Chapter 5

5.1 Introduction

A fish can exchange gases effectively by the indirect contact of blood with water in its . The excellent mechanism of fish 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 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 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 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 difference between water

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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.

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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].

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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 difference between water and blood caused by the counter- produces the effective gas exchange [2,17-18].

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Fig. 5.1 Diagram showing, in horizontal section, Fig. 5.2 Schematic diagram of piles of gill the position of the gill arches and gill filaments filaments standing on two gill arches [11,19]; and water flow: (A) Buccal cavity, (B) Buccal The end of gill filament is contacted closely to cavit y, (C) Gill arch, (D) Piles of gill filaments, the next gill filament. Water flow between slits (E) Opercul ar cavity, (F) Operculum of two gill filaments

Fig. 5.3 Diagram of a portion from a gill arch of a teleost fish [20]: direction of water and blood flow are indicated by dashed and full allows, respectively

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Fig. 5.4 Cross-sectional view of secondary lamellae: Fig. 5.5 Electromicrograph of a secondary lamella A: cross-section of several blood channels, B: blood channel of carp (Cyprinus carpio) [19,20]: enlargement of blood channel, R: erythrocyte, P: E: epithelium, P: pillar cell, R: erythrocyte Pillar c ell, E: epithelium, N: nucleus [20]

Fig. 5.6 Scanning electron micrograph of Fig. 5.7 Flow of water and blood in an a pla stic cast of a trout gill filament, showing elasmobranch fish: As in teleost fish, the flow several lamellae: Magnification 160x [20] of blood is in the opposite direction to that of the water [20].

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5.1.1.2 Gill surface area

Gill surface area per fish body 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].

A = aW m (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

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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 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 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].

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

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

p50 Oxygen cap. 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

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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]

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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.

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

Table 5.3 Details on carp gill [5] Distance between filaments (µm) 385 Distance between secondary lamella (µm) 48 Secondary lamella surface area (m2) 0.0823 Total cross sectional area of water channel (mm2) 1970 Body weight (kg) 0.319

In this chapter, the oxygen uptake performance of an artificial gill using a concentrated hemoglobin solution, which is designed in chapter 3, compared with that of a biological gill. Fig. 5.11 shows a schematic of the artificial gill system using a concentrated hemoglobin solution as the oxygen carrier solution. Table 5.4 summarizes the operating conditions of the artificial gill. Table 5.5 shows technical data on the oxygen carrier solution and the hollow fiber module. This artificial gill consists of two devices: one is oxygen uptake device from water to the oxygen carrier solution, and the other is an oxygen release device

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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.

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

Table 5.4 Operating c onditions for artificial gill Condition A B C* (Minimum water (Intermediate) (Minimum flow rate) membrane surface area) Flow rate (cm3/s) Seawater 2330 4200 6530 Oxygen carrier solution 233 233 233 Expired 93.3 93.3 93.3 Inlet oxygen partial pressure in oxygen carrier solution (kPa) In oxygen uptake 9.33 9.66 9.48 In oxygen release 22.7 22.7 22.7 Oxygen partial pressure of sea water (kPa) Module inlet 20.0 20.0 20.0 Module outlet 13.0 16.1 17.8 Total membrane surface 156 94.6 63.8 area (kPa) *Condition C is same operating condition in chapter 3.

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

5.2.2 Oxygen flux of biological and artificial gills

Humans require larger amounts of oxygen than fish because of their larger body volume. The artificial gill, therefore, requires a larger membrane surface area and larger water flow rate than a biological gill to supply enough oxygen for human . The unit of water flow rate per gas exchange surface area was used to evaluate the gills on similar scale, and oxygen flux, defined as oxygen transfer rate per gas exchange surface area, was used as the parameter of oxygen uptake. In the biological gill, the ventilation rate (water flow rate) per secondary lamella surface area W (m3 s-1 m-2) is defined as follows:

Q W = w (5.2) eAG

3 where QW is the ventilation rate (m /s) and eAg the effective surface area of the secondary lamella (m2). In the artificial gill, the water flow rate making contact with the hollow-fiber membranes is represented by

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Q W = w (5.3) AM

2 where AM is the membrane surface area of the hollow fibers (m ). Oxygen flux J (mol s-1 m-2) is defined as follows:

N J = O2 (5.4) eAG N J = O2 (5.5) AM

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

4xy d = (5.6) e 2x + 2y where x is the distance between filaments (m) and y the distance between secondary lamellae (m). Reynolds number Re is obtained by

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d u Re = e (5.7) ν 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]

Pd r = (5.8) h 4(1 − P ) 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

Q u = w (5.9) PS where S is the cross-sectional area of a flow path (m2). The Reynolds number is obtained by the following equation:

4r u Q d Re = h = w (5.10) ν (1 − P )Sν

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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

p − p U = Win Wout (5.11) pWin

where pWin and pWout are the oxygen partial in water (Pa) at the module inlet and outlet, respectively.

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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.

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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

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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 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.

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Fig. 5.14 Oxyhemoglobi n dissociation curves of carp blood and oxygen carrier solution

Fig. 5.15 Fractional oxy gen uptake efficiency as a function of water flow rate

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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

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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

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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.

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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.

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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) 3 QW Ventilation rate (m /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)

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Subscripts in Inlet out Outlet

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