoonotically transmitted diseases such as that caused by Campylobacter jejuni, the leading cause of acute human bacterial gastroenteritis world-wide. The greatest challenge in reducing the disease caused by this organism is reducing transmission of C. jejuni to humans from poultry via the food chain. Biofilms enhance the stress tolerance and antimicrobial resistance of the microorganisms they harbor and are considered to play a crucial role for Campylobacter spp. survival and transmission to humans. Unconventional approaches to control biofilms and to improve the efficacy of currently used antibiotics are urgently needed. This review summarizes the use plant- and microorganism-derived antimicrobial and antibiofilm compounds such as essential oils, antimicrobial peptides (AMPs), polyphenolic extracts, algae extracts, probiotic-derived factors, d-amino acids (DAs) and glycolipid biosurfactants with potential to control biofilms formed by Campylobacter, and the suggested mechanisms of their action. Further investigation and use of such natural compounds could improve preventative and remedial strategies aimed to limit the transmission of campylobacters and other human pathogens via the food chain.


1. Campylobacter spp. Biofilm Formation and Regulation

The formation of biofilms significantly increases the ability of C. jejuni to survive in extreme conditions [1][2]. For instant, biofilm encased campylobacter cells survive twice as long under atmospheric conditions, and had been shown to form strong biofilms under aerobic condition [3][4]. Biofilm formation is also recognized as a potential reservoir for antimicrobial resistance and is known to facilitate exchange of resistance genes between pathogenic and commensal bacteria [5]. This is particularly pertinent in case of Campylobacter spp., including C. jejuni and C. coli, which exhibit intrinsic resistance to many antimicrobial agents and are naturally conjugative [6][7][8]. In addition, Campylobacter spp. are becoming increasingly resistant to the most frequently prescribed antibiotics such as erythromycin, tetracycline and fluoroquinolones, and have been listed by WHO as a priority pathogen for the development of new antibiotics [9][10]. The usage of antibiotics in food animals to control, prevent and treat infections, and to enhance growth, has been implicated in an increased resistance to multiple antibiotics by Campylobacter spp. [11]. Majority of C. jejuni and C. coli are now resistant to at least one of the currently used antibiotics, such as penicillin, trimethoprim, sulfamethoxazole, rifampicin and vancomycin [11], requiring alternative treatments with either gentamicin or third-generation cephalosporins [12].
Several studies have shown that C. jejuni strains are able to attach to, and form mono- or mixed-species biofilms with other bacterial species such as Pseudomonas aeruginosa, Escherichia coli, Staphylococcus simulans, Enterococcus faecalis, Salmonella spp., Flavobacterium spp., and Corynebacterium spp. [13][14][15]. The evidence from these recent publications suggests that the composition of Campylobacter spp. biofilms is similar to that formed by other organisms. While there has been some investigation of the extracellular matrix components of C. jejuni biofilms, the architecture and the composition of these are yet to be fully characterized. C. jejuni NCTC strain 11168 was reported to produce an extracellular fibre-like material as a component of its biofilm, structurally resembling a net-like matrix [16]. Such matrices contribute to biofilm-mediated antimicrobial resistance, either by acting as a diffusion barrier or by binding directly to antimicrobial agents and preventing their access to the biofilm-encased cells [17]. The extracellular DNA (eDNA) is important for establishment and maintenance of C. jejuni biofilm [18][19], and appears to be a crucial component of the extracellular matrix of mature biofilms as degradation of eDNA results in reduction of biofilm formation by C. jejuni [18][19][20]. Interestingly, Gaasbeek et al. [21] found that a C. jejuni Mu-like prophage-integrated element 1 (CJIE1) containing strain, a non-naturally transformable strain, has a gene encoding an extracellular DNase (eDNase, CJE0256), and eDNase activity could be detected. It is interesting to note that no eDNase activity could be found in naturally transformable C. jejuni strains such as NCTC11168 and 81116.
Most of our current knowledge of Campylobacter spp. biofilm architecture is summarised in Figure 1. In the first stage of biofilm formation, planktonic cells attach to the surface via two types of interaction: cell-surface and cell-cell interactions using flagella, fimbriae, amyloid-like fibrils and outer membrane proteins [22][23][24]. This process is critical for bacterial adhesion and is influenced by the properties of both bacterial cells and the surface [25][26]. Secondly, after initial attachment, the cells start production of extracellular polymeric substance (EPS) consisting of polysaccharides, extracellular DNA (eDNA) [19], proteins [27], lipids and other glycosylated polymers, in order to initiate micro-colonies and progress to the third stage of a mature biofilm [28][29]. In a mature biofilm, EPS acts as an adhesive between cells and supports the intricate three-dimensional (3D) structure of the biofilm, protecting the cells from toxic compounds such as antibiotics, but allowing the movement of fluid and nutrients [30]. Finally, cell death and autolysis serve as a trigger for the mature biofilm to detach and release cells into the environmental niche in a process called dispersion [31]. Biofilm dispersion is believed to be crucial for the propagation and self-renewal of bacterial communities [30][32] and contributes to bacterial survival, pathogenicity and most importantly, disease transmission [30][33][34].
Figure 1. Cycle of biofilm development. (A) Planktonic cells swim and attach to surfaces (cell-to-surface and cell-to-cell) resulting in the formation of microcolonies. Mature biofilms can return to a planktonic lifestyle through dispersion and released seed cells complete the cycle of biofilm development. (B) Representative scanning electron microscopy (SEM) images of C. jejuni cultured under microaerobic conditions.
The understanding of gene regulation of C. jejuni biofilm formation is still limited. There are a number of genes known to be involved in the biofilm formation process and include those responsible for motility and chemotaxis [35][36][37], lipooligosaccharide biosynthesis [35][36][38][39], N-linked protein glycosylation, capsular polysaccharides (CPS) [35][39][40], and stress response proteins. Quorum sensing (QS), which allows the bacteria to regulate population cell density in biofilms was also found to play a role in Campylobacter biofilm formation and to contribute to host colonisation [15][37][41][42]. However, an important messenger, the intercellular bis-(3′-5′)-cyclic dimeric guanosine monophosphate (c-di-GMP), which plays an essential role in the transition between sessile and motile lifestyles in many other organisms [43], or its homologue, is yet to be found in the C. jejuni genome.

2. Natural Antibiofilm Compounds

Biofilm-disrupting and antimicrobial properties of many naturally occurring compounds against pathogens have been previously explored [44][45][46]. Such compounds (Table 1) include different plant extracts and their components (e.g., containing polyphenols), essential oils (e.g., containing carvacrol) and marine inhabitants (algae extracts), and a number of these have been tested against campylobacters.
Table 1. Antibiofilm activity of natural compounds with their mechanism of action.
Compounds Mechanism of Action Strains MIC * References
    Plant-derived compounds    
Essential oils (EOs)
breakdown of the extracellular matrix
inhibit the activity of AI-2 molecules
C. jejuni NCTC 11168
C. coli
C. jejuni S-8
C. jejuni NCTC 81-176
C. jejuni RC039
1.76 mg/L (75.64 mM) [47][48]
Clove oil
0.05–0.4 mg/mL [49]
2.69 mg/L (60.9 mM) [50]
31.25 mg/L (66.56 mM) [51]
Lavender essential oil
1 mg/mL [52]
Juniper essential oil
1 mg/mL [51][53]
125 mg/L [54]
Plant extracts
Grapefruit seed extract (GSE)
break-down the outer membranes
inhibit the activity of AI-2 molecules
C. jejuni NCTC 11168
C. jejuni S-8
C. jejuni F38011
C. jejuni 180ip
C. jejuni 238ip
C. coli
60 mg/L [55]
Citrus limon peel extract
225 µg/mL [56]
Ethanol solution extract (EREE)
64–1024 µg/mL [57]
Green tea (epigallocatechin gallate)
50 μg/mL [58][59]
Polyphenolic extracts
0.15–0.3 mg/L [60]
0.1–0.2 mg/mL [61]
Diallyl sulphide
0.04 mg/mL [62]
Antimicrobial peptides (AMPs) Puroindoline A (PinA)
quorum sensing-mediated inhibition of EPS production.
C. jejuni 81-176 512 μg/mL [33][63][64]
    Microorganism-derived compounds    
Algae extracts Delisea pulchra extract
inhibit the activity of AI-2 molecules
C. jejuni NCTC 11168 230 µg/mL [65]
d-amino acids (DAs)
consequence of incorporation of the DAs into the cell.
breakdown of the extracellular matrix such as EPS
C. jejuni NCTC 11168 5–100 mM [24]
Probiotic-derived factors
interfering with DNA synthesis
interfering with the membrane integrity of bacterial cells
C. jejuni
C. coli
0.025–32 µg/mL
1.5–5.8 μM
Glycolipid Biosurfactant Sophorolipid
lysis of the cell membrane
C. jejuni subsp. jejuni 33560 0.003% [65]
* Minimum inhibitory concentrations (MIC) as determined by the broth microdilution method described in individual references.


2.1. Plant-Derived Compounds

Essential oils (EOs) derived from plants are promising antimicrobial compounds, with over ~300 commercially available EOs. Many EOs (e.g., cinnamon oil, clove oil and lavender essential oil) exhibit antibacterial, antibiofilm and antifungal properties which have a wide range of applications in the food and dietary supplement industry [68][69][70][71][72]. EOs are also reported to prevent biofilm formation on abiotic surfaces, which has encouraged the development of alternative disinfection strategies, targeting contaminated surfaces and equipment used in food processing [73][74][75][76]. Moreover, EOs have been added to animal feed and water as taste enhancers for livestock nutrients and as growth promoters, particularly in poultry and porcine farming [71][77][78]. Here, we describe some compounds that exhibit promising antimicrobial and antibiofilm activities against campylobacters.
Cinnamon oil (Cinnamomum cassia) and clove oil (Eugenia caryophyllus) are reported to have bioactive compounds such as cinnamaldehyde (CA), eugenol (EG) and carvacrol (CR) [69]. These compounds act as antimicrobial and antibiofilm agents against many pathogens including P. aeruginosa, Salmonella Typhimurium, Streptococcus mutans and Listeria monocytogenes [79][80][81][82]. CA, EG and CR also exhibit an ability to significantly decrease Campylobacter spp. biofilms and remove the biofilms from stainless steel and polystyrene surfaces [48][49][50][51][83]. Several studies revealed the effectiveness of CR to reduce C. jejuni in vitro and in vivo [84][85][86][87][88][89]. For instance, Wagle et al. [83] found that the minimum inhibitory concentration (MIC) of CR (at 0.002%) was able to reduce the C. jejuni adhesion to primary chicken enterocytes (in an in vitro model of chicken intestinal physiology) up to 1.5 log cfu/mL as compared with control. Interestingly, CR downregulated the expression of C. jejuni colonisation factors, critical for persistence in the chicken gut, such as chemotaxis (aspartate chemoreceptor, CcaA), interactions with host cells (aspA) and anaerobic respiration (NapB). Similar to that, šimunović et al. [89] demonstrated that CR (MIC 0.0032%), as a pure compound or in synergistic combinations with thymoquinone, and rosmarinic acid, not only has antimicrobial activity against C. jejuni but also can increase the antibiotic susceptibility of C. jejuni by inhibiting the efflux pump activity. Unfortunately, further attempts to determine antibacterial properties of CR against C. jejuni using the broiler chicken model were inconsistent. Arsi et al. [90] reported that CR supplemented feed at 0.5–1% could significantly reduce Campylobacter counts in broiler chicks, either alone or in combination with thymol. However, their results could not be replicated in other trials, reportedly due to absorption of those compounds before they reach their target, the small intestine and caeca of chickens, or effects of other enteric microflora [86]. To improve the in vivo outcomes, Allaoua et al. [86] used a CR-based product, solid galenic CR formulation, designed to delay the CR release to allow it to reach the caeca of broiler chickens in order to control C. jejuni. This new formulation was aimed to preserve the antibacterial efficacy of CR against C. jejuni by allowing CR to reach the caeca and large intestine at an effective concentration (at MIC 0.02 mg/mL), which significantly decreased the C. jejuni caecal load (by 1.5 log). Kelly et al. [85] also reported that CR was able to reduce Campylobacter cell adhesion and invasion of chicken intestinal primary cells and also biofilm formation in vitro. They also showed that CR was able to delay colonisation of chicken broilers by inducing changes in gut microflora. Campylobacter spp. was only detected at 35 days of life in the treatment groups compared with the control group where the colonisation occurred at 21 days. Reducing the number of campylobacteria in the chicken intestine is a goal of most studies as quantitative risk assessment models indicate that a reduction of C. jejuni numbers on a broiler carcass by 100-fold (or 2 log units) could result in a significant reduction, by 30 times, in the incidence of campylobacteriosis [91]. Even a relatively small reduction in C. jejuni numbers in the chicken cecum by 1 log10 CFU can reduce the public health risk by more than 50% [16]. In addition, CR had a significant effect on E. coli numbers in the cecum of the chickens in treatment groups. Similarly, Szott et al. [88] found that CR additive could reduce C. jejuni counts in vivo by 1.17 log (up to 28 days of age); however, CR did not successfully reduce Campylobacter caecal colonisation in 33-day-old broilers. Interestingly, addition of CR to the diet decreased feed intake increased feed conversion rates and body weight at all levels of supplementation [92]. Similarly, combining basic diet with cinnamon oil (0.3 g of cinnamon oil per kg) could enhance daily weight gain of broiler chickens by 5.1% [93]. One more potential advantage of using CR is its effect on probiotic bacteria where the additional proliferation of probiotic bacteria such as Lactobacillus and Bifidobacteria spp. has been proposed to be a potential mechanism of inhibiting avian colonisation by disease-causing organisms such as Campylobacter spp. [68][94]. The important benefit, all studies agree, is that CR is safe to use as a dietary supplement in the chicken diet and could improve poultry health, feed efficiency, and delay Campylobacter colonisation in chickens.
Lavender essential oil (LEO) has antiviral activity against Herpes simplex virus type 1 [95]; antibacterial activity against piperacillin-resistant E. coli J53 R1, chloramphenicol-resistant L. monocytogenes L120, S. aureus MRSA and P. aeruginosa [96][97][98][99]; and antifungal activity against Aspergillus niger and Aspergillus tubingensis [100]. LEOs also show an antibiofilm activity against C. jejuni with MIC ranged from 0.2 mg/mL to 1 mg/mL [101]. LEOs were reported to downregulate a range of genes (i.e., Cj0719c, kpsS, lgt, maf4, waaC and Cj1467), involved in the initial attachment of Campylobacter spp. cells to abiotic and biotic surfaces. Adaszynska et al. [99] have evaluated the effect of LEO on chicken production by adding LEO to drinking water given to broiler chickens. The results of the experiments not only showed a significant inhibition of microbial growth, but also a significant increase in the body weight of the chickens in the groups receiving LEO as compared with the control group. Similarly, juniper essential oil (JEO) had shown potent anti-adherent effects against C. jejuni [44][51][53][102], where flavonoid-rich fractions from juniper, at 1 mg/mL, were able to inhibit attachment of C. jejuni cells to polystyrene by up to 70–99%, and reduced the invasion of INT407 cells by 76%. α- and β-pinene are another example of essential oil components from Alpinia katsumadai seeds that can have antimicrobial, antimalarial, and antioxidant effects [54][103][104][105]. The antimicrobial activities of (-)-α-pinene were reported against Campylobacter spp. in vitro; however, (-)-α-pinene alone showed a low efficacy with MIC50 > 500 mg/L required to inhibit 50% of the strains, but when (-)-α-pinene was combined with antibiotics ciprofloxacin and erythromycin, strong potentiating effects against different Campylobacter strains were observed. The concentrations of antibiotics could be decreased from 1 mg/mL to 0.002 mg/mL for ciprofloxacin, and from 512 mg/mL to <1 mg/mL for erythromycin [106]. Possible applications of such natural compounds could be in food packaging to maintain food quality and reduce cross-contamination, or as feed additives to increase weight gain of chickens and by reducing the costs associated with antimicrobial feed additives.


  1. Joshua, G.P.; Guthrie-Irons, C.; Karlyshev, A.; Wren, B. Biofilm formation in Campylobacter jejuni. Microbiology 2006, 152, 387–396.
  2. Brown, H.L.; Reuter, M.; Salt, L.J.; Cross, K.L.; Betts, R.P.; van Vliet, A.H. Chicken juice enhances surface attachment and biofilm formation of Campylobacter jejuni. Appl. Environ. Microbiol. 2014, 80, 7053–7060.
  3. Bronowski, C.; James, C.E.; Winstanley, C. Role of environmental survival in transmission of Campylobacter jejuni. FEMS Microbiol. Lett. 2014, 356, 8–19.
  4. Reuter, M.; Mallett, A.; Pearson, B.M.; van Vliet, A.H. Biofilm formation by Campylobacter jejuni is increased under aerobic conditions. Appl. Environ. Microbiol. 2010, 76, 2122–2128.
  5. Iovine, N.M. Resistance mechanisms in Campylobacter jejuni. Virulence 2013, 4, 230–240.
  6. Smith, J.L.; Fratamico, P.M. Fluoroquinolone resistance in Campylobacter. J. Food Prot. 2010, 73, 1141–1152.
  7. Golz, J.C.; Stingl, K. Natural competence and horizontal gene transfer in Campylobacter. In Fighting Campylobacter Infections: Towards a One Health Approach; Springer Nature: Basingstoke, UK, 2021; pp. 265–292.
  8. Vegge, C.S.; Brøndsted, L.; Ligowska-Marzęta, M.; Ingmer, H. Natural transformation of Campylobacter jejuni occurs beyond limits of growth. PLoS ONE 2012, 7, e45467.
  9. Han, J. Molecular Mechanisms Involved in the Emergence and Fitness of Fluoroquinolone-Resistant Campylobacter jejuni; Iowa State University: Ames, IA, USA, 2009.
  10. World Health Organization. WHO Publishes List of Bacteria for Which New Antibiotics Are Urgently Needed; WHO: Geneva, Switzerland, 2017.
  11. Silva, J.; Leite, D.; Fernandes, M.; Mena, C.; Gibbs, P.A.; Teixeira, P. Campylobacter spp. as a foodborne pathogen: A review. Front. Microbiol. 2011, 2, 200.
  12. Whitehouse, C.A.; Zhao, S.; Tate, H. Antimicrobial resistance in Campylobacter species: Mechanisms and genomic epidemiology. Adv. Appl. Microbiol. 2018, 103, 1–47.
  13. Ica, T.; Caner, V.; Istanbullu, O.; Nguyen, H.D.; Ahmed, B.; Call, D.R.; Beyenal, H. Characterization of mono- and mixed-culture Campylobacter jejuni biofilms. Appl. Environ. Microbiol. 2012, 78, 1033–1038.
  14. Li, J.; Feng, J.; Ma, L.; de la Fuente Núñez, C.; Gölz, G.; Lu, X. Effects of meat juice on biofilm formation of Campylobacter and Salmonella. Int. J. Food Microbiol. 2017, 253, 20–28.
  15. Scheik, L.K.; Volcan Maia, D.S.; Würfel, S.D.F.R.; Ramires, T.; Kleinubing, N.R.; Haubert, L.; Lopes, G.V.; da Silva, W.P. Biofilm-forming ability of poultry Campylobacter jejuni strains in the presence and absence of Pseudomonas aeruginosa. Can. J. Microbiol. 2021, 67, 301–309.
  16. World Health Organization. The Global View of Campylobacteriosis: Report of an Expert Consultation, Utrecht, Netherlands, 9–11 July 2012; WHO: Geneva, Switzerland, 2013.
  17. Mah, T.-F. Biofilm-specific antibiotic resistance. Future Microbiol. 2012, 7, 1061–1072.
  18. Brown, H.L.; Reuter, M.; Hanman, K.; Betts, R.P.; van Vliet, A.H. Prevention of Biofilm Formation and Removal of Existing Biofilms by Extracellular DNases of Campylobacter jejuni. PLoS ONE 2015, 10, e0121680.
  19. Svensson, S.L.; Pryjma, M.; Gaynor, E.C. Flagella-mediated adhesion and extracellular DNA release contribute to biofilm formation and stress tolerance of Campylobacter jejuni. PLoS ONE 2014, 9, e106063.
  20. Turonova, H.; Briandet, R.; Rodrigues, R.; Hernould, M.; Hayek, N.; Stintzi, A.; Pazlarova, J.; Tresse, O. Biofilm spatial organization by the emerging pathogen Campylobacter jejuni: Comparison between NCTC 11168 and 81-176 strains under microaerobic and oxygen-enriched conditions. Front. Microbiol. 2015, 6, 709.
  21. Gaasbeek, E.J.; Wagenaar, J.A.; Guilhabert, M.R.; Wösten, M.M.; van Putten, J.P.; van der Graaf-van Bloois, L.; Parker, C.T.; van der Wal, F.J. A DNase encoded by integrated element CJIE1 inhibits natural transformation of Campylobacter jejuni. J. Bacteriol. 2009, 191, 2296–2306.
  22. Van Houdt, R.; Michiels, C.W. Role of bacterial cell surface structures in Escherichia coli biofilm formation. Res. Microbiol. 2005, 156, 626–633.
  23. Turonova, H.; Neu, T.R.; Ulbrich, P.; Pazlarova, J.; Tresse, O. The biofilm matrix of Campylobacter jejuni determined by fluorescence lectin-binding analysis. Biofouling 2016, 32, 597–608.
  24. Elgamoudi, B.A.; Taha, T.; Korolik, V. Inhibition of Campylobacter jejuni biofilm formation by d-amino acids. Antibiotics 2020, 9, 836.
  25. Palmer, J.; Flint, S.; Brooks, J. Bacterial cell attachment, the beginning of a biofilm. J. Ind. Microbiol. Biotechnol. 2007, 34, 577–588.
  26. Flemming, H.-C.; Wingender, J. The biofilm matrix. Nat. Rev. Micro. 2010, 8, 623–633.
  27. Melo, R.T.; Mendonça, E.P.; Monteiro, G.P.; Siqueira, M.C.; Pereira, C.B.; Peres, P.A.; Fernandez, H.; Rossi, D.A. Intrinsic and extrinsic aspects on Campylobacter jejuni biofilms. Front. Microbiol. 2017, 8, 1332.
  28. Kostakioti, M.; Hadjifrangiskou, M.; Hultgren, S.J. Bacterial biofilms: Development, dispersal, and therapeutic strategies in the dawn of the postantibiotic Era. Cold Spring Harb. Perspect. Med. 2013, 3, a010306.
  29. Das, T.; Manefield, M. Pyocyanin promotes extracellular DNA release in Pseudomonas aeruginosa. PLoS ONE 2012, 7, e46718.
  30. Kaplan, J.B. Biofilm dispersal: Mechanisms, clinical implications, and potential therapeutic uses. J. Dent. Res. 2010, 89, 205–218.
  31. Ma, L.; Conover, M.; Lu, H.; Parsek, M.R.; Bayles, K.; Wozniak, D.J. Assembly and development of the Pseudomonas aeruginosa biofilm matrix. PLoS Pathog 2009, 5, e1000354.
  32. Renner, L.D.; Weibel, D.B. Physicochemical regulation of biofilm formation. MRS Bull. 2011, 36, 347–355.
  33. Boles, B.R.; Horswill, A.R. Staphylococcal biofilm disassembly. Trends Microbiol. 2011, 19, 449–455.
  34. Rendueles, O.; Ghigo, J.-M. Multi-species biofilms: How to avoid unfriendly neighbors. FEMS Microbiol. Rev. 2012, 36, 972–989.
  35. Tram, G.; Day, C.J.; Korolik, V. Bridging the gap: A role for Campylobacter jejuni biofilms. Microorganisms 2020, 8, 452.
  36. Whelan, M.V.; Simpson, J.C.; Cróinín, T.Ó. A novel high-content screening approach for the elucidation of Campylobacter jejuni biofilm composition and integrity. BMC Microbiol. 2021, 21, 2.
  37. Püning, C.; Su, Y.; Lu, X.; Gölz, G. Molecular mechanisms of Campylobacter biofilm formation and quorum sensing. In Fighting Campylobacter Infections: Towards a One Health Approach; Springer: Berlin/Heidelberg, Germany, 2021; pp. 293–319.
  38. Lim, E.S.; Kim, J.-S. Role of eptC in biofilm formation by Campylobacter jejuni NCTC11168 on polystyrene and glass surfaces. J. Microbiol. Biotechnol. 2017, 27, 1609–1616.
  39. Burnham, P.M.; Hendrixson, D.R. Campylobacter jejuni: Collective components promoting a successful enteric lifestyle. Nat. Rev. Microbiol. 2018, 16, 551–565.
  40. Guerry, P.; Poly, F.; Riddle, M.; Maue, A.C.; Chen, Y.H.; Monteiro, M.A. Campylobacter polysaccharide capsules: Virulence and vaccines. Front. Cell. Infect. Microbiol. 2012, 2, 7.
  41. Teren, M.; Michova, H.T.; Vondrakova, L.; Demnerova, K. Molecules autoinducer 2 and cjA and their impact on gene expression in Campylobacter jejuni. J. Mol. Microbiol. Biotechnol. 2018, 28, 207–215.
  42. Tereň, M.; Shagieva, E.; Vondrakova, L.; Viktorova, J.; Svarcova, V.; Demnerova, K.; Michova, H.T. Mutagenic strategies against luxS gene affect the early stage of biofilm formation of Campylobacter jejuni. J. Appl. Genet. 2021.
  43. Tischler, A.D.; Camilli, A. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol. Microbiol. 2004, 53, 857–869.
  44. Balta, I.; Linton, M.; Pinkerton, L.; Kelly, C.; Stef, L.; Pet, I.; Stef, D.; Criste, A.; Gundogdu, O.; Corcionivoschi, N. The effect of natural antimicrobials against Campylobacter spp. and its similarities to Salmonella spp, Listeria spp., Escherichia coli, Vibrio spp., Clostridium spp. and Staphylococcus spp. Food Control 2020, 121, 107745.
  45. Kalogianni, A.I.; Lazou, T.; Bossis, I.; Gelasakis, A.I. Natural phenolic compounds for the control of oxidation, bacterial spoilage, and foodborne pathogens in meat. Foods 2020, 9, 794.
  46. Mishra, R.; Panda, A.K.; De Mandal, S.; Shakeel, M.; Bisht, S.S.; Khan, J. Natural anti-biofilm agents: Strategies to control biofilm-forming pathogens. Front. Microbiol. 2020, 11, 2640.
  47. Wagle, B.R.; Arsi, K.; Shrestha, S.; Upadhyay, A.; Upadhyaya, I.; Bhargava, K.; Donoghue, A.; Donoghue, D.J. Eugenol as an antimicrobial wash treatment reduces Campylobacter jejuni in postharvest poultry. J. Food Saf. 2019, 39, e12704.
  48. Upadhyaya, I.; Upadhyay, A.; Arsi, K.; Liyanage, R.; Donoghue, A.; Rath, N.; Donoghue, D. Plant-derived antimicrobial eugenol modulates Campylobacter jejun proteome and virulence critical for colonization in chickens. Poult. Sci. 2017, 96, 537.
  49. Wagle, B.R.; Upadhyay, A.; Upadhyaya, I.; Shrestha, S.; Arsi, K.; Liyanage, R.; Venkitanarayanan, K.; Donoghue, D.J.; Donoghue, A.M. Trans-cinnamaldehyde, eugenol and carvacrol reduce Campylobacter jejuni biofilms and modulate expression of select genes and proteins. Front. Microbiol. 2019, 10, 1837.
  50. Yu, H.H.; Song, Y.J.; Yu, H.S.; Lee, N.K.; Paik, H.D. Investigating the antimicrobial and antibiofilm effects of cinnamaldehyde against Campylobacter spp. using cell surface characteristics. J. Food Sci. 2020, 85, 157–164.
  51. Šimunović, K.; Ramić, D.; Xu, C.; Smole Možina, S. Modulation of Campylobacter jejuni motility, adhesion to polystyrene surfaces, and invasion of INT407 cells by quorum-sensing inhibition. Microorganisms 2020, 8, 104.
  52. Gahamanyi, N.; Song, D.-G.; Cha, K.H.; Yoon, K.-Y.; Mboera, L.E.; Matee, M.I.; Mutangana, D.; Amachawadi, R.G.; Komba, E.V.; Pan, C.-H. Susceptibility of Campylobacter strains to selected natural products and frontline antibiotics. Antibiotics 2020, 9, 790.
  53. Klančnik, A.; Šimunović, K.; Sterniša, M.; Ramić, D.; Možina, S.S.; Bucar, F. Anti-adhesion activity of phytochemicals to prevent Campylobacter jejuni biofilm formation on abiotic surfaces. Phytochem. Rev. 2021, 20, 55–84.
  54. Salehi, B.; Upadhyay, S.; Erdogan Orhan, I.; Kumar Jugran, A.; LD Jayaweera, S.; Dias, D.A.; Sharopov, F.; Taheri, Y.; Martins, N.; Baghalpour, N. Therapeutic potential of α-and β-pinene: A miracle gift of nature. Biomolecules 2019, 9, 738.
  55. Silván, J.M.; Mingo, E.; Hidalgo, M.; de Pascual-Teresa, S.; Carrascosa, A.V.; Martinez-Rodriguez, A.J. Antibacterial activity of a grape seed extract and its fractions against Campylobacter spp. Food Control 2013, 29, 25–31.
  56. Castillo, S.; Heredia, N.; Arechiga-Carvajal, E.; García, S. Citrus extracts as inhibitors of quorum sensing, biofilm formation and motility of Campylobacter jejuni. Food Biotechnol. 2014, 28, 106–122.
  57. Bezek, K.; Kurinčič, M.; Knauder, E.; Klančnik, A.; Raspor, P.; Bucar, F.; Smole Možina, S. Attenuation of adhesion, biofilm formation and quorum sensing of Campylobacter jejuni by Euodia ruticarpa. Phytother. Res. 2016, 30, 1527–1532.
  58. Wagle, B.R.; Donoghue, A.M.; Jesudhasan, P.R. Select phytochemicals reduce Campylobacter jejuni in postharvest poultry and modulate the virulence attributes of C. jejuni. Front. Microbiol. 2021, 2270.
  59. Lu, X.; Samuelson, D.R.; Rasco, B.A.; Konkel, M.E. Antimicrobial effect of diallyl sulphide on Campylobacter jejuni biofilms. J. Antimicrob. Chemother. 2012, 67, 1915–1926.
  60. Castillo, S.; Heredia, N.; García, S. 2 (5H)-Furanone, epigallocatechin gallate, and a citric-based disinfectant disturb quorum-sensing activity and reduce motility and biofilm formation of Campylobacter jejuni. Folia Microbiol. 2015, 60, 89–95.
  61. Roila, R.; Ranucci, D.; Valiani, A.; Galarini, R.; Servili, M.; Branciari, R. Antimicrobial and anti-biofilm activity of olive oil by-products against Campylobacter spp. isolated from chicken meat. Acta Sci. Pol. Technol. Aliment. 2019, 18, 43–52.
  62. Duarte, A.; Alves, A.C.; Ferreira, S.; Silva, F.; Domingues, F.C. Resveratrol inclusion complexes: Antibacterial and anti-biofilm activity against Campylobacter spp. and Arcobacter butzleri. Food Res. Int. 2015, 77, 244–250.
  63. Romeo, T. When the party is over: A signal for dispersal of Pseudomonas aeruginosa biofilms. J. Bacteriol. 2006, 188, 7325–7327.
  64. McDougald, D.; Rice, S.A.; Barraud, N.; Steinberg, P.D.; Kjelleberg, S. Should we stay or should we go: Mechanisms and ecological consequences for biofilm dispersal. Nat. Rev. Microbiol. 2012, 10, 39–50.
  65. Silveira, V.A.I.; Nishio, E.K.; Freitas, C.A.; Amador, I.R.; Kobayashi, R.K.; Caretta, T.; Macedo, F.; Celligoi, M.A.P. Production and antimicrobial activity of sophorolipid against Clostridium perfringens and Campylobacter jejuni and their additive interaction with lactic acid. Biocatal. Agric. Biotechnol. 2019, 21, 101287.
  66. Asare, P.T.; Zurfluh, K.; Greppi, A.; Lynch, D.; Schwab, C.; Stephan, R.; Lacroix, C. Reuterin demonstrates potent antimicrobial activity against a broad panel of human and poultry meat Campylobacter spp. isolates. Microorganisms 2020, 8, 78.
  67. Svetoch, E.A.; Eruslanov, B.V.; Perelygin, V.V.; Mitsevich, E.V.; Mitsevich, I.P.; Borzenkov, V.N.; Levchuk, V.P.; Svetoch, O.E.; Kovalev, Y.N.; Stepanshin, Y.G. Diverse antimicrobial killing by Enterococcus faecium E 50–52 bacteriocin. J. Agric. Food Chem. 2008, 56, 1942–1948.
  68. Micciche, A.; Rothrock Jr, M.J.; Yang, Y.; Ricke, S.C. Essential oils as an intervention strategy to reduce Campylobacter in poultry production: A review. Front. Microbiol. 2019, 10, 1058.
  69. Lu, L.; Hu, W.; Tian, Z.; Yuan, D.; Yi, G.; Zhou, Y.; Cheng, Q.; Zhu, J.; Li, M. Developing natural products as potential anti-biofilm agents. Chin. Med. 2019, 14, 11.
  70. Abd Rashed, A.; Rathi, D.-N.G.; Ahmad Nasir, N.A.H.; Abd Rahman, A.Z. Antifungal properties of essential oils and their compounds for application in skin fungal infections: Conventional and nonconventional approaches. Molecules 2021, 26, 1093.
  71. Mucha, W.; Witkowska, D. The applicability of essential oils in different stages of production of animal-based foods. Molecules 2021, 26, 3798.
  72. Kurekci, C.; Padmanabha, J.; Bishop-Hurley, S.L.; Hassan, E.; Al Jassim, R.A.; McSweeney, C.S. Antimicrobial activity of essential oils and five terpenoid compounds against Campylobacter jejuni in pure and mixed culture experiments. Int. J. Food Microbiol. 2013, 166, 450–457.
  73. De Oliveira, M.M.M.; Brugnera, D.F.; das Graças Cardoso, M.; Alves, E.; Piccoli, R.H. Disinfectant action of Cymbopogon sp. essential oils in different phases of biofilm formation by Listeria monocytogenes on stainless steel surface. Food Control 2010, 21, 549–553.
  74. Puškárová, A.; Bučková, M.; Kraková, L.; Pangallo, D.; Kozics, K. The antibacterial and antifungal activity of six essential oils and their cyto/genotoxicity to human HEL 12469 cells. Sci. Rep. 2017, 7, 8211.
  75. Valeriano, C.; De Oliveira, T.L.C.; De Carvalho, S.M.; das Graças Cardoso, M.; Alves, E.; Piccoli, R.H. The sanitizing action of essential oil-based solutions against Salmonella enterica serotype Enteritidis S64 biofilm formation on AISI 304 stainless steel. Food Control 2012, 25, 673–677.
  76. Zhai, H.; Liu, H.; Wang, S.; Wu, J.; Kluenter, A.-M. Potential of essential oils for poultry and pigs. Anim. Nutr 2018, 4, 179–186.
  77. Kirkpinar, F.; Ünlü, H.; Serdaroğlu, M.; Turp, G. Effects of dietary oregano and garlic essential oils on carcass characteristics, meat composition, colour, pH and sensory quality of broiler meat. Br. Poult. Sci. 2014, 55, 157–166.
  78. Witkowska, D.; Sowińska, J. The effectiveness of peppermint and thyme essential oil mist in reducing bacterial contamination in broiler houses. Poult. Sci. 2013, 92, 2834–2843.
  79. Topa, S.H.; Subramoni, S.; Palombo, E.A.; Kingshott, P.; Rice, S.A.; Blackall, L.L. Cinnamaldehyde disrupts biofilm formation and swarming motility of Pseudomonas aeruginosa. Microbiology 2018, 164, 1087–1097.
  80. He, Z.; Huang, Z.; Jiang, W.; Zhou, W. Antimicrobial activity of cinnamaldehyde on Streptococcus mutans biofilms. Front. Microbiol. 2019, 10, 2241.
  81. Trevisan, D.A.C.; Silva, A.F.D.; Negri, M.; Abreu, B.A.D.; Machinski, M.; Patussi, E.V.; Campanerut-Sá, P.A.Z.; Mikcha, J.M.G. Antibacterial and antibiofilm activity of carvacrol against Salmonella enterica serotype Typhimurium. Braz. J. Pharm. Sci. 2018, 54.
  82. Upadhyay, A.; Upadhyaya, I.; Kollanoor-Johny, A.; Venkitanarayanan, K. Antibiofilm effect of plant derived antimicrobials on Listeria monocytogenes. Food Microbiol. 2013, 36, 79–89.
  83. Wagle, B.; Donoghue, A.; Shrestha, S.; Upadhyaya, I.; Arsi, K.; Gupta, A.; Liyanage, R.; Rath, N.; Donoghue, D.; Upadhyay, A. Carvacrol attenuates Campylobacter jejuni colonization factors and proteome critical for persistence in the chicken gut. Poult. Sci. 2020, 99, 4566–4577.
  84. Johny, A.K.; Darre, M.; Donoghue, A.; Donoghue, D.; Venkitanarayanan, K. Antibacterial effect of trans-cinnamaldehyde, eugenol, carvacrol, and thymol on Salmonella Enteritidis and Campylobacter jejuni in chicken cecal contents in vitro. J. Appl. Poult. Res. 2010, 19, 237–244.
  85. Kelly, C.; Gundogdu, O.; Pircalabioru, G.; Cean, A.; Scates, P.; Linton, M.; Pinkerton, L.; Magowan, E.; Stef, L.; Simiz, E. The in vitro and in vivo effect of carvacrol in preventing Campylobacter infection, colonization and in improving productivity of chicken broilers. Foodborne Pathog. Dis. 2017, 14, 341–349.
  86. Allaoua, M.; Etienne, P.; Noirot, V.; Carayon, J.L.; Tene, N.; Bonnafé, E.; Treilhou, M. Pharmacokinetic and antimicrobial activity of a new carvacrol-based product against a human pathogen, Campylobacter jejuni. J. Appl. Microbiol. 2018, 125, 1162–1174.
  87. Mousavi, S.; Schmidt, A.-M.; Escher, U.; Kittler, S.; Kehrenberg, C.; Thunhorst, E.; Bereswill, S.; Heimesaat, M.M. Carvacrol ameliorates acute campylobacteriosis in a clinical murine infection model. Gut Pathog. 2020, 12, 2.
  88. Szott, V.; Reichelt, B.; Alter, T.; Friese, A.; Roesler, U. In vivo efficacy of carvacrol on Campylobacter jejuni prevalence in broiler chickens during an entire fattening period. Eur. J. Microbiol. Immunol. 2020, 10, 131–138.
  89. Simunovic, K.; Bucar, F.; Klancnik, A.; Pompei, F.; Paparella, A.; Mozina, S.S. In vitro effect of the common culinary herb winter savory (Satureja montana) against the infamous food pathogen Campylobacter jejuni. Foods 2020, 9, 537.
  90. Arsi, K.; Donoghue, A.; Venkitanarayanan, K.; Kollanoor-Johny, A.; Fanatico, A.; Blore, P.; Donoghue, D. The efficacy of the natural plant extracts, thymol and carvacrol against Campylobacter colonization in broiler chickens. J. Food Saf. 2014, 34, 321–325.
  91. Robyn, J.; Rasschaert, G.; Pasmans, F.; Heyndrickx, M. Thermotolerant Campylobacter during broiler rearing: Risk factors and intervention. Compr. Rev. Food Sci. Food Saf. 2015, 14, 81–105.
  92. Hashemipour, H.; Kermanshahi, H.; Golian, A.; Veldkamp, T. Effect of thymol and carvacrol feed supplementation on performance, antioxidant enzyme activities, fatty acid composition, digestive enzyme activities, and immune response in broiler chickens. Poult. Sci. 2013, 92, 2059–2069.
  93. Chowdhury, S.; Mandal, G.P.; Patra, A.K. Different essential oils in diets of chickens: Growth performance, nutrient utilisation, nitrogen excretion, carcass traits and chemical composition of meat. Anim. Feed Sci. Technol. 2018, 236, 86–97.
  94. Santini, C.; Baffoni, L.; Gaggia, F.; Granata, M.; Gasbarri, R.; Di Gioia, D.; Biavati, B. Characterization of probiotic strains: An application as feed additives in poultry against Campylobacter jejuni. Int. J. Food Microbiol. 2010, 141, S98–S108.
  95. Minami, M.; Kita, M.; Nakaya, T.; Yamamoto, T.; Kuriyama, H.; Imanishi, J. The inhibitory effect of essential oils on herpes simplex virus type-1 replication in vitro. Microbiol. Immunol. 2003, 47, 681–684.
  96. Wińska, K.; Mączka, W.; Łyczko, J.; Grabarczyk, M.; Czubaszek, A.; Szumny, A. Essential oils as antimicrobial agents—Myth or real alternative? Molecules 2019, 24, 2130.
  97. Roller, S.; Ernest, N.; Buckle, J. The antimicrobial activity of high-necrodane and other lavender oils on methicillin-sensitive and-resistant Staphylococcus aureus (MSSA and MRSA). J. Altern. Complement. Med. 2009, 15, 275–279.
  98. Adaszyńska-Skwirzyńska, M.; Dzięcioł, M. Comparison of phenolic acids and flavonoids contents in various cultivars and parts of common lavender (Lavandula angustifolia) derived from Poland. Nat. Prod. Res. 2017, 31, 2575–2580.
  99. Adaszyńska-Skwirzyńska, M.; Szczerbińska, D. The antimicrobial activity of lavender essential oil (Lavandula angustifolia) and its influence on the production performance of broiler chickens. J. Anim. Physiol. Anim. Nutr. 2018, 102, 1020–1025.
  100. Císarová, M.; Tančinová, D.; Medo, J. Antifungal activity of lemon, eucalyptus, thyme, oregano, sage and lavender essential oils against Aspergillus niger and Aspergillus tubingensis isolated from grapes. Potravinarstvo 2016, 10, 83–88.
  101. Ramić, D.; Bucar, F.; Kunej, U.; Dogša, I.; Klančnik, A.; Smole Možina, S. Anti-biofilm potential of Lavandula preparations against Campylobacter jejuni. Appl. Environ. Microbiol. 2021, 87, e01099-21.
  102. Klančnik, A.; Zorko, Š.; Toplak, N.; Kovač, M.; Bucar, F.; Jeršek, B.; Smole Možina, S. Antiadhesion activity of juniper (Juniperus communis L.) preparations against Campylobacter jejuni evaluated with PCR-based methods. Phytother Res. 2018, 32, 542–550.
  103. Sharifi-Rad, J.; Sureda, A.; Tenore, G.C.; Daglia, M.; Sharifi-Rad, M.; Valussi, M.; Tundis, R.; Sharifi-Rad, M.; Loizzo, M.R.; Ademiluyi, A.O. Biological activities of essential oils: From plant chemoecology to traditional healing systems. Molecules 2017, 22, 70.
  104. Khalifaev, P.D.; Sharopov, F.S.; Safomuddin, A.; Numonov, S.; Bakri, M.; Habasi, M.; Aisa, H.A.; Setzer, W.N. Chemical composition of the essential oil from the roots of Ferula kuhistanica growing wild in Tajikistan. Nat. Prod. Commun. 2018, 13, 1934578X1801300226.
  105. Sharopov, F.; Satyal, P.; Wink, M. Composition of the essential oil of Ferula clematidifolia. Chem. Nat. Compd. 2016, 52, 518–519.
  106. Šimunović, K.; Sahin, O.; Kovač, J.; Shen, Z.; Klančnik, A.; Zhang, Q.; Smole Možina, S. (-)-α-Pinene reduces quorum sensing and Campylobacter jejuni colonization in broiler chickens. PLoS ONE 2020, 15, e0230423.
Contributor MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to :
View Times: 305
Entry Collection: Gastrointestinal Disease
Revisions: 2 times (View History)
Update Date: 16 Nov 2021