chapter 5 5.1 introduction - waseda universityfig. 5.3 diagram of a portion from a gill arch of a...

Chapter 5

5.1 Introduction

A fish can exchange gases effectively by the indirect contact of blood with

water in its gills. The excellent mechanism of fish gill has been studied in the

fields of biology, marine zoology, and chemical engineering. Elucidation of the

mechanism of a fish gill provides a hint on further improvement of artificial gill.

Yamamoto et al. [1] and Schumann and Piiper [2,3] observed the change in

oxygen consumption with varying the activity level of fish. Matsuda and Sakai

have evaluated the oxygen transfer rate of fish gills by computer simulation

analysis [4,5]. They demonstrate that the biological membrane is the

rate-determining for oxygen transfer through the secondary lamellae. This is

because the blood and water channels are very narrow, and these narrow

channels reduce gas transfer resistances in blood and water. They also suggested

that the optimal gas exchange module for membrane type artificial gill from the

analysis results of computer simulation.

On the other hand, the rate-determining step in artificial gill is located in the

oxygen uptake device as shown in chapters 3 and 4. Thus, the oxygen uptake

should be enhanced in order to improve the artificial gill. In the artificial gill,

oxygen is taken up from water to the oxygen carrier solution through a

gas-permeable membrane in the artificial gill, in the same way that oxygen is

taken up from water to blood through a biological membrane in a biological gill.

Elucidation of the oxygen uptake mechanisms of the biological gill would

provides a hint on further improvement of oxygen uptake in the artificial gill.

In this chapter, the oxygen transfer performance of the artificial gill were

evaluated together with that of the biological gill in terms of oxygen flux,

Reynolds number of water, oxygen partial pressure difference between water

131

Oxygen uptake efficiency of biological and artificial gills and blood (or oxygen carrier solution), and oxygen uptake efficiency.

Advantageous for oxygen uptake in biological gill were found, and the

guidelines for the further improvement of artificial gills was presented.

132

Chapter 5

5.1.1 Previous studies on fish gill

Gill consists of gill arch functioning as a pillar, gill filaments standing on

the gill arch like a shelf and secondary lamellae projecting numerously from the

gill filaments. Inspired water from mouth is made to flow among the secondary

lamellae and gill filaments. Blood channels are located in the secondary lamella,

and they are separated from water by secondary lamella membrane composed of

epithelium, basement membrane and pillar cell. Blood and water flow

counter-currently, and gas exchange occurs. A lot of morphological information

of fish gill has been obtained by many investigators up to now, and oxygen

transfer mechanism of fish gill has been clarified by several researchers.

Especially, the secondary lamella model established by Matsuda and Sakai,

provides valuable information for designing more efficient artificial gill [4,5].

133

Oxygen uptake efficiency of biological and artificial gills

5.1.1.1 Morphology of fish gill and water ventilation system Teleosts have five pairs of gill arches and many gill filaments standing on

the front four-gill arches like a shelf. The ends of gill filaments are located in the

opercular cavity. The outside of the opercular cavity is covered with an

open-and-shut operculum and opened to the exterior through a gill opening

(Fig .5.1). The end of gill filaments is contacted closely to the next gill filament,

which produces high resistance to water flow. Hence, inspired water from mouth

is made to flow through a channel between two gill filaments which has lower

resistance to water flow, and effused to the opercular cavity [6-10] (Fig. 5.2).

Numerous secondary lamellae are projected from both sides of the gill filaments

at the right angle to them. Very narrow blood channels are located in the

secondary lamella where only one blood cell can pass through (Fig. 5.3). The

blood channels are separated from water by secondary lamella membrane

composed of epithelium, basement membrane and pillar cell [10-16] (Fig. 5.4,

Fig. 5.5). Blood is introduced to secondary lamella blood channel from afferent

arch artery through afferent filamental artery. Blood and water flow

counter-currently, and gas exchange occurs [10-12] (Fig. 5.6, Fig.5.7). Large

partial pressure difference between water and blood caused by the

counter-current produces the effect ive gas exchange [2,17-18].

134

Chapter 5

Fig. 5.1 Diagram showing, in horizontal section,the position of the gill arches and gill filamentsand water flow: (A) Buccal cavity, (B) Buccalcavity, (C) Gill arch, (D) Piles of gill filaments,(E) Opercular cavity, (F) Operculum

Fig. 5.3 Diagram of a portion from a gill awater and blood flow are indicated by dashed

135

Fig. 5.2 Schematic diagram of piles of gillfilaments standing on two gill arches [11,19]; The end of gill filament is contacted closely tothe next gill filament. Water flow between slitsof two gill filaments

rch of a teleost fish [20]: direction of and full allows, respectively


Fig. 5.4 Cross-sectional view of secondary lamellae: A: cross-section of several blood channels, B: enlargement of blood channel, R: erythrocyte, P: Pillar cell, E: epithelium, N: nucleus [20]

Fig. 5.5 Electromicrograph of a secondary lamella blood channel of carp (Cyprinus carpio) [19,20]: E: epithelium, P: pillar cell, R: erythrocyte

Fig. 5.7 Flow of water and blood in an elasmobranch fish: As in teleost fish, the flow of blood is in the opposite direction to that of the water [20].

Fig. 5.6 Scanning electron micrograph of a plastic cast of a trout gill filament, showing several lamellae: Magnification 160x [20]

136

Chapter 5

5.1.1.2 Gill surface area Gill surface area per fish body weight is different for fish species. Higher

values are obtained for fast and active wandering fish and lower values for

elasmobranchs, freshwater fish or inactive fish [16,21]. The gill surface area is

depended on fish body weight of the same kind, and the relationship between

gill surface area A (mm2) and body weight W (g) is represented by the following

equation [9-10]. Parameters a and m are shown in Table 5.1 for several fish

species [10].

maWA = (5.1)

The gill surface area is strongly dependent on the number of gill filaments and

secondary lamella density.

Table 5.1 Parameters a and m in equation (5.1) representing the relationship between gill surface area and fisg body weight

137


5.1.1.3 Property of fish blood Fish blood consists of blood cells and plasma similar to other vertebrate

animals, and the blood cells are composed of erythrocytes, leukocytes and

thrombocytes. Erythrocyte is a round or ellipse shaped cell and contains dense

hemoglobin. Molecular weight of fish hemoglobin is ranged from 60,000 to

70,000, which are similar to mammalian hemoglobin. There are some kinds of

hemoglobin in a fish species, which are divided into several components by

electrophoresis. Therefore, oxygen binding affinity and effect of carbon dioxide

are different for each kinds of hemoglobin [22]. The size of erythrocyte for

active fish is smaller (major axis: 7.2-14 mm, minor axis: 6.6-10 mm) than

inactive fish (9.4-16 mm and 6.9-11 mm).The number of erythrocytes is 3.0-3.9

million /mm3 for active fish and 1.4-3.0 million /mm3 for inactive fish.

One gram of fish hemoglobin combines with 1.48 cm3 (STP) of oxygen.

The concentrations of hemoglobin for carp (Cyprinus carpio) and dogfish

(Scyliorhinus stellais) are 81 mg/cm3 and 36 mg/cm3, respectively [22]. Fig. 5.8

shows the oxyhemoglobin dissociation curve of carp blood [22], and Table 5.3

shows the half saturation p50 (mmHg) (the oxygen partial pressure when degree

of oxygen saturation of hemoglobin is 0.5). The half saturation p50 for fish blood

is ranged from 5 to 20 mmHg [22], which is lower than that of human beings

(26 mmHg) [23].

138

Chapter 5

Fig. 5.8 Oxyhemoglobin dissociation curves of carp blood [22]

Table 5.2 Half saturation of hemoglobin for fish blood [4]

p50 Oxygen cap. Temperature Fish species (mmHg) (vol%) (K) Ameiurus nebulosus 1.4 13.3 288 Cyprinus carpio 5 12.5 288 Scyliorhinus stellais 15.8 5.3 290 Amia calva 4.0 11.8 288 Salmo gairdnerii 18 13.8 288 Salvelinus fontinalis 13 11.7 288 Scomber scombrus 16 15.8 293 Human being (male) 26 19.8 310

139


5.1.4 Oxygen consumption of fish Several researchers revealed that oxygen consumption rate of fish varies

with the activity level of them [1,24,25]. Yamamoto et al. measured the oxygen

consumption rate of a Carp with various ventilation rates by the respire-chamber

method as shown Fig.5.9. The results of this study provided a lot of valuable

information. Actually, Matsuda and Sakai used the experimental results to

establish the secondary lamella model [4,5]. In this chapter, the oxygen

consumption rate that was measured Yamamoto et al., was also used to

evaluation of oxygen uptake performance of the present artificial gill.

Fig. 5.9 Schematic of apparatus used Yamamoto et al. for measuring oxygen consumption rate of carp [1]

140

Chapter 5

5.2 Experimental and Theoretical section

5.2.1 Oxygen uptake of biological and artificial gills

Fish take up oxygen from water into their blood through a secondary

lamella of the gill. The secondary lamella acts as a gas-permeable membrane.

The oxygen transfer from water to blood depends on water and blood flow

velocity and the oxygen permeability of the secondary lamella. The water flows

opposite to the direction of the blood flow in the fish gill [26]. The blood flow

into the secondary lamella decreases and blood is not supplied to all of the

secondary lamella while the fish is inactive [1]. Matsuda and Sakai [4,5] have

reported a secondary lamella model based on these flow condition. Fig. 5.10

shows the secondary lamella model of a carp gill proposed by Matsuda and

Sakai, and technical data for the carp gill are shown in Table 5.3. Matsuda and

Sakai [4,5] have found that the effective gas exchange area of the membrane

surface depends on the oxygen consumption rate of the carp. Yamamoto et al.

[1] measured the oxygen consumption rate of the carp using the respiro-chamber

method. These data are used for estimation of the oxygen flux of a biological

gill.

141


Distance betweenDistance betweenSecondary lamellTotal cross sectioBody weight (kg)

In this chapter, the o

concentrated hemoglobin

with that of a biological g

Fig. 5.11 shows a sch

hemoglobin solution as t

operating conditions of th

oxygen carrier solution an

This artificial gill con

water to the oxygen carri

Fig. 5.10 Schematic of secondary lamella model proposed by Matsuda and Sakai [4,5]

Table 5.3 Details on carp gill [5]

filaments (µm) 385 secondary lamella (µm) 48 a surface area (m2) 0.0823 nal area of water channel (mm2) 1970 0.319

xygen uptake performance of an artificial gill using a

solution, which is designed in chapter 3, compared

ill.

ematic of the artificial gill system using a concentrated

he oxygen carrier solution. Table 5.4 summarizes the

e artificial gill. Table 5.5 shows technical data on the

d the hollow fiber module.

sists of two devices: one is oxygen uptake device from

er solution, and the other is an oxygen release device

142

Chapter 5

from the oxygen carrier solution to air. In the oxygen uptake device, the oxygen

carrier solution is cooled to 293 K, which is approximately the same temperature

as seawater, to increase the oxygen affinity of the oxygen carrier solution and to

enhance oxygen uptake from the water to the oxygen carrier solution. In contrast,

in the oxygen release device, the oxygen carrier solution is heated to 310 K to

decrease the oxygen affinity of the oxygen carrier solution and thereby enhance

oxygen release from the oxygen carrier solution to the air. In this system, the

rate-determining step of oxygen transfer is in the oxygen uptake device which is

similar to a biological gill in oxygen uptake. Oxygen is taken up from water to

the oxygen carrier solution through a gas-permeable membrane in the artificial

gill in the same way that oxygen is taken up from water to blood through a

biological membrane in a biological gill. Elucidation of the oxygen uptake

mechanisms of the biological gill will enable the improvement of oxygen uptake

in the artificial gill.

143


Fig. 5.11 Artificial gill system using concentratedhemoglobin solution as the oxygen carrier

Condition

Flow rate (cm3/s) Seawater Oxygen carrier solutionExpired

Inlet oxygen partial pressure in oxygen carrier solution (kPa)

In oxygen uptake In oxygen release

Oxygen partial pressuresea water (kPa)

Module inlet Module outlet

Total membrane surfarea (kPa) *Condition C is same op

Table 5.4 Operating conditions for artificial gill

A (Minimum water

flow rate)

B (Intermediate)

C* (Minimum

membrane surface area)

2330 4200 6530 233 233 233

93.3 93.3 93.3

9.33 9.66 9.48 22.7 22.7 22.7

of

20.0 20.0 20.0 13.0 16.1 17.8

ace 156 94.6 63.8

erating condition in chapter 3.

144

Chapter 5

5.

bo

ar

fo

w

ox

ox

se

w

se

w

Table 5.5 Technical data on oxygen carrier solution and hollow fiber module Oxygen carrier solution

Hemoglobin concentration (mol/m3) 5.43 pH 6.9 Ratio of IHP to hemoglobin (mol:mol) 5:1

Hollow-fiber module Outside diameter of hollow fiber (µm) 380 Porosity of membrane packing 0.490 Membrane material Porous polypropylene

2.2 Oxygen flux of biological and artificial gills

Humans require larger amounts of oxygen than fish because of their larger

dy volume. The artificial gill, therefore, requires a larger membrane surface

ea and larger water flow rate than a biological gill to supply enough oxygen

r human respiration. The unit of water flow rate per gas exchange surface area

as used to evaluate the gills on similar scale, and oxygen flux, defined as

ygen transfer rate per gas exchange surface area, was used as the parameter of

ygen uptake. In the biological gill, the ventilation rate (water flow rate) per

condary lamella surface area W (m3 s-1 m-2) is defined as follows:

G

w

eAQW = (5.2)

here QW is the ventilation rate (m3/s) and eAg the effective surface area of the

condary lamella (m2). In the artificial gill, the water flow rate making contact

ith the hollow-fiber membranes is represented by

145


M

w

AQW = (5.3)

where AM is the membrane surface area of the hollow fibers (m2). Oxygen flux J

(mol s-1 m-2) is defined as follows:

G

2O

eANJ = (5.4)

M

2O

ANJ = (5.5)

where NO2 (mol/s) is the oxygen transfer rate.

5.2.3 Water flow rates of biological and artificial gills

Water flow velocity in the vicinity of the secondary lamella and hollow

fibers affects the oxygen flux because the mass transfer resistance of water

comprises a large part of the overall resistance of oxygen transfer [27]

The water flow path between secondary lamellae is rectangular in shape, as

shown in Fig .5.10. The equivalent diameter de (m) in the biological gill is

obtained by

y2x2xy4de +

= (5.6)

where x is the distance between filaments (m) and y the distance between

secondary lamellae (m). Reynolds number Re is obtained by

146

Chapter 5

νudRe e= (5.7)

where u is the mean linear velocity of water (m/s) and ν the kinematic viscosity of water (m2/s).

In the hollow-fiber module of an artificial gill device, the packed

hollow-fiber membranes form an intricate water flow path. Many researchers

studying mass transfer in hollow-fiber membrane modules take the hollow-fiber

module to be a packed column [26-30] The hydraulic radius rh (m) of the

hollow-fiber module is obtained by [31]

)P1(4Pdrh −

= (5.8)

where P is the porosity of membrane packing and d is the diameter of the hollow

fibers (m). The mean linear velocity of water u (m/s) is obtained by

PSQu w= (5.9)

where S is the cross-sectional area of a flow path (m2). The Reynolds number is

obtained by the following equation:

νν S)P1(dQur4Re wh

−== (5.10)

147


5.2.4 Oxygen uptake of biological and artificial gills

The amount of oxygen in water is much smaller than that in air. Higher

water flow rates are required to breathe in water with the biological and artificial

gills. Effective use of dissolved oxygen in water leads to lower water flow rates

and higher device efficiency. Oxygen uptake efficiency, which is the ratio of

oxygen uptake to dissolved oxygen in water U is obtained by

Win

WoutWin

pppU −

= (5.11)

where pWin and pWout are the oxygen partial pressures in water (Pa) at the module

inlet and outlet, respectively.

148

Chapter 5

5.3 Results and discussion

5.3.1 Oxygen uptake efficiency of biological and artificial gills

The oxygen flux in both biological and artificial gills was evaluated to

determine the oxygen uptake efficiency of them. Fig .5.12 shows the oxygen

flux in both biological and artificial gills as a function of water flow rate. The

oxygen flux increased with water flow rate. The oxygen flux in the biological

gill is approximately double that in the artificial gill. This result indicates that

the oxygen uptake efficiency in biological gill is superior to that in artificial gill,

and the biological gill takes up oxygen effectively from water despite its lower

surface area.

Reynolds number of water in the secondary lamella and artificial gill

module was computed using eqs. (5.7) and (5.10). Reynolds number of water

represents the turbulence of water flow in them, and this also represents

disruption of water-side film resistance. Thus, this number shows which

structure is favorable to disrupt water-side resistance. Fig. 5.13 shows the

Reynolds number of water in the secondary lamella and artificial gill module.

The Reynolds number in the biological gill is much lower than that in the

artificial gill. This suggests that high oxygen flux in the biological gill is not

caused by convective transport in the water flow between secondary lamellae.

The structure of secondary lamella is not responsible for high oxygen flux in

biological gill.

149


Fig. 5.12 Oxygen flux in biological and artificial gills as a function of water flow rate

Fig. 5.13 Reynolds number of water in secondary lamella and artificial gill module

150

Chapter 5

In both biological and artificial gills, oxygen is taken up from water to blood

(oxygen carrier solution) through the membrane, in other words, oxygen in

dissolved water is absorbed by the blood (oxygen carrier solution). Thus, the

characteristics of blood and oxygen carrier solution are important factors in

oxygen uptake. To elucidate of the reason for the high oxygen uptake efficiency

in biological gill, the characteristics of oxygen absorption of fish blood and

oxygen carrier solution were evaluated. Fig .5.14 shows the oxyhemoglobin

dissociation curves of carp blood and oxygen carrier solution. The oxygen

partial pressure in the carp venous blood is 1.56 kPa, and that in the inlet oxygen

carrier solution in the oxygen uptake device is 9.57 kPa. The oxygen partial

pressure difference between water and blood is approximately double that

between water and the oxygen carrier solution. This indicates that the driving

force for oxygen transfer in the biological gill is higher than that in the artificial

gill. In addition, the oxyhemoglobin dissociation curve of the carp blood rises

sharply at lower oxygen partial pressures, demonstrating that the carp blood has

higher oxygen affinity.

Fig .5.15 shows fractional oxygen uptake efficiency as a function of water

flow rate. This represents effective use of dissolved oxygen in water, and this

leads to lower water flow rates and higher device efficiency. The oxygen uptake

efficiency decreased with increasing water flow rate. The oxygen uptake

efficiency of the biological gill is higher than that of the artificial gill. These

results demonstrate that the high efficiency of the biological gill is attributable to

the large oxygen partial pressure difference between water and blood. The

biological gill, with a lower gas exchange surface area, takes up oxygen

effectively at lower water flow rates.

151


Fig. 5.14 Oxyhemoglobin dissociation curves ofcarp blood and oxygen carrier solution

Fig. 5.15 Fractional oxygen uptake efficiency asa function of water flow rate

152

Chapter 5

5.3.2 Further improvement of artificial gill

The high oxygen uptake efficiency of the biological gill can be attributed to

the lower oxygen partial pressure of blood, which causes a large oxygen partial

pressure difference, which is the driving force of oxygen transfer. A new

operating condition of the artificial gill was devised so as to decrease the oxygen

partial pressure of the oxygen carrier solution from 10.3 kPa to 8.70 kPa in the

oxygen uptake device.

Fig. 5.16 shows oxygen uptake efficiency at an oxygen partial pressure in

the oxygen carrier solution of 8.70 kPa and 10.3 kPa in the oxygen uptake

device. Oxygen flux increased with decreasing oxygen partial pressure in the

oxygen carrier solution, whereas the oxygen partial pressure of inspiration

decreased. This is because decreasing oxygen partial pressure in the oxygen

carrier solution causes a decrease in the driving force for oxygen release. In the

artificial gill, the oxygen affinity of the oxygen carrier solution is controlled by

changing the temperature. Fig. 5.17 shows the change in oxygen affinity of the

oxygen carrier solution with changing temperature. In the oxygen uptake device,

the oxygen affinity of the oxygen carrier solution is increased by cooling the

oxygen carrier solution to 293 K, and the oxygen partial pressure in the oxygen

carrier solution is decreased because hemoglobin combines with much of the

dissolved oxygen there. An increase in the oxygen partial pressure difference

between water and oxygen carrier solution enhances oxygen uptake. In contrast,

in the oxygen release device, the oxygen affinity of the oxygen carrier solution

is decreased by heating the oxygen carrier solution to 310 K, and the oxygen

partial pressure in the oxygen carrier solution is increased because hemoglobin

153


Fig. 5.16 Oxygen uptake efficiency at oxygen partial pressures in
oxygen carrier solution of 8.70 and 10.3 kPa in oxygen uptake device Fig. 5.17 Change in oxygen affinity of oxygen carrier solution with changing temperatures
154

Chapter 5

dissociates much of its oxygen into the oxygen carrier solution. An increase in

the oxygen partial pressure difference between the oxygen carrier solution and

the air enhances oxygen release.

To obtain a high oxygen partial pressure difference in the oxygen uptake, as

in the biological gill, a greater change in the oxygen affinity of the oxygen

carrier solution is required. The use of an artificial oxygen carrier that undergoes

a large change in its oxygen affinity with appropriate stimulation will lead to

high oxygen uptake efficiency of the artificial gill, comparable to that of a

biological gill.

155


5.4 Conclusions

To develop a high-performance artificial gill, the mechanism of a biological

gill is elucidated in terms of variables such as the required oxygen flux, the

Reynolds number of water, and the difference in oxygen partial pressure,

between water and blood (or oxygen carrier solution), which is the driving force

for oxygen transfer and oxygen uptake. The oxygen flux of both biological and

artificial gills increases with the water flow rate. The oxygen flux of a biological

gill is approximately double that of an artificial gill. The Reynolds number of

water flow in the biological gill is lower than that in the artificial gill. Hence the

higher oxygen transfer flux is independent of the flow velocity of water in the

biological gill. The oxygen partial pressure difference between water and blood

in the biological gill is twice that in the artificial gill. This larger partial pressure

difference leads to a higher rate of oxygen transfer. To obtain a high oxygen

partial pressure difference in the oxygen uptake, as in the biological gill, a

greater change in the oxygen affinity of the oxygen carrier solution is required.

The use of an artificial oxygen carrier that undergoes a large change in its

oxygen affinity with appropriate stimulation will lead to high oxygen uptake

efficiency of the artificial gill, comparable to that of a biological gill.

156

Chapter 5

List of symbols

A Surface area (m2)

a Parameters for gill surface area (m2/gm)

de Equivalent diameter (m)

d Diameter of the hollow fibers (m)

eAg Effective surface area of

the secondary lamella (m2)

J Oxygen flux (mol s-1 m-2)

N Oxygen transfer rate (mol/s)

m Parameters for gill surface area (-)

P Porosity of membrane packing (-)

p Oxygen partial pressure (mmHg or Pa)

Q Flow rate (m3/s)

QW Ventilation rate (m3/s)

rh Hydraulic radius (m)

Re Reynolds number

S Cross-sectional area of a flow path (m2)

U Oxygen uptake efficiency (-)

u Mean linear velocity of water (m/s)

Wf Weight of fish (g)

W Ventilation rate (water flow rate)

per secondary lamella surface area (m3 s-1 m-2)

X Distance between filaments (m)

Y Distance between secondary lamellae (m)

157


Subscripts

in Inlet

out Outlet

158

Chapter 5

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