Printer Friendly

Determination of a safe and effective ultraviolet B radiant dose in budgerigars (Melopsittacus undulatus): a pilot study.

Abstract: The object of this study was to establish a minimum dose of ultraviolet B (UVB) radiation capable of producing an erythemal reaction in budgerigars (Melopsittacus undulatus), to determine a threshold dose of UVB for vitamin D photoconversion, and to investigate the use of safer UVB wavelengths. In each of 5 experiments of this study, 20 birds were divided into a control group (n = 10) and a UVB irradiated group (n = 10). Light sources that provide broadband UVB wavelengths (280-315 nm) and narrowband UVB (310-320 nm) were used. Varied doses of UVB radiation were administered to budgerigars by altering exposure time and irradiance. Safety was determined by observing body weight and incidence of photokeratitis and photodermatitis. Efficacy was evaluated by measuring changes in serum 25-hydroxycholecalciferol levels. Serum corticosterone was measured in 1 experiment to monitor stress levels. The results demonstrated that exposure to 180 mJ/[cm.sup.2] broadband UVB induced vitamin D photoconversion, decreased body weights, and increased serum corticosterone levels. At these wavelengths, UVB-induced lesions were observed. A broadband UVB of 150 to 300 mJ/[cm.sup.2] was determined as the minimum erythema dose, and the threshold dose for vitamin D photoconversion was calculated to be in the range of 113-225 mJ/[cm.sup.2]. No erythemal lesions or vitamin D photoconversion took place after exposure to up to 1730 mJ/[cm.sup.2] narrowband UVB radiation. A minimum erythema dose and a threshold dose for vitamin D conversion need to be determined for each species if phototherapy is to be considered as a safe and effective therapeutic or husbandry tool.

Key words: minimum erythema dose, MED, ultraviolet B, UVB, irradiance, 25-hydroxycholecalciferol; 25-OH-D, photoconversion, vitamin D, avian, budgerigar, Melopsittacus undulatus

Introduction

Ultraviolet radiation (UVR) is frequently discussed as a supplemental light source for avian species. (1,2) UVR contributes to the general well being of exposed individuals and is active in vitamin D photoconversion. Indeed, physical activity increases significantly in birds kept under full-spectrum fluorescent lighting; hens under UV light preen more than hens under incandescent light, and the feathers in certain species may have UV reflectance, which enables inter- and intraspecies recognition. (3,4) In addition, plasma corticosterone concentrations were significantly higher in starlings (Sturnus vulgaris) deprived of UVR than in those exposed to UVR. (5) Recommendations for the use of UVR-emitting lamps vary and appear arbitrary. Insufficient information appears on the packaging of most of these lamps. Furthermore, no safe and effective UVR dose in birds has been determined. Therefore, at present, safe recommendations on the use of any UVR-containing lamps are unknown.

The main impetus for using UVR is its role in vitamin [D.sub.3] photosynthesis. Vitamin [D.sub.3] is essential for normal growth, calcium absorption, egg development, and the maintenance of a healthy immune system. (6,7) Vitamin [D.sub.3] deficiency in companion birds results in hypocalcemia and consequent egg-related disorders, pathologic fractures, and seizures, which are common in cockatiels (Nymphicus hollandicus), budgerigars (Melopsittacus undulatus), and African grey parrots (Psittacus erithacus). (8)

Vitamin [D.sub.3] is scarce in the food supply and even more so in that of birds fed a seed-based diet. Animal products constitute the bulk source of vitamin [D.sub.3] that occurs naturally in unfortified foods such as fish and eggs. Plants, fruits, and nuts, which are staples in many avian diets, are extremely poor sources of vitamin [D.sub.3]. Vitamin [D.sub.3] precursors are present in uropygial gland secretions. These secretions, distributed on the feathers through preening, are photoconverted under UVB exposure to the active form of vitamin [D.sub.3] and then ingested. (9) However, the nutritional importance of uropygial-derived vitamin [D.sub.3] has been questioned because ablation of the gland showed no effect over a 2-month period on several physiological parameters, including calcium metabolism, in pigeons (Columba livia). (10)

Enrichment of diets is customary. However, vitamin [D.sub.3] requirements for all species and all ages are not known, and excessive supplementation in commercial diets can occur. (11) Vitamin [D.sub.3] toxicosis manifests as hypercalcemia: excess bone deposition, mineralization of soft tissues, and nephrocalcinosis, which can result in kidney failure and death. (12,13) The consequence of long-term vitamin D supplementation in humans, and in most species, is unknown. (14) Conversely, vitamin D toxicosis cannot occur with UVR-stimulated photosynthesis because of the buildup of a reversible pool of inert metabolites in cutaneous tissues. (15)

Exposure to UVR results in the photochemical conversion of cutaneous 7-dehydrocholesterol to previtamin [D.sub.3]. In a temperature-dependent isomerization, previtamin [D.sub.3] is transformed into vitamin [D.sub.3] (cholecalciferol). Fifty percent of this conversion occurs within 28 hours, and 80% is complete in 4 days. (16) Only cholecalciferol is released into blood circulation. (17) Cholecalciferol is further hydroxylated by liver enzymes into 25-hydroxycholecalciferol (25-OH-D) and then by the kidney into the biologically active form of vitamin [D.sub.3], 1,25 (OH) cholecalciferol (1,25-OH-D). Of these 3 metabolites, serum concentration of 25-OH-D is most valuable for determining the overall vitamin D status of an individual because it is an average of dietary and sunlight-induced vitamin [D.sub.3]. (18)

UV light

UV light is situated immediately below the visible portion of the electromagnetic field. It is divided into 3 categories: UVA (315-400 nm), UVB (280-315 nm), and UVC (100-280 nm). UV B is further divided into erythemal (280-300 nm) and nonerythemal (300-315 nm) wavelengths. The greatest tissue and DNA damage occurs at the shortest wavelengths. Photokeratoconjunctivitis has been reported in reptiles exposed to short-wavelength UVB. (19) Photokeratitis and photodermatitis have been reported in an African grey parrot and a Meyer's parrot (Poicephalus meyeri) exposed to high levels of short wavelength UVB. (20) Photoadaptive cutaneous hyperplasia, which impedes the penetration of UVB radiation, occurs with repeated exposure. In humans and mice, these photoadaptations disappear within 3-4 weeks after exposure. (21)

UVR produces electromagnetic radiant energy, which is measured in watts (W). The amount of radiation that falls on a unit of surface area is called irradiance (mW/[cm.sup.2]). The UVR dose is the irradiance (mW) times the exposure time in seconds. This dose is expressed in joules per unit area (mJ/[cm.sup.2]). (22) Therefore, a dose can be altered by increasing or decreasing exposure time or irradiance levels. The minimum radiant dose required to produce an effect is called the threshold dose. The minimum erythema dose (MED) is the minimum input of UVR necessary to produce an erythemal reaction per square unit of surface area of skin after 24 hours of exposure. In humans, exposure to 0.75 MED 3 times a week is very effective in raising blood levels of 25-OH-D. (23) One MED in humans ranges from 10 to 35 mJ/[cm.sup.2]. (24) No determined MED exists for avian species.

Anything that influences the number of photons that strikes the skin affects the synthesis of previtamin [D.sub.3]. Melanin absorbs UVB photons at 290-320 nm and thus controls the amount of UV that can penetrate the skin. (25,26) Feather covering in birds effectively blocks UVR. The amount of cholesterol under skin will also influence the degree of conversion. (27) Species variation, therefore, would be expected. In a study of the effects of UVB radiation on serum calcium and 25-OH-D levels, African grey parrots showed an increase in serum levels when exposed to UVR, whereas Pionus parrots (Pionus species) did not. (28)

Two criteria used to qualify lighting are lux and color rendition index. The color rendition index is an index, on a scale of 1-100, that describes how natural an object will appear under the light source but is not indicative of the lamp's UVR content. The intensity of the light perceived by the eye is referred to as lux. This measurement represents the total amount of visible light present per area. This also does not reflect UVR content. A variety of lamps can provide UVB. Full spectrum fluorescent lamps attempt to parallel the spectral distribution of the sun, which combines visible and longer UV wavelengths. The UV output of these lamps is mostly composed of UVA radiation and little UVB. Fluorescent full-spectrum bulbs (VitaLite, Duro-Corporation, North Bergen, NJ, USA), in which 5% of output is at wavelengths between 290 and 380 nm, had no positive effects on the plasma levels of 25-OH-D for hospital patients exposed to the lights at normal illumination levels. (16)

A variety of bulbs available in the pet trade also provide UVR. In a comparative study, although some bulbs demonstrated a higher capacity for in vitro previtamin D conversion, no one lamp proved to be superior to another. (29) Corn snakes (Pantherophis guttatus) exposed to light from 2 full-spectrum coil bulbs (Sun-Glow, Fluker Farms, Port Allan, LA, USA), at a distance of 15.8 cm above the basking area for 12 hours daily for 4 weeks, experienced significant increases in serum 25-OH-D levels. (30) In a similar study, red-eared sliders (Trachemys scripta elegans) exposed to light from identical bulbs, 12 hours daily for 6 weeks, also showed increased serum 25-OH-D levels. (31) Specific wavelength information supplied with UVB lamps is often scant. Most do contain erythemal UVB radiation and, hence, although effective, are potentially dangerous for animals and humans. (19) Finally, specialty UVB-emitting fluorescent tubes, which emit broadband UVB (280-320 nm) or narrowband UVB (310-315 nm), are available for use in humans. Narrowband UVB effectively increased serum 25-OH-D levels in humans who were vitamin D insufficient. (32) The mean narrowband MED in humans ranged between 150 and 400 mJ/[cm.sup.2]. (31) Ratios of broadband to narrowband UVB have been reported as being 1:10 (33) to 1:15. (34)

UVB irradiance is a function of the type of lamp and also the distance from the light source. Irradiance diminishes with distance from the lamp: one-third of the UV energy is lost at 30 cm from the light source and only one-fifteenth remains at 75 cm below the lamp, (35) which requires lamps to be placed in close proximity to the birds to be effective. At these distances, the intensity of the light can produce ocular discomfort and physiological stress. In a preliminary study (Lupu et al, unpublished data, June 2007), budgerigars illuminated by 4 full-spectrum fluorescent bulbs (Vitalite F40T12, Duro-Corporation) for 12 hours daily at a 75-cm distance displayed photophobia and stress-related disease, while experiencing no significant increase in 25-OH-D after 11 weeks.

Overall, the UVB bandwidth necessary for vitamin D3 photoconversion in animals is 290-315 rim. (36) Photoconversion of cutaneous cholesterol (7-dehydrocholesterol) to previtamin [D.sub.3] has been shown to be maximized at wavelengths of 295 [+ or -] 2 nm in humans, both in vivo and in vitro. (16) Cutaneous cholesterol absorbs UVR most efficiently over the wavelengths of 270-290 nm. In vitro solutions of 7-dehydrocholesterol showed no photoconversion activity when irradiated at wavelengths of 313 nm or longer. (37) A total UVB dose of 500 mJ/[cm.sup.2] applied to the skin of chicken legs produced a 4-fold increase in circulating vitamin [D.sub.3] levels, which peaked at 30 hours after radiation. (17)

The cornea absorbs UVB with a peak at 270 nm. The threshold dose for corneal damage in mammals for 300 nm has been reported to be 30-80 mJ/ [cm.sup.2]. (22) In the above-mentioned preliminary study in budgerigars, no corneal damage was observed at an irradiation dose of 24 mJ/[cm.sup.2] (based on manufacturer-provided irradiance information) (C. L., unpublished data, June 2007). In another preliminary investigation that used single fluorescent UVB-emitting tubes (Exo Terra Repti Glo 8.0, Rolf C. Hagen [UK] Ltd, West Yorkshire, UK) that emitted an irradiance of 0.017 mW/[cm.sup.2] during 4 hours, results showed that a total dose of 245 mJ/[cm.sup.2] was safe and effective in preserving bone strength in 1- to 14-day-old chicks (R. H. Fleming, Roslin Institute and R(D)SVS, University of Edinburgh, written communication, July 2009). In a further investigation by using self-ballasted compact UVB reptile lamps (ZooMed ReptiSun 10.0 UVB, Desert lamps; ZooMed Laboratories Inc, San Luis Obispo, CA, USA; energy efficient [26W] with 10% UVB output) placed 1.4 m from and delivering 0.0085 mW/[cm.sup.2] at floor level for 12 hours, a total dose of 367 mJ/[cm.sup.2] was safe and effective in increasing bone density, as measured by breaking strength, in 1- to 14-day-old chicks. (38)

The purpose of this pilot study was to determine whether previtamin [D.sub.3] photoconversion can occur at nonerythemal UVR wavelengths and to investigate a safe and effective dose of administration of UVB in budgerigars. Two light sources were used: a broadband UVB lamp and a narrowband UVB lamp. Because exposure to UVR lowers plasma corticosterone concentrations in starlings, (5) we hypothesized that plasma corticosterone levels might also decrease in budgerigars exposed to UVR in our study. Therefore, the remaining serum samples from one experiment were used to measure corticosterone levels in budgerigars after UVR exposure.

Materials and Methods

Lamps

Either broadband (280-315 nm) or narrowband (310-320 nm) UVB fluorescent tubes were used as the irradiation source (Fig 1). In experiments 1 (BB1), 2 (BB2), and 3 (BB3), the light source consisted of a combination of one 4-foot "broadband'" Philips 40W Ultraviolet-B TL40W/12RS bulb (UVB 280-350 nm) (Philips International B.V., Amsterdam, The Netherlands), coupled with one Phillips F34T12/CW/RS/EW Alto H8 standard fluorescent tube. Two 4-foot "narrowband" Philips TL40W/01RS UVB fluorescent bulbs were used in experiments 4 (NB1) and 5 (NB2). Fluorescent bulbs were mounted on fixtures equipped with electronic ballasts (7 Workhorse 7, Fulham Co Inc, Hawthorne, CA, USA).

Meters

Irradiance was measured by using photometers. Different meters can result in different output measurements when exposed to the same levels of sunlight. (39) Irradiance levels presented in this study were obtained with a Daavlin X96 irradiance meter, P9710 optometer (accuracy, [+ or -] 5%). The diode was recalibrated to adjust for the change in UVB bandwidth. Parallel readings were taken for comparative purposes by using a Solartech 6.2 radiometer (accuracy, [+ or -] 10%) (Solartech Inc, Harrison Township, MI, USA) (Table 1). A Traceable Dual-Display light meter (Fisher Science Education, Pittsburgh, PA, USA) was used to measure light intensity that surrounded the cages (lux).

Methods

Experimental design: Five separate and successive experiments on the same 20 birds were conducted in this study by using a complete randomized design each time. In each experiment, the birds were randomized to either a control or a treatment group as outlined below. The randomization process was repeated for each study. The birds were randomized to groups by using 10 treatment and 10 control labeled cue cards sampled blindly without replacement. In humans, 25-OH-D has a half-life of approximately 2-3 weeks. (40) In breeding hens, the half-life of 25-OH vitamin [D.sub.3] approaches 21 days. (41) Hence, the interval chosen between experiments was a minimum of 4 weeks to allow 25-OH-D concentrations to subside.

Randomization: In each experiment of the study, the birds were divided by simple randomization into the control or the test group as follows: 10 cue cards were labeled with the word "experiment" and 10 with the word "control." The cards were shuffled and turned face down. Each bird was removed from the main cage, and one by one the first card on the pile was turned over. The bird was then allocated to the group written on the card. This card was then removed from circulation. Each successive bird was matched to the next card in the pile until all birds were assigned.

Animals: This study conformed with the regulations established by The Canadian Council of Animal Care. (42) Twenty adult male budgerigars of unknown and varied ages were collected from a pet distribution facility (mean weight for all birds was 41.97 g). All the birds received physical examinations and appeared healthy at the time of purchase. Complete blood cell counts, fecal examinations, and survey radiographs were performed on each bird, and all the results were within reference ranges. (43) The birds were provided with a seed diet with no supplemental vitamins or minerals. Adequate food dishes were provided to ensure easy access. The birds were allowed to acclimate to the facility for 1 month before the study began. Diets and management were maintained during the intervals between experiments.

For each experiment, the birds were randomly assigned to 2 groups of 10 birds. They were housed in wire cages (5 birds per cage), each measuring 53 x 46 x 71 cm. Perches were placed 15 cm from the roof of the cage. Ambient room lighting consisted of a fluorescent fixture that contained 1 standard 8-foot fluorescent bulb, in use for 1 year. The cages were placed side by side in an area protected from direct ceiling light. In each experiment, one group (2 cages) was removed to the irradiation room for the duration, while the control group (2 cages) remained in the holding room. The amount of lux (250 [+ or -] 20) was controlled for by providing an incandescent light source to the control cages. Birds in both control and irradiated groups were weighed and examined daily for changes in behavior, photophobia, epiphora, pruritus, or erythema on eyelids or feet. Ocular fluorescein stains were performed as needed to verify the presence of corneal lesions. The UV irradiation was administered in a remote room. Photometer readings were taken at perch level by personnel wearing protective glasses and long sleeves on a daily basis after the lights had warmed for 30 minutes.

The fixtures were secured to the ceiling above the cages so that lamps were 1.83 m from perch level in experiments BB1, BB2, and BB3. The perch to light source distance was reduced to 1.14 m and 0.7 m in experiments NB1 and NB2, respectively, to increase the radiant dose. A plastic meshed fabric was used to shield the lamps in experiment BB2 and BB3 to reduce irradiance levels. Both incandescent and UV lights were turned on daily for 2 days in experiment BB1, then for 5 days in each of the remaining experiments. Average UVB irradiance measured at perch level, average irradiation time, and total daily dose are presented in Table 1. Average UVB irradiance measured in the control group through all experiments was negligible (0.00009 mW/[cm.sup.2]).

Sample collection and storage

25-OH-vitamin D: A total volume of no more than 0.15 mL whole blood was collected from each bird by jugular venipuncture. Samples were placed in nonanticoagulated serum separator tubes (BD Microtainer, Franklin Lakes, NJ, USA) and allowed to clot for 30 minutes in the dark at room temperature. Samples were then centrifuged for 30 seconds at 12 000g (15 800 rpm). Serum drawn off was placed in opaque 1.5-mL microcentrifuge tubes (Sarstedt Inc, Montreal, Quebec, Canada). Samples were then stored at -20[degrees]C until analysis. The samples were analyzed in duplicate for 25-OH-D content by using a 25-OH-vitamin D commercially available enzyme-linked immunosorbent assay kit (OCTEIA AC-57Fl, IDS Ltd, Tyne and Wear, UK).

Corticosterone: Serum corticosterone was assayed by using the remaining serum samples obtained from birds in experiment BB3. Because of the small sample volume, 60 [micro]L of serum collected from each of 2 birds was combined in a common microcentrifuge tube to obtain 5 tubes per group with a minimum total volume per tube of 120 [micro]L. Each tube was then vortexed for 10 seconds, spun down, and assayed in duplicate. All the samples fell within the linear range of the standard curve and were included in the statistical analysis. Corticosterone was analyzed by using a commercially available kit (Cat. no. 500651; Cayman Chemical Company, Ann Arbor, MI, USA). Serum was stored at -80[degrees]C until assayed. The developed plate was read at 405 nm in a Tecan Infinite M1000 plate reader (Tecan USA Inc, Morrisville, NC, USA).

Statistical analysis

Results were analyzed by using Prism GraphPad Software version 5.0 (GraphPad Software Inc, San Jose, CA, USA). Serum 25-OH vitamin D, corticosterone, and body weights were analyzed before and after exposure to UVB light for the treatment and the control group. For all experiments of the study, the change in individual values between baseline and after exposure was compared between groups. The results were not found to be normally distributed when using a Shapiro-Wilk test. Therefore, in each experiment, the median of numerical differences in parameters between baseline and after exposure were compared between the control and treatment groups by using a Mann-Whitney U test. An alpha value of .05 was used for significance.

Results

The birds remained in good general health, and no complications that resulted from manipulations and venipuncture were noted, with the exception of one bird that died from blood loss after the second venipuncture of experiment BB3 (irradiated group). Four birds were eventually dropped from the study, one after experiment BB3 (control group) and 3 after experiment NB1 (one from the treatment and two from the control groups) because they were not considered fit to remain in the study. These birds were not replaced. Because equal numbers of birds were lost from control and treatment groups, no causal inference to UVB radiation could be made.

Blepharospasm, swollen eyelids, pruritus, photokeratitis, and photodermatitis of feet and eyelids were observed in all UVB irradiated birds at the outset of day 3 of experiment BB1, at which point this experiment was stopped. Mild bilateral erythema of the eyelids and swelling was observed in all treatment birds, but the swelling did not cause eye closure. Pruritus was also present but no self-trauma occurred. Ocular fluorescein stain infusion revealed distinctive half moon lesions on the upper half of the corneas in all the birds. The skin on ventral tarsometatarsal area of the legs became pink in 8 of 10 birds, and erythema was more pronounced in lutino (n = 2) and pale blue birds (n = 3); no blistering or scabbing occurred. Through this, the birds remained active and vocal, and their appetite and weights were unaffected. Eye and skin lesions resolved completely within 3 days without treatment. Results from all experiments are detailed in Table 2. There was no significant increase in serum 25-OH-D during this experiment (P = .22).

By lowering irradiance levels in experiment BB2, the UVB radiant dose was decreased. No significant increase in serum 25-OH-D occurred (P = .74). No UV-induced lesions were observed in any of the birds. UVB radiant dose was increased in experiment BB3 by lengthening exposure time. A significant increase in serum 25-OH-D levels occurred between day 0 and day 5 (P = .04). On days 4 and 5, erythema was observed on the eyelids and feet in 3 of the 10 birds exposed to UVR. Transient (1 day) photokeratitis was observed in only one eye of one bird on day 5: ocular fluorescein stain was retained on a thin crescent-shaped area on the upper third of the cornea. In experiments NB1 and NB2, the birds were irradiated with increasing doses of narrowband UVB radiation. No significant increase in serum 25-OH-D was observed in NB1 (P = .60) or NB2 (P = .23). No UVB radiation-induced lesions were observed.

Additional results

Serum corticosterone was measured in one experiment of this study (BB3) to obtain preliminary data for a future study. Serum corticosterone concentrations increased significantly in the irradiated group compared with the control group of experiment BB3 (P = .008) (Fig 2). Variations in body weights were also analyzed in experiment BB3. There was a significant decrease in the body weights in the irradiated birds compared with the control group in experiment BB3 (P = .03) (Fig 3).

Discussion

Exposing birds (and reptiles) to UVB light sources is frequently recommended to substitute for the beneficial rays of natural sunlight unavailable to animals housed indoors. Many of these light sources, which are readily available in the pet trade, contain hazardous short wavelengths of UVB radiation. Photokeratitis and photodermatitis result from excess exposure. But what is safe or excess exposure? Recommendations not based on data on how to use these lamps, therefore, are arbitrary. Because of the hazardous nature of UVB exposure, it is imperative that discourse about the use of these lamps includes the notion of "dosage."

This study explores 3 essential topics for using UVB with the object of contributing to safer use of UVB-containing lamps. First is to establish a minimum dose capable of producing an erythemal reaction (and corneal damage). Second is to determine the dose required for vitamin D photo-conversion, one of the primary reasons for using these lamps, and, finally, to investigate whether this can be accomplished by using safer UVB wavelengths. For this study, budgerigars were our bird of choice because of their size and ease with which to work, and also because they represent a large percentage of companion birds. Calcium- and vitamin [D.sub.3]-related pathologies occur frequently in reproductively active females of this species, and, therefore, the importance of vitamin [D.sub.3] may be considerable. Notwithstanding, male birds were chosen to avoid potential variations in data associated with the physiological state of female birds.

The timeline in this study took into consideration the small size of the birds. The minimum venous healing times between samplings was determined to be 5 days. Additional samples were not taken given that translocation of vitamin [D.sub.3] is 80% complete within 4 days, and, therefore, a maximal increase in serum 25-OH-D was expected to have occurred after 5 days of UVB exposure.

Determining a safe initial dose in this study was made by reviewing the literature. Results of experiment one of this study (BB1) clearly demonstrated the importance of determining a safe radiant dose. Indeed, irradiation with broadband UVB at a dose of 150 mJ/[cm.sup.2] caused serious dermal and corneal damage after only 2 days. No lesions were observed in birds exposed to half of that dose, that is, 60 mJ/[cm.sup.2] (BB2). However, a dose of 180 mJ/[cm.sup.2] (BB3), the product of a longer exposure to less than half the irradiance compared with BB1, resulted, in a few birds, in only mild signs of photodermatitis and photokeratitis after 4 days. Photoadaptive reactions may have occurred, such as an increase in the stratum corneum of the skin, thereby decreasing UVB penetration, despite the lag time of 12 weeks between these experiments. To control for this, future studies should include a crossover design balanced for carryover effects with each bird that received all treatments in a randomized sequence. This result also may be due to the 5% variation in accuracy of the photometer, especially at low radiant levels. Differences of 20-30 mJ/[cm.sup.2] can make a large difference in erythemal effects.

The MED is calculated based on a 24-hour period; in our subjects, erythemal signs occurred after 24-48 hours. When considering this, we can infer that the minimum dose (MED) of broadband UVB capable of causing photokeratitis and photodermatitis in budgerigars ranges between 150 and 300 mJ/[cm.sup.2], which is 10 times the MED for humans. Exposure to narrowband UVB radiation at a dose of 1730 mJ/[cm.sup.2] did not produce any erythemal or corneal lesions, which leads us to conclude that the MED for exposure to narrowband UVB is more than 1730 mJ/[cm.sup.2]. Given the ratio of 1:10 to 1:15 BB :NB UVB, we can expect the MED for narrowband UVB to be in the range of greater than 1730 mJ/[cm.sup.2] and up to 4500 mJ/[cm.sup.2].

In humans, exposure to 0.75 MED 3 times a week consistently resulted in vitamin D photoconversion. If this holds true in budgerigars, then, based on our calculated MED, photoconversion should occur with a dose of 113-225 mJ/[cm.sup.2] of broadband UVB. Our results showed a significant increase in serum 25-OH-D of budgerigars exposed to a dose of broadband UVB radiation equal to 180 mJ/[cm.sup.2], administered for 6 hours daily for 5 days (BB3). This dose is within our calculated threshold dose range. That there was no significant increase in serum 25-OH-D in birds exposed to a dose of 150 mJ/[cm.sup.2] over 2 days (BB1) is consistent with the findings that 80% vitamin [D.sub.3] conversion occurs after 4 days. Birds exposed to a dose of broadband UVB of 60 mJ/[cm.sup.2] (20%-40% MED) did not experience a significant increase of 25-OHD (BB2).

Although vitamin [D.sub.3] photoconversion has been shown to occur in humans after exposure to narrowband UVB radiation, this was not found to be true in our birds. Serum 25-OH-D did not increase after exposure to narrowband UVB radiation administered at a dose of 1730 mJ/[cm.sup.2]. That this did not occur may be due to photosensitization but more likely to an insufficient dose. Given the estimated MED for narrowband UVB exposure, the threshold dose should be in the range of >1730 to 3375 mJ/[cm.sup.2].

Serum corticosterone was evaluated in only one experiment (BB3) to obtain preliminary data. The increase in serum corticosterone and decrease in weight observed in the broadband UVB-irradiated birds in this study indicates that stress levels must be considered when administering UVB lighting. Corticosterone levels may have increased because of the mild cutaneous erythema. Another possibility is that broadband UVB lamps contain energy that is invisible to the human eye but may be very bright to birds given the UV sensitivity of their retina cells peaking at 370 nm. This argues for future research into the use of narrowband lights, with peak wavelengths at 311 nm, well below the 370-nm range visible to the avian eye. In addition, a filter could be placed over the UVB light source to block UV rays above 320 nm.

In conclusion, a stand-alone dose for UVB exposure conveys no information on the erythemal nature of the wavelength or the irradiance and, therefore, on safety or efficacy. The packaging of many lamps commonly available in the pet trade offers little information regarding UVB wavelength or irradiance. Although several of these lamps come with recommendations for use, in the absence of specific information, these recommendations remain unverifiable. We tested one such broadband UVB bulb for which the package insert advised use for 10 to 12 hours daily at close range. At 36 cm, the farthest animal to the light-source distance recommended on the package, irradiance measured by using the Daavlin X96 radiometer was 0.018 mW/[cm.sup.2]. After the recommended 12-hour exposure, the total dose received by the animal would be 780 mJ/[cm.sup.2], far beyond the 150 mJ/[cm.sup.2] dose, which caused lesions in the budgerigars in experiment BB1.

Species variations exist. In humans, skin color, exposed area, and cholesterol content influence the degree of vitamin D photoconversion. We can assume that the same is true in birds: in some species, more skin is exposed; in others, the skin may be more pigmented. In dark-skinned individuals, vitamin D photosynthesis is less effective than in light-skinned individuals, and, in dark-skinned women, when vitamin D serum levels fall below threshold, serum parathyroid hormone increases. (26) Similarly, in avian species in which photoconversion is less effective, vitamin [D.sub.3] may be the limiting factor that governs the incidence of pathologic fractures and egg-related pathologies. The use of UVB could be an effective therapeutic tool. Our results established a preliminary MED and threshold dose for vitamin D photosynthesis in budgerigars.

Further investigation is required to determine MED and threshold doses in other species, ensuring safe and effective use of UVB radiation. These studies may also be helpful in establishing reference ranges for 25-OH-D in avian species, which, in turn, may result in species-specific nutritional recommendations. Finally, as it is now for humans, phototherapy may become a useful veterinary tool in the treatment of vitamin [D.sub.3]-related pathologies.

Acknowledgments: We thank Bob Golding, director of research and development at Daavlin in Bryan, Ohio, for his invaluable assistance with all things lighting, and Simon Rousseau, research director and assistant professor, Department of Medicine, McGill University, Meakins-Christie Laboratories, for allowing us the use of his laboratory and equipment.

References

(1.) Bauck L. Shedding some light on the subject. HARI Web site. http://www.hagen.com/hari/docu/ shedding_light.html. Accessed July 11, 2012.

(2.) Beaudoin T. The necessity of full spectrum lighting. The Amazon Society. Parrot Island Newsletter. 1996.

(3.) Korbel RT, Gropp U. Ultraviolet perception in birds. Proc Annu Conf Assoc Avian Vet. 1999:77-81.

(4.) Boshouwers FMG, Nicaisse E. Reponses of broiler chickens to high-frequency and low-frequency fluorescent light. Br Poult Sci. 1992;33(4):711-717.

(5.) Maddocks SA, Goldsmith AR, Cuthill IC. Behavioural and physiological effects of absence of ultraviolet wavelengths on European starlings Sturnus vulgaris. J Avian Biol. 2002;33:103-106.

(6.) Lewis PD, Morris TR. Response of domestic poultry to various light sources. Poult Sci J. 1998;54:7 25.

(7.) Hurwitz S. Calcium homeostasis in birds. Vitam Horm. 1989;45:173-221.

(8.) Hochleithner M. Convulsions in African grey parrots in connection with hypocalcemia: five selected cases. Proc Euro Symp Avian Med Surg. 1989:44-52.

(9.) Cooper JE, Harrison GJ. Dermatology. In: Ritchie BW, Harrison GJ, Harrison LR eds. Avian Medicine: Principles and Application. Lake Worth, FL: Wingers Publishing; 1994:613-614.

(10.) Salibian A, Montalti D. Physiological and biochemical aspects of the avian uropygial gland. Braz J Biol. 2009:69(2):437-446.

(11.) Harrison GJ, McDonald D. Nutritional considerations--Section II: Nutritional Disorders. In: Harrison GJ, Lightfoot TL, eds. Clinical Avian Medicine. Vol I. Palm Beach, FL: Spix Publishing; 2006:110-111.

(12.) Takeshita K, Graham DL, Silverman S. Hypervitaminosis D in baby macaws. Proc Annu Conf Assoc Avian Vet. 1986:341-345.

(13.) Fraser DR. Vitamin D. Lancet. 1995;345(8942):104-107.

(14.) Lehman B. The vitamin D3 pathway in human skin and its role for regulation of biological processes. Photochem Photobiol. 2005;81(6):1246-1251.

(15.) Holick MF, MacLaughlin JA, Clark MB, et al. The photosynthesis of previtamin D3 in human skin and the physiologic consequences. Science. 1980;210(4466):203-205.

(16.) Webb AR, Holick MF. The role of sunlight in the cutaneous production of vitamin D3. Annu Rev Nutr. 1998;8:375-399.

(17.) Tian XQ, Chert TC, Lu Z, et al. Characterization of the translocation process of vitamin D3 from the skin into the circulation. Endocrinology. 1994;135(2):655-661.

(18.) Holick MF. The use and interpretation of assays for vitamin D and its metabolites. J Nutr. 1990;120(suppl 11): 1464-1469.

(19.) Baines FM, Buono M. Photo-kerato-conjunctivitis in reptiles under zoomed compact fluorescent lamps. UV Guide UK Web site. http://www.uvguide.co.uk. Accessed March, 30, 2010.

(20.) Wade LL, Baines FM. Ultraviolet-induced photokeratitis in a Meyer's parrot (Poicephalus meyeri) and ultraviolet-induced photodermatitis in an African grey parrot (Psittacus erithacus). Proc Annu Conf Assoc Avian Vet. 2008:421-422.

(21.) Zinolli M, Feldman S. Ultraviolet B phototherapy by skin type. Phototherapy Treatment Protocols for Psoriasis and Other Phototherapy Responsive Dermatoses. 2nd ed. Cleveland, OH: Taylor and Francis; 2005:52-53.

(22.) Bergmanson JPG, Soderberg PG. The significance of ultraviolet radiation for eye diseases. A review with comments on the efficacy of UV-blocking contact lens. Ophthal Physiol Opt. 1995;15(2):83-91.

(23.) Tangpricha V, Turner A, Spina C, et al. Tanning is associated with optimal vitamin D status (serum 25-hydroxyvitamin D concentration) and higher bone mineral density. Am J Clin Nutr. 2004;80(6):1645-1649.

(24.) Taylor SC. Skin of color: biology, structure, function, and implications for dermatologic disease. J Am Acad Dermatol. 2002;46(2):S41-62.

(25.) Clemens TL, Adams JS, Henderson SL, Holick MF. Increased skin pigment reduces the capacity of skin to synthesise vitamin D3. Lancet. 1982;1(8263):74-76.

(26.) Norman AW. Sunlight, season, skin pigmentation, vitamin D, and 25-hydroxyvitamin D: integral components of the vitamin D endocrine system. Am J Clin Nutr. 1998;67(6):1108-1110.

(27.) Morris JG. Ineffective vitamin synthesis of vitamin D in kittens exposed to sun and ultraviolet light is reversed by an inhibitor of 7-DHC-reductase. In: Norman AW, Boullon R, Thomasseti M, eds. Vitamin D: Chemistry, Biology and Clinical Applications of the Steroid Hormone. Riverside, CA: University of California; 1997:721-722.

(28.) Stanford, M. Effects of UVB radiation on calcium metabolism in psittacine birds. Vet Rec. 2006;159(8):236-241.

(29.) Schmidt DA, Mulkerin D, Boehm DR, et al. Quantifying the vitamin D3 synthesizing potential of UVB lamps at specific distances over time. Zoo Biol. 2010;29(6):741-752.

(30.) Acierno MJ, Mitchell MA, Zachariah TT, et al. Effects of ultraviolet radiation on plasma 25-hydroxyvitamin D3 concentrations in corn snakes (Elaphe guttata). Am J Vet Res. 2008;69(2):294-297.

(31.) Acierno MJ, Mitchell MA, Roundtree MK, Zachariah TT. Effects of ultraviolet radiation on 25-hydroxyvitamin D3 synthesis in red-eared slider turtles (Trachemys scripta elegans). Am J Vet Res. 2006;67(12):2046-2049.

(32.) Ryan C, Moran B, McKenna MJ, et al. The effect of narrowband UV-B treatment for psoriasis on vitamin D status during wintertime in Ireland. Arch Dermatol. 2010;146(8):836-842.

(33.) Flindt-Hansen H, McFadden N, Eeg-Larsen T, Thune P. Effect of a new narrow-band UVB lamp on photocarcinogenesis in mice. Acta Derm Venereol. 1991;71(3):245-248.

(34.) Serish, Srinivas CR. Minimal erythema dose (MED) to narrow band ultraviolet-B (NB-UVB) broad band ultraviolet-B (BB-UVB): a pilot study. Indian J Dermatol Venereol Leprol. 2002;68(2):63-64.

(35.) Gerhman WH. Ultraviolet irradiances of various lamps used in animal husbandry. Zoo Biol. 1987;6:117-127.

(36.) Kenny D. The role of sunlight, artificial UV radiation and diet on bone health in zoo animals. In: Holick MF, Jung EG, eds. Biological Effects of Light: Proceedings of the Biologic Effects of Light Symposium. Hingham, MA: Kluwer Academic; 1998:111-119.

(37.) Bunker JWM, Harris RS, Mosher ML. Relative efficiency of active wavelengths of ultraviolet light in activation of 7-dehydrocholesterol. J Am Chem Soc. 1940;62:508-511.

(38.) Fleming RH. Nutritional factors affecting poultry bone health. Proc Nutr Soc. 2008;67(2):177-183.

(39.) Gehrmann WH, Horner JD, Ferguson GW, et al. A comparison of responses by three broadband radiometers to different ultraviolet-B sources. Zoo Biol. 2004;23:355-363.

(40.) Holick MF. Vitamin D status: measurement, interpretation and clinical application. Ann Epidemiol. 2009;19(2):73-78.

(41.) Coto C, Cerate S, Wang Z, et al. Effect of source and level of vitamin D on the performance of breeder hens and the carryover to the progeny. Intl J Poult Sci. 2010;9(7):623-633.

(42.) Canadian Council on Animal Care. Other avian species. CCAC Web site. http://www.ccac.ca/ Documents/Standards/Guidelines/Vol2/other_ avian_species.pdf. Accessed March 2012.

(43.) Pollock C, Carpenter JW, Antinoff N. Birds. In: Carpenter JW, ed. Exotic Animal Formulary. 3rd ed. St Louis, MO: Elsevier Saunders; 2005:264-265.

Corina Lupu, DVM, Dipl ABVP (Avian), and Stephanie Robins, MSc

From the Montreal Bird and Exotic Animal Hospital, 6090 Sherbrooke St W, Montreal, Quebec H4A 1Y1, Canada.

Table 1. Irradiance, exposure time, and dose applied in
each experiment of this study.

                  Irradiance, mW/[cm.sup.2b]

                  Daavlin   Solartech   Exposure    Daily dose,
Experiment (a)      X96        6.2      time, s    mJ/[cm.sup.2]

BB1               0.021       0.028      7200          150
BB2               0.0085      0.012      7200          65
BB3               0.0085      0.012      21 600        180
NB1               0.12        0.13       5400          600
NB2               0.34        0.25       5100          1730

(a) In experiments BB1, BB2, and BB3 budgerigars were exposed to
    a broadband ultraviolet B (UVB) light source (280-315 nm); in
    experiments, NB1 and NB2 budgerigars were exposed to a
    narrowband UVB light source (310-320 nm).

(b) Irradiance was measured using a Daavlin X96, P9710 optometer
    (accuracy, [+ or -] 5%). Irradiance values obtained were used in
    dose calculations; parallel measurements were obtained by using a
    Solartech 6.2 radiometer (accuracy, [+ or -] 10%).

Table 2. Serum concentrations of 25/OH/D (nmol/L) in
budgerigars before and after exposure to daily doses of
broadband or narrowband UVB, and budgerigars not exposed to
UVB (control).

                                                        Quartiles
                  Minimum,  Maximum,  Median,   SD,
Experiment    n    nmol/L    nmol/L   nmol/L   nmol/L  Lower  Upper

BBl
  ctl day 0   10   11.99     215.20    14.80   62.42   13.35  34.60
  ctl day 3   10   12.40     164.20    16.04   50.68   14.16  46.42
  UVB day 0   10   10.41      72.96    14.75   20.86   12.06  35.39
  UVB day 3   10   10.30      21.20    14.35    3.64   11.16  17.39

BB2
ctl day 0     10    8.39      66.89    11.18   17.74   10.30  12.50
ctl day 5     10    9.69      23.00    13.32    3.61   11.56  13.94
UVB day 0     10   11.55      27.20    16.03    4.48   13.86  19.01
UVB day 5     10    7.98      60.25    15.30   16.72   12.44  24.89

BB3 (a)
ctl day 0     10    9.49      13.16    11.58    1.31    9.87  12.44
ctl day 5     10    8.46      44.24    13.13   10.28   11.22  17.19
UVB day 0     10    9.09      50.58    12.30   14.26   10.58  20.88
UVB day 5     10   10.49     118.80    27.34   33.34   21.25  53.08

NB1
ctl day 0     9     8.82      21.56    11.53    4.63    9.40  17.79
ctl day 5     9     8.75      53.60    17.42   13.79    9.88  22.39
UVB day 0     9     8.77      12.32    10.46    1.16    9.73  11.64
UVB day 5     9     9.91      28.17    16.14    5.92   12.23  20.38

NB2
ctl day 0     7     5.09      26.11     7.93    7.17    6.05  11.35
ctl day 5     7     6.89      42.72    18.53   12.89    8.56  27.39
UVB day 0     8     5.95      33.87     9.76    8.98    6.99  12.80
UVB day 5     8     6.44      19.92     9.54    5.68    7.69  18.64

Abbreviations: 25-OH-D indicates 25-hydroxycholecalciferol;
UV, ultraviolet; BB, broadband UVB (280-315 nm); ctl,
control; NB, narrowband UVB (310-320 nm).

(a) The change in 25-OH-D levels was not significantly
different among the groups except in experiment 13133, in
which the change in 25-OH-D was significantly increased in
the UVB group compared with control, P = .035.
COPYRIGHT 2013 Association of Avian Veterinarians
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2013 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Lupu, Corina; Robins, Stephanie
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Date:Dec 1, 2013
Words:7080
Previous Article:Comparison of osmolality and refractometric readings of Hispaniolan Amazon parrot (Amazona ventralis) urine.
Next Article:Normal electrocardiogram patterns and values in Muscovy ducks (Cairina moschata).
Topics:

Terms of use | Privacy policy | Copyright © 2022 Farlex, Inc. | Feedback | For webmasters |