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Hard X-rays can penetrate solid objects, and their largest use is to take images of the inside of objects in diagnostic radiography and crystallography. The roentgen (R) is an obsolete traditional unit of exposure, which represented the amount of radiation required to create one electrostatic unit of charge of each polarity in one cubic centimeter of dry air. The rad is the (obsolete) corresponding traditional unit, equal to 10 millijoules of energy deposited per kilogram. The sievert (Sv) is the SI unit of equivalent dose, which for X-rays is numerically equal to the gray (Gy). X-rays are generated by an X-ray tube, a vacuum tube that uses a high voltage to accelerate the electrons released by a hot cathode to a high velocity. In crystallography, a copper target is most common, with cobalt often being used when fluorescence from iron content in the sample might otherwise present a problem. X-ray fluorescence: If the electron has enough energy it can knock an orbital electron out of the inner electron shell of a metal atom, and as a result electrons from higher energy levels then fill up the vacancy and X-ray photons are emitted. So the resulting output of a tube consists of a continuous bremsstrahlung spectrum falling off to zero at the tube voltage, plus several spikes at the characteristic lines. In medical diagnostic applications, the low energy (soft) X-rays are unwanted, since they are totally absorbed by the body, increasing the dose. To generate an image of the cardiovascular system, including the arteries and veins (angiography) an initial image is taken of the anatomical region of interest. A specialized source of X-rays which is becoming widely used in research is synchrotron radiation, which is generated by particle accelerators. The most commonly known methods are photographic plates, photographic film in cassettes, and rare earth screens.
Before the advent of the digital computer and before invention of digital imaging, photographic plates were used to produce most radiographic images. Since photographic plates are sensitive to X-rays, they provide a means of recording the image, but they also required much X-ray exposure (to the patient), hence intensifying screens were devised.
Areas where the X-rays strike darken when developed, causing bones to appear lighter than the surrounding soft tissue. Contrast compounds containing barium or iodine, which are radiopaque, can be ingested in the gastrointestinal tract (barium) or injected in the artery or veins to highlight these vessels. An increasingly common method is the use of photostimulated luminescence (PSL), pioneered by Fuji in the 1980s. The PSP plate can be reused, and existing X-ray equipment requires no modification to use them.
For many applications, counters are not sealed but are constantly fed with purified gas, thus reducing problems of contamination or gas aging. Some materials such as sodium iodide (NaI) can "convert" an X-ray photon to a visible photon; an electronic detector can be built by adding a photomultiplier. Background: The gut microbiome, a dynamic bacterial community that interacts with the host, is integral to human health because it regulates energy metabolism and immune functions. Objectives: We investigated the effects of polychlorinated biphenyls (PCBs) and exercise on the composition and structure of the gut microbiome in mice.
Results: Oral exposure to PCBs significantly altered the abundance of the gut microbiome in mice primarily by decreasing the levels of Proteobacteria. Conclusions: Our results show that oral exposure to PCBs can induce substantial changes in the gut microbiome, which may then influence their systemic toxicity. This work was supported in part by grants P42 ES 07380, R01 CA133257, MH63022, MH072567, and DA027569 from the National Institutes of Health.
The gut microbiome is a collection of bacteria that resides in the host gastrointestinal tract.
Recent evidence has implicated the gut microbiome in the development of a wide range of disorders, including obesity, diabetes, metabolic dysfunctions, vascular disease, and inflammatory bowel disease (Kinross et al. Despite these diverse effects on human health, the influence of the microbiome on the toxicity of environmental pollutants and its role in disease risk are largely unknown (Betts 2011). The present study was designed on the basis of recent evidence implicating the role of the gut microbiome in risks associated with exposure to environmental chemicals (Betts 2011). Table 1 – The 10 bacterial taxa with the greatest decrease in abundance following exposure of sedentary mice to the PCB mixture. Table 2 – The 10 bacterial taxa with the greatest increase in abundance following exposure of sedentary mice to the PCB mixture. Exposure to the PCB mixture did not alter biodiversity of the gut microbiome; all 11,229 taxa were detected in at least one sample from sedentary mice. Among detected bacterial taxa, 93 were present exclusively in either exercised or sedentary mice. A group of 2,510 taxa showed differences in abundance between the exercised and sedentary mice. Further examination using the PAM identified 10 taxa with substantially different abundance between the exercised and sedentary mice (Table 3).
Table 3 – Prediction analysis for microarrays (PAM)-selected distinctive bacterial taxa presenting differentially in the mouse gut microbiome of excercised versus sedentary mice. We detected 10,799 taxa in sedentary mice exposed to the PCB mixture, compared with 13,383 taxa in the exercised mice treated with PCBs.
In view of recent evidence indicating that gut bacteria can be involved in the preabsorptive metabolism of heavy metals and organic chemicals (Lapanje et al. The mechanisms of exercise-mediated changes in gut ecology are not known; however, they are likely to be mediated by altering the host factors that influence the intestinal microenvironment. Short-chain fatty acids (SCFAs) may be another factor that regulates the gut microbiome in response to exercise.
Finally, exercise may influence the composition of the gut microbiome by altering the intestinal immune system.
The development of chronic diseases related to the exposure to environmental toxicants are associated with age, and the benefits of exercise are also being emphasized in older individuals; therefore, we used aged mice (11–13 months of age) in the present study. Although Enterococci are commensal bacteria, they are also important nosocomial pathogens that cause bacteremia, endocarditis, and other infections in humans. The most striking change we found in the gut microbiome of exercised mice was a > 300-fold decrease in the abundance of Erysipelotrichaceae (Table 3). Here we demonstrate that oral exposure to a mixture of environmentally relevant PCB congeners significantly altered the abundance of the gut microbiome by decreasing the levels of Proteobacteria. Viloria M, Lara-Padilla E, Campos-Rodriguez R, Jarillo-Luna A, Reyna-Garfias H, Lopez-Sanchez P, et al. EHP is now using Editorial Manager for manuscript submissions. All user accounts have been transferred to Editorial Manager—just log into Editorial Manager and reset your password. DisclaimerPublication of articles in EHP does not mean that the National Institute of Environmental Health Sciences (NIEHS) condones, endorses, approves, or recommends the use of any products, services, materials, methodology, or policies stated therein. This process produces an emission spectrum of X-ray frequencies, sometimes referred to as the spectral lines. The intensity of the X-rays increases linearly with decreasing frequency, from zero at the energy of the incident electrons, the voltage on the X-ray tube. A second image is then taken of the same region after iodinated contrast material has been injected into the blood vessels within this area. The contrast compounds have high atomic numbered elements in them that (like bone) essentially block the X-rays and hence the once hollow organ or vessel can be more readily seen. In modern hospitals a photostimulable phosphor plate (PSP plate) is used in place of the photographic plate.
The activity level of the mice correlated with a substantial shift in abundance, biodiversity, and composition of the microbiome. Toborek, Department of Biochemistry and Molecular Biology, University of Miami School of Medicine, Gautier Building, Room 528E, 1011 NW 15th St., Miami, FL 33136 USA. It was recently suggested that preabsorptive metabolism can modify toxicity of environmental pollutants, influencing their health effects (Lapanje et al. We examined whether exposure to polychlorinated biphenyls (PCBs) could affect the abundance and composition of the gut microbiome. All animal protocols were approved by the Institutional Committee on Animal Care of the University of Miami School of Medicine and followed National Institutes of Health guidelines (National Research Council 2011). We selected the type of PCB congeners and their relative ratio based on PCB content in contaminated food (Ashley et al. Data processing and multivariate statistical analyses were performed using the PhyCA-Stats analysis software package (Second Genome Inc.).

After PCB exposure, the number of taxa dropped to 10,798, but the change was not statistically significant. These taxa were then analyzed by PCoA with weighted Unifrac distance, which indicated significant differences in the composition of the microbial communities between the exercised and sedentary mice (Figure 2B).
The taxa that were more abundant in the exercised group were in phylum Firmicutes, class Bacilli, and most of these were in order Lactobacillales. Comparison of the gut microbiome among all experimental groups (sedentary and exercised mice with or without PCB exposure) identified 1,568 bacterial taxa that were differentially abundant in at least one of these groups.
Although there appeared to be a tendency toward increased biodiversity in the exercise-plus-PCB group, these changes were not significant. For example, physical activity has been reported to increase excretion of primary bile acids to the gastrointestinal tract (Meissner et al.
Some strains are resistant to multiple antibiotics and possess virulence factors, such as adhesins, invasins, pili, and haemolysin (Willems et al. This family plays an important role in metabolic disorders and energy metabolism (Chen et al. These results suggest that the gut microbiome may be one of the primary targets of PCB-induced toxicity in subjects exposed orally to these environmental toxicants. Conclusions and opinions are those of the individual authors and advertisers only and do not reflect the policies or views of the NIEHS.
The spectral lines generated depend on the target (anode) element used and thus are called characteristic lines. These two images are then digitally subtracted, leaving an image of only the iodinated contrast outlining the blood vessels. Photographic film largely replaced these plates, and it was used in X-ray laboratories to produce medical images. In the pursuit of a non-toxic contrast material, many types of high atomic number elements were evaluated. After the plate is X-rayed, excited electrons in the phosphor material remain "trapped" in "colour centres" in the crystal lattice until stimulated by a laser beam passed over the plate surface. Electrons accelerate toward the anode, in the process causing further ionization along their trajectory. Strong evidence also indicates the critical role of the gut microbiota in drug metabolism and toxicity, energy metabolism, immune functions, and postsurgical recovery (Holmes et al. Probe intensities were background subtracted and scaled to values for PhyloChip Control Mix.
HC-AN analysis based on weighted Unifrac distance confirmed a shift of the composition of the gut microbiome related to physical activity (exercised vs. The taxa that were decreased in the exercised group belonged to phyla Tenericutes, Bacteroidetes, and Firmicutes.
Analysis of these taxa for dissimilarity between the groups using PCoA with weighted Unifrac indicated significant differences between the composition of the gut microbiome before and after PCB exposure in sedentary mice.
For example, exercise was demonstrated to decrease the risk of developing several intestinal diseases, including colon cancer (Friedenreich et al. We observed that PCB-induced alterations of the gut microbiome were attenuated by voluntary exercise. Monitoring bacterial community of human gut microbiota reveals an increase in Lactobacillus in obese patients and Methanogens in anorexic patients. Linking habitat use of Hudson River striped bass to accumulation of polychlorinated biphenyl congeners. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. Polychlorinated biphenyls disrupt intestinal integrity via NADPH oxidase-induced alterations of tight junction protein expression. The effects of individual PCB congeners on the soil bacterial community structure and the abundance of biphenyl dioxygenase genes.
Physical activity and risk of colon and rectal cancers: the European Prospective Investigation into Cancer and Nutrition. Extensive personal human gut microbiota culture collections characterized and manipulated in gnotobiotic mice.
Voluntary wheel running exercise and dietary lactose concomitantly reduce proportion of secondary bile acids in rat feces.
Understanding the role of gut microbiome-host metabolic signal disruption in health and disease. Gut bacterial community structure (Porcellio scaber, Isopoda, Crustacea) as a measure of community level response to long-term and short-term metal pollution.
Phylogeny of mercury resistance (mer) operons of gram-negative bacteria isolated from the fecal flora of primates.
UniFrac—an online tool for comparing microbial community diversity in a phylogenetic context. Does a physically active lifestyle improve symptoms in women with irritable bowel syndrome? Induction of anxiety-like behavior in mice during the initial stages of infection with the agent of murine colonic hyperplasia Citrobacter rodentium. Voluntary running exercise alters microbiota composition and increases n-butyrate concentration in the rat cecum. Aroclor 1254 exposure reduces disease resistance and innate immune responses in fasted Arctic charr. Voluntary wheel running increases bile acid as well as cholesterol excretion and decreases atherosclerosis in hypercholesterolemic mice. PhyloChip microarray analysis reveals altered gastrointestinal microbial communities in a rat model of colonic hypersensitivity. Evidence for shifts in the structure and abundance of the microbial community in a long-term PCB-contaminated soil under bioremediation.
Preabsorptive metabolism of sodium arsenate by anaerobic microbiota of mouse cecum forms a variety of methylated and thiolated arsenicals.
Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Do interactions between gut ecology and environmental chemicals contribute to obesity and diabetes? Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome.
Human colon microbiota transform polycyclic aromatic hydrocarbons to estrogenic metabolites.
High-throughput clone library analysis of the mucosa-associated microbiota reveals dysbiosis and differences between inflamed and non-inflamed regions of the intestine in inflammatory bowel disease.
Immunological effects of environmental exposure to polychlorinated biphenyls and dioxins in Dutch school children.
Population biology of Gram-positive pathogens: high-risk clones for dissemination of antibiotic resistance. The radiologist or surgeon then compares the image obtained to normal anatomical images to determine if there is any damage or blockage of the vessel. In more recent years, computerized and digital radiography has been replacing photographic film in medical and dental applications, though film technology remains in widespread use in industrial radiography processes (e.g. For example, the first time the forefathers used contrast it was chalk, and was used on a cadaver's vessels. This process, known as a Townsend avalanche, is detected as a sudden current, called a "count" or "event". At the end of the exercise period, we observed no changes in gut transit or stool frequency between the two groups. Subsequently, hybridization scores were calculated as log2(mean probe fluorescence intensity) ? 1,000. As a result of these changes, the overall abundance of bacteria significantly diminished (by 2.2%) in PCB-exposed mice. The most striking change in exercised mice was a decrease in Erysipelotrichaceae bacterium C11_K211 from phylum Tenericutes, which decreased dramatically in exercised compared with sedentary mice. Importantly, exercise altered PCB-mediated effects on the gut microbiome, as indicated by a loss of bacterial clustering (Figure 3A).

As shown in Figure 3C, exercise appeared to prevent a PCB-induced decrease in abundance of Proteobacteria in sedentary mice (Figure 3C). 2011), the gut microbiome has been proposed to play a role in the assessment of health risks associated with environmental chemicals (Betts 2011; Snedeker and Hay 2012). These authors directly linked this effect to the beneficial effect of exercise on the gut microbiota and the development of gastrointestinal disorders.
These changes in the intestinal immune system may lead to secondary alternations of the host–bacterial interaction and induce selective pressure on bacterial selection. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. In: Halogenated Biphenyls, Terphenyls, Naphthalenes, Dibenzodioxins and Related Products (Kimbrough RD, Jensen AA, eds). When the film is developed, the parts of the image corresponding to higher X-ray exposure are dark, leaving a white shadow of bones on the film. The main bacterial phyla comprising the human gut microbiome are the gram-negative Bacteroidetes and Proteobacteria and the gram-positive Actinobacteria and Firmicutes (Frank et al. The most compelling evidence illustrating this phenomenon was obtained in studies on biotransformation of heavy metals by the gut microbiome.
Exercise can influence the outcomes of disorders associated with alterations in the gut microbiome (Martin 2011); therefore, we hypothesized that physical activity may affect the composition of the gut microbiota and thus influence the impact of environmental toxicants.
To minimize the influence of individual variations on the gut microbiome, each mouse served as its own control for PCB treatment. OTUs were defined by high 16S rRNA gene sequence similarity, with most demonstrating > 99% intra-OTU concordance. Therefore, our demonstration that short-term exposure to an environmentally relevant PCB mixture resulted in profound changes in the gut microbiome in mice is highly significant. 2001), and other disorders that are accompanied by changes in the gut microbiome (De Hertogh et al.
The primary bile acids, such as cholic, deoxycholic, or chenodeoxycholic acids, have established antimicrobial activity, which is mediated by the reduction in internal pH levels of bacteria, dissipation of their transmembrane electrical potential, and disturbances of membrane integrity, leading to leakage of ions and cell death (Kurdi et al. Photographic plates are mostly things of history, and their replacement, the "intensifying screen", is also fading into history.
Moreover, the gut microbiome has been reported to regulate psychiatric health and influence etiopathology of autism. Our results indicate that PCBs can induce profound changes in the microbial composition of the gut and that exercise can attenuate these PCB-induced effects on the intestinal microbiome. Mice were housed individually in plastic cages equipped with a running wheel (Coulbourn Instruments, Whitehall, PA); however, wheels were locked in cages of sedentary mice.
2010), which is comparable to plasma levels of PCBs in an acutely exposed human population (Jensen 1989; Wassermann et al.
For each sample, amplified products were concentrated using a centrifuge filtration method and quantified by electrophoresis using an Agilent 2100 Bioanalyzer (Agilent Technologies, Santa Clara, CA). These taxa belong primarily to phylum Proteobacteria, but the classes and families are diverse. The most striking change in the intestinal microbial profiles was a decrease in the overall abundance of bacterial species. Thus, our data are consistent because we observed a decrease in the number of Erysipelotrichaceae in exercised mice that had lost a substantial amount of body weight; this is associated with the role of Erysipelotrichaceae in energy production and adiposity (Claus et al.
The metal silver (formerly necessary to the radiographic & photographic industries) is a non-renewable resource. Each host has a unique composition of gut microbiota, which implies highly individual responses to environmental stressors and suggests a role for gut microbiota in future personalized health strategies (Kinross et al.
Before classification analysis, we performed data reduction via multiple filtering steps as described by Hazen et al. The group of bacterial taxa with increased abundance after PCB treatment was relatively modest, and the changes did not exceed 2-fold; the bacterial taxa of these with the highest increases in abundance are listed in Table 2. Although these results are the first to show effects of PCBs on the gut microbiome, the decrease in bacterial abundance we observed corresponds with the finding that PCB-contaminated soil is characterized by a shift in structure and abundance of bacterial community (Petric et al.
Their influence on the composition of microbial environment has been linked to a decreased pH in the gut (Wong et al.
Thus it is beneficial that this is now being replaced by digital (DR) and computed (CR) technology. Mice were allowed to exercise for 5 weeks, including 1 week to adapt to running and solitary housing.
The combined PCR products and controls were fragmented, biotin labeled, and hybridized to the PhyloChip Array (version G3). They belong to several difference phyla, including Bacteriodetes, Actinobacteria, Verrucomicrobia, and Firmicutes. Where photographic films required wet processing facilities, these new technologies do not. PhyloChip arrays were washed, stained, and scanned using a GeneArray scanner (Affymetrix, Cleveland, OH).
Taxa-sample intersections were then calculated using abundance (AT) and binary matrices (BT). Thus, the antimicrobial activity of the bile acids may elicit selective pressure on the bacterial communities in exercised mice, leading to a shift of the gut microbiome structure as observed in the present study.
Nevertheless, compared with the results of the present study, the effects of butyrate infusion on the rumen microbiome in cows was relatively minor because only 19 genera and 43 bacterial taxa were significantly affected in response to butyrate (Li et al.
Experiments on germ-free mice also provided evidence that the gut microbiome can regulate the expression of cytochrome P450 enzymes, which are involved in the metabolism of a variety of xenobiotics, including environmental chemicals (Claus et al. Pairwise BT and AT dissimilarity scores were computed using the Unifrac distance metric (Lozupone et al. 2012); these data suggest that this SCFA may be only one of several factors involved in exercise-mediated changes in the gut microbiome.
An increase in Firmicutes (such as Lactobacilli) and a decrease in Bacteroidetes have been confirmed in obese humans (Armougom et al. Hybridization scores and the fluorescence intensity for each taxon were calculated as a trimmed average, with maximum and minimum values removed before averaging. 2006) and weighted Unifrac distance metric, respectively; the weighted Unifrac metric considers OTU abundance in addition to phylogenetic distance between OTUs. Even though the gut and soil provide completely different bacterial environments, PCB exposure appears to elicit environmental stress on the structure and composition of bacterial communities that results in diminished bacterial abundance. Treatment with SCFAs may also affect host-related intestinal factors because butyrate promotes cell differentiation and cell-cycle arrest, inhibits the enzyme histone deacetylase, and decreases the transformation of primary to secondary bile acids as a result of colonic acidification (Wong et al. Indeed, human colon microbiota can transform polycyclic aromatic hydrocarbons (PAHs) to estrogenic metabolites (Van de Wiele et al. We used hierarchical clustering via average-neighbor (HC-AN) and principal coordinate analysis (PCoA) to graphically summarize intersample relationships according to AT and BT dissimilarity scores. In the present study, these changes selectively affected bacterial phylotypes in phylum Proteobacteria. Such changes may be most relevant to immune functions of the host, because the gut microbiome has been shown to play important roles in mucosal immunity and interactions with intestinal and colonic epithelial cells, dendritic cells, and T and B immune cells. These findings are significant because PAH toxicity has been linked to estrogenicity of the compounds, thus suggesting that PAH bioactivation in the colon should be taken into consideration when assessing risk (Van de Wiele et al. Microbiota composition has functional effects on T-effector- and T-regulatory-cell balance, immune responsiveness, and homeostasis (Kelly and Mulder 2012).
Thus, it is likely that alterations of the gut microbiota compromise a novel mechanism leading to immunological alterations, which develop in response to exposure to PCBs (Maule et al. In addition, the role of gut microbiota, as well as its variability in relation to the disposition of environmental chemicals in the human body and its contribution to the development of obesity and diabetes, have recently been recognized (Snedeker and Hay 2012).
In addition, alterations of the gut microbiome can affect PCB-induced disruption of the intestinal barrier and translocation of lipopolysaccharides into the blood stream (Choi JJ et al. In the present study, we observed no statistical differences in bacterial community structure in the exercised mice before and after PCB treatment.
In particular, exercise prevented a PCB-induced decrease in abundance of Proteobacteria, which was observed in sedentary mice.

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