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J. Anim. Sci. 2002. 80:2349-2361
© 2002 American Society of Animal Science

Effects of ventilation regimen on the welfare and performance of lactating ewes in summer1

A. Sevi*,2, M. Albenzio*, G. Annicchiarico{dagger}, M. Caroprese*, R. Marino* and L. Taibi{dagger}

* Istituto di Produzioni e Preparazioni Alimentari, Facoltà di Agraria di Foggia, via Napoli, 25, 71100 Foggia, Italy and and {dagger} Istituto Sperimentale per la Zootecnia, via Napoli, 71020 Segezia-Foggia, Italy

2 Correspondence:
phone: ++39-0881-589217; fax: ++39-0881-740211; E-mail:
a.sevi{at}unifg.it.


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
A 6-wk trial was performed with thirty-six lactating Comisana ewes during the summer of 2001. The animals were divided into three groups of 12, which were designated low (LVR), moderate (MVR), and programmed (PROGR) ventilation regimens. In LVR and MVR rooms, fans provided 10 ventilation cycles of 12.5 and 25 min/h, respectively, whereas in the PROGR room, the fan was programmed to operate at 30°C air temperature and 70% relative humidity. Mean ventilation rates were 33, 66, and 173 m3/h per ewe in LVR, MVR, and PROGR rooms. Air concentrations of microorganisms and dust and of gaseous pollutants were measured twice weekly. Respiration rate and rectal temperature were monitored throughout the trial at 1430. Behavioral traits of ewes were recorded once per week from 0930 to 1230. Cell-mediated immune response to phytohemagglutinin at d 3, 20, and 40 and humoral response to chicken egg albumin at d 11, 21, 30, and 40 were determined. At d 37, ewes were injected with 2 IU porcine ACTH/kg body weight0.75 and subjected to blood sampling for evaluation of cortisol concentrations immediately before and 1, 2, and 4 h after ACTH injection. Milk yield was recorded daily. Individual milk samples were analyzed weekly for composition and renneting parameters and fortnightly for bacteriological characteristics. Averages of temperature-humidity index values were 78.9, 76.8, and 74.5 in LVR, MVR, and PROGR rooms, respectively. The LVR and MVR treatments resulted in higher NH3 and CO2 air concentrations than PROGR treatment (P < 0.05). The LVR and MVR ewes had higher rectal temperatures than PROGR ewes (P = 0.001). LVR animals also exhibited higher idling compared to PROGR (P < 0.01) and lower feeding times than MVR (P < 0.05) and PROGR animals (P < 0.01). Ewes under the LVR treatment displayed significant lower averages of antibody titers and higher plasma cortisol levels than PROGR (P < 0.01) and MVR ewes (P < 0.05) 60 min after ACTH injection. The LVR treatment resulted in lower yields of milk (P < 0.01) and reduced feed efficiency (P < 0.01) than PROGR treatment. Results suggest that a fan-ventilated system, providing ventilation cycles during the warmest hours of the day and the night at a mean ventilation rate of 66 m3/ewe per hour, may sustain the performance and welfare in lactating ewes raised in warm climates during summer. A ventilation regimen, programmed to operate over upper critical air temperature and relative humidity, may be economically unattractive under these conditions.

Key Words: Hydrocortisone • Immune Response • Milk Yield • Sheep • Ventilation


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Ventilation plays a main role in sustaining the welfare and performance of farmed livestock, by affecting thermal exchanges between the animal’s body surface and the environment and by removing aerial pollutants, which originate from animals and their excreta. Indeed, poor ventilation can lead to increased airborne particulate and gaseous pollutant concentrations, which can present a significant burden to the respiratory tract of humans and livestock (Rylander, 1986; Hartung, 1994). Previous experiments have shown that poor ventilation is responsible for increased aerial concentrations of viable microbes, NH3 and CO2, reduced feed efficiency, and enhanced aggressive interactions in cattle, in pigs, and in broiler chickens (Wathes et al., 1983; Massabie et al., 1997; Marrufo Villa et al., 1999; Spoolder et al., 2000). In addition, it is known that inefficient ventilation systems result in animals avoiding more contaminated areas of livestock buildings (Smith et al., 1996). This may lead to an uneven use of space with very low and highly densely stocked areas in animal houses.

A ventilation rate of 1.22 m3/h per kilogram body weight has been suggested for maintenance of gaseous pollutants within acceptable levels in animal houses (Curtis, 1983). Practical recommendations are given for ventilation rate in cattle (Lawrence, 1994), pig (Bruce, 1981), and poultry housing (Charles, 1981). Little information is available for sheep, due to the fact that extensive production systems are predominant for this species. However, the gradual increase of intensive housing in sheep, as a consequence of the increased size of specialized dairy flocks, and the fact that this species is mainly raised in warm climates needs more specifications for ventilation rates and regimens in sheep houses.

This study was undertaken to assess the effects of ventilation regimen on behavior, immune and endocrine responses, performance and udder health of lactating ewes during summer in a Mediterranean climate.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Implications
 Literature Cited
 
General Methods.
The experiment, which lasted 6 wk, was conducted during the summer (July to August) of 2001 at Segezia research station of the Italian Istituto Sperimentale per la Zootecnia (latitude: 41° 27' 6'' and longitude: 15° 33' 5''). The climate of this area is Mediterranean, with about 500 mm of annual rainfall, mainly distributed in late autumn and winter, and a 22.1°C mean maximum air temperature (often over 30°C from June to August).

Thirty-six lactating Comisana ewes (d 170 ± 0.39 of lactation, mean ± SE) with no history of mastitis were used. The animals were housed in a prefabricated building provided with external paddocks before the experiment and were fed on a 0.65 Milk Forage Units/kg DM diet composed of a pelletted concentrate, oat grain, and vetch/oat hay in 20:10:70 ratio. Ewes were healthy, and their condition was judged as good at the commencement of the trial. The animals were divided into three groups of 12 each, which were balanced for age, parity, time of lambing, number of lambs suckled, body weight (55.55 ± 1.81 kg), body condition score (2.29 ± 0.09), milk yield (646 ± 35 g/d), and milk protein (6.17 ± 0.07%) and fat (6.18 ± 0.16%) contents. Groups were separately housed on straw litter in 8 m x 3 m and 3.5 m high rooms of the same building. The experimental rooms were adjacent, faced south, away from prevailing winds and were provided with transom windows (total glazed area = 6 m2), placed at a height of 2.5 m. Ewes could freely move within each room, which was provided with a negative-pressure mechanical system of ventilation, in which 0.28 m2 suction fans (Vortice, 20067 Tribiano, Milan, Italy) were placed at 2.5 m from the floor and two 0.36 m2 air inlets were placed at ground level on the opposite wall. Fan speed was kept constant at 4 m/s. The three groups were low (LVR), moderate (MVR), and programmed ventilation regimen (PROGR). In LVR and MVR rooms, fans provided 10 ventilation cycles per day. Each cycle duration was 12.5 vs 25 min/h, respectively; eight cycles were during daytime from 1000 to 1800 and two during nighttime at 0200 and at 0600). In the PROGR room, the fan was connected to air temperature and relative humidity sensors, which provided an on/off two stage control function switching power to the fan. Ventilation system was programmed to operate at 30°C air temperature and 70% relative humidity. These thresholds were chosen on account of previous reports about critical temperature and humidity for sheep welfare and productivity (Bhattacharya and Uwayjan, 1975; Curtis, 1983; Casamassima et al., 1991; Sevi et al., 2001). In all rooms, ventilation rate was checked daily by placing a hot wire anemometer (LSI, I-20090, Settala Premenugo, Milan, Italy) over the air outlet and converting readings to m3/h per ewe. The fans worked 2 h and 5 min, 4 h and 10 min, and 10 h and 50 min daily in LVR, MVR, and PROGR rooms, respectively, providing a mean ventilation rate of 33, 66, and 173 m3/h per ewe. A power input of 1,162, 2,325, and 6,045 kW/d was calculated for the three ventilation regimens, according to the data provided by the builders.

The air temperature and the relative humidity inside each room were continuously monitored throughout the trial and during the week before the commencement of the experiment to be sure that climatic conditions were the same in all rooms. TIG2-TH thermo-hygrographs (LSI) were used, which were placed at a height of 1.5 m from the floor. Averages of air temperature and relative humidity were 26.1, 26, and 26.2°C and 57, 56.4, and 57.1% in LVR, MVR, and PROGR rooms, respectively, during the pretreatment week. Data from thermo-hygrographs and Kelly and Bond’s (1971) formula were used to calculate the temperature-humidity index (THI). In each pen, a layer of straw (about 0.3 kg/m2) was strewn on litter daily.

Each pen was provided with two mangers; feeder space per animal was about 0.45 m. The ewes were fed on a diet composed of a pelletted concentrate, oat grains, and vetch/oat hay (24, 18, and 58% of total diet, respectively), which was offered as a total mixed ration twice daily. The chemical composition of dry matter was determined by standard procedures (AOAC, 1990) and contained 16.5% crude protein, 2.7% fat (by ether extraction), 43.1% NDF, 8.3% ash, and 0.79 Milk Forage Units/kg. DM intakes were calculated daily as the difference between the amount of feed offered and feed refusals. Water was available from automatic drinking troughs.

Air Sampling.
Air sampling was performed twice weekly in the morning, starting from 0900 (fans switched off in LVR and MVR rooms), and in the afternoon, starting from 1630 (fans switched on in all rooms). Air was sampled 0.6 m from the floor and the sequence of air sampling in the three experimental rooms changed according to a prearranged program.

The concentration of mesophilic microorganisms, coliforms, and yeasts/molds were recorded from 720 L of air (flow rate = 1.5 L/s) sampled using a Surface Air System pump (PBI International, Milan, Italy) directly onto plates containing plate count agar (Oxoid, Basingstoke, UK), violet red bile lactose agar (Oxoid), and sabouraud dextrose agar (Oxoid), respectively. All measurements were made at six locations within each room. After sampling, the plates were immediately incubated at 30°C for 24 to 36 h for mesophilic bacteria, at 37°C for 24 to 36 h for coliforms, and at 25°C for 96 h for yeasts and molds.

Air concentrations of total (particulate size > 5 µm) and respirable (particulate size = 2 to 5 µm) dust were recorded using DIGIT ISO pumps (Zambelli, Bareggio-Milan, Italy). Dust was gravimetrically collected on cellulose nitrate filters having a pore size of 0.8 µm. A Lippman cyclone was used for selecting respirable dust by centrifugation. Samples were taken in two different locations in each room, and the amount of air collected per room for each of the two parameters was 1 m3 (flow rate = 30 L/min). The dust collected was being weighed on an analytical scale. The filters were dried in an oven at 50°C for 8 h before weighed and used for air sampling.

Air concentrations of gaseous pollutants were recorded from six locations within each room, using a Gas Detection Pump (Dräger-Italia, 20094 Corsico, Milan, Italy). The concentrations of carbon dioxide, hydrogen sulphide, ammonia, and methane were colorimetrically determined in graduate detection tubes.

Rectal Temperatures and Respiration Rate.
Respiration rate (RR) and rectal temperature (RT) were monitored in all animals throughout the trial at 1430, in order to assess the effects of ventilation regimen on ewe thermal status during the warmest part of the day. Respiration rate was recorded by a trained observer by counting the rate of flank movement and soon after RT was measured with TM46 electronic thermometers (LSI) having an accuracy to 0.1°C. The thermometers, as well as thermo-hygrographs and the anemometer, were calibrated by the builders before the commencement of the trial.

Behavioral Observation.
Behavioral observations were recorded by two trained observers equipped with GR-AX 40 video cameras (JVC-Italia, 20090 Segrate, Milan, Italy) every 15 min from 0930 to 1230 once per week. Scan samples were taken from the video records and the measurement criterion at each observation period was the number of animals engaged in each of two postures (standing or lying) and of seven behavior categories, which were eating, drinking, ruminating, walking, self-grooming, and idling (i.e., animals were inactive and judged subjectively to be inattentive or phlegmatic). Postural data and behavioral activities were expressed as percentages of total observation time. Social activities (smelling, nuzzling, and rubbing each other) and aggressive interactions (butting, threat jumping, shoulder pushing) are short lasting events; therefore, their frequency of presentation was measured by continuous recording for the whole 3-h period.

Immune Response.
The phytohemagglutinin (PHA) skin test was performed to induce nonspecific delayed-type hypersensitivity. At d 3, 20, and 40 of the experiment, 1 mg of PHA (Sigma-Aldrich Italia, Milan, Italy) dissolved in 1 mL of sterile saline solution was injected intradermally into the middle of two 2-cm-wide circles stamped on shaved skin in the upper side of each shoulder. The skinfold thickness was determined before PHA injection and 24 h after with a caliper. For each animal, an average increase in skinfold thickness (24 h postinjection thickness to preinjection thickness) was computed using the two measurements taken from each shoulder.

At d 2 of the study, 6 mg of chicken egg albumin (Sigma-Aldrich Italia) dissolved in 1 mL of sterile saline solution and in 1 mL of incomplete Freund’s adjuvant (Sigma-Aldrich Italia) were injected subcutaneously in both shoulders of each ewe. A second injection without adjuvant was repeated 9 days later. Antibody titers were determined in blood samples collected in heparinized vacuum tubes (Becton Dickinson, Plymouth, United Kingdom) immediately before the first antigen injection (2 d) and then at 11, 21, 30, and 40 d of the study period. An ELISA was performed in 96-well U-bottomed microtiter plates. Wells were coated with 100 µL of antigen (10 mg of OVA/mL of phosphate-buffered saline-PBS) at 4°C for 12 h, washed and incubated with 1% skimmed milk (200 µL) at 37°C for 1 h to reduce nonspecific binding. After washing, the serum (1:1,000 dilution in PBS; 100 µL per well) was added and incubated at 37°C for 1 h. The extent of antibody binding was detected using a horseradish peroxidase-conjugated donkey anti-sheep IgG (Sigma-Aldrich Italia) (1:20,000 dilution in PBS; 100 µL per well). Optical density was measured at a wavelength of 450 nm. The inter- and intraassay CV were 3.5 and 5.1%, respectively. The assay was optimized in our laboratory for concentrations of coating antigen, serum, and detector antibody.

Cortisol Levels.
At d 37, ewes were intravenously injected with 2 IU porcine ACTH/kg body weight0.75 (Sigma-Aldrich Italia). Blood samples (10 mL) for evaluation of cortisol concentrations were collected in vacuum tubes from the jugular vein immediately before and 1, 2, and 4 h after ACTH injection. Hormone concentration was determined by a radioimmunoassay specific for ovine cortisol (Immunotech, Marseille, France). The sensitivity of the assay was 0.2 µg/dL. The inter- and intraassay variation coefficients were 1.4 and 1.2%, respectively.

All procedures were conducted according to the guidelines of the Council Directive 86/609/EEC of 24 November 1986 on the protection of animals used for experimental and other scientific purposes (European Communities, 1986). In particular, for blood sampling each ewe was swiftly caught to minimize any excitement due to chasing and catching. There were always two trained persons involved in taking jugular blood samples. One person kept the animal and securely pulled the ewe’s head to the side to stretch his neck gently. The second person obstructed jugular blood flow by applying some pressure with the thumb in order to engorge the vein before puncturing it with a sterile needle.

Sampling and Analyses of Milk.
Ewes were milked using pipeline milking machines (Alfa Laval Agri, SE-147 21 Tumbas, Sweden). Animals were moved twice daily (0800 and 1500 h) to a milking parlor which was about 30 m away from the experimental building. Milk yield was recorded daily by means of graduated measuring cylinders attached to individual milking units. Milk samples, consisting of proportional volumes of morning and evening milk, were individually collected weekly in 200 mL sterile plastic containers after cleaning and disinfection of teats (70% ethyl alcohol) and discharging the first streams of foremilk. Milk samples were carried in our laboratory by means of transport tankers at 4°C. The following measurements were carried out on milk: pH, total protein, fat, and lactose content using an infrared spectrophotometer (Milko Scan 133B; Foss Electric, Hillerød, Denmark) according to the IDF (1990) standard, casein content (IDF, 1964); renneting characteristics (clotting time, rate of clot formation, and clot firmness after 30 min) using a Foss Electric Formagraph and the method of Zannoni and Annibaldi (1981); somatic cell count (SCC) using a Foss Electric Fossomatic 90 cell counter (IDF, 1995); and polymorphonuclear neutrophil leukocyte count (PMNLC), by means of direct microscopic count in milk smears stained with May-Grünwald-Giemsa (Carlo Erba Reagenti, Milan, Italy).

All ewes were examined daily to detect the presence or confirm the absence of signs of clinical mastitis, such as fever, pain, or gland swelling. A small quantity of milk was checked visually for signs of mastitis. At the beginning of the trial and fortnightly during the study period, the following bacteriological analyses were carried out on milk: enumeration of mesophilic bacteria (IDF, 1991a), psychrotrophs (IDF, 1991b), total and fecal coliforms (IDF, 1985). A subsample (0.01 mL) was taken from all milk samples with SCC > 106/mL and PMNLC > 30% of total somatic cells and cultured for mastitis-related pathogens. Presumptive Escherichia coli, staphylococci, and streptococci were determined and identified at species level as described earlier (Sevi et al., 1999a). Pseudomonas spp. were determined using Pseudomonas selective agar (Oxoid) and Pseudomonas aeruginosa was detected after 3 d of incubation on Pseudomonas agar F and Pseudomonas agar P (Oxoid) at 32 to 37°C. Samples were considered to be bacteriologically positive when at least 102 cfu/mL of a major pathogen (E. coli, Staphylococcus aureus, Streptococcus agalactiae, Strept. bovis, Pseudomonas aeruginosa) or 103 cfu/mL of a minor pathogen (CN-staphylococci, streptococci other than Strept. agalactiae and Strept. bovis) were isolated. If three or more bacterial species were cultured from a sample, the sample was considered to be contaminated (Fox et al., 1995). Sheep whose udders were without clinical abnormalities and whose milk was apparently normal but bacteriologically positive, with SCC > 106/mL and PMNL > 30% of somatic cells were considered to have subclinical mastitis when the same bacterial species was isolated from milk samples at least in two of three consecutive samplings (Andrew et al., 1983).

The body weights and body condition scores of the ewes (in a 6-point scale with 0 = thin and 5 = fat) were recorded at the beginning, at d 21 and 42 of the study period, after the morning milking but before feeding.

Calculations and Statistical Analysis.
Milk yield was corrected for fat content using the Cannas (1999) equation. The energy content of the milk was calculated using the Sebek and Everts (1992) equation: milk energy content (MJ/kg) = 0.0419 x F + 0.0159 x P + 0.0214 x L where F, P, and L are grams of fat, protein, and lactose per kilogram of milk, respectively. Maintenance requirements and the energy content of body weight gain were calculated according to AFRC (1993). The NE of the ration was calculated as the ratio between NE output (milk energy + maintenance energy + body weight gain energy) and DM intake. All the variables were tested for normal distribution using the Shapiro-Wilk test (Shapiro and Wilk, 1965). Behavioral data, plasma cortisol levels, and milk SCC and air and milk microorganism counts were transformed into logarithmic form to normalize their frequency distributions before performing statistical analysis. Milk and air variables were processed using ANOVA for repeated measures (SAS Inst. Inc., Cary, NC). The variation due to treatment, trial week, and their interaction was tested. Individual animal variation within treatment or sampling location within room was used as the error term. Pretreatment values of airborne microorganisms, and milk yield and quality were collected twice during the week before the commencement of the trial, which were used as covariates for air and milk variables. Preantigen injection values were used as covariates for antibody titers. Body weights, body weight changes, and the NE density of the ration were analyzed using ANOVA with one factor (treatment). Results are presented as the least squares means of the ewes in each treatment, and variability of the data is expressed as the SE of the mean response over the whole experimental period. A P-value of < 0.05 was considered significant, unless otherwise noted.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Implications
 Literature Cited
 
Two peaks were recorded for mean air temperatures in all the experimental rooms: the first occurred during wk 2 and the second, more marked, during wk 5 and 6 of the study (Table 1Go). In the course of the warmest weeks of the trial, averages of mean daily temperatures were 1.5 and 3°C higher in MVR and in LVR than in PROGR room. Changes in mean tempearature values among groups substantially reflected the differences in maximum air temperatures, because the magnitude and the duration of the thermal peak increased as the ventilation rate decreased. Indeed, maximum air temperatures were recorded around 1400 in all rooms, but the time during which temperatures remained over 30°C was more than 7 and less than 6 and 4 h daily in LVR, MVR, and PROGR rooms, respectively. The ventilation regimen had a negligible effect on minimum air temperatures, because the fan in the PROGR room worked little during the nighttime, relative humidity being not very often over 70%. The lowest averages of relative humidity were recorded during the last two trial weeks in all rooms. As for air temperatures, weekly averages of minimum relative humidity were similar among rooms, whereas maximum relative humidity levels, which occurred around 0600, were about 9 and 3 points higher in the LVR and in the MVR than in the PROGR room. Daily ranges of air temperature and relative humidity were the widest in the LVR and the narrowest in the PROGR room. Weekly averages of THI almost reached or exceeded 80 throughout the trial in the LVR room and during wk 3, 5, and 6 in the MVR room (Figure 1Go). Temperature-humidity index values little over 80 were recorded in the PROGR room during the last two wk of the experiment. Averages of minimum THI were similar across treatments during the first four trial weeks, while being about 4 points higher in the LVR and the MVR rooms than in the PROGR room during wk 5 and 6.


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  		Table 1. Averages of air temperature and relative humidity in rooms provided with a low (LVR), moderate (MVR), and programmed ventilation regimen (PROGR). Values are means ± SD
 


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  		Figure 1. Means ± SD of maximum (at the top) and minimum temperature-humidity index (THI) (at the bottom) in rooms provided with a low (LVR), moderate (MVR), and programmed ventilation regimen (PROGR).

 
Higher averages of maximum aerial concentrations of NH3 and CO2 (P < 0.005) were recorded in LVR and MVR rooms than in PROGR room (Table 2Go), during the morning sampling, while no differences in gas concentrations were found in the air sampled in the afternoon. Neither dust nor airborne microorganism concentrations were changed by treatment.


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  		Table 2. Least squares means ± SEM of air dust, gaseous pollutants, and microorganism concentrations as affected by a low (LVR), moderate (MVR), and programmed ventilation regimen (PROGR)
 
Respiration rates (Figure 2Go) and rectal temperatures (Figure 3Go) significantly increased (P < 0.05) in LVR compared to PROGR ewes during wk 2 and in LVR and MVR compared to PROGR animals during wk 3 of the study. Both parameters underwent significant changes through the trial (P < 0.001) according to variations in THI values.



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  		Figure 2. Least squares means ± SEM of respiration rate of ewes subjected to a low (LVR), moderate (MVR), and programmed ventilation regimen (PROGR).

 


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  		Figure 3. Least squares means ± SEM of rectal temperature of ewes subjected to a low (LVR), moderate (MVR), and programmed ventilation regimen (PROGR).

 
Ventilation regimen did not affect the activities of the ewes (Table 3Go), except for idling, which was higher in LVR than in PROGR group (P < 0.01), and for feeding activity, which took less time in LVR than in MVR (P < 0.05) and in PROGR animals (P < 0.01).


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  		Table 3. Least squares means ± SEM of time spent in each of behavioral categories by ewes when subjected to a low (LVR), moderate (MVR), and programmed ventilation regimen (PROGR). Data are presented as frequency of presentation for social and aggressive interactions and as percentages of total observation time for all the other behavioral traits
 
Ewe immune response to PHA injection (Figure 4Go) was similar across treatments. An effect of time of sampling (P < 0.01) was found for this parameter, skinfold thickness being lower at d 20 than at d 3 and 40 in all groups.



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  		Figure 4. Least squares means ± SEM of skinfold thickness after PHA injection in ewes subjected to a low (LVR), moderate (MVR), and programmed ventilation regimen (PROGR).

 
Ewes in the LVR group displayed lower averages of antibody response to OVA than MVR and PROGR animals (0.72 vs 0.95 and 1.01, P < 0.05 and P < 0.01, respectively). Significant effects of time (P < 0.01) and of treatment x time (P < 0.05) were observed for ewe humoral immune response. Time effect may be attributed to the fact that IgG concentrations increased in all groups after the second antigen injection. The interaction may be ascribed to the failure to find any significant differences in antibody titers at d 11 and 21, whereas the IgG concentrations were lower (P < 0.05) in LVR than in PROGR ewes at d 30 and 40 of the study (Figure 5Go).



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  		Figure 5. Least squares means ± SEM of antibody response to chicken egg albumin injection in ewes subjected to a low (LVR), moderate (MVR), and programmed ventilation regimen (PROGR).

 
The changes observed in the plasma levels of cortisol are presented in Figure 6Go. A significant effect of treatment was not found (P = 0.138), whereas both time of sampling and the interaction of treatment x time influenced cortisol response to ACTH injection (P < 0.001 and P < 0.05, respectively). In fact, when sampled 60 min after ACTH injection, LVR ewes displayed significant higher plasma cortisol levels than PROGR (P < 0.01) and MVR animals (P < 0.05) (98.1 vs 68.2 and 76.2 ng/mL, respectively). In addition, for all the animals the peak of the cortisol response was reached 60 min after ACTH injection (P < 0.001), whereas at 120 and 240 min cortisol levels were not different from those detected before injection.



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  		Figure 6. Least squares means ± SEM of plasma cortisol levels after porcine ACTH injection in ewes subjected to a low (LVR), moderate (MVR), and programmed ventilation regimen (PROGR).

 
LVR ewes gave about 30% lower yields of milk than PROGR animals during wk 4 and 5 (P < 0.05), while nutritional properties of milk were not changed by ventilation regimen (Table 4).

The coagulating behavior of milk was not affected by treatment (Table 5Go). Somatic cell and mesophilic and psychrotrophic counts were similar across groups, whereas LVR and MVR treatments resulted in higher total coliform counts than PROGR treatment (P < 0.05 and P < 0.01, respectively). MVR ewes also had a higher amount of fecal coliforms in their milk than LVR (P < 0.05) and PROGR animals (P < 0.01). Regardless to ventilation regimen, renneting parameters deteriorated with the advancement of the trial and so did the hygienic quality of milk.


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  		Table 5. Least squares means ± SEM of somatic cell count (SCC), renneting parameters, and bacteria count in ewe milk as affected by a low (LVR), moderate (MVR), and programmed ventilation regimen (PROGR)
 
Daily DM intake was 3.044, 3.032, and 3.011 kg per ewe in PROGR, MVR, and LVR groups, respectively. The LVR ewes lost weight, and their body condition deteriorated during the 0- to 21-d period, while PROGR animals had the highest gains in weight and in body condition score (P < 0.05), and MVR ewes displayed intermediate values for both parameters (Table 6Go). Differences among LVR and PROGR groups disappeared during the 22- to 42-d period. Due to reduced weight gain and yield of milk, LVR ewes displayed a lower Net energy (NE) of the ration (P < 0.01) than PROGR animals during the 0- to 21-d period and than PROGR and MVR ewes during the 22- to 42-d period.


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  		Table 6. Least squares means ± SEM of body weight and body condition score changes and of NE of the ration in ewes as affected by a low (LVR), moderate (MVR), and programmed ventilation regimen (PROGR)
 
There were no cases of clinical mastitis during the study period. One case of subclinical mastitis was detected in LVR group with infection considered to have set in at d 35. Thirteen bacteriologically positive milk samples were found almost equally split among groups (5 in LVR and 4 in both MVR and PROGR groups, respectively). Escherichia coli and coagulase-negative (CN) staphylococci, primarily Staph. chromogenes, constituted the majority of bacteria isolated: they were isolated from 8 and 7 of the 13 bacteriologically positive milk samples, respectively. Streptococcus bovis and Pseudomonas aeruginosa were detected in 2 and 1 milk samples, respectively. Staphylococcus aureus and Strept. agalactiae were not found in any milk sample.


   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Implications
 Literature Cited
 
In the PROGR room, the fan operated about 70% of time during late morning and early afternoon, being started up by the air temperature sensor, and the rest of time during night-time, being switched on by the humidity sensor. Due to the fan intermittently working, ewes from the LVR group (and from MVR to a lesser extent), underwent two critical periods daily. One occurred in early morning, due to rising relative humidity and gaseous pollutant concentrations, and the other in early afternoon, depending on the increase in air temperature and THI.

Aerial concentrations of dust and microorganisms were not significantly affected by ventilation regimen. This is not surprising, because aerial dust, which is also the main carrier of microorganisms, has a very complex behavior (Wathes, 1992). Indeed, small particles may remain in the air for a long time, with elimination only achieved by sedimentation, and then return to the air relatively quickly by dispersion (Hartung, 1994). In addition, there is evidence that ventilation systems are more significant, but not the only factor that influence the concentration of airborne particulates in animal houses. Stocking density, airspace, group size, feeding system, and litter management also play a role in modifying the amount of particulates suspended in the air (Hartung, 1989). All these factors were kept strictly similar in all the experimental rooms.

Increased respiration rate is the first reaction of animals exposed to air temperatures exceeding their thermoneutral zone (Kamal, 1975). If this and the other physiological mechanisms fail to balance the excessive heat load, the body temperature rises, and the animal enters the acute phase of heat stress (Habeeb et al., 1992). Sevi et al. (2001) found that prolonged exposure to maximum air temperatures over 30°C and to THI values over 80, prevent lactating ewes from maintaining their thermal balance. Accordingly, in the present trial, respiration rates and rectal temperatures significantly increased whenever THI exceeded 80. This occurred in LVR animals during wk 2, in both LVR and MVR ewes during wk 3, and in all groups during wk 5 and 6. Under high ambient temperatures, animals benefit from ventilation directly via the heat being removed from their body surface and indirectly via the lowering of air temperature, relative humidity, and gaseous pollutant levels. Thus, the failure to find an effect of the ventilation regimen during the warmest weeks of the trial may be partly ascribed to a reduction in the effectiveness of heat removing through convection mechanisms, because of a drop in the thermal gradient between ewe body surfaces and the moving air. In addition, it is likely that the higher productivity and, consequently, the greater heat production, probably also had a role in minimizing differences in RR and RT between PROGR and the other two groups during the last two trial weeks.

Dry matter intake was substantially similar across treatments. Along with our results, Muna and Abdelatif (1992) and Sevi et al. (2001) found that any time availability of feed not very rich in fiber in the trough can minimize the adverse effect of high heat load on sheep feed intake.

Nevertheless, changing the time of feeding to late afternoon and night may be a suitable strategy for animals to reduce their heat load during the warmest hours of the day (Brosh et al., 1998). This may explain why LVR ewes were observed spending 67 to 74% less time in feeding activity than MVR and PROGR animals in the morning.

Reduction in active behaviors may help animals to reduce their heat production under high air temperatures. Indeed, decreased levels of activity has been found to have a definite thermoregulatory purpose in sheep (Shreffler and Hohenboken, 1980; Sevi et al., 2001). This accounts for idling taking 37 to 64% more time in LVR than in MVR and PROGR ewes. However, due to relatively short observation times, conclusive results cannot be provided on the effect of ventilation regimen on ewe behavioral responses.

In general, RR, RT, and behavioral data suggest that MVR and even PROGR animals underwent temporary high heat load situations, whereas LVR had to experience excessive heat load for a large part of the day.

Differences in plasma cortisol levels between LVR and the two other groups support this hypothesis. The increase in the plasma cortisol levels, as a consequence of the activation of the hypothalamic-pituitary-adrenal axis, is one of the best known and consistent neuroendocrine responses to stress (Hashizume et al., 1994; Grasso et al., 1999; Sevi et al., 1999b). In the welfare assessment of farmed animals, the administration of exogenous ACTH is aimed to stimulate the adrenal secretion of cortisol, whose release may be strengthened by the existence of concurrent stressful events. Indeed, there is evidence that the graded cortisol responses to stress can be attributed to both the relative stressfulness and the cumulative action of each stressor (Mears and Brown, 1997; Sevi et al., 1999b). Hence, capture, handling, ACTH administration, and venipuncture may account for the increase in plasma cortisol levels occurring in all groups 60 min after they were injected with ACTH. The higher cortisol response found in LVR group at this time suggests that the physiological disturbance from reduced ventilation acted as an additional stressor on the ewes in this group.

Immune functions have been recognized as reliable indicators of animal welfare and disease resistance (Minton, 1994). Attempts to quantify the role of humoral immunity in protection and to determine whether genetic selection for altered immune responses would be possible also have been made by some research groups (Mallard et al., 1982; Burton et al., 1989). An immunosuppressive effect of increased glucocorticoid secretion is well documented (Minton et al., 1992; Oldham and Howard, 1992; Grasso et al., 1999). In the present study, humoral but not cell-mediated immunity was affected by ventilation regimen, with LVR ewes displaying lower averages of IgG concentrations than PROGR animals. This might seem rather surprising, because it is known that T and B lymphocytes act as parts of an integrated system (Tompkins and Tompkins, 2000). However, Napolitano et al. (1995), when assessing the effect of early transition to artificial rearing on lamb immune response, found a lower IgG concentrations in artificially reared than in dam-suckled animals, though no difference in the proportion of lymphocytes had been observed. These authors argued that the altered humoral response in the lambs moved early to artificial rearing depended on a lack of cytokines stimulating B cell activity, rather than on the reduced number of B cells. Indeed, there is evidence that cytokines play a major role in proliferation and differentiation of B lymphocytes to plasma cells, which secrete the antibody molecules (Elgert, 1996).

The small but significant reduction in cell-mediated immunity observed in all groups when the second skin test was performed (d 20) is not easy to interpret. A tentative explanation might be in the rapid rise of mean air temperatures (3 to 4°C), which occurred in all rooms during the second trial week. A role of cortisol in this was not excluded. It is known that plasma cortisol levels rapidly increase after the exposure of animals to high air temperatures and then gradually decline, because of its thermogenic functions (Habeeb et al., 1992). It has been established that the release of cortisol has a substantial effect on the T-cell system (Harbuz and Lightman, 1992). This may account for skinfold thickness raising again when the ewes were retested at d 40. Sevi et al. (2001) found that the immune reactivity to PHA injection markedly decreased in ewes exposed to air temperatures swiftly rising from 23 to 28°C and then remained unchanged or slightly rose again for the rest of the exposure duration and even after further increments in the air temperature.

High heat loads may lead to energy deficit, even when they do not induce a marked reduction of feed intake in animals. It has been estimated that only the rise in respiration rate may result in a 7 to 25% increase in energy requirements for maintenance in animals exposed to high air temperatures (NRC, 1981). Under these conditions, the availability of sufficient nutritional reserves may help lactating animals to cope with increased energy demand for thermoregulation without affecting milk yield and constituents (Ronchi et al., 1997; Sevi et al., 2001).

During the first 3 wk of the present trial, LVR ewes widely drew on nutrients from their body reserves to sustain milk production. This led to marked loss of weight and deterioration of body condition. Conversely, during the last three weeks of the study period, LVR ewes recovered weight and improved their body condition, while yielding markedly less milk than MVR and PROGR animals. Such an event might be ascribed to both a reduction in the availability of body substrates, and the progressive change in metabolic and endocrine status of ewes with the advancement of lactation. This led to a greater portion of nutrients being addressed to body tissues at the expense of mammary gland (Hart, 1983; Sevi et al., 1998).

Only one case of subclinical mastitis was detected in LVR group. In general, few bacteriologically positive milk samples were found in all groups, and the bacterial load of the milk was quite low, mesophilic counts ranging from 203 to 307 x 103 cfu/mL of milk in LVR and PROGR groups, respectively, and coliform counts never exceeding 1 x 103 cfu/mL of milk. In addition, the number of psychrotrophic microorganisms was always < 1 x 108 cfu/ml milk, a level which Yan et al. (1983) had reported as having an adverse effect on cheese yield and quality. Undoubtedly, the scrupulous control of sanitation of housing, equipment, and personnel had a role in minimizing the impact of the ventilation regimen on the hygienic quality of milk and the udder health of ewes.


   Implications
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
Literature Cited
 
Sheep are known as one of the most heat-resistant species among farmed animals. In addition, due to reproductive seasonality, ewes are generally in their later stage of lactation during the warmest period of the year. Such peculiarities may contribute to minimize the impact of high summer temperatures on ewe welfare and milk yield. In our study, a fan ventilation system programmed to operate over upper critical air temperature and relative humidity proved to be economically unattractive in dairy sheep housing. In fact, it involved about a threefold greater energy cost and did not lead to remarkable improvements of ewe welfare and productivity compared to an intermittent regimen split in 25-min/h ventilation cycles during the warmest hours of the day. A further reduction of ventilation cycles to 12.5 min/h resulted in ewe displaying altered behavior, immune and endocrine responses, and giving lower yields of milk. Our findings suggest that a ventilation regimen, providing ventilation cycles during the warmest hours of the day and the night at a mean ventilation rate of 66 m3/ewe per h may adequately sustain the welfare and performance of lactating ewes raised in Mediterranean climates during summer.


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  		Table 4. Least squares means ± SEM of yield, protein, casein, and fat content of ewe milk as affected by a low (LVR), moderate (MVR), and programmed ventilation regimen (PROGR)
 

   Footnotes
 
1 The authors would like to thank John Eddison for revision of the English language and M. A. Mongelli and F. D’Emilio for expert technical assistance. Back

Received for publication February 18, 2002. Accepted for publication April 26, 2002.


   Literature Cited
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 


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