Changes of cell size distribution maximum, cell relative content with size distribution maximum and half-width of curves of cell size distribution of D. acetoxidans IMV B-7384 during five days of cultivation (five repeats, P ≤ 0.05)
\\n\\n
More than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\\n\\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\\n\\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\\n\\nAdditionally, each book published by IntechOpen contains original content and research findings.
\\n\\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\\n\\n\\n\\n
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'
Simba Information has released its Open Access Book Publishing 2020 - 2024 report and has again identified IntechOpen as the world’s largest Open Access book publisher by title count.
\n\nSimba Information is a leading provider for market intelligence and forecasts in the media and publishing industry. The report, published every year, provides an overview and financial outlook for the global professional e-book publishing market.
\n\nIntechOpen, De Gruyter, and Frontiers are the largest OA book publishers by title count, with IntechOpen coming in at first place with 5,101 OA books published, a good 1,782 titles ahead of the nearest competitor.
\n\nSince the first Open Access Book Publishing report published in 2016, IntechOpen has held the top stop each year.
\n\n\n\nMore than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\n\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\n\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\n\nAdditionally, each book published by IntechOpen contains original content and research findings.
\n\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\n\n\n\n
\n'}],latestNews:[{slug:"intechopen-authors-included-in-the-highly-cited-researchers-list-for-2020-20210121",title:"IntechOpen Authors Included in the Highly Cited Researchers List for 2020"},{slug:"intechopen-maintains-position-as-the-world-s-largest-oa-book-publisher-20201218",title:"IntechOpen Maintains Position as the World’s Largest OA Book Publisher"},{slug:"all-intechopen-books-available-on-perlego-20201215",title:"All IntechOpen Books Available on Perlego"},{slug:"oiv-awards-recognizes-intechopen-s-editors-20201127",title:"OIV Awards Recognizes IntechOpen's Editors"},{slug:"intechopen-joins-crossref-s-initiative-for-open-abstracts-i4oa-to-boost-the-discovery-of-research-20201005",title:"IntechOpen joins Crossref's Initiative for Open Abstracts (I4OA) to Boost the Discovery of Research"},{slug:"intechopen-hits-milestone-5-000-open-access-books-published-20200908",title:"IntechOpen hits milestone: 5,000 Open Access books published!"},{slug:"intechopen-books-hosted-on-the-mathworks-book-program-20200819",title:"IntechOpen Books Hosted on the MathWorks Book Program"},{slug:"intechopen-s-chapter-awarded-the-guenther-von-pannewitz-preis-2020-20200715",title:"IntechOpen's Chapter Awarded the Günther-von-Pannewitz-Preis 2020"}]},book:{item:{type:"book",id:"5505",leadTitle:null,fullTitle:"Superfood and Functional Food - An Overview of Their Processing and Utilization",title:"Superfood and Functional Food",subtitle:"An Overview of Their Processing and Utilization",reviewType:"peer-reviewed",abstract:"This book focuses on the usage and application of plant- and animal-based food products with significant functional properties and health benefits as well as their development into processed food. Many chapters in this book contain overviews on superfood and functional food from South America. Details on the functional properties of apiculture products are also included herein. Additionally, an area that is not widely discussed in academia - pet food with functional properties - is also covered. It is hoped that this book will serve as a source of knowledge and information to make better choices in food consumption and alterations to dietary patterns. \nIt is also recommended for readers to take a look at a related book, Superfood and Functional Food - The Development of Superfoods and Their Roles as Medicine.",isbn:"978-953-51-2920-2",printIsbn:"978-953-51-2919-6",pdfIsbn:"978-953-51-5471-6",doi:"10.5772/63180",price:139,priceEur:155,priceUsd:179,slug:"superfood-and-functional-food-an-overview-of-their-processing-and-utilization",numberOfPages:356,isOpenForSubmission:!1,isInWos:1,hash:"1c054794ab111a6e0a6bfebeb77baa8e",bookSignature:"Viduranga Waisundara and Naofumi Shiomi",publishedDate:"March 1st 2017",coverURL:"https://cdn.intechopen.com/books/images_new/5505.jpg",numberOfDownloads:26169,numberOfWosCitations:18,numberOfCrossrefCitations:23,numberOfDimensionsCitations:61,hasAltmetrics:0,numberOfTotalCitations:102,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"May 2nd 2016",dateEndSecondStepPublish:"May 23rd 2016",dateEndThirdStepPublish:"August 27th 2016",dateEndFourthStepPublish:"November 25th 2016",dateEndFifthStepPublish:"December 25th 2016",currentStepOfPublishingProcess:5,indexedIn:"1,2,3,4,5,6",editedByType:"Edited by",kuFlag:!1,editors:[{id:"194281",title:"Dr.",name:"Viduranga Yashasvi",middleName:null,surname:"Waisundara",slug:"viduranga-yashasvi-waisundara",fullName:"Viduranga Yashasvi Waisundara",profilePictureURL:"https://mts.intechopen.com/storage/users/194281/images/system/194281.jpg",biography:"Dr. Viduranga Waisundara obtained her Ph.D from the Department of Chemistry, National University of Singapore in Food Science & Technology in 2010. She was a lecturer at Temasek Polytechnic, Singapore from July 2009 to March 2013. She relocated to her motherland of Sri Lanka and spearheaded the Functional Food Product Development Project at the National Institute of Fundamental Studies from April 2013 to October 2016. She was a Senior Lecturer on a temporary basis, at the Department of Food Technology, Faculty of Technology, Rajarata University of Sri Lanka. She is currently the Deputy Principal of the Australian College of Business & Technology – Kandy Campus, in Kandy, Sri Lanka. She is also the present Global Harmonization Initiative (GHI) Ambassador to Sri Lanka.",institutionString:"Australian College of Business & Technology",position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"10",totalChapterViews:"0",totalEditedBooks:"7",institution:null}],equalEditorOne:null,equalEditorTwo:null,equalEditorThree:null,coeditorOne:{id:"163777",title:"Prof.",name:"Naofumi",middleName:null,surname:"Shiomi",slug:"naofumi-shiomi",fullName:"Naofumi Shiomi",profilePictureURL:"https://mts.intechopen.com/storage/users/163777/images/system/163777.jpeg",biography:"Dr. Naofumi Shiomi studied recombinant yeast and its utilization as a researcher at the Laboratory of Production Technology of Kanena Corporation for 15 years until 1998, and earned his PhD in Engineering from Kyoto University. 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The need for reducing dependence on fossil fuels and the promoting the use of renewable fuels requires the development of alternative sources such as waste biomass for environmental benefits and alternative global energy supplies [1]. Microbial fuel cells (MFCs) provide new opportunities for the sustainable production of energy from biodegradable and reduced compounds, and thus, have attracted substantial research efforts to develop various devices for generating electricity and removing wastes [1, 2]. The development of processes that can use bacteria to produce electricity represents a highly effective method for bioenergy production as the bacteria are self-replicating, and thus the catalysts of organic matter oxidation are self-sustaining [2]. The substrates used in MFCs range from carbohydrates (e.g. glucose, sucrose, cellulose, starch), volatile fatty acids (e.g. formate, acetate, butyrate), alcohols (e.g. ethanol, methanol), amino acids, proteins and even inorganic components such as sulfides or acid mine drainages [2, 3-9]. The type of substrate fed to a MFC potentially has an impact on the structure and composition of the microbial community. Untill now, no clear image of the effect of the type of substrate on electricity generation by the microbial fuel cells is available.
Analysis of external resistances, electron donor concentrations, cell densities, rates of electron transfer to electrodes at various voltages, and anode potentials can aid in understanding the power production capabilities using microorganisms [10]. A simplified model for the conversion of complex organic fuels to electricity is shown in figure 1 [10].
Usage of organic substrates as electron donors in microbial fuel cell [10]
Complex organic matter is hydrolyzed to constituents that in the most cases are primarily fermented, but there are microorganisms that can completely oxidize such compounds with an electrode serving as the sole electron acceptor or incompletely oxidize these substrates with electron transfer to an electrode [10]. Acetate and some other minor fermentation acids can be completely oxidized to carbon dioxide and it is typically the primary source of electrons for current production [10].
MFC is considered to be used also for hydrogen production from the generated potential of the organic matter electrolysis by bacteria [2].
Microbial fuel cell technologies also are a promising and yet completely distinct approach to wastewater treatment as the treatment process can become a method of capturing energy in the form of electricity or hydrogen gas, rather than a drain on electrical energy [2]. Wastewater treatment processes currently employ the biological activities of complex microbial biofilms to remove organic pollutants [11]. The most significant energy savings associated with the use of MFCs for wastewater treatment, besides electricity generation, result from savings in expenses for aeration and solids handling, because the major operating costs for wastewater treatment are wastewater aeration, sludge treatment, and wastewater pumping. The MFC process is inherently an anaerobic process, although, oxygen can diffuse into the system resulting in some aerobic organic matter removal [10].
At the same time, wastewater contains high concentrations of xenobiotics, such as heavy metal ions that have an overwhelming harmful effect towards all living organisms. These substances even in small concentration in the environment cause the increasing inhibition of physiological and biochemical properties of the most bacteria. Despite that, some genera of bacteria possess high resistance according to toxic heavy metals influence because of functioning of highly-efficient mechanisms of antioxidant defense system, ion efflux transport enzyme complexes etc. Examples of these genuses are Feroplasma, Streptomyces, Thiobacillus, Desulfuromonas etc [12]. The specific metal-transport systems that were found in gram-negative bacteria which support transport of iron, zinc and manganese, copper, nickel and cobalt are schematically presented in figure 2 [13].
Schematic metal homeostasis models for iron, zinc and manganese, copper, nickel and cobalt in gram-negative bacteria [13]
The variety of ion transport systems in gram-negative bacteria represents sophisticated mechanisms of bacterial cell metal homeostasis regulation. This is possible because of the formation of specific protein-metal coordination complexes used to effect uptake, efflux, intracellular trafficking within compartments, and storage [12].
Previous research has shown that gram-negative bacterium Desulfuromonas acetoxidans possesses resistance to copper, cadmium, lead, zinc, manganese, iron, etc. [14, 15]. Bacteria of Desulfuromonas genus are also shown to be highly effective in term of electricity generation [2, 16, 17]. However the research on its application as the anode biocatalyst in MFC is inadequate. Desulfuromonas sp. can be very promising for MFC development because of inexpensive cultivation medium, high survival rate and resistance to toxic xenobiotics such as the various metal ions [2].
D. acetoxidans, which belongs to the class ∂-Proteobacteria, are uncolored obligate anaerobes that inhabit sulfur containing aquatic environments [18]. D. acetoxidans supports reductive stage of sulfur cycle in the nature, but it can not possess an ability to reduce sulfate or other oxoanions of this element. Sulfur is a crucial component of various biological active substances, such as vitamins, coenzymes, several amino acids etc. This is an element with variable valence, which participates in the different chemical and biochemical redox-reactions [19]. Sulfur deposits formation is tightly bound with the process of sulfate-reduction, which is carried out exclusively by microorganisms. SO42-is the prevalent hydrogen acceptor in the processes of organic matter destructions under anaerobic conditions. Majority of strains can use unspecific electron acceptors, such as L-malate or fumarate, instead of sulfur [20]. S0-reduction by D. acetoxidans causes hydrogen sulfide production. Using metal-resistant strains of these bacteria also helps overcome H2S toxicity since divalent cations will interact with sulfide ions, forming insoluble precipitates in form of metal sulfides. D. acetoxidans contains NiFe-hydrogenase [20], which catalyses hydrogen uptake and production; polysulfide reductase [19], which supports sulfur reduction with hydrogen sulphide formation, and specific metaloreductase that reduce Fe3+and Mn4+ with formation of magnetite (Fe3O4), siderite (FeCO3) and rhodochrosite (MnCO3) as final products of Fe (ІІІ)-and Mn (IV)-dissimilative reductions [21].
Several redox-proteins have been elucidated of the cells of D. acetoxidans [22]. This bacterium, similarly to Desulfovibrio sp., contains huge amount of cytochromes c-type, which possibly are involved in the electron transport to the elemental sulfur. Multiheme cytochromes c-type are shown to possess metaloreductase activity, which possibly could have practical application in metal ions bioremediation from the environment. It was found that electric current production in MFCs operated with different organisms such as Shewanella oneidensis, Pelobacter carbinolicum or Geobacter sulfurreducens requires the presence of multiheme cytochromes c [23, 24]. Given the clear interest in D. acetoxidans for alternative processes of energy generation, the identification and understanding of the role of the macromolecular components responsible for these metabolic capabilities becomes a priority. Recently the final draft genome of D. acetoxidans was made available by the Joint Genome Institute [25] coding for "cytochromome" of 47 putative multiheme cytochromes c-type. Of those, up to now only the triheme cytochrome c7 was characterized in detail. Its structure in the fully oxidized and fully reduced states, its thermodynamic and kinetic redox properties and its thermodynamic stability has been reported in the literature [22]. It shows high similarity to tetraheme cytochrome c3, extracted from sulfate-reducing bacteria [26]. Cytochrome synthesis by bacteria is observed under usage of insoluble extracellular electron acceptors, such as sulfur.
D. acetoxidans can obtain energy as a result of sulfur respiration and complete acetate oxidation via the citric acid cycle [27]:
This is the first investigated microorganism, which obtains energy by the complete acetate oxidation under the anaerobic conditions. It was shown that only 4% of consumed acetate by bacteria was assimilated into the cell material [28]. D. acetoxidans contains a succinyl-CoA: acetate CoA transferase instead of an acetyl-CoA synthetase and a succinyl-CoA synthetase. The succinyl-CoA: acetate-CoA transferase couples the formation of succinate from succinyl-CoA with the activation of acetate. The enzymes required for the assimilation of acetate and CO2 into pyruvate are acetyl-CoA synthetase and pyruvate synthase [27]. C14-labeling experiments shown that D. acetoxidans metabolism includes synthesis of oxaloacetate from acetate and 2CO2 as anaplerotic reaction while most organisms oxidizing acetate to CO2 by using the glyoxylate bypass for this function. Besides acetate, D. acetoxidans can completely oxidize L-malate, fumarate, propionate, ethanol etc as electron donors. D. acetoxidans was one of the first electrogenic bacterium described, a microorganism performing complete oxidation of an organic substrate with electron transfer directly to the electrode. It was calculated that in the fuel cell that contains acetate as the sole electron donor up to 82% of acetate is oxidized by D. acetoxidans with an electrode as the terminal electron acceptor [29]. Therefore, D. acetoxidans accumulates energy for growth by electron transfer to the electrodes. Similar results were obtained with Geobacter metallireducens, oxidizing aromatic compounds, and the predominantly freshwater G. sulfurreducens [17, 30].
Thus, D. acetoxidans has a crucial role in the biosphere and shows prospect of prosperous development of microbial fuel cell with simultaneous control of toxic metals environmental pollution because of formation of insoluble precipitates of metal sulfides. Although profound analyses of D. acetoxidans physiology and its linkage with power generation in MFC and organic matter consumption need to be established for its efficient application as the anode biocatalyst in microbial fuel cell.
Microbial strain D. acetoxidans IMV B-7384, which was applied in these investigations, belongs to the Ukrainian Collection of Microorganisms of D.K. Zabolotny Institute of Microbiology and Virology of NAS of Ukraine. Bacteria have been cultivated under the anaerobic conditions in the modified Postgaite C medium [20] in which sterile sulfur (10 g/l) and biotin (20 μg) were added before cultivation. Biotin served as a growth factor. Optimal pH for growth was 6.8-7.5 and optimal temperature was 30 0C.
Bacterial growth commonly can be investigated by the registration of bacterial suspension turbidity or by the methods of dynamic or static light dispersion. The new method of rapid measurement of cell size distribution and their relative content, which is based on cell light scattering changes [31, 32] is proposed in this study. It includes the sounding of flow suspended bacterial cells by monochromatic coherent light, the registration of cooperative signals of sounding radiation and the explored microbiological objects by detecting of amplitudes and duration of scattered light impulses. The distribution of particles in size is determined on the basis of the measured functional dependence of the number of registered particles upon the amplitude and duration of corresponding electric impulses on the photoreceiver output by solving integral equation of Fredholm of the first kind (1):
where rmin and rmax – upper and lower limits of particle size distribution, which is registered;
n(r) – the function of particle size distribution;
K(U,t,r) – the function of distribution of normalized values of amplitude and duration of registered impulses of scattered light by the calibrating particles, which is a result of the previous probing of liquid flow by the monochromatic coherent light of the polymeric latex with set sizes and known refractive index.
However, presence of bacterial metabolism products in the growth medium could lead to errors in cell size distribution measurement because of additional light scattering. These errors were eliminated in the next way. Bacteria were cultivated in the liquid growth medium. Dependence between quantities of microbial cells and background particles in the growth medium had been determined during the time of bacterial cultivation. Liquid growth medium with and without bacterial cells was diluted in the same proportions by using highly purified liquid (deionized water). Then were registered separately the total quantity of cells and background particles in the highly purified liquid, which contains cells, and the total size distribution of background particles in the growth medium without cells. Then, relative content of bacterial cells was determined in the chosen interval of sizes, which equaled 0.3-1.9 μm. The cells relative content was measured by the calculation of quantity ratio of the set size cells to their total quantity. Specimens for determination of cell size distribution were prepared by dilution of 1 ml of bacterial suspension in 100 ml of deionized water [31, 32]. Measurements have been carried out by using the equipment PRM-6M, which was constructed at the Laboratory of Optical-Electronic Device of Faculty of Electronics of Ivan Franko National University of Lviv. The errors of cell size distribution measurement of constructed equipment are 5%.
After the third day of D. acetoxidans IMV B-7384 growth, the cells were harvested by centrifugation (2500 g, 30 min, 4°C) and washed three times in a buffer (50 mM potassium-phosphate buffer, pH 7.5). Intact cells were fixed at 1.5% KMnO4 solution during 20 min under the room temperature (20 0C). Post-fixation was carried out with 1% OsO4 in cacodylic buffer during 90 min under 0 0C. Fixed cells were washed and dehydrated in solutions with gradient concentrations of ethanol and propylene oxide. Specimens were fixed in epoxy Epon 812. Ultrathin cross-sections were obtained with the ultramicrotome UMTP-6 and contrasted by lead citrate [33]. Electron photographs were obtained by transmission electron microscopes UEMB-100B and PEM-100 at acceleration voltage 75 kV. Final photographs magnification – 10000 times.
Antioxidant defense system activity has been measured in the cell-free extract after the second, third and fourth day of bacterial growth. Cells were washed by 0.9% NaCl solution and disintegrated on the ultrasonic homogenizer at 22 kHz at 0ºC during five minutes. Cell debris were sedimented by centrifugation at 5640-8800g at 4 ºC during 30 minutes. Catalase activity was measured spectrophotometrically at λ=410 nm by the degree of breakdown of hydrogen peroxide in the cell-free extract [34]. Superoxide dismutase activity was measured by the level of inhibition of 2,3,5-triphenyltetrazolium chloride reduction that follows formazan formation (absorbance maximum λ=405 nm) [35, 36]. Reduced glutathione content has been measured by the degree of dithionitrobenzoic acid reduction in cell-free extract (absorbance maximum λ=412 nm) [37].
In this study two chamber microbial fuel cell has been constructed, in which D. acetoxidans IMV B-7384 was applied as the anode biocatalyst. Bacteria were cultivated in the modified Postgaite С medium [20] without sulfates under the anaerobic conditions and temperature 25-28 0C during twenty days in MFC. 0.1% potassium permanganate solution served as catholyte and bacterial suspension with 0.30±0.05 g/l dry cell weight/liter initial biomass served as anolyte respectively. 0.1% KMnO4 was replaced after 14 days of bacterial growth in MFC. Anode and cathode chambers with 0.3 l volume were separated by proton-exchange membrane (Millipore) with surface area of 2.5 cm2. Graphite rods with the surface area of 130 cm2 were applied as electrodes. Graphite is electrically conductive and conforms to the requirements of electrodes in MFC: non-corrosive, highly conductive, large surface area, high porosity etc [2]. Bacteria were cultivated periodically in the anode chamber of constructed MFC under separate addition of such electron donors as acetic, lactic and fumaric acids in form of sodium salts in concentrations 6 and 9 g/l. Electrode material served as the sole electron acceptor. All experiments were conducted under strictly sterile conditions.
Electric current and voltage generation in constructed MFC were determined from the measured voltage drop across the resistor by multimeter DT-830C. The external load resistor with value 2.2 kΩ, which was shown to be the most optimal in constructed microbial fuel cell, was applied. The power output of an MFC was calculated from the measured voltage, EMFC, across the load and the current as (2):
Power generation by D. acetoxidans IMV B-7384 was investigated during twenty days of bacterial growth under the application of lactic, acetic and fumaric acids in form of their sodium salts.
Biomass accumulation of D. acetoxidans IMV B-7384, its cell size distribution and relative content changes have been carried out [14, 15]. Investigated bacterium has been shown to accumulate biomass the most intensively during third-fourth days of its growth. (fig. 3). Since bacterial growth processes were shown to be maximal during third-fourth days of cultivation, possibly, the highest power output in microbial fuel cell should be observed during this period.
Changes of D. acetoxidans IMV B-7384 biomass during ten days under normal cultivation conditions (addition of lactic acid (6 g/l) and elemental sulfur (10 g/l) respectively as electron donor and acceptor)
Electron micrographs of D. acetoxidans IMV B-7384 cross-sections are presented on the fig. 4. Cells were obtained on the third day of their growth when maximal bacterial biomass accumulation was observed. These are rod shaped or slightly curved cells.
Cross-sections of the cells of D. acetoxidans IMV B-7384, harvested under normal growth conditions (third day) (electron micrograph (TEM), ×10000 times; bar, 0.5 μm)
Bacterial growth usually is characterized by increasing of cell quantity or cell size. Thus, analyses of cell size distribution and their relative content allow to obtain more detailed data of cell growth and division processes under various cultivation conditions in comparison with standard turbidimetric method of biomass measurement. Proposed method of cell light scattering determination allows to calculate possible changes of cell division on the basis of cumulative analyses of three histogram parameters: cell size distribution maximum, cell relative content and half-width of cell size distribution. It can be the basis for inventing of new methodologies for obtaining of synchronous cell cultures and also for development of new effective cytometers with low self-cost and high productivity.
Cell size distribution maximum equaled 0.55±0.01 μm on the third day of D. acetoxidans IMV B-7384 growth (period of maximal biomass accumulation). Cell relative content increased from 0.275 to 0.420 relative units under normal growth conditions on the third day of bacterial cultivation (fig. 5).
Medial values of D. acetoxidans IMV B-7384 cell relative content and size distribution during the third day of growth (five repeats, P ≤ 0.05)
From the first to the fifth day of D. acetoxidans IMV B-7384 growth the maximum of cell size distribution was 0.49-0.55±0.01 μm and cell relative content with the maximum of size distribution changed from 0.275±0.011 to 0.398±0.011 relative units (table 1). Half-width of cell size distribution curves decreased from 0.23±0.01 to 0.14±0.01 μm with the increase of bacterial cultivation time from the first to the third day.
\n\t\t\t\tTime of cultivation, day\n\t\t\t | \n\t\t\t\n\t\t\t\tCell size distribution maximum, μm\n\t\t\t | \n\t\t\t\n\t\t\t\tCell content with size distribution maximum, relative units\n\t\t\t | \n\t\t\t\n\t\t\t\tHalf-width of cell size distribution curves, μm\n\t\t\t | \n\t\t
1 | \n\t\t\t0.55±0.01 | \n\t\t\t0.275±0.011 | \n\t\t\t0.23±0.01 | \n\t\t
2 | \n\t\t\t0.55±0.02 | \n\t\t\t0.268±0.009 | \n\t\t\t0.23±0.03 | \n\t\t
3 | \n\t\t\t0.55±0.01 | \n\t\t\t0.420±0.022 | \n\t\t\t0.14±0.01 | \n\t\t
4 | \n\t\t\t0.49±0.01 | \n\t\t\t0.383±0.14 | \n\t\t\t0.14±0.02 | \n\t\t
5 | \n\t\t\t0.55±0.02 | \n\t\t\t0.398±0.011 | \n\t\t\t0.16±0.01 | \n\t\t
Changes of cell size distribution maximum, cell relative content with size distribution maximum and half-width of curves of cell size distribution of D. acetoxidans IMV B-7384 during five days of cultivation (five repeats, P ≤ 0.05)
It indicated the decrease of cell size variations with the increase of cultivation time. Obviously, it is caused by intensive bacterial division on the third-fourth days of their cultivation. As a result cell’s relative content with lower size distribution maximum (0.49±0.01 μm) increased in comparison with its initial value with higher maximum (0.55±0.01 μm). Possible inhibition of cell division on the fifth day of bacterial growth caused increase of cell relative content with higher size distribution maximum, which equaled 0.55±0.02 μm.
Thus, it was shown that the maximal biomass accumulation is observed during third-fourth day of bacterial growth. High value of cell relative content with size distribution maximum and intensive decrease of half-width of cell size distribution indicates on significant increase of cell quantity with lower size distribution maximum. It is a possible result of intensive cell division during this time. Overall analysis of mentioned above parameters allow to assume that D. acetoxidans IMV B-7384 are in the middle of exponential phase of growth during the third day of their cultivation under normal growth conditions. Thus, the most intensive biosynthesis processes and power generation in microbial fuel cell possibly overlap this period of bacterial cultivation or immediately afterwards.
The activity of antioxidant defense system of D. acetoxidans IMV B-7384 has been revealed under the influence of external stress factors, such as Ferric iron, Ferrous iron, Nickel, Cobalt and Copper salts. It includes:
biosynthesis of reduced glutathione (GSH), a tripeptide that serves as universal electron donor detoxifying reactive oxygen species [38];
activity of catalase and superoxide dismutase, a basic enzymes of antioxidant defense system [36, 39].
Reactive oxygen species (ROS) such as superoxide radical, hydrogen peroxide, hydroxyl radical etc are produced as a result of prolonged influence of oxygen or toxic xenobiotics, such as heavy metal ions, on the living cell. Glutathione (γ-L-glutamyl-L-cysteinylglycine) is the most abundant intracellular thiol-dependent antioxidant, which protects living cells against oxidative stress. It has low redox-potential (Е\'0=-240 mV under pH=7.0) and it is constantly maintained in reduced state because of NADF-glutathione reductase functioning. Therefore it serves as cellular redox-buffer [40]. Superoxide dismutase catalyzes disproportionation of superoxides with oxygen and hydrogen peroxide formation. Catalase causes decomposition of produced H2O2 with neutralization of its toxicity. Н2О and О2 are final products of this reaction [41]. Thus, aforementioned components of antioxidant defense system protect the cell against oxidative stress, which may be caused by reactive oxygen species.
It was revealed that under the influence of various concentrations of FeSO4, FeCl3, MnCl2, NiCl2, CoCl2 and CuCl2 on the cells of D. acetoxidans IMV B-7384 activity of antioxidant defense system appears in spite of their obligate anaerobic metabolism. At fig. 6 is presented the complete scheme of the dependences between the highest values of catalase and superoxide dismutase activity and glutathione content, which were observed in the cells of investigated bacteria during four days of their cultivation.
Maximal observed values of reduced glutathione content and superoxide dismutase, and catalase activity in the cell-free extract of D. acetoxidans IMV B-7384 under the influence of 0.5-2.5 mM of FeSO4, FeCl3, MnCl2, NiCl2, CoCl2 and CuCl2 during four days of bacterial cultivation [36, 38, 39]
Obtained results show that investigated bacteria possess specific mechanisms of rapid defense against toxic influence of external factors, such as high concentrations of various metal ions. It allows to assume their tolerance according to detrimental xenobiotics, which wastewaters are enriched with. This shows the prospect of D. acetoxidans IMV B-7384 application into wastewater treatment with simultaneous power generation in MFC. Also specific activity of antioxidant defense system enzymes, such as catalase and superoxide dismutase could help to prevent harmful influence of reactive oxygen species on the integrity of proton-exchange membranes in microbial fuel cells. Since catalase causes two-electron decomposition of H2O2 with O2 and H2O production, this enzyme could prevent Fenton reaction: Мn+(=Cu+, Fe2+, Ti3+, Co2+)+H2O2\n\t\t\t\t\t
External load resistance in microbial fuel cell is one of the crucial factors, which influence the electricity generation. Correlation between value of external load resistance and power generation in constructed MFC was determined. The influence of changes of external load resistance on volt-ampere characteristic of constructed MFC was investigated during D. acetoxidans IMV B-7384 cultivation in Postgaite C medium under normal growth conditions on the third-beginning of the fourth day, when the highest power generation was observed (fig. 7).
Power generation by D. acetoxidans IMV B-7384 during eight days under normal cultivation conditions in MFC, and application of 0.2 kΩ external load resistor
The maximal value of power density equaled 4.7 mW/m2 on 84 hour of bacterial cultivation with addition of lactate (6 g/l) as electron donor and elemental sulfur (10 g/l) as electron acceptor (normal growth conditions), and application of an external load resistor of 0.2 kΩ. With the increase of cultivation time till 192 hour (eighth day of growth) generated power decreased by 42% in comparison with its maximal value.
With the aim to determine the most optimal load in term of electricity generation by D. acetoxidans IMV B-7384 in constructed MFC, external load resistors with values of 0.45-8.15 kΩ were applied in this investigation. The highest current strength and voltage were observed in constructed MFC under application of external load resistor with value of 2.2 kΩ (fig. 8). The highest power density, which was obtained in MFC under these conditions, equaled 5.8 mW/m2. Increasing of external load resistor value caused decrease of generated power.
Therefore, all further experiments on MFC development were carried out with application of such external load resistance (2.2 kΩ), which was shown to be the most effective in term of electric power generation by D. acetoxidans IMV B-7384 in constructed MFC.
Volt-ampere characteristic of constructed MFC under the influence of various external load resistances on the third-beginning of the fourth days of D. acetoxidans IMV B-7384 growth under normal cultivation conditions
Accurate selection of external load resistance plays an important role in effective MFC development, because it significantly influences the value of generated power by bacteria, which are cultivated under different conditions in constructed MFC.
In previous researches it was shown that maximal power output equaled 4.3 mW/m2 under addition the external electron acceptors, such as sulfur and Ferric iron in concentrations, which are favorable for D. acetoxidans IMV B-7384 metabolism [43]. Excluding of these additional electron acceptors and external load resistance optimization caused increasing of power output in constructed MFC.
Lactic acid was applied as the sole organic electron donor in concentrations 6 and 9 g/l during D. acetoxidans IMV B-7384 cultivation in the anode chamber of constructed microbial fuel cell. The highest power output equaled 5.74±0.29 mW/m2 on the 64 hour (third day) of D. acetoxidans IMV B-7384 cultivation under addition of 6 g/l of C3H6O3 (fig. 9). Its value decreased by 41% in comparison with the maximal power, obtained in this investigation by 250 hour of bacterial cultivation (tenth day). Power output equaled 1.33±0.18 mW/m2 on the 480 hour of bacterial cultivation (twentieth day), which was lower by 77% in comparison with its maximal value.
Thus, gradual lactate oxidation and the following diminishing of its quantity in the anode chamber because of bacterial growth in MFC caused gradual decrease of produced power with the increase of duration of cultivation time. Thus, application of lactic acid as the single electron donor in the aforementioned concentration in constructed MFC can’t be used for sustainable long-term electricity generation.
Concentration of lactic acid in the anode chamber has been increased up to 9 g/l. Under these cultivation conditions the highest power output equaled 5.90±0.21 mW/m2 on the 64 hour (third day) of D. acetoxidans IMV B-7384 cultivation (fig. 10). After ten days it decreased by 37% in comparison with its highest measured value. By the 480 hour (the twentieth day) of D. acetoxidans IMV B-7384 cultivation power production in constructed MFC decreased by 33% in comparison with its maximal measured value.
Power density in MFC during twenty days under addition of 6 g/l of lactic acid into the growth medium of D. acetoxidans IMV B-7384
Increase of lactic acid content in the anode chamber caused enhance of stability of power generation in constructed MFC, but such manipulation did not boost its value significantly in comparison with application of lower concentration of lactic acid.
Power density in MFC during twenty days of D. acetoxidans IMV B-7384 cultivation under application of 9 g/l of lactic acid
Thus, lactic acid as the sole electron donor in high concentrations supports durability of constructed MFC with application of D. acetoxidans IMV B-7384 as the anode biocatalyst. However, its effectiveness does not change significantly under the application of lower and higher lactic acid concentrations.
With the aim to determine the most optimal electron donor in term of electricity generation lactic acid has been substituted by fumaric acid in the anode chamber of constructed MFC. The highest value of generated power equaled 5.69±0.29 mW/m2 on the 56 hour (the third day) of bacterial cultivation under usage of 6 g/l of fumaric acid as the sole electron donor (fig. 11). It’s value decreased by 38% on the 250 hour (the tenth day) and by 43% on the 480 hour (the twentieth day) of D. acetoxidans IMV B-7384 cultivation. The medial power density, which was observed under these cultivation conditions equaled 3.58±0.20 mW/m2.
Power density in MFC during twenty days under addition of 6 g/l of fumaric acid into the growth medium of D. acetoxidans IMV B-7384
Thus, application of fumaric acid (6 g/l) causes higher stability of power generation by investigated bacteria in constructed MFC in comparison with the lactic acid in the same concentration. Therefore, fumaric acid is more preferable electron donor in term of power generation by D. acetoxidans IMV B-7384 in comparison with application of lactic acid.
It was shown that increase of fumaric acid concentration up to 9 g/l caused maximal power generation (2.38±0.10 mW/m2) at 56 hour (fig. 12).
Power density in MFC during twenty days under addition of 9 g/l of fumaric acid into the growth medium of D. acetoxidans IMV B-7384
It was less by 2.4 times in comparison with the highest power density value, which was observed under bacterial cultivation with application of less concentration of fumaric acid (6 g/l). The minimal observed power density value equaled 1.95±0.047 mW/m2 on the 160 hour of bacterial cultivation under these conditions. Increasing of cultivation time caused insignificant enhance of power production. On the 480 hour it value equaled 1.97±0.07 mW/m2, which was less by 17% in comparison with its maximal measured value in this investigation.
Thus, increase of fumaric acid concentration from 6 to 9 g/l in the anode chamber of constructed MFC reduced its productivity but enhanced its stability in comparison to the application of lower concentration of investigated electron donor.
Acetic acid was applied as the separate electron donor in constructed MFC. It was shown that the maximal power value equaled 5.78±0.24 mW/m2 on the 40 hour (second day) of bacterial cultivation under addition of 6 g/l of CH3COOH (fig. 13).
Power density in MFC during twenty days under addition of 6 g/l of acetic acid into the growth medium of D. acetoxidans IMV B-7384
Its value decreased by 42% on the 232 hour (10 day) of D. acetoxidans IMV B-7384 growth. Generated power insignificantly enhanced with the increase of cultivation time. It equaled 3.1±0.12 mW/m2 on the 480 hour of bacterial cultivation. Thus, application of acetic acid as well as fumaric acid in low concentrations caused high stability of electricity generation in constructed fuel cell apart from application of lactic acid.
D. acetoxidans IMV B-7384 has been cultivated in MFC under addition of 9 g/l of acetic acid as the sole electron donor into the growth medium (fig. 14). Under these cultivation conditions the maximal power value equaled 3.6±0.30 mW/m2 on the 64 hour (third day) of bacterial cultivation. It was lower by 61% in comparison with the maximal power value obtained under usage of 6 g/l of lactic acid by bacteria in the anode chamber of MFC. Increase of cultivation time up to 480 hour caused decrease of power value till 1.60±0.11 mW/m2.
Thus, increase of acetic acid concentration as electron donor in the anode chamber of MFC caused partial inhibition of electricity generation in comparison with application of its lower content.
It can be summarized that low concentrations of investigated organic acids caused higher stability of power generation in constructed microbial fuel cell apart from their higher concentrations.
Power density in MFC during twenty days under addition of 9 g/l of acetic acid into the growth medium of D. acetoxidans IMV B-7384
Possibly, it may be explained because of raising of by-products concentrations in the growth medium under increasing of organic source concentration. It may cause negative influence according to D. acetoxidans IMV B-7384 metabolism and their respective ability of exoelectrogenesis.
D. acetoxidans IMV B-7384 is exoelectricigenic sulfur-reducing bacterium which influences environmental biogeochemistry by maintenance of reductive stage of sulfur cycle. Its metal-resistant strains play significant role in heavy metal ions remediation from the aquatic environments because of interaction between the final product of bacterial dissimilative sulfur-reduction – hydrogen sulfide and metal ions with their next combining in form of insoluble metal sulfide precipitates. It was shown that D. acetoxidans IMV B-7384 synthesizes such components of antioxidant defense system as catalase, superoxide dismutase and reduced glutathione under the influence of aggressive external factors, such as heavy metal ions. It causes its resistance against environmental pollution by these xenobiotics. Enzymatic and non-enzymatic components of antioxidant defense system found in the cells of D. acetoxidans IMV B-7384 are highly effective in neutralization of reactive oxygen species. Antioxidant system activity of investigated bacterial cells may be useful for increasing the durability of proton-exchange membranes in MFCs because of the creation of defensive barrier against detrimental influence of these oxidants. It shows a prospect of efficient and economic application of D. acetoxidans IMV B-7384 as the anode biocatalyst in microbial fuel cell with simultaneous wastewater treatment.
The optimal external resistance in constructed MFC in term of power generation was determined to be 2.2 kΩ. Separate application of lactic, fumaric, and acetic acids caused differences in power generation by investigated bacterium. It was shown that addition of fumaric and acetic acids in concentration 6 g/l improved stability of generated power in constructed microbial fuel cell in comparison with application of lactic acid in the same concentration. Increase of concentration of investigated organic electron donors up to 9 g/l reduced generated electric power .
Thus, D. acetoxidans IMV B-7384 may be applied for effective treatment of wastewater enriched with heavy metals, acetic and fumaric acids-containing refuses with simultaneous electricity generation in the scaled-up microbial fuel cells. Additionally it can be used for treatment of highly polluted sulfur-containing aquatic environments with alterations of sulfur cycle.
Exploration of the utility of D. acetoxidans IMV B-7384 for development of efficient MFC through determination of optimal cultivation and fuel cell construction parameters may be highly beneficial for the progress of microbial fuel cell study with simultaneous heavy metals pollution control for cost effective environmental remediation. Further research of D. acetoxidans IMV B-7384 as the anode biocatalyst may include detailed analyses of its molecular biochemistry with the aim of profound understanding of interconnections between the processes of organic source consumption and electric current generation. Further analyses of interrelations between specific reactions of sulfur cycle (e.g. polysulfide reductase activity), reduction of transition metals, such as iron and manganese, and processes of electrogenesis, which are conducted by the cells of D. acetoxidans IMV B-7384 may substantially influence the microbial fuel cell study with the aim of increasing of its productivity, reliability and durability.
We are highly grateful to Dr. Neelkanth G. Dhere, Jaroslav Ferensovych, Dr. Vasyl Getman, Dr. Dariya Fedorovych, Dr. Yurij Boretsky, Dr. Oleksandr Kulachkovskyj, and all other our coworkers for their support provided in carrying out of investigations and book chapter preparation.
One of the main factors affecting reproductive performance of dairy cattle is postpartum uterine disease. Metritis and endometritis have been associated with delays in restarting ovarian activity postpartum, prolonged intervals from calving to first service, increased number of days open, decreased conception rates, and increased culling rates [1, 2, 3, 4, 5]. Affected animals are easily identified when they show clinical signs indicative of uterine disease. Though symptoms of systemic illness are often absent, a purulent or mucopurulent vaginal discharge warrants further investigation, and therefore, clinical metritis and endometritis rarely remain undiagnosed.
\nFourteen years ago, Kasimanickam et al. [6] found that many clinically normal postpartum cows had subclinical endometritis (SE). Those authors evaluated endometrial cytologies collected from 228 healthy cows at 21–33 days postpartum and related the cytological findings with the subsequent reproductive performance of cows. They used a receiver/response operating characteristic (ROC) curve to determine a threshold percentage of polymorphonuclear leukocytes (PMN%) in the cytological smears above which fertility was significantly reduced, and therefore, subclinical endometritis was diagnosed based on PMN% threshold. Since that pioneer work, many other studies have investigated the etiology, prevalence, and impact on reproduction of SE in dairy cows.
\nSubclinical endometritis is the inflammation of the endometrium without clinical signs and often without evidence of infection [7, 8, 9]. Alteration of the inflammatory response postpartum could be at the origin of this condition.
\nThere is no doubt that uterine pathogens may negatively affect reproduction both by causing direct endometrial damage and by producing toxins [10, 11]. Bacterial endotoxins are known to have numerous effects on reproduction: (a) they may affect estradiol and progesterone secretion and alter follicular growth and the normal development of the corpus luteum [10, 11, 12], (b) may interfere with LH production and cause ovulation failure [13, 14], (c) may increase PGE2 secretion and prolong the life span of corpus luteum [15], and (d) may induce embryo mortality [16].
\nIn cows with metritis and clinical endometritis, recognized pathogens such as E. coli, Trueperella pyogenes, Fusobacterium necrophorum, or Prevotella spp. are commonly isolated from the uterus [17]. In the case of SE, in contrast, several studies [7, 8, 9] showed that bacterial populations isolated from the uterus of cows diagnosed with SE did not differ from those of healthy cows. Prunner et al. [18] found that presence of Trueperella pyogenes in the uterus postpartum was a risk factor for development of clinical endometritis, but neither Trueperella pyogenes nor E. coli were associated with SE. Results of the cited studies suggest that common pathogens associated with metritis and clinical endometritis do not have a significant role in the SE pathogenesis. It has been suggested that SE may be a response to unspecific uterine infections [19] or a prolonged inflammatory process that persists after bacterial elimination.
\nIn several studies, cows with clinical and subclinical endometritis were shown to have increased endometrial mRNA expression and elevated serum concentrations of pro-inflammatory mediators as compared with healthy cows [20, 21, 22, 23, 24]. Situations of prolonged inflammation after elimination of bacterial contamination may occur when an exacerbated production of eicosanoids concurs with a low production of anti-inflammatory substances, originating a delayed restoration of homeostasis in the affected tissues [25]. It has also been suggested that an unbalanced production of pro-inflammatory/anti-inflammatory cytokines during the first week postpartum could play a determinant role in the subsequent development of SE. A high ratio of pro-inflammatory/anti-inflammatory cytokines during the first week postpartum could lead to an excessive inflammatory response [26], whereas a low ratio of pro-inflammatory/anti-inflammatory cytokines might impair activation of inflammation and clearance of bacteria and lead to development of endometritis [22, 27].
\nOn the other hand, diet fat levels and the type of fatty acids present in diet may affect cellular immune function [28]. Linoleic acid-enriched diets fed to dairy cows during the transition period [29] induced a pro-inflammatory status during the first week postpartum. Several studies have demonstrated that excess of adipose tissue and high serum concentrations of non-esterified fatty acids constitute risk factors for postpartum pro-inflammatory diseases in dairy cows, such as metritis or mastitis [30, 31, 32]. Innate immune response is activated when an aggressor agent is recognized by toll-like receptors (TLR). Different aggressor agents are recognized by specific TLR, which might also be activated by certain molecules in the absence of aggressor agents. For instance, lipopolysaccharides present in the cell wall of gram-negative bacteria are recognized by TLR4, which may also be activated by some fatty acids (lauric, palmitic, and oleic) [33]. Thus, an inflammatory response might be induced without the existence of infection.
\nIn addition, the oxidative stress may contribute to an abnormal inflammatory response during postpartum [33, 34]. Increase of oxygen metabolism during postpartum would increase ROS production rate [33, 35]. Studies carried out in bovine endothelial cells evidenced that oxidative stress increased lipid hydroperoxide formation which enhanced a pro-inflammatory phenotype of these cells [36, 37, 38].
\nIndependently of the cause of inflammation, the inflammatory status of the endometrium may have a major impact on reproduction. A direct negative effect of SE on embryo quality and survival has already been described [39, 40], which would affect conception rates. In addition, results from various studies suggest that SE may be associated to altered patterns of prostaglandin E2 and F2α synthesis [41, 42] which could compromise luteal function and pregnancy.
\nOn the other hand, certain cytokines are known to play essential roles on the physiological regulation of ovarian function [43]. Cytokines are involved in regulation of follicular growth, ovulation, luteal formation, and regression [44, 45]. Inflammatory mediators, such as cytokines released in SE, may perturb this regulatory function.
\nCows with subclinical endometritis, by definition, do not show any clinical sign of endometritis, and therefore, the diagnosis of this condition requires the use of endometrial cytology, biopsy, or any other method able to evidence the presence of endometrial inflammation.
\nUltrasonography has been used as a method to diagnose SE based on the presence of intrauterine fluid and on the evaluation of uterine diameter. A small amount of fluid in the uterine lumen and/or thickened uterine walls can be considered signs of endometrial inflammation. However, in various studies ultrasound was found to be less sensitive than endometrial cytology [6, 46, 47] for SE diagnosis. Presence of intrauterine fluid and a thick uterine mucosa may be normal findings in physiological situations such as estrus or early postpartum [48], and perhaps the evaluation of fluid characteristics could improve the sensitivity of ultrasound diagnosis [49]. Mariño et al. [9] found a significant relationship between presence of abnormal intrauterine fluid and SE diagnosed by biopsy but not by cytology.
\nDoppler ultrasonography might be useful for the diagnosis of endometritis in cattle, but it is still an unexplored tool. Debertolis et al. [50] found significantly increased blood flow in uterine arteries of cows to which acute endometritis had been experimentally induced. Whether patterns of vascular flow may differ between healthy uterus and those with SE still has to be investigated.
\nEndometrial cytology is considered the most reliable method for the diagnosis of SE [46], and therefore, it is the one most frequently used. Samples for cytology can be obtained by two main techniques, cytobrush and uterine lavage.
\nThe cytobrush technique consists of connecting a cytobrush to the plunger of an insemination catheter [6] and, protected by the catheter, introducing it into the uterus as for doing artificial insemination. Inside the uterus, the cytobrush is pushed out of the catheter, gently rotated against the uterine wall, guarded back inside the catheter, and removed from the uterus. The brush is rolled onto a microscopic slide and stained. Cytology samples can be obtained from the uterine body or from one of the uterine horns. Mariño et al. [9] compared cytology and biopsy findings between the two horns of 100 bovine uteri collected postmortem and observed that samples collected from the left horn were more representative of both uterine horns than those collected from the right one.
\nThe uterine lavage technique consists of infusing sterile saline solution into the uterus with a catheter, gently massaging the uterus to allow fluid distribution within the lumen, and recovering some of the fluid by aspiration using the same catheter. The collected fluid is centrifuged, the supernatant discarded, and the sediment smeared onto a microscopic slide. Regardless of the collection technique, cytological smears are fixed and stained using conventional stains (e.g., Diff-Quick).
\nKasimanickam et al. [51] did a comparative study of the two sampling techniques and concluded that cytobrush had some advantages over uterine lavage: it was less time-consuming, was easier to perform independently of the uterine size, did not produce endometrial irritation, and induced lower degree of cell structure distortion and lower presence of erythrocytes. One disadvantage of cytobrush is that the sample is collected from a specific area of the endometrium, whereas uterine lavage provides cells from the whole endometrial surface.
\nRecently, Pascottini [52] described a new method for sample collection that consisted of using a paper tape rolled around the top of an insemination catheter. With this method the author observed less contamination with erythrocytes and a better preserved structure of epithelial cells than when using cytobrush. Moreover, this system would allow taking a sample for cytology at the same time of doing insemination.
\nConcerning the threshold used in different studies for the diagnosis of SE, the cutoff PMN% reported by the different authors has varied between 4 and 25% (Table 1) depending on the postpartum period at which the diagnosis was done.
\nSampling method | \nPostpartum diagnosis period | \n\n | ||
---|---|---|---|---|
Cytobrush | \nWeek 3–5 | \nWeek 5–7 | \n≥7 week | \nPMN% | \n
Lopdell et al. [53] | \n35.0% | \n\n | \n | >18.0% | \n
Kasimanickam et al. [6] | \n35.1% | \n\n | \n | >18.0% | \n
Heidarpour et al. [54] | \n13.5% | \n\n | \n | >18.0% | \n
Kaufmann et al. [55] | \n12.4% | \n\n | \n | >18.0% | \n
Barrio et al. [56] | \n17.6% | \n\n | \n | >18.0% | \n
Madoz et al. [57] | \n21.5% | \n\n | \n | >8.0% | \n
Dubuc et al. [58] | \n19.3% | \n\n | \n | >6.0% | \n
Plöntzke et al. [59] | \n38.0% | \n\n | \n | >5.0% | \n
Lopdell et al. [53] | \n\n | 7.0% | \n\n | >18.0% | \n
Kasimanickam et al. [6] | \n\n | 34.0% | \n\n | >10.0% | \n
Barlund et al. [46] | \n\n | 11.8% | \n\n | >8.0% | \n
Madoz et al. [57] | \n\n | 16.0% | \n\n | >6.0% | \n
Plöntzke et al. [59] | \n\n | 19.0% | \n\n | >5.0% | \n
Barrio et al. [60] | \n\n | 14.9% | \n\n | >5.0% | \n
Madoz et al. [57] | \n\n | \n | 16.0% | \n>4.0% | \n
Dubuc et al. [58] | \n\n | \n | 11.1% | \n>4.0% | \n
Uterine lavage | \n\n | \n | \n | \n |
Hammon et al. [61] | \n51.8% | \n\n | \n | >25.0% | \n
Barlund et al. [46] | \n15.8% | \n\n | \n | >8.0% | \n
Gilbert et al. [62] | \n\n | 53.0% | \n\n | >5.0% | \n
Cheong et al. [63] | \n\n | 25.9% | \n\n | >10.0% | \n
Cytotape | \n\n | \n | \n | \n |
Pascottini [52] (at AI, cows) | \n\n | \n | 27.8% | \n≥1% | \n
Pascottini [52] (at AI, heifers) | \n\n | \n | 7.86% | \n≥1% | \n
Reported prevalence of subclinical endometritis in some studies that used different sampling methods, postpartum diagnosis periods, and PMN% cutoff values.
Uterine contamination at parturition or in the following days is unavoidable and normal, with 80–100% of animals having bacteria in the uterine lumen in the first 2 weeks postpartum [17]. Uterine contamination elicits neutrophil migration from peripheral blood to the uterine lumen and the subsequent phagocytosis of contaminating organisms by neutrophils. Prunner et al. [18] observed that uterine bacterial growth density increased from calving to 15 days postpartum and decreased from day 21 onwards and the PMN% in cytological samples decreased from calving to day 9, then increased around days 15–21, and decreased thereafter, but at each sampling period, the proportion of PMN strongly depended on bacterial counts.
\nKasimanickam et al. [6] used ROC analysis to identify the PMN% above which fertility was significantly reduced, and this percentage was 18% for samples taken 20–33 days postpartum and 10% for those taken 34–47 days postpartum. Other authors also established the cutoff PMN% for diagnosing SE based on detrimental effects on subsequent reproductive performance [46, 57, 58, 64], and some [59, 61, 62] used arbitrary values. In general, most authors used PMN% thresholds of 15–18% for SE diagnosis at 21–30 days postpartum and values of 4–10% for diagnosis at later periods. Prunner et al. [18] categorized clinically normal cows at 21 days postpartum as having SE when PMN% ≥5% and found that SE-positive cytological samples had an average of 30% PMN; however, on day 28, cows previously categorized as having healthy uteri (i.e., <5% PMN on day 21) had a similar PMN% as those categorized as having SE, and for both groups, it averaged 15%. During the first month postpartum, healthy cows may show relatively high percentages of PMN in cytological samples, and therefore, diagnosis of SE during this period will be less accurate than a later diagnosis.
\nIt has been suggested that the stage of the estrous cycle might have an effect on the proportion of PMN present in the cytology and, therefore, on the diagnosis of SE. During the follicular phase of the estrous cycle, there is an increased infiltration of PMN in the endometrium elicited under estrogenic influence [65]. Several studies [9, 52, 57] have found that the PMN% in cytological samples taken with cytobrush was not affected by the stage of the estrous cycle. However, when the SE diagnosis was done by biopsy, a higher degree of inflammatory infiltration could be observed in the follicular phase of the cycle [9]. This was because cytology only detects PMN infiltration in the superficial epithelium, whereas biopsy allows identifying inflammatory cells in deeper layers of the endometrium.
\nAnother possibility to evidence the existence of endometrial inflammation is the use of urinary test stripes, which detect the presence of leukocytes in urine [66, 67, 68]. The diagnosis of endometritis can be done using uterine lavage fluids, or an endometrial cytobrush can be immersed in saline solution during 30 sec and then the strip introduced in the solution for 2 sec. It is a qualitative colorimetric test that showed a variable correlation with cytology. Santos et al. [66] reported a sensitivity of 96% and specificity of 98%. However, Cheong et al. [67] observed 77% sensitivity and 52% specificity. This test is rarely used in commercial dairy farms probably because it is not specifically designed for the diagnosis of endometritis.
\nUterine biopsy is commonly used in human medicine as it is considered the gold standard for evaluating the human endometrium [69]. In domestic animals, uterine biopsy has been used since the 1960s to investigate causes of infertility in mares [70], and it is a routine diagnosis method today [71]. However, in dairy cattle uterine biopsy is rarely performed by practitioners, and it is almost exclusively used for research purposes. The limited use of biopsy in clinical practice may be related with inconveniences associated to sampling time, requirement for laboratory skills, laboratory costs, and time to report [71] and also to the risk of inducing endometritis and the subsequent negative effects on fertility [72].
\nThere are few studies using uterine biopsy for the diagnosis of SE in dairy cattle [73], and when biopsy and cytology findings were compared, the two diagnosis methods showed poor agreement [8, 9, 47]. The histopathological examination of biopsy samples gives detailed information about the degree of inflammation, distribution of the inflammatory infiltrate, or the lesions that may exist, whereas cytology only assesses the superficial layer of the endometrium [47]. Thus, it is not surprising that direct comparison between biopsy and cytology results showed low agreement. Evaluation criteria for SE diagnosis on biopsy samples, as for cytology, should be established based on detrimental effect on subsequent reproductive performance rather than on the presence of an arbitrary number of inflammatory cells [47].
\nThe reported prevalence of SE in postpartum dairy cows has varied between 7 and 53% (Table 1). Such disparity among studies in SE prevalence may be due to differences in (i) postpartum period in which the diagnosis was made, (ii) PMN% established as threshold above which an endometrial cytology was considered positive for SE, and (iii) the method used to take the cytological sample, i.e., cytobrush, uterine flushing, or cytotape. In general, SE prevalence tended to be higher when the sample was collected by uterine lavage, the diagnosis was made before 30 days postpartum, and the cutoff PMN% applied was >5%.
\nThere are some discrepancies among authors concerning the effects of SE on reproductive performance of dairy cows. Whereas some authors [59, 74, 75] did not find significant effects on reproduction, many other studies described a variety of negative effects on fertility (Table 2). The disparity of results may not only be due to the different diagnosis criteria (e.g., postpartum period for SE diagnosis, threshold of PMN applied, etc.) used in the different studies but also to the numerous confounding factors that may have a negative effect on reproduction (e.g., poor heat detection, inadequate nutrition, insufficient cow comfort, old cows, poor semen quality, other diseases, etc.).
\nReference | \nCharacteristics of the study | \nReproductive impact | \nAffected parameters | \n
---|---|---|---|
Kasimanickam et al. [6] | \nn = 228; farms = 2; no cows with PVD; cytobrush; 20–33 DIM: >18% PMN; 34–47 DIM: >10%PMN | \nAdverse | \nDays open. Pregnancy rate | \n
Gilbert et al. [62] | \nn = 141; farms = 5; no cows with PVD; uterine lavage; 40–60 DIM: ≈5%PMN | \nAdverse | \nPostpartum anestrus. First-service pregnancy rate. Services per conception. Days open. Pregnancy rate | \n
Barlund et al. [46] | \nn = 221; farms = 8; no cows with PVD; cytobrush; 28–41 DIM: >8%PMN | \nAdverse | \nFirst-service pregnancy rate. Services per conception. Days open. Pregnancy rate | \n
Dubuc et al. [58] | \nn = 1044; farms = 6; some cows with PVD; cytobrush; 35 ± 3 DIM: >6% PMN; 56 ± 3 DIM: >4% PMN | \nAdverse | \nPregnancy rate | \n
Plöntzke et al. [59] | \nn = 201; farms = 3; no cows with PVD; cytobrush; 18–38 DIM: >5%PMN; 32–52 DIM: >5%PMN | \nWithout effect | \nDays to first service. Services per conception. Days open. Pregnancy rate | \n
Burke et al. [76] | \nn = 78; farms = 1; no cows with PVD; cytobrush; 42 DIM: >6%PMN | \nAdverse | \nPostpartum anestrus | \n
Green et al. [77] | \nn = 169; farms = 1; no cows with PVD; cytobrush; 21 ± 3 DIM: >18%PMN; 42 ± 3 DIM: >18%PMN | \nAdverse | \nPostpartum anestrus | \n
McDougall et al. [64] | \nn = 303; farms = 1; some cows with PVD; cytobrush; 29 ± 2.4 DIM: >9%PMN; 43 ± 2.3 DIM: >7%PMN | \nAdverse | \nPostpartum anestrus. First-service pregnancy rate. Days open | \n
Drillich et al. [39] | \nn = 48; farms = 1; no cows with PVD; cytobrush; IA: 0% PMN; embryo collection: 0% PMN | \nAdverse | \nTransferable embryo recovery rate | \n
Fernandez-Sanchez et al. [40] | \nn = 41; farms = 1; no cows with PVD; cytobrush; no PMN% cutoff; donor cows in embryo transfer programs | \nAdverse | \nTransferable embryo recovery rate | \n
Prunner et al. [74] | \nn = 383; farms = 10; no cows with PVD; cytobrush; 20–30 DIM: >5%PMN | \nWithout effect | \nDays to first service. Services per conception. Days open. Pregnancy rate. Culling rate | \n
Barrio et al. [56] | \nn = 467; farms = 1; no cows with PVD; cytobrush; 30 ± 2 DIM: >18%PMN | \nAdverse | \nFirst-service pregnancy rate | \n
Barrio et al. [60] | \nn = 65; farms = 25; no cows with PVD; cytobrush; 30–45 DIM: >5%PMN | \nAdverse | \nDays open | \n
Gobikrushanth et al. [75] | \nn = 126; farms = 1; no cows with PVD; cytobrush; 25 ± 1 DIM: >8%PMN | \nWithout effect | \nFollicular development and ovulation. First-service pregnancy rate. Cows pregnant at 150 and 250 days postpartum | \n
Reported effects of subclinical endometritis on reproduction.
n, number of animals; PVD, purulent vaginal discharge; DIM, days in milk.
Subclinical endometritis has been related with the repeat breeder cow syndrome with controversial results. Whereas in some studies [78, 79] the prevalence of SE in repeat breeder cows was reported to be close to 50%, in another study [80] the observed prevalence was lower than 15%. The PMN% thresholds used in those studies differed from 3% [78] and 5% [80] to 10% [79].
\nIn addition to the potential effects on reproduction, endometritis may negatively affect milk production [81]. Clinical and subclinical endometritis have been related with a decrease in milk production of 0.6–1.03 kg/cow/day, reduction of milk fat and protein, and with increased somatic cell counts in milk [64, 76, 82]. Nevertheless, some authors [83] question these effects.
\nAntibiotics and prostaglandins F2α, combined or individually, have constituted the most common treatment for clinical endometritis postpartum. Haimerl et al. [84] and Lefebvre and Stock [85] did a critical evaluation of the scientific literature that in the last 20 years reported the use of PGF2α alone or combined with antibiotics for the treatment of clinical endometritis in postpartum dairy cows. Both groups of researchers concluded that there was not enough clinical evidence that using PGF2α in endometritis postpartum had a beneficial effect. And the only antibiotic that seemed to be effective for clinical endometritis was cephapirin (a first-generation cephalosporin).
\nIn the case of SE, the treatment with PGF2α and/or antibiotics was tested only in a few studies that cannot be easily compared as included different hormonal protocols for synchronization of estrus or ovulation, animals in different postpartum periods, and different diagnosis criteria for SE. In the studies of Kasimanickam et al. [51], Galvão et al. [86], and Denis-Robichaud and Dubuc [87], intrauterine infusion of cephalosporins was tested as treatment of SE, and Kasimanickam et al. [51], Galvão et al. [88], and Lima et al. [89] tested the use of prostaglandins. Kasimanickam et al. [51] and Denis-Robichaud and Dubuc [87] obtained higher pregnancy rates at first insemination in cows treated with intrauterine cephapirin than in control cows, whereas Galvão et al. [86] did not observe any positive effect on reproduction when cows diagnosed with SE were treated with intrauterine ceftiofur infusion. Concerning the use of PGF2α in cows with SE, Kasimanickam et al. [51] and Galvão et al. [88] observed positive effects on reproductive performance, whereas Lima et al. [89] did not find any effect. It should be pointed out that the magnitude of the positive effects observed in some of the cited studies was dependent on other factors such as existence of ovarian activity at the time of treatment [87] or body condition [88]. The scarce number of studies done so far and the different results obtained do not allow us to draw a conclusion about the efficacy of using PGF2α and/or cephalosporins for the treatment of SE.
\nBecause in many cases of SE there is no uterine content or positive bacterial culture, treatment with antibiotics or prostaglandins should be expected to be unsuccessful. However, there is an inflammatory response that very likely is the cause of the negative effects of SE, and therefore, the use of nonsteroidal anti-inflammatory drugs (NSAID) would be fully warranted. Priest [5] tested the use of the NSAID carprofen, three doses administered at 3-day intervals between 21 and 31 days postpartum, in cows diagnosed with SE when the cytology showed >14% PMN at 14 days postpartum. The treatment did not reduce the incidence of SE at day 42, but increased pregnancy rate as compared with untreated control cows. However, in a subsequent study [90], cows were treated with carprofen at 1 or at 3 weeks after calving, and the treatment did not improve milk production, indicators of health or reproductive performance.
\nUterine lavage with sterile saline solution is a common treatment for endometrial inflammation in mares. Uterine lavage favors the elimination of inflammatory products, such as nonfunctional PMN, and induces uterine contractions that facilitate the evacuation of any content. In addition, elimination of nonfunctional PMN favors migration of new functional PMN that is able to counter the infection [91]. In bovine, potential usefulness of uterine lavage has been described in connection with treatment of repeat breeder cows, either as the only treatment or combined with prostaglandins and/or antibiotics, assuming that many repeat breeder cows may suffer chronic endometritis [92]. In cases of SE postpartum, uterine lavage with physiological saline at day 30 postpartum was associated with a reduction of the PMN% in cytological samples obtained at day 40, but its effect on reproduction was not evaluated [93].
\nOther protocols that have been used for the treatment of metritis or clinical endometritis, such as intrauterine infusion of dextrose [94], ozone [95], or N-acetylcysteine combined with amoxicillin and clavulanic [96], have not been tested in cows with subclinical endometritis. Nevertheless, the effect of those substances is mainly antibacterial or mucolytic, whereas in SE there is no mucopurulent secretion and, in most cases, no pathogen bacteria.
\nSubclinical endometritis is a uterine inflammation probably originated by the alteration of the inflammation regulatory mechanisms. The inflammatory status may abnormally persist after elimination of postpartum bacterial contamination, which may be associated with an unbalanced production of anti- and pro-inflammatory factors. Prevalence of subclinical endometritis in dairy farms may reflect the immune status of cows, which in turn would be indicative of the metabolic status of cows in transition and, eventually, of the nutritional management of farms.
\nThe study was supported by Xunta de Galicia (Programa Sectorial de Medio Rural, Proyecto Ref. PGIDIT07MRU002E) and FEFRIGA, Santiago de Compostela, Spain.
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