Thompson & Pickett, 1976). During the transport the composition of the fluid in
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1 J. Phy"iol. (1983), 336, pp With 6 text-flgure8 Printed in Great Britain MOVEMENTS OF THE LUMINAL CONTENTS IN TWO DIFFERENT REGIONS QF THE CAPUT EPIDIDYMIDIS OF THE RAT IN VITRO BY ULLA-MARJUT JAAKKOLA AND ANTTI TALO From the Laboratory of Animal Physiology, Department of Biology, University of Turklu, Turku 50, Finland (Received 4 January 1982) SUMMARY 1. Transport of the epididymal contents was studied in vitro by filming, for h, the movements of tiny, stained oil droplets injected through a micropipette into two regions of the lumen of the caput epididymidis: the most proximal part, with the widest outer diameter (region I), and the neighboring, narrowest portion (region II). 2. The movements of the oil droplets were pendular. Displacement, caused by a contraction of the wall spreading in either direction, was followed by a shorter, usually passive reflux leading to a small net displacement, Al. 3. The distance of transport during 5 min periods varied between 009 and 16B79 mm (median 1-0 mm) in region I and 0 05 and 3-62 mm (median 0-42 mm) in region II. Transport divided into periods when little or no net transport took place (slow transport) and periods when the transport was effective (fast transport). Although the periods of fast transport were infrequent, their significance in transport towards the ductus deferens was high. 4. During 5 min sampling periods of fast transport, the pendular movements were longer in both regions: Al was longer in region I and the probability of Al being in the direction of transport was higher than during slow transport in both regions. 5. The mean probability of Al being in the direction of the ductus deferens was 0-63 in region I and 0 57 in region II. 6. Higher frequency ofpendular movements, longer Al values and higher probability of Al being towards the ductus deferens in region I than II suggest that the transport speed is higher in region I than II. 7. Transport consisting of short steps occurring with variable probabilities in both directions is a stochastic process. INTRODUCTION Transport of spermatozoa through the rat epididymis, which consists of about 3-5 m of densely packed convoluted duct, takes about 8 days (Amann, Johnson, Thompson & Pickett, 1976). During the transport the composition of the fluid in which the spermatozoa are suspended changes in its ionic and macromolecular composition (Turner, Hartman & Howards, 1977; Purvis & Hansson, 1978; Jones, Pholpramool, Setchell & Brown, 1981; Setchell & Hinton, 1981). Maturation of
2 454 U-M. JAAKKOLA AND A. TALO spermatozoa taking place during the transport is assumed to be related to the changes in fluid composition. The maturation is completed when spermatozoa have passed the caput or/and corpus epididymidis (Bedford, 1966; Orgebin-Crist, 1967); in the rat this takes 3-4 days (Amann et al. 1976). The mature spermatozoa accumulate in the most distal part of the cauda epididymidis. Contractile activity of the smooth muscle lining the ductus epididymis appears to be the main source of propulsion. Although fluid transport from the testis is constant (Setchell, 1978), effective fluid uptake takes place in the ductuli efferentes and proximal ductus epididymis (Crabo, 1965), thus presumably eliminating fluid flow from the testis to the ductus deferens through the epididymis. Although there are differences in intralumninal pressure between the ductus seminiferous and epididymis and between different parts of the epididymis (Johnson & Howards, 1976), they may not be the only factors involved in transport, since when the duct is blocked by ligation transport takes place distal to the ligature (Macmillan & Aukland, 1960). Only recently have efforts been made to analyse the electrical and contractile activity of the ductus epididymis. In the most distal part of the epididymis, electrical activity may spread over several centimetres, while in the other regions the distance of spread may be very limited (Talo, Jaakkola & Markkula-Viitanen, 1979). In the cauda epididymidis, spread of electrical activity is associated with movements of the luminal contents (Jaakkola & Talo, 1982). In the caput epididymidis, the exact range and variation of spread of electrical activity have not been determined accurately, because the wall is so thin that the electrodes may interfere with the normal function of the smooth muscle, and the area which can be studied by a set of electrodes is too small to monitor the spread of contractions over a long period of time. In the present study we have analysed movements of oil droplets injected through a micropipette into the proximal caput, without recording electrical activity of the wall, in two regions differing in the frequency of muscular activity and in outer diameter. METHODS Ten male Sprague-Dawley rats were killed by decapitation, under ether anaesthesia. The testis, epididymis and a short portion of the ductus deferens were removed quickly and kept in modified Ringersolution(154 mm-naci,5 6 mm-kci,0 12 mm-mgcl2,2 2 mm-cacl2, 59 mm-nahco3,,25 mmglucose; ph 7 2) at room temperature (22 0C) and oxygenated (95% 02,5% C02). Fat and connective tissue lining the epididymis were removed under a dissection microscope. In five experiments, a portion about 3-4 cm long of region I was uncoiled and the same procedure was repeated in another five experiments for region II. Region I consisted of the most proximal part of the caput epididymidis, wider in outer diameter and about 20 cm long; region II consisted of the next and narrowest portion of the caput epididymidis, about 80 cm long. These two regions differ in the frequency of their muscular activity (Talo et al. 1979). Paraffin oil droplets stained with Sudan Black were injected into the uncoiled region through a bevelled microcapillary (Hinton & Setchell, 1978). The tissue was then placed in a water-jacketed chamber containing modified Ringer solution that was slowly exchanging and kept by a thermostat at a temperature of C. The movements of the oil droplets were filmed through a microscope (Wild M5) with a video camera (Philips) and stored on a video cassette-recorder (Sony, Betamax C7E). The total duration of the observations was 215 min in region I and 660 min in region II. In region I, the pendular movements of the oil droplets were analysed during six 5 min periods taken randomly from those showing slow transport and another six 5 min periods, taken randomly from those showing fast transport. Correspondingly, in region II, the pendular movements of the
3 MOVEMENTS OF THE EPIDID YMAL CONTENTS oil droplets were analysed during ten slow and ten fast net transport periods, and the location of the droplets was also determined at 5 min intervals. The pendular movements could begin with a movement in either direction. The first swing of the movement was associated with spread of contraction. This active phase was followed by passive reflux backwards. Sometimes the reflux was partly active, being enhanced by a separate contraction spreading in the opposite direction. Since the active component could not be measured, however, DD 455 E T min Fig. 1. Transport of an oil droplet measured at 5 min intervals in region IL of the caput epididymidis. The points of measurement are connected by straight lines. On the ordinate DD indicates direction towards the ductus deferens, T towards the testis. we ignored it. The length of the pendular movements towards the ductus deferens (Ia) and towards the testis (It) was measured to the nearest 0 5 cm on the TV screen (corresponding to 20,um in the duct), as was the net distance (Al) which the oil droplets moved during one pendular movement either towards the ductus deferens (Ald) or towards the testis (Alt). Lengths of Id and It were grouped separately, not taking into account whether they were active movements associated with spread of contraction or passive reflux. During each pendular movement the starting point, the point where the direction changed, and the end-point were determined, and the velocity of the droplet between them was assumed to be constant. This is seen as a linear movement of the droplet in the illustrations. Although this is technically inaccurate it does not affect the speed of transport. The results were tested with Mann-Whitney U test, Student's t test and regression analysis.
4 456 U-M. JAAKKOLA AND A. TALO RESULTS Transport of an oil droplet in the caput epididymidis consists of periods when little or no net transport takes place in spite of continuous back and forth movements (slow transport) and of periods when the droplet is transported in either direction (fast transport). Both types are seen in Fig. 1, in which the positions of an oil droplet at intervals of 5 min are marked. The initial period of fast transport towards the testis DD E T min Fig. 2. Pendular movements of the oil droplet during the first 5 min period of Fig. 1. The jumps are drawn as straight lines (DD, towards the ductus deferens; T, towards the testis) without taking into account the variation of the velocity during the jumps. There was no reflux at two instances shown by arrows. and the next two towards the ductus deferens were separated by periods of slow transport. The number of periods of fast transport was too low, one or two in most cases, for reliable estimation of their frequency of occurrence, their duration or the distance of transport during them. Therefore we analysed pendular movements during sample periods of 5 min to find out in which respects the periods of slow and fast transport differ. A period of 5 min contains twenty-five to forty pendular movements and is only a small part of the total duration of slow and fast periods of transport in most cases. Selection of the periods was essentially random but was made after the transport was divided into fast and slow transport. Thus some of the 5 min periods classified as fast transport also included intervals of slow transport and vice versa (Fig. 2). This diminished the statistical difference between parameters but was unavoidable due to the sampling procedure. It can be seen in Fig. 1 that the distance which the droplet moved is not the same during successive 5 min periods. It varied between 009 and mm (median 1 00 mm) in region I and 0 05 and 3-62 mm (median 042 mm) in region II. The highest incidence of occurrence was in the range below 1 mm and only a few distances were greater than 2 mm in region II (Fig. 3). However, the contribution to the net
5 MO VEMENTS OF THE EPIDID YMAL CONTENTS transport of the few cases of long-distance movement was as shown in Fig. 3B, relatively large, when no distinction was made between the directions of the transport, and even larger when transport only in the direction of the ductus deferens was considered. The longest distance of transport in a single class was in the class '49 mm. The 5 min periods during which the transport distance was greater n A mm B o mm mm Fig. 3. A, histogram of net transport distances in a 5 min period in both directions in region II. The data are from ten ducts during a total of 660 min. B, contribution to the transport distance of every class from the histogram in A, in either direction (open columns) and towards the ductus deferens (hatched columns: obtained by subtracting the transport towards the testis from the transport towards the ductus deferens in every class). than 1-5 mm represent only 11I6 % of the transport time but about 50 % of the transport distance. Pendular movements of an oil droplet during a 5 min period are shown in Fig. 2. This is the first 5 min of the period shown in Fig. 1. During the first 2-5 min transport was rapid, primarily because the reflux during the pendular movements was much shorter than the initial movement towards the testis. In two instances, shown by arrows, there was no reflux at all. Movements during the second half of the 5 min period illustrated are typical of slow transport. The movements are shorter than they were during the first 2-5 min and the droplet returned almost to its initial position during each pendular movement. Due to the sampling procedure the whole 5 min period was classified as a period of fast transport. When analyzing the pendular movements during 5 min periods, we found that their frequency remained the same during the periods of slow and fast transport. The mean frequency was min- (X+S.E.M.) in region I and min' in region II. The pendular movements were longer (z = 6-733, P < 0-001) in region I (median 0-26 mm) than in region II (median 0-15 mm) during the periods of slow transport and also during the periods of fast transport (z = , P < 0001), when the median was 0-50 mm in region I and 0-26 mm in region II. When the pendular movements were grouped according to their direction and distance, the distributions in both directions were similar during periods of slow transport in both regions and
6 458 U-M. JAAKKOLA AND A. TALO during periods of fast transport in region II (Fig. 4). In region I, however, during periods of fast transport the movements towards the ductus deferens (median 0-65 mm) were longer (z = 4-736, P < 0001) than those towards the testis (median 0'46 mm) (Fig. 4B). In region I, the pendular movements were longer during the periods of fast transport than during slow transport towards the testis (z = 10'127, A B n 202 n203 n= 177 n =187 C D 50 n264 j ~ mm mm Fig. 4. Histograms of the relative frequency of the lengths of the movements towards the ductus deferens (stippled columns) and towards the testis (open columns) during slow transport (A) and fast transport (B) in region I, and similarly in region II (C and D respectively). P < 0-001), towards the ductus deferens (z = , P < 0-001), and when both directions were grouped together (z = , P < 0-001) (Fig. 4A, B). In region II the movements were longer during fast than slow transport towards the testis (z = 34147, P < 0-01), towards the ductus deferens (z = 4*903, P < 0-001) and also when movements in both directions were combined (z = 5-711, P < 0-001) (Fig. 4C, D). Lengths of the net movements, Al, were distributed similarly to the lengths of the pendular movements in both regions (Fig. 5). During periods of slow transport the lengths of Al were similar in regions I (median 0-1I mm) and II (median 0-13 mm) (Fig. 5A, C), whereas during periods of fast transport Al lengths were longer (z = 8-557, P < 0001) in region I (median 0-26 mm) than in region II (median 0-12 mm) (Fig. 5B, D). The distributions of the lengths of Al were similar towards the testis and ductus deferens during periods of slow transport in both regions and during periods of fast transport in region II. During periods of fast transport in region I the net distances were longer (z = 2-385, P < 0 05) towards the ductus deferens
7 MOVEMENTS OF THE EPIDID YMAL CONTENTS 459 (median 0 30 mm) than towards the testis (median 0-17 mm). In region I the net distances were longer during fast than slow transport towards the testis (z = 2-518, P < 0 05), towards the ductus deferens (z = 4-265, P < 0 001), and also when the values in both directions were combined (z = 6-212, P < 0-001), but in region II there was no difference between the slow and fast transport periods. A B 50 ~~~~~~~~~~50 n n135 C D n88 95 n88 n mm mm Fig. 5. Histograms of the relative frequency of the lengths of Al towards the ductus deferens (stippled columns) and towards the testis (open columns) during slow (A) and fast (B) transport in region I, and in region II (C and D respectively). The transport of an oil droplet consists of the sum of the net movements, Al. Since the net movements take place in both directions, the distance of transport is determined not only by the frequency and length of Al values but also by the probability of individual net movements taking place in the same direction during the time interval. During the 5 min periods analysed, in eight cases out of twelve in region I and in eleven cases out of twenty in region II net transport was in the direction of the ductus deferens. There was a linear correlation between the probability of Al being towards the ductus deferens and distance of transport (Fig. 6). When the probability was over 0 5, i.e. the majority of Al were towards the ductus deferens, the transport of the droplets was in that direction except in one case in region II (Fig. 6B), and when the probability was below 0'5 the transport was towards the testis. The mean of the probability of Al being towards the ductus deferens, P(Ald) was 0'63 in region I and 0'57 in region II. The line which matched the data in region I, y = 24'4x (r = 0'94, P < 0001), was steeper (P < 0025) than the line y = 3'4x- 1'4 (r = 0'71, P < 0-001) in region II (Fig. 6). When the activity changed from the slow to fast type of transport the probability
8 460 U-M. JAAKKOLA AND A. TALO of Al occurring in the direction of transport increased in region I from 0-56 to 0-84 (t = -5052, P < 0001) and from 0-66 to 0-87 (t = 3-220, P < 0 05) in region II. This change was also seen in transport efficiency. If the efficiency is expressed as a percentage of the length which the droplet is transported from the total distance of its movements, the increase was from 3 to 26% in region I and from-6a-eo -in region II. mm 20, A B I * D {A I. -20 Fig. 6. Plot of (net) transport distances over 5 min (ordinate) against the probability of Al being in the direction of the ductus deferens, P(Ald) (abscissa). The line indicates the relation y = 244x-1P7 in region I(A) and y = 34x-1-4 in region II(B). DISCUSSION The small oil droplets moved freely in the lumen of the epididymis and therefore probably accurately indicate the bulk movements ofthe spermatozoa. The epididymal duct is so convoluted that movements of droplets can only be followed in a narrow region unless the duct is uncoiled. The uncoiling per se should not alter the hydrodynamical properties of the duct unless the wall is damaged, since the coils are separated by connective tissue in vivo and do not press each other, and we did not stretch the duct after careful tearing of the connective tissue between the coils. Transport of oil droplets consists of steps, Al, which are short in comparison with the length of the epididymal duct. About steps would be needed for transport through the duct if all steps were 0-2 mm and if all occurred in the same direction. In such a case the transport would take only 11 days, with an average frequency of steps of 8 min-, and the time would be less than 10 h if the step length were 0-8 mm. Both times are much shorter than the estimated transport time through the epididymis, which is 8-14 days. The step length 0-2 mm is about one duct-diameter
9 MOVEMENTS OF THE EPIDID YMAL CONTENTS in region II which is the narrowest region of the epididymal duct. It is unlikely that contractions of the wall can be much shorter than one diameter ofthe duct and remain effective in transporting sticky fluid. Therefore the slowness of the transport must be based on movements taking place in both directions, with only a small net bias towards the ductus deferens. In this respect sperm transport resembles the tranport of ova in the rabbit oviduct, where eggs move back and forth in short steps as a result of contractions of the oviduct wall. In the oviduct the bias is introduced partly by unidirectional ciliary beat in the ampulla (Verdugo, Blandau, Tam & Halbert, 1976) and partly by a slightly higher probability of occurrence of pro-uterine spread of electrical activity, which appears to be related to regional differences and their changes in the post-ovulatory period (Talo & Hodgson, 1978; Hodgson & Talo, 1978). In the epididymal duct there is no ciliary beat introducing the bias, the fluid flow from the testis cannot affect long stretches of narrow duct filled by viscous fluid, and the average frequency increases from region II to the next, major portion of the caput (Talo et al. 1979). Thus the mechanism which introduces the bias may not be the same as in the oviduct. Transport of spermatozoa, which consists of short steps occurring with variable probability in both directions, is a stochastic process. In this respect too the epididymis resembles the rabbit oviduct. Transport of ova has been considered as a one-dimensional random walk (Portnow, Talo & Hodgson, 1977) and has been simulated by a Monte Carlo model (Portnow, Hodgson & Talo, 1977). Our results suggest that, as in the oviduct, simulation studies might provide further insight into how the various parameters such as frequency, probability of movements towards the ductus deferens, and length of the pendular and net distances, are related to speed of transport. The change from slow to fast transport is very striking, when, after having moved back and forth sometimes for min in an area a few duct-diameters long, the droplet suddenly starts to move and is displaced in a few minutes over a distance tens of duct-diameters long. A similar change takes place in the seminiferous ductules in vivo (Setchell, Davies, Gladwell, Hinton, Main, Pilsworth & Waites, 1978). Thus this might be a general property of the proximal male excurrent duct and it also suggests that our findings in vitro may have a counterpart in vivo. The reasons for the change from slow to fast transport are not known. Three possible mechanisms may be suggested. Activation may be the result of stretch due to increase in fluid volume, a result of increased nervous activity, or an inherent property of muscular activity of the epididymal duct. The first and second possibilities would require an additional mechanism introducing the bias. The third possibility would mean that the epididymal musculature acts like a chain of bidirectionally coupled oscillators which may have periods of increased co-ordination (Brown, Duthie, Horn & Smallwood, 1975). Several properties of the intestinal tract have been explained by comparing it to the oscillator chain (Sarna, Daniel & Kingma, 1971; Akwari, Kelly Steinbach & Code, 1975). Although the epididymal wall is much less complex than the intestinal wall, and the properties of its electrical activity are not known in sufficient detail, this possibility needs to be studied. The lower transport speed through the cauda than the caput epididymidis (Amann et al. 1976) may result from the lower frequency of the contractions (Talo et al. 1979) 461
10 462 U-M. JAAKKOLA AND A. TALO and from the lower probability of spread ofelectrical activity (Jaakkola & Talo, 1982) and occurrence of Al towards the ductus deferens. The longer Al values during fast transport, and the higher probability and higher frequency ofthe pendular movements in region I compared with those in region II of the caput may lead to a higher speed of transport in this region, agreeing closely with the results found in vivo by Macmillan & Aukland (1960). In the cauda, contractions spread over long distances and the pendular movements were also long ( cm) Jaakkola & Talo, 1982). Thus the longer movements in region I of the caput may indicate that the contractions spread in general over longer distances there than in region II. No direct conclusion concerning the electrical activity of the wall musculature, however, can be drawn from the movements of the epididymal contents, since activity may spread over distances longer than the actual movement of the epididymal contents. But the frequency of the pendular movements corresponded to that of electrical activity in these regions of the caput (Talo et al. 1979) when the temperature in this study, about 2-5 deg C lower, is taken into account (Jaakkola & Talo, 1980); and in most cases the direction of Al was the same as the direction of the spreading contractions. Thus the linear correlation found in the cauda between the distance of net transport and the probability of the spread of activity towards the ductus deferens (Jaakkola & Talo, 1982) is comparable to the correlations found in this study between the net transport distance and the probability of Al being in the direction of the ductus deferens. The steeper correlation found in the cauda (possibly caused by long Al values) than in the caput may indicate that a small increase in probability together with an increase in frequency of the contractions may more effectively accelerate the speed of transport in that region, e.g. during ejaculation. This study was supported by the Academy of Finland. REFERENCES AKWARI, 0. E., KELLY, K. A., STEINBACH, J. H. & CODE, C. F. (1975). Electric pacing of intact and transacted canine small intestine and its computer model. Am. J. Physiol. 229, AMANN, R. P., JOHNSON, L., THOMPSON, D. L. & PICKETT, B. W. (1976). Daily spermatozoal production, epididymal spermatozoal reserves and transit time of spermatozoa through the epididymis of the rhesus monkey. Biol. Reprod. 15, BEDFORD, J. M. (1966). Development of the fertilizing ability of spermatozoa in the epididymis of the rabbit. J. exp. Zool. 163, BROWN, B. H., DUTHIE, H. L., HORN, A. R. & SMALLWOOD, R. H. (1975). A linked oscillator model of electrical activity of human small intestine. Am. J. Physiol. 229, CRABO, B. (1965). Studies on the composition of epididymal content in bulls and boars. Acta vet. 8cand. 6 (Suppl. 5), 1. HINTON, B. T. & SETCHELL, B. P. (1978). Fluid movement in the seminiferous tubules and the epididymal duct of the rat. J. Physiol. 284, 16P-17P. HODGSON, B. J. & TALO, A. (1978). Spike bursts in rabbit oviduct. II. Effects of estrogen and progesterone. Am. J. Physiol. 234, E JAAKKOLA, U.-M. & TALO, A. (1980). Effect of temperature on the electrical activity of the rat epididymis in vitro. J. thermal Biol. 5, JAAKKOLA, U.-M. & TALO, A. (1982). Relation ofelectrical activity to luminal transport in the cauda epididymidis of the rat. J. Reprod. Fert. 64,
11 MO VEMENTS OF THE EPIDID YMAL CONTENTS JOHNSON, A. L. & HOWARDS, S. S. (1976). Intratubular hydrostatic pressure in testis and epididymis before and after long-term vasectomy in the guinea pig. Biol. Reprod. 14, JONES, R., PHOLPRAMOOL, C., SETCHELL, B. P. & BROWN, C. R. (1981). Labelling of membrane glycoproteins on rat spermatozoa collected from different regions of the epididymis. Biochem. J. 200, MACMILLAN, E. W. & AUKLAND, J. (1960). The transport of radio-opaque medium through the initial segment of the rat epididymis. J. Reprod. Fert. 1, ORGEBIN-CRIST, M.-C. (1967). Sperm maturation in rabbit epididymis. Nature, Lond. 216, PORTNOW, J., HODGSON, B. J. & TALO, A. (1977). Simulation of oviductal ovum transport. Can. J. Physiol. Pharmacy. 55, PORTNOW, J., TALO, A. & HODGSON, B. J. (1977). A random walk model of ovum transport. Bull. math. Biol. 39, PURVIS, K. & HANSSON, V. (1978). Androgens-and androgen-binding protein in the rat epididymis. J. Reprod. Fert. 52, 59. SARNA, S. K., DANIEL, E. E. & KINGMA, Y. J. (1971). Simulation of slow wave electrical activity of small intestine. Am. J. Physiol. 221, SETCHELL, B. P. (1978). The Mammalian Te8ti8. London: Finn. SETCHELL, B. P., DAVIES, R. V., GLADWELL, R. T., HINTON, B. T., MAIN, S. J., PILSWORTH, L. & WAITES, G. M. H. (1978). The movement of fluid in the seminiferous tubules and rete testis. AnnI8 Biol. anim. Biochim. Biophy8. 18(2B), SETCHELL, B. P. & HINTON, B. T. (1981). The effects on spermatozoa of changes in the composition of luminal fluid as it passes along the epididymis. Prog. reprod. Biol. 8, TALO, A. & HODGSON, B. J. (1978). Spike bursts in rabbit oviduct. I. Effect of ovulation. Am. J. Physiol. 234, E430-E438. TALO, A., JAAKKOLA, U.-M. & MARKKULA-VIITANEN, M. (1979). Spontaneous electrical activity of the rat epididymis in vitro. J. Reprod. Fert. 57, TURNER, T. T., HARTMANN, P. K. & HOWARDS, S. S. (1977). In vivo sodium, potassium and sperm concentrations in the rat epididymis. Fert. Steril. 28, 191. VERDUGO, P., BLANDAU, R. J., TAM, P. Y. & HALBERT, S. A. (1976). Stochastic elements in the development of deterministic models of egg transport. In Ovum Transport and Fertility Regulation, ed. HARPER, M. J. K., PAUERSTEIN, C. J., ADAMS, C. E. COUTINHO, E. M., CROXATTO, H. B. & PATTON, D. M. pp Copenhagen: Scriptor. 463
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