Congenital laryngeal paralysis in Alaskan Huskies: 25 cases (2009–2014)

Dirsko J. F. von Pfeil Friendship Surgical Specialists of the Friendship Hospital for Animals, 4105 Brandywine St NW, Washington, DC 20016.
Department of Small Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824.

Search for other papers by Dirsko J. F. von Pfeil in
Current site
Google Scholar
PubMed
Close
 Dr med vet, DVM
,
Eric Zellner Department of Small Animal Clinical Sciences, College of Veterinary Medicine, Iowa State University, Ames, IA 50011.

Search for other papers by Eric Zellner in
Current site
Google Scholar
PubMed
Close
 DVM
,
Michele C. Fritz Department of Epidemiology and Biostatistics, College of Human Medicine, Michigan State University, East Lansing, MI 48824.

Search for other papers by Michele C. Fritz in
Current site
Google Scholar
PubMed
Close
 BSc
,
Ingeborg Langohr Department of Pathobiological Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, LA 70803.

Search for other papers by Ingeborg Langohr in
Current site
Google Scholar
PubMed
Close
 DVM
,
Caroline Griffitts The Traveling Vet LLC, 7640 W County Rd 20, Loveland, CO 80537.

Search for other papers by Caroline Griffitts in
Current site
Google Scholar
PubMed
Close
 DVM
, and
Bryden J. Stanley Department of Small Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824.

Search for other papers by Bryden J. Stanley in
Current site
Google Scholar
PubMed
Close
 BVMS, MVetSc

Click on author name to view affiliation information

Abstract

OBJECTIVE To characterize congenital laryngeal paralysis (CLP) in Alaskan Huskies.

DESIGN Prospective case series.

ANIMALS 25 Alaskan Huskies with CLP.

PROCEDURES Data were collected for each dog regarding signalment; history; results of physical, orthopedic, neurologic, and laryngeal examinations; esophagraphic findings; treatments; histologic findings; and outcomes.

RESULTS Severely affected dogs were profoundly dyspneic at birth or collapsed after brief exercise; less affected dogs reportedly tired easily or overheated with minimal exercise. Mean age at initial onset of clinical signs was 6.4 months. Blue eyes, white facial markings, and oral mucosal tags or tissue bands were noted in 23 (92%), 19 (76%), and 13 (52%) dogs. Neurologic examination revealed signs of mononeuropathy of the recurrent laryngeal nerve but not of polyneuropathy. Histologic examination revealed neurogenic atrophy of the cricoarytenoideus dorsalis muscle but no polyneuropathy. Eight (32%) dogs underwent unilateral cricoarytenoid lateralization, resulting in substantial clinical improvement, including ability to compete in sled dog races. Without surgery, 4 (16%) dogs died of asphyxiation, 10 (40%) had spontaneous improvement of clinical signs (but insufficient improvement to race), and 3 (12%) remained affected. Results of pedigree analysis suggested an autosomal recessive mode of CLP inheritance, with variable penetrance.

CONCLUSIONS AND CLINICAL RELEVANCE CLP in the evaluated Alaskan Huskies involved mononeuropathy of the recurrent laryngeal nerves, without polyneuropathy. Most affected dogs had blue eyes, white facial markings, and oral mucosal tags or tissue bands. Given the apparent genetic component to CLP in this breed, we recommend that dogs with these features be prevented from breeding.

Abstract

OBJECTIVE To characterize congenital laryngeal paralysis (CLP) in Alaskan Huskies.

DESIGN Prospective case series.

ANIMALS 25 Alaskan Huskies with CLP.

PROCEDURES Data were collected for each dog regarding signalment; history; results of physical, orthopedic, neurologic, and laryngeal examinations; esophagraphic findings; treatments; histologic findings; and outcomes.

RESULTS Severely affected dogs were profoundly dyspneic at birth or collapsed after brief exercise; less affected dogs reportedly tired easily or overheated with minimal exercise. Mean age at initial onset of clinical signs was 6.4 months. Blue eyes, white facial markings, and oral mucosal tags or tissue bands were noted in 23 (92%), 19 (76%), and 13 (52%) dogs. Neurologic examination revealed signs of mononeuropathy of the recurrent laryngeal nerve but not of polyneuropathy. Histologic examination revealed neurogenic atrophy of the cricoarytenoideus dorsalis muscle but no polyneuropathy. Eight (32%) dogs underwent unilateral cricoarytenoid lateralization, resulting in substantial clinical improvement, including ability to compete in sled dog races. Without surgery, 4 (16%) dogs died of asphyxiation, 10 (40%) had spontaneous improvement of clinical signs (but insufficient improvement to race), and 3 (12%) remained affected. Results of pedigree analysis suggested an autosomal recessive mode of CLP inheritance, with variable penetrance.

CONCLUSIONS AND CLINICAL RELEVANCE CLP in the evaluated Alaskan Huskies involved mononeuropathy of the recurrent laryngeal nerves, without polyneuropathy. Most affected dogs had blue eyes, white facial markings, and oral mucosal tags or tissue bands. Given the apparent genetic component to CLP in this breed, we recommend that dogs with these features be prevented from breeding.

Congenital laryngeal paralysis has been identified in several dog breeds or types, including Bouviers des Flandres,1,2 Dalmatians,3 Rottweilers,4,5 white-coated German Shepherd Dogs,6 Bull Terriers,7 Alaskan Malamutes,a Siberian Husky–Alaskan Malamute crosses,8 Leonbergers,9 and Great Pyrenees.10 In most of these breeds or types, CLP is reportedly hereditary and frequently part of a polyneuropathy complex that often includes esophageal dysfunction.4,5,9,10,a Esophageal dysfunction has also been described in some breeds as a component of laryngeal paralysis in elderly dogs, which is also referred to as geriatric onset laryngeal paralysis polyneuropathy.11

In contrast to CLP in other canine breeds, a paucity of information exists in the veterinary literature regarding CLP in Alaskan Huskies, which are commonly owned, bred, and worked as sled dogs in North America and used for ultramarathon sled dog competitions.12 The information that does exist consists of a single case report13 published in 1986, and although a studyb was performed involving 7 affected Alaskan Huskies, the results were never published. Despite this minimal scientific evidence, the authors' experience suggests that CLP in Alaskan Huskies is a well-known condition among professional mushers in Northern America and that the disease may be associated with phenotype.

Our communications with sled dog mushers and othersc as well as our own experience suggest that the most important and easily recognized clinical signs of CLP in Alaskan Huskies are various degrees of stridor, dysphonia, or both (commonly referred to by mushers as wheezing). Affected dogs are known as wheezers within the sled dog community. The abnormal respiratory bruit (wheezing) is most pronounced during inspiration and is markedly accentuated by exercise or excitement. Professional mushers have long noted that affected Alaskan Huskies have a characteristic phenotype, specifically blue eyes and white facial markings. To the authors' knowledge, signs of polyneuropathy or esophageal disorders, as noted in other breeds with CLP, have not been observed in Alaskan Huskies.13,b,c The purpose of the study reported here was to characterize the phenotype and clinical history of CLP in Alaskan Huskies, evaluate neurologic and esophageal function in affected dogs, and review their pedigrees.

Materials and Methods

Case selection criteria

The study protocol was approved by the Institutional Animal Care and Use Committee of Michigan State University (protocol No. 10-06-25). Between August 1, 2009, and January 1, 2014, Alaskan Huskies with typical anamnesis and clinical signs of CLP were identified through personal contacts with mushers or through internet postings, presentations, and distribution of information during sled dog races and related meetings with the aid of a standardized data collection form (Supplementary Appendix S1, available at avmajournals.avma.org/doi/suppl/10.2460/javma.253.8.1057).

Alaskan Huskies identified in this manner were included in the study when laryngeal examination by the authors confirmed the diagnosis of laryngeal paralysis and complete medical records, data collection forms, and historical information were available. Dogs were excluded from the study if they had no diagnosis of laryngeal paralysis, an incomplete medical record or data collection form, unclear history, no information on age at first clinical signs, clinical signs noted only after mushing a distance of ≥ 8 km (5 miles), or other respiratory conditions diagnosed. Owners of included dogs consented to their dogs' participation, which included full physical, neurologic, and orthopedic examinations; other diagnostic tests to confirm the CLP; and, for dogs that required it, surgery, including various pre- and intraoperative diagnostic tests.

Data collection

A comprehensive history was obtained for each dog; patient data documents were completed; physical, neurologic, and orthopedic examinations were performed; and findings were recorded. Veterinary records from referring practices and pedigree information were requested.

Dogs were grouped by age when clinical signs were first observed into 2 categories: ≤ 6 months and > 6 months. This was done on the basis of the authors' experience, which suggested that some dogs were more affected at a younger age than others, and some improved considerably during adolescence. To determine whether age at onset of clinical signs or presence of multiples of the 3 main phenotypic features (blue eyes, white facial markings, and oral mucosal tags, oral mucosal tissue bands, or both) was related to the severity of clinical signs, a clinical severity scoring system was created on the basis of responses captured by the data collection forms. Presence of wheezing was scored as 0 (never), 1 (occasional), 2 (intermittent), 3 (frequent), or 4 (all the time). Level of exercise at which respiratory noise was first noted was scored as 1 (when running in a harness), 2 (during rough play), 3 (during gentle play), 4 (while walking around), or 5 (at rest). Amount of respiratory noise when exercising was scored as 0 (none), 1 (mild), 2 (moderate), 3 (marked), or 4 (severe or loud). Clinical signs when exercising were scored as 0 (normal), 1 (tires more easily), 2 (requires owner to limit activity to prevent breathing problems), 3 (collapses, develops cyanosis, or both), or 4 (cannot exercise). In addition, a tendency to overheat with minimal exercise or short runs in a harness was scored as 0 (no) or 1 (yes), and a general ability to bark was scored as 0 (yes) or 1 (no). By this system, the total clinical severity score could range from 1 to 19, with high scores reflecting greater severity. This total was divided by 6 to obtain a mean clinical severity score for each dog.

Each dog was evaluated with a CBC and serum biochemical analysis. Three-view thoracic and 2 orthogonal cervical radiographs were obtained whenever possible. Esophagraphy was also performed by use of a previously described protocol11 when possible. Videolaryngoscopy and cranial videotracheoscopyd were performed during a screening examination or immediately prior to surgery to assess laryngeal function and record any abnormalities within the cranial portion of the trachea. Bilateral laryngeal paralysis was diagnosed as a lack of abduction of the arytenoid cartilages during considerable inspiratory effort.

In preparation for imaging or surgery, anesthesia was performed as reported elsewhere.11,14 For dogs requiring surgery, a board-certified veterinary surgeon experienced in laryngeal surgery (DJFvP and BJS) performed a UCAL or LI-UCAL procedure.11,14 Laryngeal examination was repeated after surgery at extubation, and adequate abduction was confirmed. For these surgically treated dogs, biopsy specimens were obtained from the cricoarytenoideus dorsalis muscle, recurrent laryngeal nerve, cranial tibialis muscle, and peroneal nerve when possible.15 Tissue specimens from these regions were also obtained from dogs that had been euthanized as a result of CLP or for other reasons.

Specimen processing

Tissue specimens were fixed in neutral-buffered 10% formalin, trimmed, and embedded in paraffin wax. Five-micrometer sections were stained with H&E stain. Additional sections were treated with the Gomori trichrome staining protocol. Skeletal muscle sections were examined via light microscopy for range of fiber diameter, evidence of single or small contiguous group fiber atrophy, endomysial and perimysial fibrosis or fatty infiltration, and morphological alterations of muscle spindles and intramuscular nerves. Nerves were evaluated for axonal degeneration, demyelination, fiber loss, and Schwann cell proliferation.

Statistical analysis

Descriptive methods were used to summarize findings for signalment, clinical signs, history, histologic examination, and pedigree analysis. Distribution curves and Q-Q plots were used to assess continuous data for normality. The χ2 or Fisher exact test (when variable categories were represented by < 5 dogs) was used to compare distributions of dogs with and without all 3 phenotypic features between age categories (≤ 6 months or > 6 months). The unpaired t test was used to compare ages between dogs with and without all 3 phenotypic features and mean clinical severity scores between age categories (≤ 6 months or > 6 months). Pearson or Spearman correlations were also calculated for these analyses. Statistical softwaree was used for all analyses, and values of P < 0.05 were considered significant.

Results

Dogs

Eighty-nine Alaskan Huskies were initially enrolled in the study; 64 (72%) dogs failed to meet the inclusion criteria, leaving 25 dogs in the study (Supplementary Table S1, available at avmajournals.avma.org/doi/suppl/10.2460/javma.253.8.1057). Dogs included 9 sexually intact males, 7 spayed females, 6 neutered males, and 3 sexually intact females. Mean ± SD age at initial onset of clinical signs was 6.4 ± 3.6 months (median, 6.0 months; range, 1 to 13 months). Mean ± SD body weight at study inclusion was 7.5 ± 4.0 kg (16.5 ± 8.8 lb; median, 6.0 kg [13.2 lb]; range, 3.0 to 17.0 kg [6.6 to 37.4 lb]).

Phenotype

Twenty-three (92%) Alaskan Huskies had blue eyes, and 2 (8%) had brown eyes. Nineteen (76%) dogs had white facial markings, and the remaining 6 (24%) had combinations of tan, beige, gray, or black facial markings. Thirteen (52%) had oral mucosal tags, oral mucosal tissue bands, or both (Figures 1 and 2). Although dental abnormalities were not specifically evaluated, supernumerary teeth were voluntarily reported for 4 (16%) dogs. No significant association was identified between age as a categorical variable (≤ 6 months or > 6 months; Fisher exact test, P = 1.00) or age as a continuous variable (unpaired t test, P = 0.90) and the presence of all 3 phenotypic features (blue eyes, white facial markings, and oral mucosal tags, oral mucosal tissue bands, or both).

Figure 1—
Figure 1—

Photographs of young and adult Alaskan Huskies with CLP (also known as wheezer disease). Blue eyes and white facial markings with occasional black freckles were a common phenotype associated with this condition. However, the facial markings alone did not confirm whether a dog was affected or carried a genetic defect.

Citation: Journal of the American Veterinary Medical Association 253, 8; 10.2460/javma.253.8.1057

Figure 2—
Figure 2—

Photographs obtained during oral examination of 4 Alaskan Huskies with CLP. Findings in affected dogs typically included oral mucosal tags (A), oral mucosal tissue bands (B), or both (C; yellow arrows). Supernumerary teeth (D; black arrow) have been suspected to be associated with the disease, but the study data provided no support for such an association.

Citation: Journal of the American Veterinary Medical Association 253, 8; 10.2460/javma.253.8.1057

History

None of the dogs had a history consistent with esophageal dysfunction. However, 1 dog had undergone soft palate resection at 11 weeks of age 2 days prior to evaluation at the Michigan State University veterinary teaching hospital for life-threatening dyspnea and regurgitation. Esophagraphy in that dog revealed a paraesophageal hiatal hernia, and clinical signs resolved with surgery to treat the hernia as well as with UCAL to treat CLP.

Five (20%) dogs had undergone vocal cordectomy by other veterinarians during puppyhood because of clinical signs consistent with CLP. Three dogs had undergone this procedure at 7, 4, and 4 months of age, but clinical signs returned at 4, 4, and 8.5 years of age, respectively. The remaining 2 dogs underwent vocal cordectomy at 3 and 5 months of age, without recurrence of clinical signs at the time of last examination, when they were 2 and 3 years old, respectively.

Examination findings

Apart from audible wheezing that originated from the larynx region in all dogs and the aforementioned oral abnormalities, no abnormalities were detected on physical, orthopedic, or neurologic examination. One dog was reported as deaf, but no diagnostic testing was pursued to confirm this. No laryngeal or tracheal abnormalities were palpated in any dog, and no dog had evidence of polyneuropathy.

Blood samples were available for 18 (72%) dogs, and no serum biochemical or CBC abnormalities were detected. Thoracic and cervical radiographs were available for 14 (56%) dogs, including all 8 surgically treated dogs; no laryngeal, tracheal, pulmonary, or cardiac abnormalities were identified, nor was evidence of megaesophagus. Esophagraphy was performed for 5 dogs, revealing no esophageal dysfunction in 4. The fifth dog was the one with a hiatal hernia. Laryngeal examination via laryngotracheoscopy revealed bilateral laryngeal paralysis in all but 1 dog. That 1 dog with classic respiratory signs, complete white coat, and mucosal tags but with brown rather than blue eyes had unilateral laryngeal paralysis. Cranial tracheoscopy revealed no tracheal abnormalities in any dog.

Clinical signs and severity

The nature of breathing when not exercising was characterized as rattling or stridor for 11 (44%) dogs, squeaking or wheezing for 9 (36%) dogs, croaking for 3 (12%) dogs, snoring or stertor for 1 (4%) dog, and normal for 1 (4%) dog. Clinical signs of upper respiratory tract bruit (wheezing) were noted at various activity levels. Without exercise, 3 (12%) dogs never had wheezing, 8 (32%) had it occasionally, 1 (4%) had it intermittently, 9 (36%) had it frequently, and 4 (16%) had it all the time. This noise started when running in a harness for 7 (28%) dogs, during rough play for 5 (20%) dogs, during gentle play for 6 (24%) dogs, while walking around for 3 (12%) dogs, and at rest for 4 (16%) dogs. The amount of noise when exercising was characterized as severe and loud for 3 (12%) dogs, marked for 10 (40%) dogs, moderate for 8 (32%) dogs, and mild for 4 (16%) dogs. Clinical signs while exercising were characterized as tires more easily for 12 (48%) dogs, requires limiting of activity for 6 (24%) dogs, collapse or cyanosis for 6 (24%) dogs, and cannot exercise for 1 (4%) dog. Sixteen (64%) dogs were able to bark, and 9 (36%) were unable to bark, regardless of activity, at all times. The nature of this bark in the 16 dogs that were able was characterized as squeaking for 6 dogs, hoarse for 5 dogs, normal for 4 dogs, and hacking for 1 dog.

In 10 (40%) dogs, clinical signs had first been noticed at ≤ 6 months of age (mean ± SD, 2.8 ± 1.2 months; median, 3 months; range, < 1 to 4 months). In 15 (60%) dogs, clinical signs had first been noticed at > 6 months of age (mean ± SD, 8.9 ± 2.2 months; median, 9.0 months; range, 6 to 13 months).

Overheating with minimal exercise or short runs in a harness, sometimes after a few minutes to an hour of only walking, was reported for 6 (24%) dogs. Such overheating was summarily characterized as rapid panting, particularly in humid and warm conditions with associated extended recovery times, compared with other dogs; heat sensitivity when exercising; and respiratory distress during training and confinement.

The mean value for clinical severity scores was similar between dogs with (1.85) and without (1.47) all 3 phenotypic features (unpaired t test, P = 0.06). The mean value for dogs ≤ 6 months of age was 1.54, and that for dogs > 6 months of age was 1.73 (unpaired t test, P = 0.38). No correlation was identified between numeric age and mean clinical severity score (Pearson correlation coefficient, r = 0.2; P = 0.33).

Treatment

Eight (32%) dogs underwent a left-sided UCAL procedure (5 UCAL and 3 LI-UCAL) as described.11,14 In 3 dogs that had previously undergone vocal cordectomy but had recurrence of clinical signs, ventral laryngotomy with removal of the webbed mucosa and suturing of mucosal edges was performed in addition to UCAL. In 1 dog that underwent LI-UCAL, the thyroid cartilage was abnormal in shape. This cartilage was smaller than typical, bent caudomedially, and extended over the caudal aspect of the cricoid cartilage. Surgery was more difficult in this dog because of this unusual anatomic finding; however, the outcome was still successful.

Postoperative laryngeal examination revealed an appropriately opened airway in all surgically treated dogs. In the dog with CLP and concurrent hiatal hernia, the hernia was repaired with a combination of herniorrhaphy, phrenoesophagopexy, and tube gastropexy.

Histologic examination

Tissue specimens from 8 (32%) dogs were available for histologic examination, revealing neurogenic atrophy of all cricoarytenoideus dorsalis muscles (Figure 3). The cranial tibialis muscle appeared unremarkable in all but 1 dog, in which mild atrophic changes were identified. This dog was reported to have been mildly affected throughout its life, with clinical signs first appearing at 4 months of age, but never underwent surgery. It was euthanized at 16 years of age, and histologic examination of motor nerves and motor endplates revealed Wallerian degeneration in the recurrent laryngeal nerves. Surgically treated dogs for which nerve sections were examined had no histologic changes; however, within the recurrent laryngeal nerve specimen of 1 dog that was euthanized for reasons unrelated to CLP, Renaut bodies were found. Evaluation of a mucosal tag from a representative dog revealed redundant, otherwise unremarkable mucosal and submucosal tissue consisting of abundant paucicellular collagen-rich fibrous tissue with interspersed vessels and nerves covered by nonkeratinizing squamous epithelium. No brain specimens were available for histologic examination.

Figure 3—
Figure 3—

Representative photomicrographs of muscle biopsy specimens from a 1-year-old spayed female Alaskan Husky with CLP. A—Cranial tibialis muscle with no histologic alterations. H&E stain; bar = 200 μm. B—Dorsal cricoarytenoideus dorsalis muscle with multiple angular atrophic fibers present individually and in small contiguous clusters, indicative of denervation involving a limited number of motor units. H&E stain; bar = 100 μm.

Citation: Journal of the American Veterinary Medical Association 253, 8; 10.2460/javma.253.8.1057

Outcome

Mean ± SD interval between surgery and final follow-up for the 8 surgically treated dogs was 39.8 ± 28.5 months (median, 28.0 months; range, 14.0 to 104.0 months). All owners of the surgically treated dogs reported a substantial improvement in breathing and activity in their dogs after surgery. All dogs reportedly had occasional noises, best described as throat clearing, up to 6 months after surgery. This noise decreased in frequency and was reported to occur only rarely in 2 dogs at the last follow-up. One dog developed aspiration pneumonia 3 months after surgery and improved with marbofloxacin administration (2.75 mg/kg [1.25 mg/lb], PO, q 24 h for 2 weeks). No recurrence was reported at the final follow-up examination 26 months after surgery. No other cases of aspiration pneumonia or other complications were observed.

For the 1 surgically treated dog with CLP and concomitant hiatal hernia, esophagraphy was repeated 12 weeks after surgery, revealing unremarkable motility during liquid and canned-food phases but delayed contraction of the caudal third of the esophagus during the kibble phase. On follow-up examination 6 months and 1.5 years after surgery, this dog was reported to have made a full recovery without any signs of difficulty swallowing, regurgitation, or aspiration pneumonia. Esophagraphy was not repeated at these later evaluation points. For the 7 other surgically treated dogs, activity was gradually increased from slow and brief walks to training runs of 8 to 16 km (5 to 10 miles) in harness at 4 months after surgery, covering distances of up to 30 to 50 km (18 to 30 miles) thereafter. No breathing abnormalities except for mild throat clearing were noted in these dogs. One dog successfully completed preparation for and participation in an approximately 1,600-km (1,000-mile) sled dog race without evidence of respiratory problems. Five dogs were used for recreational mushing, and 1 was used as a companion dog.

Of the 17 nonsurgically treated dogs (68% of all 25 dogs), 4 died of asphyxiation secondary to CLP. In contrast, spontaneous improvement of clinical signs between birth and maturity without any surgical intervention was reported for 10 (40%) dogs. These dogs had no remaining respiratory noise and continued as pets; however, none became active, racing sled dogs. Mean ± SD age by which clinical signs had resolved was 10.0 ± 2.4 months (median, 10.5 months; range, 7.0 to 12.0 months). One of these dogs had moderate clinical signs and evidence of bilateral laryngeal paralysis at 4 months of age, but owing to the owner's financial concerns, no surgery was performed at that time. Laryngeal examination was repeated at 12 months of age, when clinical signs had improved, revealing mild bilateral movement of the larynx. The remaining 3 dogs had no improvement but continued to have signs of wheezing whenever exposed to stress or exercise.

Pedigrees

Available pedigree records were insufficient to clearly provide evidence of a relationship between all dogs, and it was not possible to trace all 25 dogs back to 1 common ancestor. The collected pedigrees suggested that the condition had an autosomal recessive mode of inheritance with variable penetrance (Figure 4).

Figure 4—
Figure 4—

Annotated genogram showing the phenotype and selected additional features of 3 litters of Alaskan Huskies with CLP. Circles indicate females, and squares indicate males. Black symbols indicate affected dogs, and white symbols indicate clinically normal dogs that were suspected of being carriers of the disease. + = Mildly affected. ++ = Moderately affected. +++ = Severely affected and died or was euthanized shortly after birth. N/A = Not applicable. *Determined via laryngoscopy.

Citation: Journal of the American Veterinary Medical Association 253, 8; 10.2460/javma.253.8.1057

Discussion

The present study represented the first comprehensive evaluation of CLP in Alaskan Huskies. Overall, 92% of included dogs had blue eyes, 76% had white facial markings, and 52% had oral mucosal tags, oral mucosal tissue bands, or both. These results suggested that CLP in Alaskan Huskies might be associated with these phenotypic features.

Our conversations with professional mushers have suggested that Alaskan Huskies with both blue eyes and white facial markings are often excellent dog-team leaders with alpha-dog characteristics and can therefore be valuable for a sled dog team. This facial phenotype also represents what many people consider the typical appearance of an ideal sled dog. This ideal sled dog image mainly stems from the old stories and pictures of working Husky breeds. Most of those larger and heavier breeds are not the type that is bred and raced in current mushing circles. Nevertheless, this misconception of the ideal sled dog could be contributing to the continued breeding of the phenotype, particularly by recreational mushers, and could be the reason that the so-called wheezer disease has not been eliminated from the Alaskan Husky breed.b

An association between CLP and white coat color and blue eyes has been reported for Dalmatians, Great Pyrenees, white-coated German Shepherd Dogs, and Siberian Husky–Malamute crosses.6,8,10,13 Genetic associations between white hair and blue eyes have been established in dogs.3,6,8,10 In Alaskan Huskies with CLP, gene mutations could also be responsible for the various phenotypes such as white facial markings and blue eyes. In contrast to hair and eye color, no genetic basis of oral mucosal tags or bands has been reported for dogs. However, in people, frenal attachments with an appendix or nichum (2 adjacent frenula) that appear to be similar to the abnormal oral mucosal bands detected in some dogs of the present study have been reported in association with other genetic abnormalities.16 In rare cases, bad dentition (malpositioned or supernumerary teeth, brachygnathism, prognathism, or occasional cleft palate) has also been suggested to be a phenotypic characteristic of Alaskan Huskies with CLP.b Precise details on dental, mandibular, maxillary, or hard palate abnormalities were not specifically recorded for dogs in the present study, although 4% of dogs reportedly had supernumerary teeth. It remains unknown whether such abnormalities are associated with CLP in Alaskan Huskies, and additional research is needed in this regard.

Although pedigree information was limited for the dogs in the study reported here, the information collected suggested an autosomal recessive mode of inheritance with variable penetrance. Indeed, despite a lack of scientific evidence supporting the heritability of CLP in Alaskan Huskies, and purely on the basis of experiences in their kennels, some mushers have told us that they purposely avoid breeding dogs with blue eyes and white facial markings and anecdotally report recurrence of the condition within specific bloodlines.b,c On the other hand, breeding practices vary, and breeding of littermates and close family members can result in a higher likelihood of heritable disease,17 so ethical breeding practices, potentially including genetic screening, have been recommended for purebred dogs.18 Given that screening for genetic mutations related to laryngeal abductor paralysis has been used to diagnose CLP in human medicine,19 further investigation into the potential genetic basis of and genetic screening for CLP in Alaskan Huskies is warranted.

The recurrent laryngeal nerve innervates not only the laryngeal muscles but also the cervical and cranial thoracic portion of the esophagus via the pararecurrent laryngeal nerve.20,21 The pararecurrent nerves can arise either directly from the vagus nerve at the level of the recurrent laryngeal nerve branches or as the first branch of the recurrent laryngeal nerves. Therefore, dogs with CLP may be prone to development of esophageal dysmotility or megaesophagus, similar to what is believed to occur in dogs with geriatric onset laryngeal paralysis polyneuropathy.11 However, esophageal dysfunction was identified clinically or historically in only 1 (4%) dog in the present study. Regurgitation in that 1 dog was associated with a hiatal hernia that likely developed secondary to the chronic negative pressure from CLP in the upper respiratory tract.22 The abnormal shape of the thyroid cartilage in another surgically treated dog could be explained in a similar fashion.

Findings in the present study supported the existence of 2 distinct populations of Alaskan Huskies with CLP: 1 that developed clinical sings in puppyhood, and 1 that developed no signs until training begins (ie, at approx 9 months of age). The dogs that developed clinical signs later in life were likely less affected than younger dogs were, only having clinical signs when exercised; however, this possibility was not formally analyzed. Such a clinical observation may be an important part when recording the history of an Alaskan Husky with respiratory distress during the initial examination, and CLP should be included among the differential diagnoses in these scenarios.

Surgical treatment of Alaskan Huskies with CLP in the present study resulted in considerable improvement in all that received it. However, even without surgery, 40% of dogs had improvement in their clinical signs with age. Similarly, in human medicine, spontaneous improvement of CLP has been described, and therefore a conservative approach is often initially advised.23 A potential explanation for dogs apparently outgrowing the clinical signs of CLP as they age could be that, in mature dogs, the laryngeal lumen diameter and thus oxygen supply increase. Purely hypothetically, delayed laryngeal innervation or cross innervation may also occur in rare instances. Despite the possibility of spontaneous improvement, for severely affected, immature Alaskan Huskies with CLP, we recommend surgical intervention over a conservative approach to prevent death from devastating asphyxiation, which occurred in 4 dogs of the present study.

In other canine breeds, evidence exists to suggest that CLP is 1 part of a widespread polyneuropathy complex, occasionally confirmed by means of electrodiagnostic evaluations (nerve conduction testing and electromyography).1–5,9,10 Although such testing was beyond the scope of our study, it might have provided additional information and is recommended for future research. Even so, histologic findings for cranial tibialis muscle specimens and a lack of neurologic examination abnormalities and esophageal dysmotility suggested that CLP is not part of a polyneuropathy in Alaskan Huskies.

Histologic examination of motor nerves and motor endplates in some dogs in the present study revealed Wallerian degeneration in the recurrent laryngeal nerve, providing evidence of motor neuron loss. Renaut bodies identified in the recurrent laryngeal nerve of 1 dog were believed to have been the result of repeated nerve compression.24 Although this finding could have resulted from a dog running without neck lines applied, this dog had been unable to run more than a few hundred yards and for that reason had not proceeded to training. Therefore, the cause of the Renaut bodies remains unexplained. The lack of changes in the peroneal and recurrent laryngeal nerves provided further evidence that CLP in Alaskan Huskies is a mononeuropathy and not part of a complex polyneuropathy.

The motor nucleus for the laryngeal muscles in dogs is located in the nucleus ambiguus,25–29 which is located bilaterally in the medulla oblongata.30 Dysgenesis of this motor nucleus is a reported cause of CLP in people, and neuronal degeneration of this motor nucleus is a possible cause of CLP in Bouviers des Flandres, Siberian Huskies, and Alaskan Malamute puppies.8,31 Because the Alaskan Husky breed originated through breeding of other Nordic breeds, such as Siberian Husky and Malamute, the defect may have been transmitted from these breeds, and a defective nucleus ambiguus could therefore be the cause of CLP in Alaskan Huskies. Logistic challenges prohibited complete necropsy of dogs in the present study, and thorough histologic examination of the brain, particularly of the nucleus ambiguus, is needed to further explore this possibility.

A limitation of the present study was the small number of clinically affected dogs. We had difficulty convincing mushers to participate. Because breeding and selling racing sled dogs can be lucrative, some kennel owners may have feared that their kennel name would be associated with CLP, despite having been assured strict confidentiality. A case-control study, with detailed examinations of all dogs and appropriate statistical comparisons, is needed to further investigate whether specific phenotypic features are indeed associated with CLP in Alaskan Huskies. Incompleteness of available pedigrees also precluded definitive identification of the mode of inheritance, if any, of CLP in Alaskan Huskies. Despite these limitations, the present study provided valuable information regarding CLP in Alaskan Huskies that can be useful in the identification and treatment of this condition. This information may also be useful when counseling owners of affected dogs and breeders of Alaskan Huskies.

Acknowledgments

Supported by the Michigan Animal Health Foundation of the Michigan Veterinary Medical Association and Michigan State University College of Veterinary Medicine Endowed Research Funds.

The authors declare that there were no conflicts of interest.

Presented in part as a poster at the American College of Veterinary Surgeons Veterinary Symposium, Chicago, November 2011.

The authors thank David Frost and Dr. Heather Huson for editorial help and assistance with results interpretation as well as Dr. Michael Edwards for logistic support.

ABBREVIATIONS

CLP

Congenital laryngeal paralysis

LI-UCAL

Less invasive unilateral cricoarytenoid lateralization

UCAL

Unilateral cricoarytenoid lateralization

Footnotes

a.

Moe L, Bjerkås I. Hereditary polyneuropathy in the Alaskan Malamute (abstr), in Proceedings. 3rd Annu Symp Eur Coll Vet Neurol 1989;28–31.

b.

Leach J, Iditarod Sled Dog Race head veterinarian (retired), Wasilla, Alaska: Personal communication, 2015 and 2016.

c.

Wakshlag J, Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY: Personal communication, 2014.

d.

Endogo HD portable digital video endoscopy camera, Medicine Technology and You LLC, Marietta, Ga.

e.

SAS, version 9.3, SAS Institute Inc, Cary, NC.

References

  • 1. Venker-van Haagen AJHW, Goedege SA. Spontaneous laryngeal paralysis in young Bouviers. J Am Anim Hosp Assoc 1978;14:714720.

  • 2. Venker-van Haagen AJBJ, Hartman W. Hereditary transmission of laryngeal paralysis in Bouviers. J Am Anim Hosp Assoc 1981;17:7576.

  • 3. Braund KG, Shores A, Cochrane S, et al. Laryngeal paralysis-polyneuropathy complex in young Dalmatians. Am J Vet Res 1994;55:534542.

    • Search Google Scholar
    • Export Citation
  • 4. Mahony OM, Knowles KE, Braund KG, et al. Laryngeal paralysis-polyneuropathy complex in young Rottweilers. J Vet Intern Med 1998;12:330337.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Salvadori C, Tartarelli CL, Baroni M, et al. Peripheral nerve pathology in two Rottweilers with neuronal vacuolation and spinocerebellar degeneration. Vet Pathol 2005;42:852855.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Ridyard AE, Corcoran BM, Tasker S, et al. Spontaneous laryngeal paralysis in four white-coated German Shepherd Dogs. J Small Anim Pract 2000;41:558561.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Braund KG, Steinberg HS, Shores A, et al. Laryngeal paralysis in immature and mature dogs as one sign of a more diffuse polyneuropathy. J Am Vet Med Assoc 1989;194:17351740.

    • Search Google Scholar
    • Export Citation
  • 8. Polizopoulou ZS, Koutinas AF, Papadopoulos GC, et al. Juvenile laryngeal paralysis in three Siberian Husky x Alaskan Malamute puppies. Vet Rec 2003;153:624627.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Shelton GD, Podell M, Poncelet L, et al. Inherited polyneuropathy in Leonberger dogs: a mixed or intermediate form of Charcot-Marie-Tooth disease? Muscle Nerve 2003;27:471477.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Gabriel A, Poncelet L, Van Ham L, et al. Laryngeal paralysis-polyneuropathy complex in young related Pyrenean Mountain Dogs. J Small Anim Pract 2006;47:144149.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Stanley BJ, Hauptman JG, Fritz MC, et al. Esophageal dysfunction in dogs with idiopathic laryngeal paralysis: a controlled cohort study. Vet Surg 2010;39:139149.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Huson HJ, Parker HG, Runstadler J, et al. A genetic dissection of breed composition and performance enhancement in the Alaskan sled dog. BMC Genet 2010;11:71.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. O'Brien JAHJ. Inherited laryngeal paralysis. Analysis in the Husky cross. Vet Q 1986;8:301302.

  • 14. von Pfeil DJ, Edwards MR, Dejardin LM. Less invasive unilateral arytenoid lateralization: a modified technique for treatment of idiopathic laryngeal paralysis in dogs: technique description and outcome. Vet Surg 2014;43:704711.

    • Search Google Scholar
    • Export Citation
  • 15. Dickinson PJ, LeCouteur RA. Muscle and nerve biopsy. Vet Clin North Am Small Anim Pract 2002;32:63102.

  • 16. Priyanka M, Sruthi R, Ramakrishnan T, et al. An overview of frenal attachments. J Indian Soc Periodontol 2013;17:1215.

  • 17. Leroy G. Genetic diversity, inbreeding and breeding practices in dogs: results from pedigree analyses. Vet J 2011;189:177182.

  • 18. Bell JS. Researcher responsibilities and genetic counseling for pure-bred dog populations. Vet J 2011;189:234235.

  • 19. Manaligod JM, Skaggs J, Smith RJ. Localization of the gene for familial laryngeal abductor paralysis to chromosome 6q16. Arch Otolaryngol Head Neck Surg 2001;127:913917.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Lemere F. Innervation of the larynx; I. Innervation of laryngeal muscles. Am J Anat 1932;51:417437.

  • 21. Lemere F. Innervation of the larynx; II. Ramus anastomoticus and ganglion cells of the superior laryngeal nerve. Anat Rec 1932;54:389.

  • 22. Burnie AGSJ, Corcoran BM. Gastro-esophageal reflux and hiatus hernia associated with laryngeal paralysis in a dog. J Small Anim Pract 1994;30:414416.

    • Search Google Scholar
    • Export Citation
  • 23. Raza SA, Mahendran S, Rahman N, et al. Familial vocal fold paralysis. J Laryngol Otol 2002;116:10471049.

  • 24. Summers B, De Lahnuta A, Cummings JF. Diseases of the peripheral nervous system. In: Summers BA, Cummings JF, DeLahunta A, eds. Veterinary neuropathology. St Louis: Mosby, 1995;409.

    • Search Google Scholar
    • Export Citation
  • 25. Kosaka K. Über die Vaguskerne des Hundes. Neur Centralbl 1909;28:406410.

  • 26. Szentagothai S. Die Lokalisation der Kehlkopfmuskulatur in den Vagus Kernen. Z Anat Entw Gesch 1943;112:704710.

  • 27. Fürstenberg AC, Magielski JE. A motor pattern in the nucleus ambiguus; its clinical significance. Ann Otol Rhinol Laryngol 1955;64:788793.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Gacek RR. Localization of laryngeal motor neurons in the kitten. Laryngoscope 1975;85:18411861.

  • 29. Higgs B, Kerr FW, Ellis FH. The experimental production of esophageal achalasia by electrolytic lesions in the medulla. J Thorac Cardiovasc Surg 1965;50:613625.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30. DeLahunta A. Cranial nerve—lower motor neuron: general somatic efferent system, special visceral system. In: DeLahunta A, ed. Veterinary neuroanatomy and clinical neurology. Philadelphia: WB Saunders, 1977;101, 408409.

    • Search Google Scholar
    • Export Citation
  • 31. Plott D. Congenital laryngeal-abductor paralysis due to nucleus ambiguus dysgenesis in three brothers. N Engl J Med 1964;271:593597.

All Time Past Year Past 30 Days
Abstract Views 897 0 0
Full Text Views 1562 1004 310
PDF Downloads 1200 493 40
Advertisement