Jinlong ZHANG,Xinhua LI,Shengjun JIA

1.College of Veterinary Medicine,Yangzhou University/Jiangsu Co-innovation Center for the Prevention and Control of Important Animal Infectious Diseases and Zoonoses,Yangzhou 225009,China;

2.Poultry Institute,Chinese Academy of Agricultural Sciences,Yangzhou 225003,China

Observation on Activities of Air Sac in Opened Body Cavity of Chicken

Jinlong ZHANG1*,Xinhua LI2,Shengjun JIA1

1.College of Veterinary Medicine,Yangzhou University/Jiangsu Co-innovation Center for the Prevention and Control of Important Animal Infectious Diseases and Zoonoses,Yangzhou 225009,China;

2.Poultry Institute,Chinese Academy of Agricultural Sciences,Yangzhou 225003,China

The body cavity of chicken under anesthesia was opened,and then the state of breathing and activities of air sac wall were observed.The results showed that,although the body cavity was opened,the chicken could still breathe.When the chicken breathed in,the chest sidewall,thoracico-abdominal diaphragm and lung diaphragm all initiatively became larger,inflating the prethoracic and metathoracic air sacs;the cervical,clavicular and abdominal air sac walls all contracted,shrinking the air sacs.When the chicken breathed out,the chest sidewall,thoracico-abdominal diaphragm and lung diaphragm initiatively contracted,shrinking the prethoracic and metathoracic air sacs;the cervical,clavicular and abdominal air sac walls all expanded,expanding the air sacs.Therefore,the chicken could still breathe after the body cavity was opened.When the chicken breathed in,the prethoracic and metathoracic air sacs were all expanded,and the air flowed from the cervical,clavicular and abdominal air sacs and respiratory tract to the prethoracic and metathoracic air sacs through the lung,shrinking the cervical,clavicular and abdominal air sacs;when the chicken breathed out,the prethoracic and metathoracic air sacs walls all contracted,and the air was extruded from the prethoracic and metathoracic air sacs into the cervical,clavicular and abdominal air sacs and respiratory tract trough the lung,expanding the cervical,clavicular and abdominal air sacs.During the entire breathing process,the prethoracic and metathoracic air sacs all can expand and shrink initiatively,making the air flow though the lung.

Chicken;Body cavity;Breath;Air sac

A ir sac is a peculiar organ in birds.It is a mucosa membrane sac formed by bronchi outside the lung[1-2].During the breathing process,the lungs of birds can not expand and contract like those of mammals.For the birds,the gas exchange is achieved though the activities of air sac[3-5].So the activities of air sac play an important role in the breathing process of birds.How the air sac participates in the breathing of birds is still controversial[6-8].At home and abroad,it has been relatively widely recognized that when someone inhales,the body wall is expanded,so the negative pressure in the body cavity is increased,inflating various air sacs.The air flows through the respiratory tract and enters the primary bronchi of lung.One part of the fresh air enters directly the metathoracic and abdominal air sacs through the primary bronchi of lung and is stored there.The other part of the fresh air enters the secondary and tertiary bronchi for gas exchange.The exchanged gas is extruded by the newlyentered air to the cervical,clavicular and abdominal air sacs and is stored there.When some exhales,the body chest is contracted,shrinking all the air sacs.At that time,the fresh air stored in the metathoracic and abdominal air sacs enters the lung for gas exchange. The exchanged gas in the cervical, clavicular and prethoracic air sacs and lung is exhaled though the respiratory

Materials and Methods

A total of 4 healthy adult chickens were selected.They were deeply anesthetized by the Sumianxian injection produced by the College of Veterinary Medicine,Jilin University.The prethoracic skin was cut open.The connective tissues were carefully removed,and the air sacs were kept intact.The activities of front walls of cervical and clavicular air sacs were observed.The abdominal wall was cut open longitudinally along the ventral midline,and then the activities of free wall of abdominal air sac and thoracico-abdominal diaphragm were observed.Then,the trachea was held with a hemostatic clamp for a few seconds,within which the activities of various air sacs were observed. Among the 4 chickens,the thoracicoabdominal diaphragm of abdominal air sac on one side of one chicken was damaged,and the activities of chest wall of abdominal air sac and lung diaphragm on that side were observed from the inner side under the assistance of torch lighting;the free wall of abdominal air sac of one chicken was damaged,and the activities of the other walls were observed;the front wall of cervical air sac of one chicken was damaged,and the activities of the other walls were observed from the inner side under the assistance of torch lighting;the front wall of clavicular air sac of one chicken was damaged,and the activities of the other walls were observed from the inner side under the assistance of torch lighting.During the experimental process,a feather or a certain amount of cotton was placed near the nostrils of one chicken so as to determine the inhalation and exhalation.Finally,all the chickens were bled to death.

Results and Analysis

State of breathing after the body cavity of chicken was opened

The body cavities of chickens under anesthesia were opened.It was fount that the breath of chickens was not affected significantly,and the chickens still could breathe normally.

Activities of various air sac walls after the body cavity of chicken was opened

As shown in Fig.1a,when the chicken breathed in,with the movement of chest sidewall forward and the expanding of chest sidewall toward back and belly,the thoracico-abdominal diaphragm expanded outward the belly.The spacing between the thoracico-abdominal diaphragm and chest side wall was enlarged.The free wall of abdominal air sac contracted;the front wall of clavicular air sac contracted inward,and the subcutaneous diverticula of clavicular air sac located in the rear of shoulder joint became smaller;the front wall of cervical air sac also contracted.As shown in Fig.1b,when the chicken breathed out, with the movement and shrinking of chest sidewall backward and inward, the thoracico-abdominal diaphragm was first relaxed,and then it was contracted and shrunk.At the end of exhalation,the spacing between the thoracico-abdominal diaphragm and chest sidewall became smaller.The free wall of abdominal air sac expanded outward.The front wall of clavicular air sac also expanded outward,and subcutaneous diverticula of clavicular air sac located in the rear of shoulder joint became larger.The front wall of cervical air sac expanded outward. During the blocking of trachea,the movement ranges of chest side wall and air sac wall were all increased.No obvious changes were found in other parts.

Activities of some air sac walls after the others were destroyed

When the chicken breathed in, with the movement of chest side wall frontward and outward,the lung diaphragm was driven frontward and outward,and the rib-lung muscle relaxed;the frontward and outward movement of chest sidewall enlarged the joint angle between vertebrosternal ribs and sternal ribs,and the area of chest sidewall was enlarged,driving the sternum move frontward and downward.The non-free wall of abdominal air sac was fixed.With the frontward and downward movement of sternum and frontward and outward movement of chest sidewall,the intrathoracic organs(i.e.heart)were extruded forward,narrowing slightly the spacing between walls of cervical and clavicular air sacs.

When the chicken breathed out, with the backward and inward movement of chest sidewall,the lung diaphragm relaxed,and under the action of resilience of lung diaphragm itself and contraction of rib-lung muscle,the lung diaphragm shrank backward and inward;the chest sidewall contracted backward and inward,narrowing the joint angle between vertebrosternal ribs and sternal ribs and the area of chest sidewall,and the sternum was pulled backward and upward.The non-free wall of abdominal air sac was fixed.With the backward and upward movement of sternum and backwardand inward movement of chest sidewall,the intrathoracic organs were pulled backward,enlarging slightly the spacing between walls of cervical and clavicular air sacs.

Conclusions and Discussion

Activities of air sacs after the body cavity of chicken was opened

During the breathing process,the lungs of birds cannot expand and contract like those of mammals and the gas exchange is achieved by the activities of air sacs[2,9].After the body cavity was opened,the chicken could still breathe.It was suggested that the air sacs of chicken were still functioning.When the birds breathe in,the air sacs should be inflated[3].In this study, the activities of abdominal,cervical and clavicular air sacs showed that these air sacs were all shrunk during the inhalation,but all expanded during the exhalation.

During the inhalation,the abdominal,cervical and clavicular air sacs all shrank,and the extruded air from these air sacs and the inhaled air from the respiratory tract flowed into the prethoracic and metathoracic air sacs probably through the lung,expanding the prethoracic and metathoracic air sacs.Similarly,during the exhalation, the prethoracic and metathoracic air sacs all shrank.It was indicated that the prethoracic and metathoracic air sacs were all inflated during the inhalation and narrowed during the exhalation.When the trachea of chicken was blocked,the abdominal,cervical and clavicular air sacs could still shrink and expand.At that time,the air completely flew among the air sacs through the lung.

The prethoracic and metathoracic air sacs are located among the chest sidewall,thoracico-abdominal diaphragm and lung diaphragm[3].In the embryo stage,the sac is formed by the enlargement of developed bronchus that extends into the pulmonary fold. The sac is divided into two parts by a diaphragm,and the two parts are named as prethoracic and metathoracic air sacs[1,9].The lung diaphragm is located on the rear side,and on the edge of the lung diaphragm,there are 4 thin rib-lung muscles,which are connected to the 3rd,4th,5thand 6thvertebral ribs;the thoracico-abdominal diaphragm is located in the inner side of the abdomen,and there is a thin layer of smooth muscle in the center of the diaphragm;the chest sidewall constitutes the outer side,and it moves frontward and outward or backward and inward under the action of respiratory muscles.During the inhalation, the chest sidewall of chicken moves frontward and outward.On one side, the chest sidewall itself expands towards the back and belly;on the other side,the lung diaphragm and thoracico-abdominal diaphragm are forced to become larger.Thus the 3 sides of prethoracic and metathoracic air sacs all expand,resulting in their initiative expanding.So the air flows from the lung to the prethoracic and metathoracic air sacs.During the exhalation, the chest sidewall of chicken moves backward and inward and shrinks.At this time,the lung diaphragm and thoracico-abdominal diaphragm all relax. The lung diaphragm contracts due to its own resilience and the contraction of rib-lung muscle.At the same time, the thoracico-abdominal diaphragm also contracts due to its own resilience and the contraction of smooth muscle layer inside.Finally,the prethoracic and metathoracic air sacs all contract initiatively,extruding the air though the lung.

The activities of chest sidewall (expanding and contraction of prethoracic and metathoracic air sacs)are the result of role of the respiratory muscles in the chest wall[9].In the exhalation,the rib-lung muscle and muscle in the thoracico-abdominal diaphragm also play important roles. Therefore,during the entire breathing process,the initiative expanding and shrinking of the prethoracic and metathoracic air sacs play a decisive role.It is the“engine”for breathing, and it also affects the activities of the other air sacs.So,after the body cavity of chicken was opened,during the inhalation,the prethoracic and metathoracic air sacs expanded initiatively, and the air flowed from the cervical, clavicular and abdominal air sacs and respiratory tract to the prethoracic and metathoracic air sacs through the lung, shrinking the cervical,clavicular and abdominal air sacs(Fig.1);during the exhalation,the prethoracic and metathoracic air sacs shrank initiatively,and the gas was extruded from the prethoracic and metathoracic air sacs to the cervical,clavicular and abdominal air sacs and respiratory tract though the lung,expanding the cervical,clavicular and abdominal air sacs. Through the respiratory tract,the fresh air can be inhaled and the waste gas can be exhaled continuously,supplementing needed oxygen and discharging carbon dioxide.In addition,the structure of prethoracic and metathoracic air sacs is all simple on both sides,and there are no diverticula[9], which benefit the initiative expanding and shrinking of the prethoracic and metathoracic air sacs and ensure the highly efficient flowing of air only through the lung.However,the cervical,clavicular and abdominal air sacs contain many diverticula,and this benefits the storage of more gas.

The breathing of mammals is caused by the pressure changes in the pleural cavity.Once the gas enters the pleural cavity,the pneumothorax will occur,affecting the breathing of mammals.When the body cavity of chicken is opened,the activities of the prethoracic and metathoracic air sacs paly a decisive role for the breathing. To avoid the occurrence of pneumothorax,the prethoracic and metathoracic air sacs of birds must be not damaged during the surgery.

Effect of pressure change in the body cavity on breath of chicken

Most scholars believe that the activities of air sacs in normal chicken are caused by the pressure changes in the body cavity produced by the movement of the body wall[9].In this study,after the body cavity of chicken is opened,although the pressure changes in the body cavity are destroyed during the breathing process, the chicken can still breathe without asphyxial death due to the initiative expanding and shrinking of the prethoracic and metathoracic air sacs. It suggested that the pressure changes in the body cavity are not necessary for the breathing of chicken. Around the opening of the body cavity of chicken,the activities of chest sidewall are not changed.The cervical,clavicular and abdominal air sacs in normal chickens should also expand and shrink initiatively.Therefore,the pressure changes in the body cavity may affect the activities of the prethoracic and metathoracic air sacs.But the activities of the walls of prethoracic and metathoracic air sacs also play important a role.Some researchers consider that in birds,the cervical, clavicular and abdominal air sacs expand during the inhalation,and shrink during the exhalation[1-3],which are just the opposite in the body cavity-opened chicken.The effects of pressure changes in the body cavity seem to be greater on the activities of the air sacs. The specific effects of pressure change in body cavity on activities of air sacs in birds are needed to be further studied.

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Responsible editor:Tingting XU

Responsible proofreader:Xiaoyan WU

鸡体腔被打开后气囊活动情况

张金龙1*，李新华2，贾胜军1
（1.扬州大学兽医学院/江苏省动物重要疫病与人兽共患病防控协同创新中心，江苏扬州225009；2.中国农业科学院家禽研究所，江苏扬州225003）

打开麻醉状态下鸡的体腔，观察其呼吸情况及气囊壁的活动情况。结果显示，鸡体腔被打开后仍能呼吸。鸡吸气时，胸侧壁、胸腹膈和肺膈主动扩展变大，使胸前气囊和胸后气囊膨大；颈气囊、锁骨气囊和腹气囊壁则收缩，气囊缩小。鸡呼气时，胸侧壁、胸腹膈和肺膈主动收缩变小，使胸前气囊和胸后气囊缩小；颈气囊、锁骨气囊和腹气囊壁则扩张，气囊扩大。所以，体腔打开后鸡仍能呼吸。鸡吸气时，胸前气囊和胸后气囊膨大，气体从颈气囊、锁骨气囊、腹气囊和呼吸道经肺被吸入胸前气囊和胸后气囊，引起颈气囊、锁骨气囊和腹气囊缩小；呼气时，胸前气囊和胸后气囊缩小，气体被压出胸前气囊和胸后气囊，经肺进入颈气囊、锁骨气囊、腹气囊和呼吸道，引起颈气囊、锁骨气囊和腹气囊扩大。在整个呼吸过程中，胸前气囊和胸后气囊能主动地膨大和缩小使气体通过肺。

鸡；体腔；呼吸；气囊tract[1-3,9].Therefore,there is still fresh air entering the lung for gas exchange during both the inhaling and exhaling.During the entire breathing process,the pressure changes in the body cavity play a vital role.Once the air enters the pleural cavity of mammals,pneumothorax will be caused. Since the pressure change in the body cavity plays a vital role in the breathing process of birds,how the birds will breathe and whether the pneumothorax will occur once the body cavity of birds is opened(i.e.trauma and surgery)and the air enters the body cavity are still unknown.For this end, the body cavity of chicken under anesthesia was opened,and the state of breathing and activities of various air sacs were observed and studied.

江苏高校优势学科建设工程资助项目（PAPD）；扬州大学自然科学基金（NK0313103）。

张金龙（1965-），男，江苏如皋人，硕士，副教授，从事动物解剖学方面的研究，E-mail：zjl@yzu.edu.cn。*通讯作者。

2015-01-29

修回日期 2015-05-17

Supported by the Project Funded by Priority Academic Program Development of Jiangsu Higher Education Institutions(PAPD);Natural Science Foundation of Yangzhou University(NK0313103).

*Corresponding author.E-mail:zjl@yzu.edu.cn

Received:January 29,2015 Accepted:May 17,2015