A Retrospective Study of The Medical Status On 63 African - 2015 - Journal of Ex

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AEMV FORUM

A RETROSPECTIVE STUDY OF THE MEDICAL STATUS


ON 63 AFRICAN HEDGEHOGS (ATELERIX
ALBIVENTRIS) AT THE TAIPEI ZOO FROM 2003
TO 2011
Hsieh Pei-Chi, DVM, BA, Yu Jane-Fang, DVM, MS, and Wang Lih-Chiann, DVM, PhD

Abstract
Inbreeding of African hedgehogs (Atelerix albiventris) is considered a problem as breeders try to meet the
demands of the pet trade. Most studies of African hedgehogs are concentrated in the USA. This study
investigates and compares the life span and medical conditions of captive African hedgehogs at the Taipei
Zoo, Taiwan. The medical records of 63 African hedgehogs at the Taipei Zoo from 2003 to 2011 were
collected and analyzed statistically for this retrospective study. The mean life span of the 39 deceased
hedgehogs in the study was 3.4 ⫾ 1.1 years. The average weight was 401 ⫾ 98 g. Female hedgehogs were
heavier than males. The primary cause of death in this group of animals was neoplasia (35.9%). Oral
squamous cell carcinoma was the most common form of neoplasia diagnosed (35.7%). Hematologic and
serum biochemical tests from 9 healthy adults revealed increased alanine aminotransaminase, aspartate
aminotransferase, total bilirubin, and albumin values compared with references. Decreased values for
alkaline phosphatase, amylase, and creatinine levels were also found. The results of this study may
provide a better understanding of African hedgehog health and may help to determine potential
management problems. Copyright 2014 Elsevier Inc. All rights reserved.
Key words: African hedgehogs; Atelerix albiventris; neoplasia; retrospective study

A
frican hedgehogs (Atelerix albiventris), also known as white-bellied or 4-toed African pygmy
hedgehogs, are now commonly maintained in zoological parks. These animals have recently
become popular exotic pets worldwide. Hedgehogs are nocturnal, solitary creatures that rely on
olfactory and auditory senses rather than visual stimuli.1 There are an increasing number of
reports and research studies on African hedgehog diseases being published, especially regarding
spontaneous tumors.1-17 However, most of this information is based on research in the United States. There
are few African hedgehog veterinary medical articles that originate from other countries. This study
summarizes the medical records (2003 to 2011) of 63 African hedgehogs at the Taipei Zoo. Comparisons are
made to previous studies in an attempt to point out discrepancies in hedgehogs in different geographic areas
and to provide further information on the medical care and husbandry of hedgehogs.

MATERIALS AND METHODS used in this study. Of the 63 hedgehogs,


58 originated at the Taipei Zoo, whereas the other
Animals
5 were donated from owners who lived in Taipei.
The medical records of 63 African hedgehogs There were 24 males, 24 females, and 15 animals
located at the Taipei Zoo from 2003 to 2011 were of unknown sex that died immediately after birth.

From the School of Veterinary Medicine, National Taiwan University, Taipei, Taiwan; and the Taipei Zoo, Taipei, Taiwan.
Address correspondence to: Wang Lih-Chiann, DVM, PhD, School of Veterinary Medicine, National Taiwan University, No 1, Sec 4, Roosevelt
Rd, Taipei 10617, Taiwan. E-mail: [email protected].
Ó 2014 Elsevier Inc. All rights reserved.
1557-5063/14/2101-$30.00
http://dx.doi.org/10.1053/j.jepm.2014.11.003

Journal of Exotic Pet Medicine 24 (2015), pp 105–111 1 0 5


These 15 neonates were excluded from the University (NTU), and histopathology was
analysis. All hedgehogs were kept in plastic boxes performed at the Graduate Institute of Molecular
(74  51.5  42 cm3) with shaved wood as and Comparative Pathobiology, School of
bedding and wooden huts for hiding. For the time Veterinary Medicine, NTU. Tissue samples were
period evaluated, no exercise devices of fixed in 10% neutral, buffered formalin and then
significance were provided. Most hedgehogs were transported to the NTU laboratory where they were
kept alone in the box, except those maintained as embedded in paraffin, sectioned at 5 μm, and
pairs for breeding, or females nursing young. stained with hematoxylin and eosin for
A number of animals were rotated through the microscopic examination.
display area, which had room for 2 to 4 individuals
(approximately 150  120  120 cm3), hiding Statistical Analysis
places, and a running wheel. The diet offered the
hedgehogs included Mazuri Insectivore Diet (PMI Chi-square tests, the Student t test, and Z tests were
Nutrition International LLC, St. Louis, MO USA) used to analyze the data. The chi-square test was
and mealworms ad libitum. All animals had free used to look for associations with neoplasia. The
access to water. The environmental temperature of Student t test was applied for comparing average
the room that housed the hedgehog enclosures was weight between males and females. The Z test was
approximately 241C to 281C, and the humidity employed for analyzing hematologic and serum
was 60%. A 12-hour light-dark cycle was provided. biochemical values. A P o 0.05 was used to
At the time the retrospective study was being determine statistical significance.
conducted, 39 of 48 hedgehogs had died. The
average age of the remaining 9 individuals was 2.4 ⫾ RESULTS
0.5 years (range: 1.9 to 3.1 years). Average weight,
life span, causes of death, diseases, and blood test The mean life span of the 39 deceased hedgehogs
values were analyzed from selected groups of was 3.4 ⫾ 1.1 years. The average weight for the
hedgehogs within the study population. Only hedgehogs was 401 ⫾ 98 g, with males weighing
nonpregnant adults (46 months) and those less (373 ⫾ 104 g) than females (421 ⫾ 88 g).
without any current disease and treatment were used The causes of death are shown in Table 1. The
for body weight analysis (n = 48). Weight values highest percentages of deaths were due to
were obtained at various time intervals during the neoplasia. Neoplasia was diagnosed in 14 (35.9%)
investigation (total n = 565 recordings). A total of of the 39 hedgehogs; 4 were males and 10 were
13 blood samples were collected from 13 individuals females. All hedgehogs with neoplasia were adults,
who were alive from 2010 to 2011. Blood was and the mean age was 3.9 ⫾ 1.1 years. There was
collected during physical examination; 3 blood no sex predisposition associated with an outcome
samples were from hedgehogs with neoplasia, and 1 of neoplasia (P ¼ 0.12). Among 15 tumors
additional sample showed leukocytosis (35.4  109/L; diagnosed, the physical systems associated with the
reference range: 5 to 17  109/L).18,19 All 4 of these cancers were as follows: digestive (n ¼ 8),
individuals died within months after their blood hemolymphatic (n ¼ 3), respiratory (n ¼ 2),
was collected; therefore, these 4 samples were not
used in the study. Blood samples from the
remaining 9 apparently healthy adult hedgehogs,
TABLE 1. Causes of death in 39 African hedgehogs at
5 males and 4 females, were used for analysis. In
the Taipei Zoo from 2003 to 2011
preparation for venipuncture, animals were fasted
for 1 night before the blood draw. Blood samples Numbers of
Classification Cases Percentage
were collected from the cranial vena cava18 for
hematologic evaluation (Exigo Veterinary Neoplasia 14 35.9
Hematology Analyzer, Sweden) and serum Respiratory system 10 25.6
biochemical analysis (Spotchem EZ SP-4430, Japan). Digestive system 4 10.3
Causes of death were determined for all 39 deceased Respiratory and cardiac 3 7.7
systems
hedgehogs following full necropsy examination.
Bacterial infection 3 7.7
Cardiac system 2 5.1
Histopathology Hemolymphatic system 2 5.1
Musculoskeletal system 1 2.5
Necropsies were performed at the Taipei Zoo by
veterinary pathologists from the National Taiwan Total 39 100.0

1 0 6 Pei-Chi et al./Journal of Exotic Pet Medicine 24 (2015), pp 105–111


endocrine (n ¼ 1), and reproductive (n ¼ 1). lower alkaline phosphatase, amylase, and
The most commonly diagnosed tumors were oral creatinine values.
squamous cell carcinoma (SCC) (n ¼ 5),
lymphosarcoma (n ¼ 3), pulmonary
DISCUSSION
adenocarcinoma (n ¼ 2), mucoepidermoid
carcinoma of the parotid gland (n ¼ 1), The mean body weight of female hedgehogs
hepatocellular carcinoma (n ¼ 1), intestinal (421 ⫾ 88 g) at the Taipei Zoo was higher than the
adenocarcinoma (n ¼ 1), and uterine average weight of 385 g reported in the
adenocarcinoma (n ¼ 1). Only 1 hedgehog (7.1%) International Species Information System.20 Mean
presented with more than 1 type of tumor ⫾ standard deviation for female body weight was
(Table 2). also greater than that reported in another report
Overall, 10 hedgehogs died of respiratory (250 to 400 g),21 indicating that female hedgehogs
disorders, the second most common cause of at the Taipei Zoo were likely overweight or obese.
death. There were 4 cases of pneumonia, including Furthermore, females were heavier than males,
chronic diffuse pneumonia (n ¼ 2), purulent which also varied from the references.19,21
pneumonia (n ¼ 1), and aspiration pneumonia Hedgehogs were fed mealworms (larvae of
(n ¼ 1). There were 2 cases of emphysema, 2 cases Tenebrio molitor) and Mazuri Insectivore Diet ad
of diffuse pulmonary hemorrhage, 1 case of libitum, with superworms (larvae of Zophobas
pulmonary edema, and 1 death attributed to morio) occasionally being offered. A previous study
respiratory distress of unknown origin. indicated hedgehogs focus on a preferred type of
Moreover, 4 hedgehogs died of gastrointestinal food if the food source is abundant. According to
disease, which was the third most common cause another study, female hedgehogs choose food that
of death. These included intestinal obstruction is much richer in fat and protein.22 Long-term
(n ¼ 2), gastritis and duodenitis (n ¼ 1), and observation verified that hedgehogs at the Taipei
gastric ulceration (n ¼ 1). Zoo preferred mealworms over dry Mazuri
Blood samples obtained from apparently Insectivore Diet. Recommended protein and fat
healthy adults (n ¼ 9) were used for blood analysis requirements for hedgehogs are 22% and 5%,
(Table 3). Compared with reference ranges,19 respectively, but nutritional analysis shows crude
African hedgehogs at the Taipei Zoo had higher protein and crude fat percentages in living
albumin, alanine aminotransaminase (ALT), mealworms are 52.7% and 32.8%, respectively.23
aspartate aminotransferase (AST), and total Because African hedgehogs at the Taipei Zoo ate
bilirubin values. These animals also demonstrated mealworms as their major food source, they

TABLE 2. Neoplasia diagnosed in African hedgehogs at Taipei Zoo from 2003 to 2011
ID Sex Age (y)a Neoplasm Location
11 F 2.9 Islet cell carcinoma Pancreas and metastasized to liver
14 M 4.8 Squamous cell carcinoma Oral cavity
15 F 3.1 Lymphosarcoma Right axillary lymph node
16 F 4.3 Lymphosarcoma Submandibular lymph nodes and mediastinal lymph node
19 F 4.5 Lymphosarcoma Right axillary and left inguinal lymph nodes
24 F 3.8 Mucoepidermoid Right parotid gland region and extended to neck
carcinoma
25 M 4.8 Hepatocellular carcinoma Right anterior lobe, right medial lobe, and left anterior lobe
26 F 3.8 Squamous cell carcinoma Oral cavity
29 F 4.3 Squamous cell carcinoma Oral cavity
31 F 3.7 Squamous cell carcinoma Oral and nasal cavity
32 F 4.3 Squamous cell carcinoma Oral and nasal cavity
46 M 4.5 Pulmonary Bilateral superior and inferior lobes and right middle lobe
adenocarcinoma
49 F 5.1 Pulmonary Bronchus
adenocarcinoma
Uterine adenocarcinoma Inside uterus, where it is attached to the uterine wall with a pedicle
66 M 0.7 Intestinal adenocarcinoma In intestine approximately 10 cm away from pylorus
M, male; F, female.
a
Age of death.

Pei-Chi et al./Journal of Exotic Pet Medicine 24 (2015), pp 105–111 1 0 7


TABLE 3. The hematologic and serum biochemical values of hedgehogs at the Taipei Zoo (n ¼ 9)
Measurement Values Reference Range
Hematology
PCV (%) 37.0 ⫾ 2.5 (33.1 to 41.0) 36 ⫾ 7 (22 to 64)
RBC (106/mL) 5.9 ⫾ 0.4 (5.3 to 6.6) 6 ⫾ 2 (3 to 16)
Hb (g/dL) 13.3 ⫾ 0.8 (12.0 to 14.4) 12.0 ⫾ 2.8 (7.0 to 21.1)
MCV (fL) 62.6 ⫾ 2.7 (59.3 to 67.3) 67 ⫾ 9 (41 to 94)
MCH (pg) 22.5 ⫾ 1.0 (21.5 to 24.4) 22 ⫾ 4 (11 to 31)
MCHC (g/dL) 35.9 ⫾ 0.6 (35.0 to 37.0) 34 ⫾ 5 (17 to 48)
Platelets (103/mL) 187.0 ⫾ 41.9 (129 to 236) 226 ⫾ 108 (60 to 347)
WBC (103/mL) 10.3 ⫾ 4.1 (5.8 to 16.8) 11 ⫾ 6 (3 to 43)

Chemistries
Alkaline phosphatase (IU/L)a b 51 ⫾ 21 (8 to 92)
ALT (IU/L)c 104.8 ⫾ 48.4 (42 to 189) 53 ⫾ 24 (16 to 134)
Amylase (IU/L)a 311.2 ⫾ 103.9 (153 to 450) 510 ⫾ 170 (244 to 858)
AST (IU/L)c 85.7 ⫾ 56.8 (6 to 197) 34 ⫾ 22 (8 to 137)
Bilirubin, total (mg/dL)c 0.6 ⫾ 0.2 (0.3 to 0.8) 0.3 ⫾ 0.3 (0.0 to 1.3)
BUN (mg/dL) 30.8 ⫾ 8.5 (22 to 47) 27 ⫾ 9 (13 to 54)
Cholesterol (mg/dL) 132.9 ⫾ 28.6 (103 to 195) 131 ⫾ 25 (86 to 189)
Creatinine (mg/dL)a 0.2 ⫾ 0.1 (0.0 to 0.4) 0.4 ⫾ 0.2 (0.0 to 0.8)
Glucose (mg/dL) 101.6 ⫾ 28.4 (62 to 151) 89 ⫾ 30
Phosphorus (mg/dL) 4.6 ⫾ 0.6 (3.4 to 5.4) 5.3 ⫾ 1.9 (2.4 to 12.0)
Protein, total (g/dL) 6.2 ⫾ 1.4 (3.8 to 9.0) 5.8 ⫾ 0.7 (4.0 to 7.7)
Albumin (g/dL)c 3.3 ⫾ 1.7 (0.1 to 5.0) 2.9 ⫾ 0.4 (1.8 to 4.2)
BUN, blood urea nitrogen; Hb, hemoglobin; MCH, mean corpuscular hemoglobin; MCHC, mean corpuscular hemoglobin
concentration; MCV, mean corpuscular volume; PCV, packed cell volume; RBC, red blood cell; WBC, white blood cell.
a
Lower values (P o 0.05).
b
The values were too low to be correctly estimated during the serum biochemical test because of the false-negative effect of EDTA
on the alkaline phosphatase (ALKP) value.
c
Higher values (P o 0.05).

over-ingested protein and fat, which likely observed in this study. The family tree of 58
contributed to obesity. individuals with a known blood relationship
Several previous studies showed the top 3 among the 63 hedgehogs is depicted in the Figure,
systems affected by neoplasia in African hedgehogs which implies a severe inbreeding problem at the
were the integumentary, hemolymphatic, and Taipei Zoo. We speculate that inbreeding might be
digestive systems. In the United States, the most the potential cause of variability in tumor type.
common tumor types were mammary gland Statistical differences in the prevalence of
adenocarcinoma, lymphoma, and oral SCC.11,15,24 lymphosarcoma and SCC in hedgehogs at the
However, the results of this study showed that Taipei Zoo were compared with the prevalence in
tumor types encountered at the Taipei Zoo were animals submitted to an exotic pathology service
remarkably different from other studies. There were in the United States from 1994 to 1999
no cases of mammary gland adenocarcinoma, but (Northwest ZooPath, Monroe, WA USA).11 There
relatively higher rates of oral SCC. In these cases, were no statistical differences in lymphosarcoma
SCC mostly infiltrated into the propria-submucosa (P ¼ 0.97) or oral SCC (P ¼ 0.39) by chi-square
of the oral cavity; however, SCC also extended into analysis. Sex also had no effect on tumor
nasal cavities in a few individuals. prevalence (P ¼ 0.79).11 In general, the average
Genetic boundary might play a role in this age of hedgehogs with neoplasia was 0.5 years
discrepancy. The importation of African hedgehogs longer than that of all hedgehogs in this
into the United States has been prohibited since retrospective study, suggesting that increased age
1991 (Title 9 Code of Federal Regulations Section is a potential risk factor for this disease process.
93.701) owing to their potential to carry foot-and- These results agree with those of another
mouth disease.25 Therefore, most of the hedgehogs retrospective study, which concluded that the
in the United States may lack genetic variability increased life span associated with captivity led to
owing to inbreeding.26 A similar situation was an increase in neoplasia.11

1 0 8 Pei-Chi et al./Journal of Exotic Pet Medicine 24 (2015), pp 105–111


FIGURE. The family tree of African hedgehogs at Taipei Zoo from 2003 to 2011.

Pei-Chi et al./Journal of Exotic Pet Medicine 24 (2015), pp 105–111 1 0 9


Considering the relatively short life span of The death rate for the neonates in this
hedgehogs and the high cost of therapy, none of population of hedgehogs was high (27.8%). The
the hedgehogs affected with neoplasia were treated. 15 neonates that died were apparently healthy and
When quality of life was judged to be poor and without obvious external abnormalities at birth;
could not be improved with supportive therapy, however, all died within a few days and were
euthanasia was performed. severely injured, lacking limbs or other body parts.
Among the 10 hedgehogs that died of respiratory Because expectant females were kept in isolation,
disorders, more than half (n ¼ 6) were combined the authors speculate that the major cause of death
with other diseases. Moreover, 2 chronic diffuse was maternal attack. This behavior was limited to
pneumonia cases were accompanied with only a few specific female hedgehogs. Other
neoplasia, 1 purulent pneumonia case was females under the same environmental conditions
accompanied with purulent hepatitis, and 2 raised their young without problems, including
pulmonary hemorrhage cases and 1 pulmonary any signs of attack or abandonment. Therefore, it is
edema case had concurrent heart enlargement and presumed that poor mothering skills played a
congestion. This observation indicated that other larger role than environmental stress in these cases.
disorders, and not just simple respiratory disease, Because the maternal attacks only occurred in the
may play an important role in this cause of death. litters of a few females, it was recommended that
Overall, 4 hedgehogs died of gastrointestinal these animals not be selected for reproductive
disorders; 2 diagnosed with intestinal foreign body activity in the future.
obstruction exhibited large amounts of bedding Most published articles on hedgehogs are from
(shaved wood) in the stomach. Moreover, 1 the United States, including retrospective
individual with gastritis and duodenitis had a studies7,9,11,14,15,27,30,31 and sporadic case
number of decayed teeth and severe gingivitis. The reports.2-6,8,10,12,17,32 Little information on the
authors’ suspect the gastritis in this case may have health status of hedgehog populations is known
been related to poor mastication followed by from other geographic areas. The authors found
chronic impairment of the gastric mucosal barrier that the hedgehogs from the Taipei Zoo showed
by food boluses. Another individual died of gastric differences in body weight, serum biochemical
ulceration, exhibiting anorexia and soft stool values, and tumor prevalence compared with those
immediately before death. Unfortunately, the found in previous publications. Geographic and
cause of these ulcers could not be determined at genetic discrepancies with unequal husbandry may
necropsy. have played a role in these differences. Genetic
The hematologic values of 9 apparently healthy analysis from various geographic areas may be
hedgehogs were all within reference ranges, but the beneficial to clarify the role of genetics in African
serum biochemical values revealed higher ALT, hedgehog health. In the future, recommendations
AST, total bilirubin, and albumin levels when for captive care include improved diet with limited
compared with the reference values.19 In total, 5 high-fat items and increased opportunities for
animals (3 females and 2 males) were considered enrichment and exercise.
obese, with body condition scores of 5/5 and an
average weight of 512 g. Although serum
cholesterol levels for these animals were within the ACKNOWLEDGMENT
reference range and serum triglyceride was not
analyzed, it was not possible to rule out lipemia in The authors would like to thank the curator and
these samples, which could have caused artifactual keepers of the Taipei Zoo for their assistance with
elevations of ALT, AST, and total bilirubin levels. this study.
Higher albumin values in the hedgehogs from this
study may have been caused by ingesting excessive
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