Respiratory quotient

Last updated

The respiratory quotient (RQ or respiratory coefficient) is a dimensionless number used in calculations of basal metabolic rate (BMR) when estimated from carbon dioxide production. It is calculated from the ratio of carbon dioxide produced by the body to oxygen consumed by the body, when the body is in a steady state. Such measurements, like measurements of oxygen uptake, are forms of indirect calorimetry. It is measured using a respirometer. The respiratory quotient value indicates which macronutrients are being metabolized, as different energy pathways are used for fats, carbohydrates, and proteins. [1] If metabolism consists solely of lipids, the respiratory quotient is approximately 0.7, for proteins it is approximately 0.8, and for carbohydrates it is 1.0. Most of the time, however, energy consumption is composed of both fats and carbohydrates. The approximate respiratory quotient of a mixed diet is 0.8. [1] Some of the other factors that may affect the respiratory quotient are energy balance, circulating insulin, and insulin sensitivity. [2]

Contents

It can be used in the alveolar gas equation.

Respiratory exchange ratio

The respiratory exchange ratio (RER) is the ratio between the metabolic production of carbon dioxide (CO2) and the uptake of oxygen (O2). [3] [4]

The ratio is determined by comparing exhaled gases to room air. Measuring this ratio is equal to RQ only at rest or during mild to moderate aerobic exercise without the accumulation of lactate. The loss of accuracy during more intense anaerobic exercise is among others due to factors including the bicarbonate buffer system. The body tries to compensate for the accumulation of lactate and minimize the acidification of the blood by expelling more CO2 through the respiratory system. [5]

The RER can exceed 1.0 during intense exercise. A value above 1.0 cannot be attributed to the substrate metabolism, but rather to the aforementioned factors regarding bicarbonate buffering. [5] Calculation of RER is commonly done in conjunction with exercise tests such as the VO2 max test. This can be used as an indicator that the participants are nearing exhaustion and the limits of their cardio-respiratory system. An RER greater than or equal to 1.0 is often used as a secondary endpoint criterion of a VO2 max test. [5]

Calculation

The respiratory quotient (RQ) is the ratio:

RQ = CO2 eliminated / O2 consumed

where the term "eliminated" refers to carbon dioxide (CO2) removed from the body in a steady state.

In this calculation, the CO2 and O2 must be given in the same units, and in quantities proportional to the number of molecules. Acceptable inputs would be either moles, or else volumes of gas at standard temperature and pressure.

Many metabolized substances are compounds containing only the elements carbon, hydrogen, and oxygen. Examples include fatty acids, glycerol, carbohydrates, deamination products, and ethanol. For complete oxidation of such compounds, the chemical equation is

CxHyOz + (x + y/4 - z/2) O2 → x CO2 + (y/2) H2O

and thus metabolism of this compound gives an RQ of x/(x + y/4 - z/2).

For glucose, with the molecular formula, C6H12O6, the complete oxidation equation is C6H12O6 + 6 O2 → 6 CO2 + 6 H2O. Thus, the RQ= 6 CO2/ 6 O2=1.

For oxidation of a fatty acid molecule, namely palmitic acid: [6]

A RQ near 0.7 indicates that fat is the predominant fuel source, a value of 1.0 is indicative of carbohydrate being the predominant fuel source, and a value between 0.7 and 1.0 suggests a mix of both fat and carbohydrate. [6] In general a mixed diet corresponds with an RER of approximately 0.8. [7] For fats, the RQ depends on the specific fatty acids present. Amongst the commonly stored fatty acids in vertebrates, RQ varies from 0.692 (stearic acid) to as high as 0.759 (docosahexaenoic acid). Historically, it was assumed that 'average fat' had an RQ of about 0.71, and this holds true for most mammals including humans. However, a recent survey showed that aquatic animals, especially fish, have fat that should yield higher RQs on oxidation, reaching as high as 0.73 due to high amounts of docosahexaenoic acid. [8]

The range of respiratory coefficients for organisms in metabolic balance usually ranges from 1.0 (representing the value expected for pure carbohydrate oxidation) to ~0.7 (the value expected for pure fat oxidation). In general, molecules that are more oxidized (e.g., glucose) require less oxygen to be fully metabolized and, therefore, have higher respiratory quotients. Conversely, molecules that are less oxidized (e.g., fatty acids) require more oxygen for their complete metabolism and have lower respiratory quotients. See BMR for a discussion of how these numbers are derived. A mixed diet of fat and carbohydrate results in an average value between these numbers.

RQ value corresponds to a caloric value for each liter (L) of CO2 produced. If O2 consumption numbers are available, they are usually used directly, since they are more direct and reliable estimates of energy production.

RQ as measured includes a contribution from the energy produced from protein. However, due to the complexity of the various ways in which different amino acids can be metabolized, no single RQ can be assigned to the oxidation of protein in the diet.

Insulin, which increases lipid storage and decreases fat oxidation, is positively associated with increases in the respiratory quotient. [2] A positive energy balance will also lead to an increased respiratory quotient. [2]

Applications

Practical applications of the respiratory quotient can be found in severe cases of chronic obstructive pulmonary disease, in which patients spend a significant amount of energy on respiratory effort. By increasing the proportion of fats in the diet, the respiratory quotient is driven down, causing a relative decrease in the amount of CO2 produced. This reduces the respiratory burden to eliminate CO2, thereby reducing the amount of energy spent on respirations. [9]

Respiratory Quotient can be used as an indicator of over or underfeeding. Underfeeding, which forces the body to utilize fat stores, will lower the respiratory quotient, while overfeeding, which causes lipogenesis, will increase it. [10] Underfeeding is marked by a respiratory quotient below 0.85, while a respiratory quotient greater than 1.0 indicates overfeeding. This is particularly important in patients with compromised respiratory systems, as an increased respiratory quotient significantly corresponds to increased respiratory rate and decreased tidal volume, placing compromised patients at a significant risk. [10]

Because of its role in metabolism, respiratory quotient can be used in analysis of liver function and diagnosis of liver disease. In patients with liver cirrhosis, non-protein respiratory quotient (npRQ) values act as good indicators in the prediction of overall survival rate. Patients having a npRQ < 0.85 show considerably lower survival rates as compared to patients with a npRQ > 0.85. [11] A decrease in npRQ corresponds to a decrease in glycogen storage by the liver. [11] Similar research indicates that non-alcoholic fatty liver diseases are also accompanied by a low respiratory quotient value, and the non protein respiratory quotient value was a good indication of disease severity. [11]

Recently the respiratory quotient is also used from aquatic scientists to illuminate its environmental applications. Experimental studies with natural bacterioplankton using different single substrates suggested that RQ is linked to the elemental composition of the respired compounds. [12] By this way, it is demonstrated that bacterioplankton RQ is not only a practical aspect of Bacterioplankton Respiration determination, but also a major ecosystem state variable that provides unique information about aquatic ecosystem functioning. [12] Based on the stoichiometry of the different metabolized substrates, the scientists can predict that dissolved oxygen (O2) and carbon dioxide (CO2) in aquatic ecosystems should covary inversely due to the processing of photosynthesis and respiration. [13] Using this quotient we could shed light on the metabolic behavior and the simultaneous roles of chemical and physical forcing that shape the biogeochemistry of aquatic ecosystems. [13]

Moving from a molecular and cellular level to an ecosystem level, various processes account for the exchange of O2 and CO2 between the biosphere and atmosphere. Field measurements of the concurrent consumption of oxygen (-ΔO2) and production of carbon dioxide (ΔCO2) can be used to derive an apparent respiratory quotient (ARQ). [14] This value reflects a cumulative effect of not only the aerobic respiration of all organisms (microorganisms and higher consumers) in the sample, but also all the other biogeochemical processes which consume O2 without a corresponding CO2 production and vice versa influencing the observed RQ.

Respiratory quotients of some substances

Name of the substanceRespiratory Quotient
Carbohydrates 1
Proteins 0.8 - 0.9 [1]
Ketones (eucaloric)0.73 [15]
Ketones (hypocaloric)0.66 [16] [17] [18]
Triolein (Fat)0.71
Oleic acid (Fat)0.71
Tripalmitin (Fat)0.7
Malic acid 1.33
Tartaric acid 1.6
Oxalic acid 4.0

[19]

See also

Related Research Articles

<span class="mw-page-title-main">Carbon dioxide</span> Chemical compound with formula CO₂

Carbon dioxide is a chemical compound with the chemical formula CO2. It is made up of molecules that each have one carbon atom covalently double bonded to two oxygen atoms. It is found in the gas state at room temperature, and as the source of available carbon in the carbon cycle, atmospheric CO2 is the primary carbon source for life on Earth. In the air, carbon dioxide is transparent to visible light but absorbs infrared radiation, acting as a greenhouse gas. Carbon dioxide is soluble in water and is found in groundwater, lakes, ice caps, and seawater. When carbon dioxide dissolves in water, it forms carbonate and mainly bicarbonate, which causes ocean acidification as atmospheric CO2 levels increase.

<span class="mw-page-title-main">Carbohydrate</span> Organic compound that consists only of carbon, hydrogen, and oxygen

A carbohydrate is a biomolecule consisting of carbon (C), hydrogen (H) and oxygen (O) atoms, usually with a hydrogen–oxygen atom ratio of 2:1 and thus with the empirical formula Cm(H2O)n, which does not mean the H has covalent bonds with O. However, not all carbohydrates conform to this precise stoichiometric definition, nor are all chemicals that do conform to this definition automatically classified as carbohydrates.

<span class="mw-page-title-main">Ketone bodies</span> Chemicals produced during fat metabolism

Ketone bodies are water-soluble molecules or compounds that contain the ketone groups produced from fatty acids by the liver (ketogenesis). Ketone bodies are readily transported into tissues outside the liver, where they are converted into acetyl-CoA —which then enters the citric acid cycle and is oxidized for energy. These liver-derived ketone groups include acetoacetic acid (acetoacetate), beta-hydroxybutyrate, and acetone, a spontaneous breakdown product of acetoacetate.

<span class="mw-page-title-main">Red blood cell</span> Oxygen-delivering blood cell and the most common type of blood cell

Red blood cells (RBCs), referred to as erythrocytes in academia and medical publishing, also known as red cells, erythroid cells, and rarely haematids, are the most common type of blood cell and the vertebrate's principal means of delivering oxygen to the body tissues—via blood flow through the circulatory system. Erythrocytes take up oxygen in the lungs, or in fish the gills, and release it into tissues while squeezing through the body's capillaries.

<span class="mw-page-title-main">Ketosis</span> Using body fats as fuel instead of carbohydrates

Ketosis is a metabolic state characterized by elevated levels of ketone bodies in the blood or urine. Physiological ketosis is a normal response to low glucose availability. In physiological ketosis, ketones in the blood are elevated above baseline levels, but the body's acid–base homeostasis is maintained. This contrasts with ketoacidosis, an uncontrolled production of ketones that occurs in pathologic states and causes a metabolic acidosis, which is a medical emergency. Ketoacidosis is most commonly the result of complete insulin deficiency in type 1 diabetes or late-stage type 2 diabetes. Ketone levels can be measured in blood, urine or breath and are generally between 0.5 and 3.0 millimolar (mM) in physiological ketosis, while ketoacidosis may cause blood concentrations greater than 10 mM.

<span class="mw-page-title-main">Cellular respiration</span> Process to convert glucose to ATP in cells

Cellular respiration is the process by which biological fuels are oxidized in the presence of an inorganic electron acceptor, such as oxygen, to drive the bulk production of adenosine triphosphate (ATP), which contains energy. Cellular respiration may be described as a set of metabolic reactions and processes that take place in the cells of organisms to convert chemical energy from nutrients into ATP, and then release waste products.

<span class="mw-page-title-main">Ketogenesis</span> Chemical synthesis of ketone bodies

Ketogenesis is the biochemical process through which organisms produce ketone bodies by breaking down fatty acids and ketogenic amino acids. The process supplies energy to certain organs, particularly the brain, heart and skeletal muscle, under specific scenarios including fasting, caloric restriction, sleep, or others.

<span class="mw-page-title-main">Arterial blood gas test</span> A test of blood taken from an artery that measures the amounts of certain dissolved gases

An arterial blood gas (ABG) test, or arterial blood gas analysis (ABGA) measures the amounts of arterial gases, such as oxygen and carbon dioxide. An ABG test requires that a small volume of blood be drawn from the radial artery with a syringe and a thin needle, but sometimes the femoral artery in the groin or another site is used. The blood can also be drawn from an arterial catheter.

Carbohydrate metabolism is the whole of the biochemical processes responsible for the metabolic formation, breakdown, and interconversion of carbohydrates in living organisms.

Alkalosis is the result of a process reducing hydrogen ion concentration of arterial blood plasma (alkalemia). In contrast to acidemia, alkalemia occurs when the serum pH is higher than normal. Alkalosis is usually divided into the categories of respiratory alkalosis and metabolic alkalosis or a combined respiratory/metabolic alkalosis.

Basal metabolic rate (BMR) is the rate of energy expenditure per unit time by endothermic animals at rest. It is reported in energy units per unit time ranging from watt (joule/second) to ml O2/min or joule per hour per kg body mass J/(h·kg). Proper measurement requires a strict set of criteria to be met. These criteria include being in a physically and psychologically undisturbed state and being in a thermally neutral environment while in the post-absorptive state (i.e., not actively digesting food). In bradymetabolic animals, such as fish and reptiles, the equivalent term standard metabolic rate (SMR) applies. It follows the same criteria as BMR, but requires the documentation of the temperature at which the metabolic rate was measured. This makes BMR a variant of standard metabolic rate measurement that excludes the temperature data, a practice that has led to problems in defining "standard" rates of metabolism for many mammals.

<span class="mw-page-title-main">Oxygen cycle</span> Biogeochemical cycle of oxygen

Oxygen cycle refers to the movement of oxygen through the atmosphere (air), biosphere (plants and animals) and the lithosphere (the Earth’s crust). The oxygen cycle demonstrates how free oxygen is made available in each of these regions, as well as how it is used. The oxygen cycle is the biogeochemical cycle of oxygen atoms between different oxidation states in ions, oxides, and molecules through redox reactions within and between the spheres/reservoirs of the planet Earth. The word oxygen in the literature typically refers to the most common oxygen allotrope, elemental/diatomic oxygen (O2), as it is a common product or reactant of many biogeochemical redox reactions within the cycle. Processes within the oxygen cycle are considered to be biological or geological and are evaluated as either a source (O2 production) or sink (O2 consumption).

Fatty acid metabolism consists of various metabolic processes involving or closely related to fatty acids, a family of molecules classified within the lipid macronutrient category. These processes can mainly be divided into (1) catabolic processes that generate energy and (2) anabolic processes where they serve as building blocks for other compounds.

<span class="mw-page-title-main">Hitting the wall</span> Sudden fatigue during endurance sports

In endurance sports such as road cycling and long-distance running, hitting the wall or the bonk is a condition of sudden fatigue and loss of energy which is caused by the depletion of glycogen stores in the liver and muscles. Milder instances can be remedied by brief rest and the ingestion of food or drinks containing carbohydrates. Otherwise, it can be remedied by attaining second wind by either resting for approximately 10 minutes or by slowing down considerably and increasing speed slowly over a period of 10 minutes. Ten minutes is approximately the time that it takes for free fatty acids to sufficiently produce ATP in response to increased demand.

In biochemistry and metabolism, beta oxidation (also β-oxidation) is the catabolic process by which fatty acid molecules are broken down in the cytosol in prokaryotes and in the mitochondria in eukaryotes to generate acetyl-CoA. Acetyl-CoA enters the citric acid cycle, generating NADH and FADH2, which are electron carriers used in the electron transport chain. It is named as such because the beta carbon of the fatty acid chain undergoes oxidation and is converted to a carbonyl group to start the cycle all over again. Beta-oxidation is primarily facilitated by the mitochondrial trifunctional protein, an enzyme complex associated with the inner mitochondrial membrane, although very long chain fatty acids are oxidized in peroxisomes.

<span class="mw-page-title-main">Medium-chain triglyceride</span> Medium-chain fatty acids

A medium-chain triglyceride (MCT) is a triglyceride with two or three fatty acids having an aliphatic tail of 6–12 carbon atoms, i.e. a medium-chain fatty acid (MCFA). Rich food sources for commercial extraction of MCTs include palm kernel oil and coconut oil.

The alveolar gas equation is the method for calculating partial pressure of alveolar oxygen. The equation is used in assessing if the lungs are properly transferring oxygen into the blood. The alveolar air equation is not widely used in clinical medicine, probably because of the complicated appearance of its classic forms. The partial pressure of oxygen in the pulmonary alveoli is required to calculate both the alveolar-arterial gradient of oxygen and the amount of right-to-left cardiac shunt, which are both clinically useful quantities. However, it is not practical to take a sample of gas from the alveoli in order to directly measure the partial pressure of oxygen. The alveolar gas equation allows the calculation of the alveolar partial pressure of oxygen from data that is practically measurable. It was first characterized in 1946.

<span class="mw-page-title-main">Bioenergetic systems</span> Metabolic processes for energy production

Bioenergetic systems are metabolic processes that relate to the flow of energy in living organisms. Those processes convert energy into adenosine triphosphate (ATP), which is the form suitable for muscular activity. There are two main forms of synthesis of ATP: aerobic, which uses oxygen from the bloodstream, and anaerobic, which does not. Bioenergetics is the field of biology that studies bioenergetic systems.

Blood gas tension refers to the partial pressure of gases in blood. There are several significant purposes for measuring gas tension. The most common gas tensions measured are oxygen tension (PxO2), carbon dioxide tension (PxCO2) and carbon monoxide tension (PxCO). The subscript x in each symbol represents the source of the gas being measured: "a" meaning arterial, "A" being alveolar, "v" being venous, and "c" being capillary. Blood gas tests (such as arterial blood gas tests) measure these partial pressures.

<span class="mw-page-title-main">Indirect calorimetry</span> Measurement of the heat of living organisms through indirect means

Indirect calorimetry calculates heat that living organisms produce by measuring either their production of carbon dioxide and nitrogen waste, or from their consumption of oxygen. Indirect calorimetry estimates the type and rate of substrate utilization and energy metabolism in vivo starting from gas exchange measurements. This technique provides unique information, is noninvasive, and can be advantageously combined with other experimental methods to investigate numerous aspects of nutrient assimilation, thermogenesis, the energetics of physical exercise, and the pathogenesis of metabolic diseases.

References

  1. 1 2 3 Widmaier, Eric P.; Raff, Hershel; Strang, Kevin T. (2016). Vander's Human Physiology: The Mechanisms of Body Function (14th ed.). New York: McGraw Hill. ISBN   9781259294099.
  2. 1 2 3 Ellis, Amy C; Hyatt, Tanya C; Gower, Barbara A; Hunter, Gary R (2017-05-02). "Respiratory Quotient Predicts Fat Mass Gain in Premenopausal Women". Obesity. 18 (12): 2255–2259. doi:10.1038/oby.2010.96. ISSN   1930-7381. PMC   3075532 . PMID   20448540.
  3. ↑ Schmidt-Nielsen, Knut (1997). Animal Physiology. Cambridge, UK: Cambridge University Press. p. 171. ISBN   0-521-57098-0.
  4. ↑ Ramos-Jiménez, Arnulfo; Hernández-Torres, Rosa P.; Torres-Durán, Patricia V.; Romero-Gonzalez, Jaime; Mascher, Dieter; Posadas-Romero, Carlos; Juárez-Oropeza, Marco A. (2008-02-01). "The Respiratory Exchange Ratio is Associated with Fitness Indicators Both in Trained and Untrained Men: A Possible Application for People with Reduced Exercise Tolerance". Clinical Medicine. Circulatory, Respiratory and Pulmonary Medicine. 2: 1–9. doi:10.4137/CCRPM.S449. ISSN   1178-1157. PMC   2990231 . PMID   21157516 – via SAGE journals.
  5. 1 2 3 Katch, Victor L.; McArdle, William D.; Katch, Frank I. (2011). Essentials of exercise physiology (4th ed.). Philadelphia: Wolters Kluwer/Lippincott Williams & Wilkins Health. pp. 219–223. ISBN   9781608312672. OCLC   639161214.
  6. 1 2 Kenney, W. Larry.; Wilmore, Jack H.; Costill, David L. (2012). Physiology of sport and exercise (5th ed.). Champaign, IL: Human Kinetics. pp. 117–118. ISBN   9780736094092. OCLC   747903364.
  7. ↑ Widmaier, Eric P.; Vander, Arthur J.; Raff, Hershel; Strang, Kevin T. (2018). Vander's human physiology: the mechanisms of body function (15th ed.). New York, NY. p. 460. ISBN   9781259903885. OCLC   1006516790.{{cite book}}: CS1 maint: location missing publisher (link)
  8. ↑ Price, E. R.; Mager, E. M. (2020). "Respiratory quotient: Effects of fatty acid composition". Journal of Experimental Zoology. 333 (9): 613–618. Bibcode:2020JEZA..333..613P. doi:10.1002/jez.2422. PMID   33063463. S2CID   222833275.
  9. ↑ Kuo, C. D.; Shiao, G. M.; Lee, J. D. (1993-07-01). "The effects of high-fat and high-carbohydrate diet loads on gas exchange and ventilation in COPD patients and normal subjects". Chest. 104 (1): 189–196. doi:10.1378/chest.104.1.189. ISSN   0012-3692. PMID   8325067.
  10. 1 2 McClave, Stephen A.; Lowen, Cynthia C.; Kleber, Melissa J.; McConnell, J. Wesley; Jung, Laura Y.; Goldsmith, Linda J. (2003-01-01). "Clinical use of the respiratory quotient obtained from indirect calorimetry". Journal of Parenteral and Enteral Nutrition. 27 (1): 21–26. doi:10.1177/014860710302700121. ISSN   0148-6071. PMID   12549594.
  11. 1 2 3 Nishikawa, Hiroki; Enomoto, Hirayuki; Iwata, Yoshinori; Kishino, Kyohei; Shimono, Yoshihiro; Hasegawa, Kunihiro; Nakano, Chikage; Takata, Ryo; Ishii, Akio (2017-01-01). "Prognostic significance of nonprotein respiratory quotient in patients with liver cirrhosis". Medicine. 96 (3): e5800. doi:10.1097/MD.0000000000005800. ISSN   1536-5964. PMC   5279081 . PMID   28099336.
  12. 1 2 Berggren, Martin; Lapierre, Jean-François; del Giorgio, Paul A (May 2012). "Magnitude and regulation of bacterioplankton respiratory quotient across freshwater environmental gradients". The ISME Journal. 6 (5): 984–993. Bibcode:2012ISMEJ...6..984B. doi:10.1038/ismej.2011.157. ISSN   1751-7362. PMC   3329109 . PMID   22094347.
  13. 1 2 Vachon, Dominic; Sadro, Steven; Bogard, Matthew J.; Lapierre, Jean-François; Baulch, Helen M.; Rusak, James A.; Denfeld, Blaize A.; Laas, Alo; Klaus, Marcus; Karlsson, Jan; Weyhenmeyer, Gesa A. (August 2020). "Paired O 2 –CO 2 measurements provide emergent insights into aquatic ecosystem function". Limnology and Oceanography Letters. 5 (4): 287–294. Bibcode:2020LimOL...5..287V. doi: 10.1002/lol2.10135 . ISSN   2378-2242.
  14. ↑ Angert, A.; Yakir, D.; Rodeghiero, M.; Preisler, Y.; Davidson, E. A.; Weiner, T. (2015-04-07). "Using O<sub>2</sub> to study the relationships between soil CO<sub>2</sub> efflux and soil respiration". Biogeosciences. 12 (7): 2089–2099. Bibcode:2015BGeo...12.2089A. doi: 10.5194/bg-12-2089-2015 . hdl: 11572/225681 . ISSN   1726-4189.
  15. ↑ Mosek, Amnon; Natour, Haitham; Neufeld, Miri Y.; Shiff, Yaffa; Vaisman, Nachum (2009). "Ketogenic diet treatment in adults with refractory epilepsy: A prospective pilot study". Seizure. 18 (1): 30–3. doi: 10.1016/j.seizure.2008.06.001 . PMID   18675556. S2CID   2393385.
  16. ↑ Johnston, Carol S; Tjonn, Sherrie L; Swan, Pamela D; White, Andrea; Hutchins, Heather; Sears, Barry (2006). "Ketogenic low-carbohydrate diets have no metabolic advantage over nonketogenic low-carbohydrate diets". The American Journal of Clinical Nutrition. 83 (5): 1055–61. doi: 10.1093/ajcn/83.5.1055 . PMID   16685046.
  17. ↑ Phinney, Stephen D.; Horton, Edward S.; Sims, Ethan A. H.; Hanson, John S.; Danforth, Elliot; Lagrange, Betty M. (1980). "Capacity for Moderate Exercise in Obese Subjects after Adaptation to a Hypocaloric, Ketogenic Diet". Journal of Clinical Investigation. 66 (5): 1152–61. doi:10.1172/JCI109945. PMC   371554 . PMID   7000826.
  18. ↑ Owen, O. E.; Morgan, A. P.; Kemp, H. G.; Sullivan, J. M.; Herrera, M. G.; Cahill, G. F. (1967). "Brain Metabolism during Fasting*". Journal of Clinical Investigation. 46 (10): 1589–95. doi:10.1172/JCI105650. PMC   292907 . PMID   6061736.
  19. ↑ Telugu Academi, Botany text book, 2007 Version[ verification needed ]
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.