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Suspected bilateral phrenic nerve damage following a mediastinal mass removal in a 17

week old pug

Mathieu Raillard, Pamela J. Murison, Ivan P. Doran

School of Clinical Veterinary Science, University of Bristol, Langford, North Somerset, UK

Dr. Raillard’s current address is Vetsuisse Faculty, University of Bern, Switzerland; Dr.

Murison’s current address is Royal (Dick) School of Veterinary Studies, University of

Edinburgh, UK.

Address all correspondence to Dr. Mathieu Raillard; e-mail: [email protected]

Acknowledgement: The authors wish to thank Jenny Reeve for her contribution to the case

management.

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Abstract

We describe the anesthetic management of a paediatric pug for removal of a

mediastinal mass. During recovery from anesthesia, the dog’s respiratory pattern was

compatible with bilateral diaphragmatic paralysis. Incidence, complications, possible

treatments of phrenic nerve injury, problems of long-term mechanical ventilation and

alternative case management are discussed.

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The phrenic nerves arise from the 5th to the 7th (occasionally also from the 4th) cervical

nerves and run caudally, dorsomedial to the brachial plexus, in the fascia adjacent to the

external jugular vein. They then unite cranial to the thoracic inlet and pass through the

thoracic inlet between subclavian and omocervical arteries where they are joined by a fine

sympathetic branch. Within the thoracic cavity, each of them lies in narrow plicae of pleura.

They spread out over their respective half of the diaphragm dividing into 3 main branches

(ventral, lateral and dorsal) and supply this muscle with motor and sensory fibres (1). The

diaphragm is the most important muscle of inspiration. When it contracts, its tendinous centre

pushes against the abdominal contents, elevating intra-abdominal pressure, which displaces

the caudal ribs outward and its dome is pulled caudally, enlarging the thoracic cavity (2).

When a phrenic nerve is sectioned, diaphragmatic contraction on that side ceases (3).

Phrenic nerve injury (PNI) is a well-recognized complication of human thoracic

surgery, especially of pediatric cardiac surgery (4,5). To our knowledge PNI has not been

reported in dogs. This case report describes the clinical signs and management of a suspected

bilateral PNI leading to diaphragmatic paralysis following the removal of a large mediastinal

mass in a young pug.

Case description

A 17-week-old pug weighing 2.5 kg was presented at Langford Veterinary Services with a 3-

day history of dyspnea. Since adoption, the dog had had a history of regurgitation post

feeding but this did not occur after ingestion of liquids. Dyspnea had developed acutely.

Thoracic radiographs performed by the referring veterinary surgeon documented a marked

pleural effusion and a mass cranial to the heart. There had been moderate clinical

improvement with furosemide and clavulanate potentiated amoxicillin.

On presentation the dog was bright, alert and playful. He was mildly tachypneic, with

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a moderately restrictive respiratory pattern with an increased expiratory effort. On pulmonary

auscultation, lung sounds could be heard over both lung fields. Hematology revealed a

hematocrit of 27% with mild lymphocytosis [3.7 109 L-1, reference interval (RI): 0.70 to

3.60 109 L-1). Alkaline phosphatase was mildy elevated (6.7 mmol L-1, RI: 3.0 to 5.0 mmol

L-1), changes consistent with the age of the dog. Jugular venous blood gas values and

electrolytes were within reference ranges.

Thoracic computed tomography (CT) identified a heterogeneous, soft-tissue

attenuating cranial thoracic mediastinal mass. The heart was displaced caudally, the great

vessels and esophagus dorsally because of the significant space occupying effect. The right

cranial lung lobe was collapsed and displaced caudally (Figure 1). Abdominal CT scan was

unremarkable.

Anesthesia was scheduled for median sternotomy and mass removal. A 22 gauge

catheter was placed in the left cephalic vein. Methadone (Comfortan, Dechra Veterinary

products, Shrewsbury, Shopshire, UK), 0.2 mg/kg body weight (BW), IV, was given as

premedication. Oxygen was administered by facemask for 5 min prior to induction of

anesthesia with midazolam (Hypnovel, Roche Products, Welwyn Garden City, Hertfordshire,

UK), 0.2 mg/kg BW, IV, and propofol titrated to effect (Propoflo plus; Abbott Laboratories,

Vanwall Road, Maidenhead, UK), 2.4 mg/kg BW, IV. Oro-tracheal intubation was readily

performed with a 3.5 mm cuffed tube. Anesthesia was maintained with sevoflurane (SevoFlo,

Abbott Laboratories) vaporized in oxygen and medical air (FiO2 60%) via a T-piece. During

surgical preparation, the dog breathed spontaneously. Analgesia included paracetamol 25 mg

(Perfalgan, Bristol-Myers Squibb Pharmaceuticals, Uxbridge, Middlesex, UK), 10 mg/kg

BW, administered IV over 15 min before surgery and fentanyl (Fentadon, Dechra Veterinary

products), 5 g bolus followed by infusion, 4 to 6 g/kg BW/h. Hartmann’s solution, 5 mL/kg

BW/h, was infused with a fluid pump throughout the procedure. A multiparametric anesthetic

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monitor (Datex-Ohmeda S/5, GE Healthcare, Little Chalfont, Buckinghamshire, UKMadison,

Wisconsin, USA) was used to monitor pulse-oximetry (SpO2), electrocardiography (ECG),

sidestream capnography and gas analysis (inspired and expired fractions of oxygen and

isoflurane) sampled through an appropriate connector placed between breathing system and

endotracheal tube, spirometry, non-invasive blood pressure (oscillometry with a neonatal size

2 cuff, above the left tarsus) and esophageal temperature. The SpO2 sensor was placed on the

tongue. Heart rate was calculated from the ECG and the lead II was displayed. Several

attempts to catheterize a dorsal metatarsal artery then an auricular artery were unsuccessful.

Clavulanate potentiated amoxicillin (Augmentin, GlaxoSmithKline, Brentford, Middlesex,

UK), 50 mg, was administered IV every 90 minutes.

Once in the operating theatre, intermittent positive pressure ventilation (IPPV) was

applied using a small animal ventilator (Merlin, Vetronics, Abbotskerswell, Devon, UK) in

volume cycle mode. The tidal volume (VT) was initially set at 25 mL, the inspiratory-

expiratory ratio (I:E) was 1:2, and the peak inspiratory pressure (PIP) was 9 cmH2O.

Respiratory rate was adjusted to maintain the expired carbon dioxide tension (PE’CO2)

between 35 and 45 mmHg (4.7 to 6.0 kPa). Two hypodermic needles were positioned

proximal and distal on the medial aspect of the elbow, over the ulnar nerve and connected to a

peripheral nerve stimulator (Model 750 Digital; Dakmed, Buffalo, New York, USA). A bolus

of 0.75 mg of atracurium (GlaxoSmithKline, Brentford, Middlesex, UK) was administered IV

once IPPV had commenced, the peripheral nerve stimulator was positioned and depth of

anesthesia was stable.

Median sternotomy was performed and the mass was exposed. There was no evidence

of gross invasion into the great vessels or the lung lobes although the mass was firmly

adherent to the cranial vena cava and brachiocephalic trunk. The left phrenic nerve ran

through the mass and, as it could not be separated, was transected. The right phrenic nerve

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was adherent to the mass and was progressively freed from its adhesions. The mass was

carefully separated from the great vessels and removed. Atracurium administration was

repeated when 1 or more twitches returned on the train-of-four, at the dose of 0.25 mg IV

(approximately every 25 min: 5 administrations in total). A 10-French thoracic drain was

inserted through the left thoracic wall and the chest was closed in routine fashion. During

closure 0.75 mL of bupivacaine 0.25% (Marcain, AstraZeneca, London, UK) was infiltrated

subcutaneously in the layers over the sternum. The total blood loss was estimated to be less

than 10% of the dog’s blood volume.

Before recovery, after return of 4 twitches on train-of-four, 25 μg of glycopyrrolate

(Martindale Pharmaceuticals, Romford, Essex, UK) and 50 μg of neostigmine (Hameln

pharmaceuticals, Gloucester, UK) mixed in the same syringe were administered IV to

antagonise the effect of atracurium without inducing bradycardia. The fentanyl infusion was

decreased from 6 to 2 μg/kg BW/h. The thoracic cavity was drained until negative pressure

was achieved. Respiratory rate was initially decreased to 15 movements per minute (mpm)

then the dog was connected to a T-piece circuit and the lungs were inflated manually 2 to 3

times per min. At this stage anesthesia and surgery time were 4 and 2.5 h, respectively. Once

spontaneously breathing, respiratory efforts appeared to be due solely to intercostal muscle

activity whereas the diaphragm appeared to be inactive: the ribs were moving cranially and

outwards and the abdomen looked “sucked in” during inspiration. Neostigmine and

glycopyrrolate administration were repeated but no change was observed. The fentanyl

infusion was discontinued. An attempt to recover the dog was made; when he became

intolerant to intubation (gag reflex and head movements), the trachea was extubated and

oxygen was administered via facemask.

After approximately 3 min, agonal gasps were observed. Peripheral pulses and an apex

beat were no longer palpable. The trachea was re-intubated and manual ventilation was

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instituted immediately; a cycle of external cardiac massage was performed for approximately

2 min. Return of spontaneous circulation was then observed. The thoracic cavity was drained

and approximately 45 mL of blood were removed. Mechanical ventilation was then re-

initiated (VT, 35 mL; I:E, 1:2; PIP, 11 cmH2O; RR , 30 mpm). Initial PE’CO2 was 105 mmHg

but normalized within 5 min. As the heart rate was 200 beats per minute (bpm), a bolus of 20

mL of 6% hydroxyethyl starch (Voluven 6% solution for infusion; Fresenius Kabi, Runcorn,

Cheshire, UKGrand Island, New York, USA) was administered IV. The fentanyl infusion was

also restarted.

A second attempt to recover the dog was made 15 min later. As the respiratory pattern

was not improved compared to the first attempt and desaturation occurred, anesthesia was re-

induced with propofol (2 mg IV), the trachea was re-intubated and lung ventilation

recommenced. The ventilator was set to inspiratory assist mode with a threshold of -2 cmH2O

with a TV of 40 mL. This resulted in maintenance of SpO2 around 94% and moderate PE’CO2

increase (65 mmHg). When the threshold for assisted ventilation was decreased below -2

cmH2O (e.g. -3 cmH2O or less), CO2 accumulation was marked (PE’CO2 > 80 mmHg) and

respiration ineffective. As there appeared to be a gradually decreasing efficacy of ventilation

and decision to maintain IPPV overnight was made, volume-controlled ventilation was

recommenced and the dog was moved to the intensive-care-unit (ICU). The dog was kept on

the same ventilator used for the surgery in the ICU.

Anesthesia was initially maintained on sevoflurane vaporized in oxygen and air (FiO2

60%); fentanyl infusion was continued. The thoracic cavity was drained again (approximately

8 mL of blood were collected). A urinary catheter was placed and a new attempt at placement

of an arterial catheter (surgical approach to the femoral artery) was unsuccessful. Haematocrit

and total proteins were at this stage 23% and 40 g/L, jugular venous blood gas analysis was

unremarkable. The dog was positioned in sternal recumbency. Sevoflurane administration was

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discontinued and replaced by a propofol infusion (0.2 to 0.4 mg/kg BW/min; Vetofol,

Norbrook, Carlisle, Cumbria, UK). Fentanyl was continued at 5 μg/kg BW/h, and a bolus of

atracurium, 0.3 mg/kg BW, IV, followed by an infusion at 0.2 mg/kg BW/h. FiO2 was

decreased to 40% and IPPV (volume-controlled ventilation) was adjusted to maintain

normocapnia (VT, 35 mL; I:E, 1:2; PIP, 11 cmH2O; RR, 30 mpm). Continuous monitoring

included evaluation of the pulse quality, colour of mucous membranes, ECG, pulse oximetry,

capnography and non-invasive blood pressure. Urine output was recorded every 2 h,

temperature every 4 h. The cuff of the endo-tracheal tube was deflated, the tube’s position

was altered slightly and the cuff re-inflated every 6 h. The tube was also suctioned every 4 h

and changed 12 h after intubation. The eyes were lubricated every 2 to 4 h and the mouth and

prepuce were cleaned at the same time.

The following morning, an attempt to gradually wean off ventilation was performed.

Atracurium infusion was stopped, propofol infusion decreased to 0.2 mg/kg BW/min, fentanyl

decreased to 2 μg/kg BW/h. Considerable twitching and movements were initially observed

and, as this resembled seizure activity, midazolam 0.5 mg IV was administered. When 4 clear

twitches were observed on TOF, neostigmine, 0.05 mg/kg BW and glycopyrrolate, 0.01

mg/kg BW were administered together IV. Propofol infusion was decreased to 0.1

mg/kg/min. The ventilator was initially set to assisted-mode then a T-piece was attached

in order to observe bag movement. This was minimal. There was, as after surgery, large

intercostal excursion but no evidence of diaphragmatic function. Ventilation was

recommenced until the appropriate staff could contact the owners and the decision was

made to perform euthanasia.

Microscopic appearance of the lesion was of extensive necrosis and hemorrhage

within a background matrix of reactive fibrous connective tissue. There was no clear evidence

of neoplastic changes on histology; the etiology of the lesion was unclear.

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Discussion

Two main mechanisms of PNI have been reported: hypothermia-induced injury and

mechanical trauma (5). The incidence of PNI remains unknown; it has decreased from 24 -

73% to 0.46 - 20% after topical hypothermia - used as a method of myocardial protection -

was identified as an important etiology of PNI in the late 1980’s (6-9). There is in fact close

contact of the phrenic nerves with the pericardium in humans (10). Mobilization of the

internal mammary artery or direct surgical trauma are described mechanical causes of PNI;

indirect injuries by sternal retractors or misuse of the electrocautery device are also reported

(5). The main consequence of PNI is diaphragmatic paralysis of the side(s) concerned.

Clinically, PNI can be suspected by failure to wean from assisted ventilation, paradoxical

movement of the epigastrium during spontaneous ventilation and elevation of the diaphragm

on chest X-rays (11). Several methods of verification of PNI have been used: fluoroscopy (9),

spirometry (12), transdiaphragmatic pressures studies (12), ultrasound (13) and

electrophysiological measurements (6,7,13). In this case neurotmesis of the left phrenic nerve

was known from surgery and left hemidiaphragmatic paralysis was expected. The nature of

the lesion of the right phrenic nerve was likely mechanical (surgical trauma or stretching

during the separation of the nerve from the mass) and unpredictable. Our suspicion of

bilateral diaphragmatic paralysis was clinical. A paradoxical respiratory pattern and inability

to wean off the ventilator guided us towards continuing mechanical ventilation.

Two aspects have to be considered for this animal’s prognosis: the potential

respiratory performance of a dog with bilateral diaphragmatic paralysis and the chances and

timing of recovery of the phrenic nerve function. Electromyography of the respiratory

muscles in experimental dogs (14) demonstrated an integrated strategy of respiratory muscles

compensation for diaphragmatic paralysis with contribution of different respiratory muscles

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(costal, crural, parasternal and transversus abdominis) adjusted according to the degree of

diaphragmatic dysfunction. A physiological study on adult healthy dogs investigated the

effects of acute bilateral diaphragmatic paralysis (15). Silicone cuffs were implanted around

each phrenic nerve and attached to an injection line tunnelled subcutaneously for local

anesthetic injection. Spirometry and alveolar partial pressure of CO2 were assessed. Unilateral

diaphragmatic paralysis resulted in increased rib cage contribution and little effect on

ventilation. Bilateral diaphragmatic paralysis resulted in marked abdominal paradoxical

breathing and increased rib cage expansion. There was no effect on resting ventilation but a

decrease in tidal and minute volume and a mild increase in PACO2 during REM (rapid eye

movement) sleeping. Adult healthy experimental dogs of this study seemed to be able to cope

well with bilateral PNI therefore attempting to recover our dog despite the PNI was not

unreasonable, independent of whether PNI was unilateral or bilateral. It has been shown that

hemidiaphragmatic paralysis in the dog has a direct detrimental effect on the expansion of

both lungs (16). In this case the dog was both pediatric and brachycephalic. In pediatric

animals, the pulmonary reserve is minimal and the thoracic wall is more compliant which

results in less efficient ventilation and greater work of breathing (17). In addition, post-

anesthetic respiratory complications are common in brachycephalic dogs (18). This could

explain why our attempt to wean this dog off the ventilator after anesthesia was unsuccessful.

A prospective study using electrophysiologic measurements of phrenic nerve latency

in infants undergoing cardiac surgery has investigated the incidence of PNI and its effects on

morbidity and prognosis (7). Findings were that PNI led to an increased duration of

mechanical ventilation after surgery. Post-operatively, approximately 1/3 of the patients with

PNI had recovered diaphragmatic function within 1 mo and 2/3 within 3 mo. Spontaneous

recovery is therefore possible but it is unpredictible and rarely happens early (13,19). In this

case the recovery of the left phrenic nerve was impossible as a whole section had been

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removed; recovery of the right side may have been possible as neuropraxia or axonotmesis

were more likely. In cases of traumatic PNI, return of normal diaphragmatic function could be

expected within up to 6 to 12 months in adults (20). In human medicine, the management of

diaphragmatic paralysis is controversial: options are continuation of mechanical ventilation

until recovery of the phrenic nerve function or diaphragmatic plication, especially in cases of

hemidiaphragmatic paralysis (13,19). Diaphragmatic plication was unlikely to be helpful in

this case because of the bilateral PNI. Furthermore, a 15-hour period of ventilation was

unlikely to be sufficient to permit nerve recovery. With hindsight, euthanasia after the first

attempt to recover the dog from anaesthesia was a reasonable option given its poor prognosis

of recovery and the increased risk factors associated with prolonged mechanical ventilation.

Prolonged mechanical ventilation (ventilation of more than 24 h) has been described in

dogs using a variety of anaesthetic techniques and ventilation strategies. Indications are

generally divided into 2 categories: inadequate blood oxygenation (parenchymal pulmonary

disease) and inadequate CO2 elimination (21). Our case belongs to the second category.

Overall, the outcome for ventilated animals is fair, with 41% of animals successfully weaned

off ventilators and 28% of animals surviving discharge; outcome is better in animals

ventilated for inadequate CO2 elimination (up to 50% of animals successfully weaned off

ventilators and 39% discharged) (21). Cats and smaller dogs and animals of less than 1 year

old have been shown to have poorer outcomes than larger young adult animals (21-23). The

success of ventilation depends on the underlying pathology (21). Long term ventilation is

generally more complex and the rate of ventilator associated complications is high (21,22, 24-

26). Long-term ventilation requires constant monitoring and staff commitment. It is also

expensive. For these reasons it should not be undertaken lightly. In this case, many factors of

poor prognosis were present: the dog was pediatric and very small. He was also

brachycephalic which, in case of recovery, would have resulted in a potentially more critical

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weaning (27). However, if the choice of the owners had been to continue treatment, long-

term ventilation to allow recovery was an acceptable alternative. In that case, regular

electrophysiologic study of the phrenic nerve conduction could have been used to monitor the

phrenic nerve recovery and set end-points to the ventilation. Diaphragmatic plication could

have been considered at a later stage if right diaphragmatic function was recovered but

weaning from ventilation failed again.

Bilateral PNI is rare in humans and, to our knowledge, not reported in dogs. This case

was particularly challenging because of his breed, age, small size and the severity of the

lesions he exhibited after surgery. Although it could have been managed differently,

euthanasia was always the most likely outcome.

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