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Experimental Physiology 89.4 pp 427-433
DOI: 10.1113/expphysiol.2004.027656
© The Physiological Society 2004
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Effect of metabolic cage housing on immunoglobulin A and corticosterone excretion in faeces and urine of young male rats

Emma Eriksson, Felix Royo, Karin Lyberg, Hans-Erik Carlsson and Jann Hau

Division of Comparative Medicine, Department of Neuroscience, Uppsala University, BMC Box 572, 75123 Uppsala, Sweden


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
Six 8-week-old Sprague-Dawley rats were studied for 9 days divided into three periods of 3 days each: before transferral to metabolism cages, during metabolic cage housing and after return to their home cages. Faeces were collected daily when the animals were housed in their home cages and every 6 h when the animals were housed in metabolic cages during which time urine was also collected every 6 h. The rate of weight gain was slightly reduced during the 3 days in metabolic cages and the animals produced significantly larger amounts of faeces when housed in metabolic cages than when housed in their home cages. The total faecal excretion of corticosterone (nanograms excreted per hour per kilogram body weight) and immunoglobulin A (IgA) (milligrams excreted per hour per kg body weight) quantified by enzyme-linked immunosorbent assays (ELISAs) exhibited a clear diurnal rhythm in the metabolic cage. Urinary excretions of corticosterone and IgA also followed a clear diurnal cycle. The mean daily amounts of corticosterone excreted were not significantly affected by cage change and by housing in metabolic cages. However, the excretion of faecal IgA was significantly reduced during the 3 days after the period in metabolic cages. Taken together the results indicate that metabolic cage housing is mildly stressful for young adult male rats.

(Received 12 March 2004; accepted after revision 22 April 2004; first published online 6 May 2004)
Corresponding author J. Hau: Division of Comparative Medicine, Department of Neuroscience, Uppsala University, BMC Box 572, 75123 Uppsala, Sweden. Email: jann.hau{at}bmc.uu.se


   Introduction
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 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
Corticosteroids are secreted from the adrenal cortex as a response to environmental as well as psychological stressors and are well known to increase the susceptibility to infections through immunosuppression, although adrenal hyperactivity induced by chronic environmental stressors does not always have this effect (Klein et al. 1992). Corticosterone is the major glucocorticoid found in rats and mice. The level of corticosterone in rats and mice is of the same order of magnitude as that of cortisol in humans, and may be used as an index of adrenal function (O'Brien et al. 1995). The normal cyclic variation in corticotrophin-releasing hormone results in a diurnal variation in levels of corticosterone in the circulation (Loeb & Quimby, 1989).

It has been suggested that faecal glucocorticosteroid measurements are useful for non-invasive assessment of preceding stress (4–12 h prior to faecal sampling) in a number of species including cats and dogs (Schatz & Palme, 2001; Palme et al. 2001), mice, deer mice and voles (Harper & Austad, 2000, 2001), rats (Pihl & Hau, 2003, Royo et al. 2004), roe deer (Dehnhard et al. 2001) and non-human primates (Whitten et al. 1998; Bahr et al. 2000).

In the immune system, glucocorticoid receptors can be found in all of the major subsets of leucocytes at different densities. Total serum levels of IgA, IgG and IgM are reduced after administration of high doses of glucocorticoids, but treatment with lower doses may instead increase the level of IgA, IgG and IgM production (Griffin & Thomson, 1998).

A healthy 70-kg adult human produces about 3 g of antibodies every day (Greger & Windhorst, 1996; Abbas et al. 2000). About 60–70% of this is IgA. Secretory IgA is present in saliva, tears, bile, milk and vaginal, respiratory and intestinal secretions and acts as a first defence against pathogens, in particular viruses and bacteria. IgA is produced by interstitial immunocytes in mucosal lymphoid tissues and secreted by B-cells in the walls of the gastrointestinal and respiratory tracts and actively transported through the mucosal epithelial cells into the lumens of the organs by an IgA-specific Fc receptor called the poly Ig receptor. This receptor is synthesized by mucosal epithelial cells and expressed on their basal and lateral surfaces. The large amount of IgA produced reflects the large surface areas of these organs.

A correlation between a surge in glucocorticoid concentration and subsequent decrease in secretory IgA levels in mucosal secretions would not be entirely unexpected as the steroids inhibit the production of IgA. In humans, several studies have indicated a correlation between stress and lower than normal levels of secretory IgA in saliva samples (Deinzer & Schuller, 1998; Ng et al. 1999; Ohira et al. 1999) and this was also observed in the dog in which a negative correlation between salivary cortisol and IgA levels was recorded (Skandakumar et al. 1994). Studies of rats have indicated the potential use of salivary IgA levels to assess stress in this species (Guhad & Hau, 1996) and a negative correlation between faecal amounts of excreted corticosterone and IgA was observed in rats (Royo et al. 2004).

Metabolic cages are often used in biomedical research and it is debated whether housing in these cages is more stressful than single housing in standard rodent cages and how long rodents need to acclimate to metabolic cages prior to a study. Gil et al. (1999) found an age difference in the catecholamine responses of rats to metabolic cage housing for 1 week. In 3-month-old rats, urinary noradrenaline (norepinephrine) excretion decreased during the period, whereas in 10-month-old rats the levels remained constant during the time in metabolic cages. Urinary adrenaline (epinephrine) excretion was similar in both age groups and did not differ significantly during the period housed in the metabolic cage. Gomez-Sanchez & Gomez-Sanchez (1991) reported that transfer of rats to metabolic cages was associated with an increase in corticosterone synthesis and advised that scientists allow rats to acclimate to the metabolism cages prior to experiment. Later reports have also indicated that housing rats on grid floor as compared with housing in cages with saw dust bedding was associated with significantly higher corticosterone levels (Heidbreder et al. 2000) and an increase in blood pressure and heart rate (Krohn et al. 2003).

The aim of the present study was to quantify excretory amounts of corticosterone and IgA in faeces and urine in young rats housed under standard conditions for metabolic studies and subjected to standard sampling procedures. In addition to this we also wanted to analyse the diurnal rhythmicity of the excretion of these molecules.


   Methods
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 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
Animals and housing

Six 8-week-old male Sprague-Dawley rats (B & K, Sollentuna, Sweden) were used. The rats were housed individually in polycarbonate type IV cages, each furnished with a wooden hut structure as environmental enrichment, according to university practice for rats, for 10 days before they were transferred to and housed in metabolic cages with stainless steel grid floor, 23 cm in diameter and 18 cm high (Techniplast no. 3700M071, Scanbur, Koge, Denmark). They were studied for 3 days (72 h) in the metabolic cage (hour 0 = 14.00 h) after which they were transferred back to their original polycarbonate type IV home cages and studied for a further 3 days. Throughout the study the individual animals were handled approximately 5 min every day. The rats were kept in standard animal rooms under normal conditions: 12 h dark (18.00–06.00 h)–12 h artificial light (06.00–18.00 h) cycle; temperature maintained at 21 ± 1 °C; and relative humidity varied between 30 and 60%. Wooden chips (Finn Tapvei, Finland) were used as bedding in the polycarbonate cages. The animals were supplied with water and standard pelleted diet (R36, Lactamin, Stockholm, Sweden) ad libitum.

Sampling

All faecal pellets were collected daily when the animals were housed in polycarbonate cages. All faecal pellets and all urine were collected every 6 h (at 08.00, 14.00, 20.00 and 02.00 h) when the animals were housed in metabolic cages. The pellets and urine were stored in plastic test tubes at –20 °C before analysis. The frozen samples were dried in a heat cabinet at 30 °C for approximately 2 h. After weighing, 4 ml Millipore H2O per 1 g sample was added, and the suspension was homogenized with a Severin Profi-mix hand blender (Severin Elektrogenerate GmBH, Sundern, Germany).

The urine samples were weighed at the time of collection from the cages. The rats were weighed daily and at each sampling occasion.

Extraction methods

To extract corticosterone, 5 ml dichloromethane (CH2Cl2) was added to 1 g of faecal homogenate, and vortexed for 30 s in pulses of 5 s. The mixture was centrifuged for 15 min at 1690 g. The aqueous layer and the solid phase were removed and the remains were washed once with 1 ml NaOH (0.1 M) and once with 1 ml distilled water. At each of the washes, the tubes were mixed on a vortex mixer for 10 s and centrifuged at 1690 g for 10 min. A volume of 1000 µl of the eluate was transferred to glass tubes and left to evaporate to dryness under nitrogen (approximately 40 min).

To extract IgA, 1 mg of the homogenate was added to 2 ml dilution buffer (PBS, 0.1% Tween 20, pH 7.2). The suspension was homogenized by gently shaking for 60 min and vortexing it 4–5 times during that time. After centrifugation for 15 min at 1690 g and at 7200 g for 10 min, the supernatant was extracted and suspended 20 times with the dilution buffer.

Quantification of corticosterone and IgA

The corticosterone concentration in serum was analysed without any preceding extraction procedures. The residue in the evaporated faecal samples for corticosterone analysis was dissolved in 300 µl dilution buffer (PBS, 0.05% Tween 20, pH 7.4). Immunoreactive corticosterone metabolites were quantified using Correlate-EIA (Assaydesigns INC, MI, USA) according to the manufacturer's manual. The assay had a reported cross reactivity of 21% against deoxycorticosterone, 21% against desoxycorticosterone, < 1% against progesterone, testosterone, tetrahydrocorticosterone and aldosterone, and < 0.1% against cortisol, pregnenolone, beta-oestradiol, cortisone, and 11-dehydrocorticosterone acetate. It is uncertain to which extent this kit also reacts with corticosterone metabolites, which are present in faeces. The term ‘immunoreactive corticosterone metabolites’ instead of corticosterone would have been more correct when addressing faecal concentrations. However, for clarity this was not done. The intra-assay coefficient of variation was 5.5%, and the inter-assay coefficient of variation was 13%.

To analyse the concentration of IgA in the samples, a sandwich ELISA was used as described by Hau et al. (2001). The intra-assay coefficient of variation was 2.3%, and the inter-assay coefficient was 5.8% for faecal samples.

Good stability of immunoreactive corticosterone metabolites and IgA in rat faeces maintained at room temperature for up to 24 h was documented by Royo et al. (2004).

Statistics

The statistical analysis was performed as ANOVA tests. Differences with P < 0.05 were considered significant. Line trends and line fit equations were calculated using Excel (Microsoft).

Ethics committee approval

The Uppsala regional ethics committee in Tierp, Sweden approved the experimental procedures.


   Results
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 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
The rats gained weight during the experiment, from a mean value of 306.1 ± 2.7 g to 377.0 ± 4.8 g. The daily weight gain was slightly reduced during the time period when the animals were housed in metabolic cages. Figure 1 shows the best straight line fits and line equations for the three periods. The slope is flatter during the time spent in metabolic cages (2.6) compared with the periods before (5.3) and after (3.8).



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  		Figure 1.  Linear fit equations of the mean body weights
Values (n= 6) during the 3 days before metabolic cage housing (pre-assay), during the 3 days in metabolic cages (assay, during which period the animals were weighed every 6 h), and the first 3 days after the animals had been returned to their home cages (post-assay). Error bars represent S.E.M.

 
Faecal excretion varied between the different time periods. The daily amount of faeces excreted during the time period in the metabolic cage (mean ±S.E.M, 7.88 ± 0.2 g) was significantly higher than the daily amount produced in the pre-metabolic housing period (6.1 ± 0.1 g) or during the post-metabolic housing period (5.7 ± 0.2 g).

During the time spent in the metabolic cage a diurnal pattern of faecal excretion was observed as shown in Fig. 2. The largest excretion was observed during the dark period, which is the active period for rats.



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  		Figure 2.  Mean weights of faeces voided when the rats were housed in metabolic cages
The dark areas on the x-axis represent the dark periods (18.00–06.00 h). Error bars represent S.E.M.(n= 6).

 
When the rats were housed in metabolic cages a diurnal pattern of urine excretion was observed with the largest excretion during the dark period (Fig. 3).



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  		Figure 3.  Mean weights of urine voided when the rats were housed in metabolic cages
The dark areas on the x-axis represent the dark periods (18.00–06.00 h). Error bars represent S.E.M.(n= 6).

 
The daily mean excretion of faecal corticosterone is shown in Fig. 4. There was no significant increase during and shortly after housing in metabolic cages. During the 3 days of housing in metabolic cages, a diurnal rhythmicity in faecal corticosterone excretion was observed with the largest excretion in the period from 20.00–02.00 h (Fig. 4).



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  		Figure 4.  Total daily faecal corticosterone excretion
Values expressed as nanograms per 24 h, and per kilogram body weight (error bars represent S.E.M., n= 6). The animals were housed in metabolic cages during days 3, 4 and 5, and the different shades of grey in the bars represent the contribution to the total excretion in each 6- h time interval, corresponding to the intervals shown in the Figure.

 
The average daily faecal excretion of IgA is shown in Fig. 5. During the 3 days after the metabolic cage housing the animals secreted significantly lower amounts of faecal IgA (P= 0.0005) than they did beforehand (days 0–5).



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  		Figure 5.  Total daily faecal IgA excretion
Values expressed as milligrams per 24 h, and per kilogram body weight (error bars represent S.E.M.,n= 6). The animals were housed in metabolic cages during days 3, 4 and 5, and the different shades of grey in the bars represent the contribution to the total excretion in each 6- h time interval, corresponding to the intervals shown in the Figure.

 
During the 3 days housing in metabolic cages, a diurnal cycle in faecal IgA excretion was observed with the largest excretion in the time window 20.00–02.00 h (Fig. 5). The amounts excreted in urine did not seem to exhibit diurnal variation although a diurnal variation in the amount of urine excreted was observed. This is in contrast to the amounts of IgA excreted in faeces, which showed a significant increase during night-time even when making allowance for the larger faecal excretion during night-time than during daytime.

The proportions of corticosterone found present in urine and in faeces varied between the different periods (Fig. 6).



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  		Figure 6.  Total amounts of corticosterone excreted via urine and via faeces
Values expressed as nanograms corticosterone excreted per hour per kilogram body weight during the four 6- h time periods of the day during the 3-day housing in metabolic cages (means ±S.E.M., n= 18).

 
IgA is secreted by the gastrointestinal mucosa, and Fig. 7 shows the amounts excreted at various time points in rats housed in metabolic cages.



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  		Figure 7.  Total amounts of IgA excreted via urine and via faeces
Values expressed as milligrams IgA excreted per hour per kg body weight during the four 6- h time periods of the day during the 3-day housing in metabolic cages (means ±S.E.M., n= 18).

 

   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
An increased frequency of defecation as well as a reduced body weight gain in growing animals is classical signs of anxiety and stress (Morton & Hau, 2003). Both of these features were observed in the present study when rats were housed in metabolic cages. Although the animals were maintained in the same room with stable room temperature during the study they would have to eat more food in the metabolic cages in order to maintain body temperature and weight gain rate because of the grid floor and absence of bedding. A clear diurnal pattern of excretion of faeces and urine was observed in the metabolic cages. The amounts excreted during the dark period when the animals are active were significantly larger than the amounts excreted during the light period when the animals were resting.

In the present study we measured the total amounts of corticosterone excreted in urine and faeces and the total amounts of IgA excreted in faeces per unit time per kg body weight. This is in contrast to most other studies which measured concentrations in excreted products only. We consider concentration measurements in samples unreliable because the concentration differences between neighbouring faecal pellets in rats may vary by up to 40% (Pihl & Hau, 2003). An obvious advantage of our approach, collecting all faeces and all urine, is that by measuring the total amounts excreted we obtain direct information about diurnal rhythmicity of excretion. In most endocrinological studies using repeated measures of concentrations in, for example, blood the ‘area under the curve’ is a frequently used integrative method to attempt to obtain measures of secretion over a specific time period (Preussner et al. 2003). Using our approach accurate measures are obtained directly. In this context it is important to bear in mind that changes in corticosteroid concentration taking place in the animal's circulation will not be apparent in faecal excretions until 6–18 h later.

Increased amounts of faecal corticosterone excretion in rats may be indicative of preceding stress. We found that anaesthesia and surgery were associated with a significant increase of corticosterone in the circulation followed by an increase in faecal amounts excreted in male rats of the same age and stock used in the present study (Royo et al. 2004). In the present study no significant changes in faecal excretion of corticosterone were observed. This is in contrast with the findings of Gomez-Sanchez & Gomez-Sanchez (1991) and Heidbreder et al. (2000) who reported an increased corticosterone synthesis when animals were housed on grid floor. An explanation to this difference in results may be the short duration of the metabolic cage housing in the present study. We recorded a trend towards increasing amounts of faecal corticosterone excreted throughout the stay in the metabolic cages but this trend was not significant. It remains uncertain whether this trend would have continued if the animals had been maintained for a longer period in the metabolic cages. The faecal excretion of corticosterone in metabolic cages showed a stable diurnal rhythmicity with larger amounts excreted during the night than during the day. This confirms earlier findings of higher nocturnal secretion in this stock (Pihl & Hau, 2003).

The daily faecal excretion of IgA was significantly reduced during the 3 days after the housing in metabolic cages. This agrees with our previous findings suggesting that faecal excretion of IgA may be reduced as a consequence of preceding stress (Royo et al. 2004). As for corticosterone, IgA faecal excretion showed a clear diurnal rhythmicity with larger amounts excreted during the night than during the day. This deviates from the findings of Pihl & Hau (2003), who did not observe any significant difference between daytime and night-time excretion.

Corticosterone in the circulation of the rat is excreted in urine and in faeces. The proportion of the corticosterone excreted in faeces and urine, varied between day and night. During daytime the amounts excreted in urine and faeces were fairly similar, but during the night the amounts excreted in the urine increased dramatically whereas only a moderate increase in faecal corticosterone excretion was seen. This is in contrast with what has been described in the mouse (C57BL) injected intraperitoneally with radio-labelled corticosterone. Most radioactivity was recovered in the faeces of male mice and only minor radioactivity was recorded in the urine (Touma et al. 2003). Large differences were found between male and female mice and taking the species difference and difference in methodology into consideration makes it difficult to speculate about the reasons for the difference in results of the two studies.

In conclusion, the increase in excreted amounts of faeces combined with the reduction in body weight gain during the rats' stay in the metabolic cages and subsequent reduction in faecal IgA excretion indicate that this type of housing may be associated with a certain stress perception in rats. However, the stress was not of sufficient magnitude or duration to result in a significant increase in corticosterone excretion, indicating that housing for a few days in metabolic cages is not associated with major stress for laboratory rats. If the metabolic cage housing had been really stressful it would have been logical to examine the source(s) of the stressors, for example disturbance every 6 h, cage size, cage shape, absence of bedding, grid floor or absence of cage furniture. However, given that the complete change in environment seems associated with very minor stress perception a larger study with many different housing systems seems uncalled for.


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 
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