Symptoms of abdominal infection may include Symptoms can range from mild diarrhea to septic shock and sometimes death. They usually occur after trauma.
Symptoms may include edema, pain, gas with crepitation, foul-smelling Symptoms are watery diarrhea and abdominal cramps. Diagnosis is by identifying C. Botulism may occur without infection if toxin is ingested, injected, or inhaled. Symptoms are initial constipation followed by Symptoms are intermittent tonic spasms of voluntary muscles.
Spasm of the masseters accounts for the name lockjaw Symptoms are diarrhea, sometimes bloody, rarely Peptostreptococcus and Finegoldia : Oral, respiratory, bone and joint, soft-tissue, and intra-abdominal infections.
Cutibacterium formerly Propionibacterium : Foreign body infections eg, in a cerebrospinal fluid shunt, prosthetic joint, or cardiac device. Anaerobic infections are typically suppurative, causing abscess formation and tissue necrosis and sometimes septic thrombophlebitis, gas formation, or both. Many anaerobes produce tissue-destructive enzymes, as well as some of the most potent paralytic toxins known. Usually, multiple species of anaerobes are present in infected tissues; aerobes are frequently also present mixed anaerobic infections Mixed Anaerobic Infections Anaerobes can infect normal hosts and hosts with compromised resistance or damaged tissues.
Mixed anaerobic infections can include both single anaerobic species or multiple anaerobic species Specimens for anaerobic culture should be obtained by aspiration or biopsy from normally sterile sites. Anaerobic exercise leads to a buildup of lactic acid in our tissues. We need oxygen to remove the lactic acid. When sprinters breathe heavily after running a race, they are removing the lactic acid by providing oxygen to their bodies.
Exercise physiology. Philadelphia, PA: Elsevier; chap 6. Anaerobic infections: general concepts. Philadelphia, PA: Elsevier; chap Updated by: Linda J. Editorial team. Through experiments using fecal transplants into germ-free mice, these authors also verified that obesity-associated microbiome is ameliorated by Christensenella minuta which reduces the weight gain and alters the microbiome pattern of recipient mice.
As the first member of the family Christensenellaceae phylum Firmicutes , C. Alongside the potential use of C. Similarly, to other Gram-negative bacteria, C. Nonetheless, it was demonstrated that LPS of C. Although these studies suggest that C. The increasing causal evidences linking the depletion of butyrate-producing bacteria in the intestinal ecosystem to the onset of inflammatory conditions has been attracting increasing attention due to its clinical applications.
In this context, the butyrate producer Butyricicoccus pullicaecorum is considered to play a major part in gut health due to its beneficial effects on inflammatory bowel disorders Eeckhaut et al. Firstly, isolated from the caecal content of a broiler chicken, B. Following the observation of the reduced abundance of the genus Butyricicoccus in fecal samples of IBD patients, B.
Eeckhaut and coworkers reported that oral administration of this bacterium resulted in a decrease of lesion sizes and inflammation in a rat colitis model. In parallel, in vitro assays demonstrated that the supernatant of B. Similarly, Bajer and colleagues verified that ulcerative colitis was related to a reduction in B. Is also of importance to note that whole genome sequencing revealed that B.
This safety profile was further reinforced when this strain was shown to be safe and well-tolerated by rats Steppe et al. Also, the favorable intrinsic tolerance of B. Years after the Bacteroides genus thorough revision, Sakamoto and Benno reclassified three Bacteroides strains into the novel genus Parabacteroides spp.
Among the different strains, Parabacteroides goldsteinii exhibits potential to stand for a NGP position Chang et al. Belonging to the phylum Bacteroidetes, P. Recently, the oral administration of live P. However, the beneficial role of this bacterial species should be thoroughly analyzed since P.
Notwithstanding the emerging proof-of-concept data validating the favorable functional health effects on host fitness by probiotic anaerobes their introduction in pharmaceutical and nutraceutical products unravels several challenges for both industry and researchers Douillard and de Vos, One of the issues facing anaerobic development is related to adequate presumptions of safety O'Toole et al.
According to FAO criteria guidelines, every strain must be correctly identified and followed by several in vitro assays in order to explore its functional properties. After taxonomic identification and functional properties investigation, potential probiotics must be characterized in terms of safety and technological usefulness FAO and WHO, Considering that maintaining cell viability and metabolic activity is of essence for potential probiotic functional food incorporation and disease therapy inclusion, in the next section we will review the technological barriers and challenges that researchers have been attempting to surpass for their effective delivery, and which tactics are being adopted to overcome them.
Several constraints are known to challenge the viability and efficacy of these bacteria, which are generally associated to industrial processes and storage conditions. Indeed, the typical stressors go beyond the clear oxygen-sensitive nature of these commensals, in that low levels of pH, heat treatment, water activity Aw , the physicochemical properties of matrices, dehydration processes, and other factors can be responsible for possible viability reductions Terpou et al.
Moreover, when the stress factors faced during the biomanufacturing process and storage duration are bypassed, formulations don't guarantee the cultures protection from the harsh environment conditions of the gastrointestinal tract GIT. Once ingestion occurs bacteria will face a hostile physicochemical and biological environment composed of low pH levels, digestive enzymes, and bile salts which could affect their cell structure Barer, As such, in the following section some of the current technological strategies implemented will be discussed, with focus on their ability to protect the classical probiotics as well as the new potential anaerobic NGPs when exposed to detrimental conditions during production process, storage and GIT passage.
Bifidobacteria have been used for a long time now, especially in the development of foods and food supplements. Due to this usage, large-scale biomass production is already established. However, there is limited information in the literature about industrial production of bifidobacteria biomass which, according to El Enshasy et al. The manufacturing processes of bifidobacteria follow the same general steps of the production systems of other industrial microorganisms i.
A stock-culture checked for strain purity and absence of contaminants is used in a specific number of sequential seed fermentations to achieve the desired inoculum volume and transferred to the main fermenter for growth.
The medium used in the propagation and main fermentation is composed of carbon carbohydrates and nitrogen sources, minerals, and growth factors and is heat-treated before being used. Fermentation parameters such as growth temperature, pH, and the base used to control it, have an impact on the final product performance and characteristics and are dependent on the specific strain being cultivated Ouwehand et al.
After the fermentation is completed, the cells are concentrated by separating them from the cultivation broth, usually, through centrifugation. The concentrated biomass is normally stabilized by dehydration processes with freeze-drying lyophilization and spray-drying being the most widely used techniques Broeckx et al.
Each step should be optimized for the specific strain being produced as it can impact the robustness of the product and its ability to recover after rehydration Ouwehand et al. Figure 3. Schematic representation of the industrial production of bifidobacterial biomass adapted from Gomes et al. In Table 1 one may find a summary of the fermentation systems reported in the literature for bifidobacterial cultivation. In this process, the culture inoculum is added to the fermenter containing the culture medium and fermentation is conducted until the desired cell concentration is achieved.
Once the fermentation is finished, the cells are harvested, and the process is repeated. To improve biomass concentration, fed-batch fermentation has also been applied to bifidobacteria production El Enshasy et al.
This fermentation technique allows the addition of a limiting substrate during the fermentation, which can help increase the bacterial concentration. Fed-batch can also be applied to adapt bacteria to a specific carbon source or to induce a stress response to protect them from subsequent processing steps. Table 1. Selected bifidobacteria fermentation systems reported in the literature.
The use of continuous cultures has also been investigated to produce bifidobacteria Doleyres and Lacroix, After optimization, this technology can lead to both high cell yield and volumetric productivity and to contribute to decrease in the demand for downstream processing. However, the use of continuous fermentations at industrial scale may be more difficult as they are highly susceptible to contamination and to cell instability. Nevertheless, this technology has shown some potential to obtain cells with different physiologies and to apply stresses under well-controlled conditions see also section Improving the Stress Tolerance of Bifidobacteria Lacroix and Yildirim, For example, a two-stage continuous fermentation has been used to screen sublethal stress conditions for improvement of Bifidobacterium longum Mozzetti et al.
A first reactor was operated under normal conditions, whereas a second reactor, placed in series, was operated under stress conditions. In another approach, Mozzetti et al. A stable strain with higher tolerance to oxygen than the wild type cells was isolated in this manner. Cell immobilization consists of physical confinement or localization of microorganisms in a fermentation system to attain high cell concentrations Doleyres and Lacroix, Besides high cell densities, several other advantages over free-cell fermentations have also been reported including: the possibility of reusing the cells, improved resistance to contamination and bacteriophage attack, enhanced plasmid stability, prevention from washing-out during continuous cultures, and the physical and chemical protection of cells Lacroix and Yildirim, There are several methods for immobilizing microorganisms but for bifidobacteria two of them are the most used, namely immobilization in polysaccharide gel beads and membrane bioreactors Doleyres and Lacroix, Continuous cultures with B.
Kwon et al. Similarly, Jung et al. In a membrane system with a constant feeding of fresh medium, the bacteria are kept in the bioreactor by an ultrafiltration or microfiltration membrane.
Any growth inhibitory metabolites are removed from the system in this way, allowing for more bacterial growth. The concentrated biomass can be harvested with no or minimal additional downstream treatment for cell concentration before stabilization. The manufacturing process should result in a highly concentrated biomass without detrimental effects on the cells. The microorganisms must be metabolically stable during processing and active in the product and remain viable at sufficiently high levels during the gastrointestinal tract transit in order to exert the beneficial effects in the host.
However, during the manufacture and storage, bifidobacteria may be submitted to several stresses such as osmotic, heat, and cold or exposure to oxygen, which may have a detrimental impact on cell viability and hence on its functionality Ruiz et al.
Furthermore, after oral ingestion, bifidobacteria have to cope with low pH in the stomach and with high bile salt concentrations and digestive enzymes in the small intestine. Bifidobacteria are considered anaerobes but their oxygen sensitivities are reported to vary among the species.
Among the most studied species of bifidobacteria, B. Oxygen stress can affect bifidobacteria during their production, downstream processes, and storage as strict anaerobic conditions are not easily maintained in all these steps. Ahn et al. Ninomiya et al. Decreased EPS production during culture may have an impact on the ability to adhere to the intestinal epithelium. In contrast, Qian et al. Additionally, those grown under oxidative stress showed higher EPS production, acid tolerance, and cell surface hydrophobicity, which has been positively correlated with adhesion ability to host cells.
High temperatures can cause denaturation of proteins and destabilize membranes, conceivably leading to cell death. Simpson et al. It was found that survivability was best for bacteria with high oxygen and heat tolerance. Bifidobacterium animalis subsp.
Furthermore, Bifidobacterium strains that had better heat and oxygen tolerance also exhibited better stability during storage. Freeze-drying is a milder process than spray-drying resulting in higher cell viability.
However, the low temperature still compromises cellular integrity with the main consequences being reduction in membrane fluidity, protein folding, and disturbance of enzyme activity Mills et al. To increase cell viability during freeze drying and storage some cell-protecting agents such as skimmed milk powder, milk whey, butter milk, trehalose, sucrose, or lactose are usually added see also section Drying Processes. During dehydration, the osmolality of the milieu increases, leading to excessive passage of water from the cell to the extracellular environment that compromises essential cell functions Poolman, Exposure to acid leads to a proton accumulation inside the cell that may negatively affect the proton motive force PMF across the membrane.
Besides cell membrane structural damage caused by changes in PMF, acid stress also causes damage to nucleic acids and proteins Anandharaj et al. Bifidobacteria are generally considered to have low tolerance to exposure to acidic conditions.
Moderate tolerance to low pH after 60 min of exposure was reported for strains of B. Bifidobacterium adolescentis, B. Bile acids and salts are the main components of bile and are the responsible agents for its antimicrobial and detergent-like properties. Bile acids are weak organic acids that can passively enter the bifidobacteria cytoplasm Kurdi et al.
This intracellular accumulation of deconjugated bile acids have a profound impact on the cell metabolic processes, causes leakage of ions and other cellular components, and ultimately, may lead to cell death Ruiz et al.
The resistance to bile is very dependent on the species within the Bifidobacterium genus. It has been stated that almost all bifidobacteria possess metabolic capacity to cope with bile acids namely, by deconjugating them via mediation of a bile salt hydrolase El Enshasy et al. Different Bifidobacterium strains may present big differences in their tolerance to technological and gastrointestinal stresses as seen above.
Improving stress tolerance of bifidobacteria, and therefore ensuring their high survival, is important for both economic reasons and health effects. In this regard, stress adaptation by using exposure to sub-lethal conditions has been an important area of research Ruiz et al. Like other microorganisms, when bifidobacteria are exposed to sub-lethal stresses, the tolerance to subsequent stresses is improved.
This exposure leads to an adaptation to adverse environments, which is normally associated with the induction of many genes, the synthesis of shock-proteins and the development of cross-resistance to other types of stress Santos et al.
The same authors also reported that prolonged incubation at pH 2. An adaptation at pH 5. Sub-lethal H 2 O 2 treatments were shown to be beneficial to increase cell resistance to oxidative stress by certain B. Salt pretreatment resulted in an increased tolerance to freeze-thawing cycles or lethal heat stress in strains of B. Drying technology, which leads to anhydrobiosis, the state at which an organism stops its vital functions temporarily, is the oldest method used to improve probiotic stability, allowing them to maintain viability and their beneficial action over a long period of time Broeckx et al.
Dehydration of bacteria can be achieved by the application of different methods, namely freeze-drying, spray-drying, vacuum-drying, and fluidized-bed drying, the decision on which to select being based on industrial scale-up and the cost-effectiveness parameters Marcial-Coba et al.
As previously mentioned, it is generally acknowledged that each drying process poses stress to bacteria and to some extent causes inactivation due to the bacterial damage that can be caused by freezing and thawing Broeckx et al. Cryopreservation has several disadvantages from a commercial point of view, namely the need for subzero transportation and storage temperatures, and thus high energy costs Broeckx et al.
The drying process implies the removal of intracellular water that causes a mechanical stress on the bacterial membrane altering its plasticity and desiccation enhances the contact of bacterial surfaces with oxygen molecules, inducing the intracellular accumulation of reactive oxygen species which may lead to damage in bacteria macromolecules such as proteins, DNA, or lipids Foerest and Santivarangkna, ; Marcial-Coba et al.
Based on these facts, the decision of drying bacteria suspension needs to be carefully optimized. Freeze-drying is a process involving freezing and water removal by sublimation under high vacuum Barbosa et al. Briefly, it consists in three steps: i freezing where the extracellular ice crystal formed can lead to bacterial damage, due to chemical and osmotic injuries Broeckx et al.
Drying steps affect bacterial integrity, by the water removal from the cells, leading to a negative impact on the structure of sensitive proteins, cell wall and the physical state of the lipid membranes. These changes can also lead to a decrease in metabolic activity, and consequently, it may lead to a decrease in the viability of bacteria Cassani et al.
Nevertheless, freeze-drying is a preferred drying method for thermally sensitive bacteria, as it keeps their survival at a reasonably high level Goderska, Spray-drying is the most popular and widely studied alternative to freeze-drying due to its easiness to operate and scale-up. In all combinations, the ration protein: carbohydrate was They also tested different drying processes: freeze-drying, spray-drying and a two-step drying process first spray-drying followed by vacuum-drying.
The authors demonstrated that spray-drying only fails in terms of bifidobacteria viability maintenance during storage after 1 month only 0. This result suggests that the two-step drying process seems to be an alternative to freeze-drying to produce viable probiotics.
Moreover, this alternative is estimated to be 3 times cheaper than freeze-drying. Taking into consideration the previous results, the authors also studied the effect of different carrier materials on the viability of bacteria, using the two-step drying process. Tanimomo et al. They showed that the protective agents tested had little impact on cell viability prior to freeze-drying. However, after the freeze-drying process, the maximum survival rate obtained was Nevertheless, sucrose exhibited a significant preservation level during storage, however, this protectant was less efficient during freeze-drying.
Based on these findings, the freeze-drying process seems to be a better method for stabilization and storage of Bifidobacterium spp. Celik and O'Sullivan studied the development of a freeze-drying protocol for bifidobacteria with different stress tolerances: B.
Chen et al. They used different cryoprotectants and evaluated the survival rate and viable cell numbers per unit weight of the resulting freeze-dried powder. The results suggested that the best cryoprotectant for B.
Another study using freeze-drying with Bifidobacterium spp. They explored the growth of nine bifidobacterial strains B. As reported previously by Celik and O'Sullivan , B. In terms of ability to grow in milk, seven out of the nine studied strains grew in milk without any added growth factor, and four of these registered an increase of 1—2 log cycles.
Concerning the viability of bacteria in dairy products during cold storage, B. Therefore, different protective strategies like encapsulation have been explored and proposed as a solution for improvement of probiotics. Over the past years, research has focused on alternative strategies to probiotics drying, in order to improve the survival, stability, and delivery of probiotics.
Encapsulation has been highlighted as one such solution since it is known to enhance stability, facilitate handling, and storage of probiotics cultures, protecting them from oxygen and gastrointestinal tract conditions Terpou et al. Sometimes, it can also be used coupled to freeze-drying, improving the stability and storage of probiotics, as described by Heidebach et al. They showed that co-encapsulation of prebiotic resistant starch corns had a negative influence on the physical barrier of the protein matrix, leading to a decrease of the protective effect of the probiotic Heidebach et al.
Thantsha et al. Wang et al. Their findings suggested that chickpea protein-alginate capsules offered a suitable probiotics protection against acid conditions and indicated that such capsules could serve as a suitable probiotic carrier for food applications.
The encapsulation method has an important role in the survival of probiotics, offering protection against unfavorable environmental conditions and allowing for their controlled release under intestinal conditions Terpou et al. There are several methods available for the encapsulation of probiotics, such as spray-drying, freeze-drying, extrusion, emulsion, and ionotropic gelation Table 2.
Table 2. Methods and materials for microencapsulation of Bifidobacterium spp. Spray-drying is also a common method for probiotic encapsulation, where an emulsion or a suspension of the probiotic and the encapsulating agents are atomized in a hot air-drying chamber, resulting in fast evaporation of water. Both studies obtained microcapsules with a higher viability and encapsulation yield after spray-drying, and encapsulated bacteria remained viable and stable during a long period of time and were able to resist simulated gastrointestinal conditions.
Freeze-drying can be used as an encapsulation method but also as a method to improve the probiotic microcapsules storage. Bhat et al. In many cases, Bifidobacterium spp. Amakiri and Thantsha encapsulated B. Moreover, freeze-drying offered an increased protection to bacteria-loaded lipid microparticles, protecting the probiotics from gastric acid and enabling their release at sufficiently high viable cell numbers into the simulated intestinal fluid, allowing them to efficiently colonize the colon.
Microencapsulation by extrusion is the major process for the production of probiotic microcapsules. The probiotic-matrix-mixture is mixed homogeneously and then the mixture is extruded through a syringe needle at high pressure to produce droplets, which will solidify by gelation or formation of a membrane on their surface Rebecca et al.
The obtained capsule size is dependent on the viscosity of the encapsulation material, the nozzle diameter and the droplet height Rebecca et al. However, these capsules are generally large 0. Extrusion was used to encapsulate B. The findings showed that the encapsulation was only effective in promoting protection at freezing temperatures, independently of the strain sensitivity Rebecca et al.
Emulsification is another common technique for probiotics encapsulation; it consists of a mixture of two immiscible liquids in which one of them is in small droplets within another liquid to form a stable mixture Costa et al. The difficulty to obtain uniformly shaped microcapsules between batches is the major drawback of the emulsification technique Marcial-Coba et al. Ji et al. These findings differed from the results of Yeung et al.
Despite the several microencapsulation methods employed to improve probiotic stability and viability further research is required on the design and optimization of appropriate technologies to encapsulate probiotic cells. Key factors that remain true challenges include the probiotic strain type and the processing conditions, namely temperature, oxygen stress, as well as encapsulation material; the probiotic cell size and its concentration can have a direct influence on capsule size which may have negative effect on the sensory proprieties of food Terpou et al.
Among the few potential NGPs, Akkermansia muciniphila , the only cultured member of Verrucomicrobia phylum that abundantly colonizes the human gut Derrien et al.
However, sensitivity to challenging factors such as molecular oxygen, low pH levels found in gastric environment, and bile salts, demand the development of a technological logistic pathway that enables the survival of this anaerobic probiotic candidate. As all other anaerobic bacteria, oxygen levels, and redox potential are a major issue that can lead to a loss in cell viability. Curiously, the idea that A. The manifested oxygen tolerance was previously argued when A. This intrinsic oxygen tolerance A.
Interestingly, the potential temperature effect associated with an oxygen exposure can be further assessed in data pertaining to the strategies explored to successfully protect and deliver viable functional A. According to Marcial-Coba et al. Furthermore, this formulation was able to enhance A. Later, the same authors analyzed the efficacy of dark chocolate as a carrier for A.
These results differ from the first report of encapsulation of A. The generated EE was high Indeed, the implementation of physical protective systems, such as encapsulation, are required to mitigate any viability losses A.
Despite the major differences that were found between aerobic and anaerobic storage, A. Conversely, the A. In this sense, a synthetic media was recently developed that respected safety clinical parameters for human administration allowing large scale cultivation approaches Plovier et al.
These results were further substantiated in vivo with the administration of A. Furthermore, progress was already made relative to a potentially scalable preservation and preparation protocol for the use of viable A. Such efforts will allow the use of this anaerobic NGP as an interventional therapeutic tool in cardiometabolic diseases, just as in the first A.
As mentioned before Faecalibacterium prausnitzii has become one of the most promising commensal and ubiquitous bacteria among NGPs candidates due to its positive impact on the microbiota and the host's health Benevides et al. Despite multiple health promoting-effects, F.
However, it has been found that it can endure low levels of oxygen by adherence to the gut mucosa where oxygen diffuses from epithelial cells, through an extracellular electron shuttle of flavins and thiols to transfer electrons to oxygen Khan et al. Based on the previous finding, it was demonstrated that F. Improved formulations were obtained by addition of the bulking agents corn starch and wheat bran, easing the handling Khan et al. Recently, Bircher et al.
Interestingly, they verified that F. In this alignment, Allouche et al. Nevertheless, these researchers highlighted the need to find alternatives to anaerobic storage as well as the urgency to develop an optimal coating to protect bacteria against gastric acidity Allouche et al. Thus, to reduce or eliminate the presence of oxygen in technological processes such as formulation or freeze drying, the employment of antioxidants, cryoprotectants, and prebiotic agents is of extreme importance in order to enhance the viability and stability during aerobic storage of NGPs Almeida et al.
The inherent novelty to NGPs entails little data concerning the production of delivery vehicles of commensal anaerobic bacteria, as well as their viability and stability during storage, considering that these parameters are modified with the probiotic strain involved O'Toole et al.
In this context, cryopreservation, and freeze-drying techniques have also been explored as strategies to enhance the viability and stability of commensal anaerobic bacteria Bircher et al.
In this study, researchers concluded that B. Results revealed that gut butyrate producers can be well-preserved with glycerol and inulin during frozen storage Bircher et al. Moreover, encapsulation techniques have been employed to develop delivery systems containing commensal gut anaerobic bacteria. In fact, Eeckhaut and colleagues developed hydroxypropylmethylcellulose capsules containing commensal anaerobic bacterium B. It is important to note that in this study B.
Later, Boesmans et al. Furthermore, they verified that these capsules were safe and well-tolerated by the human host, without causing disruptive alterations in the composition or metabolic activity of health-associated microbiota Boesmans et al. Still in the context of strict anaerobic bacteria encapsulation, Cui showed that double encapsulation of C.
Furthermore, this researcher incorporated C. Certain human commensals, such as those discussed above, which are particularly abundant in healthy individuals compared to patients in various diseases groups, are already being sought to be used to address and mitigate some clinical situations. Other novel microorganisms may be expected to emerge in the next years from the continuous efforts made to investigate the role of the human microbiome. These developments will present substantial challenges for the scientific community and for the interested industry stakeholders.
In order to enable intervention performance in clinical trials, biomass has to be produced in high amounts as economically as possible , be adequately stable and safe for human usage. Bifidobacteria are human anaerobic commensals that are supported by a long tradition of being used in the food and supplement industries, but still only a few technological robust strains are commonly used.
Continuous efforts are being made to obtain stable and functional products containing bifidobacteria as other probiotics. In this context, the use of sublethal stresses and of microencapsulation have been two of the most investigated strategies and with some promising results. The experience gathered in the studies with bifidobacteria may be applied and be used as a basis for the development of other anerobic commensals products.
In fact, some preliminary promising studies of microencapsulation of Akkermansia strains have already been reported. AF, AG, and JA contributed to the concept and design of the manuscript, critical revision, editing, and funding acquisition.
All authors contributed to manuscript revision, read, and approved the submitted version. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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