Veterinary Medicine International

Volume 2013 (2013), Article ID 617803, 6 pages

http://dx.doi.org/10.1155/2013/617803

Research Article

Prevalence of Swimming Puppy Syndrome in 2,443 Puppies during the Years 2006–2012 in Thailand

Korakot Nganvongpanit1,2 and Terdsak Yano³

¹Animal Bone and Joint Research Laboratory, Department of Veterinary Biosciences and Public Health, Faculty of Veterinary Medicine, Chiang Mai University, Chiang Mai 50100, Thailand

²Materials Science Research Center, Faculty of Science, Chiang Mai University, Chiang Mai 50200, Thailand

³Department of Food Animals, Faculty of Veterinary Medicine, Chiang Mai University, Chiang Mai 50100, Thailand

Received 12 March 2013; Revised 11 May 2013; Accepted 14 May 2013

Academic Editor: Remo Lobetti

Copyright © 2013 Korakot Nganvongpanit and Terdsak Yano. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract.

The purpose of this study was to report on the prevalence of swimming puppy syndrome (SPS) and investigate predisposing factors. Data were recorded from 2,443 puppies (1,183 males and 1,260 females) in Thailand, October 2006–September 2012, including breed, sex, number of puppies per litter, type of nest floor, number of affected limbs, and occurrence of pectus excavatum. Fifty-two puppies (2.13%) were diagnosed with SPS. The breed most frequently affected was English Bulldog (8.33%). There was no significant difference between presence and absence of disease based on sex, breed, and nest floor type. The number of puppies per litter was associated with SPS; puppies from smaller litters (1.92 ± 1.12) had a higher prevalence of the disease than puppies from larger litters (3.64 ± 2.24). Moreover, 15.38% of puppies with affected limbs showed signs of pectus excavatum (8/52); this clinical sign was more prevalent in puppies with all four limbs affected with SPS.

1. Introduction

Swimming puppy syndrome—also known as swimmer syndrome, flat pup syndrome, splay leg (paraparesis), splay weak (tetraparesis), and myofibrillar hypoplasia—is one of the musculoskeletal disorders in puppies [1]. In the initial weeks of life, newborn puppies seem normal: they gain weight quickly, suck well, and appear to be completely healthy. Signs begin to appear when the puppy learns to walk (2nd-3rd week), with spreadout legs like a swimmer [1]. In some cases, there are additional complications, because such puppies tend to lie on their bellies most of the time. The center of gravity is shifted to the chest, while the soft ribs cannot maintain their correct shape; thus the chest, under the pressure of body weight, splays on both sides, and the thorax becomes flat (funnel chest) [2–4]. Some puppies show snake-like or walrus-swimming movements, crawling on their bellies with limbs extended and exorotated. Sterna concave, dorsoventral flattening of the chest, or pectus excavatum will present when forelimbs are affected [2, 3]. In cases of pectus excavatum, puppies show respiratory insufficiency, with dyspnoea, mouth continuously open, and bluish mucous membranes [3, 4]. The differential diagnosis of this disease includes encephalomeningitis, canine distemper, toxoplasmosis, neosporosis, myopathies, and spina bifida [4, 5]. The treatment success rate is dependent on the time of diagnosis and treatment [4, 5]. Usually puppies with this disease recover well after early diagnosis and treatment such as limb realignment, bandages, and physical rehabilitation [4, 5].

However, little is known about the prevalence of swimming puppy syndrome, other than from observational experience and a limited amount of information available on the internet (based on a search of PubMed and Scopus databases). Also, several of these publications were in the format of case reports in which only a few puppies showed signs of this disease [1–6]. From the existing information [5], it can be concluded that some of the predisposing causes of the disease are small breeds (Dachshund and Yorkshire Terrier) and also breeds with a large thorax and short limbs (Pekingese, Basset Hound, French, and English Bulldogs). Other predisposing causes [4] include puppies of normal size at birth but with faster growth than the rest of the litter and, in particular, a low number of puppies per litter.

In the present study, the number of cases of swimming puppy syndrome was recorded by breed, together with other factors; statistical analysis was used to study the prevalence, incidence, and risk factors of this disease.

2. Materials and Methods

2.1. Animals

In this retrospective study of clinical records (Table 1) of 2,443 puppies (1,183 males and 1,260 females) that were 3 months old or younger were reviewed. The puppies had undergone treatment for various reasons at 19 animal clinics/hospitals in Thailand (Figure 1) from October 2006 to September 2012.

Table 1: Number of puppies in each breed included in the study.

Breed
Total
Male
Female
Number of litters
Number of puppies/litter (mean ± SD)

Small breed (<10 kg)

    Chihuahua
256
125
131
111

    Dachshund
18
8
10
5

    Jack Russell Terrier*
19
15
4
6

    Pekingese
58
27
31
22

    Pomeranian
293
131
162
130

    Poodle
82
45
37
26

    Pug
77
31
46
23

    Shih Tzu
265
123
142
76

    Yorkshire Terrier
165
74
91
79

Medium breed (10–25 kg)

    Beagle*
60
36
24
13

    Bulldog (English)
48
25
23
14

    French Bulldog
53
23
30
14

    Crossbreed
122
48
74
21

    Shetland Sheepdog*
11
5
6
2

    Thai Bangkaew
85
49
36
13

    Thai Ridgeback*
13
5
8
2

Large breed (25–40 kg)

    American Pit Bull Terrier*
71
32
39
9

    German Shepherd*
76
42
34
11

    Golden Retriever
217
103
114
36

    Labrador Retriever
213
115
98
36

    Rottweiler*
109
48
61
16

    Siberian Husky
132
73
59
28

Total
2,443
1,183
1,260
=
—

Breed was not affected with swimming puppy syndrome.

Figure 1: Geographic distribution of cases and clinics/hospitals included in the study in Thai.

The data collected included breed, age, weight, sex, number of puppies per litter, and floor condition on which the puppies were fostered. Moreover, the findings of the clinical examination of all affected puppies were reviewed, including affected limbs and the occurrence of pectus excavatum.

In case there was missing data, the authors called the pet owner to ask for the necessary information. If the pet owner was unable to supply the missing data, or when information about other puppies in the same litter could not be obtained, the puppy was excluded from the study.

2.2. Statistical Analysis

Demographic data of the samples were described by descriptive statistics. Sex, breed size, floor conditions, and number of puppies per litter were assumed to be the associated risk factors for swimmer puppy syndrome and were investigated to determine the correlation between these factors and swimming puppy syndrome. The correlation between affected limb(s) and the occurrence of pectus excavatum was analyzed using the R statistical software program. For statistical analysis, dogs were categorized according to weight into three groups: large (>25 kg), medium (10–25), and small (<10 kg) breeds. The epi2x2 function in the epibasix package was used to examine the correlation between sex and the occurrence of the disease. A chi-squared test was used to evaluate the correlation between breed size, type of floor, and occurrence of the disease. Fisher’s exact test was used to determine the correlation between affected limbs and the occurrence of pectus excavatum. Finally, the mean number of puppies per litter and the presence of diseased and nondiseased animals were analyzed by a t-test. The significance level was set at .

3. Results

The present study found that the disease started to present beginning at week , but the owner brought puppy to the visiting veterinarian at week .

3.1. Breed

A total of 2,443 puppies (1,183 males and 1,260 females) were included in this study. Twenty-two breeds of puppies were recorded in the clinical notes and of these, swimming puppy syndrome was recorded in 15 breeds. Comparing within breed, English Bulldog was found to have the highest percentage of diseased puppies, 8.33% (4/48); second was French Bulldog, 7.54% (4/53), and third was Pekingese, 6.89% (4/58). The other breeds were found to have a mean prevalence of 2.65% (range 0.78–5.55%), as shown in Table 2.

Table 2: Number of puppies in different breeds affected with swimming puppy syndrome.

Healthy puppies
Swimming puppy syndrome
%**

Male
Female
Total
Male
Female
Total (%*)

Small breed (<10 kg)

    Chihuahua
125
131
256
1
1
2 (0.78)
3.85

    Dachshund
8
10
18
1
—
1 (5.55)
1.92

    Pekingese
27
31
58
1
3
4 (6.89)
7.69

    Pomeranian
131
162
293
1
1
2 (0.68)
3.85

    Poodle
45
37
82
2
1
3 (3.65)
5.77

    Pug
31
46
77
—
2
2 (2.59)
3.85

    Shih Tzu
123
142
265
1
2
3 (1.17)
5.77

    Yorkshire Terrier
74
91
165
1
1
2 (1.21)
3.85

Medium breed (10–25 kg)

    Bulldog (English)
25
23
48
2
2
4 (8.33)
7.69

    French Bulldog
23
30
53
1
3
4 (7.54)
7.69

    Crossbreed
48
74
122
3
—
3 (2.45)
5.77

    Thai Bangkaew
49
36
85
2
1
2 (2.35)
3.85

Large breed (25–40 kg)

    Golden Retriever
103
114
217
6
2
8 (3.68)
15.38

    Labrador Retriever
115
98
213
3
2
5 (2.34)
9.62

    Siberian Husky
73
59
132
4
3
7 (5.30)
13.46

Total
1,000
1,084
2,084
29
23
52
100

Percentage of affected puppies compared within breeds.

Percentage of affected puppies compared between breeds.

Comparison of all affected breeds revealed that Golden Retriever had the highest percentage of affected puppies (15.38%), followed by Siberian Husky (13.46%) and Labrador Retriever (9.62%). The lowest prevalence was found in Dachshunds (1.92%), followed by five other breeds, including Chihuahua, Pomeranian, Pug, Yorkshire Terrier, and Thai Bangkaew, all with the same percentage (3.85%).

Affected puppies were compared within the same sized groups; medium-size puppies were found to have the highest number of affected animals (3.32%). Affected percentages of large and small sizes were 2.44% and 1.54%, respectively. Comparatively, the number of affected puppies in terms of breed size was not significantly different ().

3.2. Sex

As shown in Table 2, of the 52 number of puppies affected by swimming puppy syndrome, 56% was males (), and 44% was females (). The prevalence of swimming puppy syndrome was not significantly different between male and female dogs () (Table 3).

Table 3: Factor of sex on expression of disease.

Sex
Total
Disease present (cases)
Disease absent (controls)

Male
1,184
29 (2.45%)
1,155 (97.55%)

Female
1,259
23 (1.83%)
1,236 (98.17%)

Pearson’s chi-squared statistic (includes Yates’ continuity correction) = 0.423; value using Fisher’s exact test (1 degree of freedom) = 0.484; estimate of odds ratio = 1.248; 95% confidence limits for true odds ratio = [0.72, 2.166]; estimate of risk difference () in case-control studies = 0.055; 95% confidence limits for risk difference = [0.006, 0.105].

3.3. Number of Puppies per Litter

This study found a significant decrease () in the number of puppies per litter in the affected group () compared to clinical unaffected dogs () (Table 4). The number of puppies per litter in healthy small breeds was dogs, while in affected puppies it was dogs. In medium breeds, there were healthy puppies per litter and affected puppies per litter. Large breeds showed a similar result, with healthy puppies per litter versus affected puppies per litter (Table 5).

Table 4: Number of puppies per litter with presence or absence of disease.

Data
Disease present (cases)
Disease absent (controls)

Number of samples
52
641

Mean number of puppies per litter
1.92
3.65

Standard deviation
1.12
2.24

= 9.6906; degrees of freedom = 88.859; < 0.001.

Table 5: Number of puppies per litter in normal and affected groups.

Breed
Number of puppies per litter
value

Disease absent
Disease present

Small breed

    Chihuahua

0.000

    Dachshund

—
—

    Jack Russell

    Terrier

—
—

    Pekingese

0.001

    Pomeranian

0.001

    Poodle

0.000

    Pug

0.001

    Shih Tzu

0.006

    Yorkshire

    Terrier

0.000

    Mean ± SD
3 ± 1
1 ± 1

Medium breed

    Beagle

—
—

    Bulldog

    (English)

0.002

    French Bulldog

0.008

    Crossbreed

0.000

    Shetland

    Sheepdog

—
—

    Thai Bangkaew

0.005

    Thai Ridgeback

—
—

    Mean ± SD
5 ± 3
2 ± 1

Large breed

    American pit

    Bull Terrier

—
—

    German

    Shepherd

—
—

    Golden

    Retriever

0.000

    Labrador

    Retriever

0.000

    Rottweiler

—
—

    Siberian Husky

0.011

    Mean ± SD
6 ± 3
3 ± 1

3.4. Nest Floor

Swimming puppy syndrome was found to be the highest among puppies raised on concrete floors, followed by tile and wood floors, respectively (Table 6). The percentages of the disease present in animals raised on tile; wood and concrete floors were similar: 2.25%, 2.64% and 1.28%, respectively. However, no significant difference () was established in the prevalence of swimming puppy syndrome between the different floor types.

Table 6: Number of litters on different floor types.

Floor type
Total

Tile
Concrete
Wood

Disease present (cases)
29 (2.25%)
15 (2.64%)
8 (1.28%)
52

Disease absent (controls)
1,261 (97.75%)
554 (97.36%)
617 (98.72%)
2,432

Total
1,290
569
625
2,484

Chi squared = 2.9861; degrees of freedom = 2; value = 0.2247.

3.5. Pectus Excavatum

Eight puppies with swimming puppy syndrome had pectus excavatum. Puppies affected in all limbs with swimming puppy syndrome showed a significantly higher () prevalence of pectus excavatum (87.5%). When only the forelimbs were affected, 20% showed signs of pectus excavatum; no signs of pectus excavatum were found when only the hindlimb was affected (Table 7).

Table 7: Relationship between affected limb and occurrence of pectus excavatum.

Affected limb
Pectus excavatum
Total

Present
Absent

Forelimb
1 (20%)
4 (80%)
5

All limbs
7 (87.5%)
1 (12.5%)
8

Hindlimb
—
39 (100%)
39

Total
8 (15.38%)
44 (84.62%)
52

P < 0.001.

4. Discussion

Despite numerous investigations, the etiology and pathogenesis of swimming puppy syndrome are poorly understood [1, 4, 5]. Moreover, previous publications have reported that swimming puppy syndrome is an uncommon developmental abnormality observed in puppies [5, 6]. However, the present study established a prevalence (52) of 2.1% of 2,443 puppies. According to previous investigations [5–9], the etiopathogenesis of this disease is unclear; the authors propose that nutritional, neurological, hereditary, and orthopaedic causes are possible underlying factors. The results from the present study further clarify some of the unclear underlying causes of this disease.

From our observations, body weight has a significant effect on the likelihood of disease presentation. However, we did not weigh all puppies (diseased and nondiseased) at all ages to conduct a thorough statistical analysis. Another limitation of this study is that puppies were not brought to a clinic/hospital immediately upon presenting the disease. In most cases, the owner delayed bringing the pet to a clinic/hospital until week of age, while the disease typically presents at week . For this reason, puppies could not be weighed at a young enough age to determine whether weight was one of the primary risk factors of this disease. However, based on veterinarians’ observations, more than 90% of the affected puppies were overweight and were typically larger than puppies of the same breed at the same age. The primary focus of the present study was on the number of puppies per litter and its effect on presentation of the disease. We also documented that a lower number of puppies per litter resulted in higher body weight of puppies. This study found that a significantly () lower number of puppies per litter were observed in the case of affected puppies () compared to unaffected puppies (). Therefore, the statements as mentioned above can conclud that lower number of puppies per litter might be associated with higher body weight of the puppies, but this is not examined.

The results of this study indicate the possibility that hereditary or genetic factors are not the underlying cause of this disease, since out of 52 diseased puppies in this study only 2 puppies (Siberian Husky) were from the same litter. Also, their parents had never given birth to puppies with this syndrome before (in 3 previous litters). Information from other owners also indicated that the puppies affected with the disease were the first that had been born to a particular set of parents. For this reason, we believe that the disease is not genetically related. However, to fulfill the data and elucidate the possible genetic basis of swimming puppy syndrome, our group is conducting a molecular genetics study of candidate genes for this disease; the results are to be published in the near future.

In the case of pigs, splay leg has been proven to be a hereditary disorder [10, 11]. Maak and others [11] pinpointed the candidate genes for splay leg in piglets using DNA microarray data, comparing the genome-wide gene expression of three hindlimb muscles between affected and healthy piglets. They found 63 transcripts with differences in two muscle groups and 5 gene differences in three muscle groups. Based on their study results, they concluded that certain genes were associated with splay leg in piglets and that future studies of the genetic mechanism needed to be performed in order to achieve a better understanding of the pathogenesis of this disease.

The present study found that the disease started to present beginning at week , when normal puppies are learning to stand and walk, that is, after 10–14 days of age [8, 12]. Previous reports also found that the disease started in the 2nd to 4th week [5, 13]. However, in this study, owners typically did not bring their puppies to a clinic or hospital when the disease first presented, but instead waited until puppies were weeks of age. Almost none of the owners recognized that the swimming movement was an abnormality. This is responsible for the delay in treatment, which leads to a reduction in the success rate of treatment. All previous reports agree that early diagnosis and treatment will result in a good prognosis, while delayed treatment results in poor prognosis.

A surprising result from this study, when comparing the 52 affected puppies, was that Golden Retrievers (15.38%) had the highest number of puppies affected with swimming puppy syndrome, followed by Siberian Husky (13.46%) and Labrador Retriever (9.62%). Moreover, we also found that many medium breeds (Bulldog, French Bulldog, Crossbreed, and Thai Bangkaew) were affected by this disease. However, these figures could be explained because those medium and large breeds that were more affected by swimming puppy syndrome had a small number of average puppies per litter ( and puppies per litter for large and medium breeds, resp.). This low number of puppies per litter is a cause of overweight puppies, to the extent where puppies may not be able to stand and walk properly. However, when comparing the number of affected puppies within a breed, the highest percentage of disease was found in Bulldogs (8.33%), French Bulldogs (7.54%), and Pekingese (6.89%), findings which were in agreement with previous reports [4, 5, 9, 12] where swimming puppy syndrome was commonly found in brachycephalic and chondrodystrophoid breeds.

Some clinicians have discussed the effects of the nest floor on the prevalence of this disease, but no scientific research on this issue has yet been published. In this study, tile floors produced the highest number (56%) of cases, followed by concrete floors (29%) and wood floors (15%); however, there was no significant difference () between the types of floor.

Affected limb (pathological limb) is a topic which has been widely discussed in the literature concerning this disease. The present results found that in 75% of cases the affected limb was predominantly a hindlimb; a lower number of cases (15.38%) were found to have all four limbs affected; the lowest number represented cases where only the forelimb was affected (9.62%). Together with an affected limb, pectus excavatum was found in 8 puppies: 7 puppies with all limbs affected and 1 puppy with a hindlimb affected. Only 1 puppy with all limbs affected did not show signs of pectus excavatum. Because of continuous sternal recumbency, particularly in puppies affected in the forelimb, the pressure of the body weight against the sternum causes flattening of the chest. The study data showed that an affected forelimb was significantly related to the presence of pectus excavatum. This was in agreement with previous case reports [3–5, 13, 14], which found that all puppies with an affected forelimb also had pectus excavatum.

One disadvantage of this study is that we could not conclude that swimming puppy syndrome is one of the risk factors of pectus excavatum, because this study did not record the number of puppies affected only with pectus excavatum, without swimming puppy syndrome. A search of previous publications revealed that the prevalence of pectus excavatum in dogs has not been reported; however, in cats it was found to be 2.05% (5/244) [15] and in humans 1.0–1.27% [16, 17]. Although the present study did not primarily focus on the incidence of pectus excavatum, 0.33% of puppies (8 out of 2,443) were found to have pectus excavatum. Compared with the previous study, it seems possible that a higher percentage of cats are affected by pectus excavatum.

Swimming puppy syndrome has been considered to be uncommon, based on clinical observations and a low number of published reports. But our study indicated that a few number of puppies are affected by this disease. The primary risk factor of this disease is a lower number of puppies per litter, while other factors, including sex and floor type, may not be involved. The present results could be applied for use in future studies: for example, the possible genetic control of this disease and the potential involvement of other risk factors. Moreover, all limb lesions are associated with pectus excavatum.

Acknowledgments

The authors gratefully acknowledge the veterinarians and technician assistants in all small animal clinics and hospitals in Thailand for their kind support during the study. The authors wish to thank the National Research University Project under Thailand’s Office of the Higher Education Commission for grant support.

References

J. E. Harkness and L. F. McCormick, “Swimming-puppy syndrome in a litter of German Shepherd pups,” Veterinary Medicine Small Animal Clinician, vol. 76, no. 6, pp. 817–821, 1981.

T. W. Fossum, R. J. Boudrieau, and H. P. Hobson, “Pectus excavatum in eight dogs and six cats,” Journal of the American Animal Hospital Association, vol. 25, pp. 595–605, 1989.

S. C. Rahal, M. M. Morishin Filho, E. Hatschbach, V. M. V. Machado, K. P. Aptekmann, and T. P. Corrêa, “Pectus excavatum in two littermate dogs,” Canadian Veterinary Journal, vol. 49, no. 9, pp. 880–884, 2008.

G. Verhoeven, H. de Rooster, M. Risselada, P. Wiemer, L. Scheire, and H. van Bree, “Swimmer syndrome in a Devon rex kitten and an English bulldog puppy,” Journal of Small Animal Practice, vol. 47, no. 10, pp. 615–619, 2006.

C. Yardimci, A. Özak, H. O. Nisbet, and Y. S. Şirin, “Swimming syndrome in two Labrador puppies,” Kafkas Universitesi Veteriner Fakultesi Dergisi, vol. 15, no. 4, pp. 637–640, 2009.

V. M. Stein, M. Kohlbach, M. Fehr, and A. Tipold, “Swimmer syndrome in puppies—no indication for euthanasia!,” Kleintierpraxis, vol. 52, no. 4, pp. 225–230, 2007.

G. Hosgood and J. D. Hoskins, “Swimmer puppy syndrome,” in Small Animal Paediatric MedicIne and Surgery, G. Hosgood and J. D. Hoskins, Eds., p. 271, Butterworth-Heinemann, Oxford, UK, 1998.

J. D. Hoskins, “Swimmer puppies and kittens,” in VeterInary Pediatrics, J. D. Hoskins, Ed., pp. 419–420, W.B. Saunders, Philadelphia, Pa, USA, 2001.

P. F. Suter, “Swimmers flat pup syndrome,” in Thoracic Radiography: A Text Atlas of Thoracic Diseases of the Dog and Cat, P. F. Suter, Ed., pp. 164–165, Wettswil, Zürich, Switzerland, 1984.

D. Boettcher, R. Schmidt, C. Rehfeldt, G. Thaller, H. H. Swalve, and S. Maak, “Evaluation of MAFbx expression as a marker for congenital splay leg in piglets,” Developments in Biologicals, vol. 132, pp. 301–306, 2008.

S. Maak, D. Boettcher, J. Tetens et al., “Identification of candidate genes for congenital splay leg in piglets by alternative analysis of DNA microarray data,” International Journal of Biological Sciences, vol. 5, no. 4, pp. 331–337, 2009.

M. D. Lorenz, “The “swimming puppy” syndrome,” in Current VeterInary Therapy VI: Small Animal Practice, R. W. Kirk, Ed., pp. 905–906, W. B. Saunders, Philadelphia, Pa, USA, 6th edition, 1977.

S. Kongsawasdi, B. Chuatrakoon, and K. Nganvongpanit, “Physical rehabilitation treated swimming puppy syndrome,” Chiang Mai Veterinary Journal, vol. 9, no. 2, pp. 105–112, 2011.

R. J. Boudrieau, T. Fossum, S. M. Hartsfield, H. P. Hobso, and R. L. Rudy, “Pectus excavatum in dogs and cats,” Compendium on Continuing Education for the Practicing Veterinarian, vol. 12, pp. 341–355, 1990.

T. M. Charlesworth and C. P. Sturgess, “Increased incidence of thoracic wall deformities in related Bengal kittens,” Journal of Feline Medicine and Surgery, vol. 14, no. 6, pp. 365–368, 2012.

F. L. Westphal, L. C. de Lima, J. C. Lima Neto, A. R. Chaves, V. L. dos Santos Júnior, and B. L. C. Ferreira, “Prevalence of pectus carinatum and pectus excavatum in students in the city of Manaus, Brazil,” Jornal Brasileiro de Pneumologia, vol. 35, no. 3, pp. 221–226, 2009.

A. M. Williams and D. C. G. Crabbe, “Pectus deformities of the anterior chest wall,” Paediatric Respiratory Reviews, vol. 4, no. 3, pp. 237–242, 2003.