Findings of this study were presented at the 18th ECVIM-CA Congress, Ghent, Belgium, 2008
Pulmonary Artery Thrombosis in Experimental Angiostrongylus vasorum Infection Does Not Result in Pulmonary Hypertension and Echocardiographic Right Ventricular Changes
Article first published online: 11 MAY 2010
Copyright © 2010 by the American College of Veterinary Internal Medicine
Journal of Veterinary Internal Medicine
Volume 24, Issue 4, pages 855–862, July/August 2010
How to Cite
Kranjc, A., Schnyder, M., Dennler, M., Fahrion, A., Makara, M., Ossent, P., Morgan, J., Deplazes, P. and Glaus, T.M. (2010), Pulmonary Artery Thrombosis in Experimental Angiostrongylus vasorum Infection Does Not Result in Pulmonary Hypertension and Echocardiographic Right Ventricular Changes. Journal of Veterinary Internal Medicine, 24: 855–862. doi: 10.1111/j.1939-1676.2010.0529.x
- Issue published online: 1 JUL 2010
- Article first published online: 11 MAY 2010
- Submitted December 3, 2009; Revised February 24, 2010; Accepted March 19, 2010.
- Blood gas;
Background: Dogs experimentally inoculated with Angiostrongylus vasorum develop severe pulmonary parenchymal lesions and arterial thrombosis at the time of patency.
Hypothesis: A. vasorum-induced thrombosis results in arterial hypoxemia, pulmonary hypertension (PH), and altered cardiac morphology and function.
Animals: Six healthy Beagles experimentally inoculated with A. vasorum.
Methods: Thoracic radiographs and arterial blood gas analyses were performed 8 and 13 weeks postinoculation (wpi) and 9 weeks posttherapy (wpt). Echocardiography was done before and 2, 5, 8, 13 wpi and 9 wpt. Invasive pulmonary artery pressure (PAP) measurements were obtained 8 wpi. Two untreated dogs were necropsied 13 wpi and 4 treated dogs 9 wpt.
Results: All dogs had patent infections at 7 wpi and clinical respiratory signs at 8 wpi. Moderate hypoxemia (median PaO2 of 73 and 74 mmHg) present at 8 and 13 wpi had resolved by 9 wpt. Echocardiographically, no evidence of PH and no abnormalities in cardiac size and function were discernible at any time point. PAP invasively measured at 8 wpi was not different from that of control dogs. Severe radiographic pulmonary parenchymal and suspected thrombotic lesions at 13 wpi were corroborated by necropsy. Most histopathologic changes had resolved at 9 wpt, but focal inflammatory, thrombotic, and fibrotic changes still were present in all dogs.
Conclusion: In experimentally infected Beagles, pulmonary and vascular changes induced by A. vasorum are reflected by marked radiographic changes and arterial hypoxemia. These did not result in PH and echocardiographic changes in cardiac size and function.
pulmonary artery pressure
pulmonic valve insufficiency
pressure gradient of PI
partial oxygen pressure
tricuspid valve insufficiency
pressure gradient of TI
Angiostrongylus vasorum is a ubiquitous metastrongylid heartworm of dogs and related canids. It has an indirect life cycle with gastropods (slugs and snails) acting as intermediate hosts.1,2 Infected dogs develop severe pulmonary parenchymal lesions at the time of patency because of intense immune responses to egg and larval antigens, including eosinophilic inflammation, hemorrhage, arterial thrombosis, periarteritis, and coalescing granulomata.3 These pathological changes result in various degrees of radiographic changes.4,5 In experimentally infected dogs, these abnormalities have been described to be most pronounced at 7–9 weeks postinoculation (wpi).4
Pulmonary vascular inflammation and pulmonary thrombosis (PT) are important mechanisms of secondary pulmonary hypertension (PH), heartworm infection being the most important cause in dogs.6–9 However, despite its widespread distribution, reports of PH in natural A. vasorum infection are scant,10−12 and the authors are unaware of any study evaluating the development of PH under clearly defined experimental conditions. The goal of the present study was to evaluate by echocardiography ventricular size and function in dogs experimentally infected with A. vasorum. Of special interest were time point and severity of developing PH and secondary changes in parameters of right ventricular (RV) function. Secondary goals were to relate echocardiographic changes to clinical, radiographic, and arterial blood gas changes, and to assess the situation after anthelmintic therapy.
Materials and Methods
This study was part of a project at the Institute of Parasitology, Vetsuisse Faculty, University of Zurich, primarily designed to establish an experimental A. vasorum model in dogs for additional diagnostic and therapeutic investigations. Study design including infective load, time until treatment, anthelmintics used, time until euthanasia, and necropsy was dictated by that project. Approval by the Cantonal Veterinary Office of Zurich was obtained before the start of the study. Briefly, 6 Beagles were studied (2 males, 4 females), 5 dogs were 2 years old and 1 dog was 6 years old, and body weights were 12–15 kg. These Beagles were inoculated with A. vasorum, 3 with 50 3rd stage larvae (light grade, lgr) and 3 with 500 3rd stage larvae (high grade, hgr). Dogs received a daily clinical examination with focus on respiratory abnormalities. The success of inoculation was demonstrated by repetitive Baermann examinations of feces with all dogs having patent infection 7 wpi (Schnyder et al, unpublished data). Two dogs were euthanized at 13 wpi, and 4 dogs (2 lgr and 2 hgr) received anthelmintic therapy. Of these, 2 dogs (1 lgr and 1 hgr) received moxidectin-imidacloprida (5.08 and 5.84 mg/kg for moxidectin, 20.33 and 23.35 mg/kg for imidacloprid), the other 2 dogs received an experimental compound. Ten weeks posttherapy (wpt), these 4 dogs were euthanized. At necropsy, the lungs were first examined macroscopically, then flushed by a special perfusion procedure to recover and quantitate the number of worms.13 Thereafter, in treated and untreated dogs, samples for routine microscopic examination were chosen from the lesions macroscopically most affected.
Echocardiography was performed before and 2, 5, 8, and 13 wpi, and 9 wpt with the operator blinded to the infectious load. Images were obtained with an Acuson Sequoia 512,b from the unsedated dogs placed in right and left lateral recumbency on a cardiac table using standard views.14 Two-dimensional (2D) and motion mode (M-mode) echocardiographic images were obtained with a 7 MHz transducer, and color, pulse wave, and continuous wave images were obtained with a 3.5 MHz transducer. Images to calculate left ventricle (LV) and RV Tei-indices were obtained as described previously.15,16 Primary parameters to assess the presence and degree of PH were peak pressure gradients of pulmonic and tricuspid valve insufficiencies (PI-PG and TI-PG). PH was considered to be present, if a clinically significant increase in PI-PG or TI-PG over time occurred or if PI-PG was >20 mmHg and TI-PG was >30 mmHg; an estimated right atrium (RA) pressure was not added to the TI-PG to more exactly calculate systolic pulmonary artery pressure (sPAP).17–19 Additional parameters to estimate the presence of PH were RV acceleration time and acceleration to ejection time ratio.20−22
Routine left lateral and ventrodorsal thoracic radiographs were obtained at 8 and 13 wpi, and 9 wpt in unsedated dogs. Radiographs were evaluated by 2 different radiologists blinded to the time of inoculation and inoculation grade. Predetermined radiographic criteria were presence, degree and distribution of bronchial, interstitial, and alveolar patterns, pulmonary vascular lesions, pleural fluid or air, evidence of hilar lymphadenopathy, tracheal or mediastinal lesions, and presence of right-sided cardiomegaly.5,23
Arterial blood gas analysis was performed at 8 and 13 wpi, and 9 wpt. Blood samples, collected from the femoral artery with a heparinized syringe, were immediately analyzed with a portable clinical analyzer.c
Invasive PAP measurements were obtained 8 wpi. The dogs were sedated with a combination of fentanyld (5 μg/kg IV) and diazepame (0.25 mg/kg IV). The aseptically prepared venipuncture site was locally anesthetized with lidocaine.f Propofolg was added as needed to keep the dogs immobile but anesthesia as light as possible. A Swan-Gantz catheter was inserted into the left jugular vein and advanced into RA, RV, and pulmonary artery (PA) under fluoroscopic control. Systolic and diastolic PAP (sPAP, dPAP) were measured while the dogs were breathing room air and again 5 minutes after providing 100% inhaled O2. Ten 2–4-year-old healthy Beagles from the same colony were used as controls.
Statistical analyses were done by commercial softwareh and nonparametric tests. The Wilcoxon test was used to compare the differences in the infected Beagles over time and the Mann-Whitney U-test to compare results between infected and control Beagles. P values < .05 were considered significant. Results are given as median and range.
Patency and Clinical Signs
The prepatent period in A. vasorum-inoculated dogs was 47–49 days. The respiratory rate at baseline was 24 bpm (range, 10–32 bpm). The 1st respiratory signs (eg, very short bouts of hacking cough when excited, tachypnea, increased abdominal respiratory efforts, increased lung sounds) were observed 42–56 days postinoculation (dpi) and increased in severity until 56–70 dpi. The peak respiratory rate was 58 bpm (range, 32–92 bpm) at 63 dpi. One dog had mildly cyanotic mucous membranes at 70 dpi. Decreased appetite with loss of body weight was observed in all dogs and intermittent increased rectal temperature up to 40.5°C in 5 of 6 dogs. In all dogs with lgr-infection clinical signs had virtually resolved by 13 wpi. All dogs with hgr infection were still symptomatic at 13 wpi, but signs tended to improve. All treated dogs were asymptomatic 2 wpt and had negative fecal examination results 2–3 wpt.
No abnormalities were detectable on 2D echocardiography, and parasites were not seen in the pulmonary artery or right heart at any time during the study. Although mild to moderate pleural effusion was found at 8 wpi in 5 dogs, no signs of increased RA pressure (eg, enlarged RA, distended veins, ascites) were detected. Furthermore, no significant changes could be observed in cardiac size or function on M-mode or Doppler echocardiography. The results of quantitative parameters to assess LV and RV size and function as well as to assess PH are summarized in Tables 1 and 2; and Figure 1 shows the calculated RV Tei index during the course of infection.
|Time 0||8 wpi||13 wpi||9 wpt|
|LVDd (cm)||3.1 (2.8–3.6)||3.0 (2.7–3.5)||3.0 (2.6–3.4)||3.0 (2.8–3.1)|
|LVDs (cm)||2.0 (1.8–2.1)||2.1 (1.7–2.3)||1.9 (1.5–2.1)||2.1 (1.8–2.1)|
|Ao Vmax (m/s)||1.6 (1.3–1.8)||1.5 (1.3–1.8)||1.6 (1.3–1.8)||1.4 (1.4–1.5)|
|Ao VTI||0.16 (0.13–0.17)||0.15 (0.13–0.15)||0.15 (0.13–0.17)||0.15 (0.14–0.16)|
|LV PEP (ms)||58 (47–61)||58 (51–65)||57 (53–60)||55 (51–61)|
|LV ET (ms)||174 (172–183)||173 (172–181)||174 (171–183)||176 (172–183)|
|LV PEP/ET||0.33 (0.28–0.35)||0.33 (0.29–0.36)||0.33 (0.30–0.35)||0.31 (0.28–0.35)|
|LV AT (ms)||49 (39–57)||47 (45–55)||48 (44–51)||55 (44–57)|
|LV AT/ET||0.28 (0.22–0.32)||0.28 (0.26–0.32)||0.28 (0.26–0.29)||0.31 (0.30–0.32)|
|MV E (m/s)||0.89 (0.70–1.02)||0.60 (0.57–0.81)||0.80 (0.69–0.85)||0.76 (0.72–0.87)|
|MV A (m/s)||0.70 (0.37–0.95)||0.48 (0.44–0.57)||0.58 (0.47–0.75)||0.52 (0.47–0.54)|
|TA (ms)||85 (73–93)||91 (87–95)||94 (78–102)||84 (81–99)|
|Dec TE (ms)||92 (82–103)||96 (83–105)||98 (85–114)||79 (71–93)|
|LV Tei index||0.39 (0.32–0.40)||0.40 (0.34–0.41)||0.39 (0.32–0.41)||0.38 (0.33–0.41)|
|Time 0||8 wpi||13 wpi||9 wpt|
|RVWDd (cm)||1.0 (0.7–1.3)||1.2 (0.8–1.5)||1.1 (0.4–1.3)||1.1 (0.9–1.3)|
|RVDd (cm)||0.35 (0.31–0.56)||0.51 (0.31–0.55)||0.42 (0.30–0.49)||0.43 (0.30–0.54)|
|PA Vmax (m/s)||1.1 (0.8–1.3)||0.9 (0.9–1.2)||1.0 (0.9–1.2)||1.0 (0.8–1.1)|
|PA VTI||0.13 (0.11–0.15)||0.11 (0.10–0.14)||0.13 (0.12–0.14)||0.12 (0.09–0.19)|
|RV PEP (ms)||45 (43–52)||46 (41–51)||47 (39–50)||48 (46–49)|
|RV ET (ms)||185 (183–187)||185 (182–188)||184 (180–186)||186 (184–189)|
|RV PEP/ET||0.25 (0.23–0.28)||0.25 (0.23–0.27)||0.25 (0.22–0.27)||0.26 (0.24–0.27)|
|RV AT (ms)||75 (63–86)||78 (75–84)||81 (77–86)||90 (81–96)|
|RV AT/ET||0.41 (0.34–0.46)||0.43 (0.41–0.45)||0.44 (0.42–0.46)||0.48 (0.44–0.52)|
|TV E (m/s)||0.72 (0.66–0.83)||0.69 (0.47–0.77)||0.67 (0.59–0.73)||0.68 (0.62–0.84)|
|TV A (m/s)||0.52 (40–69)||0.49 (40–76)||0.55 (44–57)||0.44 (37–64)|
|TV E/A||1.4 (1.2–1.7)||1.3 (0.9–1.8)||1.3 (1.2–1.4)||1.6 (1.3–1.7)|
|RV Tei index||0.22 (0.19–0.23)||0.21 (0.19–0.22)||0.22 (0.19–0.24)||0.21 (0.18–0.23)|
|TI PG (mmHg)||25 (6–32)||23 (12–24)||19 (14–23)||21 (15–24)|
In all dogs, a trivial to mild tricuspid valve insufficiency (TI) jet could be identified, but not at each time point. Pulmonic valve insufficiency (PI) could not be documented consistently with color Doppler at all time points in all dogs. A TI-PG of 33 mmHg (ie, above the predefined threshold of PH) was obtained in 1 Beagle before inoculation. No echocardiographic evidence of PH could be documented at any time point during the study. The calculated TI-PG was 25 mmHg (range, 6–33 mmHg) at baseline, and did not change significantly during the course of infection (Fig 2). The calculated PI-PG was always <20 mmHg (median, 7 mmHg; range, 4–13 mmHg) without change during or after infection.
At 8 wpi, marked radiographic abnormalities with a mixed pattern were observed in all dogs. All dogs showed a generalized slight to moderate bronchial pattern with bronchial wall thickening. A generalized interstitial pattern was observed in all dogs. It was slight to moderate in lgr- and moderate to severe in hgr-infected dogs. All dogs showed an alveolar pattern with air bronchograms, which was multifocal but mainly peripheral (Fig 3A), and earlier and more pronounced in hgr-infected dogs. In 4 dogs (2 lgr and 2 hgr infected) enlarged pulmonary arteries were observed and in 1 hgr-infected dog tortuous pulmonary arteries were found (Fig 4). Pleural effusion was present in 5 dogs, a moderate amount in 2 hgr-infected dogs (Fig 3B) and a slight amount in 1 hgr- and 2 lgr-infected dogs. In 2 hgr-infected dogs slight to moderate hilar lymphadenopathy was suspected. At 13 wpi compared with 8 wpi, the bronchial and interstitial lung patterns were static, but the alveolar pattern had clearly progressed in all dogs (Fig 3C), lgr-infected dogs were still less severely affected than hgr-infected dogs. Vascular findings were unchanged. The pleural effusion was markedly diminished. The shape, radiopacity, and position of the main stem bronchi were suspicious for hilar lymphadenomegaly. Widening of the cranial mediastinum was found in 1 hgr and suspected in 1 lgr-infected dog.
At 9 wpt, the alveolar pattern had resolved (Fig 3D). A slight to moderate interstitial pattern still was present in all dogs and a slight bronchial pattern was observed in 3 dogs. The previously enlarged pulmonary arteries had returned to normal size, but tortuous vessels still were observed in 1 dog. The changes in the hilar area and the pleural fissure lines had resolved. The cardiac silhouette was of normal size and shape in all dogs at all time points.
Arterial Blood Gas
At 8 wpi, moderate hypoxemia with a partial oxygen pressure (PO2) of 73 mmHg (range, 66–85 mmHg) was found, the corresponding oxygen saturation (SO2) was 93% (range, 91–95%). At 13 wpi, hypoxemia was not significantly different compared with 8 wpi with a PO2 of 74 mmHg (range, 65–99 mmHg; P= .463) and SO2 of 93% (range, 90–97%; P= .844). At 8 wpi but not 13 wpi, PO2 was lower in hgr-infected dogs compared with lgr-infected dogs, but not significantly (P= .127). By 9 wpt, hypoxemia had significantly improved to a PO2 of 94 mmHg (range, 75–98; P= .038) compared with 8 wpi. The corresponding SO2 was 97% (range, 94–97%).
Invasive PAP Measurements
At 8 wpi, sPAP and dPAP were 31 mmHg (range, 26–35 mmHg) and 15 mmHg (range, 12–22 mmHg) while the dogs were breathing room air, and nonsignificantly decreased to 26 mmHg (range, 23–35 mmHg; P= .174) and 14 mmHg (range, 11–19 mmHg; P= .340) after 5 minute of breathing 100% oxygen. In control dogs, sPAP and dPAP were 23 mmHg (range, 15–36 mmHg) and 12 mmHg (range, 7–21 mmHg) on room air, and not significantly different from infected dogs.
The detailed findings at necropsy are available elsewhere (Schnyder et al, unpublished data). Briefly, 10 and 170 adult A. vasorum specimens were recovered in the 2 untreated dogs. One worm was recovered from 1 hgr-infected dog treated with the registered drug, and 13 worms were recovered from 1 lgr-infected dog treated with the investigational compound. Approximately 80% of the lungs of the 2 untreated animals were consolidated. The treated dogs had far less affected lung tissue, usually restricted to disseminated pale beige slightly raised foci of roughly 1 cm diameter and patches of yellowish discoloration in the aerated tissues. The pulmonary lymph nodes were enlarged and moist in treated and untreated dogs.
Histologically, many parasitic larvae were found in the 2 untreated dogs, and adult parasites but no larvae were found in 1 treated dog with hgr inoculation. The consolidated lung tissue consisted mainly of masses of plasma cells and macrophages. The granulomata consisted mainly of macrophages, multinucleated giant cells, and lymphocytes that had accumulated around larvae and eggs. The inflammatory changes were severe in the 2 untreated dogs, and mild to focally moderate in the 4 treated dogs. Many thrombi were present in the 2 untreated dogs, often associated with parasitic larvae, and some were recanalizing. Often, the arterial walls were thickened. Thrombi also were found in 3 of 4 treated dogs. All 6 dogs showed interstitial fibrosis, which varied from mild to focally severe independent of infectious load or treatment.
In this experimental study, dogs with differing infectious loads of A. vasorum larvae all developed clinical signs of pulmonary disease around the time of patency at 7 wpi. Radiographically, 1 week later marked pulmonary parenchymal abnormalities, evidence of pulmonary arterial abnormalities, and pleural effusion were documented. The infectious load was important for the degree as well as the time course of the pulmonary changes (ie, the hgr-infected dogs developed more severe radiographic changes earlier than did lgr-infected dogs). The specific distribution of the radiographic changes induced by A. vasorum infection was quite typical for this disease; as in previous studies the most pronounced changes occurred at the lung periphery.4,5 This peripheral distribution was not discerned at necropsy, where 80% of the lungs were found to be affected. In some respects, our radiographic findings differed from previous reports. First, in 1 experimental study, the severity of radiographic changes in dogs infected with 150 larvae peaked at 7–9 wpi and thereafter regressed.4 In our study, independent of the infectious load, lesion severity progressed from 8 to 13 wpi. Second, in contrast to the 2 cited studies, we were able to document pulmonary vascular changes suggestive of PT.
Clinical signs and morphological pulmonary changes were associated with abnormalities in gas exchange reflected by moderate arterial hypoxemia. However, whereas radiographic pulmonary lesions progressed in all dogs, hypoxemia did not follow the development of radiographic changes. Specifically, in 2 hgr-infected dogs, hypoxemia was marked at 8 wpi and improved until 13 wpi, into the reference range in 1 dog. On the other hand, at 9 wpt, when the lungs appeared normal radiographically, 3 of 4 dogs had normal PaO2, but 1 dog had not improved compared with 13 wpi. This discrepancy between radiographic lung changes and functional gas exchange might be because of underestimation of lung damage, radiography being an insensitive method in diseases with severe ventilation-perfusion mismatch (eg, in PT).24 At necropsy, thrombosis still was present in this and 2 other treated dogs. Another reason for persisting moderate hypoxemia may have been the persistence of arterio-venous (AV) shunts. Presence of AV shunts in dog lungs has been documented.25–27 Despite persisting hypoxemia at 9 wpt, this dog was clinically normal, and had adapted to chronic moderate hypoxemia.19
Despite important clinical respiratory abnormalities and marked radiographic pulmonary changes including vascular abnormalities suggestive of thrombosis, moderate hypoxemia, and objective pathological findings of endarteritis, relevant pulmonary artery thrombosis, and medial thickening, we were unable to document PH or alteration in cardiac size or function by echocardiography. Underestimation because of technical error was ruled out by invasive PAP measurements, which yielded systolic pressures very similar to calculated pressures based on RV-RA peak pressure gradients. The observation period in our dogs could have been too short, and PH might have developed later during infection. However, PaO2 was already improving in some severely affected dogs and thrombotic vessels were already recanalizing at 13 wpi, indicating improvement at the histologic level. Likewise, during the experimental study by Prestwood et al,3 thrombotic vessels were recanalizing. The described endarteritis with medial hypertrophy in small- and medium-sized arteries and intimal proliferation in large arteries ultimately may result in PH. However, chronic vascular remodeling seems unlikely to be an important cause for development of PH, because in the few reported clinical cases PH quickly normalized after therapy.10,12 Such a quick resolution seems possible if thrombi rather than lesions of vascular remodeling disappear.
The question therefore remains, why, when, and which naturally infected dogs develop PH secondary to A. vasorum infection. Some naturally infected dogs exhibited severe hyperglobulinemia reflecting chronic infection rather than 1 acute high infectious load, even though clinically some of these dogs showed only an acute illness.12 Alternatively, this may reflect individual variability with respect to severity of immunologic response to A. vasorum.28 Individual predisposition for severe thrombosis, individual variation in vascular reactivity or individual capability (or incapacity) for opening AV shunts may be important predisposing factors. Even though AV shunts normally are present in dogs, in 1 out of 4 investigated normal dogs no AV shunt could be documented.26 Absence of such shunts in the lung of some individuals could predispose to development of PH in a case of acute and clinically relevant PT. Finally, relevant PH may only develop at the moment of spontaneous death of a large number of worms. Likewise, in Dirofilaria immitis PH is of special concern within the first 2 weeks of adulticide treatment. Therefore, the chance of detecting PH might have been highest during the first days after treatment. However, no clinical deterioration was observed at any time in any of our dogs posttherapy.
Lastly, experimental infection is not identical to natural infection. Specifically, in our experiment dogs were infected once whereas in nature dogs may repeatedly ingest infected snails. Furthermore, it is unknown how many adult worms develop in naturally infected cases with PH. Therefore, even though the worm burden and objective pulmonary lesions in our experiment were considered severe, both may be more pronounced in naturally infected dogs with PH.
In summary, Beagles experimentally inoculated with A. vasorum developed severe, radiographically visible pulmonary parenchymal and arterial thrombotic changes that correspond to histopathological findings that were largely reversible. Associated clinical signs were attributable to moderate hypoxemia and inflammation. It is unclear why these severe changes did not result in PH. Lack of PH explains lack of changes in cardiac shape and function as assessed by echocardiography.
Limitations of the Study
Arterial blood gas analysis, thoracic radiographs, and PAP were not obtained at each examination time point and particularly not at baseline. Whereas it is unlikely that these clinically, hematologically, and biochemically normal Beagles had relevant pulmonary disease with impaired gas exchange, it is possible that they had significantly lower PAP at baseline compared with 8 wpi. Thus, the omission of this gold standard to obtain PAP does not allow the definitive conclusion that infection with A. vasorum had no effect on PAP. However, PAP calculated noninvasively by echocardiography did not change over the course of infection and invasively and noninvasively obtained results were very similar, which makes a significantly lower PAP at baseline less likely. Most importantly and in view of the goals of this study, the 1 time point of invasive PAP measurement proves that lack of echocardiographic evidence of PH and lack of altered cardiac function at the moment of significant clinical disease associated with severe radiographic changes and moderate arterial hypoxemia was not because of technical error.
After anthelmintic therapy, echocardiographic examinations were only performed at 9 wpt. In naturally infected dogs, PH had already resolved within 3–8 weeks of therapy.10,12 Transient PH associated with acute death of many worms would have been missed. Clinically, however, none of the dogs showed evidence of acute deterioration suggestive of more severe hypoxemia, and the dog most affected clinically did receive an echocardiographic examination 48 hours postanthelmintic therapy without any observable change (data not shown).
aAdvocate, Bayer AG, Leverkusen, Germany
bAcuson Sequoia 512, Siemens, Glattbrugg, Switzerland
cAbbott i-STAT Portable Clinical Analyzer, i-STAT Corporation, East Windsor, CA
dSintenyl, Sintetica S.A., Mendrisio, Switzerland
eValium, Roche Pharma AG, Reinach, Switzerland
fLidocain HCl 2%, Kantonsapotheke, Zürich, Switzerland
gPropofol 1% MCT Fresenius, Fresenius Kabi AG, Stans, Switzerland
hSPSS 11.0 for Windows, SPSS Inc, Chicago, IL
This study was supported by a grant from Bayer Animal Health GmbH, Germany.
- 3Experimental canine angiostrongylosis: I. Pathologic manifestations. J Am Anim Hosp Assoc 1981;17:491–497., , , et al.
- 4Experimental canine angiostrongylosis: II. Radiographic manifestations. J Am Anim Hosp Assoc 1981;17:499–502., , , et al.
- 12Natural Angiostrongylus vasorum infection, characterisation of 3 dogs with pulmonary hypertension (in German). Schweiz Arch Tierheilk 2010;152, in press., , , et al.
- 20Abnormal left ventricular diastolic filling patterns in acute hypoxic pulmonary hypertension at high altitude. Am J Noninvas Cardiol 1993;7:33–38., , , et al.