MYOCARDIAL FAILURE WITH ALTERED RESPONSE TO ADRENALINE IN ENDOTOXIN SHOCK
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1 Br. J. Phrmc. (1975), 54, MYOCARDIAL FAILURE WITH ALTERED RESPONSE TO ADRENALINE IN ENDOTOXIN SHOCK L.T. ARCHER & M.R. BLACK Veterns Administrtion Hospitl, Oklhom City, Oklhom 73104, U.S.A. L.B. HINSHAW Veterns Administrtion Hospitl nd Deprtments of Physiology & Biophysics nd Surgery, University of Oklhom Helth Sciences Center, Oklhom City, Oklhom 73104, U.S.A. 1 There is growing concensus tht myocrdil performnce in the erly stges of experimentl endotoxic nd septic shock is reltively norml; however, recent reports hve identified n intermedite phse of shock when myocrdil dysfunction is clerly pprent. 2 The mechnism of dysfunction hs become subject of intense investigtion. A current view is tht ltered myocrdil responsiveness to circulting ctecholmines my ply n importnt role in the dysfunction observed fter endotoxin dministrtion. The present studies, in which n isolted working hert preprtion of the dog ws used, were designed to test this hypothesis. This prticulr experimentl preprtion ws selected to provide n dequte interprettion of results; crdic output, fterlod, nd concentrtions of drenline reching the coronry vsculr bed were controlled in ll experiments. Responses to infusions of drenline were recorded in the 'stedy-stte' condition. Control (non-shocked) hert responses to drenline were highly reproducible in terms of inotropic, chronotropic nd coronry vsculr behviour. 3 Results from the study document myocrdil dysfunction within 4-6 h following n LD70 endotoxin dministrtion on the bsis of incresed left ventriculr end distolic pressure (LVEDP), decresed crdic power nd myocrdil efficiency, nd depressed negtive nd positive dp/dt prmeters. 4 Findings suggest significntly ltered responsiveness of the myocrdium to infused drenline t rtes of 1, 2, nd 5 pg/min with concentrtions between 10 nd 1 ng/ml blood. LVEDP ws elevted while clculted power nd efficiency prmeters remined significntly below control vlues during infusion of drenline in endotoxin-treted herts. Depressions of responsiveness were interpreted to occur on the bsis of filure to restore positive nd negtive dp/dt to norml vlues nd depressed coronry blood flow responses during drenline dministrtion. Increses in coronry flow were regulrly less in experimentl herts thn the controls. Hert rte responses to drenline in both filing nd non-filing herts were identicl. 5 In conclusion, it is suggested tht myocrdil contrctile nd relxtion chrcteristics nd coronry vsculr responses to drenline infusion re depressed in endotoxin shock during the period of demonstrted myocrdil dysfunction. No distinct cusl reltionships were observed between the iltered myocrdil responsiveness nd pthogenesis of hert dysfunction since myocrdil dysfunction nd ltered responsiveness to drenline were generlly observed together. Myocrdil oedem formtion fter endotoxin s previously reported by this lbortory my ber reltionship to the depressed negtive dp/dt response to drenline. Introduction Clssiclly described erly hemodynmic chnges Colson, 1970). However, since erly peripherl in endotoxin shock consist of progressive decreses sequestrtion of blood is clerly observed to occur, in venous return nd crdic output occurring the decrese in crdic output hs been ccounted concomitntly with mrked systemic hypotension for on the bsis of diminished venous return (Weil in both cnine (Weil, McLen, Visscher & Spink, et l., 1956). There is growing concensus of 1956; McLen & Weil, 1956) nd subhumn opinion tht myocrdil performnce in the erly primte species (Hinshw, Shnbour, Greenfield & stges of shock (0-3 h) is reltively norml nd
2 146 L.T. ARCHER, M.R. BLACK & L.B. HINSHAW tht depressed crdic performnce per se performs n insignificnt role in the erly reduction of crdic output (Weil et l., 1956; Goodyer, 1967; Hinshw, Archer, Greenfield & Guenter, 1971 ; Hinshw, Archer, Greenfield, Guenter & Miller, 1972; Hinshw, Greenfield, Owen, Blck & Guenter, 1972c; Siegel, Frrell, Goldwyn & Friedmn, 1972). It hs been proposed by Goodyer (1967) nd Hinshw et l. (197 l) nd inferred from the work of Siegel et l. (1972) tht ventriculr performnce in the initil stge of endotoxin or septic shock is supported by sympthodrenl response initited subsequent to the development of systemic hypotension, which is consistent with the findings of others (Nykiel & Glvino, 1961; Hbkfelt, Bygdemn & Sekkenes, 1962; Cvngh, Ro, Sutton, Bhgt & Bchmnn, 1970; Hll & Hodge, 1971). Incresed neurohumorl ctivity ssocited with the erly compenstory period of shock should provide substntil crdiovsculr support towrd the mintennce of norml hemodynmics in the fce of diminished venous return. Recent reports hve identified subsequent phse of shock, following the erly compenstory period, when myocrdil performnce begins to flter or fil ltogether (Solis & Downing, 1966; Goodyer, 1967; Siegel, Greenspn & Del Guercio, 1967; Cvngh et l., 1970; Bell & Thl, 1970; Cnn, Stevenson, Fillos & Thl, 1972; Hinshw et l., 1972c; Hinshw, Archer, Blck, Greenfield & Guenter, 1973; Prrtt, 1973; Nishijim, Weil, Shubin & Cvnilles, 1973; Hinshw, Archer, Blck, Elkins, Brown & Greenfield, 1974; Prrtt & Winslow, 1974; Greenfield, Jckson, Elkins, Colson & Hinshw, 1974) in both niml endotoxic studies nd clinicl septic shock. The observed myocrdil dysfunction in not merely preterminl event nd is not necessrily ssocited with systemic hypotension, cidemi, or depressed oxygen delivery (Hinshw et l., 1972c, 1973; Hinshw, Archer, Spitzer, Blck, Peyton & Greenfield, 1974b), nd does not pper to be due to the relese of myocrdil depressnt fctor (Hinshw, Greenfield, Owen, Archer & Guenter, 1972b; Hinshw et l., 1974). One possible cuse of the dysfunction my be depressed response of the myocrdium to circulting ctecholmines following the period of incresed sympthetic ctivity, nd this potentil mechnism is the subject of the present study. Recent reserch, supportive of this view, is tht of Cvngh et l. (1970), Bhgt, Cvngh, Merrild, Rn & Ro (1970), nd Prrtt (1973), who reported depressed inotropic, chronotropic or ltered coronry blood flow responses in vrious species of nimls subjected to endotoxin shock. Reltively depressed myocrdil responsiveness to neurlly-induced sympthetic stimultion in shock hs been reported by Glvino & Kloud (1965) nd Geocris, Quebbemn, Dewoskin & Moss (1973). On the other hnd, excessive sympthetic stimultion of the myocrdium in rbbits dministered endotoxin my elicit subendocrdil hemorrhge nd necrosis of myocrdil fibres (Plmerio, Ming, Frnk & Fine, 1962). Results from the present study prtilly support the erlier observtions by Cvngh et l. (1970), Bhgt et l. (1970), nd Prrtt (1973) once myocrdil filure is clerly demonstrted, but provide no evidence for their inititing roles in the pthogenesis of myocrdil dysfunction. Methods Experiments were crried out on nineteen isolted working cnine herts supported with rteril blood from heprinized support dog, prepred s previously described (Hinshw et l., 1971, 1973). The donor dog ws nesthetized, nd the chest opened by medin sternotomy fter the niml ws plced on constnt volume respirtor. The zygos vein nd subclvin rtery were ligted nd divided. Ligtures were loosely plced round the thorcic ort distl to the subclvin rtery, the brchiocephlic rtery, nd superior nd inferior vene cve. The pericrdil sc ws opened long its ventrl surfce nd the niml ws injected with heprin (3-5 mg/kg). The vgi were then cut in the neck nd the brchiocephlic rtery ws cnnulted with Tygon tube elevted to height of -125 cm bove the hert level. The superior ven cv ws cnnulted with bloodfluled plstic tube led through roller blood pump prepred to drw blood from the ort of the support dog. Blood ws llowed to flow through the brchiocephlic cnnul nd to fill the Tygon tube. The ort of the isolted hert ws then tied distl to the origin of the brchiocephlic rtery, the superior ven cvl inflow from the pump ws strted t bout 120 ml/min, nd the inferior ven cv ws immeditely ligted. Blood from the ortic outflow of the isolted hert ws collected in plstic reservoir plced within heted wter bth, nd returned to the dog t flow rte equl to the superior ven cvl inflow. Hert, lungs nd djoining tissue were then removed from the chest nd supported by the trche in the externl system with dequtely provided coronry pressure nd blood flow. The lungs of the isolted hert were ventilted, while the support niml ws respired spontneously. Herts were removed without interruption of blood flow from dult donor nimls weighing between 4.5 nd 8.0 kg nd continuously supported by pump-delivered
3 ENDOTOXIN AND CARDIAC RESPONSE TO ADRENALINE 147 blood from dult support dogs weighing between 22 nd 32 kg. The right hert ws then bypssed fter first pssing sline-filled plstic tube into the right ventricle vi the trium, nd then cnnulting the pulmonry rtery from 'T'-connector previously secured to the superior ven cvl inflow tubing. The cnnultion of the pulmonry rtery required only few seconds during which time the coronry vessels were retrogrdely perfused with blood by hydrosttic pressure from the ortic outflow tubing. Left ventriculr pressure ws mesured simultneously for end distolic pressure (0-40 mmhg) nd systolic pressure (0-200 mmhg) by mens of seprte Stthm pressure trnsducers ttched by 'Y'-connector to plstic cnnul inserted through purse-string suture in the pex of the left ventricle. Coronry venous blood ws collected from the right ventriculr drin into plstic reservoir nd returned together with brchiocephlic outflow to the support dog vi second pump. Crdic output ws tken s the sum of ortic outflow nd coronry flow, both mesured with cylinder nd stopwtch. Aortic pressure, left ventriculr pressures, crdic contrctility nd ECG of the isolted hert, nd systemic pressure of the support niml, were monitored continuously on Snborn recorder. The first derivtive of the left ventriculr pressure, dp/dtmx, ws continuously recorded by mens of resistnce-cpcitnce differentiting network. Men ortic pressure ws controlled in the isolted hert preprtion by djustment of screw clmp on the ortic outflow. Crdic output ws mintined t 76 ml kg-' min-' by djustment of pump speed supplying the pulmonry rtery. Following n equilibrium period of pproximtely 30 min when stedy-stte condition ws reched, smples of coronry rteril nd venous blood were collected nd nlyzed for blood gses, with n Instrumenttion Lbortories blood gs nlyzer. Oxygen content in coronry rteril nd venous blood ws mesured by Vn Slyke mnometric blood gs nlyzer. Blood tempertures of isolted hert nd support dog were mesured continuously with thermistor probes nd held constnt by use of heting pds nd wter bth temperture regultion. Methods used for experimentl procedures nd sttisticl tretment of dt hve been described previously (Hinshw et l., 1974, 1974b). All isolted herts received periodic nd vrible dose infusions of drenline (Prke, Dvis & Co.) introduced into the left ventricle vi polyethylene ctheter whose disti tip ws plced in the chmber of the left trium with the proximl end ttched to motor-driven syringe. Following mesurement of control myocrdil prmeters without drenline, dose-response curves were crried out t regulr intervls, ll vlues being recorded during stedy-stte conditions. Adrenline infusion rtes were vried between 1, 2 nd 5 mg/minute. These rtes of infusion resulted in drenline blood concentrtions of 1-10 ng/ml, bsed on the dilution of the infused drug with the crdic output (verge, 0 ml/min). Adrenline ws infused t fterlods of mmhg nd crdic output of 76 ml min-' kg-l, bsed on the weight of the hert donor niml. Afterlods were mintined t mmhg between drenline infusions. A control group of six herts, receiving no endotoxin, ws monitored t nd mmhg fterlods for 4-5 h fter the beginning of the hert perfusion period when pressures nd flows becme stbilized. Inotropic, chronotropic nd coronry vsculr responses to drenline infusions dministered to control (non-shocked) herts demonstrted high degree of reproducibility during the 4-5 h period in the isolted stte. The experimentl group consisted of thirteen isolted herts nd support nimls receiving n LD70 dose of Escherichi coli endotoxin, 1.5 mg/kg. Endotoxin ws obtined from Difco Lbortories, Detroit, Michign (Lipopolyscchride B, E. coli 0127: B8, Boivin procedure with TCA extrction). The degree of lethlity ws previously determined on group of 3040 nimls. Seven nesthetized support dogs nd seven hert donor nimls dministered endotoxin were observed pproximtely 1-2 h before isoltion of the left ventricle nd its removl to the perfusion pprtus. In ddition, six herts nd their respective support dogs were given endotoxin following trnsfer, equilibrtion nd smpling for control vlues. As in the control group, smples were tken t nd t mmhg fterlod, nd drenline responses were reported t mmhg. Experimentl nd control isolted hert preprtions were observed like during the 4-5 h period in the isolted stte. Results Results re divided into three ctegories: () those describing the effects of endotoxin on the support niml supplying blood to the isolted hert; (b) those documenting the development of myocrdil dysfunction in the isolted hert during the 6 h post-endotoxin period; nd (c) those illustrting chnges in myocrdil function (LVEDP, + nd -dp/dtm,), work performnce (power), hert rte, nd myocrdil
4 148 L.T. ARCHER, M.R. BLACK & L.B. HINSHAW I E 0- LU > 1 -i 5 O 11 A n 0nA b ** -* co ) 10 * 5 0 1)0 60 to 90 Afterlod (mmhg) 120 to to 220 Time ( min) post-endotoxin 240to to360 Figure 1 Chnges in left ventriculr end distolic pressure (LVEDP) following dministrtion of endotoxin (men + s.e., fterlods of nd mmhg). Isolted cnine herts, () 6 control (no endotoxin), nd (b) 13 experimentl preprtions, 0-6 h post-endotoxin. * P < 0.05; ** P. nf nln 10 nf.0 I I t ).2 C E 10 - ) Afterlod (mm Hg) 60to90 120to to to to360 Time (min) post- endotoxin Figure 2 Effects of endotoxin on myocrdil efficiency (men + s.e., fterlods of nd mmhg). () 6 control (no endotoxin) nd (b) 13 experimentl hert preprtions studied 0-6 h post-endotoxin. * P < 0.05; ** P.
5 ENDOTOXIN AND CARDIAC RESPONSE TO ADRENALINE cx 1-1 E C E ~0 E 200 MLn fl nf n fl n fl 0 M io6 io6sd b Afterlod (mmhg) 60 to to to to to 360 Time (min) post-endotoxin Figure 3 Decreses in men negtive dp/dt (-dp/dt) in () 6 isolted control (no endotoxin) herts nd (b) 13 experimentl herts studied 0-6 h post-endotoxin (men ± s.e.). *P < 0.05; ** P. hemodynmics (coronry blood flow) in response to grded doses of infused drenline. Tble 1 describes responses of support nimls used in the current series of experiments to endotoxin dministrtion nd documents the sustined presence of systemic hypotension, in contrst to the normlly mintined systemic pressures in control dogs not receiving endotoxin. Figures 1, 2 nd 3 nd Tble 2 illustrte the development of detrimentl myocrdil performnce chrcteristics documenting crdic dysfunction fter endotoxin in the current series of hert studies. No sttisticlly significnt differences between experimentl nd control herts were seen in the observed prmeters until 4 h fter endotoxin injection. Dt from thirteen experimentl hert preprtions demonstrte significnt elevtions in left ventriculr end distolic pressure (LVEDP) (P < 0.05, Figure 1), depressions in myocrdil efficiency (P < 0.05, Figure 2), negtive dpidtmx (P < 0.05, Figure 3), nd positive dp/dtmx (P < 0.05, Tble 2) t fterlods of nd mmhg between 4 nd 6 h post-endotoxin. The most outstnding redily Tble 1 Systemic rteril pressure response* of hert-support nimls following LD70 endotoxin dministrtion Time post-endotoxin (min) Experimentl group (n = 13) p Control group (n = 6) +60 to to to to to (7) 85(5) 80(8) 81(6) 104(9) 109(7) 90(8) 91(6) 83(10) 90(6) < (5) 133(5) 138(8) 138(8) 138(6) 137(7) 143(5) 133(5) 138(6) 137(7) * mmhg; men with (s.e. men)
6 1 L.T. ARCHER, M.R. BLACK & L.B. HINSHAW observble chnges signlling the onset of myocrdil dysfunction re increses in LVEDP to vlues exceeding 10 mmhg t low fterlods nd progressively developing depressions of negtive dp/dt. The possible significnce of the ltter is discussed in recent report (Hinshw et l., 1 974b). Tble 3 summrizes stedy-stte chnges in myocrdil 02 uptke following endotoxin dministrtion. In generl, men 02 uptke vlues re lower in the experimentl herts compred with the controls not receiving endotoxin, nd re significntly decresed within 4-5 h t fterlods of nd mmhg, nd from 5-6 h postendotoxin t mmhg (P < 0.05). Myocrdil rteril Po2 ws significntly decresed (P < 0.05) from 2-5 h fter endotoxin, mximum decreses rnging from n initil vlue of 1 12(±6) to 98(±3) mmhg t 5 hours. Figures 4-6 summrize stedy-stte responses of the isolted hert preprtion to different concentrtions of drenline t vrious times following endotoxin during controlled fterlods nd crdic outputs. Control herts not receiving endotoxin re similrly infused with drenline t the sme time intervls. Adrenline is infused into the left trium during fixed crdic output (76 ml min-' kg-', in order to void problems of vrible dilution of drenline in the pulmonry bed nd to insure delivery of identicl drenline concentrtions to the coronry bed. Afterlods were fixed t mmhg in order to insure identicl coronry perfusion pressure chrcteristics. All responses shown re stedy-stte vlues, ordinrily Tble 2 Chnges in left ventriculr positive dp/dt* (+dp/dt) following endotoxin dministrtion * Time post-endotoxin (min)' +60 to to to to to +360 Afterlod (mmhg) Experimentl group (n = 13) 2281(125) 1295(45) 2030(135) 1145(65) 2040(1) 1160() 1715(135) 1075(45) 1675(80) 945(90) mmhg/s; men (+ s.e.) (76 ml min-' kg-' crdic output t ll fterlods) p 2120(115) 1200(75) 2055(85) 1110(40) 2110(90) 1185(65) < (115) 1200(75) < 0.05 Control group (n = 6) 2110(90) 1185(65) Tble 3 Chnges in 02 uptke* following endotoxin dministrtion Time post-endotoxin (mini +60 to to to to to +360 Afterlod (mmhg) Experimentl group (n = 13) 11.3(1.0) 8.5(0.7) 9.8(1.6) 7.6(1.2) 11.9(0.8) 9.1(0.7) 10.1(0.6) 7.6(0.4) 10.7(0.5) 7.0(0.7) p < 0.05 < 0.05 < 0.05 Control group (n = 6) 12.0(0.6) 9.0(0.5) 11.3(0.4) 9.0(0.4) 11.9(0.5) 8.9(0.6) 12.0(0.6) 9.0(0.5) 11.9(0.5) 8.9(0.6) * ml min-' per g lef5 ventricle; men (± s.e.)
7 ENDOTOXIN AND CARDIAC RESPONSE TO ADRENALINE 151-0) Wi J 0 b 5 m C lpg 2pg C 1pg 21j9 C 1pg 2pg C l1g 2pg C 1pg 2pg 5pg -Brn IiiIIITNliii 5 C 1Jg 2pg C 1pg 2pg C l1g 2pg C 1pg21g C l1pg 2pg5pg 60 to90 120to to to to360 Time (min) post-endotoxin Figure 4 Men stedy-stte vlues (± s.e.) of left ventriculr end distolic pressure (LVEDP) during drenline infusion into left trium of isolted hert fter endotoxin (LD70). () Six control (no endotoxin) nd (b) 13 experimentl herts studied 0-6 h post-endotoxin. * P < 0.05; ** P r 0Sl [t< t\ t[ \]8 E C 1lpg2pg C lpg 2pg C 1ipg 2pg C 1ig 2pg C1pg 2pg5pg.8 b, ) 10 -** * C lpg 2ug C lpg 2ug C lpg 2ug C lpg 2pg C 1pg2 J5pg 60 to to to to to 360 Time (min) post-endotocxin Figure 5 Men stedy-stte vlues (± s.e.) of left ventriculr negtive dp/dt (-dp/dt) during drenline infusion into left trium, 0-6 h post-endotoxin. () Six control (no endotoxin) nd (b) 13 experimentl herts. * P < 0.05; ** P.
8 152 L.T. ARCHER, M.R. BLACK & L.B. HINSHAW.80 0).70} ::11~~~~~~~~~~ T:T n T-0 E Clpg 2p C1pJg 2pg C 1pg 2Jg C 1pg 2pg C 1pg 2pg 5pg ) b.60 C 80uum 1111 iii iiii C lpg2ug C lpg 2ug C lpg2ug C lpg 2ug C ipg 2pg 5pg 60 to to to to to 360 Time (min) post-endotoxin Figure 6 Men stedy-stte vlues of left ventriculr power (g.m s-' kg-' ) during left tril infusions of drenline 0-6 h fter endotoxin. () Six control (no endotoxin) nd (b) 13 experimentl herts (men + s.e.). * P < 0.05; ** P. chieved within 2-4 min of drenline infusion. The upper pnel of Figure 4 shows men LVEDP responses of six control herts (no endotoxin) to drenline during 4-5 h period. Results show tht successive responses to 1 nd 2,g/min infusions of drenline in control herts re reproducible nd indistinguishble in mgnitude t the sme doses. On the other hnd, the lower frme of Figure 4 shows tht vlues of LVEDP in endotoxin-treted herts re considerbly higher, nd significnt differences occur between control nd experimentl (endotoxin) preprtions from 3-6 h fter endotoxin before nd during drenline dministrtion (P < 0.05). LVEDP vlues in filing herts decresed during infusion of drenline but remined consistently higher thn those from herts not subjected to endotoxin t 1, 2 nd 5,g/min infusions (P < 0.05). Probbility vlues shown in Figure 4 refer to differences between control (no endotoxin) nd experimentl (endotoxin) groups in response to drenline infusion t the sme time intervl. Figure 5 shows negtive dp/dtm, vlues in response to drenline infusion, s dministered in the previous figure. Results from dysfunctioning herts show decreses in negtive dp/dtmx (P < 0.05) during the lter phse of shock (4-6 h), which were little chnged by the dministrtion of drenline. Decreses in positive dpidtmx were evident t 6 h post-endotoxin during drenline infusions of 1 nd 2 mg/min (P < 0.05). Depressions in myocrdil power re observble within 3 h fter endotoxin nd decline progressively (P< 0.05) up to the sixth hour (Figure 6). Infusions of 1 nd 2,g/min drenline filed to restore myocrdil power to norml vlues (P < 0.05). At termintion of the experiments, 5 mg/min drenline ws infused nd restored power to control vlues. Coronry blood flow fter endotoxin ws higher during the erly phse of shock thn in the control non-shocked hert, reching pek of 96 ml min-' per g left ventricle (control, 78 ml/min) t 2 h post-endotoxin, therefter declining stedily to 72 ml/min (control, 73 ml/min) within 6 hours. Men increses in coronry blood flow in response to 1-2,jg/min infusions of drenline were regulrly less in experimentl herts thn the controls (P < 0.05), nd this is prticulrly evident by 6 h of shock during n infusion of 5 jg/min drenline (P < 0.05). Results indicte tht hert rte chnges fter endotoxin were no different from control non-shocked preprtions. Hert rte responses to drenline infusions of 1, 2 nd 5 ug/min were identicl in both control nd experimentl herts, showing notble increses in both series. At termintion of the studies, during 5,g/min infusions, rtes of experimentl herts incresed from 144 to 170 while controls were elevted similrly from 143 to 168 bets/ minute.
9 ENDOTOXIN AND CARDIAC RESPONSE TO ADRENALINE 153 Discussion The primry initil fctors previously reported to be instrumentl in lowering crdic output during the first 1-2 h of endotoxin shock re peripherl vsculr pooling, extrvstion of plsm, nd the resultnt effect of decresed venous return (Weil et l., 1956; McLen & Weil, 1956; Hinshw, Shnbour, Greenfield & Colson, 1970). Myocrdil performnce in the erly phse of shock ppers to be reltively norml (Goodyer, 1967; Hinshw et l., 1971, 1972; Hinshw, Greenfield, Archer & Guenter, 1971 b), nd the subsequent induction of systemic hypotension elicits sympthodrenl stimultion of the hert, ugmenting its function (Nykiel & Glvino, 1961; Hokfelt et l., 1962; Cvngh et l., 1970; Hll & Hodge, 1971; Hinshw et l., 1971 ; Siegel et l., 1972; Geocris et l., 1973). Substntil evidence hs been produced for prominent role of the myocrdium in the ultimte development of irreversible endotoxin (septic) shock in wide spectrum of niml species nd in mn himself (Hinshw, 1974). The purpose of the present study ws to evlute drenergiclly relted mechnisms which might ccount for the eventul depression of myocrdil function occurring from 2-6 h fter dministrtion of endotoxin or live E. coli orgnisms, s reported by Goodyer (1967), Cvngh et l. (1970), Hinshw et l. (1972c, 1973), Prrtt (1973), Prrtt & Winslow (1974), nd Greenfield, Jckson, Elkins, Colson & Hinshw (1974). It ws hoped tht similr mechnisms to those observed in certin mmmlin species might lso pply to n understnding of the development of hert dysfunction in clinicl septic shock (Siegel et l., 1967, 1972; Bell & Thl, 1970; Cnn et l., 1972; Nishijim et l., 1973). One possible cuse of crdic dysfunction s studied in the present investigtion ws n ltered myocrdil responsiveness to circulting ctecholmines which could presumbly reduce crdic output. Substntil evidence for this possibility hs been presented by others (Cvngh et l., 1970; Bhgt et l., 1970; Prrtt, 1973). Limittions of these erlier reports were tht either only portions of the hert were used in the tests for responsiveness, excluding the left ventricle itself, or tht provisions were lcking to insure constnt delivery of ctecholmine to the myocrdil coronry circultion fter the induction of shock. The methodology of the present study, while fixing crdic inflow (crdic output) nd fterlod t constnt vlues (76 ml min-1 kg-1 nd mmhg, respectively) in the isolted working hert preprtion during constnt infusion rtes of drenline into the left ventricle, rther thn peripherl vein, ssured better controlling fetures of the experiments for dequte interprettion of the dt. Another dvntge of the present preprtion ws tht responses of control (nonshocked) herts to drenline were found to be highly reproducible during 4-5 h period of observtion. Responses of experimentl herts, on the other hnd, were notbly different. Results from the present study document myocrdil dysfunction within 4-6 h fter n LD70 endotoxin dministrtion, s evidenced by sttisticlly significnt elevtions of LVEDP nd depressions of myocrdil efficiency, power, nd negtive nd positive dp/dtmx t fterlods of nd mmhg. Intct support dogs, exchnging blood with the isolted hert nd lso receiving endotoxin, were mrkedly hypotensive during the 6 h observtion period. The notble decrese in negtive dpidtmx vlues is considered to be ssocited with diminished effectiveness of crdic filling during distole (Hinshw et l., 1974b). Findings from the present study suggest significntly ltered responsiveness of certin myocrdil performnce nd hemodynmic prmeters to drenline infusions in herts receiving endotoxin. LVEDP vlues in filing herts decresed during dministrtion of drenline but remined consistently higher thn those in control herts, even when high concentrtions of drenline (5,ug/min) were used to chllenge the myocrdium. Decreses in both positive nd negtive dp/dtmx in dysfunctioning herts could not be restored to norml by drenline infusion, nd this ws prticulrly noted by the observed negtive dpidtmx responses, presumbly reflecting impired crdic filling chrcteristics. On the other hnd, lrge doses of drenline (5 pg/min) essentilly restored crdic power clcultions to norml in filing herts, which ws pprently due to improved crdic contrctility chrcteristics. Men increses in coronry blood flow in response to drenline infusion were regulrly less in experimentl herts thn the controls, nd this observtion my ber cusl reltionship to the development of hert dysfunction fter endotoxin. This ws prticulrly evident within 5-6 h of shock during n infusion of 5 Mg/min drenline (P < 0.05). Hert rte, in contrst, responded similrly to drenline in both filing nd non-filing (control) preprtions. These findings suggest reltively depressed responsiveness of the cnine hert model to drenline dministrtion during the development of myocrdil filure. Depressed myocrdil efficiency nd decresed inotropic nd coronry blood flow responses to drenline were regulrly
10 154 L.T. ARCHER, M.R. BLACK & L.B. HINSHAW observed while chronotropic chrcteristics were not modified in the shocked stte. These results re in greement with Prrtt's study (1973) in endotoxin-treted cts, except tht decresed chronotropic responsiveness to drenline ws lso reported. Bhgt et l. (1970) observed reduced sensitivity of isolted guine-pig tri to nordrenline fter endotoxin which reched mximum depression within 6-18 h fter endotoxin dministrtion. Cvngh et l. (1970) described depressed responsiveness of the isolted bboon trium to nordrenline within 4 h fter endotoxin. These guine-pig nd bboon tril responses ber distinct similrities to our cnine hert results with drenline, both s to type of depression nd time required for its ppernce fter endotoxin. Resons for reduced responsiveness to drenline or nordrenline re not known. In n interesting recent investigtion, Drucker, Pindyck, Brown, Elwyn & Shoemker (1974) pointed out tht hypertonic glucose infusion in ptients gretly enhnced the myocrdil inotropic effect of dministered glucgon. The ugmented myocrdil response to glucgon in the presence of dequte glucose included incresed crdic output nd left ventriculr stroke work. In recent study (Hinshw, Peyton, Archer, Blck, Colson & Greenfield, 1 974c), significntly incresed survivl rte ws observed when hypoglycemi elicited by endotoxin in dogs ws prevented by infusing hypertonic glucose in mounts sufficient to mintin rteril blood glucose concentrtions constnt. In view of both this study nd the findings of Drucker et l. (1974), it might be surmised tht myocrdil inotropic responses to ctecholmines in shock could be improved in the presence of dequte substrte delivery to the my ocrdium. Another suggested mechnism for reduced myocrdil responsiveness to drenline is tht endotoxin my inhibit denosine 5'-triphosphte (ATP)-dependent clcium uptke by the srcoplsmic reticulum, which could depress the contrction process (Hess & Briggs, 1971). Shinebourne, Hess, White & Hmer (1969) reported tht the effect of nordrenline on myocrdil contrctility is directly relted to the incresed rte of clcium uptke by the srcoplsmic reticulum. A similr linkge my hve explined the incresed inotropic responses of herts dministered endotoxin nd treted with digoxin (Hinshw et l., 1973). Finlly, decreses in ph hve been implicted in explining ltered myocrdil responsiveness to ctecholmine stimultion (Thrower, Drby, Aldinger, Tenney & Westbrook, 1959; Drby, Aldinger, Gdsen & Thrower, 1960). In the present study, men rteril ph vlues in both control nd experimentl groups rnged between 7.35 nd 7.45, nd there ws no pprent correltion between responsiveness to drenline nd ph in individul experiments. The precise role of the sympthodrenl system in shock is difficult to interpret. Depression of myocrdil responsiveness to circulting ctecholmines nd sympthetic stimuli hve been implicted in explining decresed hert function in shock. On the other hnd, excessive sympthodrenl stimuli re known to elicit severe myocrdil tissue dmge (Plmerio et l., 1962; Lundsgrd-Hnsen, Meyer, Riedwyl & Zierrot, 1969). The reltive dverse contributions of these influences on the pthogenesis of myocrdil dysfunction in shock remin to be elucidted. This reserch ws supported by the USPHS NIH grnt HL 137, U.S. Nvy Contrct N A-0496, the Oklhom Hert Assocition, nd the Veterns Administrtion Hospitl. Apprecition is expressed to Beverly Beller, Jenette Glsgow nd R.T. Brntley for technicl ssistnce. References BELL, H. & THAL, A. (1970). The peculir hemodynmics of septic shock. Postgrd. Med., 48, BHAGAT, B., CAVANAGH, D., MERRILD, B.N. RANA, M.W. & RAO, P.S. (1970). Nordrenline nd tyrmine ction on isolted tril muscle of endotoxin-treted guine-pigs. Br. J. Phrmc., 39, CANN, M., STEVENSON, T., FIALLOS, E. & THAL, A.P. (1972). Depressed crdic performnce in sepsis. Surg. Gyniec. Obstet., 134, CAVANAGH, D., RAO, P.S., SUTTON, D.M.C., BHAGAT, B.D. & BACHMANN, F. (1970). Pthophysiology of endotoxin shock in the primte. Am. J. Obstet. Gvnec., 108, DARBY, T.D., ALDINGER, E.E., GADSEN, R.H. & THROWER, W.B. (1960). Effects of metbolic cidosis on ventriculr isometric systolic tension nd the response of epinephrine nd levrterenol. Circ. Res., 8, DRUCKER, M.R., PINDYCK, F., BROWN, R.S., ELWYN, D.H. & SHOEMAKER, W.C. (1974). The interction of glucgon nd glucose on crdiorespirtory vribles in the criticlly ill ptient. Surgery, 75, GEOCARIS, T.V., QUEBBEMAN, E., DEWOSKIN, R. & MOSS, G.S. (1973). Effects of grm negtive endotoxemi on myocrdil contrctility in the wke primte. Ann. Surg., 178, GLAVIANO, V.V. & KLOUDA, M.A. (1965). Myocrdil
11 ENDOTOXIN AND CARDIAC RESPONSE TO ADRENALINE 155 ctecholmines nd stimultion of the steilte gnglion in hemorrhgic shock. Am. J. Physiol., 209, GOODYER, A.V.N. (1967). Left ventriculr function nd tissue hypoxi in irreversible hemorrhgic nd endotoxin shock. AnL J. Physiol., 212, GREENFIELD, L.J., JACKSON, R.H., ELKINS, R.C., COALSON, J.J. & HINSHAW, L.B. (1974). Crdiopulmonry effects of volume loding of primtes in endotoxin shock. Surgery, 76, HALL, R.C. & HODGE, R.L. (1971). Vsoctive hormones in endotoxin shock: A comprtive study in cts nd dogs. J. Physiol., Lond., 213, HESS, M.L. & BRIGGS, F.N. (1971). The effect of grm negtive endotoxin on the clcium uptke ctivity of srcoplsmic reticulum isolted from cnine myocrdium. Biochemn Biophysics. Res. Comm., 45, HINSHAW, L.B. (1974). Role of the hert in the pthogenesis of endotoxin shock: A review of the clinicl findings nd observtions on niml species. J. Surg. Res., 17, HINSHAW, L.B., ARCHER, L.T., BLACK, M.R., ELKINS, R.C., BROWN, P.P. & GREENFIELD, L.J. (1974). Myocrdil function in shock. Am. J. Physiol., 226, HINSHAW, L.B., ARCHER, L.T., BLACK, M.R., GREENFIELD, L.J. & GUENTER, C.A. (1973). Prevention nd reversl of myocrdil filure in endotoxin shock. Surg. Gynec. Obstet., 136, HINSHAW, L.B., ARCHER, L.T., GREENFIELD, L.J. & GUENTER, C.A. (1971). Effects of endotoxin on myocrdil hemodynmics, performnce nd metbolism. Am J. Physiol., 221, HINSHAW, L.B., ARCHER, L.T., GREENFIELD, L.J., GUENTER, C.A. & MILLER, J.A. (1972). Effect of endotoxin on myocrdil performnce. J. Trum, 12, HINSHAW, L.B., ARCHER, L.T., SPITZER, J.J., BLACK, M.R., PEYTON, M.D. & GREENFIELD, L.J. (1974b). Effects of coronry hypotension nd endotoxin on myocrdil performnce. Am. J. PhysioL, 227, HINSHAW, L.B., GREENFIELD, L.J., ARCHER, L.T. & GUENTER, C.A. (1971b). Effects of endotoxin on myocrdil hemodynmics, performnce nd metbolism during bet drenergic blockde. Proc. Soc. exp. Biol. Med., 137, HINSHAW, L.B., GREENFIELD, L.J., OWEN, S.E., ARCHER, L.T. & GUENTER, C.A. (1972b). Crdic response to circulting fctors in endotoxin shock. Am. J. PhysioL, 222, HINSHAW, L.B., GREENFIELD, L.J., OWEN, S.E., BLACK, M.R. & GUENTER, C.A. (1972c). Precipittion of crdic filure in endotoxin shock. Surg. Gynec. Obstet., 135, HINSHAW, L.B., PEYTON, M.D., ARCHER, L.T., BLACK, M.R., COALSON, J.J. & GREENFIELD, L.J. (1974c). Prevention of deth in endotoxin shock by glucose dministrtion. Surg. Gynec. Obstet., 139, HINSHAW, L.B., SHANBOUR, L.L., GREENFIELD, L.J. & COALSON, J.J. (1970). Mechnism of decresed venous return in subhumn primte dministered endotoxin. Arch. Surg.,, HOKFELT, B., BYGDEMAN, S. & SEKKENES, J. (1962). The prticiption of the drenl glnds in endotoxin shock. In Shock, Pthogenesis nd Therpy, Internt. Symp., ed. Bock, K.D. pp Berlin: Springer. LUNDSGAARD-HANSEN, P., MEYER, C., RIEDWYL, H. & ZIERROT, G. (1969). Crdic metbolism in experimentl hemorrhgic shock. Minn. Med., 52, MACLEAN, L.D. & WEIL, M.H. (1956). Hypotension (shock) in dogs produced by Escherichi coli endotoxin. Circ. Res., 4, NISHIJIMA, H., WEIL, M.H., SHUBIN, H. & CAVANILLES, J. (1973). Hemodynmic nd metbolic studies on shock ssocited with grm negtive bcteremi. Medicine, 52, NYKIEL, F. & GLAVIANO, V.V. (1961). Adrenl ctecholmines in E. coli endotoxin shock. J. Appl. Physiol., 16, PALMERIO, C., MING, S.C., FRANK, E.D. & FINE, J. (1962). Crdic tissue response to endotoxin. Proc. Soc. exp. BioL Med., 109, PARRATT, J.R. (1973). Myocrdil nd circultory effects of E. coli endotoxin; modifiction of responses to ctecholmines. Br. J. Phrmc., 47, PARRATT, J.R. & WINSLOW, E. (1974). The hemodynmic effects of quzodine, crdic stimulnt, in experimentl E. coli endotoxin shock in the ct. Clin. exp. Phrmc. Physiol, 1, SHINEBOURNE, E.A., HESS, M.L., WHITE, R.J. & HAMER, J. (1969). The effect of nordrenline on the clcium uptke of the srcoplsmic reticulum. Crdiovsc. Res., 3, SIEGEL, J.H., GREENSPAN, M. & DEL GUERCIO, L.R.M. (1967). Abnorml vsculr tone, defective oxygen trnsport nd myocrdil filure in humn septic shock. Ann. Surg., 165, SIEGEL, J.H., FARRELL, E.J., GOLDWYN, R.M. & FRIEDMAN, H.P. (1972). Myocrdil function in humn septic shock sttes. In Shock in Low- nd High-Flow Sttes, ed. Forscher, B.K., Lillehei, R.C. & Stubbs, S.S. pp Amsterdm: Excerpt Medic. SOLIS, R.T. & DOWNING, S.E. (1966). Effects of E. coli endotoxemi on ventriculr performnce. Am. J. Physiol., 211, THROWER, W.B., DARBY, T.D., ALDINGER, E.E., TENNEY, J.M. & WESTBROOK, S.H. (1959). Studies on the reltionship between sympthodrenl function, cid bse derngements nd ventriculr contrctile force. Surg. Forum, 10, WEIL, M.H., MACLEAN, L.D., VISSCHER, M.B. & SPINK, W.W. (1956). Studies on the circultory chnges in the dog produced by endotoxin from grm-negtive microorgnisms. J. Clin. Invest., 35, (Received October 15, Revised December 24, 1974) I I
Comparison of three simple methods for the
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