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Delayed growth in a young fruit bat (Pteropus pumilus) due to nutritional hypovitaminosis C
  1. C. Aitken-Palmer, DVM, PhD1,
  2. R. Isaza, DVM, MS, DiplACZM2,
  3. B. Pope3 and
  4. D. Reese, DVM, DiplACVR4
  1. Department of Small Animal Clinical Sciences, University of Florida, 2015 SW, 16th Ave, Gainesville, Florida, 32610, USA
  2. Department of Small Animal Clinical Sciences, University of Florida, 2015 SW, 16th Ave, Gainesville, Florida, 32610, USA
  3. Lubee Bat Conservancy, 1309 NW, 192nd Ave, Gainesville, Florida, 32609, USA
  4. Department of Small Animal Clinical Sciences, University of Florida, 2015 SW, 16th Ave, Gainesville, Florida, 32610, USA
  1. E-mail for correspondence copperdvm{at}gmail.com

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AN eight-week-old, male, little golden-mantled flying fox, Pteropus pumilus, presented for lethargy of one week duration. This bat pup (59 g), rejected by his mother, was hand raised using a formulated milk (Zoologic Milk Matrix Powders; PetAg). During the first seven weeks of hand rearing, the pup was active and gaining weight (0.595 g/day). On physical examination, the P pumilus pup had swelling at the right carpal and bilateral tarsal joints. Additionally, the bat pup's weight gain had slowed (0.175 g/day). Infectious causes, congenital abnormalities, and nutritional deficiencies were considered possible causes of the clinical signs and diagnostics were pursued.

Diagnostics included radiographs and a venous blood sample. Because of the small blood sample (0.5 ml), haematological evaluation was limited to a complete blood count (CBC) and limited chemistry panel (Abaxis Vetscan VS2). Elevated serum phosphorus (9.8 mg/dl, normal 4±1.6 mg/dl) with normal serum calcium (9.8 mg/dl, normal 8.4±0.8 mg/dl) was noted (International Species Information System 2002). The CBC yielded a normal total white blood cell count of 12, 080 cell/µl (normal 17,720±7117 cell/µl) and decreased hematocrit 29.6 per cent (normal 45.8±3.2 per cent) (International Species Information System 2002). Generalised decreased bone opacity and widening of the proximal radial metaphysis were seen on whole body (ventrodorsal and lateral projections) radiographs (Fig 1a, b) taken with computed radiography (Kodak DirectView CR 950; Eastman Kodak).

Fig 1

Computed radiography (CR) radiographs of juvenile Pteropus pumilus. (a) Lateral and, (b) ventrodorsal projection radiographs of Pteropus pumilus pup (eight weeks old) with nutritional hypovitaminosis C with diffuse osteopenia and soft tissue swelling of carpi and tarsi. (c) Lateral and, (d) ventrodorsal projection radiographs of the same bat pup at 14 weeks of age after supplementation of nutritional vitamin C. Radiographs indicate resolved osteopenia, normal carpi and normal tarsi compared with projections (a) and (b)

Differential diagnoses causing observed radiographic changes included metabolic, nutritional or endocrine aetiologies. Although the hematocrit was low, there was no evidence of systemic infection in the CBC results supporting a diagnosis of nutritional deficiency. Specifically, deficiencies of ascorbic acid, calcium and vitamin D were considered. Vitamin D was considered less likely because as a dim light/nocturnal species (Shen and others 2010), P pumilus have been documented to have low vitamin D requirements (Cavaleros and others 2003). The ingredients of formulated milk used were reviewed (www.petag.com/PDFs/Product%20Information.pdf) and found adequate in calcium (10 mg/1 gram milk powder), but lacking ascorbic acid supplementation.

Although there are no studies on the nutritional need of ascorbic acid in P pumilus, nutritional vitamin C is required for some bat species (Roy and Guha 1958, Birney and others 1976). Because of this, hypovitaminosis C was suspected as the cause of the clinical signs seen in this P pumilus juvenile. Treatment was initiated with 1.5 mg of vitamin C (50 mg/ml) subcutaneously, followed by 1 mg vitamin C daily given orally. Within three days of treatment, the bat pup had improved ambulation. After seven days, the joint swelling resolved and the pup begun rapidly gaining weight (1.78 g/day).

At 11 weeks of age, repeat physical examination and radiographic evaluation indicated unchanged diffuse osteopenia, but the previous proximal radial metaphyseal widening was improving. At 14 weeks of age, the bat pup was consistently gaining weight (1.78 g/day) and appeared to be thriving. Recheck radiographs (Fig 1c, d) showed a generalised increase in the mineral opacity of the axial and appendicular skeleton (Fig 1c, d) indicating resolved osteopenia. All of the cuboidal bones and phalanges were more easily distinguished and the proximal radial metaphysis were considered normal (Fig 1c, d). The bat continued on supplemental ascorbic acid until 16 weeks of age when it began eating citrus fruits and no longer consumed exclusively milk formula. The bat pup continued to mature to a healthy adult P pumilus.

There is no previous documentation that P pumilus require nutritional ascorbic acid, but the quick clinical response to parenteral and nutritional supplementation of ascorbic acid in this hand raised bat suggests nutritional vitamin C is essential for this species. P pumilus, a fruit and nectar eating bat, is classified within the suborder Megachiroptera (Shen and others 2010). Ascorbic acid has been reported as a required nutritional supplement in only one species of Megachiroptera (P giganteus), but is a nutritional requirement for numerous species of bat in the suborder Microchiroptera (Roy and Guha 1958, Birney and others 1976). These specific bat species, like guinea pigs and primates, lack L-gulono oxidase and D-glucourono reductase enzymes preventing the de novo synthesis of L-ascorbic acid making them dependent on a nutritional source of ascorbic acid (Chatterjee and others 1961, Birney and others 1976).

Deficiency in ascorbic acid, hypovitaminosis C or scurvy, as described in human beings and guinea pigs results in decreased collagen synthesis, abnormalities in connective tissues (Kipp and others 1996, Dolberg and others 2010), and abnormal osteoblast and osteoclast function (Carinci and others 2005). These animals, when lacking a nutritional source of vitamin C can develop nondescript clinical signs such as lethargy (Dolberg and others 2010), anaemia (Dolberg and others 2010), joint swelling (Fain 2005), slowed growth (Schwager and Schulze 1998), osteopenia (Kipp and others 1996) and weight loss (Fain 2005, Dolberg and others 2010). Radiographic joint widening at the radial metaphysis is a hallmark seen in juvenile macaques with nutritional hypovitaminosis C (Morgan and Eisele 1992). Interestingly, the same radiographic abnormality was seen in radiographs of this P pumilus pup. This similarity provides additional support for the diagnosis of hypovitaminosis C.

It seems unexpected that the clinical signs of scurvy in this bat pup developed at eight weeks of age since this bat pup received formulated milk without supplemented ascorbic acid from birth. Although speculation, it is possible that the delay in clinical signs is associated with maternal transfer of ascorbic acid to the neonate during gestation, that then depleted over the eight weeks of hand rearing. Although this is unknown for bat species, maternal transfer of ascorbic acid is known to occur in human beings via the umbilical cord (Wang and others 2009). Perhaps similar transfer occurs in the P pumilus, but there are no studies to indicate how ascorbic acid is transferred vertically between any bat species.

Although, only one species of bat within the suborder Megachiroptera is known to require nutritional vitamin C (Roy and Guha 1958, Birney and others 1976), it is possible that all species within this suborder rely on a nutritional source of vitamin C. Additionally, until the role of ascorbic acid is better understood in the neonatal bat, nutritional supplementation of vitamin C should always be included in the milk formula for hand reared P pumilus.

  • Accepted September 12, 2011.

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Footnotes

  • Provenance not commissioned; externally peer reviewed

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