Dutch belted rabbits were given single intravenous injections of 100 or 200 mg/kg doses of bovine serum albumin (BSA). BSA in serum and uterine fluid at various times after injection was estimated by a quantitative radial immunodiffusion test, which could measure a minimum of 40 ng. The presence of BSA in uterine fluid was confirmed by immuno-electrophoresis and double diffusion in agar.

BSA passes readily into uterine fluid of non-pregnant rabbits, reaching a peak at 12 h after injection, when its concentration is 7–15 % of that in serum. About 72 h seems to be required for equilibration of BSA between serum and uterine fluid, at which time the concentration in the former is about 5 times that in the latter. The kinetics of the process is discussed. Compared to the above, passage of BSA into uterine fluid of pregnant rabbits (5–7 days post coitum) is restricted in the following ways. Significant amounts of BSA appear in the fluid only after a maternal dose of 200 mg/kg. BSA in uterine fluid reaches a peak at 24 h after injection, when it is only 4·5 % of the serum level. The permeability rate seems to decrease with early gestation.

Approximate rates of entry of BSA into uterine lumen of non-pregnant and pregnant rabbits are 0·4 and 0·25 μg/h. BSA seems to be treated like rabbit albumin in its passage across the uterine epithelium. There is no evidence of selection between these proteins.

In most mammals, proteins from the mother enter the fetus in utero or the neonate via colostrum and milk (Brambell, 1970). Intra-uterine transmission has been studied mostly in the second half of gestation and it was thought that proteins passed directly in the placenta until Brambell et al. (1949) discovered that antibodies take an indirect route through the uterine fluid and yolk sac splanchnopleur, in the rabbit. This route was confirmed for non-antibody proteins by Kulangara (1958). In other species, proteins may pass via chorionic villi (Bangham, Hobbs & Terry, 1958; Kulangara, Krishna Menon & Willmott, 1965), without involvement of the uterine fluid. Before implantation, however, molecules from the mother have to enter the luminal fluid first, before they can enter the segmenting egg in the oviduct or the blastocyst in the uterus. During these stages, passage into all mammalian embryos must occur in two distinct steps, namely from the circulation into luminal fluid and from this fluid into the developing embryo. It has not been generally recognized that these two processes may be quite different and that their kinetics have to be studied for a proper understanding of overall passage.

Lutwak-Mann, Boursnell & Bennett (1960) detected ions in rabbit uterine fluid shortly after their injection into the mother. Marley & Robson (1971) demonstrated the passage of Na into perfusates of rat uterus. Others have studied overall passage of maternally introduced proteins into blastocysts (Brambell, Hemmings & Rowlands, 1948; Smith & Schechtman, 1962; Glass, 1963) but only Glass detected them in preimplantation stages. It is quite important to know what levels of substances (antibiotics, contraceptives, anti-bodies, etc.) administered to the mother are obtained in uterine and blastocyst fluids and for how long, since the early developmental stages seem to be more susceptible to chemical damage than later fetal stages (Gottschewski, 1964; Clegg, 1971). Such information may also shed light on the maximum reproductive loss, which surrounds implantation (Brambell, 1948; Frazer, 1955; Hertig, Rock, Adams & Menkin, 1959).

The paucity of quantitative data is another major gap in the literature on passage of proteins. Most of the results are reported in titers. Although amounts of protein have been derived from them, the uncertainty of at least one dilution in determining the end point makes such data at best semi-quantitative. Use of radioactive isotopes has provided some quantitative data (DuPan et al. 1959; Dancis et al. 1961; Kulangara & Schjeide, 1962; Gitlin&Koch, 1968;,Sonoda & Schlamowitz, 1972), but they were all obtained from fetal stages.

A quantitative study of the passage of bovine serum albumin into the uterine fluid and into unimplanted rabbit blastocysts was therefore undertaken. The results are reported in two papers, this one on passage into uterine fluid of non-pregnant and pregnant rabbits and the following one on passage into the blastocyst during 5–7 days post coitum (p.c.).

Dutch belted rabbits (l·8–3·0kg body weight) were obtained from commercial sources and housed in separate cages for about 2 weeks before use.

An approximately 15 % solution of bovine serum albumin (BSA), purchased from Mann Laboratories, was made up using 0·9 % NaCl. The solution was filtered through a Millipore filter, its protein concentration estimated by the biuret test (Gornall, Bardawill & David, 1949) and it was frozen in 5 ml lots for storage. The rabbits were given single intravenous injections of appropriate volumes of the solution to provide doses of 100 or 200 mg BSA/kg body weight. Blood was sampled 5 min later and blood and uterine fluid were obtained at various times after injection (Tables 1, 2).

Table 1.

Concentration of bovine serum albumin (BSA) in serum and uterine fluid at various times after intravenous injection of non-pregnant rabbits

Concentration of bovine serum albumin (BSA) in serum and uterine fluid at various times after intravenous injection of non-pregnant rabbits
Concentration of bovine serum albumin (BSA) in serum and uterine fluid at various times after intravenous injection of non-pregnant rabbits
Table 2.

Concentration of bovine serum albumin (BSA) in serum and uterine fluid at various times after intravenous injection of pregnant rabbits at 5 days post coitum

Concentration of bovine serum albumin (BSA) in serum and uterine fluid at various times after intravenous injection of pregnant rabbits at 5 days post coitum
Concentration of bovine serum albumin (BSA) in serum and uterine fluid at various times after intravenous injection of pregnant rabbits at 5 days post coitum

Collection of uterine fluid

Two methods were used to collect uterine fluid. The first one involved rinsing the uterine lumen with a known volume of 0·9 % NaCl and collecting the rinse at the cervix as previously described (Kulangara, 1972). Luminal BSA con-centrations were calculated using the mean uterine fluid volume reported in that paper. In spite of the large variability of uterine fluid volumes, results obtained from such rinses were in general agreement with those from undiluted uterine fluid, collected as follows. The second method, used in experiments reported here, consisted of direct aspiration with a thick-walled glass capillary tube. The rabbit under anesthesia was opened midventrally and the vaginal wall slit longitudinally to expose the cervices. Each cervix was mopped free of fluid or rinsed with saline and mopped. The glass tube (0·8 mm internal and 1·7 mm external diameter) was coated on the outside with mineral oil and carefully inserted through the cervix to the anterior end of the horn. The tube was slowly withdrawn, while suction was exerted through a plastic tube and mouthpiece. Mineral oil was applied to the outside of the uterine horn, which was gently manipulated during collection. Columns of uterine fluid so obtained were usually free of contamination. The fluid was examined under a dissecting microscope for red blood cells and contaminated samples were discarded.

Estimation of BSA

The concentration of BSA in uterine fluid and rabbit serum was estimated using a rabbit antiserum against BSA in the radial immunodiffusion test. A modification of Fahey & McKelvey’s (1965) method was used, which employed a thin layer of agar on 3 ×1 in. (7·6 ×2·5 cm) slides. Two μl each of 20, 50 and 80 μg/ml standard solutions of BSA and duplicate aliquots of a sample were spotted in five wells on each slide. The test system was checked in the following ways.

  1. Uterine fluid and serum from normal rabbits were used to detect non-specific reactions; none were detectable.

  2. Solutions of known BSA concentration were used to check reproduci-bility and position effects of the wells.

  3. Co-precipitation was examined and corrected for as follows. Known concentrations of BSA in saline were compared with the same concentrations in normal rabbit serum and 1/10 and 1/25 dilutions of it. The diameter of precipitin rings differed by about 10–15% and therefore the standards were routinely made up in rabbit serum dilutions of approximately the same total protein concentration as the sample to be tested.

  4. Aspirated samples of uterine fluid were often only a few μl and obtaining their supernatant after centrifugation involved losses. Since the samples had cells and other debris, the effect of such particulates on the test was studied. Such material obtained from oral washing was added to known concentrations of BSA. These mixtures gave precipitin rings not significantly different from expectation.

The test finally adopted required only 2 μl of the sample and could measure a minimum of 40 ng of BSA with 3–4 % error. However, the minimum concentration of BSA that could be accurately determined was 20μg/ml. More dilute samples also gave precipitin rings, but since results calculated from them showed more than 3–4% error such samples are recorded hereafter as < 20 μg/ml.

Passage into uterine fluid of non-pregnant rabbits

Concentrations of BSA in the serum and uterine fluid at various times after an intravenous injection of 100 or 200 mg/kg doses are given in Table 1 and Fig. 1. BSA is cleared from the vascular compartment at semilogarithmic rates; a rapid rate until about 12 h, when 50 % of the 5 min level is reached and at a slower rate after that. BSA is readily measurable in uterine fluid at 4 h after injection and its concentration continues to rise until it reaches a peak at 12 h and then declines. This is confirmed with both 100 and 200 mg/kg doses. The peak values in uterine fluid are 6·8 % and 15·3 % of the serum level after injection of 100 and 200 mg/kg. A rough idea of the rate of passage may be obtained from the 4 and 6 h points on the curve (Fig. 1). About 0·2 and 0·4 μg of BSA enter the uterine fluid per hour with 100 and 200 mg/kg doses, respectively. The kinetics of passage was followed up to 96 h after injection of 100 mg/kg. Two other peaks at 30 and 72 h were recorded. At 72 h after injection BSA concentration in uterine fluid is 20 % of that in serum. These results are discussed later.

Fig. 1.

BSA concentration in serum and uterine fluid (mean ± standard error) of non-pregnant (non-preg.) and pregnant (preg.) rabbits at various times after intravenous injection of 100 or 200 mg/kg doses. Pregnant rabbits injected at 5 days post coitum. Data from individual rabbits normalized to the mean serum concentration at 5 min after injection. The serum curve (upper) applies to pregnant and non-pregnant rabbits.

Fig. 1.

BSA concentration in serum and uterine fluid (mean ± standard error) of non-pregnant (non-preg.) and pregnant (preg.) rabbits at various times after intravenous injection of 100 or 200 mg/kg doses. Pregnant rabbits injected at 5 days post coitum. Data from individual rabbits normalized to the mean serum concentration at 5 min after injection. The serum curve (upper) applies to pregnant and non-pregnant rabbits.

Passage into uterine fluid of pregnant rabbits

Mated Dutch belted rabbits were given injections of 100 or 200 mg/kg doses of BSA at 5 daysp.c. After a maternal dose of 100 mg/kg, very little BSA appears in the uterine fluid up to 48 h (Table 2). It may be noted that out of seven samples, five were negative or < 20 μg/ml, one had 30 μg/ml and the other (59 μg/ml) was from the empty horn of a unilaterally pregnant rabbit. After the mother was given 200 mg/kg, greater amounts of BSA were present in uterine fluid. However, its concentration rises more slowly than in non-pregnant rabbits, reaching a peak at 24 h instead of at 12 h (Fig. 1) and declining thereafter. The peak value is 4·5 % of maternal serum concentration. Thus passage into uterine fluid of pregnant rabbits is restricted in the time it takes to reach the peak value as well as the percentage of serum BSA present in uterine fluid at the peak. Approximately 0·25 μg BSA enters the uterine lumen per hour after a dose of 200 mg/kg.

Confirmation of BSA in uterine fluid

The identity of BSA in uterine fluid was confirmed by immunoelectrophoresis of samples from injected non-pregnant (Fig. 2) and pregnant rabbits. A sheep antiserum against normal rabbit serum was also used to distinguish rabbit proteins in uterine fluid from the arc due to BSA. These results were confirmed by Ouchterlony type double diffusion in agar.

Fig. 2.

Immunoelectrophoretic pattern of uterine fluids from normal and injected (given 200 mg/kg BSA 16 h before collection) non-pregnant rabbits. (a) Rabbit antiserum against BSA in both troughs. Upper well, normal uterine fluid with BSA added. Middle well, uterine fluid from injected rabbit. Lower well, normal uterine fluid. (b) Sheep antiserum against normal rabbit serum in trough. Upper well, normal uterine fluid with BSA added. Lower well, normal uterine fluid. There is some distortion of these bands, due to overflow from the trough.

Fig. 2.

Immunoelectrophoretic pattern of uterine fluids from normal and injected (given 200 mg/kg BSA 16 h before collection) non-pregnant rabbits. (a) Rabbit antiserum against BSA in both troughs. Upper well, normal uterine fluid with BSA added. Middle well, uterine fluid from injected rabbit. Lower well, normal uterine fluid. (b) Sheep antiserum against normal rabbit serum in trough. Upper well, normal uterine fluid with BSA added. Lower well, normal uterine fluid. There is some distortion of these bands, due to overflow from the trough.

The experiments described above clearly establish that molecules, antigenically and immunoelectrophoretically indistinguishable from BSA, appear in uterine fluid after their intravenous injection into non-pregnant and pregnant rabbits. Titers of maternally injected antibodies (Brambell et al. 1949) and heterologous serum proteins (Kulangara & Schechtman, 1962) in uterine fluid, at later stages of gestation, have been reported before. Passage is also suggested by the evidence that most of the proteins in uterine fluid seem to be plasma proteins (Albers & Castro, 1961). Stevens, Hafs & Hunter (1964) observed 13 components in fluid from ligated rabbit uteri, only three of which were absent from serum.

This study provides the first quantitative data on passage of proteins into the uterine fluid. The data present peak levels and the time taken to reach them and also give an approximate idea of the rate. BSA passes rapidly into uterine fluid of non-pregnant rabbits, reaching a peak at 12 h, when the concentration is 7–15 % of that in serum. Passage in early pregnancy requires a higher maternal dose and is slower, the peak concentration being reached at 24 h, when it is 4·5 % of the maternal serum level. This twofold restriction on passage in pregnant rabbits may be due to the larger volume (Kulangara, 1972) and greater viscosity of their uterine fluid. Fluid from non-pregnant rabbits has been reported as thin and clear (Lutwak-Mann, 1962), whereas uterine contents in early pregnancy have been invariably described as viscous (Lutwak-Mann et al. 1960; Schwick, 1965; Beier, 1970). A film of viscous fluid on the endometrial surface would slow diffusion of large molecules. However, the differences in peak levels and rates indicate that there is a true decrease in transmural permeability with pregnancy. Passage of PO4 into rabbit uterine fluid has been shown to decrease from 3 to 6–7 days p.c. (Lutwak-Mann et al. 1960).

Comparison of similar proteins in uterine fluid and plasma indicates that a difference in concentration is maintained between these fluids. Uterine fluid of non-pregnant rabbits has 14·5 mg of total protein per ml (Kulangara, 1972), most of which appear to be plasma proteins (Stevens et al. 1964). This is about 23 % of the total protein concentration of plasma (62 mg/ml, Altman & Dittmer, 1971). In rabbits pregnant for 6 days there is 75 ± 13 mg of protein per ml of uterine fluid, most of which is locally secreted but some have been shown to be plasma proteins by immunoelectrophoresis (1·2–1·7% gamma globulin, Schwick, 1965; 13 % albumin, Beier, 1970). It may be calculated that these concentrations are 18 and 24 % of the plasma level, assuming that rabbit plasma contains 10 % gamma globulin and 65 % albumin. Therefore in non-pregnant and pregnant rabbits, the uterine fluid/plasma ratio is about 1/5 (18–24 %) for plasma protein concentrations at equilibrium.

A difference in concentration of a substance can be maintained between two compartments, in equilibrium and separated by a permeable membrane, only if (1) there is net transport of the substance in one direction across the membrane, or (2) there is continuous or periodic loss from one compartment, either by breakdown in it or by efflux into a third space. There is no evidence for net transport of protein from the uterine lumen to plasma and breakdown of protein in the uterine lumen appears to be negligible (Hemmings, 1958). However, there may be loss of fluid via the vagina. Long & Evans (1922) recorded discharge of uterine fluid through the vagina at late estrus in the rat.

Estimates of BSA at any one time show great variation (Fig. 1). In spite of this, the concentration in uterine fluid of non-pregnant rabbits shows three peaks at 12, 30 and 72 h, with troughs in between (Table 1). These fluctuations may be due to variability among rabbits, such as different lengths of the uterine horn. Even after normalizing values from different rabbits, there is a collective trend which suggests that the BSA concentration in uterine fluid rises and falls. These fluctuations may be due to either (1) the uterine fluid volume being constant in any one rabbit, but very different in different rabbits, or (2) a cyclical change in the uterine fluid volume of each rabbit, the volume going from 1 to 2 vols in about 6–12 h and from 2 to 1 vol. in the next similar period, and so on. Further experiments are necessary to distinguish between these alternatives.

Oviduct fluid will enter the rabbit uterus when the oviduct is ligated (Hafez, 1963) and the sheep uterus without any ligation (Belve & McDonald, 1968). Influx of oviduct fluid, which in the rabbit has 2–3 mg of protein per ml, would lower the concentration in uterine lumen. The troughs in the BSA curve, discussed above, suggest such influxes. In an earlier study (Kulangara, 1972) rabbit uterine horns were found to fall into two groups, one with a lower volume of fluid of higher protein concentration and another with about double the volume of fluid with half the protein concentration, which is consistent with the view that uterine fluid in non-pregnant rabbits undergoes cyclical changes in volume and concentration.

It was shown above that the equilibrium concentration of plasma proteins in uterine fluid is about a fifth of the plasma level. A tracer such as BSA would be expected to reach this value at equilibrium, unless it is treated very differently from rabbit albumin. In non-pregnant rabbits, BSA in uterine fluid reaches 20% of the serum concentration at 72 h after injection (Table 1), and then declines. This interval of 3 days seems long, compared to about 12 h, in which equilibrium is reached between rabbit plasma and extra vascular fluid. However, if the uterine fluid volume changes cyclically, involving losses into the vagina, equilibration may take a long time. The results also indicate that BSA in uterine fluid does reach the equilibrium value for rabbit albumin (20 %). Therefore, the two albumins seem to be treated similarly during passage. There does not appear to be any selection between native and foreign protein.

The maintenance in uterine fluid of proteins derived from plasma at a fifth of the plasma level may be considered as a maternal protective device, since it would reduce the concentration of toxins and deleterious antibodies in the embryonic environment. It would be interesting to know whether smaller molecules which are embryotoxic or teratogenic are also similarly restricted from entering the uterine lumen. On the other hand, if such restriction applies to drugs which are supposed to act in the uterine lumen or on the blastocyst, intravenous administration of these compounds is a wasteful overloading of the maternal organism. Intra-uterine injection would be more rational and perhaps less dangerous to the mother. Passage of small amounts of [131I]gamma globulin from the uterine lumen to plasma in 24-day-pregnant rabbits has been reported (Hemmings, 1958). However, considerable amounts would have to be passed this way in order to obtain even small concentrations in the plasma, due to its large volume. We have found that, although one third to half the amount of BSA injected into the uterine lumen at 5 days p.c. entered maternal plasma in 24 h, the concentration in plasma was only 20–27 μg/ml (Kulangara & Crutchfield, 1973).

This study was supported by a grant from the Lalor Foundation. One of us (F. L. C.) was the recipient of a Predoctoral Fellowship from the National Institutes of Health.

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