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PubMed1987

Stability of radioiodinated ferritin.

Ferritin which had been radioiodinated using chloramine T exhibited marked instability on storage at 4 degrees C. Both [125I]human liver and heart ferritins showed a similar rate of decline in immunoreactivity (t 1/2 = 20-23 days) indicating that deterioration with storage was not a function of isoferritin composition. The decrease in radioactivity associated with ferritin was due not only to loss of 125I from the molecule but also to protein degradation as shown by enzyme-linked immunoassay and gel filtration. The degradation products had an Mr of at least 69,000 although low Mr material could be identified by gel filtration when a marked reduction in immunoreactivity had occurred. Ferritin instability was much more pronounced than when other proteins such as immunoglobulin and albumin were radioiodinated with chloramine T. These observations indicate that when performing in vivo and in vitro studies with labeled ferritin, degradation of the protein during storage should be carefully monitored and the protein repurified before use.

Antibodies↗

PubMed2001

Fluorodeoxyuridine improves imaging of human glioblastoma xenografts with radiolabeled iododeoxyuridine.

Use of radiolabeled nucleotides for tumor imaging is hampered by rapid in vivo degradation and low DNA-incorporation rates. We evaluated whether blocking of thymidine (dThd) synthesis by 5-fluoro-2'-deoxyuridine (FdUrd) could improve scintigraphy with radio-dThd analogues, such as 5-iodo-2'-deoxyuridine (IdUrd). We first show in vitro that coincubation with FdUrd substantially increased incorporation of [125I]IdUrd and [3H]dThd in the three tested human glioblastoma lines. Flow cytometry analysis showed that a short coincubation with FdUrd (1 h) produces a signal increase per labeled cell. We then measured biodistribution 24 h after i.v. injection of [125I]IdUrd in nude mice s.c. xenografted with the three glioblastoma lines. Compared with animals given [125I]IdUrd alone, i.v. preadministration for 1 h of 10 mg/kg FdUrd increased the uptake of [125I]IdUrd in the three tumors 4.8-6.8-fold. Compatible with previous reports, there were no side effects in mice observed for 2 months after receiving such a treatment. The tumor uptake of [125I]IdUrd was increased < or =13.6-fold when FdUrd preadministration was stepwise reduced to 1.1 mg/kg. Uptake increases remained lower (between 1.7- and 5.8-fold) in normal proliferating tissues (i.e., bone marrow, spleen, and intestine) and negligible in quiescent tissues. DNA extraction showed that 72-80% of radioactivity in tumor and intestine was bound to DNA. Scintigraphy of xenografted mice was performed at different times after i.v. injection of 3.7 MBq [125I]IdUrd. Tumor detection was significantly improved after FdUrd preadministration while still equivocal after 24 h in mice given [125I]IdUrd alone. Furthermore, background activity could be greatly reduced by p.o. administration of KClO4 in addition to potassium iodide. We conclude that FdUrd preadministration may improve positron or single photon emission tomography with cell division tracers, such as radio-IdUrd and possibly other dThd analogues.

Animals↗

PubMed1991

Differences in the intracellular processing of the radiolabel following the uptake of iodine-125- and technetium-99m-neogalactosyl albumin by the isolated perfused rat liver.

Neogalactosyl albumin (NGA) is a synthetic ligand to the asialoglycoprotein receptor (hepatic binding protein), which has been proposed as a useful receptor binding radiopharmaceutical for the noninvasive assessment of liver function. We have compared the uptake and intracellular processing of iodine-125- (125I) and technetium-99m- (99mTc) NGA following its administration as a 1-min pulse (147 pmol) to the isolated perfused rat liver. Approximately 40% of a pulse of either 125I- or 99mTc-NGA were taken up first pass by the liver. Of the 125I taken up by the liver, 82% was released after 15-20 min at the sinusoidal pole of the hepatocyte, predominantly as small molecular weight metabolites. A further 8% of the 125I-associated radioactivity was secreted as intact NGA into bile by the non-lysosomal (direct) pathway while 6% remained in the liver 1 hr after the pulse. In contrast, of the 99mTc taken up by the liver, only 4% reappeared in the perfusate while 40% was secreted into bile by the lysosomal (indirect) pathway and 55% remained in the liver 1 hr after the pulse. Since labeled metabolites of 99mTc-NGA do not appear in plasma, this permits kinetic modeling with 99mTc-NGA without correction for labeled metabolites. Thus, 99mTc-NGA is an excellent candidate as a receptor-binding radiopharmaceutical.

Albumins↗

PubMed1990

Radioiodination of peptide hormones and immunoglobulin preparations: comparison of the chloramine T and iodogen method.

Following optimization of the reaction conditions, e.g. concentration of oxidizing agents, reaction time, volume of reaction mixture, and pH, chloramine T and the new iodination reagent, Iodogen, were compared for their effectiveness in radioiodination of insulin, glucagon, human growth hormone (hGH), and rabbit anti-mouse IgG. The radioactive peptide hormones prepared were analyzed for the presence of aggregate and breakdown products by polyacrylamide gel electrophoresis (PAGE) at pH 8.9, the rabbit anti-mouse IgG was tested for the presence of low molecular weight damage products by gel filtration on Sephadex G-50. The results demonstrate that with respect to iodine incorporation, specific activity, and immunological reactivity either method can be used to prepare under carefully controlled conditions a wide range of tracers with high specific activity at minimal oxidation damage. These tracers are shown to be highly suitable in radioimmunoassays after previous purification by PAGE and gel filtration, respectively.

Chloramines↗

PubMed2004

Marked survival prolongation of mice bearing a transplantable colon adenocarcinoma by treatment with radioactive platinum-[125I]histamine complex. Preliminary report.

BACKGROUND: Recently, a new PtCl2-histamine complex, and its radioactive analogues labelled with I-131 and I-125 have been synthesised and investigated both in vitro and in vivo. In this preliminary report the survival rate of radioactive platinum-[125I] histamine therapy in tumour-bearing mice is demonstrated. MATERIAL AND METHODS: A murine model of transplantable colon adenocarcinoma (C38) in C57BL/6 mice (15 days postimplantation) was used for the experiment. Three groups of animals were treated every 2-3 days with five intraperitoneal injections of the following preparations: PtCl2Hist (total dose of Pt--125 micromol/kg), PtCl2[125I]Hist (total dose of I-125--4.2 MBq; Pt--13 micromol/kg), and "Active/Cold"--PtCl2[125I]Hist/PtCl2Hist (I-125--4.2 MBq; Pt--125 micromol/kg). A solution of 15% dimethylformamide in saline was applied to the control group. A survival analysis with the Kaplan-Meier estimation of survival curves and a statistical comparison by a log-rank test was applied to evaluate the anticancer activity of the tested preparations. RESULTS: Treatment of the animals with platinum-histamine preparations resulted in a significant prolongation of survivals, especially if the radioactive complex with carrier-added PtCl2Hist (p < 0.005) was applied. The highest, almost a 60% prolongation of survival was observed in the Active/Cold group (MStr/MScon ratio = 1.58, 95% CI 1.22-1.93). For this group there was the lowest risk of death (hazard ratio HR = 0.29), whereas HR = 0.45 and 0.47 were found in the animals treated with unattended PtCl2Hist and 125I-labelled complex, respectively. CONCLUSION: The significant enhancement of in vivo anti-cancer activity by a concomitant combination of the therapeutic factors, i.e. cytotoxic/cytostatic activity of the platinum(II)-histamine and the Auger electrons effects generated by the attached I-125 radionuclide, was found on the murine model of transplantable colon adenocarcinoma.

Adenocarcinoma↗

PubMed1997

Pharmacokinetics, absorption, distribution and disposition of [125I]-oligotide following intravenous or oral administration in the rat.

Oligotide (O) was labelled with 125I. The radiolabelled compound ([125I]-Oligotide ([125I]-O)) retained the biological activity of parent O. Following single intravenous administration the half lives of radioactivity associated with O and/or O related components in plasma were 9-10 min and 9-10 h for alpha and beta phases respectively. Following single oral administration the half life of radioactivity associated with O and/or O related components in plasma was 11.45-12.76 h for beta fase. Following multiple oral administration once daily for 7 days, the half life of radioactivity associated with O and/or O related components following the 7th dose was 10-12 h for beta phase. The areas under plasma total radioactivity versus time curves were dose-dependent. Following single intravenous administration the major proportion of the administered dose was excreted via urine, while following single oral administration excretion via urine and faeces accounted for similar proportions of the administered dose. Following both single and oral administration the levels of radioactive components derived from [125I]-O in organs examined were generally highest in highly perfused organs.

Absorption↗

PubMed1990

Treatment of choroidal melanoma: MR imaging in the assessment of radioactive plaque position.

Verification of the position of an episcleral iodine-125 gold plaque in relation to underlying choroidal melanoma is essential during early radiation therapy to ensure accurate plaque placement and thus optimum dose delivery. The authors used magnetic resonance (MR) imaging to examine 15 patients with choroidal melanoma after plaque placement to assess tumor coverage. The relationship of the plaque to the tumor was well defined in all cases, including two tumors anterior to the ora serrata. MR imaging measurements of the plaques were within 1 mm of the actual plaque sizes, while tumor measurements were within 2 mm of the preoperative ultrasound estimations of tumor dimensions. Tumors as small as 3 mm thick were readily visualized with MR imaging. Associated subretinal effusion was demonstrated in seven cases.

Aged↗

PubMedDate not supplied

Concentration of [16 alpha-125I]iodoestradiol in human ovarian tumors in vivo and correlation with estrogen receptor content.

The gamma emitting estrogen [16 alpha-125I]iodoestradiol was administered to 11 patients with ovarian cancer and 1 patient with endometrial cancer. At specific times after the administration of the tracer, portions of the tumor and of control tissues, fat and muscle, were removed and counted. The amount of radioactivity in these tissues was compared to the cytosolic estrogen receptor content of the tumor, measured by Sephadex LH-20 gel filtration, in biopsy specimens taken before the injection of the tracer. There was a strong correlation (p less than 0.005) between the estrogen receptor concentration in the biopsied tumor and the amount of radioactivity in the tumor. There was no correlation between the isotope in the muscle and the tumor receptor, nor between the radioactivity in the tumor and that in fat or muscle. As would be expected for a steroid receptor mediated process, the bulk of the total tissue radioactivity was present in the nuclear compartment of the tumors. This pattern was not observed in the muscle. Furthermore, the nuclear radioactivity in the tumors was positively correlated with the cytosolic estrogen receptor content. These experiments demonstrate that under in vivo conditions this gamma emitting estrogen is concentrated in tumors in a manner that is dependent upon the estrogen receptor. It was also found that the concentrations of radioactivity in the blood were high, producing low tumor to blood ratios. The blood level of isotope was not due to the presence of the unmetabolized steroid, which disappeared from blood rapidly, but was caused by circulating metabolites of the injected steroid. Since the concentration of the isotope in the tumor was dependent upon the estrogen receptor level, it would appear from these experiments that it is theoretically possible to use such compounds to image and monitor tumors that contain estrogen receptors. However, rapid metabolism would seem to preclude the use of 16 alpha-iodoestradiol itself for this purpose. These studies point to the possibility that the synthesis of analogs of 16 alpha-iodoestradiol, sterically protected against inactivation by rapid metabolism, may lead to a radiopharmaceutical agent that would be useful for imaging and monitoring estrogen receptor containing tumors.

Adult↗

PubMed1988

N-(3-(p-azido-m-[125I]iodophenyl)propionyl)-succinimide--a heterobifunctional reagent for the synthesis of radioactive photoaffinity ligands: synthesis of a carrier-free 125I-labeled cardiac glycoside photoaffinity label.

A new heterobifunctional reagent, N-(3-(p-azido-m-iodophenyl)propionyl)-succinimide (AIPPS), was synthesized and chemically characterized. The radiochemical form of the reagent, [125I]AIPPS, should be of general use as a photoactive reagent for the derivatization of free amino groups on a large variety of biologically active compounds, including many hormones. Amino-containing ligands can be derivatized with [125I]AIPPS in a method which is similar to that used for the 125I-labeled Bolton-Hunter reagent (N-(3-(p-hydroxyphenyl)propionyl)-succinimide). The added advantage with [125I]AIPPS, however, is that the ligand derivative is made both photoactive and radioactive in a single step. As an example of how this reagent can be used, we have prepared carrier-free [125I]AIPPS and reacted it with the amino-containing cardiac glycoside, 4-amino-4,6-dideoxyglucosyl digitoxigenin (GluD). The radioiodinated cardiac glycoside, [125I]AIPP-GluD, was purified by thin-layer chromatography and was carrier-free with a specific radioactivity of 2175 Ci/mmol. [125I]AIPP-GluD was an effective photoaffinity label for Na,K-ATPase as shown by specific photoaffinity labeling of purified canine kidney enzyme and human erythrocyte enzyme.

Affinity Labels↗

PubMed1989

A novel derivative of the chelon desferrioxamine for site-specific conjugation to antibodies.

We describe the preparation of the modified chelator aminooxyacetyl-ferrioxamine, and the replacement of its iron atom by 67Ga at high specific activity. The aminooxy function of this compound was allowed to react with the aldehyde groups generated by the periodate oxidation of the oligosaccharide of a mouse IgG1 monoclonal antibody (MAb) directed against carcino-embryonic antigen (CEA). The use of the aminooxy group allowed a stable bond to be formed between the chelon and the antibody with no need for reduction. Iron was removed from the ferrioxamine moiety and replaced by 67Ga either before or after conjugation of the chelon to the antibody. In either case the labelled antibody was injected into nude mice bearing a human colon carcinoma having the appropriate antigenicity. Unoxidized antibody, labelled with 125I by conventional methods, was co-injected as an internal control. Additional control experiments were carried out with a non-immune IgG using the same 67Ga-labelled modified chelon as above. The in vivo distribution of the modified antibodies was evaluated at various times between 24 and 96 hr after injection. The methods used were gamma-camera imaging and, more quantitatively, gamma-counting of the various organs after dissection. Interestingly, with the metal-chelon-labelled antibody, the intensity and specificity of tumor labelling was comparable and in some cases superior to the results obtained with radio-iodinated antibody. In particular, there was almost no increase in liver and spleen uptake of radioactive metal relative to radio-iodine, contrary to what has been observed with most antibodies labelled with 111In after conjugation with DTPA.

Animals↗

PubMed1975

Binding of the 35-s of 35-s-propylthiouracil by follicular thyroglobulin in vivo and in vitro.

Radioactivity was found bound to follicular thyroglobulin after administration of 35-S-propylthiouracil (PTU) to rats. Denaturation of the thyroglobulin using various procedures could not separate the 35-S from the protein; it was concluded that the 35-S is bound to thyroglobulin covalently. Fractionation of saline-soluble thyroid proteins was performed by ultracentrifugation on sucrose gradients. The PTU-sulphur/thyroglobulin (S/Tg) molar ratio was calculated in all fractions. One hour after the injection of PTU the S/Tg molar ratio was the same for 19S thyroglobulin from rats on stock diet and 18S thyroglobulin from rats on low iodine diet. Injection of KI to the animals before administration of 35-S-PTU significantly reduced the ratio. The highest S/Tg ratio 1.10 was noted at 19S thyroglobulin, 17 h after a single injection of PTU. Daily injection of PTU for six days increased the S/Tg ratio to 3.3. Inverse relationship between dose of PTU and S/Tg ratio was noted at one hour. In animals injected with large dose of 35-S-PTU and sacrificed several hours later the S/Tg was higher at the 12S subunits than at the 19S protein. The amount of PTU bound to 3-8S subunits was minimal. Sulphite liberated 64 percent of the 35-S bound to thyroglobulin which appeared as four compounds on thin layer chromatography plates. The main 35-S compound liberated by sulphite was sulphate.

Animals↗

PubMed1991

Six methods for direct radioiodination of mouse epidermal growth factor compared: effect of nonequivalence in binding behavior between labeled and unlabeled ligand.

Mouse epidermal growth factor (EGF) was radioiodinated by six different direct iodination methods. The 125I-labeled EGF preparations were distinguished by analyzing the binding of the radioligand to the EGF receptor (EGFR)-containing human placental membranes. The receptor-binding affinity of EGF labeled with Chloramine T was less than the affinity of unlabeled EGF, which precluded an accurate determination of the specific radioactivity of the 125I-labeled EGF preparation by "self-displacement analysis." Scatchard analysis of competitive binding data (increasing concentrations of unlabeled EGF) obtained with commercially prepared 125I-labeled EGF (Chloramine T method), according to the specific radioactivity stated by the manufacturer, resulted in a substantial underestimation of the apparent number of receptors. Iodination of EGF with Iodogen or Iodo-beads, reagents claimed to be more gentle because of their solid state, also yielded 125I-labeled EGF preparations that were not equivalent to the native EGF in receptor binding. In contrast, equivalence in the ligand-receptor interaction between labeled and unlabeled EGF could be achieved by iodinating EGF with iodine monochloride (ICl), Protag-125, or lactoperoxidase-glucose oxidase-coupled beads (Enzymobeads). Scatchard plots of saturation and competitive binding data obtained with these 125I-labeled EGF preparations produced identical results for apparent receptor number and apparent dissociation constants. Such radioiodinated EGF preparations yield relevant binding data in competition studies of labeled and unlabeled EGF.

Animals↗

PubMed1999

Omental transfer to the brain: an experimental study in hydrocephalic rabbits.

Hydrocephalus is a common and potentially lethal condition in children that results from an imbalance between absorption and production of cerebral spinal fluid (CSF). Silastic shunts are inserted to drain excess CSF, but they are prone to a number of problems, and at times may be unreliable and ineffective. This study examines the physiological basis of a pedicled omental transfer to the brain as a functional conduit for CSF in an experimentally induced hydrocephalic rabbit model. The ability of the omentum to transport CSF from the subarachnoid space was tested using radioactive tracer substances: radio-iodinated serum albumin (125I-RISA), chromium 51-ethylenediaminetetraacetate (51Cr-EDTA), and technetium 99m (99mTc) glucoheptonate. Immediate ability of exteriorized omentum to transport artificial CSF, as well as transposed omental transport of subarachnoid CSF at 1 month, were examined. Nuclear scan measurements were correlated with clinical observation and a double-blind histological analysis with trichrome and hematoxylin-eosin stain. Exteriorized omentum rapidly absorbed 99mTc glucoheptonate-labeled artificial CSF, with a rapid appearance in the systemic circulatory and urinary systems. Transposed omentum to the brain in animals with artificially created hydrocephalus showed evidence of CSF-labeled 125I-RISA and 51Cr-EDTA absorption in those animals demonstrating histologically viable omentum.

Animals↗

PubMed2001

Photochemical oxidation of iodized X-ray contrast media (XRC) in hospital wastewater.

Iodized X-ray contrast media (XRC) for medical applications are responsible for the high concentration of AOX (halogenated organic compounds adsorbable on activated carbon) in hospital wastewater exceeding the legal German discharge limit. The refractory properties of these substances lead to an accumulation in the natural waterbody. The elimination of contrast media from hospital wastewater by photochemical oxidation with hydrogen peroxide was investigated. The mechanism and the kinetics of the degradation of XRC were examined. These experiments demonstrate that a complete removal of the organically bonded iodine and a partial mineralization is feasible. The degradation in the UV reactor could be enhanced by adding hydrogen peroxide and by using a bubble column to remove the formed elemental iodine from the solution by stripping. Furthermore, the influence of various operating parameters such as gas flowrate, H2O2 input, XRC concentration and kind of XRC were investigated. Experiments showed that a recycling of elemental iodine from the exhaust gas is technically and economically possible.

Contrast Media↗

PubMed2004

An activity-based probe for the determination of cysteine cathepsin protease activities in whole cells.

We describe a novel diazomethylketone-containing irreversible inhibitor (BIL-DMK) which is specific for a subset of pharmaceutically important cysteine cathepsin proteases. BIL-DMK rapidly inactivates cathepsins B, F, K, L, S, and V in isolated enzyme assays and labels cathepsins in whole cells. The presence of catalytically active cathepsins B, L, and K or S was demonstrated using radioiodinated BIL-DMK in HepG2 (hepatoma), HIG82 (rabbit synoviocyte), and Ramos (B lymphoma) cell lines, respectively. The identity of each protein labeled was confirmed from the isoelectric point and molecular mass of the radioactive spots on two-dimensional gel and by comigration with each cathepsin as identified by immunoblotting. These cell lines were used to establish whole-cell enzyme occupancy assays to determine the potency of both irreversible and reversible inhibitors against each cathepsin in their native cellular lysosomal or endosomal environment. These whole-cell enzyme occupancy assays are useful to determine the cellular permeability of competing inhibitors and have the advantage of not requiring specific substrates for each cathepsin of interest.

Animals↗

PubMed1988

Glomerular filtration rate in adults estimated from 123iodine-hippuran and 99mtechnetium-diethylenetriaminepenta-acetic acid gamma camera renography.

In a retrospective study a close relationship was found between the rate constant for renal clearance of the radioactive indicator (lambda pk) and the glomerular filtration rate (GFR) measured by 51Cr-EDTA plasma clearance. The material comprised eighteen adult subjects submitted to 123I-hippuran gamma camera renography (IHGR) and twenty-two adult subjects to 99mTc-DTPA gamma camera renography (TDGR). The rate constant was calculated from a bi-exponential decomposition of the activity-time curve recorded within a small region of interest over the left ventricle. The total cleared renal fraction (TCRF) of the cardiac output with respect to the radioactive indicator has previously been shown to be closely related to GFR. A pooled estimate of GFR (GFRp) was calculated from the stochastically independent estimates of GFR based on lambda pk and TCRF. The comparison of GFRp with measured GFR was satisfactory and yielded substantially smaller standard deviations (SD) of GFRp than estimates based on lambda pk and TCRF separately. The standard deviations of GFRp were about 7 and 12 ml/min/1.73 m2 in IHGR for GFR equal to 50 and 100 ml/min/1.73 m2, respectively. The corresponding SD in TDGR were about 7 and 11 ml/min/1.73 m2. These standard deviations are sufficiently small for many clinical purposes and the method requires no blood samples or urine collections.

Adult↗

PubMed1978

Entry of [3H]norepinephrine, [125I]albumin and Evans blue from blood into brain following unilateral osmotic opening of the blood-brain barrier.

The blood-brain barrier in adult rats was opened unilaterally by infusing 1.58 M L (+)-arabinose in 0.9% NaCl solution into the internal carotid artery, via a catheter in the external carotid. The common carotid remained patent during the procedure. Osmotic barrier opening allowed entry into the brain of three intravascularly administered tracers--a visual tracer Evans blue (pulsely injected) and radioactive tracers [3H]norepinephrine (continuously infused) and [125I]albumin (pulsely injected). In osmotically perfused brain tissue, uptake of both 3H and 125I from blood was increased 2-5-fold above control, with maximal increases observed in the caudate nucleus, hippocampus and thalamus. In control brain regions, Evans blue and albumin remained intravascular, whereas norepinephrine was taken up, possibly by sympathetic nerve endings in cerebral vessels, as a function of blood plasma concentration and duration of exposure. The barrier closed within 4 h after intracarotid arabinose infusion, and barrier opening was not associated with edema as measured two days after infusion.

Animals↗

PubMed1999

Evaluation of radioiodinated medium chain fatty acids as new diagnostic agents for the determination of hepatic viability.

Radiopharmaceuticals which reflect beta-oxidation in hepatocytes will provide useful information on the prognosis after surgery or on the efficacy of treatment, since beta-oxidation is the main pathway responsible for adenosine triphosphate in hepatocytes. We have previously developed [1-11C]octanoate as a diagnostic agent for determination of hepatic viability by means of positron emission tomography (PET). The goal of the present study was to develop a new radiopharmaceutical for single-photon emission tomography (SPET), which has the advantage of being more widely used than PET. To this end, two radioiodinated omega-(4-iodophenyl)-medium chain fatty acids, p-iodophenylvaleric acid (IPVA) and p-iodophenylenanthic acid (IPEA), were synthesized and evaluated as radiopharmaceuticals for determination of hepatic viability. Metabolite analyses in vitro and in vivo and a biodistribution study in normal mice indicated that both compounds were taken up by the liver actively and metabolized by beta-oxidation. However, these studies also indicated that IPEA is more suitable as an imaging agent than IPVA. Based on these results, SPET imaging studies were performed in normal and hepatitis model rats using [123I]IPEA. The time-activity curves of the liver showed two-phase clearance of radioactivity in both normal and hepatitis model rats, but the clearance was delayed depending on the severity of hepatitis. Furthermore, the clearance rate of the first phase was correlated with the ATP level in hepatocytes, which was used as an index of the energy production capacity of hepatocytes. In conclusion, IPEA was metabolized predominantly by beta-oxidation, and the clearance of IPEA from the liver was closely associated with the ATP concentration in the liver. Thus, [123I]IPEA is a potentially useful new radiopharmaceutical for diagnosis of hepatic viability based on energy metabolism.

Animals↗