An Outbreak of Pre-parturient and Post-parturient Clinical Hypocalcemia in a Camel’s Herd in Iran

1. Introduction
Camels which are resistant species to dehydration and heat are adapted for living in arid lands and eating prickly desert resources (Lamuka et al., 2017). Nevertheless, such desert plants cannot provide all the animal’s nutritional requirements, especially in pregnant camels. Minerals, including calcium, are essential in the metabolic profile of camels (Deeba et al., 2020; Dereje et al., 2016). The population of Iranian camels is 180000, and almost all of them are raised in the traditional system and in desert areas where along with nutritional deficiencies (Mohammadpour et al., 2020), they are exposed to wild animals attack, which jeopardizes camels’ health by diseases such as rabies (Ahmed et al., 2020; Esmaeili et al., 2012). Mineral deficiency in camels is mostly visible in dry years in this country, and the breeders lack easy access to veterinary utilities. Moreover, in this system, camels rarely receive mineral-rich supplementary feeds. 
Several studies have shown a decline in the level of calcium and phosphorus as the weather gets warmer and water availability reduces (Ahmed et al., 2013; Aichouni et al., 2011; Deeba et al., 2020). In a study in 2007 in southern Darfur, the blood profile of camels was investigated in the dry season. In this research, the calcium level in the dry season was 2.03 mmol/L, while in the green season, it was 2.2 mmol/L (Amin et al., 2007). Adding 0.5%-0.6% calcium and 0.3%-0.35% phosphorus to the camel diet fulfills the animal’s requirements (Deeba et al., 2020). This paper investigated an outbreak of hypocalcemia in prepartum and parturiated Kalekuhi camels which showed different stages of clinical signs of the disease during late winter and early spring in a farm located in a desert region between Tehran and Qom provinces, Iran. To our knowledge, it is the first report of hypocalcemia occurrence in Iranian camels. 

2. Materials and Methods
Study animals
 There were 96 pregnant camels among a herd of 300 Kalekuhi camels kept between Tehran and Qom cities. A total of 25 pregnant animals showed clinical signs such as depression, muscle tremors, stiffness of the limbs, and recumbency within 7-10 days post-parturition. Two camels aborted their fetuses after 7 days of recumbency and during the disease course, and 9 ones died. 
Collection of blood
 Blood samples were collected from 16 animals with clinical signs. A volume of 10 mL of blood was poured into the heparinized tubes and then centrifuged at 1800 g for 20 minutes in the lab. Plasma was separated for the determination of calcium concentration.
Calcium and phosphorus determination
 The total concentration of plasma calcium and phosphorus was measured by spectrophotometry using a commercial kit (Pars Azmoon, Tehran, Iran) by an automated analyzer. 

3. Results
The observed clinical signs in the involved animals were teeth grinding, profound depression, muscle tremors, increased heart rate, stiffness of the limbs, ataxia, and finally, sternal recumbency, which indicated hypocalcemia in the animals. Sternal recumbency was visible within a week post-parturition. The level of calcium and phosphorus fell below the normal range in all the tested blood (Table 1). 

After the administration of calcium, magnesium, and phosphorus (Nasr Company, Iran) and improved nutritional status by adding supplements, all animals recovered except 9 camels who died of severe hypocalcemia.
Post-mortem examinations
 Necropsy findings of the 9 dead camels included enlarged yellow liver, muscle necrosis of the limbs, and distended bladder. 
Treatment protocols
As the laboratory results showed hypocalcemia and hypophosphatemia in the camels, 250 mL of Calcimaphor 40 (Nasr Company, Iran) was injected slowly into the jugular vein, followed by 250 mL subcutaneous injection in sick animals. Moreover, 250 mL of the drug was injected subcutaneously into the healthy, recently parturiated animals. The animals’ feed was enriched by adding 0.5% calcium and 0.3% phosphorus.

4. Discussion
In the present study, the clinical signs were close to milk fever disease in cattle. Moreover, the necropsy findings of the 9 dead camels included injuries such as fatty liver, which indicated negative energy balance and muscle damage due to the ischemia resulting from prolonged recumbency. Distended bladder due to the inability of the animals to urinate occurred following smooth muscle paralysis. Our laboratory results indicated that the herd suffered hypocalcemia, so we treated the animals using Calcimaphor 40, which along with calcium, provided magnesium and phosphorus. After the treatment protocols, the camels, which had shown primary stages of hypocalcemia, and even two animals in the sternal recumbency stage of the disease, gradually recovered. As our laboratory results showed in the Table, hypocalcemia is associated with hypophosphatemia, and treatment with calcium borogluconate will restore both conditions. 
In the studied herd, the pregnant camels grazed in harsh circumstances with roughage grasses such as Tamarix and Haloxylon, so as they parturiated and produced milk, blood calcium declined in levels which showed severe signs of milk fever in the animals. The calcium level depends on the type of plants, season, and soils of the area in which camels are kept. In a study in Algeria in 2013, the serum calcium and phosphorus levels in summer were 2.07 mmol/L and 1.94 mmol/L, respectively, while in winter, these levels rose to 2.47 mmol/L and 2.23 mmol/L, respectively (Ahmed et al., 2013). 
Because 25 out of 96 pregnant and parturiated camels suffered hypocalcemia in the current study and economic losses due to the death of 9 animals, paying attention to mineral deficiency in the last months of pregnancy and, recently, parturiated camels is crucial. In other words, although camel is a resistant species among ruminants, inadequate minerals and malnutrition can affect the health status and productivity of the animal, especially in a transitional period. In addition to calcium, magnesium, and phosphorus are essential in maintaining blood calcium levels in their normal range, so other minerals imbalance should be considered in cases of camels with hypocalcemia. 

Ethical Considerations

Compliance with ethical guidelines
There were no ethical considerations to be considered in this research.

Funding
This research was supported by the Research Council of the University of Tehran (Grant No.: 28786).

Authors' contributions
Methodology, data collection, and data analysis: Hossein Esmaeili and Ali Khanjari; Conceptualization and writin–original draft: Hossein Esmaeili and Mona Hamedi; All authors contributed to the article and approved the submitted version.

Conflict of interest
The authors declared no conflict of interest.

Acknowledgments
The authors acknowledge the staff of the Microbiology Laboratory of the Faculty of Veterinary Medicine, University of Tehran.

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