Respiration Physiolog); 89 (1992) 147-155 O 1992 Elsevier Science Publishers B.V. All rights reserved. 0034-5687/92/$05.00
147
RESP 01931
Respiratory mechanics of the coatimundi and woodchuck Dona F. Boggs a and Charles G. Irvin b aDi~,ision of Biological Sciences. Uni~,ersiO,of Montana. Missoula. Monmm~. and b Di~,isio, of Pulmonary Sciences. Departme, t of Medic#w. National Jewish Centerfor bm,tmology a,d Respiratory Medici~w a,d U, iversiO, of Colorado Health Science Center. Dem,er. Colorado. USA (Accepted 13 April 1992) Abstract. The coatimundi breathes with a large tidal volume and relatively short TE/TTOT while the woodchuck has a relatively long TE/TTOT compared to other mammals. Hence, the respiratory mechanics of the coatimundi and woodchuck were studied to determine whether mechanics play any role in the differences in breathing pattern observed in these two mammals of similar body size. Although static respiratory system compliance was less and lower airway resistance was greater in the woodchuck compared to the coati there was no significant difference in deflationary time constant that could contribute to the difference in expiratory time. Both species exhibit less compliant chest walls than would be predicted for animals this size (4.5 and 5 kg) and the coati lung compliance is greater than that of the woodchuck or the prediction. The large tidal volume in the coati may be attributed in part to the large lung volume of this species (2.2 times the allometric prediction). The differences in breathing pattern are more likely related to differences in the control of breathing (i.e. regulation of expiratory airflow and inspiratory onset) than to differences in respiratory mechanics.
Mammals, coatimundi: Mammals, woodchuck: Mechanics of breathing, coatimundi t,s woodchuck; Pattern of breathing, respiratory mechanics (coatimundi t:~,woodchuck)
The pattern of the respiratory cycle of a given animal is the result of a complex interaction of the integrated output of the central control network directing the respiratory pump, and the mechanical characteristics of that pump. Bennett and Tenney (1982) suggested that passive respiratory mechanics play a major role in determining expiratory time (TE) and total breath time (TTOT) during quiet breathing. Boggs and Tenney (1984)subsequently demonstrated that the ratio of TE/TTOT is, as predicted from mechanical considerations, an interspecific constant with a value of 0.65 during awake quiet breathing in eleven species ranging in size from 0.03 to 520 kg. However, quiet expiration is not strictly a passive relaxation, but may be slowed by laryngeal and diaphragmatic 'braking' mechanisms, as observed in the cat and human (Gautier et al.,
Correspondence to: D. F. Boggs, Division of Biological Sciences, University of Montana, Missoula, Montana 59812, USA.
148
O.F. BOGGS AND C.G. IRVIN
1973; England et eL, 1982), or accelerated by active contraction of the abdominal muscles as observed in the dog (Farkas et eL, 1989) or horse (Koterba et el., 1988). The extent to ~vhich such mechanisms are or are not employed by other species may be a function both of the mechanics of the respiratory system (e.g., chest wall compliance, Stradling et al., 1987) and the chemosensitivity of the control system. Furthermore the duration of an end-expiratory pause may vary depending on the chemosensitivity of the inspiratory 'on-switch' mechanism (Bowes et al., 1982). In the course of other studies of the coatimundi (Nasua naria) (Boggs et el., 1984) and the woodchuck (Marmota monax) (Boggs and Birchard, 1989), it was noted that these species deviated in opposite ways from the usual mammalian breathing pattern. The coatimundi spends a shorter fraction of each breath in expiration while the woodchuck h~s a longer TP/TToT. The coati also has quite a large tidal volume for its body size (see average spirograms in Fig. 1). A number of different mechanisms could account for the clearly different breathing patterns of these two species presented in the different spirograms. The purpose of this study was to investigate the mechanical properties of the respiratory systems of these two species which might account for their peculiar breathing patterns. In particular, we hypothesized that, relative to other species, the woodchuck might have increased airflow resistance and/or high respiratory system compliance which would account for its long expiratory phase. On the other hand, the coatimundi might be expected to have a low airway resistance and/or low respiratory system compliance which would account for its short expiratory phase. As the results show, the mechanical properties of these animals do not totally explain their individual breathing patterns which prompted a second investigation (Boggs et eL, 1992) which focussed on the species differences in chemosensitivity and control of breathing.
Materhils sad method1
Animal subjects The coatimundis (N~tropical relatives ofthe raccoon) were obtained from zoos or zoo suppliers. Eleven adults were studied, of which 6 were raised in captivity. The mean body weight was $.12 kg (_+ 1.25). The seven adult woodchucks studied were trapped in Maryland, and had an average body weight of 4.5 kg ( ± 0.4). Not all the measurements were made on every animal, hence the numbers studied are presented in each table.
Spont,,eo,s memlestketi=edbre,thing patter, Ventilation was measured by the barometric method while the animal was unanesthericed and unrestrained in a whole-body plethysmograph (Bartlett and Tenney. 1970). The ambient temperature was maintained below 26 °C and the measurer~ents were taken only while the animal was awake but quiet. Body temperature was monitored either as rectal temperature measured with a YSI thermistor probe before and after
RESPIRATORY MECHANICS OF COATIS AND WOODCHUCKS
149
recordings in the plethysmograph, or with Mini-mitter transmitters (Sunriver, OR) implanted in the dorsal region of the abdominal cavity. Respirato~ mechanics Respiratory system compliance was measured in the anesthetized intubated animal by the single breath method ofZin et al., 1982, as well as post=mortem by inflationary and deflationary pressure-volume curves (Bennett and Tenney, 1982). The animal was anesthetized initially with ketamine (22 mg/kg l.M.), followed by small doses of pentobarbital as needed (6-10 mg/kg l.V.). They were intubated with an endotracheal tube (Rusch 4.0) which was connected to a heated Fieisch pneumotachograph (Statham PMIS). Differential pressure (flow), integrated inspiratory flow (= tidal volume, VT) and airway pressure (Validyne DP45) were recorded on an oscillographic recorder (Gould 2400). The airway was occluded at end=inspiration in the spontaneously breathing animal and the volume of that breath was divided by the tracheal pressure during the relaxation against the closed airway to obtain a measure of respiratory system compliance (CRS). These maneuvers were performed at least three times and the average value obtained. Later, post=mortem measurements of inflationary and deflationary pressure-volume curves were made for the whole system, and in some instances for the excised lungs as well. Six known volumes (Hewlet~ Packard Calibration Syringe) were injected and airway pressure recorded (Validyne Differential Pressure DP45). The respiratory system time constant (zRS) was obtained from the decay of the deflationary flow record after inflation to a pressure of 8 cmH.,O (Bennett and Tenney, 1982). Lower airway resistance was then calculated from the time constant and compliance, (¢RS - CRS' RRS), subtracting the resistance of the pneumotach and endotrachoal tube. Upper airway resistance was assessed by administering a known flow into the trachea in a rostral direction with the mouth closed while measuring the pressure difference across the upper airway. Lung volumes wor¢ measured by volume displacement. Excised lungs wore dried in the inflated state (at 30 cmH20 pressure), coated with a thin layer of paraffin, and submerged in a water volume displacement measuring device. Measurements ofthe static and dynamic lung compliance and resistance characteristics of three of the coatis were also made with somewhat different techniques (at Na= tional 3ewish Hospital in Denver). The anesthetized, intubated animals were placed supine within a volume displacement plethysmograph. Volume was measured with a linear displacement transducer (Schavitz Engineering, Pennsachen, NJ; ~ype ES00) and a plexiglass Krogh spirometer. An esophageal balloon/suction catheter was placed in the lower esophagus to measure esophageal pressure. The balloon was positioned to achieve maximal swings in pressure, maximal negative pressure at end-expiration and minimal transpulmonu~y pressure changes during occlusion. The plethysrnograph was tested for frequency response and was pressure compensated (Macklern and Mead, 1968). Adequate frequency response and phase respon':e of flow, volume and pressure were achieved up to 15 Hz. The endotracheal tube was externalized to a heated Fleisch pneumotachograph (Gould Electronics). Flow and pressures were oh-
150
D.F. BOGGS AND C.G. IRVIN
rained with differential pressure transducers (Validyne MP-45, Northridge, CA). All signals were connected to AC carrier demodulators (Validyne, CD-19). Pulmonary compliance and resistance were derived from an analog computer (Hewlett-Packard; Model 8816A) using the electrical subtraction technique. A record ofquiet breathing was obtained from which breathing pattern and dynamic lung mechanics were derived. The animals were then paralyzed with pancuronium bromide (Pavulon) (0.3 cc) to obtain pressure-volume and flow-volume relationships. The lungs were inflated three times to a transpuimonary pressure of 30 cmH20 to provide a constant lung volume history. Lungs were then twice inflated to TLC with each deflation interrupted at frequent intervals so that an adequate number (20) of pressure and volume points were obtained. The data from these deflations were pooled and an exponential curve fit to the data points. Static lung compliance was calculated over a range of volume twice that of a tidal volume. Respiratory system time constant and resistance were calculated from the slope of the flow-volume trace (subtracting apparatus resistance) during tidal ventilations of the paralyzed animal. (Static compliance measurements from these paralyzed animals did not differ substantially from values obtained postmortem). The data are presented as mean values plus or minus one standard error. The comparisons between measured values and allometrically predicted values were made
60-
/
A
/
.40 E
\
Coati
\
n
\ \
E
\
m
>o
\
2O
\ 1
2 Time
3
(see)
Fig, I, A schematic representation of the average spin)gram of the coatimundi and woodchuck, indicating the difference in volume and timing characteristics of the average breath cycle.
RESPIRATORY MECHANICS OF COATIS AND WOODCHUCKS
151
using a 2-tailed t-test. Predicted values (p) were calculated for each individual for which there were measured values (m) and combined for a mean predicted value (as opposed to making one calculation on the basis of the mean weight of the group). Comparisons between species were also made using 2-tailed t-tests (Sokal and Rohlf, 1981). R e s u l t s and d i s c u s s i o n
The comparative resting breathing patterns of awake unrestrained coatimundis a n d woodchucks are presented in Table 1, and schematically in Fig. 1. Coatimundis tend to be slightly but not significantly larger than the woodchucks. The coatimundi has a significantly larger tidal volume than either the woodchuck or the value predicted for a mammal this size (Stahl, 1967). The breathing frequency of the coatimundi is not significantly different from the woodchuck although both breathe more slowly than predicted (Table 1). The total breath time is not significantly different but the coatimundi spends more of it in inspiration and less of it in expiration. Therefore the fraction of total breath time spent in inspiration, 0.48, is significantly longer in the coatimundi than the woodchuck, 0.26, or the expected 0.35 (Boggs and Tenney, 1984), and the fraction of time in expiration is correspondingly significantly shorter in the coatis, 0.52, than in the woodchucks, 0.74, or the expected case, 0.65. The total ventilation in the coati is not significantly different from that predicted from their body mass
TABLE i
Comparative resting breathing patterns Species
Coatis (5.1 kg) (n- 11) Predicted" P value Woodchucks (4.48 kg) (, = 6) Predicted P value P value (interspeciflc)
VT f (ml BTPS) (rain ~:t)
Tt (sec)
Te
5$ 3
23.2 1.8
1.28 0.09
!.38 0.10
42 3 0.01
35.3 0.7 0.001
35 4.7
23 3
36 3.6 NS
36 0.8 0.05
0.005
NS
0.7 0. I 1
TTOT
TI/TTOT
TE/TTOT (ml/min)
2.4 0.5
2.68 0.48 0.27 0.02
3,1 0,6
0.005 0.001 NS
Means ± I SE. a Predictionsfrom Stahl, 1967, or Boggs and Tenney, 1984.
0.52 0.02
1248 89
0.35 0,004 0.001
0.65 0.004 0.001
1393 82 NS
0.26 0.028
0.74 0.028
743 53
0.35 0.004 0.001
0.65 0.004 0.00 i
0.001
0.001
1252 98 0.001 0.01
152
D.F. BOGGS AND C.G. IRVIN TABLE 2
Lung volumes Lung vol. (m)
Lung vol. (p)"
Measured/Predicted
VT/VL
616 74
286 32
2.2 0.18
0.09 0.006
295 47
292 42
I 0.04
O.! I 0.02
(ml)
Coatis 4.85 kg
(0.52) (.~,8)
Woodchucks 4.96 kg
(0.67) (n - 3)
" Prediction from Stahl. 1967. VL = :ung volume.
but is substantially greater than total ventilation in the woodchuck. The woodchuck value is significantly less than predicted for an animal its size. The large tidal volume in the coati can be explained in part by the large lung volume of this species. As indicated in Table 2, the woodchuck lung volume is equivalent to the predicted for a mammal this size whereas the coati's lung volume is 2.2 times greater than expected. The tidal volumes represent a similar fraction of total lung volume in both species (9-11%). it is apparent from Table 3 that there is substantial variation in lung volume per unit body mass. The coati seems to share the characteristic of a large lung volume with dogs (Robinson and Gillespk;, 1973) and ferrets (Boyd
trod Mangos, 198 l), TABLE 3
Comparative lung volumes and tidal volumes
Species
Body weight
TLC or VI.
(kg)
(ml)
TLC or VUk8
YT (% TLC)
127 $9,6 86 130 90 35 158 36 59
9 II 8 15
........
Coati Woodchuck Human* Dogh Rhesus monkey~
Rabbit° Ferret~ Ratr Hamster~
4,85 4.95 70 9,7 3,4 3.2 03 0,23 0,12
616 29:$ 6000 1264 503 III 50 8 7
21 8 17 17
TLC ~ total lung cap;icily; VL - lung volume; VT = tidal volume, * Comroe er ~d,, 1%9; ~' Robinson and Gillespie, 1973; ': Pare et,l,, 1978; 'j Caldwell and Fry, 1969; '=Boyd and Mangos, 1981: r Diamond and O'Donnell, 1977; t~Ken e r e I., 1976,
153
RESPIRATORY MECHANICS OF COATIS AND WOODCHUCKS TABLE 4 Comparative respiratory system mechanics Woodchucks Measured CRS (ml/cmH_,O)
Coatimundis Predicted"'
5.24b'~ 0.313
7.5 0.73
n = 7
CL
10.15 0.59
0.41 n = 3
RAW
(cmHaO/mi sec - i)
24.9
2.2 11=3 0.0242 ~ 0.002
1.6 0.0234 0.0015
(s~) TRAW+RUA
0.138 0.023 n = 7 0.281 0.065 n - 3
3.3
18,6 4. I
14.6b
2.5 11=4 0.018 0.0036
30.5
5.1 0.0235 0.0027
n = 5
0.028 ! 0.0048
0.0206 0.0014
n = 3
t
I0 38.8 b
9.02 0.98
n= 4
I 1.2b
n = 7
RUA
8.394 0.922
Predicted
n =
9.47 ~
Cow
Measured
0.0229 0.0048
0.0193 0.0018
n = 5
0.174
0,15
0.175
0.004
0.028
0.016
n = 5
,
0.303 0.009
0.292 0.049
0.313 0.018
n - 4
" Predictions from Bennett and Tenney, 1982, h Significantly different from predicted. Significantly different from the other species, CRs - respiratory system compliance; CL - lung compliance; Cow - chest wall compliance, (computed from l:Clts - IICL + I/Cow); RAW - lower airway resistance; RUA - upper airway resistance (t.e. larynx, pharo ynx and nasal passages); T-time constant (computed from Cas RAw); tR+AU^ ~ total time constant (comput~l from CRs [RAW + RUR]).
The comparative static respiratory mechanics are presented in Table 4. The static respiratory system compliance (CRs) of the woodchuck is significantly less than that of the coati and the predicted value. The coati has substantially higher lung compliance (CL) than the woodchuck or the prediction and both species have less compliant chest walls (Ccw) than predicted. The lower airway resistance (RAw) of the coati is significantly less than the woodchucks but not statistically different from the predicted value. Upper airway resistance (RuA) tended to be somewhat greater in both species than predicted but not significantly so. The time constants, particularly those calculated from the combined upper and lower airway resistances (tR + tRUA), are remarkably similar between species and not significantly different from predicted values.
154
D.F. BOGGS AND C.G. IRViN TABLE 5 Mean dynamic compliance and resistance of three coatis
Lung compliance (ml (cmH20)- l)
32
Resistance (cmU20 ml- ! sec- 1) Insp.
Expir.
Peak-to-Peak
0.0092
0.01082
0.00886
Another possible explanation for the unusual breathing pattern observed in the coatimundi would be the occurrence of a marked difference in the inspiratory to expiratory resistance. Specifically, we thought that there might be a marked phasic reduction in expiratory resistance. Although the data on dynamic lung compliance and resistance (Table 5) in the coatimundis studied did demonstrate, by another method, high lung compliance, it did not show a marked phasic difference in inspiratory and expiratory resistance. The differences between these species in breathing pattern are not readily attributable to differences in mechanical characteristics of their respiratory systems. The large tidal volume in the coati is consistent with its large lung volume. The high lung compliance and low chest wall compliance in the coati is similar to that observed in dogs (Mead and Collier, 1959) and rhesus monkeys (Pare et al., 1978). The relatively stiff chest wall may be associated with the coatis locomotor behavior in being both climbers and long distance runners. The woodchucks share the characteristic of a stiff chest wall with the coatis, which, in the absence of a similarly elevated lung compliance, contributes to a reduced total system compliance. Although the woodchuck total system compliance was less, the resistance was $reatcr, creating the not effect of no difference in passive deflationary time constant of the respiratory systems even when including the upper airways. Without any difference in passive deflationary time constants, the differences in expiratory times and Te/TTOT must be attributable to differences in control of expiratory airflow and inspiratory onset. Such differences in the respiratory control system of these two species are pursued in the following paper (Boggs et al., t992). Acknowledllements. This study was supported by NSF Grant no. DCB -8608661. We wish to acknowledge the assistance of S.E. Hol'meister and George Baltopoulos w~th the ¢oatis,
References Bartlett, D. Jr. and S. M, Tenney (1970). Control of breathing in experimental anemia. Respir. PkystoA 10: 384-395. Bennett, F. M. and S. M. Tenney (1982). Comparative mechanics of mammalian respiratory system. RespiP. Pllystol. 49: 131--140.
RESPIRATORY MECHANICS OF COATIS AND WOODCHUCKS
155
Boggs, D.F., S.E. Hofmeister and W.W. Wagm:r, Jr. (1984). Large hypoxic presser responses in the coatimundi. Fed. Prec. 43: 920. Boggs, D.F. and S.M. Tenney (1984). Scaling respiratory pattern and respiratory 'drive'. Respir. Physiol. 58: 245-251. Boggs, D.F. and G.F. Birehard (1989). Cardio-respiratory responses of the woodchuck and porcupine to CO, and hypoxia. J. Comp. Physiol. 159B: 641-648. Boggs, D.F., C. Colby, B.R. Williams, Jr. and D.L.Kilgore, Jr. (1992). Chemosensitivity and breathing pattern regulation of the coatimundi and woodchuck. Respir. Physiol. 89:147-156 Bowes, G., S.M. Andre),, L.F. Kozar and E.A. Phillipson (1982). Role of carotid chemoreceptors in regulation of inspiratory onset. J. Appl. Physiol. 52: 863-868. Boyd, R.L. and J.A. Mangos (1981). Pulmonary mechanics of the normal ferret. J. Appl. Physiol. 50: 799-804. Caldwell, E.J. and D.L. Fry (1969). Pulmonary mechanics in the rabbit. J. Appl. PIL~viol. 27: 280-285. Comroo, J.H., R.E. Forstor, A.B. DuBois, W.A. Briscoe and E. Carlson (1969). The lung: clinical physiology and pulmonary function tests. Chicago, IL: Year Book, pp. 323-329. Diamond, L. and M. O'DonnoU (1977). Pulmonary mechanics in normal rats. J. Appl. Physiol. 43: 942-948. England, S., D. Bartlett, Jr. and J.A. Daubonspock (1982). Influence of human vocal cord movements on airflow and resistance in eupnea. J. Appl. Phyviol. 52: 773-779. Farkas, G.A., M. Estonne and A. DeTroyvr (1989). Expiratory musole contribution to tidal volume in head-up dogs. J. Appl. Physiol. 67: 1438-1442. Gautier, H., J. E. Rommors and D. Bartlett, Jr. (1973). Control of the duration of expiration. Re.vpir. Playsiol. 18:205-22 I. Kotorba, A. M., P.C. Kosch, J. Beech and T. Whitlock (I 988). Breathing strategy of the adult horse (Equus caballus) at rest. J. Appl. Phy.~'ol. 64: 337-346. Koo, W. K., D.E. Leith, C.B. Shorter and G.L. Snider (1"976). Respiratory mechanics in normal hamster. J. Appl. Physiol. 40: 936-942. Macklem, P.T. and J. Mead (1968). Factors determining maximum expiratory flow in dogs. J. Appl. Phy~viol. 25: 159-169. Mead, J. and C. Collier (1959). Relation of volume history of lungs to respiratory mechanics in anesthetized dogs. J. Appl, Plo',vlol. 14: 669. Pare, P. D., R, Boucher, M.-C. Michoud and J.C. Hogg (1978). Static lung mechanics of intact and excised rhesus monkey lungs and lobes. J. Appl. Phy~'i,l. 44: 547-552. Robinson, N, E, and J.R, Oillespie (1973). Lung volumes in aging beagle dogs. J. Appl. Phyviol. 35: 317321, Sokal, R. R. and F.J. Rohlf(1981). Biometry: Principles and practice of statistics in biological research. San Francisco: W, H. Freeman. Stahl, W.R. (1967). Scaling of respiratory variables in mammals. J. Appl. Phy~iol. 22: 453=460. Stradling, J. R., S.J. England, R. Harding, L. F. Kozar, S. Andrey and E.A. Phillipson (1987). Role of upper airway in vontilatory control in awake and sleeping dogs. J. Appl. Physiol. 62: 1167-I 173. Zin, W.A., L.D. Pongolly and J. Milie-Emili (1982). Single breath method for measurement of respiratory mechanics in anesthetized animals. J. Appl. Physiol. 52:1266-127 I.
147
RESP 01931
Respiratory mechanics of the coatimundi and woodchuck Dona F. Boggs a and Charles G. Irvin b aDi~,ision of Biological Sciences. Uni~,ersiO,of Montana. Missoula. Monmm~. and b Di~,isio, of Pulmonary Sciences. Departme, t of Medic#w. National Jewish Centerfor bm,tmology a,d Respiratory Medici~w a,d U, iversiO, of Colorado Health Science Center. Dem,er. Colorado. USA (Accepted 13 April 1992) Abstract. The coatimundi breathes with a large tidal volume and relatively short TE/TTOT while the woodchuck has a relatively long TE/TTOT compared to other mammals. Hence, the respiratory mechanics of the coatimundi and woodchuck were studied to determine whether mechanics play any role in the differences in breathing pattern observed in these two mammals of similar body size. Although static respiratory system compliance was less and lower airway resistance was greater in the woodchuck compared to the coati there was no significant difference in deflationary time constant that could contribute to the difference in expiratory time. Both species exhibit less compliant chest walls than would be predicted for animals this size (4.5 and 5 kg) and the coati lung compliance is greater than that of the woodchuck or the prediction. The large tidal volume in the coati may be attributed in part to the large lung volume of this species (2.2 times the allometric prediction). The differences in breathing pattern are more likely related to differences in the control of breathing (i.e. regulation of expiratory airflow and inspiratory onset) than to differences in respiratory mechanics.
Mammals, coatimundi: Mammals, woodchuck: Mechanics of breathing, coatimundi t,s woodchuck; Pattern of breathing, respiratory mechanics (coatimundi t:~,woodchuck)
The pattern of the respiratory cycle of a given animal is the result of a complex interaction of the integrated output of the central control network directing the respiratory pump, and the mechanical characteristics of that pump. Bennett and Tenney (1982) suggested that passive respiratory mechanics play a major role in determining expiratory time (TE) and total breath time (TTOT) during quiet breathing. Boggs and Tenney (1984)subsequently demonstrated that the ratio of TE/TTOT is, as predicted from mechanical considerations, an interspecific constant with a value of 0.65 during awake quiet breathing in eleven species ranging in size from 0.03 to 520 kg. However, quiet expiration is not strictly a passive relaxation, but may be slowed by laryngeal and diaphragmatic 'braking' mechanisms, as observed in the cat and human (Gautier et al.,
Correspondence to: D. F. Boggs, Division of Biological Sciences, University of Montana, Missoula, Montana 59812, USA.
148
O.F. BOGGS AND C.G. IRVIN
1973; England et eL, 1982), or accelerated by active contraction of the abdominal muscles as observed in the dog (Farkas et eL, 1989) or horse (Koterba et el., 1988). The extent to ~vhich such mechanisms are or are not employed by other species may be a function both of the mechanics of the respiratory system (e.g., chest wall compliance, Stradling et al., 1987) and the chemosensitivity of the control system. Furthermore the duration of an end-expiratory pause may vary depending on the chemosensitivity of the inspiratory 'on-switch' mechanism (Bowes et al., 1982). In the course of other studies of the coatimundi (Nasua naria) (Boggs et el., 1984) and the woodchuck (Marmota monax) (Boggs and Birchard, 1989), it was noted that these species deviated in opposite ways from the usual mammalian breathing pattern. The coatimundi spends a shorter fraction of each breath in expiration while the woodchuck h~s a longer TP/TToT. The coati also has quite a large tidal volume for its body size (see average spirograms in Fig. 1). A number of different mechanisms could account for the clearly different breathing patterns of these two species presented in the different spirograms. The purpose of this study was to investigate the mechanical properties of the respiratory systems of these two species which might account for their peculiar breathing patterns. In particular, we hypothesized that, relative to other species, the woodchuck might have increased airflow resistance and/or high respiratory system compliance which would account for its long expiratory phase. On the other hand, the coatimundi might be expected to have a low airway resistance and/or low respiratory system compliance which would account for its short expiratory phase. As the results show, the mechanical properties of these animals do not totally explain their individual breathing patterns which prompted a second investigation (Boggs et eL, 1992) which focussed on the species differences in chemosensitivity and control of breathing.
Materhils sad method1
Animal subjects The coatimundis (N~tropical relatives ofthe raccoon) were obtained from zoos or zoo suppliers. Eleven adults were studied, of which 6 were raised in captivity. The mean body weight was $.12 kg (_+ 1.25). The seven adult woodchucks studied were trapped in Maryland, and had an average body weight of 4.5 kg ( ± 0.4). Not all the measurements were made on every animal, hence the numbers studied are presented in each table.
Spont,,eo,s memlestketi=edbre,thing patter, Ventilation was measured by the barometric method while the animal was unanesthericed and unrestrained in a whole-body plethysmograph (Bartlett and Tenney. 1970). The ambient temperature was maintained below 26 °C and the measurer~ents were taken only while the animal was awake but quiet. Body temperature was monitored either as rectal temperature measured with a YSI thermistor probe before and after
RESPIRATORY MECHANICS OF COATIS AND WOODCHUCKS
149
recordings in the plethysmograph, or with Mini-mitter transmitters (Sunriver, OR) implanted in the dorsal region of the abdominal cavity. Respirato~ mechanics Respiratory system compliance was measured in the anesthetized intubated animal by the single breath method ofZin et al., 1982, as well as post=mortem by inflationary and deflationary pressure-volume curves (Bennett and Tenney, 1982). The animal was anesthetized initially with ketamine (22 mg/kg l.M.), followed by small doses of pentobarbital as needed (6-10 mg/kg l.V.). They were intubated with an endotracheal tube (Rusch 4.0) which was connected to a heated Fieisch pneumotachograph (Statham PMIS). Differential pressure (flow), integrated inspiratory flow (= tidal volume, VT) and airway pressure (Validyne DP45) were recorded on an oscillographic recorder (Gould 2400). The airway was occluded at end=inspiration in the spontaneously breathing animal and the volume of that breath was divided by the tracheal pressure during the relaxation against the closed airway to obtain a measure of respiratory system compliance (CRS). These maneuvers were performed at least three times and the average value obtained. Later, post=mortem measurements of inflationary and deflationary pressure-volume curves were made for the whole system, and in some instances for the excised lungs as well. Six known volumes (Hewlet~ Packard Calibration Syringe) were injected and airway pressure recorded (Validyne Differential Pressure DP45). The respiratory system time constant (zRS) was obtained from the decay of the deflationary flow record after inflation to a pressure of 8 cmH.,O (Bennett and Tenney, 1982). Lower airway resistance was then calculated from the time constant and compliance, (¢RS - CRS' RRS), subtracting the resistance of the pneumotach and endotrachoal tube. Upper airway resistance was assessed by administering a known flow into the trachea in a rostral direction with the mouth closed while measuring the pressure difference across the upper airway. Lung volumes wor¢ measured by volume displacement. Excised lungs wore dried in the inflated state (at 30 cmH20 pressure), coated with a thin layer of paraffin, and submerged in a water volume displacement measuring device. Measurements ofthe static and dynamic lung compliance and resistance characteristics of three of the coatis were also made with somewhat different techniques (at Na= tional 3ewish Hospital in Denver). The anesthetized, intubated animals were placed supine within a volume displacement plethysmograph. Volume was measured with a linear displacement transducer (Schavitz Engineering, Pennsachen, NJ; ~ype ES00) and a plexiglass Krogh spirometer. An esophageal balloon/suction catheter was placed in the lower esophagus to measure esophageal pressure. The balloon was positioned to achieve maximal swings in pressure, maximal negative pressure at end-expiration and minimal transpulmonu~y pressure changes during occlusion. The plethysrnograph was tested for frequency response and was pressure compensated (Macklern and Mead, 1968). Adequate frequency response and phase respon':e of flow, volume and pressure were achieved up to 15 Hz. The endotracheal tube was externalized to a heated Fleisch pneumotachograph (Gould Electronics). Flow and pressures were oh-
150
D.F. BOGGS AND C.G. IRVIN
rained with differential pressure transducers (Validyne MP-45, Northridge, CA). All signals were connected to AC carrier demodulators (Validyne, CD-19). Pulmonary compliance and resistance were derived from an analog computer (Hewlett-Packard; Model 8816A) using the electrical subtraction technique. A record ofquiet breathing was obtained from which breathing pattern and dynamic lung mechanics were derived. The animals were then paralyzed with pancuronium bromide (Pavulon) (0.3 cc) to obtain pressure-volume and flow-volume relationships. The lungs were inflated three times to a transpuimonary pressure of 30 cmH20 to provide a constant lung volume history. Lungs were then twice inflated to TLC with each deflation interrupted at frequent intervals so that an adequate number (20) of pressure and volume points were obtained. The data from these deflations were pooled and an exponential curve fit to the data points. Static lung compliance was calculated over a range of volume twice that of a tidal volume. Respiratory system time constant and resistance were calculated from the slope of the flow-volume trace (subtracting apparatus resistance) during tidal ventilations of the paralyzed animal. (Static compliance measurements from these paralyzed animals did not differ substantially from values obtained postmortem). The data are presented as mean values plus or minus one standard error. The comparisons between measured values and allometrically predicted values were made
60-
/
A
/
.40 E
\
Coati
\
n
\ \
E
\
m
>o
\
2O
\ 1
2 Time
3
(see)
Fig, I, A schematic representation of the average spin)gram of the coatimundi and woodchuck, indicating the difference in volume and timing characteristics of the average breath cycle.
RESPIRATORY MECHANICS OF COATIS AND WOODCHUCKS
151
using a 2-tailed t-test. Predicted values (p) were calculated for each individual for which there were measured values (m) and combined for a mean predicted value (as opposed to making one calculation on the basis of the mean weight of the group). Comparisons between species were also made using 2-tailed t-tests (Sokal and Rohlf, 1981). R e s u l t s and d i s c u s s i o n
The comparative resting breathing patterns of awake unrestrained coatimundis a n d woodchucks are presented in Table 1, and schematically in Fig. 1. Coatimundis tend to be slightly but not significantly larger than the woodchucks. The coatimundi has a significantly larger tidal volume than either the woodchuck or the value predicted for a mammal this size (Stahl, 1967). The breathing frequency of the coatimundi is not significantly different from the woodchuck although both breathe more slowly than predicted (Table 1). The total breath time is not significantly different but the coatimundi spends more of it in inspiration and less of it in expiration. Therefore the fraction of total breath time spent in inspiration, 0.48, is significantly longer in the coatimundi than the woodchuck, 0.26, or the expected 0.35 (Boggs and Tenney, 1984), and the fraction of time in expiration is correspondingly significantly shorter in the coatis, 0.52, than in the woodchucks, 0.74, or the expected case, 0.65. The total ventilation in the coati is not significantly different from that predicted from their body mass
TABLE i
Comparative resting breathing patterns Species
Coatis (5.1 kg) (n- 11) Predicted" P value Woodchucks (4.48 kg) (, = 6) Predicted P value P value (interspeciflc)
VT f (ml BTPS) (rain ~:t)
Tt (sec)
Te
5$ 3
23.2 1.8
1.28 0.09
!.38 0.10
42 3 0.01
35.3 0.7 0.001
35 4.7
23 3
36 3.6 NS
36 0.8 0.05
0.005
NS
0.7 0. I 1
TTOT
TI/TTOT
TE/TTOT (ml/min)
2.4 0.5
2.68 0.48 0.27 0.02
3,1 0,6
0.005 0.001 NS
Means ± I SE. a Predictionsfrom Stahl, 1967, or Boggs and Tenney, 1984.
0.52 0.02
1248 89
0.35 0,004 0.001
0.65 0.004 0.001
1393 82 NS
0.26 0.028
0.74 0.028
743 53
0.35 0.004 0.001
0.65 0.004 0.00 i
0.001
0.001
1252 98 0.001 0.01
152
D.F. BOGGS AND C.G. IRVIN TABLE 2
Lung volumes Lung vol. (m)
Lung vol. (p)"
Measured/Predicted
VT/VL
616 74
286 32
2.2 0.18
0.09 0.006
295 47
292 42
I 0.04
O.! I 0.02
(ml)
Coatis 4.85 kg
(0.52) (.~,8)
Woodchucks 4.96 kg
(0.67) (n - 3)
" Prediction from Stahl. 1967. VL = :ung volume.
but is substantially greater than total ventilation in the woodchuck. The woodchuck value is significantly less than predicted for an animal its size. The large tidal volume in the coati can be explained in part by the large lung volume of this species. As indicated in Table 2, the woodchuck lung volume is equivalent to the predicted for a mammal this size whereas the coati's lung volume is 2.2 times greater than expected. The tidal volumes represent a similar fraction of total lung volume in both species (9-11%). it is apparent from Table 3 that there is substantial variation in lung volume per unit body mass. The coati seems to share the characteristic of a large lung volume with dogs (Robinson and Gillespk;, 1973) and ferrets (Boyd
trod Mangos, 198 l), TABLE 3
Comparative lung volumes and tidal volumes
Species
Body weight
TLC or VI.
(kg)
(ml)
TLC or VUk8
YT (% TLC)
127 $9,6 86 130 90 35 158 36 59
9 II 8 15
........
Coati Woodchuck Human* Dogh Rhesus monkey~
Rabbit° Ferret~ Ratr Hamster~
4,85 4.95 70 9,7 3,4 3.2 03 0,23 0,12
616 29:$ 6000 1264 503 III 50 8 7
21 8 17 17
TLC ~ total lung cap;icily; VL - lung volume; VT = tidal volume, * Comroe er ~d,, 1%9; ~' Robinson and Gillespie, 1973; ': Pare et,l,, 1978; 'j Caldwell and Fry, 1969; '=Boyd and Mangos, 1981: r Diamond and O'Donnell, 1977; t~Ken e r e I., 1976,
153
RESPIRATORY MECHANICS OF COATIS AND WOODCHUCKS TABLE 4 Comparative respiratory system mechanics Woodchucks Measured CRS (ml/cmH_,O)
Coatimundis Predicted"'
5.24b'~ 0.313
7.5 0.73
n = 7
CL
10.15 0.59
0.41 n = 3
RAW
(cmHaO/mi sec - i)
24.9
2.2 11=3 0.0242 ~ 0.002
1.6 0.0234 0.0015
(s~) TRAW+RUA
0.138 0.023 n = 7 0.281 0.065 n - 3
3.3
18,6 4. I
14.6b
2.5 11=4 0.018 0.0036
30.5
5.1 0.0235 0.0027
n = 5
0.028 ! 0.0048
0.0206 0.0014
n = 3
t
I0 38.8 b
9.02 0.98
n= 4
I 1.2b
n = 7
RUA
8.394 0.922
Predicted
n =
9.47 ~
Cow
Measured
0.0229 0.0048
0.0193 0.0018
n = 5
0.174
0,15
0.175
0.004
0.028
0.016
n = 5
,
0.303 0.009
0.292 0.049
0.313 0.018
n - 4
" Predictions from Bennett and Tenney, 1982, h Significantly different from predicted. Significantly different from the other species, CRs - respiratory system compliance; CL - lung compliance; Cow - chest wall compliance, (computed from l:Clts - IICL + I/Cow); RAW - lower airway resistance; RUA - upper airway resistance (t.e. larynx, pharo ynx and nasal passages); T-time constant (computed from Cas RAw); tR+AU^ ~ total time constant (comput~l from CRs [RAW + RUR]).
The comparative static respiratory mechanics are presented in Table 4. The static respiratory system compliance (CRs) of the woodchuck is significantly less than that of the coati and the predicted value. The coati has substantially higher lung compliance (CL) than the woodchuck or the prediction and both species have less compliant chest walls (Ccw) than predicted. The lower airway resistance (RAw) of the coati is significantly less than the woodchucks but not statistically different from the predicted value. Upper airway resistance (RuA) tended to be somewhat greater in both species than predicted but not significantly so. The time constants, particularly those calculated from the combined upper and lower airway resistances (tR + tRUA), are remarkably similar between species and not significantly different from predicted values.
154
D.F. BOGGS AND C.G. IRViN TABLE 5 Mean dynamic compliance and resistance of three coatis
Lung compliance (ml (cmH20)- l)
32
Resistance (cmU20 ml- ! sec- 1) Insp.
Expir.
Peak-to-Peak
0.0092
0.01082
0.00886
Another possible explanation for the unusual breathing pattern observed in the coatimundi would be the occurrence of a marked difference in the inspiratory to expiratory resistance. Specifically, we thought that there might be a marked phasic reduction in expiratory resistance. Although the data on dynamic lung compliance and resistance (Table 5) in the coatimundis studied did demonstrate, by another method, high lung compliance, it did not show a marked phasic difference in inspiratory and expiratory resistance. The differences between these species in breathing pattern are not readily attributable to differences in mechanical characteristics of their respiratory systems. The large tidal volume in the coati is consistent with its large lung volume. The high lung compliance and low chest wall compliance in the coati is similar to that observed in dogs (Mead and Collier, 1959) and rhesus monkeys (Pare et al., 1978). The relatively stiff chest wall may be associated with the coatis locomotor behavior in being both climbers and long distance runners. The woodchucks share the characteristic of a stiff chest wall with the coatis, which, in the absence of a similarly elevated lung compliance, contributes to a reduced total system compliance. Although the woodchuck total system compliance was less, the resistance was $reatcr, creating the not effect of no difference in passive deflationary time constant of the respiratory systems even when including the upper airways. Without any difference in passive deflationary time constants, the differences in expiratory times and Te/TTOT must be attributable to differences in control of expiratory airflow and inspiratory onset. Such differences in the respiratory control system of these two species are pursued in the following paper (Boggs et al., t992). Acknowledllements. This study was supported by NSF Grant no. DCB -8608661. We wish to acknowledge the assistance of S.E. Hol'meister and George Baltopoulos w~th the ¢oatis,
References Bartlett, D. Jr. and S. M, Tenney (1970). Control of breathing in experimental anemia. Respir. PkystoA 10: 384-395. Bennett, F. M. and S. M. Tenney (1982). Comparative mechanics of mammalian respiratory system. RespiP. Pllystol. 49: 131--140.
RESPIRATORY MECHANICS OF COATIS AND WOODCHUCKS
155
Boggs, D.F., S.E. Hofmeister and W.W. Wagm:r, Jr. (1984). Large hypoxic presser responses in the coatimundi. Fed. Prec. 43: 920. Boggs, D.F. and S.M. Tenney (1984). Scaling respiratory pattern and respiratory 'drive'. Respir. Physiol. 58: 245-251. Boggs, D.F. and G.F. Birehard (1989). Cardio-respiratory responses of the woodchuck and porcupine to CO, and hypoxia. J. Comp. Physiol. 159B: 641-648. Boggs, D.F., C. Colby, B.R. Williams, Jr. and D.L.Kilgore, Jr. (1992). Chemosensitivity and breathing pattern regulation of the coatimundi and woodchuck. Respir. Physiol. 89:147-156 Bowes, G., S.M. Andre),, L.F. Kozar and E.A. Phillipson (1982). Role of carotid chemoreceptors in regulation of inspiratory onset. J. Appl. Physiol. 52: 863-868. Boyd, R.L. and J.A. Mangos (1981). Pulmonary mechanics of the normal ferret. J. Appl. Physiol. 50: 799-804. Caldwell, E.J. and D.L. Fry (1969). Pulmonary mechanics in the rabbit. J. Appl. PIL~viol. 27: 280-285. Comroo, J.H., R.E. Forstor, A.B. DuBois, W.A. Briscoe and E. Carlson (1969). The lung: clinical physiology and pulmonary function tests. Chicago, IL: Year Book, pp. 323-329. Diamond, L. and M. O'DonnoU (1977). Pulmonary mechanics in normal rats. J. Appl. Physiol. 43: 942-948. England, S., D. Bartlett, Jr. and J.A. Daubonspock (1982). Influence of human vocal cord movements on airflow and resistance in eupnea. J. Appl. Phyviol. 52: 773-779. Farkas, G.A., M. Estonne and A. DeTroyvr (1989). Expiratory musole contribution to tidal volume in head-up dogs. J. Appl. Physiol. 67: 1438-1442. Gautier, H., J. E. Rommors and D. Bartlett, Jr. (1973). Control of the duration of expiration. Re.vpir. Playsiol. 18:205-22 I. Kotorba, A. M., P.C. Kosch, J. Beech and T. Whitlock (I 988). Breathing strategy of the adult horse (Equus caballus) at rest. J. Appl. Phy.~'ol. 64: 337-346. Koo, W. K., D.E. Leith, C.B. Shorter and G.L. Snider (1"976). Respiratory mechanics in normal hamster. J. Appl. Physiol. 40: 936-942. Macklem, P.T. and J. Mead (1968). Factors determining maximum expiratory flow in dogs. J. Appl. Phy~viol. 25: 159-169. Mead, J. and C. Collier (1959). Relation of volume history of lungs to respiratory mechanics in anesthetized dogs. J. Appl, Plo',vlol. 14: 669. Pare, P. D., R, Boucher, M.-C. Michoud and J.C. Hogg (1978). Static lung mechanics of intact and excised rhesus monkey lungs and lobes. J. Appl. Phy~'i,l. 44: 547-552. Robinson, N, E, and J.R, Oillespie (1973). Lung volumes in aging beagle dogs. J. Appl. Phyviol. 35: 317321, Sokal, R. R. and F.J. Rohlf(1981). Biometry: Principles and practice of statistics in biological research. San Francisco: W, H. Freeman. Stahl, W.R. (1967). Scaling of respiratory variables in mammals. J. Appl. Phy~iol. 22: 453=460. Stradling, J. R., S.J. England, R. Harding, L. F. Kozar, S. Andrey and E.A. Phillipson (1987). Role of upper airway in vontilatory control in awake and sleeping dogs. J. Appl. Physiol. 62: 1167-I 173. Zin, W.A., L.D. Pongolly and J. Milie-Emili (1982). Single breath method for measurement of respiratory mechanics in anesthetized animals. J. Appl. Physiol. 52:1266-127 I.
