STARZL, TE

WEBB, RC

English

PubMed

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THE EFFECT OF BLOOD VESSEL PULSATIONS ON LYMPH PRESSURE IN LARGE LYMPHATICS ROSCOE C. WEBB, JR., AND T. E. STARZL Dcpnrlntcnl qf Sttrccrv, Ike Jnlrns Ilophitrr U~:iz~ersilv ScItool O/ Medicinc and fJospild :i i Received for pul)licstion Octoher 8, 1953 ! {  Rhythmic alterations in lymph pressure a t  the same rate as the heart beat l:avc long Lee11 believed on circumstantial grounds to be an important factor in the propagation of lymph. I t  was not un ti1 1939, however, that the presence of such lymphatic pulsations was demonstrated by Cressman and Blalock (1). who suggested that the impulses were transmitted from contiguous arteries. By measuring lymph output from local areas to which extrinsic pulses~could be 1 imparted or withdrawn a t  will, Parsons and McMaster (2 ,3)  have shown that I lymph formation and drainage are remarkably facilitated in regions subjected to transmitted arterial pulsations. Because it had never been proved that rhythmic intralymphatic pressure I . changes are actually due to transmitted arterial pulsations, the present study of the origin and fate of intralymphatic pulsations was undertaken. :;I[ ! METHODS :;v r Thirty-five large mongrel dogs were used, and technically satisfactory conditions were realized in 20 experiments. The dogs were given condensed milk and 30 minutes later were anesthetized with 30 mgm. pcr Kg. of nembutal given intravenously. In most of the experi- ments the chest was opened and a positive pressure respirator used thereafter. Umbilical tapes for controlled occlusions were placed about the aorta, the two vessels arising from the aortic arch, and the left innominate vein through a thoracotomy in the left 3rd interspace. The abdominal aorta was isolated through a separate incision. Arterial, venous and lymphatic vessels were cannulated with polyethylene catheters or blunt 20 gauge steel needles filled with heparin. Inductance type transducers were used to measure arterial and venous pres- sures; lymphatic pressures were detected with a capacitance manometer. All pressures were recorded simultaneously on a multichannel direct writing oscillograph. The frequency re- sponse of the measuring and recording systems employed was in excess of 50 cycles per second when tested by recording pressure within a balloon during explosion. Two sites were chosen for study: the lower portion of the thoracic duct, which was exposed at  the level of the l l t h  and 12th thoracic vertebrae through a thoracotomy in the l l t h  left interspace, and the terminal portion of the thoracic duct, which was exposed through a left supraclavicular incision. In each location pressures were obtained either by cannulating a tributary so that the main lymphatic channel was unobstructed, or by directly cannulating the thoracic duct in which case the central lymph flow was blocked. In this paper the former method is refcrred to as sidc p lc rswe mmtwcmd, and the latter as end f lcrswc m d a s w m .  Aided by a grant from the United States Public ~ealth' Service; National Institutes of 9 : Health, Bethesda, Maryland. 401 \ \ a 402 ROSCOE (:. WEBB. Jll.  I \ND 'L'. E. S'I'ARZI. 111 order lo mcasurc crlrl prcssllrrs thc Iynil)hatic channel was mol~ilizc:~l ovvr a rlistancc of 8 to 10 tnti~. it1111 liftctl carefully so ~lt;rt thc rccortling systcm ant1 lymph vcsscl tvr~uld t ~ c  conil>lclt4y free of contact with any othcr structure, insuring that any pressure alterations rmbrdrrl \vc.rc tliscrctrly intralymphatic. Sitlc pressures wcrc ohtaincd t ~ y  placing thc pdy- rtliylcnr !ul)c or 1)lunt s~c*cl trc.cdlc through R tril~utary until its tip rcachctl thc main iym- phntic ch;~nnel. In this siluntion all othcr vcsscls in thc immccliatc vicinity which might ilnpnrt Iilovctncnt artefact to the recording systcm were rctractcd or rcmovc I. RESULTS Recordirtg from the thoracic duct jusl above the diaphragm. Mean side pressures ranged from 35 to 55 mm. water. After several minutes of obstruction to flow, -- *. --- . -  . L I D  FIG. 1A. Side pressure recording from thoracic duct a t  the level of TI2 showing lymphatic pulsations (L) and how these were unaffected by aortic occlusion below the renals (DA) and eliminated by occlusion a t  the first intercostal level (PA). Concurrent right common carotid (C) and left femoral (F) arterial tracings are shown. B. Similar record (1) in which a ligature tightened in position to prevent lymph from reach- ing the tip of the recording catheter obliterated both pressure and pulsations (2), with restoration of the original pattern after ligature was loosened (3). Lymph pressure calibra- tions are in mm. saline, and arterial pressures in mm. mercury. end pressures were as high as 350 mm. water, but by intermittent release of the lymph between recordings the pressures were generally maintained a t  less than 100 mm. water. There were only two types of demonstrable variations from the mean level. The first type consisted of respiratory alterations (Figs. 1-3), which could be kept a t  a minimum by maintaining the positive pressure respirator at  a low exchange. The second type of pressure variation consisted of rapid lymphatic pulsations in phase with the heart beat, which were essentially the same irrespective of whether side or end pressure furnished the background. The pulse pressure of these rapid lymphatic cycles was surprisingly great, usually being 20 to 30 mm. water and amounting to a significant fraction of the peak lymph pressure. Thus typical pressures in millimeters of water could \ be tabulated as 70 systolic and 40 diastolic, or 55 systolic and 35 diastolic. nT.OOD VESSEI, PUT.SATIONS AND 1.YMPII I'RXSSURE 403 'The pattern of the lymphatic pulse tracing was variable from animal to animal and a t  rlilTercrrt tinies i r i  the same animal, sometimes bcing very sharp with conil~les form (Fig. 4A), and a t  othcr times being a simple wave (Fig. ID). In all instances, however, the chief (always the first) component had a fixed time relationship to the arterial pulse (Fig. 4AS, starting after the carotid and before the femoral pulsations in the position one would predict for adjacent aortic pulsations. FIG. 2. Side pressure recordings showing cffcct upon pulsations in the cervical thoracic duct (L) of: A. Occlusion of the aorta at  the first intercostal (AO), causing a carotid hyper- tension with concurrent augmentation of the lymphatic pulsations. B. Serial occlusion and release of the left su~clavian (LSC) and brachiocephalic (BCT) arteries, and the thoracic aorta at  the first intercostal (AO). Right common carotid (C) and left femoral (I?) arterial pressures are included. The verti- cal indicator dashes beneath the lymph recording in B show the time of onset of femoral pulses. Lymph and venous pressure are in mm. saline, and arterial pressures are in mm. mercury. Occlusion of the aorta distal to the site of the lymphatic catheter had little or no effect on the lymphatic pulsations (Fig. lA), whether the occlusion was a t  the level of the superior mesenteric artery, renal arteries, or a t  the bifurca- tion. Similarly, occlusion of the ascending lymphatic channels at any point 2 or 3 cm. or more below the level of the cannulation did not appreciably alter the pulsations although the mean lymphatic pressure generally fell. On the olher hand, occlusion of the aorta proximal to the lymphatic cannula always completely obliterated the intrinsic lymphatic pulsations (Fig. lA), usually with An attendant fall in mean lymphatic pressure. Pulsations promptly reappeared upon release of the aorta. That the pulsations recorded were representative of pressure events in the -. 4-H ROSCOE C. \Vl?B13, JR. AND T. E. STARZL lyinph rathcr than of rhythmic catheter movcmcnt or other artcfact. was - .  cvitlcnt from several considerations. With either end or side prcssurc mcasure- ment. when the tip of the lymph filled catheter was trapped by a ligature in silu so lymph could not reach it (Fig. lB), the pressure fell and pulsations ceased, to return again when intralymphatic contents were brought back into FIG. 3. Side recordings from the cervical thoracic duct (L) showing in each case a trans- mitted venous contribution to the lymphatic pulsations. Concurrent pressures were taken from the internal jugular vein (J) and left common carotid artery (C). Lymph and venous pressure calibrations are in mm. saline and arterial pressures in mm. mercury. A. Effcct of ascending aortic occlusion (AA), showing elimination of the arterial com- ponent of thc lymph pulsations. Vertical indicator dashes in lymph channel mark onset of left common carotid pulses. B. Different animal showing disappearance of pulse and elevation of mean intralymphatic pressure upon occlusion of innominate vein (IV). C. Immediately after record shown in B the thoracic duct was ligated a t  its entry into the left subclavian vein. Pulsations persisted, were not affected by ascending aortic occlusion (.4A), but were abolished by innominate vein occlusion (IV). ' contact with the recording system. Furthermore, it was demonstrated grossly by several techniques that the contents of lymphatic vessels pulsated with considerable sharpness and vigor. When a catheter was placed in the thoracic duct, the lymph could clearly be seen to pulsate as it rose in the tube; or if a small opening was made in the vessel wall, the escaping lymph was seen to issue in a pulsatile manner. Moreover, if either a small air bubble or a tiny amount of ink was injected into the duct, i t  slowly passed rostrdy,  moving about with each aortic pulsation, pausing transiently a t  the valves, and finally passing out of sight into the neck. l j1 .001)  VESSEL I'ULSATIONS AND LYMPlI PRESSURE 405 liccar(ling.irortr Il~r rcnlirnl lkorncir drrcl. Mean side pressures ranged from 25 to 100 mm. water, and mean end pressures were maintained a t  approximately 100 mm. water by intermittent lymph letting to relieve the obstruction. Intralymphatic pulsations, similar to those described above, were evident. Tllc lymph pulsated either in synchrony with adjacent arteries (Fig. 2) or in FIG. 4. Lymphatic pulsations in magnified detail showing time relationship to pulsations of adjacent vessels. 1 .4. Side pressure recording from thoracic duct a t  the T-12 level. The record is a n  enlarged I segment of that illustrated in Fig. lA,  and has the same legend. 1 i B. Similar enlarged segment of record obtained from the cervical thoracic duct. The - record is a magnified portion of that shown in Fig. 3A, and has the same legend. phase with the pulsations of the neck veins (Fig. 3B, C). Often pressure i changes were coordinated with both arterial and venous pulses, resulting in an 1 irregular double lymphatic pulse for every cardiac cycle (Figs. 3A, 4B). The transmitted arterial component of the lymphatic pressure waves was synchronous with the carotid (Figs. 2, 3A, 4B) or subclavian pulse. Ac- cordingly, if the blood or pulse pressure in these vessels was altered, dramatic changes occurred in the.lymphatic pulsations. When the third portion of the 400 ROSCOE (:. WEBn, JR. AND T. I?, STARXI, I i nortic* nrcli was oc.clodctl (1;ig. 21\) rarotitl hy1)crtcnsion and witlcning of the arterial l ~ ~ l s c  pressure occurrvtl i~nmc~li:~tcly, acc.ornl)anicrl l)y augmentation of tlic lymphatic 1)ulsations. (_'onvcrscly, il the artcrics of the hcatl ant1 ncck wcrtn serially Idorkctl a clecrclnent or a fall-out of lymph pulsations was dcmon- stral~le. Such an instance is shown (f"ig. 2B) in which left subclavian occlusion rausctl a reduction in size of lymph pulsations, followed by virtual disap- ~'carancc of pulsations when the hrachiocephalic artery was occluded. 11' A mute pulsations which remained could then he aholishcd by occlusion of the third portion of the aortic arch. More simply, occlusion of the ascending aorta also eliminated the transmitted arterial element of the lymphatic pulse, leaving, in those instances where it had been present before (Fig. 3A), a lymphatic pressure wave related only to venous pulsations. :jlterations of lymphatic pressure that occurred in phase with the jugular or subclavian venous pulsations could be recorded with either end or side pressure methods, suggesting at  the outset that they were transmitted by contiguity rather than by retrograde flow from the subclavian vein into the thoracic duct. This component of the lymphatic pulse was not significantly affected by occlusion of the ascending aorta (Fig. 3C) but was eliminated by occlusion of the innominate vcin (1:ig. 3 R ,  C) or the superior vena cava. Ligation of the thoracic duct a t  its entry into the subclavian vcin, which broke intraluminal contact between the two systems, failed to eliminate this type of lymphatic pulse (Fig. 3 B, C)--emphasizing that any venous component of the lym- phatic pulses is chiefly activated by adjacent pulsating veins rather than by venous reflux into the duct. t I DISCUSSION With recording techniques and by direct observation, it is evident that I movements from the great arterial trunks are imparted to the larger collecting lymphatics. These transmitted pressure changes apparently keep the lymph in I continual pulsatile motion which, because of the high degree of valve compe- tence (I) ,  is oi necessity oriented toward the venous drainage sites. In  the neck, I where the thoracic duct is in close relation to large pulsating veins, venous pulsations are similarly transmitted to the lymph, a process which is probably i peculiar to a few anatomic areas such as the subclavian triangle and of limited I functional significance. The type of experimentation performed on the lower thoracic duct yielded I valuable information on the fate of the transmitted intralymphatic pressure I alterations. Occlusion of the aorta just proximal to the level of pressure measurement routinely obliterated the lymphatic pulses at  distal levels, in- I dicating that retrograde lymphatic conduction of these transmitted effects does I not occur. Similarly, blockage of ascending lymph channels or elimination of 1 BLOOll VRSSEI- PULSATIONS AND CYMPlI PRESSURE 407 distal aortic ptllsations did not al)l)rc~.ial>ly alter the lymphatic palsations, siiggesti~lg that n~stral propagation of the lymph pressure changes is likcwiw for !-cry short distances. The information prezented is dimtly relevant only to the effect of the great arteries on the larger lymphatic channels. 'The possible extension of such a concept to the distal vascular and lymphatic beds has been stressed in the skilh~l rzl~crin~cntations of Parsons and McMasters (2, 3), although at present one can only speculate upon the role of this mechanism in peripheral lymph clearance. SUMMARY A study was made in dogs of rhythmic intralymphatic pressure changes in the supradiaphragmatic and cervical thoracic duct. In 110th areas lymphatic pulses were found to be tran~mitted from contiguous large arteries, the lymphatic pulse pressure representing a significant fraction of the peak lymphatic pressure. In the neck venous pulsations were also shown to be trans- mitted to the lymph in a similar manner. These pulsations were shown to be propagated for only a few millimeters. By "tagging" the lymph i t  could be demonstrated that the pulsations were associated with its proximal flow. The possible functional significance of such a mechanism in general lymph clearance is reemphasized. BIBLIOGRAPHY 1. CRESSMAN. R. D. AND BUUKK, A.: The effect of the pulse upon the flow of lymph. Proc. Soc. Exp. Biol. and Mcd. 1939, 41: 140. 2.  PARSONS, R. J. AXD MCMASTER, P.D.: The effect of the pulse upon the formation and flow of lymph. J. Exp. Med. 1938, 68: 353. 3. MCMASTER. P  D. AND PARSONS, R. I.: The effect of the pulse on the spread of sub- stances through tissues. J. Exp. Med. 1938. 68: 377. - ,  'J' . '  t. .... ': . . . .  . : '  -: . . . ., !. - .  . . - .  ti;,;; ' : I  . : J ,,.,. ;, $.< .... . .  .--...!. :: 0 .. . . . . . <  - -  -:.. : 1 ;, :A; .-i . I . . . . L;:- , : E - . . - . :  -. . -. .4 - . * !. . 1 .~ 

The effect of blood vessel pulsations on lymph pressure in large lymphatics.

Webb Jr, RC

Starzl, TE

Name not available

The effect of blood vessel pulsations on lymph pressure in large lymphatics

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The effect of blood vessel pulsations on lymph pressure in large lymphatics.

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