Physiological aspects of placental ontogeny and phylogeny

Placenta (I985), 6, 14I-I54

Physiological Aspects of Placental Ontogeny and Phylogeny W. MOLL Institut .[~'r Physiologie der Universitdt Regensburg, Posfach 397, D--84oo Regensburg, FR Germany

INTRODUCTION For fetal life and growth, oxygen and nutrients must be transferred from maternal to fetal blood, and fetal waste products must be transferred from fetal to maternal blood. The transfer has to be performed by an organ that allows for fetal circulatory autonomy, that maintains a fetal-maternal immunological barrier, and that can be readily delivered after birth. The functional element of this organ, that is, of the placenta, is not necessarily a system of apposed maternal and fetal membranes as Mossman's definition of a placenta (Mossman, i937) states, but rather a system ofapposed channels for maternal and fetal blood with arteries and veins on both sides adapted for blood supply and drainage (see Figure i). The substances to be transferred are conveyed by blood flow to the contact area between maternal and fetal blood (the placental membrane), transferred across the membrane by the usual mechanisms for trans- and intercellular transport, and finally carried away by the blood flow on the other side. During ontogeny, maternal and fetal blood supply is established by adapting the respective supplying arteries. The exchange channels for fetal blood, the fetal capillaries, are formed by embryonic mesoderm. To provide exchange channels for maternal blood, different principles, developed during phylogeny, are applied: during epitheliochorial and endotheliochorial placentation, the trophoblast exposes the pre-existing microvascular system in the (maternal) Fetal arteries and veins for blood supply and drainage

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Fsgure z. The functional element of the placenta: a system of apposed channels for exchange providinga contact area (placental membrane) between maternal and fetal blood, adapted to maternal and fetal arteries for blood supply and drainage.

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uterine mucosa and expands it by inducing growth as discribed for sheep by Barcroft and Barron (I946). During haemochorial placentation, the trophoblast taps the maternal vascular system and channels the maternal blood. Throughout pregnancy the fetus grows. Increase in fetal mass requires increase in placental transfer. The placenta is distinguished from other organs in being under steady pressure to raise its own performance. From a functional point of view, the placenta is an evolvinl~, developing organ throughout its life. Flow rate and the apparent permeability of the placental membrane, as defined by their physical and morphological properties, including the mechanisms for passive and active transport, are the determining parameters of placental transfer. Thus, placental ontogeny means continuous adjustment of apparent permeability of the placental membrane and of placental blood flow. In the first part of this paper, which deals with functional aspects ofontogeny, the adjustment of apparent placental permeability and blood flow will be described on the basis of the data available from various species. In the second part, devoted to functional aspects of phylogeny, the functional meaning of the various ways of establishing channels for maternal blood is discussed.

F U N C T I O N A L ASPECTS OF P L A C E N T A L O N T O G E N Y T h e a d j u s t m e n t o f the a p p a r e n t placental p e r m e a b i l i t y With respect to oxygen, placental permeability is determined by surface area and attenuation (i/thickness) of the placental membrane. The surface area of the true placental membrane, that is, of the true contact area of maternal and fetal blood, is not precisely known, but the chorionic villous surface area is usually used as a measure of it. As shown by Wilkin and Burszstein (I958) and Aherne and Dunnill (i966) chorionic villous surface area increases throughout pregnancy but lags behind fetal weight (Figure 2). Baur (I977) has shown, in an extensive comparative morphometric study, that this is true also in the cat, horse, cow and pig. However, there are various histological indications that the placental membrane attenuates during the course of 4

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Figure 2. Fetal weight (average curve according to Hytten and Leitch, I97t) and chorionic villous surface (data from Aherne and Dunnill, t966) related to gestational age in the human. Chorionic villous surface increases throughout pregnancy but lags behind fetal weight.

Physiological Aspects

143

pregnancy so that the permeability for gases appears to be better adjusted than the rise in surface area would indicate. This has been verified by physiological measurements. The adjustment of placental permeability for gases can be examined by physiological methods. For gases, the placental permeability is usually expressed by the diffusing capacity, that is, by the rate of gas transfer per time and partial pressure difference. There is general agreement that this figure can be measured with CO without interference by the effects of unequal distribution of blood flow and metabolism. Longo and Ching (I977) followed the diffusing capacity in sheep over a longer period of gestation and found that its rise is proportional to fetal weight (see Figure 3). This was true even during a period of time when placental weight in sheep remains fairly constant. According to these data the diffusing capacity seems to be adjusted rather well to fetal weight. For some other species, data on the placental diffusing capacity at term are available. Table i shows the diffusing capacity per fetal weight for three species of similar body weight but of different placental structure. The diffusing capacity is roughly the same in these three species. It is higher than needed for 9o per cent equilibration in the concurrent placenta even if no facilitating difference in oxygen affinity exists. Thus, the placental permeability for gases appears to be adequately adjusted to fetal weight so that oxygen transfer seems to be never limited by placental permeability. While the permeability for gases depends on the attenuation of the whole placental membrane, the permeability for hydrophilic substances, such as urea and electrolytes, depends upon the density and diameters of pores in and between the cell membranes. Meschia (i 972) reported that the placental clearance of urea in sheep is related to fetal weight (Figure 4)- The clearance of urea as a measure of placental permeability for urea is obviously proportional to fetal weight. Flexner

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Figure 3. CO diffusing capacity of the placenta related to the estimated fetal weight in unanaesthetized sheep (according to data Longo and Ching, I977). A proportional relationship is obvious.

Table 1. CO diffusing capacity per fetal weight in three species with different placental structures (modified according to Bissonnette et al, i979) Species

Placental structure

Dp/Mf (ml/min/Torr/kg)

Authors

Sheep Dog Monkey

Epitheliochorial Endotheliochorial Haemochorial

o.54 o-57 o.65

Longo and Ching (I977) Longo, Power and Forster (I967) Bissonnette et al (1979)

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{kg)

F~gure 4. Placental clearance of urea as a measure of placental permeability for urea related to fetal weight in sheep (according to data of Meschia, i972). The diagram shows a proportional relationship between the permeability for this hydrophilic substance and fetal weight.

and Pohl (194 I) measured the permeability for sodium in the unanaesthetized guinea pig (Figure 5); here, too, in spite of a large scatter of the data, a proportional relationship between permeability and fetal weight is seen. A similar relationship between sodium permeability and fetal weight has been observed by Flexner and his coworkers in the sow, goat, rabbit and rat (see Flexner and Gellhorn, t942 ). Obviously, even the overall permeability for hydrophilic substances appears to be generally adjusted to fetal weight according to the available data. This adjustment may be partially explained by the increase in placental surface area, but in view of the lag in surface adaptation, we ought to postulate an increase in pore density or diameter in order to explain the complete adjustment. Even the facilitated transport of glucose seems to be continuously adjusted to fetal weight. Data on glucose concentrations in the human during midgestation (Gennser and Nilson, i97i ) and at term (Lumley and Wood, I967) indicate that the apparent placental permeability for glucose per placental weight at term is twice that at midgestation (see Moll, I98I); related to fetal weight, the apparent permeability stays constant during the second part of pregnancy. The total number of carriers seems to keep up with the increasing fetal weight. Probably, this adjustment occurs on the basis of an increase in surface area and carrier density of trophoblast cell membranes. r

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Physiological Aspects

x45

In summary, all pertinent properties of the placental membrane that determine the apparent placental permeability (the area, the attenuation, and the number of pores) appear to be well adjusted to fetal growth. Placental ontogeny implies fairly precise adjustment of the functional properties of the placental membrane. Net active transport of amino acids is controlled by the concentration in fetal blood affecting back diffusion (Hill and Young, I973) and by the intracellular concentration of amino acids which controls the transport activity (Smith and Depper, I974)- Hence, the amino acid transfer is automatically adjusted to fetal weight. It is also to be expected that transport mechanisms increase in number during pregnancy. A d j u s t m e n t o f fetal p l a c e n t a l blood flow Umbilical circulation has been studied extensively in sheep. During the early part of gestation, the conductance of the umbilical circulation increases; during the last' four weeks, a rise in fetal blood pressure occurs (Dawes, I962). Both changes cause the umbilical blood flow to increase. The available data show that the product of umbilical blood flow rate and haemoglobin concentration (the umbilical flow of haemoglobin) increases proportionally with fetal weight. Under conditions where the haemoglobin concentration does not change, umbilical blood flow per fetal weight remains constant (Meschia et al, I965) whereas the rise in umbilical blood flow is slowed down when the haemoglobin concentration rises (Dawes and Mott 1964). In both cases, the transport capacity for oxygen is adjusted to fetal growth. T h e a d j u s t m e n t o f m a t e r n a l p l a c e n t a l blood flow On the maternal side of the placenta, no biologically significant changes in arterial blood pressure occur during normal pregnancy in the human (Schwarz, 1964) or in any other species investigated so far. T h e adjustment of maternal placental flow is based on the rise in the vascular conductance of the uteroplacental vascular system. This rise in conductance during pregnancy is brought about by the expansion of the placental exchange channels and by the widening of the supplying arteries. The exchange channels formed during haemochorial placentation, the trophoblastic lacunae, and the intervillous space, have a high vascular conductance; they accommodate the normal placental flow at a few m m H g driving pressure difference (Herberger and Moll, I976 , Moll et al, I978 ). In species with a haemochorial placenta (guinea pig, rat, rabbit and monkey) the intra-arterial blood pressure at the entry into the placenta (at the myometriodecidual junction) was found to be only a small fraction of the central arterial blood pressure (see Table 2). When the maternal placental vascular bed ofa haemochorial placenta is formed, the local peripheral resistance is almost completely removed and blood flow rate is

Table 2. Central arterial and preplacental arterial blood pressure in pregnant animals. The figures in parentheses give the standard deviation

Pressure (mmHg) Species

central preplacentala

Guinea pig Rat Rabbit Monkey Sheep

65 (6) 13o (9) lOO (12) 8o (13) iio (21)

Authors

12 (3) Moll and Kiinzel (1973) 14 (i) 8 (2) 12 (3) Moll et al (1974) 84 (13) Moll and Kiinzel (1973)

a The preplacental blood pressure is defined as the intra-arterial pressure at the myometriodecidualjunction.

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W. Moll

limited p r e d o m i n a n t l y by the conductance of the supplying arteries. I n sheep, different conditions prevail. T h e blood pressure in o.5 to i ram-wide arteries leading to the placenta was found to be close to the central arterial pressure (see T a b l e 2); in the epitheliochorial placenta of sheep the rise in peripheral conductance by growth of the endometrial microvascular system seems to parallel the rise in conductance of the supplying arteries, and the normal distribution of vascular resistance and pressure drop are maintained. In the supplying arteries, that is, the uterine, radial and spiral arteries, a large increase in internal diameter is observed. T h e widening is especially pronounced near the entry into the placenta, as shown in Figure 6 for the guinea pig, where the internal diameter rises 7-fold. Even when the arteries lengthen d u r i n g pregnancy, the overall conductance of the arteries increases more than IOO--fold resulting in a proportional rise in blood flow. T h e m a g n i t u d e of blood flow increase d u r i n g pregnancy may be illustrated by the flow rates across a radial (mesometrial) artery of a guinea pig before pregnancy and at term (Table 3). T h e flow rate in this artery rises 2oo-fold d u r i n g the course of pregnancy.

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Figure 6. Internal diameter of placental mesometrial arteries of pregnant guinea pigs at their point of entry into the

uterine muscle during the course of pregnancy. The internal diameter rises 7-fold so that the local resistance is almost abolished (according to Moll, Espach and Wrobel, 1983).

Table 3. Blood flow through mesometrial arteries supplying a virgin uterus and a placenta at term

Non-pregnant uterus Placenta

Total blood flow

Number of arteries

0.22 ml/min

19

12 pl/min

8.4 ml/min

3

28oo gl/min

Flow/artery

Blood flow across the arteries supplying a nonpreguant uterus was calculated from the total blood flow across the virgin uterus and the number of arteries supplying the uterus. Blood flow across a mesometrial artery supplying a placenta was determined from the blood flowacross a placenta and the number of arteries supplying the placenta. (Data from Hartmann, I98I.)

t47

Physiological Aspects

How is the widening of the supplying arteries brought about? The arteries in the guinea pig prove to be rather resistant to relaxing drugs: when excised radial arteries are incubated in solutions containing papaverine, which normally relaxes the vascular musculature, no change in diameter is found (Moll, G6tz and Klappstein, I983). Thus, the widening is not based on smooth muscle relaxation, as during acute blood flow control, but on remodelling of the vessel wall. The increase in diameter is associated with massive growth. At the very beginning of pregnancy, the 3H-thymidine incorporation, a quantitative measure of the DNA synthesis, is more than i0-fold greater than that found in dioestrous animals (Makinoda and Moll, i982 ). Wet weight, protein content and DNA content increase 3~ to 50-fold in these arteries during pregnancy (see Figure 7)- The widening of supplying arteries seems to be part of an intricate growth process. The adjustment of the maternal supplying arteries appears to be controlled by placental tissue. As shown in man (Harris and Ramsey, x966), rhesus monkeys (Ramsey, Chez and Doppman, I979) and in the guinea pig (Egund and Carter, i98o), the arteries dilate progressively as they approach the placenta. The cross sectional area of the arterial wall is particularly large in the proximity of the placenta (Moll, Espach and Wrobei, I983) indicating a high local growth rate. The arterial changes seem to proceed under the impact of factors originating from the placenta. These factors are still unknown. Widening and growth may be induced by invading trophoblastic cells, haemodynamic forces (as they occur in the widening arteries of arteriovenous fistulae), and by placental factors such as hormones diffusing toward the arterial wall. How precise is the adjustment of the maternal placental flow? For the unanaesthetized guinea pig a proportional relationship between the maternal placental flow and the fetal weight has been demonstrated by Peeters, Grutters and Martin, (i98o) (Figure 8, left). Similar results were obtained in other animals. Even in the rat, where fetal weight increases 7-fold during the last five days of gestation, placental flow keeps up with the combined fetal and placental weight (see Figure 8, right). In the unstressed pregnant sheep (Rosenfeld, I977), blood flow per uterine weight is nearly the same as it is in nonpregnant animals and only 3o per cent lower than at midProtein Content

Wet Weight

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Figure 7. Wet weight,proteincontentand DNA contentofplacentalmesometrialarteriesduringthe courseofpregnancy (accordingto the data of Moll, Espach and Wrobel, 1983).

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Figure 8. Maternal placental flowrelated to fetal weight in guinea pigs (accordingto Peeters, Grutters and Martin, i98o)

and in the rat (Parish and Moll, unpublished observations).

gestation. In summary, even when the scatter of data precludes precise conclusions, a fairly strong adaptation of maternal placental flow to fetal growth is evident. Looking back on the data so far presented, we may conclude that both parameters that affect placental transport and thereby fetal concentrations, placental blood flow as well as apparent placental permeability, rise roughly proportionally with fetal weight. Placental ontogeny means continuous adjustment of placental functional properties to fetal growth.

PHYSIOLOGICAL ASPECTS OF PLACENTAL PHYLOGENY Physiological aspects of placental ontogeny are an intriguing subject for everyone who works experimentally on the placenta since he is confronted by species differences and has to inquire into their biological origin and meaning. A discussion of these aspects, however, remains highly speculative because we do not know for sure why and how placentae developed. There is no general consent as to which sequence the epitheliochorial, endotheliochorial and haemochoriai placentae arose during phylogeny (for review see Starck, I975; Luckett, 1975). The present material allows for different concepts. However, the following two phylogenic arguments appear decisive (see Luckett, 1975). (i) All unrelated eutherian taxa with an epitheliochorial placenta exhibit detailed homology in the morphogenesis of all their fetal membranes as would be expected in cases of primitive retention of the ancestral condition in distantly related taxa. (2) Diffuse, epitheliochorial placentation in some primates (e.g. lemuroidea) is associated with development of a choriovitelline placenta and amniogenesis by folding which are characteristic for metatheria and therefore considered as primitive. These facts suggest that the ancestral placenta was epitheliochorial and diffuse. Later during phylogeny the compact placenta was formed where the placentation is confined to a part of the endometrial

Physiological Aspects

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surface; the endotheliochorial placenta developed by involution of the endometrial epithelium and selective growth of the endometrial capillaries and, finally, the haemochorial placenta emerged when the trophoblast began to tap the maternal blood vessels and channelled the maternal blood. What was the reason for this development? Why did it occur in some species, and why was the so-called primitive situation retained in others? In order to find the answers to these questions we should learn the pertinent functional differences of the various types of placentation and their significance for the requirements of the living conditions of the species. L a r g e surface area in c o m p a c t p l a c e n t a e According to Baur (I977) placental surface area, related to the combined fetal and placental weight, is about eight times higher in species with compact placentae than in species with diffuse placentae. This surface expansion allowed for restriction of placentation to a small portion of the endometrial surface. Strangely enough, in contrast to what we would expect, no facilitation of gas transfer seems to occur: the degree of equilibration of maternal and fetal oxygen partial pressures in the compact placenta of the cow is less than that in the diffuse placenta of the mare (Comline and Silver, I974) whereas the placental surface area in the cow's placenta is six times that in the mare's placenta (Baur, I977). Possibly, shunt diffusion and oxygen consumption hamper oxygen transfer in the compact epitheliochorial placenta. Other factors, not referred to gas exchange, such as reduction in placental weight, must have favoured the evolution of the compact placenta. Progressive a t t e n u a t i o n o f the placental m e m b r a n e by r e d u c t i o n in the n u m b e r o f tissue layers in the placental m e m b r a n e ? Endotheliochorial and haemochorial placentation are generally considered as ways for further attenuation of the placental membrane assuming that reduction in the number of layers of the placental membrane means progressive attenuation. This concept, however, lost its basis when histology showed that intra-epithelial capillaries occur in the epitheliochorial placenta of the sow (Wimsatt, 1962 ) and that no obvious correlation exists between the number of tissue layers and the degree of attenuation of the placental membrane. Even functional measurements of the diffusing capacity for CO, which is proportional to the attenuation, failed to give any indication for attenuation by diminution of tissue layers (Table 4): the diffusing capacity of the compact epitheliochorial placenta of the sheep is higher than that of the haemochorial placenta of the Table 4. CO Diffusingcapacityper placental weight (Dp/Mp) in species with various placental structuresa

Species

Placentalstructure

Sheep Monkey Guinea pig

Epitheliochorial Haemomonochorial Haemomonochorial

Rabbit Rat

Haemodichorial Haemotrichorial

DdM p (ml/min/mmHg/kg)

Authors

7 2 55 38 29 16

Longo & Ching (i977) Bissonnette et ai (i979) Gilbert et al 0979) Bissonnette & Wickham (1977) Rocco, Bennett & Power (1975) Bissonnette et al (1979)

a Haemomonochorial,haemodichorialand haemotrichorialplacentaeare haemochorialplacentae with one, two and three layers of trophoblastic cells respectively(Enders, 1965). The data were calculated (except that for the monkey)from the figureson the diffusingcapacityper fetal weight given by the authors quoted and by the ratio of placental over fetal weightcompiled by Dawes ( 1 9 6 8 ) .

W. Moll

15o

monkey. There is certainly no indication of a progressive attenuation with the reduction of tissue layers when species of similar size are compared. Some placentae may well have extraordinary diffusing capacities. The guinea-pig placenta has the highest diffusing capacity so far known (see Table 4). It is more than eight times higher than that in sheep, dogs and monkeys. This high diffusing capacity enables the guinea-pig fetus to use effectively the exchange properties of a placental countercurrent exchange system which requires especially high diffusing capacity. There are great differences in diffusing capacity between the different species, but these differences cannot simply be related to the classification ofepitheliochorial and haemochorial placentae since the scatter of diffusing capacities within the group of haemochorial placentae is larger than the differences between the groups. L o w m a t e r n a l p l a c e n t a l flow in h a e m o c h o r i a l p l a c e n t a e Is haemochorial placentation a more efficient way of providing maternal placental flow? Table 5 gives data on maternal placental flow. The largest flow rates, absolute as well as relative to fetal weight, are seen in the epitheliochorial placentae. After haemochorial placentation the rate of maternal placental flow appears even less than after epitheliochorial placentation. Possibly, increasing placental efficiency, due to the particular vascular arrangement, can compensate for a lower flow rate. Table 5. Maternal placental blood flow per fetal weight in species with epitheliochorial and haemochorial placentae

Placental structure

Species

Haemochorial

Monkey

Haemochorial Haemocborial Epitheliochorial Epitheliochorial Epitheliochorial

Blood flow (ml/min/kg)

Author

Guinea pig Rabbit

izo 84 i6o Io6

Peterson& Behrman (t969) Meschiaet al (1967) Peeters,Grutters & Martin (198o) Duncan& Lewis (i969)

Sheep Cow Horse

z5o 3zo 33o

Silver & Comline !1976)

Differences in p e r m e a b i l i t y for h y d r o p h i l i c s u b s t a n c e s There are large differences between epitheliochorial and haemochorial placentae in respect of their permeabilities for sodium. Since the classical studies of Flexner and Gellhorn (i94z), and their coworkers, it has been known that haemochorial placentae have a similar permeability which is xo to 3oo times higher than the permeability of endotheliochorial and epitheliochorial placentae (Table 6). The correlation between histological structure and permeability was weakened when the so-called syndesmochorial placenta was recognized as an epitheliochorial placenta, hut it is still obvious. It is therefore beyond doubt that the haemochorial placenta equilibrates more rapidly, and more closely, the electrolyte concentrations of maternal and fetal blood. In the compact epitheliochorial placenta of the sheep a higher concentration gradient is needed for transplacental electrolyte transfer than is the case in the haemochorial placenta. In the diffuse epitheliochorial placenta of the sow, where the sodium permeability is again thirty times lower, placental electrolyte transfer requires active sodium transport. However, it is by no means clear whether low placental permeability is a pertinent drawback. The gradient needed for electrolyte transport in sheep is rather small (a few mM according to measurements of the hydraulic permeability of the sheep placenta reported by Armentrout et al, I977)- Energy

Physiological Aspects

ISI

Table 6. Placental permeability for sodium in species with various placental structuresa

Species

Placental structure

Rat Rabbit Guinea pig Monkey Man Cat Goat Sheep Sow

Haemotrichorial Haemodichorial Haemomonochorial Haemomonochorial Haemomonochorial Endotheliochorial Epitheliochorial Epitheliochorial Epitheliochorial

Placental permeability (/al/s/g) 0.7 0.6 0.5 o.4 o.6 o.o6 o.o4 o.o4 0.002

Authors Flexner and Gellhorn 0942) Battaglia et al (I968) Flexner and Gellhorn 0942) Tbornburg, Binder and Faber (1979) Flexner and Gellhorn 0942)

a Haemomonochorial,haemodichorialand haemotrichorialplacentaeare haemochorialplacentaewith one, two and three layers of trophoblastic cells, respectively (Enders, i965).

requirement for active transport of sodium and potassium in the sow is about o. i per cent of the total energy requirement of the fetus during intrauterine life (see Appendix). Furthermore, lower placental permeability may be even advantageous. Under stress, as during fight, flight and fright, where maternal concentrations may be far from being optimal for fetal growth, lower placental permeability may protect the fetus from transient harmful concentration changes in maternal blood. So, transient maternal lactic acidosis occurring in a cow, during flight, has little impact on her fetus because of the low placental permeability. Maternal and fetal metabolism may obtain higher degrees of autonomy. So, while differences in permeabilities of the various placentae are quite obvious, the biological meaning of these differences remains obscure. R a p i d iron t r a n s f e r in the h a e m o c h o r i a l p l a c e n t a Iron is more easily transmitted after haemochorial placentation. Haemochorial placentation enables the trophoblast to pick up transferrin directly from maternal blood and thus provides a most rapid transfer of iron into the fetus (see van Dyke, 198 I). This direct uptake of transferrin seems to be impossible in endothelio- and epitheliochorial placentae where iron transfer occurs by the sluggish process of uteroferrin synthesis and secretion (see Roberts and Bazer, I98o). The amount of serum iron transferred 2 h after injecting ferrous citrate is 5 per cent or greater in species with haemochorial placentation, and less than o. i per cent in species with epitheliochorial or endotheliochorial placentation (Ulysses et al, I972). Possibly, the facilitation of iron transfer is the most pertinent advantage of haemochorial placentation, this being specially significant in species with low body weight and high growth rate. Speed and safety o f delivery When evaluating the advantages of the various placental structures, we should consider also the period of delivery. It is biologically important that the delivery of the placenta occurs rapidly and with a minimum of complications. Veterinarians know the rapid delivery of the diffuse epitheliochorial placenta of the mare and point out the rarity of complications such as placental retention in this species. Speed of placental delivery appears to be especially significant for large gregarious animals where we often find the diffuse epitheliochorial placenta; these animals cannot hide during delivery and have to follow the herd rapidly. Furthermore, the diffuse epitheliochorial placenta appears to be suited best for safe delivery in large animals with a low rate of reproduction.

x52

W. Moll

CONCLUSIONS The various placentae, so different in their histological structure, are nevertheless very similar in many pertinent functions. There are no essential differences in gas permeability that can be clearly related to classical placental structures. All placental systems provide the same oxygen saturation in fetal arterial blood (see Table 7). There are major differences in permeability for hydrophilic substances, but their biological meaning is not clear. The hypothesis may be tentatively set out that the diffuse epitheliochorial placenta was conserved in some species because it can be delivered particularly quickly and safely, while other species developed the haemochorial placenta because this type of placenta facilitates placental transport of iron. This concept is consistent with the observation that the epitheliochorial placenta occurs frequently in larger animals where safety and speed of delivery count particularly, and that we find haemochorial placentae usually in smaller animals with high growth rate where the requirement for iron transfer is high. It should be emphasized, however, that such speculations are not yet substantiated by data on speed and safety of placental deliveries and on iron supply in free nature. The variety of placentae we see at present is still not conclusively explained and may well be correlated with aspects not discussed in this paper. Knowledge of the biologically important functional differences of the various types of placentae are still lacking. We still cannot answer the question: why do so many types of placental structure occur in the kingdom of mammals?

Table 7. Fetal arterial oxygen saturation (So) of haemoglobin in species with various placental structures

Species Man Monkey Guinea pig Sheep Horse Cow Pig

Placental structure Haemochorial Haemochorial Haemochorial Epitheliochorial Epitheliochorial Epitheliochorial Epitheliochorial

SO(% )

Authors

6o (U) 6o(U) 59 (U) 6z (U) 6o (L)a 5~ (L)" 46 (L)a

Berg and Saling 0972) Dawes et al (I96O) Girard et al (1983) Dawes, Mott & Widdicombe(1954)

U = upper body; L = lower body. 9 The oxygensaturation in the horse,cowand pig wascalculatedfromthe figuresfor Po: PH and P~oas given by Comline and Silver (i974).

APPENDIX T o t a l fetal e n e r g y e x p e n d i t u r e a n d the r e q u i r e m e n t o f p l a c e n t a l electrolyte t r a n s f e r across the p l a c e n t a in the pig According to Baur (i 977) fetal weight (M) in pigs, as a function of gestation age in weeks (w), is described by the formula M I/3 =

o.65w

Using this formula, fetal weight can be calculated for each week of gestation. Averaged over the II2 d of gestation, mean fetal weight comes out to be 3oog, while birthweight is IX25 g. Assuming the oxygen uptake per weight to be 7 ml/min/kg, as in sheep (James et al, 1972), the total oxygen consumed during gestation is about 15 mol, that is, equivalent to an energy consumption of 7 MJ (2 kWh). For a I.z kg piglet, around zoo mmol sodium and potassium are

Physiological Aspects

x53

t r a n s f e r r e d across t h e placenta. Since, usually, ~ m m o l A T P , that is, ~ m m o l oxygen, is c o n s u m e d p e r m m o l ion t r a n s p o r t e d , the total e n e r g y r e q u i r e m e n t for placental s o d i u m a n d p o t a s s i u m t r a n s p o r t p e r piglet is a b o u t 17 m m o l , e q u i v a l e n t to 8 kJ (2 W h ) , t h a t is, a b o u t o n e t h o u s a n d t h o f the total fetal oxygen c o n s u m p t i o n d u r i n g i n t r a u t e r i n e life.

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