Antibacterial and Wound Healing Activity of the Leaves of   Annona squamosa Linn. (Annonaceae)

 

Chitra Shenoy*1, M B Patil1 and Ravi Kumar2

1Department of Pharmacognosy and Phytochemistry, K.L.E.S’s College of Pharmacy, Belgaum, Karnataka, India.

2Department of Pharmaceutics, K.L.E.S’s College of Pharmacy, Ankola-581314, Karnataka, India.

 

 

ABSTRACT

Natural remedies from medicinal plants are considered to be effective and safe alternative treatment for wounds. In traditional literature, it is found that Annona squamosa leaves were used as folk medicine for the treatment of wound in different parts of the world. The leaves of Annona squamosa (Linn.) were exhaustively extracted by soxhlet apparatus with different solvents like petroleum ether, solvent ether, chloroform, alcohol and chloroform water in ascending order of the polarity. All the five extracts were subjected to antibacterial screening by using the cup plate method. The petroleum ether, alcoholic and chloroform water extract showed maximum zone of inhibition. So these extracts were taken for wound healing activity. The petroleum ether extracts of Annona squamosa at a dose of 300 mg/kg b.w. (orally) in all models showed significant results. The percentage contraction of wound are  at  18 th day, was found to be (91.12±0.62, P < 0.05) in excision wound model, wound breaking strength (299.83 ± 5.446 grams, P < 0.05) in incision wound model, granuloma breaking strength (378.56 ± 5.520, P < 0.05) in granuloma studies. All the results were significant for different parameters in wound healing activity when compared with control group. Presence of sterols, flavonoids, tannins in various extracts was also confirmed by preliminary phytochemical investigation, TLC and HPTLC methods.

Keywords: Annona squamosa, wound healing activity, antibacterial activity, petroleum ether extract.

 

 

INTRODUCTION

Wounds are inescapable events of life; wound may arise due to physical, chemical or microbial agents and wound healing has been one of the earliest medical problems. Healing is essentially a survival mechanism and represents an attempt to maintain normal anatomical structure and function. Healing of wound takes place in a direction away from its normal course and it is common to have none, under or over healing. Treatment is therefore aimed at either shortening the time required for healing or minimizing the undesired consequences. Advances in surgical skill and technique have overcome the latter to some extent.

 

Wound is a breach in the normal tissue continuum, resulting in a variety of cellular and molecular sequelae. The basic principles of optimal wound healing which include minimizing tissue damage, debriding nonviable tissue, maximizing tissue perfusion and oxygenation, proper nutrition and moist wound healing environment have been recognized for many years1. A number of drugs ranging from simple non-expensive analgesics to complex and expensive chemotherapeutic agents administered in the management of wound affect healing either positively or negatively2.Aspirin, indomethacin, cytotoxic agents and immunosuppressant have been proved experimentally to affect healing negatively3-6.

 

 


Management of wound healing, particularly the under healing is complicated and expensive programme. Research on wound healing drugs is a developing area in modern biomedical sciences. Several drugs from plant are known to have wound healing properties. Some of these plants have been screened scientifically for evaluation of their wound healing activity in different pharmacological models and patients, but the potential of most remains unexplored. In a few cases, active chemical constituents were identified. Hence, there is a dearth of safe, economic and effective prohealing agents for the wound management programme, which can enhance healing as well as control infection.

 

The plant Annona squamosa (annonaceae) is commonly called as custard apple in English sharifa in Hindi7. This plant is reputed to possess varied medicinal properties8. It is used as an insecticidal agent has been investigated by several workers9. Free radical scavenging activity of Annona squamosa10 was reported in the leaf extracts. Hypoglycemic and antidiabetic effect of Annona squamosa11-12 was reported in the leaf extract. From the bark of Annona squamosa, a bioactive acetogenin with anticancer activity13-15 have been isolated. Flavonoids from leaves16, Aporphine alkaloids17-18, glycoside19 and squamoline20 were isolated from this plant.

 

In the Ayurvedic system of medicine, herbal extracts but not purified compounds have been used from centuries because many constituents with more than one mechanism of action are considered to be beneficial. However no scientific reports were available on the literature for its wound healing activity. Thus, the present study is designed to fill up the lacunae in the literature for its wound healing activity with a view to provide scientific evidence on modern lines.

 

In this communication we report the preliminary phytochemical investigations of the ethanolic, petroleum ether, solvent ether, chloroform and chloroform water extract of Annona squamosa leaves, the acute toxicity studies and their wound healing activity.

 

MATERIALS AND METHODS

Plant material and Preparation of Extracts

The fresh leaves of Annona squamosa were collected in the month of July 2008 from the Belgaum and authenticated by Dr. Harsha Hegde, Chief Botanist, Indian Council of Medical Research (RMRC), Belgaum branch, shade dried and powdered then passed from 40# mesh size.

 

Preparation of Various Extracts of Annona squamosa Linn

Around 1 kg fresh shade dried leaves were powdered and extracted by hot percolation method by soxhlet apparatus with five liters of each petroleum ether, solvent ether, chloroform, alcohol, chloroform water and. The percolation process was continued until the extraction process was completed (indicated by fade coloured menstrum). All the extracts finally reduced to dryness at 40oC by Rotovapour (Rotavapour Buchi, Switzerland). The traces of the solvents were removed by keeping the dried extracts in to a desiccator. The concentrated extracts were stored carefully for phytochemical investigation.

 

PRELIMINARY PHYTOCHEMICAL INVESTIGATION

All the extracts were screened for the presence of various secondary metabolites like steroids, alkaloids, carbohydrates, proteins, flavonoids, tannins and glycosides using the standard methods.

 

Powder Analysis

The powdered crude drug was subjected to determination of pH, extractive value, total ash, water soluble ash, acid insoluble ash and loss on drying as per Indian Pharmacopoeia.

 

Microorganisms
The test microorganisms used for the antimicrobial activity screening were 4 bacteria       (2 Gram positive) – Bacillus subtilis, Staphylococcus aureus, (2 Gram negative)-Pseudomonas aeruginosa, Escherichia coli. These organisms were identified and procured from National Chemical Laboratory (NCL), Pune, India.

 

Antibacterial Activity

The agar diffusion method21 was used to evaluate the antibacterial activity. Bacteria were cultured overnight at 37 o C in Mueller Hinton 10 µl Broth (MHB, Oxoid) and used as inoculum. A final inoculums, using 100 µl of suspension containing 108 CFV/ml of bacteria spread on Mueller Hinton Agar (MHA) medium.

 

The disc (6 mm in diameter) was impregnated with 10 µl of 200µl/ml, 150µl/ml, 125 µl/ml, 100 µl/ml, 75 µl/ml and 50 µl/ml of each extracts and for each organism placed on seeded agar. Streptomycin (200µl/ml, 150µl/ml,125 µl/ml, 100 µl/ml,75 µl/ml and 50 µl/ml) was used as positive control bacteria. The test plates were incubated at 37 o C for 24h for bacteria depending on the incubation time required for a visible growth.

 

Pharmacological activity

Experimental animals

Albino wistar rats of either sex (150-200g weight) and Swiss albino mice of either sex   (18-22g weight) were procured from Venkateshwara Enterprises, Bangalore. The animals were divided into different groups comprising of six animals in each group. They were kept in polypropylene cages at 23±1̊ C in 12:12h dark: light cycle, with free access to standard pellet feed (Chakan Oil Mill, India) and water ad libitum. This project was cleared by Institutional Animal Ethical committee.

 

Acute Oral Toxicity study

Swiss albino mice of either sex (18-22g weight) and of 90 days were used to determine the LD50 of various test extracts. The animals were fasted over night prior to the acute experimental procedure. The acute oral toxicity study was carried out as per the guidelines set by Organization for Economic Co-operation and Development (OECD)22. The LD 50 was found to be more than 3000 mg/ kg b.w. p.o. in acute toxicity testing. The therapeutic dose 300mg/ kg b.w. p.o. (ED50) was calculated as 1/10 th of the lethal dose for the purpose of wound healing investigation.

 

WOUND HEALING ACTIVITY

Albino wistar rats of either sex (150-200g weight) were selected, and divided into six groups of six each ( n = 6). Animals were depilated at the desired site before wounding. They are housed individually with free access to food and water, the basal food intake and body weights to the nearest gram were noted. The animals were starved for 12 h prior to wounding. Under light ether anesthesia wounding was performed semi-aseptically. The first, third and fifth group served as control similarly second, fourth and sixth groups received alcoholic, petroleum ether and chloroform water extract by oral route at a dose of 300 mg/kg body weight by oral route daily for 10 consecutive days in incision and dead space wound model and for 20 days in the excision wound model. The suspensions of desired concentrations were prepared in gum acacia 2% solution, and were administered as per the ED50.

 

Wound models:

1.      Resutered incision

2.      Excision wound

3.      Dead space wound (granuloma studies)

Resutered, excision and dead space wound models in albino rats, were selected for assessing the wound healing activity. These parameters were selected because of the easy availability of albino rats and the simplicity in handling them. The rats were anaesthetized prior to incision and other surgical   procedures, and were sacrified by exposing to a higher dose of anaesthetic ether prior to determination of the tensile strengths of the resutured wounds, and the removal of granuloma tissue (grass pith). 

 

Excision wound

An excision wound was inflicted by cutting away 500 mm2 full thickness of a  pre-determined area on the depilated back of the rat. Epithelialization period was noted as the number of days after wounding required for the eschar to fall off leaving no raw wound behind. Wound contraction rate was monitored by planimetric measurement of the wound area on alternate days. This was achieved by tracing the wound on a graph paper on 4 th, 8 th, 12 th,16 th and18 th  post wound days and thereafter daily until healing was complete. Reduction in the wound area was expressed as percentage of the original wound size23.

 

Incision wound

On the depilated backs of the animals, two paravertebral incisions of 6 cm length were made cutting through the full thickness of the skin. Interrupted sutures, 1 cm apart, were placed to approximate the cut edges of the skin24. The sutures were removed on the 8th post wound day and skin breaking strength was measured on the 10th day by continuous water flow technique of Lee25.

 

Dead Space wounds (Granuloma studies)

Physical changes in the granuloma tissue were studied in this model. Under light ether anaesthesia, subcutaneous dead space wounds were inflicted in the region of the axilla and grion, by making a pouch through a small neck in the skin. Granuloma formation was induced by implanting grass pith and cotton pellet. Cylindrical grass piths measuring 2.5 cm in length and 0.3 cm diameter were introduced into the pouch similarly. Each animal received 2 grass piths in different locations.

 The wounds were sutured and mopped with an alcoholic swab. Animals were placed into their individual cages after recovery from anaesthesia. Excision of the granulation tissue from the surrounding tissue was performed on the 10th post wounding day under light ether anaesthetic condition. Granuloma surrounding the grass piths was excised and slit open by longitudinal rectangular strips. The tensile strength of piece measuring about 15 mm in length and 8 mm in width (obtained after trimming the granulation tissue) was determined on 10th post wounding day continuous constant water flow technique of Lee. The granulation tissue so harvested was subjected to hydroxyproline estimation. Their weights were expressed as mg/100 gms body weight as suggested by Dispaquale and Meli26.

 

Histopathological studies

A section of the granuloma tissue was subjected to histopathological examination to determine the pattern of lay-down for collagen using two special stains i.e.Van Gieson and Masson Trichrome.

 

STATISTICAL ANALYSIS

All the results were analyzed by One-way Analysis of Variance (ANOVA) followed by Dunnett’s test. The level of significance was set at P<0.05.

 

RESULTS AND DISCUSSION

The average percentage yield of various extracts of Annona squamosa is shown in table 1.       

 

Table 1: The percentage yield of various extracts of Annona squamosa L.

Sl. No.

Extracts

Nature of extract

Colour

Yield (% w/w)

1.

Petroleum ether

Semisolid

Dark yellow

8.05

2.

Solvent ether

Semisolid

Dark brown

5.00

3.

Chloroform

Semisolid

Dark brown

7.00

4.

Alcohol

Semisolid

Dark brown

17.45

5.

Chloroform water

Semisolid

Dark yellow

12.00

 

Powder analysis parameters like pH, extractive value, total ash, water soluble ash, acid insoluble ash and loss on drying were determined on the powder of Annona squamosa. In powder analysis ash values are useful in determining the quality and purity of crude drug, especially in the powder form and the extractive values are useful for their evaluation, especially when the constituents of a drug can not be readily estimated by any other means. Further these values indicate the nature of the constituents present in a crude drug. The results of physicochemical characterization of Annona squamosa are presented in table 2.

 

Table 2:  Physicochemical Characterization of Annona squamosa

Sl. No.

Parameters

Result

1.

Total ash (%)

2.25

2.

Acid insoluble ash (%)

1.0

3.

Water soluble ash (%)

1.8

4.

Loss on drying (%)

1.25

5.

Extractive value (%)

9.5

6.

pH

6.9

 

The phytochemical tests revealed that the leaves of the plant possess Sterols in petroleum ether and solvent ether extract. The other constituents like flavonoids, tannins, glycosides, carbohydrates and proteins were found in ethanolic and chloroform water extract. Leaves of the plant possess alkaloids in chloroform extracts. The results of phytochemical screening are given in table3.

 

 


Table 3: Phytochemical Screening of different extracts of Annona squamosa

Extracts

Steroids

Alkaloids

Glycosides

Saponin

Flavonoid

Tannin

Carbohydrates

Petroleum Ether

+++

-

-

-

-

-

-

Solvent Ether

++

-

-

-

-

-

-

Chloroform

+

++

-

-

-

-

-

Alcohol

-

+

+

-

++

++

+

Chloroform water

-

-

+

+

+

+

++

+++: high concentration; ++: medium concentration; +: low concentration; - : constituents not detectable


 

Table4: Results of Acute oral toxicity studies of various extracts of Annona squamosa

Sl. No

Extracts

LD50 (mg/kg)

ED50(mg/kg)

1.

Petroleum ether

3000

300

2.

Solvent ether

3000

300

3.

Chloroform

3000

300

4.

Alcohol

3000

300

5.

Chloroform water

3000

300

 

The LD50 was found to be more than 3000 mg/ kg b.w. p.o. in acute toxicity testing. The therapeutic dose 300mg/ kg b.w. p.o. was calculated as 1/10 th of the lethal dose for the purpose of wound healing investigation. The results of oral toxicity studies of various extracts of Annona squamosa is presented in table 4.

 

Antibacterial activity was done for all the five, pet ether, solvent ether, chloroform, ethanol and chloroform water extracts. During antibacterial study chloroform water, petroleum ether and alcoholic extracts showed maximum zone of inhibition against almost all organisms in cup plate method. So the chloroform, alcohol and petroleum ether extract were taken for wound healing activity. The results of antibacterial activity of various extracts of Annona squamosa  are shown in table 5.

 

The results of the excision wound model are given in table 6. In an excision wound model, petroleum ether extract at a dose 300mg/kg BW p.o. of Annona squamosa  showed significant wound healing activity (% wound contraction on 18th day         (91.12 ± 0.620, P < 0.05) compared to control (39.56± 0.47). It also showed complete epithelization (16.00 ± 0.43 days P < 0.05) when compared to control (24.66 ± 0.211). The petroleum ether extract showed a scar area of (9.83 ± 0.479 mm 2, P< 0.05) as compared to control 15.5 ± 1.52 mm 2.

The results of incision wound model are given in table 7. In incision study, the petroleum ether extract showed significant (299.83±5.446, P< 0.05) breaking strength when compared to control (144.2±8.052).

 

The results of dead space wound model are given in table 8. The tensile strengths of the granuloma tissue were determined by the water flow technique of Lee. Petroleum ether extract showed highly significant increase in breaking strength (378.56±5.520, P<0.05) when compared to control (157.035±8.765) and petroleum ether also showed significant increase in the dry weight of granulation tissue (53.88±0.46, P<0.05) as compared to control (30.42±0.47). Petroleum ether also showed significant increase in the hydroxyproline content

 

 

(2514.17±21.11, P<0.05) as compared to control (1395±9.66).

 

Histological studies of granulation tissue of the petroleum ether extract treated animals showed significant increase in collagen deposition with macrophages, tissue edema and more fibroblasts. (fig.1) than alcohol extract compared to control.

 

DISCUSSION

Granulation, collagen maturation and scar formation are some of the many phases of wound healing which run concurrently, but independent of each other. The use of single model is inadequate and no reference standard exists that can collectively represent the various phases of wound healing. Hence three different models have been chosen in our study to assess the effect of Annona squamosa on wound healing. The wound breaking strength is determined by the rate of collagen synthesis and more so by the maturation process where there is covalent binding of collagen fibrils through inter and intra molecular cross linking. In our study dead space wound model showed significant increase in breaking strength and hydroxyproline concentration, and also dry weight of the granulation tissue was significantly increased in Annona squamosa  treated group. By this we can assume that the Annona squamosa might have increased the collagen and also probably have altered the maturation process, by affecting the cross linking of collagen or improving the quality of collagen fibrils. The increase in weight in Annona squamosa  treated group could be due to high protein concentration and collagen bundle formation27.

 

Measurement of the hydroxyproline could be used as an index for collagen turnover. In the present study significant increase in the hydroxyproline content of the granulation of the animals treated with petroleum ether extract and chloroform extract were observed indicating rapid collagen turnover. Increase in breaking strength of granulation tissue indicated the enhanced collagen maturation by increased cross linking. In addition, increase in dry granulation tissue weight indicated the presence of higher protein content.

 

The preliminary phytochemical analysis of leaf extract of Annona squamosa  revealed the presence of flavonoids, saponins28, alkaloids29, tannins and sterols. Flavonoids are known to reduce lipid peroxidation not only by preventing or slowing the onset of cell necrosis but also by improving vascularity. Hence, any drug that inhibits lipid peroxidation is believed to increase the viability of collagen fibrils by increasing the strength of collagen fibres, increasing the circulation, preventing the cell damage and by promoting the DNA synthesis30.

 

 


TABLE 5: Results antibacterial activity of various extracts of Annona squamosa 

Sl. No.

Name of the Extract

Zone of Inhibition in mm at conc. of 200 mg/ 0.1 ml

Bacillus subtilis

Staphylococcus aureus

Pseudomonas aeruginosa

Escherichia coli

1.

Petroleum ether

20

19

20

22

2.

Chloroform

17

16

19

20

3.

Chloroform water

19

19

19

21

4.

Solvent ether

12

14

14

17

5.

Alcohol

20

18

18

20

6.

Control (DMF)

R

R

R

8

7

Standard

21

20

22

24

 

 

 

 

 

Diameter of cup – 6mm; Standard drug – Streptomycin; DMF - Dimethyl formamide; R – Resistance

Table6: Influence of different extracts of Annona squamosa on incision wound healing

Group

(N)

 
Dose (oral)

Excision Wound

% Wound Contraction

4th day

8th day

12th   day

16th day

18th day

Mean size

of scar

area mm2

Period of epithelization (days)

Control

1 ml of 2% Gum acacia

13.90±

0.32

20.04±

0.14

23.52±

0.57

32.55±

0.06

39.56±

0.47

15.5±

1.52

24.66±

0.211

Petroleum ether

300 mg/kg suspended in 2% acacia

25.19±

0.36

30.21±

0.02

50.63±

0.35

74.36±

1.07

91.12±

0.62*

9.83±

0.479*

16.00±

0.43*

Chloroform water

300 mg/kg suspended in 2% acacia

45.98 ±1.10

52.75±

1.23

70.46±0.45

76.35±

1.39

90.21±

0.66

10.66±

0.3346

19.00±

0.366

Alcohol

300 mg/kg suspended in 2% acacia

39.36±

1.286

49.63±

1.300

67.47±

0.46

72.12±

1.47

88.21±

0.67*

10.11±

0.35*

18.33±

0.211*

 

* indicates significant difference at P<0.05 when compared to control. Values are Mean ± SEM from 6 animals in each group), Data analyzed by One-way ANOVA followed Dunnett’s  test.

 

Table7: Influence of various extracts of Annona squamosa on healing of Incision wound

Group (n)

Dose (oral)

Wound breaking strength (g)

Control

1 ml of 2% Gum acacia

144.2±8.052

Petroleum ether

300 mg/kg suspended in 2% acacia

299.83±5.446*

Chloroform water

300 mg/kg suspended in 2% acacia

280.67±4.213

Alcohol

300 mg/kg suspended in 2% acacia

263.63±4.48*

* indicates significant difference at P<0.05 when compared to control. Values are Mean ± SEM from 6 animals in each group), Data analyzed by One-way ANOVA followed Dunnett’s  test.

 

Table 8: influence of various extracts of Annona Squamosa on healing of dead space wound

Group (n)

Dose (oral)

Breaking strength   (g)

Granulation tissue dry weight (mg/100g)

Hydroxyproline (µg/100mg)

Control

1 ml of 2% Gum acacia

157.035± 8.765

30.42±0.47

1395±9.66

Petroleum ether

300 mg/kg suspended in 2% acacia

378.56± 5.520*

53.88±0.46*

2514.17±21.11*

Chloroform water

300 mg/kg suspended in 2% acacia

289.8± 4.351

30.98±0.85

1465±11.76

Alcohol

300 mg/kg suspended in 2% acacia

283.82± 4.44*

40.99±0.37

1910±5.63*

* indicates significant difference at P<0.05 when compared to control. Values are Mean ± SEM from 6 animals in each group), Data analyzed by One-way ANOVA followed Dunnett’s  test.


Flavonoids31-32, triterpenoids33 are also known to promote the wound-healing process mainly due to their astringent and antimicrobial property, which seems to be responsible for wound contraction and increased rate of epithelialisation. Tannins the main components of many plant extracts, act as free radical scavengers34-39. Research into the role of antioxidants from plant extracts in wound healing has been published widely40.

 

CONCLUSION

The use of Annona squamosa in Indian traditional systems of medicine for various skin diseases, has been justified by this work, as it showed a wound healing potential and commendable activity against several microorganisms. These findings could justify, at least partially, the inclusion of this plant in the management of wound healing in folk medicine. Since the role of free radicals and antioxidants in wound healing are very clearly defined, wound healing potential Annona squamosa may be partly due to the potent antioxidant activity of the plant. Further experiments are needed to test the effect of this plant in the treatment of chronic wounds. To conclude, the petroleum ether extract of Annona squamosa exhibited significant wound healing activity in excision, incision, burn and dead space wound model. Hence the present findings provide scientific evidence that petroleum ether extract of Annona squamosa as a potent wound healer.

 

Figure1. Histology of the Granulation tissue of Pet ether treated animal showing more collagen and less macrophages (Vangeison stain).

 

ACKNOWLEDGMENT

The authors are thankful to Dr. F.V. Manvi, Principal, K.L.E.S’s College of Pharmacy, Belgaum, Karnataka, India for providing all the facilities and support to carry out the research work.

 

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Received on 03.05.2009

Accepted on 22.05.2009     

© A&V Publication all right reserved

Research Journal of Pharmacognosy  and Phytochemistry. 1(1): July.-Aug. 2009, 44-50