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ORIGINAL ARTICLE
Year : 2019  |  Volume : 22  |  Issue : 10  |  Page : 1328-1334

Evaluation of the effect of honey on the healing of tooth extraction wounds in 4- to 9-year-old children


1 Department of Pediatric Dentistry, Dental School, Tehran University of Medical Sciences, Tehran, Iran
2 Pedodontist, Private Practice, Tehran, Iran
3 Department of Orthodontics, Dental School, Yazd University of Medical Science, Yazd, Iran

Date of Acceptance31-Jul-2019
Date of Web Publication14-Oct-2019

Correspondence Address:
Dr. Z Hosseini
North Kargar St, Po. Code: 14399-55991, Tehran
Iran
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/njcp.njcp_102_19

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   Abstract 


Objective: The aim of the this study was to evaluate the effect of honey on the healing of tooth extraction wounds in children 4‒9 years of age. Subjects and Methods: In the present randomized clinical trial, 51 patients, 4‒9 years of age were selected randomly. All the subjects required extraction of one deciduous molar tooth. The subjects were randomly assigned to two groups. In group 1, after extraction of the tooth, the dentist used a cotton swab applicator to place a layer of honey on a piece of gauze moistened with normal saline solution (NSS) and placed it on the socket. In group 2, honey was not used; rather, NSS was applied. On days 3 and 7 after tooth extraction, the wound sizes were measured. Results: In both groups, the wound sizes decreased significantly on the third day compared with baseline and on the seventh day compared with the third day (P < 0.05). On the third and seventh days after tooth extraction, wound sizes in the honey group were significantly lower than those in the NSS group (P < 0.05). Conclusion: Honey resulted in a decrease in wound sizes and faster healing after extraction of teeth in children. Therefore, use of honey can be recommended after minor surgeries in the oral cavity.

Keywords: Honey, normal saline, tooth socket, wound healing


How to cite this article:
Mokhtari S, Sanati I, Abdolahy S, Hosseini Z. Evaluation of the effect of honey on the healing of tooth extraction wounds in 4- to 9-year-old children. Niger J Clin Pract 2019;22:1328-34

How to cite this URL:
Mokhtari S, Sanati I, Abdolahy S, Hosseini Z. Evaluation of the effect of honey on the healing of tooth extraction wounds in 4- to 9-year-old children. Niger J Clin Pract [serial online] 2019 [cited 2019 Nov 20];22:1328-34. Available from: http://www.njcponline.com/text.asp?2019/22/10/1328/269004




   Introduction Top


Honey has been used in traditional medicine for prevention and treatment of many medical conditions.[1] A large number of studies on the therapeutic use of honey have focused on Manuka honey from the Leptospermum species, indigenous to New Zealand and Australia.[2],[3]

Natural antioxidants and flavonoids of honey have exhibited a wide range of biological effects, including antibacterial, anti-thrombotic, anti-inflammatory, anti-allergic, and vasodilatory effects.[4],[5]

Honey has traditionally been used for the treatment of ulcers and wounds and has also been used in modern medicine.[6] Manuka honey has recently been approved by the FDA for the treatment of burns and ulcers.[7]

The physical and bioactive properties of honey affect the wound healing process. The activity of honey results in an increase in the release of oxygen from hemoglobin, creating an unfavorable environment for the activity of destructive proteases.[8] In addition, honey stimulates peripheral monocytes to release cytokines and chemokines, such as TNF-α, IL-6, IL-1β, and TGF-β, accelerating the wound healing process.[9]

Some studies have evaluated the effect of honey on different wounds. Jull et al. (2008) evaluated the effect of honey on the rate of healing of acute wounds (such as burn wounds, lacerations, and other traumatic wounds) and chronic wounds (such as venous wounds, arterial wounds, diabetic wounds, compression wounds, and contaminated surgical wounds) in a systematic review. The results of the evaluation of 19 articles showed that honey, compared with some other conventional local medicaments, improves the healing process in mild-to-moderate surface burn wounds.[10]

At first look, although it might seem that there is no need for the use of honey in children due to the low complications resulting from tooth extraction and the rapid healing process in these subjects; in fact, if the positive effect of honey on wound healing is substantiated in children, it is possible to use honey to improve the healing process of wounds resulting from more extensive surgeries such as those to remove mesiodens and odontomas and also frenectomy procedures. On the other hand, in patients in which a large number of teeth are extracted under general anesthesia, honey can play an important role in decreasing pain and other postoperative morbidity, complications, and in accelerating wound healing. In addition, a large number of children suffer from systemic conditions, such as leukemia, cyclic neutropenia, and oral ulcers resulting from therapeutic procedures of such conditions are very prevalent in them. Given the compromised immune system in these patients, they exhibit very slow healing processes and might have infectious wounds, which might be seriously life-threatening. Therefore, use of an effective, inexpensive, and available medication, which can accelerate the wound healing process in such children, will be very effective. Therefore, the aim of this study was to evaluate the effect of honey on tooth extraction wound healing in children 4‒9 years of age.


   Methods Top


The protocols of this randomized clinical trial study were approved by the Regional Committee for Medical Research Ethics of Dental school of Tehran University of Medical Sciences. The sample size in the present randomized clinical trial was determined at 21 subjects in each group with the use of PASS software program by considering α = 0.05 and β = 0.2, using the “test for two means” option, based on the results of a pilot study on six samples in each group, evaluating the amount of decrease in the size of wound, which yielded a decrease of about 30% and 46%, in the control and honey groups, respectively. In order to accommodate dropouts, a larger sample size was used in the study. In total, 76 children, aged 4‒9 years, who were referred to the Department of Pediatric Dentistry, and needed removal of one deciduous molar tooth, were randomly selected for this study. The subjects had no history of systemic conditions, use of medications and allergy to honey, and had not repeatedly used honey during the previous 6-month period. Subjects who exhibited a root length less than one-third of the normal root length or those who suffered from widespread iatrogenic trauma during tooth extraction, or subjects who used mouthwashes or any specific medications from the day of tooth extraction until day 7 were excluded from the study. The subjects' parents signed informed consent forms so that their children could be included in the study. The subjects were randomly (opening sealed envelope) assigned to two groups. Each subject was assigned to a group according to the chosen envelope:

Group 1: First, the infiltration technique in the upper jaw and inferior alveolar nerve block in the lower arch were used to get anesthesia, using one cartridge containing 0.2% lidocaine (Darou Pakhsh, Iran). After achieving adequate anesthesia, the tooth was removed and the dentist placed a 1-mm layer of Iranian Kurdistan Mountains honey with the use of a cotton swab applicator on a piece of gauze moistened with normal saline solution. The honey was freshly acquired from the Iranian Kurdistan Mountains. The honey was placed in contact with the socket wound. Then, the parents and children were asked to keep the gauze piece in place for 45 min.

Group 2: The anesthetic and extraction procedures were carried out in a manner similar to those in group 1. After extraction of tooth, a piece of gauze moistened with normal saline solution (NSS) was placed on the socket wound. The parents and the children were asked to keep the gauze piece in place for 45 min (same time of gauze placement as group 1).

Postoperative instructions were provided for all the subjects, which included the use of soft and cold food items, no use of straws, etc. The subjects were also asked to rinse their oral cavities with cold water after removing the gauze piece in order to remove the remnants of the honey and to prevent its probable cariogenicity. This was also done for control group subjects to have the similar situation for all subjects. Also, all of the samples were asked not to use any mouthwashes up to the seventh day after tooth extraction.

In all the subjects, the study variables were recorded at baseline (i.e. after extraction of tooth and before placing the gauze piece) and on days 3 and 7 after extraction of teeth.

The variables that were evaluated consisted of the following (based on Landry, Turnbull, and Howley Index)[11]:

  1. 1. Wound size: To determine wound size, a trained dentist measured the mesiodistal and buccolingual dimensions of each socket with the use of digital calipers (ITAL ELECTRONIC CALIPER) accurate up to 0.01 mm. The product of these two values was considered as the wound size [Figure 1]. Measurements to determine the mesiodistal and buccolingual dimensions of each socket were repeated twice and to have an acceptable intraexaminer reliability, in cases in which the difference between the two measurements was >0.2 mm, the measurements were repeated and the mean of the measurements was then recorded as the final value.
  2. 2. Tissue color: This variable consisted of the normal gingival color and the red color (inflamed).
  3. 3. Bleeding on palpation: This variable was recorded as bleeding or absence of bleeding on palpation.
  4. 4. The presence of granulation tissue: This was recorded as the presence or absence of granulation tissue.
  5. 5. Presence of pus: This variable was recorded as the presence or absence of pus.
  6. 6. Gingival margin status: This was recorded as the presence or absence of epithelialization.
  7. 7. Pain: Based on Numeric Pain Rating Scale,[12] the parents were asked to assign a value from zero to 10 to their children's pain severity on the day of tooth extraction (baseline) and on days 3 and 7 after tooth extraction, with zero indicating the absence of pain and 10 indicating severe pain. Overall, three scores for pain were recorded for each subject.
Figure 1: Schematic wound size measurement method

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As the aim of the study was to evaluate the effect of honey on tooth extraction wound healing in children 4‒9 years of age, repeated measures analysis of variance (ANOVA) was used to compare the effect of honey on the healing process of the socket wound between the control and case groups by considering the intervention as the intersubject factor.

Since the effect of intervention proved significant from baseline to day 7 after tooth extraction, covariance analysis was used to compare the two groups by considering the baseline as the covariant. In addition, repeated measures one-way ANOVA with LSD two-by-two-comparisons for different time intervals was used.


   Results Top


Seventy-six subjects were evaluated in this study (n = 38 in the control and intervention groups). Of all these subjects, 25 subjects (14 in the intervention group and 15 in the control group) were excluded from the study due to their absence in the scheduled recall appointments and use of medications after tooth extraction. Finally, the study was carried out on 51 subjects, 4–9 years of age, in two groups; in group 1 (n = 26), honey was used, and in group 2 (n = 25), NSS was used after tooth extraction.

Wound size

[Table 1] presents the mean wound sizes in the two groups at baseline and 3 and 7 days after tooth extraction.
Table 1: Wound sizes in the two study groups at baseline and 3 and 7 days after tooth extraction

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Based on the results of repeated measures ANOVA, the interactions were significant in the present study. In addition, covariance analysis, by considering the baseline time limit as a covariant, was used to compare the two groups (P = 0.289). Comparison of the two groups at different time intervals showed that wound sizes 3 and 7 days after tooth extraction were significantly lower in the honey group compared with the NSS group (P = 0.002 and P = 0.006, respectively).

In addition, in both honey and NSS groups, the wound sizes on day 3 were significantly smaller than those at baseline; in addition, on day 7, they were significantly smaller compared with day 3 (P < 0.001).

Response to palpation

On day 3 after tooth extraction, palpation resulted in bleeding from the socket in 72% of the subjects in the NSS group and in 92% of the subject in the honey group. On day 7 after tooth extraction, palpation did not result in bleeding in any of the subject in the two study groups [Table 2].
Table 2: Comparison of response to palpation after tooth extraction at different time intervals

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Granulation tissue

In the honey group, no cases of granulation tissue were found; in the NSS group, one case of granulation tissue was found on day 3, which had resolved on day 7 [Table 3].
Table 3: Comparison of the presence of granulation tissue after tooth extraction at different time intervals

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Gingival margin

In relation to gingival margin, epithelialization had increased in both groups; however, only in the honey group complete epithelialization had occurred in all subjects and the socket was completely closed [Table 4].
Table 4: Comparison of gingival margins after tooth extraction at different time intervals

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Pus

No purulent secretions were detected in any of the samples during tooth extraction and at 3- and 7-day postoperative intervals.

Pain due to tooth extraction

At baseline and on days 3 and 7 after tooth extraction, the subjects' pain perception was recorded as follows (0 = the least pain; 10 = the most severe pain):

In the honey group, of 26 subjects, at baseline, 9 patients had a score of 1, 10 patients had a score of 2, and 7 patients had a score of 3.

In the NSS group (n = 25), at baseline, 16 patients had a score of 1, 5 patients had a score of 1, and 4 patients had a score of 3. None of the subjects reported a pain score >3.

On days 3 and 7 after tooth extraction, all the patients were free of pain (pain score of zero) [Table 5].
Table 5: Comparison of pain severities after tooth extraction at baseline in both groups

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   Discussion Top


The aim of this study was to evaluate the effect of honey on wound healing after tooth extraction in children 4‒9 years of age. Based on the results, the wound sizes in the honey group were significantly less than those in control group.

Previously, various topical medications have been applied on tooth sockets to induce wound healing and decrease postoperative pain.[13] One of these medications is honey, which is a natural product with rich nutritional properties; it can catalyze biological reactions to improve the immune system and create an environment, which cannot be tolerated by microorganisms.[14]

The effect of honey on infections is not only attributed to its antibacterial activity but also to its effect on proliferation of B- and T-lymphocytes. In addition, 1% honey in the culture medium can induce the release of TNF, IL-1, and IL-6 from monocytes.[15] Covering of the wound with a layer of honey resulted in a decrease in the oxygenation of the injured tissue and in a decrease in pain severity 30 s after its application.[16]

Consistent with the results of this study, various studies have demonstrated the positive effects of honey on wound healing. Soni et al. (2016) evaluated the effect of honey on the resolution of alveolar osteitis and reported that C-reactive protein levels decreased significantly after treatment with honey, indicating rapid healing of the wound. In addition, the severity of pain, erythema, and swelling, too, decreased significantly on days 2, 3, and 5 compared with day 1.[14] Singh et al. (2014), too, reported significant decreases in the severity of pain, inflammation, hyperemia, edema, exudation, and halitosis in patients receiving honey for resolving alveolar osteitis. They attributed these results to the anti-inflammatory properties of honey, which is predominantly due to the disinfecting action of hydrogen peroxide in its chemical composition.[17]

El-Haddadi et al. (2013) carried out a pilot study to evaluate the clinical efficacy of local application of honey for the treatment of some common inflammatory, vesiculobullous, and ulcerative lesions of the oral cavity. Their lesions included recurrent aphthous stomatitis, recurrent herpes labialis, recurrent intraoral herpetic ulcers, atrophic/erosive oral lichen planus, oral candidiasis, and oral psoriasis. The results showed that in all the subjects, pain, itching, and lesion sizes decreased, and the patients generally reported improvements in lesions based on the parameters described in the study. They believed that topical application of honey might prevent the secondary infection, which is very common in many vesiculobullous and ulcerative lesions, such as recurrent aphthous stomatitis (RAS), recurrent herpes labialis (RHL), and bulbous lichen planus. They attributed this effect of honey to its property to decrease the synthesis of prostaglandins in the area it is applied, to increase nitric oxide in the wound area, and to decrease the proliferation of bacteria and fungi and also to the antioxidative properties of honey.[18]

A study by Mohamed et al. (2008) on patients with minor aphthous lesions showed that use of honey three times a day for 3 days was more effective than kenalog for the treatment of these lesions and resulted in better shrinkage of the ulcer, greater decrease in pain severity and in bleeding, and in greater epithelialization. Therefore, it is a useful medicament for wound healing.[19]

Motalebnejad et al. (2014) evaluated the effect of honey on resolution of mucositis resulting from radiotherapy. In that study, patients used honey as a mouthwash 15 min before and 15 min and 6 h after radiotherapy. The results showed significant improvements in the treatment of mucositis compared with the control group.[15]

Abdulrahman et al. (2012) evaluated the effect of honey and a mixed solution of honey, olive oil extract and wax oil (HOPE) on oral mucositis in patients undergoing chemotherapy, with a mean age of 6.9 years and reported that generally honey resulted in better resolution of grade II and grade III mucositis compared with HOPE and the control group.[20] Se Hwang et al. (2014) evaluated the effect of honey on postoperative pain after tonsillectomy in a systematic review and reported that pain was less severe postoperatively; therefore, there was less need for analgesics compared with the control group.[21]

Honey has antimicrobial activity, too, which was discovered in the late 19th century by Van Ketel. Rapid resolution of infections by honey, as one of its most important properties, is attributed to its effect on Gram-positive, Gram-negative, aerobic and anaerobic bacteria, and a number of fungi.[22] Studies have shown that a large number of bacteria and fungi are sensitive to honey.[23],[24],[25] Honey can completely inhibit proliferation of Candida albicans in the wound bed. In addition, diluted honey can neutralize toxins of microorganisms.[18]

The results of a study by Abedlmegid et al. (2015) showed that irrigation of the oral cavity with a solution of honey and green tea for 2 min can decrease S. mutans counts in 7- to ‒10-year-old boys.[26] On the other hand, Eick et al. (2014) reported that Manuka honey can inhibit the proliferation of planktonic P. gingivalis up to 50%, inhibiting formation of biofilms and decreasing the counts of this bacterial species in 24-h-old biofilms.[27] In addition, honey has been effective in the treatment of recurrent herpes labialis lesions and infectious ulcers after surgeries and in decreasing salivary counts of S. mutans in patients with xerostomia and in decreasing plaque and hemorrhage in patients with gingivitis.[28],[29],[30],[31] Therefore, this significant ability of honey to heal oral ulcers might be attributed to its effect on prevention of the proliferation of common pathological microorganisms in the oral cavity, resulting in shortening of the healing period.[19]

This excellent property of honey creates a unique environment after oral cavity surgeries because in such conditions microorganisms that are normally found in the oral cavity are pathogenic and prevent wound healing. In addition, honey is not toxic; therefore, it does not retard the healing process and has no deleterious side effects.[22]

This antibacterial property of honey also always concerns about the cariogenicity of this natural substance. Based on the results of a study by Mohabatra et al. (2011), raw and processed honey has great antibacterial activity with a high potential to decrease tooth sensitivity to caries.[32] In addition, English et al. (2004) and Atwa et al. (2014) reported that this natural product prevents aggregation of dental plaque, gingivitis, and other gingival diseases.[31],[33] Some studies have shown that honey is not cariogenic but has anticariogenic activity. Khamverdi et al. (2013) showed that honey significantly decreased S. mutans and Lactobacillus counts.[34] The ability of honey to help achieve oral health is probably due to its antibacterial potential, which prevents bacterial proliferation, decreasing the pathogenicity of dental caries.[35] It should be pointed out that in this study, a small amount of honey was applied, in an approximate 1-mm-thick layer, on a piece of gauze and was only used in the tooth extraction site, and the subjects in both groups were asked to gently rinse their oral cavities with cold water after 45 min to remove the remnants of honey in order to prevent its probable cariogenicity.

Different kinds of honey produced from different plants exhibit different properties.[2] The duration of wound healing in the oral cavity might be different depending on the anatomic location and the size of the wound and the presence of local and systemic predisposing factors such as the patients' therapeutic regimen after surgery.[22]

On the other hand, evaluation of wound healing is still a clinical challenge because the terminology used for its description is not completely standardized and there is no consensus about the most appropriate parameters for estimating wound healing and reporting it. However, recent studies have shown that measuring the wound periphery alone is sufficient for reporting wound healing even if the wound depth is not measured.[2] In this study, in addition to measuring the dimensions, other parameters of wound healing were evaluated based on Landry, Turnbull, and Howley Index, which has been used as a criterion in valid studies.[11] However, the tools used for describing and reporting the healing of surgical wounds, such as rulers and calipers, despite their validity, sensitivity, and reliability, might not provide comprehensive and adequate evaluations.[22]

Based on the results of this study, honey decreased wound size and accelerated wound healing after extraction of teeth in children.

Use of this natural substance is a simple and cost-effective technique. In addition, honey is a natural product without any side effects and is easily tolerated by the child due to its pleasant taste and aroma. Therefore, its use is recommended after minor and even major surgeries in the oral cavity. This natural substance can also be used in patients who undergo several tooth extractions under general anesthesia or those undergoing major surgeries or those with systemic conditions that disrupt the wound healing process.


   Conclusion Top


Based on the results of this study, honey decreased wound size and accelerated wound healing after tooth extraction in children. Use of this natural substance is easy and cost-effective. In addition, honey has no side effects as a natural substance and due to its good taste and aroma it is easily tolerated by children. Therefore, it is recommended that it can be used after minor and major surgeries of the oral cavity. However, the positive effect of the honey can be due to the additive effect of honey and normal saline, so to specify the pure effect of honey more studies are recommended.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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