HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) All Versions of this Article: 289/1/H146    most recent 01284.2004v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Faber, J. Articles by Davis, L. Search for Related Content PubMed PubMed Citation Articles by Faber, J. Articles by Davis, L.

Function curve of the membranes that regulate amniotic fluid volume in sheep

¹Department of Physiology and Pharmacology, ²Department of Obstetrics and Gynecology, ³Heart Research Laboratory and ⁴Surgery, School of Medicine, Oregon Health and Sciences University, Portland, Oregon

Submitted 20 December 2004 ; accepted in final form 25 February 2005

	ABSTRACT

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION GRANTS REFERENCES

 
Seven singleton 120-day fetal lambs were prepared with a shunt from the lung to the gastric end of the esophagus, a bladder catheter, and multiple amniotic fluid and vascular catheters. The urachus was ligated. Beginning 7 days later, amniotic fluid volumes were determined by drainage, followed by replacement with 1 liter of lactated Ringer (LR) solution. Urine flow into the amnion was measured continuously. In 14 of 27 experiments, amniotic fluid volumes were determined again 2 days after the inflow into the amnion had consisted of urine only and in 13 experiments after the inflow of urine had been supplemented by an intraamniotic infusion of LR solution. Intramembranous absorption was calculated from the inflows and the changes in volume between the beginning and end of each experiment. The relations between absorption rate and amniotic fluid volume, the "function curves," were highly individual. Urine production during the infusion of LR solution did not decrease, fetal plasma renin activity decreased (P < 0.001), and amniotic fluid volume increased by 140% [SE (27%), P < 0.005], but the increase in the amniochorionic absorption rate of 411% [SE (48%), P < 0.001] was greater (P < 0.005) than the increase in volume. Each of the seven fetuses was proven capable of an average intramembranous absorption rate that exceeded 4.5 liters of amniotic fluid per day. During the infusion of LR solution, the increase in the rate of absorption matched the rate of infusion (both in ml/h), with a regression coefficient of 0.75 (P < 0.001). Thus, even for large amniotic fluid volumes, volume is not limited by the absorptive capacity of the amniochorion, and, at least in these preparations, the position of the function curve and not the natural rate of inflow was the major determinant of resting amniotic fluid volume.

fetus; polyhydramnios; amniochorion; intramembranous absorption

Production of amniotic fluid results from fetal urination and lung fluid secretion (5, 13, 16). There is good evidence that urine production and lung fluid flow do not serve to regulate amniotic fluid volume because neither lung fluid flow nor urine production properly respond to induced changes in volume (9, 11). Thus, although substances secreted in these fluids may affect volume regulation (14), whatever regulatory mechanism exists must modulate the rate of fluid elimination to adapt to changes in fluid production. Fluid elimination consists of swallowing by the fetus and of absorption of fluid by the amniochorion, the membrane that surrounds the amniotic cavity. Amniochorionic absorption of amniotic fluid ["intramembranous absorption" (7, 14)] proceeds by means of an as-yet-unresolved mechanism (7, 12). Whether swallowing serves a regulatory function is not settled (16). However, absorption by the amniochorion has been shown to serve a regulatory function because augmentation of inflow by means of experimental infusion of fluid into the amnion leads to increases in the amniochorionic absorption rate; it is also known that a large part of amniochorionic absorption occurs in the form of bulk flow (6, 11, 12).

There are numerous studies that show directly or indirectly that the regulation of amniotic fluid volume by amniochorionic absorption responds appropriately to various experimental interventions that have the potential to affect this volume (8, 11, 13–15, 18). However, the power of this regulation is unknown. For this reason, the present experiments were designed to establish the relation between the volume of amniotic fluid present at any given time and the rate at which it is absorbed. The results to be presented supported our hypothesis that the volume of amniotic fluid is for a large part independent of the fluid production rate and that the amniochorionic membrane is capable of daily absorbing volumes that are many times larger than the amniotic fluid volume itself.

	MATERIALS AND METHODS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION GRANTS REFERENCES

 
Principle of methods and animal preparation. Changes in amniotic fluid volume are the result of lung fluid production, swallowing, urine production, and amniochorionic absorption. To measure the latter, we eliminated lung fluid inflow and swallowing and measured urine production.

All surgical and experimental procedures were approved by the Institutional Animal Care and Use Committee of the Oregon Health and Sciences University. Seven time-bred pregnant ewes carrying singletons were sterilely operated at a gestational age of 120 days (range 118–122 days); term is about 147 days. The ewes were premedicated with 7.5 mg atropine, 400 mg ketamine, and 10 mg diazepam intravenously, intubated, and continued on a mixture of oxygen and nitrous oxide with sufficient halothane or isoflurane (about 1–1.5%) to maintain a surgical level of anesthesia in both the ewe and her fetus.

After exposure of the uterus, the uterine wall and amniochorion were incised at the location of the fetal head and sutured together with interrupted sutures to ensure the proper apposition of the fetal membranes at the time of closure. To permit the continuation of lung fluid production without allowing lung fluid to enter the amnion as well as to prevent swallowing, we connected the pulmonary end of the fetal trachea to the gastric end of the esophagus with a short length of polyvinyl tubing. The cranial ends of the trachea and esophagus were separately ligated. Indwelling catheters were placed in a fetal carotid artery and jugular vein. After closure of the fetal skin, a catheter of 2.5 mm internal diameter, ending in a 10-ml plastic screw top vial with multiple side holes, was attached to the skin. It served later to quickly drain all amniotic fluid for the purpose of measuring its volume, a technique adapted from the one published by Dickson and Harding (9). A smaller amniotic fluid catheter was attached also for the later measurement of amniotic fluid pressure.

After this first uterine incision had been closed with multiple interrupted sutures oversewn with a continuous suture, a similar incision was made over the fetal hindquarters. The fetal urachus was ligated. This stopped all inflow into the allantoic sac and led to the disappearance of the allantoic fluid, as described by Wlodek et al. (20). A polyvinyl catheter with a soft silicon rubber tip was placed into the fetal bladder. Intravascular catheters were placed in a tibial artery and saphenous vein, and two more large-bore drain catheters and two small amniotic fluid catheters were attached to the fetal skin at the abdomen and at a hind leg. After the fetal skin and the uterus had been closed as described, the catheters were routed underneath the maternal skin to the flank, where they emerged and were stored in a small pouch attached to the skin of the ewe. A single dose of 1 million units of penicillin G were injected into the amniotic fluid; no other antibiotics were routinely used. Vascular catheters were filled with a saline solution of 500 U heparin/ml. For 2 days after recovery from anesthesia, the ewes were given twice daily doses of 0.6 mg bupremorphine for pain prevention.

Experimental procedures. All animals were given 7–9 days for postoperative healing. For the experiments, the ewes were placed in stanchions with free access to water and food at all times. The bladder catheter was connected to a small bottle with electrodes. All urine drained into this bottle. A Gilson Minipuls-3 roller pump was used to keep the urine in the bottle at the level of the electrodes. Excess urine was pumped back into the amnion. By recording the activity of the roller pump, we obtained a record of the inflow of urine into the amnion over the entire duration of each experiment without affecting that inflow.

At the beginning of each 2-day period, all amniotic fluid was drained and replaced with 1 liter of isotonic lactated Ringer solution. At the end, all amniotic fluid was again drained, and its volume was measured and replaced with 1 liter of Ringer solution. Two protocols were used. In a "control period," urine inflow into the amnion was monitored but no interventions occurred. Because lung fluid inflow had been eliminated by the surgical procedure, the total inflow volume into the amnion consisted of the initial 1 liter of Ringer solution plus the volume of urine pumped back into the amnion over the 2-day period. The total volume absorbed, therefore, equaled this inflow volume, reduced by the volume of amniotic fluid retrieved at the end. The rate of removal of amniotic fluid was obtained by dividing the absorbed volume by the exact duration of the experiment. Because swallowing had also been eliminated, the rate of amniochorionic absorption was equal to the removal rate.

The second protocol ("infusion period") was identical with the exception that the inflow into the amnion was augmented by the infusion of isotonic Ringer solution into the amnion. These rates of infusion remained constant over the entire 2-day period. Rates from 86 to 238 ml/h (from 2,064 to 5,712 ml/day) with a mean of 164 ml/h were used in different infusion periods. Thus the total inflow in an infusion period was the sum of the initial 1 liter, the urine volume, and the volume of Ringer solution administered in this period. Five of the fetuses were tested at different infusion rates. The infusion periods were interspersed with additional control periods, during which time only the urine was infused. Thus a total of 14 control and 13 infusion experiments were performed. Control and infusion experiments were performed in no set order to randomize any effect the one might have on the other.

In addition to the measurements of amniotic fluid volume at the end of each experimental period, we measured fetal plasma renin activities, amniotic fluid pressures, fetal arterial and venous blood pressures, heart rates, arterial blood pH, PO₂, PCO₂, oxygen contents, hemoglobin concentrations, and hematocrits to monitor the well-being of the fetuses.

Materials and instrumentation. Hydrostatic pressures were measured with Abbott Transpac transducers and a Macintosh-based commercial recording system. The transducers were calibrated each day against a mercury manometer and zeroed before every measurement. Pressures are accurate to 0.5 mmHg. Intravascular pressures are reported with respect to amniotic fluid pressure. Heart rates were derived from arterial pressure pulsations.

Arterial blood pH, PCO₂, PO₂, hemoglobin concentrations, and oxygen contents were determined with an Instrumentation Laboratories IL306 and IL482 system. Plasma renin activities were analyzed as described by Binder and Anderson (4).

The Ringer solution was commercial Lactated Ringer USP with a stated composition of (in meq/l) 130 Na⁺, 4 K⁺, 110 Cl^–, 28 lactate, and 3 Ca²⁺, and an osmolality of 275 mosm/kg.

Statistical methods. All statistical analyses were done with the use of a Graph Pad Prism (Graph Pad Software; San Diego, CA) commercial software package. A level of P < 0.05 was required for statistical significance. Measures of dispersion are 1 SD.

	RESULTS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION GRANTS REFERENCES

 
Condition of the experimental fetuses. The fetuses remained in good condition, as evidenced by blood gas data obtained at the ends of every control period and every infusion period. The means ± SD values were, respectively, pH 7.346 ± 0.009 and 7.357 ± 0.019, PCO₂ 53.0 ± 2.6 and 52.6 ± 2.8 mmHg, PO₂ 19.7 ± 2.4 and 19.3 ± 1.9 mmHg, hematocrit 28.8 ± 2.9% and 28.6 ± 4.2%, hemoglobin content 97.7 ± 12.6 and 97.1 ± 11.9 g/l, and [O₂] 68.9 ± 9.0 and 68.4 ± 15.5 ml/l. Arterial blood pressures were 45 ± 3 and 43 ± 4 mmHg, venous pressures were 6.9 ± 2.0 and 5.0 ± 1.1 mmHg, and heart rates were 161 ± 12 and 162 ± 8 beats/min. None of the differences between the control and infusion data reached statistical significance by paired t-test.

Comparison of the results of control and infusion experiments. Because not every infusion period was immediately preceded by a control period to which its results could be compared, we averaged the control amniotic fluid volumes and control intramembranous absorption rates of a given animal and compared its individual infusion data with its average control. The results are shown in Fig. 1.

View larger version (22K): [in this window] [in a new window]   Fig. 1. Amniochorionic absorption rate as a function of amniotic fluid volume. The results on each of the 7 fetuses are connected by solid lines; the different symbols represent individual fetuses. The lowest point of each line is the average control point for that fetus. The dotted lines through the origin indicate the number of amniotic fluid half-lives that elapsed in the 2-day test periods. For instance, the filled triangle at the far right on the locus marked "4" represents an average absorption rate of 218 ml/h and a final volume of 5,130 ml. Because 218 ml/h amounts to an absorbed volume of 10,464 ml in 2 days, the volume absorbed during the period was about twice the final volume of 5,130 ml, or 4 half-volumes.

Urine production was not reduced and, therefore, played no regulatory role during the intraamniotic volume challenges with Ringer solution. To the contrary, urine production increased from 40.7 ± 13.4 to 52.7 ± 24.8 ml/h, although this increase was not statistically significant.

Figure 2 shows the relation between the increase in the amniochorionic absorption rate (above mean control rate) and the corresponding rate of infusion of Ringer solution. The slope of the least-squares linear regression is 0.75 (P < 0.001), and the zero infusion intercept is 27 ml/h (not significant). It highlights the precise response of the regulatory mechanism.

View larger version (12K): [in this window] [in a new window]   Fig. 2. Increase in the amniochorionic absorption rate above the mean control rate of absorption as a function of the intra-amniotic infusion rate of Ringer solution in 13 infusion periods. P < 0.001 by least-squares linear regression; r = 0.80.

At the end of intra-amniotic infusions of Ringer solution, fetal plasma renin activities were lower than at the end of control periods, decreasing from a control value of 10.6 ± 3.4 ng·ml^–1·h^–1 to a post-Ringer solution infusion value of 4.2 ± 3.1 ng·ml^–1·h^–1. This decrease was highly significant (P < 0.001). Plasma renin activities correlated with the rates of infusion, but this correlation, although statistically significant (P < 0.02), was weak, with r being only –0.50.

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION GRANTS REFERENCES

 
Effect of temporary drainage of amniotic fluid. Except in the presence of large volumes of amniotic fluid, the uterus fits snugly around the fetal lamb and the amniotic fluid volume is somewhat compartmentalized. Although these compartments communicate, there may not be rapid mixing. Perhaps for that reason, determinations of amniotic fluid volumes by tracer dilution methods, at least in our hands, have not been uniformly reliable when verified against volumes obtained at autopsy. For this reason also, it is essential to place drainage catheters at several sites and to drain from all three catheters into evacuated bottles at the time of volume measurement. We compared autopsy volumes with volumes determined by drainage in 11 animals (not all of them from the present study). The least-squares linear regression yielded a correlation coefficient of 0.994, a regression coefficient of 1.053, and an intercept of 48 ml. It should be noted that we drained fluid into sterile evacuated bottles, not by unassisted gravity, and that complete drainage is usually obtained in <30 min. However, even gravity-drained volumes correlate well with autopsy volumes (8), although they take longer to accomplish.

As could be seen from the excellent blood gas values, momentarily draining all amniotic fluid as often as every 2 days had no discernable long-term deleterious effects on the fetus. In the past, we used drainage catheters with "wiffle" balls or plastic vials with large side holes at the end (2, 3). Occasionally, one of these preparations was lost because a small loop of the flaccid umbilical cord became incarcerated through one of the holes. The use of side holes no larger than 3 mm eliminated that problem.

Fate of the absorbed fluid. Some of the volumes infused into the amnion were very large compared with the volume of the amnion or the fetus, exceeding 10 liters over the period of 2 days. In the past, we acutely infused as much as 3 liters of Evans blue-stained saline into uteri from which all fluid had been drained into evacuated bottles, following it with an immediate autopsy. No leaks have ever been found. This may be because no more than one catheter is allowed to emerge from the uterus between each pair of sutures and because the individual sutures in the uterine wall are oversewn with a continuous suture. It is likely that an adequate time for postoperative healing is also beneficial.

Direct passage of amniotic fluid to and from the maternal circulation is only barely detectable and then only under the influence of extreme osmotic gradients; under the present circumstances, it could have been of the order of only few milliliters per day (2). It may be surmised, therefore, that the fluid was absorbed first into the fetal circulation and then cleared to the maternal circulation by way of the placenta. Because fetal fluid exchange with its mother appears to be controlled by the fetal renin-angiotensin system (1, 10), we expected the steep decrease in fetal plasma renin activity after the infusions of Ringer solution. The negligible changes in fetal blood hematocrit and hemoglobin concentration after intraamniotic infusions of Ringer solution attested to the adequacy of fetal fluid control.

Function curves of the amniochorion. To interpret the results shown in Fig. 1, we kept in mind that the volumes plotted on the abscissa are the volumes that existed at the end of each 2-day period, whereas the absorption rates on the ordinate are the average absorption rates during the 2 days of each period. Ideally, one would like to see the absorption rate that existed at the moment the volume was measured and one would like to measure the amniotic fluid volumes and the amniochorionic absorption rates only after a steady state has been achieved. To our knowledge, there is no presently available technique to make such measurements.

To evaluate how well the results shown in Fig. 1 represent the steady-state relations between absorption rate and volume, we considered the following. During the experimental periods, the volumes changed from the initial volume of 1 liter to the final volume depicted in Fig. 1. Thus for those cases where the final volume was about 1 liter or a little less, the volume was close to the volume shown in Fig. 1 during the entire experimental period. Thus, for the cases at the left side of Fig. 1, the average rate of absorption on the vertical axis and the volume on the horizontal axis are good approximations for the steady-state function curve.

For those cases in which the final volume was much larger than the initial volume of 1 liter, the volumes changed during the period of the experiment from the initial 1 liter to the volume shown in Fig. 1. Because the absorption rate increases with increasing volume, it is likely that the rate of absorption initially was less than the average rate of absorption and increased as volume increased so that the rate of absorption at the end of 2 days was higher than the average rate of absorption. If this reasoning is valid, it would mean that the steepness of the function curves on the right side of Fig. 1 underestimates the steepness of the steady-state function curves.

Thus the amniotic fluid function curves shown in Fig. 1 will be close to the average steady-state characteristics for the animals whose data belong in the top left half of Fig. 1 because of the multiple amniotic fluid half-lives covered by the 2-day test periods. For the data in the bottom right half of Fig. 1, the relevance to a steady state depends on how fast the absorption rate responds to an induced change in volume. If the stimulus of the absorptive process is primarily mechanical, depending, for instance, on the stretch of the amniochorion, the response could be quite rapid. The response could be much slower if the stimulus depends on a cascade of biochemical reactions within the amniotic fluid, a cascade that could well be concentration sensitive and, therefore, volume sensitive. It should be noted that a mechanical stimulus would cause the regulation of total intrauterine volume, including the fetus, whereas a chemical stimulus would regulate amniotic fluid volume per se, a vital distinction. Previous experiments performed in our laboratory (21) support the existence of a biochemical process because isovolumic replacement of amniotic fluid with artificial fluid caused an increase in amniotic fluid volume. However, a biochemically mediated control does not preclude the concurrent operation of a mechanical process.

The maximum rates of absorption observed in these experiments were greater than those we believed possible. The largest previously published rate known to us is about 1 l/day, although this was stated to be somewhat of an underestimate (17). Each of the present seven fetuses was shown to be capable of an amniochorionic absorption rate in excess of 4.5 l/day. It should be noted that these rates may not represent the maximal possible absorption rates because we did not attempt to measure the maximum rates.

Perspective. Figure 1 shows one animal (open circles) in which a further increase in absorption was associated with a decrease in amniotic fluid volume, and another animal (filled triangles) in which two different amniotic fluid volumes were associated with almost the same absorption rates. It is possible, therefore, that the function curves of the amniochorion are not unalterable but can be modulated by other, as-yet-unknown, factors. The nature of such factors would be of considerable practical interest. However, when operating on any given function curve, the amniochorionic absorption process is capable of large changes in the rate of absorption. We conclude, therefore, that the differences between animals in the naturally occurring (control) amniotic fluid volumes were more related to differences in the individual amniochorionic function curves than to differences in naturally occurring urine production rates. Whether this conclusion remains valid in surgically unmodified preparations remains to be determined.

	GRANTS

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION GRANTS REFERENCES

 
Financial support was received from National Institutes of Health Grants HD-37376, PO1-HD-34430, and HL-45043.

	ACKNOWLEDGMENTS

 
The authors thank Julie Booth and Robert Webber for expert technical assistance.

	FOOTNOTES

 

Address for reprint requests and other correspondence: J. J. Faber, Dept. of Physiology & Pharmacology, L334, Oregon Health and Sciences Univ., Portland, OR 97239

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

	REFERENCES

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION GRANTS REFERENCES

 

1. Adamson SL, Morrow RJ, Bull SB, and Langille BL. Vasomotor responses of the umbilical circulation in fetal sheep. Am J Physiol Regul Integr Comp Physiol 256: R1056–R1062, 1989.[Abstract/Free Full Text]
2. Anderson DF, Borst NJP, Boyd RDH, and Faber JJ. Filtration of water from mother to conceptus via paths independent of fetal placental circulation in sheep. J Physiol 431: 1–10, 1990.[Abstract/Free Full Text]
3. Anderson DF, Faber JJ, and Parks CM. Extra-placental transfer of water in the sheep. J Physiol 406: 75–84, 1988.[Abstract/Free Full Text]
4. Binder ND and Anderson DF. Plasma renin activity responses to graded decreases in renal perfusion pressure in fetal and newborn lambs. Am J Physiol Regul Integr Comp Physiol 262: R524–R529, 1992.[Abstract/Free Full Text]
5. Brace RA. Fetal blood volume, urine flow, swallowing and amniotic fluid volume responses to long-term intravascular infusions of saline. Am J Obstet Gynecol 161:1049–1054, 1989.[ISI][Medline]
6. Brace RA and Huijssoon E. Regulation of amniotic fluid volume: intramembranous solute and volume fluxes in late gestation fetal sheep. Am J Obstet Gynecol 191: 837–846, 2004.[CrossRef][ISI][Medline]
7. Cheung CY. Vascular endothelial growth factor activation of intramembranous absorption: a critical pathway for amniotic fluid regulation. J Soc Gynecol Investig 11: 63–74, 2004.[ISI][Medline]
8. Cock ML and Harding R. Renal and amniotic fluid responses to umbilicoplacental embolization for 20 days in fetal sheep. Am J Physiol Regul Integr Comp Physiol 273: R1094–R1102, 1997.[Abstract/Free Full Text]
9. Dickson KA and Harding R. Decline in lung volume and secretion rate during oligohydramnios in sheep. J Appl Physiol 67: 2401–2407, 1989.[Abstract/Free Full Text]
10. Faber JJ and Anderson DF. Angiotensin mediated interaction of fetal kidney and placenta in the control of fetal arterial pressure and its role in hydrops fetalis. Placenta 18: 313–326, 1997.[ISI][Medline]
11. Faber JJ and Anderson DF. Regulatory response of intramembranous absorption of amniotic fluid to infusion of exogenous fluid in sheep. Am J Physiol Regul Integr Comp Physiol 277: R236–R242, 1999.[Abstract/Free Full Text]
12. Faber JJ and Anderson DF. Absorption of amniotic fluid by amniochorion in sheep. Am J Physiol Heart Circ Physiol 282: H850–H854, 2002.[Abstract/Free Full Text]
13. Mann SE, Nijland MJM, and Ross MG. Ovine fetal adaptations to chronically reduced urine flow: preservation of amniotic fluid volume. J Appl Physiol 81:2588–2594, 1996.[Abstract/Free Full Text]
14. Matsumoto LC, Cheung CY, and Brace RA. Effect of esophageal ligation on amniotic fluid volume and urinary flow rate in fetal sheep. Am J Obstet Gynecol 182: 699–705, 2000.[CrossRef][ISI][Medline]
15. Matsumoto LC, Cheung CY, and Brace RA. Increased urinary flow without development of polyhydramnios in response to prolonged hypoxia in the ovine fetus. Am J Obstet Gynecol 184: 1008–1014, 2001.[CrossRef][ISI][Medline]
16. Ross MG and Nijland MJM. Fetal swallowing: relation to amniotic fluid regulation. Clin Obstet Gynecol 40: 352–365, 1997.[CrossRef][ISI][Medline]
17. Thurlow RW and Brace RA. Swallowing, urine flow, and amniotic fluid volume responses to prolonged hypoxia in the ovine fetus. Am J Obstet Gynecol 189: 601–608, 2003.[CrossRef][ISI][Medline]
18. Tomoda S, Brace RA, and Longo LD. Amniotic fluid regulation: basal volumes and responses to fluid infusion in sheep. Am J Physiol Regul Integr Comp Physiol 252: R380–R387, 1987.[Abstract/Free Full Text]
19. Wlodek ME, Challis JRG, and Patrick J. Urethral and urachal urine output to the amniotic and allantoic sacs in fetal sheep. J Dev Physiol 10: 309–319, l988.
20. Wlodek ME, Harding R, and Thorburn GD. Fetal-maternal fluid and electrolyte relations during chronic fetal urine loss in sheep. Am J Physiol Renal Fluid Electrolyte Physiol 263: F671–F679, 1992.[Abstract/Free Full Text]
21. Yang Q, Davis L, Hohimer A, Faber J, and Anderson D. Regulatory response to washout of amniotic fluid in sheep. Am J Physiol Heart Circ Physiol 288: H1339–H1343, 2005.[Abstract/Free Full Text]

This article has been cited by other articles:

				C. Y. Cheung and R. A. Brace Unidirectional Transport Across Cultured Ovine Amniotic Epithelial Cell Monolayer Reproductive Sciences, December 1, 2008; 15(10): 1054 - 1058. [Abstract] [PDF]

This Article Abstract Full Text (PDF) All Versions of this Article: 289/1/H146    most recent 01284.2004v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Faber, J. Articles by Davis, L. Search for Related Content PubMed PubMed Citation Articles by Faber, J. Articles by Davis, L.