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A
Post-graduate
Credit Seminar
On
ARTIFICIAL BLOOD
Speaker: Patel Mehul D.
Reg. No. 04–VETMA–01194–2013
Course No. : VPY-691
Major Advisor
Dr. A. Lateef
Minor Advisor
Dr. B.S. Chandel
DEPARTMENT OF PHYSIOLOGY AND
BIOCHEMISTRY
CONTENTS
 Introduction
 History
 Types :
i. Perfluorocarbons
ii. Hemoglobin-based Products
 Advantage of Artificial Blood
 Other Promising Technique
 Artificial Blood Controversy
 Future Scope
 Conclusion
3
INTRODUCTION
Blood is circulated in the body through blood vessels by the pumping action of the
heart. With lungs, arterial blood carries oxygen from inhaled air to the tissues of the
body, and venous blood carries carbon dioxide, a waste product of metabolism
produced by cells, from the tissues to the lungs to be exhaled.
WHOLE BLOOD
RED BLOOD CELLS or
Erythrocytes (93%)
WHITE BLOOD
CELLS or Leucocytes
(0.16%)
AGRANULOCYTS
Lymphocytes- 20-40% of white
cells
MonocyteS – 1-10% white cells
GRANULOCYTES
Neutrophils – 50-70% of white cells
Eosinophils ~ 3% of white cells
Basophils ~ 1% of white cells
SOLID FRACTION
(Cells-45%)
PLATELETS or
Thrombocytes (6-7%)
FLUID FRACTION
(Plasma-55%)
5
What is blood?
Blood has many functions :
 Transportation
 Regulation of Body temperature and pH
 Protection against blood loss through clotting
 Protection against diseases through phagocytic
white blood cells and antibodies
6
“Blood is the life” (Riess, 2001)
•When a patient looses too much blood due to trauma
or surgery, the blood volume and RBCs will be reduced
•In such an emergency situation, doctors will often give patients
volume expanders to make up for lost blood volume.
•This helps to restore normal blood pressure and lets the remaining
red blood cells continue to carry oxygen.
•If it is not enough, doctors can give patients blood transfusions to
replace some of the lost blood.
7
Clinical perspective of blood transfusion?
Do animals need blood transfusion?
 Animals need blood transfusions for the same reasons that
humans do, including surgery, trauma and diseases.
(http://k9bloodbank.com)
8
Usually, the need for blood
transfusions is acute, as in acute
hemorrhage
Transfusions are also appropriate in
treatment of acute or chronic anemias.
Animals with hemostatic disorders
often require repeated transfusions
(Cotter, 2013)
What are blood types?
Another protein, an antigen, may be found on some red blood cells - called Rh factor. Blood
cells that have Rh factor are RhD positive, those that don't are RhD negative. 9
Animals Blood types
Dogs DEA 1.1, 1.2, 3, 4, 7, and Dal. (DEA system=Dog Erythrocyte antigen
system)
DEA 1.1 negative= Universal Donor
DEA 1.1 positive=Universal Recipient
(Wardrop, 2007)
Cats The main blood group system in cats is the A-B grouping. Cats can be
either type A, type B or type AB.
(http://www.catblooddonors.com/for-cat-owners/about-cat-blood-
transfusions.php)
Cattle The polymorphic systems in cattle include the A, B, C, F, J, L, M, S,
and Z polymorphisms.
(http://en.wikipedia.org/wiki/Blood_type_non-human)
Horses There are eight major recognized blood groups in horses Viz., A, C,
D, K, P, Q, U and T.
( http://en.wikipedia.org/wiki/Blood_type_non-human)
Blood types in animals
 When transfusion is required, cross matching should be
performed or a universal donor may be used.
Cross-match should be performed in the following situations:
1) Naturally occurring antibodies to foreign blood group
antigens. This occurs in the cat. In this species, a cross-match
should be performed on the first and every transfusion
 Type A cats should receive only type A blood and type B cats
should receive only type B blood. However type AB cats can
receive either Type A or Type B blood with minimal or no clinical
reactions
(Henset, 2011)
11
2) Sensitization of an animal to foreign red cell
antigens, in a species without naturally occurring
antibodies. This is the situation in the dog and horse,
resulting in the production of acquired antibodies. In
these species, a cross-match does not need to be
performed on the first transfusion the animal receives
but should be performed at subsequent transfusions.
 Also in cow, buffalo, sheep, goat and pig, a single,
unmatched whole blood transfusions are generally safe
(Weiss and Wardrop, 2010)
12
13
Blood collection :
The donor cow restrained in a
head bail and given a small
injection of sedation if needed.
Blood collection takes around
20-30 minutes.
Blood transfusion :
The recipient cow restrained
by halter (and in a head bail if
possible). Blood transfusion
takes around 20 minutes.
http://www.franklinvets.co.nz/Dairy++BeefSheep/Farm+Services/Animal+Health/theileria.html
Blood transfusions can be critical, life-saving
procedures.
Blood needs to be readily available—and that
requires a blood bank.
Do animas have blood bank ?
14
India's 1st government blood bank for dogs started in Chennai by the
Tamil Nadu Veterinary and Animal Sciences University (TANUVAS)
in 2010.
(http://timesofindia.indiatimes.com/india/Indias-1st-blood-bank-for-dogs-
opens-in-TN/articleshow/5861905.cms) 15
 Even in veterinary field, there are several blood
banks which store animal blood for future
transfusion.
Animal Blood Bank
16
Volunteer donor dog during a donation: The dog lies
comfortably on his side and a needle is placed in his
jugular vein to extract the blood. The procedure takes
about 15 to 20 minutes in most dogs.
Drawbacks:
According to Riess (2001) blood transfusion carries and will always carry a certain
level of risk.
Blood has to be kept cool (4° C ), and it has a shelf life of 42 days
(Lockwood et al.,2003)
 Prolonged RBC storage before transfusion increases multiorgan failure and
mortality in patients (Eldad et al., 2010)
 The effects of prolonged storage on red cells include decreased deformability;
depletion of 2,3-diphosphoglycerate (2,3-DPG); increased adhesiveness and
aggregability; reduction in the concentrations of nitric oxide and adenosine
triphosphate etc
(Koch et al., 2008)
17
 Blood supply shortages :
– A country needs a minimum stock of blood equal to 1 per cent of its
population.
– The total recorded blood collection in India is 4 million units, which meet
only 40% of need against a least requirement of 10 million units.
(World Health Organization, 2008)
 Safety of blood supply and risk of infections
– Risk of transmission of HIV, Hep B, Hep C, and other blood borne diseases
– Mistransfusions due to error – Blood Group matching required.
(Scott et al., 1997)
 Cost
– Donations, screening, storage, and administration ~ 800-1200 Rs.
(Maiti, 2012)
18
The term “artificial blood” is really a misnomer. The
complexity of blood is far too great to allow for
absolute duplication in a laboratory.
(Kresie, 2001)
Artificial blood is a product made to act as a substitute
for blood for the transportation of oxygen throughout the
body.
(Shalini, 2012)
It is also called as Blood Substitute or Arificial Oxygen
Carrier.
19
This is where artificial blood comes in
The most promising artificial blood products are
1. Perflourocarbons (PFCs) and
2. Haemoglobin based oxygen carriers (HBOCs).
(Mohankrishna et al., 2011)
The delivery of oxygen by oxygen carriers of the these two
classes of have both benefits and risks which are unique to their
class.
(Tremper et al., 1980)
20
21
HISTORY OF
ARTIFICIAL BLOOD
In 1616, when William
Harvey first described
the circulation of blood
In 1665, the first
recorded successful
blood transfusion on dog
by Richard Lower
22
(http:// www.redcrossblood.org)
History
Many materials used for transfusion that include beer,
urine, milk, plant resins, and sheep blood.
In 1854, patients were injected with milk to treat Asiatic
cholera.
Other materials that were tried during the 1800s include
hemoglobin and animal plasma.
(Chang, 2004)
In 1883,there was a creation of Ringer's solution. In
research using part of a frog's heart, Sydney Ringer,
found that the heart could be kept beating by applying the
solution.
(Hoffman et al., 1990)
23
Contd...
In 1909, Karl Landsteiner
classified human blood into four
different groups: A, B, AB, and
O.
A fourth group AB was
discovered the following year.
(Squires, 2002)
Karl Landsteiner
24
Contd...
 During World War I, galactoso-
gluconic acid was used to extend
plasma.
 World War II, human plasma was
used to replace blood and to save
soldiers from hemorrhagic shock.
 Eventually, this led to the
establishment of blood banks by the
American Red Cross in 1947.
(Kirschman and Ruth , 2005)
25
Contd...
 In 1966, experiments with mice suggested a new type of blood
substitute, perfluorocarbons (PFCs).
 In 1968, the rat's blood replaced with a PFC emulsion and it
lived for a few hours and recovered fully after blood was
replaced.
(Sarkar, 2008)
 However, the established blood bank system in developed
countries worked so well that research on blood substitutes
waned in those countries. It received renewed interest when
the shortcomings of the blood bank system were discovered
during the Vietnam conflict. This prompted some
researchers to begin looking for hemoglobin solutions
(Jani et al., 2012)
26
Contd...
Ideal Artificial Blood
 Increased availability that would rival that of donated blood, even surpass it
 Oxygen carrying capacity, equaling or surpassing that of biological blood
 Volume expansion
 Universal compatibility: elimination of cross matching
 Pathogen free: elimination of blood contained infections
 Minimal side effects
 Survivability over a wider range of storage temperatures
 Long shelf life
 Cost efficient
(Squires, 2002)
27
Types of Blood Substitutes
1) Perfluorocarbons (PFCs), chemical compounds which can carry
and release oxygen
2) Haemoglobin-based oxygen carriers (HBOCs) derived from
humans, animals, or artificially via recombinant technology
28(Jani et al.,2012)
Perfluorocarbons
29
Perfluorocarbons (PFCs)
Perfluorocarbons are low-molecular-weight linear or cyclic
hydrocarbons in which hydrogen atoms of the carbon chain
have been substituted by fluorine atom, leading to total
chemical inertness and a complete lack of metabolism in
vivo. (Jahr et al., 2007)
1st Generation
Fluosol-DATM
2nd Generation
OxyfluorTM
OxygentTM
30
3rd Generation
PerftoranTM
PHER-O2
TM
31
Fluosol-DATM OxygentTM
PerftoranTM
The PFC particles are about 0.2 microns in diameter
(1/40th of RBC size), with a perfluorocarbon core and a
thin lecithin phospholipids as a coating
(Mohankrishna et al., 2011)
 The perfluorocarbons are not hydrosoluble and administered
as emulsions called perfluorocarbon emulsions (PFCEs)
(Squires, 2002)
32
 Perfluorocarbons do not have the oxygen-bonding properties but act as
simple solvents.
 The transport and liberation of gases based on their physical solubility,
and the quantity of gas dissolved linearly related to its partial pressure.
(Jahr et al., 2007)
 They Can dissolve more oxygen than the biological blood.
(Cabrales and Intaglietta, 2013)
 They carry much less oxygen than hemoglobin-based products
(Jani et al., 2012)
33
Physiology of carrying oxygen
Structure of PFC
34(Tao and Ghoroghchian, 2014)
Ingredients Quantity (%)
Perfluoro-octyl bromide 28
FO-9982 12
Yolk lecithin 2.4
DSPE-50 H 0.12
Distilled water 57.48
Table 1. Composition of PFC based blood substitute
(Mitsuhiro et al., 2005)
35
Where, DSPE= Distearoyl phosphatidyl
ethanolamine (ammonium salt)
FO =Perfluoroalcohol esters with oleic acid
 The first generation of PFCEs developed was Fluosol-DATM in 1989.
 Fluosol-DATM was approved by US FDA in human, but withdrawn later
because of marginal benefits and development of flu-like symptoms
(Castro and Briceno, 2010)
 The second generation of PFCEs developed were OxyfluorTM and
OxygentTM, with improved lipophilicity
(Modery et al., 2013)
36
Developments in PFCEs
 However, OxyfluorTM was terminated after early clinical
trials due to its severe side effects
 OxygentTM was also terminated, because of an increased
incidence of stroke in coronary bypass patients
The third generation PFCEs are PerftoranTM and PHER-O2
TM
Pulmonary complications has been reported with the use of
PerftoranTM and, PHER-O2
TM is in reasearch
(Modery et al., 2013)
37
Contd…
Table 2. Current status of PFC based products
Name Sponsor Status
OxygentTM Alliance
pharmaceuticals
(USA)
Discontinued
OxycyteTM Oxygen
biotherapeutics
(USA)
Discontinued
PHER-O 2TM Sanguine Corp
(USA)
In research
PerftoranTM PERFTORAN
(Russia)
Approved in Russian clinical
application.
38
 Cheap and easy to manufacture in large quantities
 Can be stored at room temperature for more than 1 year
 Can be mixed safely with any blood group without the need to
check first
 The molecules are smaller than red blood cells, allowing them to
bypass arterial blockages and penetrate small capillaries with
ease, delivering oxygen to areas which need it most
 Effect of chemotherapy or radiation in tumour treatment can be
enhance when patient pretreated with PFCs
(Jani et al., 2012; Singh et al.,2012)
Benefits of Perfluorocarbon based products
39
Adverse
Effects
Of PFC
Allergy
Especially 1st Gen
Repeated doses
may cause hepatic
engorgement
Retained in RE
system
Decrease
platelet count
Impaired neutrophil
function
•Early: Headache
•Late: Flu like
symptoms
(Dietz et al., 1996; Jahr et al., 2007; )
40
Hemoglobin-based oxygen
carriers
41
Understanding Hemoglobin (Hb) :
 The structure of Hb was determined in 1959 by Max
Perutz.
 Molecular weight 64.5 kDa
 Tetrameric protein comprised of two α and two ß-
globin subunits that fold into compact quaternary
structure (α 2 ß 2).
 Each α and ß subunit contain an iron-heme group that
binds to oxygen molecule allowing for transport.
42
43
 A Hb molecule carries a maximum of four oxygen
molecules.
 Various factors such as low pH and high CO2 and high
2,3-diphosphoglycerate (DPG) level in the tissues,
cause a lower oxygen affinity state facilitating oxygen
offloading.
 As oxygen is being unloaded, CO2 binds to Hb,
resulting in carbamino-Hb.
44
Contd…
 Local conditions in the lungs including higher O2,
higher pH, and lower 2,3 DPG level, cause Hb to shift
back to the higher oxygen affinity state.
 Such a transition favors CO2 release, which is then
exhaled.
45
Contd…
HBOCs
In search for an alternative to PFCs,
considerable efforts have been made in
the development of acellular Hb based
oxygen carriers…
46
 To prepare acellular Hb, Hb is derived from human or
bovine blood by chemical modifications or from
bacteria host systems by genetic recombinantion
(Alayash, 2014)
 Human hemoglobin is obtained from donated blood that
has reached its expiration date
 One unit of hemoglobin solution can be produced for every
2 units of discarded blood
(Lesley, 2001)
47
HBOCs (Hemoglobin-based oxygen carriers)
Once obtained from any of these sources, the
hemoglobin must be purified and modified to decrease
its toxicity and increase its effectiveness
• The first clinical study with free hemoglobin resulted in
nephrotoxicites. The hemoglobin used was found to
have erythrocyte membrane stromal lipids as well as
bacterial endotoxins.
(Shalini, 2012)
• To side-step these problems, stroma-free hemoglobin was
developed, but new problems arose,
o 1) too short intravascular half life
o 2) too high affinity for oxygen
(Jean, 2001)
48
1) Stroma free Hb had too short of an intravascular half life
because tetrameric Hb (α 2 ß 2) dissociated into αß
dimmers that were filtered by the kidneys and excreted in
the urine.
2) Stroma free Hb had too high of an oxygen affinity because
2,3-DPG was lost during the purification process.
(Shalini, 2012)
 To increase the intravenous half life of hemoglobin solutions,
manufacturers had to develop methods to stabilize the
hemoglobin tetrameric structure and increase its size.
 Additional modifications in the hemoglobin, such as
pyridoxylation, will create a product with near-normal
oxygen-binding affinity.
(Lesley, 2001)
49
(Mohankrishna et al., 2011)50
Stabilization of stroma free Hb
(A,B) Tetrameric stabilization by intramolecular
crosslinking between the two α or ß
(C) The effective molecular weight of Hb can be
increased by conjugating it to polyethylene glycol.
(D) Polymerized Hb may be produced through
polyfunctional crosslinking agents.
E) Hb can also be encapsulated into liposomes
51
Intramolecular cross-linking
 Because the alpha/beta (α-ß) dimers are relatively stable,
the goal of intramolecular modification is to cross-link the
two alpha (α-α) or beta (ß-ß) subunits and stabilize the
association of the two alpha/beta (α-ß) dimers.
 The popular cross-linkers used are 3,5-dibromosalicyl
fumarate (DBBF) and nor-2-formylpyridoxal 5-phosphate
(NFPLP).
(Mohankrishna et al., 2011)
 The cross-linking not only prevents tetramer dissociation,
but also reduces the affinity of Hb for O2.
52
 Addition of 2,3 DPG analogs such as pyridoxal-5’-phospoate can fix the
too high oxygen affinity of stroma-free hemoglobin.
 The more DPG in the cell the more oxygen delivered to the tissue. The
less DPG; the less oxygen delivered to tissues.
 Pridoxylated stroma-free hemoglobin has nearly normal oxygen affinity
(p50 = 22-24 mmHg)
(Jean, 2001)
 E.g., HemopureTM (Hemoglobin Glutamer-250 (bovine) or HBOC
201)
53
Polymerized Hemoglobin
Polymerization of Hb through intermolecular cross-
linking increases the size of molecules through the
formation of Hb oligomers. In the process multiple Hb
proteins are linked together through the use of
dialdehydes, such as glutaraldehyde and glycoaldeyde.
(Betts and Whittet, 1962)
E.g., PolyHemeTM
54
Conjugated Hemoglobin
 Conjugation of Hb is the binding of Hb to a biocompatible
polymer, such as polysaccharide, in order to increase its overall
size.
 In a specific case of pegylation, multiple polyethylene glycol
(PEG) chains are added to the Hb protein as a means to
increasing the molecule's size.
55(Mohankrishna et al., 2011; Shalini, 2012)
56
 Size increases from 3 nm to 15 nm once pegylated
 Hb conjugation with PEG appears to protect the
molecule from renal excretion.
 Conjugating Hb with a macromolecule extends the
intravascular circulation time of a HBOC.
E.g. HemospanTM
(Shalini, 2012)
Hemoglobin Vesicles (Hemoglobin
encapsulated vesicles)
 The encapsulation of Hb is based on the
idea of recreating the natural properties
of RBC without the presence of blood
group antigens
 Encapsulated Hb is often referred to as
―hemosome
The process of involves the encapsulation of Hb within lipid vesicles
using a solution of phospholipids.
 Lipid membrane allow better diffusion of O2 and Co2
57
(Shalini, 2012)
Recombinant Hemoglobin
With advances in recombinant DNA technologies,
specially modified Hb may be produce from
microorganisms, like E. coli
Recombinant human hemoglobin was produced in E.
coli using an expression vector containing two mutant
human globin genes. One was a low oxygen affinity
mutant, and the other fused α-globins.
These recombinant hemoglobin products advanced to
clinical trials, but it was stopped due to
vasoconstriction and other harmful effects.
58
(Mohankrishna et al., 2012)
Table 3. HBOC Products
Name Sponsor
Description
HemopureTM Biopure Corp
It is made of chemically stabilized, cross-linked bovine haemoglobin in a salt
solution. Hemopure is approved for Phase III trials in the United States and
South Africa (Stefan et al., 2007)
OxyglobinTM Biopure Corp
It consists of chemically stabilized bovine haemoglobin in a balanced salt
solution. Oxyglobin is aproved by US FDA and European Commission for
veterinary use particularly for routine use in canine anaemia (Jahr et.al.,2007)
PolyHemeTM Northfield
Laboratories
human hemoglobin-based oxygen- carrying blood but discontinued due to
adverse effects.
HemospanTM Sangart
It was produced in powder form, which could then be mixed into liquid form
and transfused immediately but discontinued due to adverse effects
HemotechTM HemoBiotech
Hemotech is currently approved for Phase I trials.
59
Hemopure and oxyglobin
60
Characteristics Biopure’s Oxygen
Therapeutics
Red Blood Cells
Storage Room temperature (2o to
30o C)
Refrigerated
Shelf life 36 months 42 days
Preparation Ready to use Testing, typing and
crossmatching
Compatibility Universal Type specific
Effectiveness Immediate oxygen delivery Dependent on length of
storage
Purity Processed to remove
infectious agents
Tested and screened for
infectious agents
Raw material Bovine haemoglobin Human Blood
Cost $ 600 - 800 $ 125 - 425
(http://biomed.brown.edu)
61
Table 4. Biopure’s Oxygen Therapeutics vs. RBC’s
Table 5. Current developmental status of HBOCs
Product type Product name Developer Source and /or
technology
Status
Cross-linked Hb HemAssist
TM
Baxter (USA) αα cross-linked
human Hb
Discontinued
Optro (rHb)
TM
Somatogen (USA) Recombinant Hb Discontinued
Polymerized Hb PolyHeme
TM
Northfield Lab
(USA)
Glutaraldehyde,
pyridoxal human
Hb
Discontinued
Hemopure
TM
Biopure (USA) Glutaraldehyde
bovine Hb
Approved *
Conjugated Hb Hemospan
TM
Sangart (USA) Maleimide PEG-
human Hb
Discontinued
PEG-Hb
TM
Enzon (USA) PEG conjugated
bovine Hb
Discontinued
PHP
TM
Apex (USA) Polyoxyethylene-
conjugated human
Hb
Discontinued
* Approved in South Africa for perioperative anemia; approved in USA and Europe
for veterinary use under the name ‘Oxyglobin’.
(Tao and Ghoroghchian, 2014)62
Benefits
of
HBOCs
No prior
planning
Faster &
better O2
distribution
Long shelf
life
No
refrigeration
Universally
compatible
Immediately
offloads
oxygen
Ready to use
(Mohankrishna et al., 2011;
Singh et al., 2012)63
Side effects
of HBOCs
Vasoactivity/
hypertension
Gastrointestinal
side effects
Pancreatic
and liver
enzyme
elevation
Antigenicity
Cardiac
involvement
Platelet
aggregation
Neurotoxicity
Renal effects
(Cole et al., 1997; Mohankrishna et al., 2011;
Singh et al., 2012; Winslow , 2004) 64
Advantages of Artificial blood
No risk of infection
 Biological blood transfusion is the second largest source of
HIV infections in Nigeria. In certain regions of southern
Africa, it is believed that as much as 40% of the population
has HIV/AIDS. A disease-free source of blood
substitutes would be incredibly beneficial in these region
(Shalini, 2012)
Can be kept at room temperature and carry a shelf life of
more than 1 year
Rapid treatment of patients in trauma situations
Medical care in the armed services would get benefit from
artificial blood
65
 Artificial blood allows for immediate full capacity oxygen
transport
(Schimmeyer, 2002)
 An alternative for those patients that refuse blood transfusions
for religious or cultural reasons.
(Jani et al., 2012)
 Synthetic oxygen carriers may also show potential for cancer
treatment, as their reduced size allows them to diffuse more
effectively through poorly vasculated tumour tissue, increasing
the effectiveness of treatments like photodynamic therapy and
chemotherapy.
(Won, 2005)
 Transfused blood is currently more cost effective, but there are
reasons to believe this may change. For example, the cost of
artificial blood may fall as manufacturing becomes refined.
66
Contd…
 There is a possibility of using stem cells as a means of
producing an alternate source of transfusable blood.
 A study performed by Giarratana et al. (2013) describes a large
scale ex-vivo production of mature human blood cells using
hematopoietic stem cells.
 A team of IIT-Madras scientists from the department of
engineering design has been successful in creating enough red
blood cells from stem cells.
(Narayan, 2013)
 To date, the use of red blood cells (RBCs) produced from stem
cells in vitro has not proved for routine transfusion.
(Kim, 2014)
67
Other Promising Technique
Artificial blood controversy
• Doctors abandoned the use of HemAssistTM in the United States,
after patients who received the HBOC died more often than those
who received donated blood.
• Haemoglobin-based blood substitutes may increase the odds of
deaths and heart attacks.
• Sometimes, pharmaceutical companies may get trouble in proving
that their oxygen carriers are effective, i.e. Northfield Laboratories
• Blood substitutes may be misused as performance-enhancing
drugs.
(Shalini, 2012)
68
• Blood supply demand are increasing as compared to blood
donations in the world.
• Artificial blood is especially useful in circumstances when
donor RBC units are unavailable or when transfusion of
real blood is not an acceptable option.
• Two distinctly different classes of oxygen carriers are being
developed, each capable of transporting and delivering
oxygen to peripheral tissues.
• Most of the initial attempts at synthesizing blood
substitutes were not favorable because of significant
adverse effects.
69
Conclusion
 However, Considering the need, there are several
companies still working on the production of a safe and
effective artificial blood substitute.
 Though, there are many challenges in this aspect,
advancing science and technology may result in
development of better blood substitutes in future for
overcoming the need for biological blood transfusions
in the operative and trauma settings.
70
Contd…
Thank you.
71

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Artificial blood seminar

  • 1. A Post-graduate Credit Seminar On ARTIFICIAL BLOOD Speaker: Patel Mehul D. Reg. No. 04–VETMA–01194–2013 Course No. : VPY-691 Major Advisor Dr. A. Lateef Minor Advisor Dr. B.S. Chandel DEPARTMENT OF PHYSIOLOGY AND BIOCHEMISTRY
  • 2. CONTENTS  Introduction  History  Types : i. Perfluorocarbons ii. Hemoglobin-based Products  Advantage of Artificial Blood  Other Promising Technique  Artificial Blood Controversy  Future Scope  Conclusion
  • 4.
  • 5. Blood is circulated in the body through blood vessels by the pumping action of the heart. With lungs, arterial blood carries oxygen from inhaled air to the tissues of the body, and venous blood carries carbon dioxide, a waste product of metabolism produced by cells, from the tissues to the lungs to be exhaled. WHOLE BLOOD RED BLOOD CELLS or Erythrocytes (93%) WHITE BLOOD CELLS or Leucocytes (0.16%) AGRANULOCYTS Lymphocytes- 20-40% of white cells MonocyteS – 1-10% white cells GRANULOCYTES Neutrophils – 50-70% of white cells Eosinophils ~ 3% of white cells Basophils ~ 1% of white cells SOLID FRACTION (Cells-45%) PLATELETS or Thrombocytes (6-7%) FLUID FRACTION (Plasma-55%) 5 What is blood?
  • 6. Blood has many functions :  Transportation  Regulation of Body temperature and pH  Protection against blood loss through clotting  Protection against diseases through phagocytic white blood cells and antibodies 6
  • 7. “Blood is the life” (Riess, 2001) •When a patient looses too much blood due to trauma or surgery, the blood volume and RBCs will be reduced •In such an emergency situation, doctors will often give patients volume expanders to make up for lost blood volume. •This helps to restore normal blood pressure and lets the remaining red blood cells continue to carry oxygen. •If it is not enough, doctors can give patients blood transfusions to replace some of the lost blood. 7 Clinical perspective of blood transfusion?
  • 8. Do animals need blood transfusion?  Animals need blood transfusions for the same reasons that humans do, including surgery, trauma and diseases. (http://k9bloodbank.com) 8 Usually, the need for blood transfusions is acute, as in acute hemorrhage Transfusions are also appropriate in treatment of acute or chronic anemias. Animals with hemostatic disorders often require repeated transfusions (Cotter, 2013)
  • 9. What are blood types? Another protein, an antigen, may be found on some red blood cells - called Rh factor. Blood cells that have Rh factor are RhD positive, those that don't are RhD negative. 9
  • 10. Animals Blood types Dogs DEA 1.1, 1.2, 3, 4, 7, and Dal. (DEA system=Dog Erythrocyte antigen system) DEA 1.1 negative= Universal Donor DEA 1.1 positive=Universal Recipient (Wardrop, 2007) Cats The main blood group system in cats is the A-B grouping. Cats can be either type A, type B or type AB. (http://www.catblooddonors.com/for-cat-owners/about-cat-blood- transfusions.php) Cattle The polymorphic systems in cattle include the A, B, C, F, J, L, M, S, and Z polymorphisms. (http://en.wikipedia.org/wiki/Blood_type_non-human) Horses There are eight major recognized blood groups in horses Viz., A, C, D, K, P, Q, U and T. ( http://en.wikipedia.org/wiki/Blood_type_non-human) Blood types in animals
  • 11.  When transfusion is required, cross matching should be performed or a universal donor may be used. Cross-match should be performed in the following situations: 1) Naturally occurring antibodies to foreign blood group antigens. This occurs in the cat. In this species, a cross-match should be performed on the first and every transfusion  Type A cats should receive only type A blood and type B cats should receive only type B blood. However type AB cats can receive either Type A or Type B blood with minimal or no clinical reactions (Henset, 2011) 11
  • 12. 2) Sensitization of an animal to foreign red cell antigens, in a species without naturally occurring antibodies. This is the situation in the dog and horse, resulting in the production of acquired antibodies. In these species, a cross-match does not need to be performed on the first transfusion the animal receives but should be performed at subsequent transfusions.  Also in cow, buffalo, sheep, goat and pig, a single, unmatched whole blood transfusions are generally safe (Weiss and Wardrop, 2010) 12
  • 13. 13 Blood collection : The donor cow restrained in a head bail and given a small injection of sedation if needed. Blood collection takes around 20-30 minutes. Blood transfusion : The recipient cow restrained by halter (and in a head bail if possible). Blood transfusion takes around 20 minutes. http://www.franklinvets.co.nz/Dairy++BeefSheep/Farm+Services/Animal+Health/theileria.html
  • 14. Blood transfusions can be critical, life-saving procedures. Blood needs to be readily available—and that requires a blood bank. Do animas have blood bank ? 14
  • 15. India's 1st government blood bank for dogs started in Chennai by the Tamil Nadu Veterinary and Animal Sciences University (TANUVAS) in 2010. (http://timesofindia.indiatimes.com/india/Indias-1st-blood-bank-for-dogs- opens-in-TN/articleshow/5861905.cms) 15  Even in veterinary field, there are several blood banks which store animal blood for future transfusion. Animal Blood Bank
  • 16. 16 Volunteer donor dog during a donation: The dog lies comfortably on his side and a needle is placed in his jugular vein to extract the blood. The procedure takes about 15 to 20 minutes in most dogs.
  • 17. Drawbacks: According to Riess (2001) blood transfusion carries and will always carry a certain level of risk. Blood has to be kept cool (4° C ), and it has a shelf life of 42 days (Lockwood et al.,2003)  Prolonged RBC storage before transfusion increases multiorgan failure and mortality in patients (Eldad et al., 2010)  The effects of prolonged storage on red cells include decreased deformability; depletion of 2,3-diphosphoglycerate (2,3-DPG); increased adhesiveness and aggregability; reduction in the concentrations of nitric oxide and adenosine triphosphate etc (Koch et al., 2008) 17
  • 18.  Blood supply shortages : – A country needs a minimum stock of blood equal to 1 per cent of its population. – The total recorded blood collection in India is 4 million units, which meet only 40% of need against a least requirement of 10 million units. (World Health Organization, 2008)  Safety of blood supply and risk of infections – Risk of transmission of HIV, Hep B, Hep C, and other blood borne diseases – Mistransfusions due to error – Blood Group matching required. (Scott et al., 1997)  Cost – Donations, screening, storage, and administration ~ 800-1200 Rs. (Maiti, 2012) 18
  • 19. The term “artificial blood” is really a misnomer. The complexity of blood is far too great to allow for absolute duplication in a laboratory. (Kresie, 2001) Artificial blood is a product made to act as a substitute for blood for the transportation of oxygen throughout the body. (Shalini, 2012) It is also called as Blood Substitute or Arificial Oxygen Carrier. 19 This is where artificial blood comes in
  • 20. The most promising artificial blood products are 1. Perflourocarbons (PFCs) and 2. Haemoglobin based oxygen carriers (HBOCs). (Mohankrishna et al., 2011) The delivery of oxygen by oxygen carriers of the these two classes of have both benefits and risks which are unique to their class. (Tremper et al., 1980) 20
  • 22. In 1616, when William Harvey first described the circulation of blood In 1665, the first recorded successful blood transfusion on dog by Richard Lower 22 (http:// www.redcrossblood.org) History
  • 23. Many materials used for transfusion that include beer, urine, milk, plant resins, and sheep blood. In 1854, patients were injected with milk to treat Asiatic cholera. Other materials that were tried during the 1800s include hemoglobin and animal plasma. (Chang, 2004) In 1883,there was a creation of Ringer's solution. In research using part of a frog's heart, Sydney Ringer, found that the heart could be kept beating by applying the solution. (Hoffman et al., 1990) 23 Contd...
  • 24. In 1909, Karl Landsteiner classified human blood into four different groups: A, B, AB, and O. A fourth group AB was discovered the following year. (Squires, 2002) Karl Landsteiner 24 Contd...
  • 25.  During World War I, galactoso- gluconic acid was used to extend plasma.  World War II, human plasma was used to replace blood and to save soldiers from hemorrhagic shock.  Eventually, this led to the establishment of blood banks by the American Red Cross in 1947. (Kirschman and Ruth , 2005) 25 Contd...
  • 26.  In 1966, experiments with mice suggested a new type of blood substitute, perfluorocarbons (PFCs).  In 1968, the rat's blood replaced with a PFC emulsion and it lived for a few hours and recovered fully after blood was replaced. (Sarkar, 2008)  However, the established blood bank system in developed countries worked so well that research on blood substitutes waned in those countries. It received renewed interest when the shortcomings of the blood bank system were discovered during the Vietnam conflict. This prompted some researchers to begin looking for hemoglobin solutions (Jani et al., 2012) 26 Contd...
  • 27. Ideal Artificial Blood  Increased availability that would rival that of donated blood, even surpass it  Oxygen carrying capacity, equaling or surpassing that of biological blood  Volume expansion  Universal compatibility: elimination of cross matching  Pathogen free: elimination of blood contained infections  Minimal side effects  Survivability over a wider range of storage temperatures  Long shelf life  Cost efficient (Squires, 2002) 27
  • 28. Types of Blood Substitutes 1) Perfluorocarbons (PFCs), chemical compounds which can carry and release oxygen 2) Haemoglobin-based oxygen carriers (HBOCs) derived from humans, animals, or artificially via recombinant technology 28(Jani et al.,2012)
  • 30. Perfluorocarbons (PFCs) Perfluorocarbons are low-molecular-weight linear or cyclic hydrocarbons in which hydrogen atoms of the carbon chain have been substituted by fluorine atom, leading to total chemical inertness and a complete lack of metabolism in vivo. (Jahr et al., 2007) 1st Generation Fluosol-DATM 2nd Generation OxyfluorTM OxygentTM 30 3rd Generation PerftoranTM PHER-O2 TM
  • 32. The PFC particles are about 0.2 microns in diameter (1/40th of RBC size), with a perfluorocarbon core and a thin lecithin phospholipids as a coating (Mohankrishna et al., 2011)  The perfluorocarbons are not hydrosoluble and administered as emulsions called perfluorocarbon emulsions (PFCEs) (Squires, 2002) 32
  • 33.  Perfluorocarbons do not have the oxygen-bonding properties but act as simple solvents.  The transport and liberation of gases based on their physical solubility, and the quantity of gas dissolved linearly related to its partial pressure. (Jahr et al., 2007)  They Can dissolve more oxygen than the biological blood. (Cabrales and Intaglietta, 2013)  They carry much less oxygen than hemoglobin-based products (Jani et al., 2012) 33 Physiology of carrying oxygen
  • 34. Structure of PFC 34(Tao and Ghoroghchian, 2014)
  • 35. Ingredients Quantity (%) Perfluoro-octyl bromide 28 FO-9982 12 Yolk lecithin 2.4 DSPE-50 H 0.12 Distilled water 57.48 Table 1. Composition of PFC based blood substitute (Mitsuhiro et al., 2005) 35 Where, DSPE= Distearoyl phosphatidyl ethanolamine (ammonium salt) FO =Perfluoroalcohol esters with oleic acid
  • 36.  The first generation of PFCEs developed was Fluosol-DATM in 1989.  Fluosol-DATM was approved by US FDA in human, but withdrawn later because of marginal benefits and development of flu-like symptoms (Castro and Briceno, 2010)  The second generation of PFCEs developed were OxyfluorTM and OxygentTM, with improved lipophilicity (Modery et al., 2013) 36 Developments in PFCEs
  • 37.  However, OxyfluorTM was terminated after early clinical trials due to its severe side effects  OxygentTM was also terminated, because of an increased incidence of stroke in coronary bypass patients The third generation PFCEs are PerftoranTM and PHER-O2 TM Pulmonary complications has been reported with the use of PerftoranTM and, PHER-O2 TM is in reasearch (Modery et al., 2013) 37 Contd…
  • 38. Table 2. Current status of PFC based products Name Sponsor Status OxygentTM Alliance pharmaceuticals (USA) Discontinued OxycyteTM Oxygen biotherapeutics (USA) Discontinued PHER-O 2TM Sanguine Corp (USA) In research PerftoranTM PERFTORAN (Russia) Approved in Russian clinical application. 38
  • 39.  Cheap and easy to manufacture in large quantities  Can be stored at room temperature for more than 1 year  Can be mixed safely with any blood group without the need to check first  The molecules are smaller than red blood cells, allowing them to bypass arterial blockages and penetrate small capillaries with ease, delivering oxygen to areas which need it most  Effect of chemotherapy or radiation in tumour treatment can be enhance when patient pretreated with PFCs (Jani et al., 2012; Singh et al.,2012) Benefits of Perfluorocarbon based products 39
  • 40. Adverse Effects Of PFC Allergy Especially 1st Gen Repeated doses may cause hepatic engorgement Retained in RE system Decrease platelet count Impaired neutrophil function •Early: Headache •Late: Flu like symptoms (Dietz et al., 1996; Jahr et al., 2007; ) 40
  • 42. Understanding Hemoglobin (Hb) :  The structure of Hb was determined in 1959 by Max Perutz.  Molecular weight 64.5 kDa  Tetrameric protein comprised of two α and two ß- globin subunits that fold into compact quaternary structure (α 2 ß 2).  Each α and ß subunit contain an iron-heme group that binds to oxygen molecule allowing for transport. 42
  • 43. 43
  • 44.  A Hb molecule carries a maximum of four oxygen molecules.  Various factors such as low pH and high CO2 and high 2,3-diphosphoglycerate (DPG) level in the tissues, cause a lower oxygen affinity state facilitating oxygen offloading.  As oxygen is being unloaded, CO2 binds to Hb, resulting in carbamino-Hb. 44 Contd…
  • 45.  Local conditions in the lungs including higher O2, higher pH, and lower 2,3 DPG level, cause Hb to shift back to the higher oxygen affinity state.  Such a transition favors CO2 release, which is then exhaled. 45 Contd…
  • 46. HBOCs In search for an alternative to PFCs, considerable efforts have been made in the development of acellular Hb based oxygen carriers… 46
  • 47.  To prepare acellular Hb, Hb is derived from human or bovine blood by chemical modifications or from bacteria host systems by genetic recombinantion (Alayash, 2014)  Human hemoglobin is obtained from donated blood that has reached its expiration date  One unit of hemoglobin solution can be produced for every 2 units of discarded blood (Lesley, 2001) 47 HBOCs (Hemoglobin-based oxygen carriers) Once obtained from any of these sources, the hemoglobin must be purified and modified to decrease its toxicity and increase its effectiveness
  • 48. • The first clinical study with free hemoglobin resulted in nephrotoxicites. The hemoglobin used was found to have erythrocyte membrane stromal lipids as well as bacterial endotoxins. (Shalini, 2012) • To side-step these problems, stroma-free hemoglobin was developed, but new problems arose, o 1) too short intravascular half life o 2) too high affinity for oxygen (Jean, 2001) 48
  • 49. 1) Stroma free Hb had too short of an intravascular half life because tetrameric Hb (α 2 ß 2) dissociated into αß dimmers that were filtered by the kidneys and excreted in the urine. 2) Stroma free Hb had too high of an oxygen affinity because 2,3-DPG was lost during the purification process. (Shalini, 2012)  To increase the intravenous half life of hemoglobin solutions, manufacturers had to develop methods to stabilize the hemoglobin tetrameric structure and increase its size.  Additional modifications in the hemoglobin, such as pyridoxylation, will create a product with near-normal oxygen-binding affinity. (Lesley, 2001) 49
  • 50. (Mohankrishna et al., 2011)50 Stabilization of stroma free Hb
  • 51. (A,B) Tetrameric stabilization by intramolecular crosslinking between the two α or ß (C) The effective molecular weight of Hb can be increased by conjugating it to polyethylene glycol. (D) Polymerized Hb may be produced through polyfunctional crosslinking agents. E) Hb can also be encapsulated into liposomes 51
  • 52. Intramolecular cross-linking  Because the alpha/beta (α-ß) dimers are relatively stable, the goal of intramolecular modification is to cross-link the two alpha (α-α) or beta (ß-ß) subunits and stabilize the association of the two alpha/beta (α-ß) dimers.  The popular cross-linkers used are 3,5-dibromosalicyl fumarate (DBBF) and nor-2-formylpyridoxal 5-phosphate (NFPLP). (Mohankrishna et al., 2011)  The cross-linking not only prevents tetramer dissociation, but also reduces the affinity of Hb for O2. 52
  • 53.  Addition of 2,3 DPG analogs such as pyridoxal-5’-phospoate can fix the too high oxygen affinity of stroma-free hemoglobin.  The more DPG in the cell the more oxygen delivered to the tissue. The less DPG; the less oxygen delivered to tissues.  Pridoxylated stroma-free hemoglobin has nearly normal oxygen affinity (p50 = 22-24 mmHg) (Jean, 2001)  E.g., HemopureTM (Hemoglobin Glutamer-250 (bovine) or HBOC 201) 53
  • 54. Polymerized Hemoglobin Polymerization of Hb through intermolecular cross- linking increases the size of molecules through the formation of Hb oligomers. In the process multiple Hb proteins are linked together through the use of dialdehydes, such as glutaraldehyde and glycoaldeyde. (Betts and Whittet, 1962) E.g., PolyHemeTM 54
  • 55. Conjugated Hemoglobin  Conjugation of Hb is the binding of Hb to a biocompatible polymer, such as polysaccharide, in order to increase its overall size.  In a specific case of pegylation, multiple polyethylene glycol (PEG) chains are added to the Hb protein as a means to increasing the molecule's size. 55(Mohankrishna et al., 2011; Shalini, 2012)
  • 56. 56  Size increases from 3 nm to 15 nm once pegylated  Hb conjugation with PEG appears to protect the molecule from renal excretion.  Conjugating Hb with a macromolecule extends the intravascular circulation time of a HBOC. E.g. HemospanTM (Shalini, 2012)
  • 57. Hemoglobin Vesicles (Hemoglobin encapsulated vesicles)  The encapsulation of Hb is based on the idea of recreating the natural properties of RBC without the presence of blood group antigens  Encapsulated Hb is often referred to as ―hemosome The process of involves the encapsulation of Hb within lipid vesicles using a solution of phospholipids.  Lipid membrane allow better diffusion of O2 and Co2 57 (Shalini, 2012)
  • 58. Recombinant Hemoglobin With advances in recombinant DNA technologies, specially modified Hb may be produce from microorganisms, like E. coli Recombinant human hemoglobin was produced in E. coli using an expression vector containing two mutant human globin genes. One was a low oxygen affinity mutant, and the other fused α-globins. These recombinant hemoglobin products advanced to clinical trials, but it was stopped due to vasoconstriction and other harmful effects. 58 (Mohankrishna et al., 2012)
  • 59. Table 3. HBOC Products Name Sponsor Description HemopureTM Biopure Corp It is made of chemically stabilized, cross-linked bovine haemoglobin in a salt solution. Hemopure is approved for Phase III trials in the United States and South Africa (Stefan et al., 2007) OxyglobinTM Biopure Corp It consists of chemically stabilized bovine haemoglobin in a balanced salt solution. Oxyglobin is aproved by US FDA and European Commission for veterinary use particularly for routine use in canine anaemia (Jahr et.al.,2007) PolyHemeTM Northfield Laboratories human hemoglobin-based oxygen- carrying blood but discontinued due to adverse effects. HemospanTM Sangart It was produced in powder form, which could then be mixed into liquid form and transfused immediately but discontinued due to adverse effects HemotechTM HemoBiotech Hemotech is currently approved for Phase I trials. 59
  • 61. Characteristics Biopure’s Oxygen Therapeutics Red Blood Cells Storage Room temperature (2o to 30o C) Refrigerated Shelf life 36 months 42 days Preparation Ready to use Testing, typing and crossmatching Compatibility Universal Type specific Effectiveness Immediate oxygen delivery Dependent on length of storage Purity Processed to remove infectious agents Tested and screened for infectious agents Raw material Bovine haemoglobin Human Blood Cost $ 600 - 800 $ 125 - 425 (http://biomed.brown.edu) 61 Table 4. Biopure’s Oxygen Therapeutics vs. RBC’s
  • 62. Table 5. Current developmental status of HBOCs Product type Product name Developer Source and /or technology Status Cross-linked Hb HemAssist TM Baxter (USA) αα cross-linked human Hb Discontinued Optro (rHb) TM Somatogen (USA) Recombinant Hb Discontinued Polymerized Hb PolyHeme TM Northfield Lab (USA) Glutaraldehyde, pyridoxal human Hb Discontinued Hemopure TM Biopure (USA) Glutaraldehyde bovine Hb Approved * Conjugated Hb Hemospan TM Sangart (USA) Maleimide PEG- human Hb Discontinued PEG-Hb TM Enzon (USA) PEG conjugated bovine Hb Discontinued PHP TM Apex (USA) Polyoxyethylene- conjugated human Hb Discontinued * Approved in South Africa for perioperative anemia; approved in USA and Europe for veterinary use under the name ‘Oxyglobin’. (Tao and Ghoroghchian, 2014)62
  • 63. Benefits of HBOCs No prior planning Faster & better O2 distribution Long shelf life No refrigeration Universally compatible Immediately offloads oxygen Ready to use (Mohankrishna et al., 2011; Singh et al., 2012)63
  • 64. Side effects of HBOCs Vasoactivity/ hypertension Gastrointestinal side effects Pancreatic and liver enzyme elevation Antigenicity Cardiac involvement Platelet aggregation Neurotoxicity Renal effects (Cole et al., 1997; Mohankrishna et al., 2011; Singh et al., 2012; Winslow , 2004) 64
  • 65. Advantages of Artificial blood No risk of infection  Biological blood transfusion is the second largest source of HIV infections in Nigeria. In certain regions of southern Africa, it is believed that as much as 40% of the population has HIV/AIDS. A disease-free source of blood substitutes would be incredibly beneficial in these region (Shalini, 2012) Can be kept at room temperature and carry a shelf life of more than 1 year Rapid treatment of patients in trauma situations Medical care in the armed services would get benefit from artificial blood 65
  • 66.  Artificial blood allows for immediate full capacity oxygen transport (Schimmeyer, 2002)  An alternative for those patients that refuse blood transfusions for religious or cultural reasons. (Jani et al., 2012)  Synthetic oxygen carriers may also show potential for cancer treatment, as their reduced size allows them to diffuse more effectively through poorly vasculated tumour tissue, increasing the effectiveness of treatments like photodynamic therapy and chemotherapy. (Won, 2005)  Transfused blood is currently more cost effective, but there are reasons to believe this may change. For example, the cost of artificial blood may fall as manufacturing becomes refined. 66 Contd…
  • 67.  There is a possibility of using stem cells as a means of producing an alternate source of transfusable blood.  A study performed by Giarratana et al. (2013) describes a large scale ex-vivo production of mature human blood cells using hematopoietic stem cells.  A team of IIT-Madras scientists from the department of engineering design has been successful in creating enough red blood cells from stem cells. (Narayan, 2013)  To date, the use of red blood cells (RBCs) produced from stem cells in vitro has not proved for routine transfusion. (Kim, 2014) 67 Other Promising Technique
  • 68. Artificial blood controversy • Doctors abandoned the use of HemAssistTM in the United States, after patients who received the HBOC died more often than those who received donated blood. • Haemoglobin-based blood substitutes may increase the odds of deaths and heart attacks. • Sometimes, pharmaceutical companies may get trouble in proving that their oxygen carriers are effective, i.e. Northfield Laboratories • Blood substitutes may be misused as performance-enhancing drugs. (Shalini, 2012) 68
  • 69. • Blood supply demand are increasing as compared to blood donations in the world. • Artificial blood is especially useful in circumstances when donor RBC units are unavailable or when transfusion of real blood is not an acceptable option. • Two distinctly different classes of oxygen carriers are being developed, each capable of transporting and delivering oxygen to peripheral tissues. • Most of the initial attempts at synthesizing blood substitutes were not favorable because of significant adverse effects. 69 Conclusion
  • 70.  However, Considering the need, there are several companies still working on the production of a safe and effective artificial blood substitute.  Though, there are many challenges in this aspect, advancing science and technology may result in development of better blood substitutes in future for overcoming the need for biological blood transfusions in the operative and trauma settings. 70 Contd…

Editor's Notes

  1. Perfluorocarbons are low-molecular-weight linear or cyclic hydrocarbons in which hydrogen atoms of the carbon chain have been substituted by fluoride, leading to total chemical inertness and a complete lack of metabolism in vivo. They have a high solubility coefficient for oxygen, higher than the coefficient for oxygen dissolved in plasma oxygen