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Poult Sci 2008. 87:56-60. doi:10.3382/ps.2007-00328
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IMMUNOLOGY, HEALTH AND DISEASE

Hematology and Enzyme Histochemistry of the Peripheral Blood Leucocytes in Rock Partridges (Alectoris graeca)

H. H. Dönmez1 and E. Sur

Department of Histology and Embryology, Veterinary Faculty, Selcuk University, 42031, Konya, Turkey

1 Corresponding author: hdonmez{at}selcuk.edu.tr


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The purpose of this study was to determine the percentages of {alpha}-naphthyl acetate esterase (ANAE)-positive and acid phosphatase (ACP)-positive peripheral blood lymphocytes (PBL) and the percentages of leukocytes in the rock partridge at different ages. Blood samples obtained from the vena basilica of 18 healthy rock partridges (Alectoris graeca) at 1 d, 5 wk, and 12 wk of age were used. Mean percentages of ANAE-positive PBL for the 3 age groups were 37, 29.83, and 47.83% for 1 d, 5 wk, and 12 wk of age, respectively. Heterophils also gave ANAE-positive reactions. Mean percentages of ACP-positive PBL for the 3 age groups were 70, 81, and 86.1% for 1 d, 5 wk, and 12 wk of age, respectively. Although monocytes showed a diffuse granular staining pattern, heterophils displayed a weak positive reaction for ACP. Thrombocytes showed a small granular staining pattern. This study contributes by broadening the hematological research on avian species and provides a guideline for identifying blood cells in the rock partridge.

Key Words: rock partridge • {alpha}-naphthyl acetate esterase • acid phosphatase


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The morphological characteristics of avian blood cells are heterogeneous. Enzyme histochemical tests have practical value for the study of immature blast cells and lymphocytes, because Romanowsky-stained films might be insufficient for identifying the differentiation and maturation features of the cells (Catowsky, 1991). {alpha}-Naphthyl acetate esterase (ANAE) and acid phosphatase (ACP) activities have been used as cytochemical markers to identify neutrophils and monocytes, as well as lymphocyte subtypes (Osbaldiston et al., 1978; Sur et al., 2004). These enzymes are supposed to participate in the activation and proliferation of leukocytes (Kaczmarczyk et al. 2004), whereas in granulocytes (Kaczmarczyk et al. 2005) and fish thrombocytes (Passantino et al., 2005), they participate in the destruction of phagocytosed pathogenic microorganisms.

{alpha}-Naphthyl acetate esterase is a lymphocyte lysosomal enzyme (Knowles et al., 1978) that has been demonstrated in mature and immunocompetent T lymphocytes. The positivity of ANAE has widely been used to differentiate T and B lymphocytes and monocytes in various species, including chickens (Maiti et al., 1990), ostriches (Ergün et al., 2004a), turkeys (Ergün et al., 2004b), painted storks (Salakij et al., 2003), cattle (Celik et al., 1994), dogs (Sur et al., 2003), and Angora rabbits (Özcan, 2005). The ANAE technique has been found useful in differentiating granulocytic, monocytic, and lymphocytic leukemias (Osbaldiston et al., 1978) and has also been used to detect these cells in malignant nonlymphoid human tumors (Svennevig, 1980). The enzyme is assumed to be responsible for the cytotoxic effects of T lymphocytes and the phagocytic activity of monocytes (Mueller et al., 1975).

Acid phosphatase is a member of the acid hydrolases. The enzymatic activity is gained at early stages of T-lymphocyte maturation in the human thymus (Basso et al., 1980). The reaction is positive in fetal thymocytes, and it has also been shown to persist in some of the mature T lymphocytes localized in the thymus-dependent T-cell areas of lymphoid tissues from humans and rodents (Kaplow and Burstone, 1964; Catowsky et al., 1974; Catowsky, 1991). However, ACP is considered to be related to B-lymphocyte maturation and is regarded as a B-cell marker in the chicken (Graczyk, 1987; Sur, 2001), because the enzyme is commonly present in lymphocytes originating from the bursa of Fabricius. The enzyme has diagnostic value in the differential diagnosis of lymphoproliferative disorders (Wehinger and Möbius, 1976), and its reaction increases dramatically in almost all types of acute and chronic T-cell lymphoproliferation humans (Catowsky, 1991).

Partridge breeding is mostly done to provide birds for hunting, but breeding for meat production has become widespread in recent years (Kirikci et al., 2004). However, basic hematological values in the histochemistry of peripheral blood cells have not been described in these species. The purpose of this study was to determine the percentages of ANAE- and ACP-positive PBL and the differential leukocyte counts in the rock partridge at different ages.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Blood samples obtained from the vena basilica of 18 healthy rock partridges (Alectoris graeca) at 1 d, 5 wk, and 12 wk of age were used. Each age group consisted of 6 animals. Two blood smears for each staining procedure from each partridge were prepared and air-dried. Two blood smears from each animal were stained with May-Grünwald-Giemsa stain according to a standard staining method (Konuk, 1981).

To determine ANAE activity, blood smears were fixed in a glutaraldehyde-acetone solution at –10° for 3 min, rinsed in distilled water, and then air-dried. An incubation solution was prepared by mixing 20 mg of substrate, {alpha}-naphthyl-acetate (N-8505, Sigma, Steinheim, Germany) dissolved in 0.8 mL of acetone (Merck, Darmstadt, Germany), 4.8 mL of hexazotized pararosaniline [hexazotization was performed by mixing equal volumes (2.4 mL each) of 4% sodium nitrite (Merck) and 2% pararosaniline (Merck)], and 80 mL of PBS (pH 5). Final pH of the incubation solution was adjusted to 5.8 with 1 N NaOH, and the solution was filtered. After a 4-h incubation at 37°C, the smears were rinsed 3 times in distilled water, and nuclei were stained for 20 min in 1% methyl green prepared in acetate buffer (pH 4.2). Control specimens were prepared by incubating the smears in incubation solution without {alpha}-naphthyl acetate (Celik et al., 1991).

Acid phosphatase was demonstrated by the method of Goldberg and Barka (1962) with minor modifications. In this technique, blood smears were fixed in formal-calcium at +4°C for 10 min, and the smears were rinsed 3 times in distilled water. An incubation solution was prepared by mixing 10 mg of naphthol AS-BI phosphate (N-2125, Sigma) dissolved in 1 mL of N,N-dimethyl formamide (Sigma), 13 mL of distilled water and 1.6 mL of hexazotized pararosaniline (prepared as in the ANAE incubation solution), and 5 mL of Michaelin’s veronal acetate buffer (pH 5). Final pH of the solution was adjusted to 5.0 with 1 N NaOH, and the solution was filtered. After a 1-h incubation at 37°C, the slides were rinsed 3 times in distilled water, and the nuclei were stained for 20 min with 1% methyl green prepared in acetate buffer (pH 4.2). The incubation solution for the control smears did not contain naphthol AS-BI phosphate.

All specimens were examined under a light microscope (Leica DM 2500, Leica Microsystems GmbH, Wetzlar, Germany). The May Grünwald-Giemsa-stained smears were used to determine differential leukocyte counts. In each of the specimens demonstrating ANAE and ACP, 200 lymphocytes were counted and positivity rates were expressed as the percentage of counted cells.

The data were analyzed by 1-way ANOVA (SPSS, 1999). When the F-values were significant, Duncan’s multiple-range tests was performed. Results were considered significant when P-values were less than 0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
In the blood smears examined, most of the peripheral blood lymphocytes (PBL) staining ANAE positive showed 1 or 3 dot-like brownish granules (Figure 1aGo, arrow); however, a few positive PBL showed 5 to 8 brownish granules (Figure 1bGo, arrow). Heterophils gave positive reactions, and the positivity was shown by 1 to 3 dot-like brownish granules (Figure 1aGo, letter H). Monocytes showed a weak, diffuse staining pattern (Figure 1cGo, letter M). Erythrocytes and thrombocytes (Figure 1bGo) gave negative enzymatic reactions. Mean ANAE positivities of PBL for the 3 age groups were 37, 29.83, and 47.83% for 1 d, 5 wk, and 12 wk of age, respectively.


Figure 1
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  		Figure 1. {alpha}-Naphthyl acetate esterase (ANAE) demonstrated in peripheral blood cells in rock partridges. a) {alpha}-Naphthyl acetate esterase-positive peripheral blood lymphocytes (arrow), and heterophils (letter H; b) 5 to 8 dot-like ANAE positivities in PBL (arrow), ANAE-negative PBL (*), and ANAE-negative thrombocytes (letter t); and c) a monocyte (letter M) showed a weak diffuse staining pattern were observed in a 5-wk-old rock partridge.

 
A large number of PBL have shown strong ACP positivity (Figure 2aGo, arrows). The PBL having 1 to 4 pinkish cytoplasmic granules were considered ACP positive. Monocytes showed a diffuse granular staining pattern (Figure 2bGo, letter M). Heterophils displayed a weak positive reaction for ACP (Figure 2a and 2bGo, letter H). Thrombocytes showed a small granular staining pattern (Figure 2aGo, letter t). Erythrocytes gave a negative enzymatic reaction. Mean percentages of ACP-positive PBL for the 3 age groups were 70, 81, and 86.1% for 1 d, 5 wk, and 12 wk of age, respectively. The mean ratios (mean ± SE) of the ANAE-positive and ACP-positive PBL and differential leukocyte counts are shown in Table 1Go.


Figure 2
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  		Figure 2. Acid phosphatase (ACP) demonstrated in peripheral blood cells in rock partridges. a) Acid phosphatase-positive peripheral blood lymphocytes (PBL; arrows), a thrombocyte (letter t), and a weak positive heterophil (letter H); b) a monocyte (letter M) showing a diffuse granular staining pattern; and c) an ACP-negative PBL (arrow) were observed in a 5-wk-old rock partridge.

 

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  		Table 1. Mean ratios (mean ± SE) of the {alpha}-naphthyl acetate esterase (ANAE)-positive and acid phosphatase (ACP)-positive peripheral blood lymphocytes (PBL) and differential leukocyte counts
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Enzyme histochemical techniques have largely been used to identify mature T lymphocytes to differentiate types of leukocytes and leukemia cells (Inoue et al., 1991) and some hematological disorders (Kulenkampff et al., 1977; Sur et al., 2003). In the lymphoid leucosis of cattle (Kajikawa et al., 1983), in Marek’s disease in chickens (Jeurissen et al., 1989), and in distemper in dogs (Sen et al., 2002), significant changes have been reported either in PBL percentages or in their enzymatic positivity rates. Sen et al. (2002) determined changes in the enzymatic positivity profile of PBL through the development of experimentally induced canine distemper virus infections, in which a sharp decrease was observed in the percentages of ANAE and ACP. Izci et al. (2002) reported that total percentages and ANAE positivity rates of PBL in dogs with keratoconjunctivitis sicca were decreased by using ophthalmically administered 2% cyclosporine. These studies (Izci et al., 2002; Sen et al., 2002) demonstrated that the rates of ANAE-and ACP-positive PBL might be used as a laboratory aid in the early diagnosis and monitoring of specific treatments for different diseases.

{alpha}-Naphthyl acetate esterase activity has been demonstrated in several reports on avian species (Asti et al., 1999; Dönmez et al., 2002; Salakij et al., 2003; Ergün et al., 2004a,b; Sur et al., 2004). However, the demonstration of ANAE activity in the partridge is not available in the literature. The patterns of ANAE staining in peripheral blood cells of the partridge seem to agree with those found in other avian species (Salakij et al., 2003; Ergün et al., 2004a,b; Sur et al., 2004). A granular staining pattern with 1 to 8 specific reddish-brown granules was observed in T lymphocytes, but B lymphocytes gave a negative reaction. {alpha}-Naphthyl acetate esterase is a specific enzyme for T lymphocytes (Asti et al., 1999). Positive granular ANAE staining is specific to lymphocytes and has been used successfully as a cytochemical marker for identifying mature T lymphocytes (Ergün et al., 2004a). The granulocytes gave a granular-positive ANAE staining reaction in the partridge in this study. Previously, the granulocytes were shown to give a positive reaction in chickens (Asti et al., 1999), painted storks (Salakij et al., 2003), and turkeys (Ergün et al., 2004b), and a weak diffuse positivity in pheasants (Sur et al., 2004), whereas these cells were ANAE negative in ostriches (Ergün et al., 2004a) and in some mammalian species, such as pigs (Osbaldiston et al., 1978), cats (Yörük et al., 1998), dogs (Sur et al., 2003), and humans (Osbaldiston et al., 1978). In monocytes, a weak diffuse staining pattern was noted.

There is a good correlation between the proportion of T cells and the percentage of ANAE-positive lymphocytes in the chicken (Maiti et al., 1990), pheasant (Sur et al., 2004), turkey (Ergün et al., 2004b), and ostrich (Ergün et al., 2004a). In this study, the percentages of ANAE-positive lymphocytes were 37.0 ± 1.15, 29.83 ± 2.09, and 47.83 ± 3.63% at 1 d, 5 wk, and 12 wk of age, respectively. The positivity of ANAE was significantly higher at 12 wk of age than in the other age groups. Sur (2001) found the proportion of ANAE-positive PBL in chickens to be 37.2% at hatching and 55.6% at 4 wk after hatching. Dönmez et al. (2002) reported that 54.4% of the PBL were positive for ANAE in healthy chickens. Sur et al. (2004) reported 36.82 and 33.73% ANAE-positive PBL for young and adult pheasants, respectively. {alpha}-Naphthyl acetate esterase-positive PBL values of 51.8% in turkeys (Ergün et al., 2004b) and 59.3% in ostriches (Ergün et al., 2004a) have also been reported. These results showed that the ANAE positivity of PBL in partridges was similar to that of pheasants but different from that of other avian species, except chickens at hatching.

Studies of ACP in avian species are lacking, and no studies of ACP in rock partridges are available in the literature. In this study, a large number of lymphocytes showed a strong ACP positivity. Monocytes showed a diffuse granular positivity, heterophils showed a weak positivity, and thrombocytes showed a small granular staining pattern. Sur (2004) reported that PBL of merino sheep displayed 1 to 3 pinkish granular staining patterns. Sur et al. (2003) reported that PBL and monocytes of dogs of the Kangal breed (Anatolian shepherd dogs) showed a strong ACP positivity; however, neutrophils showed a weak ACP positivity.

The proportions of ACP-positive PBL were 70.5, 81.0, and 86.17% at d 1, wk 5, and wk 12 of the experiment, respectively. Sur (2001) reported that the proportions of ACP-positive lymphocytes in chickens were 63.7% at hatching and 71.5% at 4 wk after hatching. The proportion of ACP-positive lymphocytes was approximately 32% in sheep (Sur, 2004) and 39% in Kangal dogs (Sur et al., 2003). It has been pointed out in histochemical studies that T lymphocytes give an ACP-positive reaction in mammalian species (Goldberg and Barka, 1962; Yang et al., 1982; Sur et al., 2003; Sur, 2004); however, bursa-dependent lymphocytes give an ACP-positive reaction in avian species (Moriya and Ichikawa, 1989; Sur and Celik, 2003; Sur, 2004). These results showed that there was a negative correlation between ANAE-positive lymphocytes and ACP-positive lymphocytes in rock partridges. It could be said that T lymphocytes give an ANAE-positive reaction in rock partridges, whereas B lymphocytes give an ACP-positive reaction.

The proportions of lymphocytes were approximately 56, 69, and 53.5% in rock partridges of 3, 6, and 14 wk of age, respectively (Keskin et al., 2002); 45.2% in painted storks (Salakij et al., 2003); 56 and 52.9% in young and adult pheasants, respectively (Sur et al., 2004); and 16.3 and 50.1% in chicks on the first day of hatching and at 4 wk of age, respectively (Sur, 2001). The proportions of heterophils were approximately 35.3, 25, and 37% in rock partridges of different ages (Keskin et al., 2002); 43.6% in painted storks (Salakij et al., 2003); and 30 and 41% in young and adult pheasants, respectively (Sur et al., 2004). In this study, we determined that the proportions of lymphocytes in rock partridges were 47, 49, and 46% at hatching, 5 wk, and 12 wk of age, respectively. The proportions of heterophils in rock partridges were 33, 46, and 49% at hatching, 5 wk, and 12 wk of age, respectively.

In conclusion, these results provide comparative hematological data and a guide for identifying blood cells in the rock partridge. This may be beneficial for further immunological and functional studies and could be used as a laboratory aid in the early diagnosis and monitoring of specific treatments for different diseases.

Received for publication August 7, 2007. Accepted for publication September 10, 2007.


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