1 Introduction

The Ethiopian or desert hedgehog (Paraechinus aethiopicus) belongs to the mammalian order Insectivora (Lipothyphyla) which is one of the most complicated orders in mammalian taxonomy (Symonds, 2005). This group of animals was once regarded as “waste-basket” as it contains the mammalian species lacking some mammalian characteristics and being insectivores (Butler, 1972; Symonds, 2005). They were reclassified and placed into a separate order (Erinaceomorpha) with two subfamilies (Hutterer, 2005; Bannikova et al., 2014): Erinaceidae (spiny hedgehogs or true hedgehogs) and Galerucinae (hairy hedgehogs; gymnures and moonrats). The Erinaceidae contains five genera and Paraechinus is among them. The desert hedgehog is distributed in Africa from Morocco and Algeria to Egypt, Sudan, Ethiopia, Eretria and Somalia. In the Arabian Peninsula its distribution extends from Yemen, Saudi Arabia through to Jordan, Syria and Iraq (Harrison and Bates, 1991; Kock and Ebenau, 1996). P. aethiopicus is highly adapted to desert and arid environment and they prefer oases and areas with vegetation where food is available.

Only few and scattered reports on the reproduction, parasites and temperature regulation on the desert hedgehog have been published recently (Yamaguchi et al., 2013; Amin et al., 2016; Amin and Heckman, 2016; Abu Baker et al., 2017; Alagaili et al., 2017; Boyles et al., 2017).

Yamaguchi et al. (2013) and Alagaili et al. (2017) studied the reproductive biology of the desert hedgehog and the latter confirmed that it is s seasonal breeder as a result of the progesterone profile in females and the size of the testes in males while the first suggested that free-ranging Ethiopian hedgehogs breed more than twice a year in Qatar based on frequency of courtship behavioural observations. Abu Baker et al. (2017) conducted a research using the GPS to study the effect of land use and sex on the home range size and movement of the Ethiopian hedgehog in Qatar.

Routine health check or screening is generally practiced in many domestic, zoo animals and wildlife in several collections. It involves haematological, biochemical and faecal investigations.

Haematological values play and important role in the determination of the health condition as well as following up any treatment or surgical procedures (Mori et al., 2004; Satue et al., 2009). Haematological profiles from other hedgehog species have been limited to Rossi et al. (2014) and Okorie-Kanu et al. (2015). The haematological and biochemical reference intervals for the European hedgehog (Erinaceus europaeus) were established by Rossi et al. (2014). Whereas, Okorie-Kanu et al. (2015) studied the haematological and biochemical profiles of the African hedgehog (Atelerix albiventris) in Nigeria.

There was no study available on the hematological and biochemical reference intervals of the Ethiopian or desert hedgehog. Therefore, the objective of the present study was to establish reference intervals for desert hedgehog following the guidelines published by the American Society of Veterinary Clinical Pathology (ASVCP). Furthermore, the effect of sex and hibernation on the haematological and biochemical variables was also investigated in the desert hedgehog.

2 Materials and methods

3 Results

There was no significant difference in the body weight (gm) between males (345 ± 90.9) and females 347 ± 101.5) in the present study (p = 0.89). Animals which were weighed before hibernation (363.14 ± 115.2) were found to be significantly heavier than animals after hibernation (331.35 ± 66.2) (p = 0.01).

3.3

3.3 Effect of hibernation on the haematological and biochemical variables

The weight of the animals after hibernation was lower (331 ± 25) than what they were before hibernation (363 ± 16), however, the differences in weight was not significant (p = 0.3140) (Fig. 1). There was a noticeable increase in most of the haematological values in animals which were sampled post hibernation (Table 5). However, the increase in the values of the RBCs, HB, HCT and MCHC collected from animals post hibernation was significant (p < 0.05). On the other hand, there was a decrease in most biochemical variable investigated in the animals post hibernation. There was a significant decrease (p < 0.05) in the TP and P in animals post hibernation unlike most other biochemical variables (Table 6).

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Fig. 1

Body weight in grams of hedgehogs (Mean ± s.e.) before and after hibernation.

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Table 5 Haematological changes in the desert hedgehog (Paraechinus aethiopicus) before and after hibernation.

Parameter	Units	Before Hibernation (n = 21)		After Hibernation (n = 17)		p value
		Mean ± SD	Range	Mean ± SD	Range
WBC	109/l	7.81 ± 2.7	3.8–12.6	7.83.3 ± 3.3	4.4–13.8	1.00
LYMPH	109/l	3.42 ± 1.9	1.1–6.7	3.43 ± 1.5	1.5–6.7	1.00
MONO	109/l	0.46 ± 0.25	0.17–0.93	0.39 ± 0.19	0.24–0.87	0.47
GRANULO	109/l	3.98 ± 2.0	2.2–8.9	3.56 ± 1.7	1.7–6.9	0.62
LYMPH	%	42.87 ± 16.6	16.6–69.6	48.7 ± 10.9	31.4–66.6	0.319
MONO	%	5.31 ± 2.3	2.0–9.2	4.8 ± 2.0	2.4–6.8	0.559
GRANULO	%	51.77 ± 15.4	26.6–75.3	46.52 ± 11.3	27.0–66.0	0.349
RBC	1012/l	5.1 ± 1.01	3.6–7.01	6.3 ± 1.06	3.5–7.9	0.002**
HGB	g/dl	10.3 ± 1.7	8.1–14.4	12.4 ± 1.4	10.7–14.8	0.0008***
HCT	%	30.6 ± 4.6	24.3–43.5	37.7 ± 5.6	23.6–45.6	0.0003***
MCV	fl	59.8 ± 4.6	54.0–67.0	61.1 ± 5.3	52.0–68.0	0.475
MCH	pg	20.4 ± 2.9	17.3–30.0	19.5 ± 31.7	16.8–21.5	0.065
MCHC	g/dl	33.0 ± 1.4	30.7–35.6	31.9 ± 1.2	30.1–34.6	0.034*
RDWc	%	20.5 ± 2.1	16.5–25.3	19.8 ± 1.3	17.5–27.2	0.238
PLT	109/l	63.3 ± 83.9	11.0–361.0	107.2 ± 105.8	38.0–452	0.247
PCT	%	0.05 ± 0.1	0.01–0.48	0.15 ± 0.07	0.04–0.28	0.357
MPV	fl	9.1 ± 3.5	0.3–13.5	10.8 ± 3.9	6.1–13.4	0.618
PDWc	%	37.9 ± 3.9	30.2–44.7	34.8 ± 10.7	9.2–44.2	0.952

* Significant difference and the level of significance < 0.05, ^** p < 0.01, ^*** p < 0.001.

Table 6 Biochemical changes in the desert hedgehog (Paraechinus aethiopicus) before and after hibernation.

Parameter	Units	Before Hibernation (n = 18)		After Hibernation (n = 19)		p value
		Mean ± SD	Range	Mean ± SD	Range
ALB	g/L	19.1 ± 4.5	10–26	18.3 ± 3.4	10–25	0.537
GLOB	g/L	52.8 ± 8.1	39–66	47.7 ± 5.9	40–64	0.051
TP	g/L	71.9 ± 8.7	57–86	66.1 ± 6.4	56–80	0.04*
ALP	U/L	58.5 ± 12.9	34–74	50.2 ± 14.5	30–78	0.129
ALT	U/L	135.1 ± 48	70–267	116.7 ± 42.8	52–198	0.245
AMY	U/L	388.1 ± 75.9	248–549	447.6 ± 70.9	320–560	0.064
TBIL	µmol/L	0.24 ± 0.06	0.2–0.4	0.23 ± 0.05	0.2–0.3	0.594
BUN	mmol/L	13.7 ± 4.0	4.3–18.5	14.4 ± 3.4	7.0–19.9	0.522
CA	mmol/L	2.9 ± 0.39	1.8–3.5	2.7 ± 0.18	2.4–3.1	0.051
PHOS	mmol/L	2.5 ± 0.47	1.2–3.2	2.1 ± 0.23	1.7–2.4	0.0003***
CREAT	µmol/L	43.7 ± 14.1	26.5–79.6	44.2 ± 13.9	26.5–79.6	0.915
GLU	mmol/L	7.2 ± 0.95	5.3–8.9	7.15 ± 1.2	5.6–8.8	1.0
NA	mmol/L	134.8 ± 4.4	124–140	134.4 ± 2.8	128–138	0.744
K	mmol/L	5.1 ± 0.68	3.6–6.5	4.8 ± 0.56	3.9–8.0	0.162
ALB/GLOB	ratio	0.4 ± 0.2	0.21–0.67	0.39 ± 0.08	0.2–0.5	0.557
BUN/CREAT	ratio	0.33 ± 0.13	0.12–0.55	0.35 ± 0.10	0.16–0.52	0.697

* Significant difference and the level of significance < 0.05, ^*** p < 0.0005.

4 Discussion

In the present study, the reference intervals for the haematology and biochemistry variables were established for the desert hedgehog (Paraechinus aethiopicus) in Saudi Arabia. This report constitutes the first report of haematological and biochemical data on the desert hedgehogs throughout its range of distribution in Africa and Asia. The haematological as well as the biochemical variables are important for disease diagnosis and prognosis of almost all animal species. They are also useful in the follow up of treatment of any condition from which a particular animal species is suffering from (Cebuli-Kaudune et al., 2002). Comparisons were made between male and female hedgehogs collected from the same environment. The effect of hibernation on the haematology and biochemistry variables was also evaluated in the present study.

Few reports are available on the normal haematological and biochemical values of the European (Erinaceus europaeus) as well as the African (Atelerix albiventris) hedgehogs (Lewis et al., 2002; Bexton and Robinson, 2003; Rossi et al., 2014; Okorie-Kanu et al., 2015). Rossi et al. (2014) documented the reference intervals of the European hedgehog and they found out there was relatively high counts of RBCs and platelets. In the present study as well as in Okorie-Kanu et al. (2015) lower values for RBCs have been recorded unlike what has been reported by Rossi et al. (2014). The reference interval for platelets was comparable to what has been reported by Rossi et al. (2014). The increase in the RBCs and the reticulocytes in other species may suggest erythroid regeneration due to erythropoietin release or in cases of nonregenerative anaemia (Cowgill et al., 2003; Barger, 2010; Tvedten, 2010). Rossi et al. (2014) attributed to the increase in RBCs and reticulocytes counts to the age of the animals they investigated as they were mostly juvenile and such group of animals have intense erythropoiesis. They also related their finding to the possibility of splenic contractions due to animal stress and suggested that RBCs in hedgehogs are probably released to blood earlier than in other animal species, a hypothesis which requires further investigation.

In our investigation, unexpectedly, the RBCs count in the females was significantly higher than in males. The sex specific difference in RBCs count was generally attributed to the effect of androgens which is believed to stimulate erythropoiesis (Shahidi, 1973). Other investigators have reported no relationship between the gender and differences in haematologic profile in the pronghorn antelope (Antelope americana). In women with adrenal hyperplasia and Cushing’s syndrome polycythemia was reported (Shahani et al., 2009) hence, the status of the female adrenal glands of hedgehogs requires further studies to find out if there is any evidence to explain the increased RBCs count in females. The platelets count in the present study which showed high 90% upper reference limit same as what has been found by Rossi et al. (2014) can be a characteristic to this group of animal species. Similar finding was recognized earlier by Alagaili et al. (2013) in the Libyan jird (Meriones libycus) and they explained their finding as a natural feature of that particular species. The same may applies to the desert hedgehog as it lives under the same desert conditions. The MCV was in agreement with what has been reported by Rossi et al. (2014) and females showed significantly higher value compared to males. The MCV values overlap in the male and female which suggest that the difference is statistically significant but it does not have biological relevance and it may not affect the interpretation of the haematologic variables. The white blood cell count in the present study was comparable to what has been reported by Rossi et al. (2014), however, they were much lower that what has been recorded by Okorie-Kanu et al. (2015) for the African hedgehog. Monocytes were significantly higher in males compared to females in the present study. Monocytes are generally increased in cases of chronic infections. The increased monocytes in the desert hedgehogs requires further investigations.

The reference intervals for the biochemical profiles were comparable with previous reports from other species of hedgehogs (Rossi et al., 2014; Okorie-Kanu et al., 2015). However, significant increase in the female BUN values compared to males. BUN is generally utilized to evaluate the renal function in different animal species. Although no apparent clinical signs of renal impairment were noted especially if we considered the creatinine values recorded in the present study. BUN level is affected by circadian rhythm, diet, liver function, hydration and intestinal absorption (Melillo, 2007). However, the observed increase in the BUN concentrations could be due to one of these reasons which requires further investigation. The ALP levels in the desert hedgehog are far much lower than those reported from the European hedgehogs and they are slightly higher than those reported from the African hedgehog. The increased levels of ALP are always associated with liver, gallbladder or bone affections or it is age related. In the present study the ALP level in females was found to be significantly higher than in males which may have been age-related or due to intestinal isoenzyme that contributes to the total ALP activity in some animal species such as rodents in case of fasting or damage (Wada et al., 2001). This point requires further investigations in future studies.

There was a change in the animals’ body weight post hibernation being lower than before hibernation despite the period of hibernation was one month. Weight loss in hibernating animals was noticed previously in some animal species such as arctic ground squirrel and the common dormouse (Buck and Barnes, 1999; Csorba, 2003). During hibernation animals such as the borwn bear decrease metabolism and reduce renal and liver function and a rise in HB, HCT and RBCs counts were noticed (Græsli et al., 2015). In the present study hedgehogs after hibernation showed high values for haematological variables and the change was significant in the RBCs, HB, HCT and MCHC. Conversely, animals after hibernation showed lower values for most of the variables studied and the reduction in the values of the TP and P were significant. The variation in the haematological variables in the erythrocytes and their indices has been noticed in other hibernating animal species such as, echidnas and bears (Seal et al., 1967; Anderson et al., 2000). A notable observation was the increase in the MCHC in hibernating echidnas which is in agreement with Anderson et al. (2000). The high values for MCHC means higher HB concentration in an individual RBC hence, a higher oxygen-delivery capacity by circulating RBCs and this could be an adaptation for hibernating animals to maintain oxygen delivery when the blood flow is reduced during hibernation. Furthermore, RBCs in hibernating individuals are not replaced quickly and they are ageing and in a senescent state hence show increased HB content in contrast to newly formed RBCs which has low MCHC (Nikinmaa, 1990). An acceptable explanation of the increase in RBCs indices may be related the effect of the reduction in blood volume during hibernation as has been shown in the northern birch mouse (Elżbieta, 1985). Investigation of the blood volume in hibernating hedgehogs may prove this assumption. Body proteins in the European hedgehog (Erinaceus europaeus) represent a significant proportion of body mass loss, and their utilization covers 9% of the energy expenditure (Cherel et al., 1995). The reduction in the total protein in the desert hedgehogs after hibernation was likely linked to energy utilization. Loss or reduction in total protein is associated with body water because each gram of protein requires 2–4 g of intracellular water (Cahill et al., 1970).

5 Conclusion

Results from the present study provide RI for a number of haematological and biochemical variables in the hedgehogs in central Saudi Arabia, and demonstrate the importance of the effect of gender as well as the effect of hibernation on these variables. These RI constitutes a baseline data to which will give accurate indicators for healthy hedgehog. It will undoubtedly help in evaluating the health conditions of hedgehogs in central Saudi Arabia. Results indicated that hedgehogs lose weight during hibernation and also hibernation was associated with increase in the HB, HCT and RBCs count. Additional controlled studies may explain the physiology of hibernation in the desert hedgehog.