The Effect of Inhaling Mother’s Breast Milk Odor on the Behavioral Responses to Pain Caused by Hepatitis B Vaccine in Preterm Infants: A Randomized Clinical Trial

doi:10.21203/rs.3.rs-45921/v1

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The Effect of Inhaling Mother’s Breast Milk Odor on the Behavioral Responses to Pain Caused by Hepatitis B Vaccine in Preterm Infants: A Randomized Clinical Trial

https://doi.org/10.21203/rs.3.rs-45921/v1

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Background: Pain control in preterm infants is especially important if the necessary measures are not taken in this regard, the evolutionary process of the brain will be disrupted, and the unrelieved pain can have lifelong consequences. The aim of this study was to compare the effect of maternal breast milk odor (MBMO) with that of another mother’s breast milk odor (BMO) on the behavioral responses to pain caused by hepatitis B vaccine (HBV) injection in preterm infants.

Methods: This single-blind randomized clinical trial was performed in the neonatal intensive care unit of Babol Rouhani Hospital, Iran from February 2019 to March 2020. Totally, 90 preterm infants who were to receive the HBV for the first time were randomly selected by random sampling. The neonates were randomly assigned into three groups of (A) MBMO (B) another mother’s BMO and (C) control (distilled water).

The data were collected using a questionnaire of demographic characteristics and premature infant pain profile (PIPP). Physiological data were recorded by the pulse oximeter immediately before and after the intervention. The data were analyzed using SPSS18 through chi-square, ANOVA and ANCOVA, and P<0.05 was considered as significant level.

Results: Before intervention, there was no significant difference between groups in the mean of heart rate, blood pressure and arterial oxygen saturation (SaO2) percentage (P>0.05). After intervention, there was no significant difference between these A, B and C groups in the mean of systolic blood pressure (70.90±8.29, 70.27±6.70 and 71.77±9.07), diastolic blood pressure (43.63±9.59, 41.77±7.10 and 44.03±10.76) and SaO2 percentage (95.20±5.20, 94.00±6.23 and 91.13±11.78), respectively (P>0.05).

However, after intervention, there was a significant difference between groups of A, B and C in the mean of heart rate (146. 6±14.3, 153.70±17.5 and 155.70±17.7), respectively (P=0.01). Moreover, the mean PIPP score was 6.6±1.3, 10 ±2 and 11.4±1.9 in groups A, B and C respectively, so that a significant statistical difference was found between groups (P<0.001).

Conclusions: Stimulation with MBMO is effective in reducing the pain of preterm infants, so it can be used in less invasive procedures such as vaccination.

Trial registration: IRCT, IRCT20190220042771N1. Registered 18 May 2019- Retrospectively registered, https://en.irct.ir/trial/37646

Pediatrics

Pain

Premature infant

Human milk

Odor

Hepatitis B vaccine

Preterm infants need specialized care in the neonatal intensive care unit (NICU) (1). Many of the measures taken in these units are accompanied by pain. Neonatal pain management is very important because infants are unable to express their pain verbally (2). The infant’s brain is growing, and in response to the painful stimulus, there are changes in response to subsequent stimuli that cause permanent damage to the developing organs and cognitive development (3).

Many clinical studies have shown that failure to treat pain leads to short-term complications and long-term physiological, behavioral and cognitive consequences including changes in pain processing, attention deficit disorder, impaired visual-perceptual ability, visual-motor integration and poor performance (4).

Pain assessment methods are performed using physiological (heart rate and respiration rate) and behavioral criteria (crying time, facial expression changes and organ movements) (5).

The premature infant pain profile (PIPP) is a set of measurable behavioral and physiological responses such as facial expression changes (squeezing eyes, raising eyebrows, wrinkling nasolabial groove) as well as changes in heart rate and decreased arterial oxygen saturation (SaO2), intrauterine age and behavioral status of the infants which are definite reasons for their pain (6).

Since painful treatments are very common in sick and preterm infants and there are concerns about the side effects of medications, there is a strong tendency to use non-pharmacological interventions as a simple and safe way for infants’ pain relief. Several methods have been applied to relieve pain based on five senses (7). Among them, the smell sense is fully developed at birth (8).

The human baby indicates significant changes even in low-concentration odors (9). Familiar odors for neonates such as maternal odor have soothing effects on the neonate. The human infant has the ability to detect the mother's breast odor without experiencing breastfeeding on the first day of life (10). On the other hand, the smell sense affects the neonate’s emotional relationship with his/her mother (11).

The breast milk odor (BMO) enhances infant’s sucking through the facial and trigeminal motor nerves in the brainstem, which, in turn, stabilizes the physiological state in the infant (12). In addition to health, nutritional, evolutionary, psychological, social and environmental benefits, mother’s breast milk effectively reduces infant’s pain during painful processes (13).

Some studies have shown that fetal-maternal odors (mother’s breast milk, body and amniotic fluid odors) can decrease stress responses including crying and motor activities in infants separated from breast milk or under painful interventions (14). In a study, it was suggested that the maternal breast milk odor (MBMO) had a soothing effect on preterm infants, and their pain score was lower than that in the infants exposed to formula odor (15).

Nevertheless, the results of Alemdar et al. (2017) demonstrated that the BMO had no statistically significant difference in the physiological and behavioral responses of MBMO group compared to other groups (amniotic fluid odor, maternal body odor and control groups) (16).

Given the contradictory studies, lack of evidence for the effect of MBMO and another mother’s BMO on preterm infants as well as importance of pain relief, this question arises in mothers who cannot breastfeed their baby for various reasons or perform kangaroo mother care, “is the use of this method effective in relieving the pain and soothing the infant?

Therefore, the aim of the present study was to determine the effect of inhaling the MBMO and another mother’s BMO on the behavioral responses of pain caused by HBV in preterm infants admitted to the NICU of Babol Rouhani Hospital.

Design

The study adopted a randomized clinical trial with single-blind to compare the effect of inhaling the MBMO and another mother’s BMO on the behavioral responses of pain caused by HBV. Ninety premature infants needing HBV procedures were randomly assigned to three groups.

The primary outcome was the pain experienced during HBV injection which was measured using PIPP. The secondary outcome was the effect of MBMO or another mother’s BMO on improving the physiological responses of hospitalized preterm infants, variables including systolic blood pressure (SBP), diastolic blood pressure (DBP), SaO2 percentage and heart rate. This study followed the CONSORT guidelines for reporting randomized controlled trials.

Setting and sample

The sample was recruited From a NICU at Rouhani Hospital in Babol, Iran from February 2019 to March 2020. Sampling was determined using available and random method through the rank of intervention and control groups. After obtaining written consent from the parents, each of the eligible subjects was assigned a number. The numbers were written on paper and tossed into the box, and the desired number was taken out of the box by drawing lots based on the assigned rank. Statistics specialist generated the random allocation sequence, the fifth Author enrolled participants, and assigned participants to interventions.

Then, 90 preterm infants were randomly selected based on hospital stay time and divided into three groups of 30 (control, MBMO and another mother's BMO). The minimum sample size was calculated to be 30 infants in 3 groups (MBMO, another mother's BMO and distilled water) with test power of 80% and error of 0.05.

The inclusion criteria were infants with:(1) a gestational age of 28-37 weeks,(2) no painful procedure for up to one hour before the intervention,(3) no feeding for one hour before the intervention,(4) stability in terms of vital signs,(5) no head and skull abnormalities such as choanal atresia as well as no receiving painkillers,(6) sedatives and anticonvulsants. The exclusion criteria were: maternal withdrawal from the study and infant mortality.

Data collection and processing

Every preterm neonate was individually taken to a quiet room with no noise to inject HBV for the first time. According to the ward's schedule, the first to fourth days after the birth of preterm infant, the HBV was given.

The neonate was placed on a warmer at 37C. All conditions including room temperature at 25◦C, light, vaccine administration, injection device were the same for all three groups as well as the vaccine was administered to all infants under the same conditions and devices by one person.

The researcher and nurse did not use aromatic substances in vaccine room during the study. The oximeter pulse was placed by the researcher on the right wrist of the preterm infant without applying additional pressure. In both groups of MBMO and another mother's BMO, the breast milk samples taken in the early morning before eating breakfast were used to stimulate the smell sense of neonates. Pouring 2 cc of maternal breast milk and another mother’s breast milk on a cotton swab was done as an intervention, and 2 cc of distilled water was poured on a cotton swab in control group. Next, these swabs were placed three centimeters away from the baby's nose. This process started 3 min before vaccination and continued until the vaccination was completed (2).

Pain measurement

The Premature Infant Pain Profile (PIPP) was used as the primary outcome variable. PIPP scores were recorded immediately before and after the vaccination for each infant. The PIPP is a behavioral measure of pain for premature infants. It includes seven indicators: 1) gestational age, 2) the behavioral state, 3) change in heart rate, 4) change in oxygen saturation, 5) brow bulge; 6) eyes squeeze and 7) nasolabial furrow. The scoring is presented in Table 1.

Table 1

Premature infant pain profile
Indicators	0	1	2	3
GA in weeks	≥ 36weeks	32 to 35weeks and days	28 to 31weeks and 6days	< 26weeks
Alertness	Active	Quiet	Active	Quiet
	Awake	Awake	Sleep	Sleeping
	Open Eyes	Open eyes	Closed eyes	Closed eyes
	Facial movements present	Nofacial movements	Facial Movements present	No
facial movements
Maximal HR	↑ 0 to 4bpm	↑ 5 to 14bpm	↑ 15 to 24bpm	↑ ≥25bpm
Minimal Saturation	↓ 0 to 2.4%	↓2.5 to 4.9%	↓ 5 to 7.4%	↓ ≥7.5%
Frowned forehead	Absent	Minimal	Moderate	Maximal
Eyes squeezed	Absent	Minimal	Moderate	Maximal
Nasolabial furrow	Absent	Minimal	Moderate	Maximal

The heart rate and SaO2 percentage of all preterm infants were recorded before starting the intervention as the initial time and immediately after the completion of the vaccination using the standard pulse oximeter and EKG monitor (Saadat Company, Iran).

Filming of behavioral responses was taken from the beginning to the end of the process using PIPP by the fifth Author, and then scoring was performed through watching video by the first author. She was blind to the infants’ assignment into three groups. Throughout the intervention, any actions on the neonates such as contact, movement and so on were avoided.

Data were collected by using the demographic questionnaire (birth weight, current disease, sex, fetal age, neonatal age, Apgar score) and PIPP. The tool is used to assess pain in premature infants with 7 indications including gestational age, behavioral status, heart rate, squeezing eyes, raising eyebrows, SaO2 and nasal groove. Each item has a score of 0 to 3, and the total score is between 0 and 21 (2). The PIPP tool was used in the study of Badiee et al. (2013) who confirmed its reliability and validity (2).

The data was entered into SPSS Version 18. Descriptive information was shown as frequency, percentage, mean and standard deviation. The pain reported as mean ± SD .The collected data were analyzed through chi-square, ANOVA and ANCOVA tests. Chi-square test for the relationship between two qualitative variables (demographic and PIPP qualitative variables with group variable), ANOVA test for comparing quantitative variables at the levels of more than two variables (quantitative demographic variables with group variable) and ANCOVA test for comparing research outcomes (SBP, DBP, SaO2 percentage and heart rate) were used to remove the pretest effect. The level of significance was set at p < 0.05 in all tests.

Ethical consideration

The study protocol was approved by the Ethics Committee of the Ethics Committees of Babol University of Medical Sciences (IR.MUBABOL.REC.1397.253). The trial is registered in the IRCT20190220042771N1 Before participation in the study, written informed consent was obtained from each child’s primary guardian.

Study subjects

In the present study of 90 preterm infants, The infants of the three groups were not significantly different in terms of gender, Infant’s age, Infant's current disease, gestational age, Infant’s weight and Infant’s Apgar score (p>0.05) (table 2).

Table 2

Comparison of demographic variables of preterm infants in three groups
Group Variables		Control N=30	Another mother’s BMO N=30	MBMO N=30	Significant level
Group Variables		Frequency (Percentage)	Frequency (Percentage)	Frequency (Percentage)	Significant level
Gender	Male	(40) 12	(3/53) 16	(50) 15	56/0 P= Chi²
Gender	Female	(60) 18	(7/46)14	(50)15	56/0 P= Chi²
Infant’s age (Day)	One-day	(7/66)20	(40)12	(3/53)16	11/0 P= Chi²
Infant’s age (Day)	Two-day	(3/33)10	(60)18	(7/46)14	11/0 P= Chi²
Infant's current disease	Respiratory distress	(10)3	(3/13)4	(10)3	94/0 P= Chi²
	Preterm	(7/67)23	(7/67)23	(3/73)22
	Transient tachycardia of the newborn	(3/13)4	(10)3	(7/16)5
Infant’s gestational age (WK) (SD±Mean)		44/2±53/32	17/2±53/31	49/2±93/32	07/0P= ANOVA
Infant’s weight (g) (SD±Mean)		02/404±83/1688	03/425±1620	72/553±33/1806	29/0 P= ANOVA
Infant’s Apgar score(SD±Mean)		95/0±30/8	32/1±63/7	08/1±83/7	07/0 P= ANOVA

In evaluating the effect of BMO on improving the physiological responses of hospitalized preterm infants, variables including SBP, DBP, SaO2 percentage and heart rate were analyzed using ANCOVA before and after the intervention (Table 3).

Table 3

Mean and standard deviation scores of SBP, DBP, SaO2 percentage and heart rate in the studied groups
Groups	MBMO		Another mother’s BMO		Control
Variables	Pre intervention	Post intervention	Pre intervention	Post intervention	Pre intervention	Post intervention
SBP (mm Hg)	45/9±33/69	29/8±90/70	62/7±50/69	06/6±27/70	05/9±73/69	09/9±77/71
DBP (mm Hg)	87/9±63/40	59/9±63/43	93/9±87/40	10/7±77/41	59/7±90/40	76/10±03/44
SaO2 (%)	76/2±00/97	27/5±23/95	78/3±10/97	23/6±00/94	26/3±47/96	78/11±13/91
Heart rate	17/16±00/139	37/14±67/146	66/15±70/141	53/17±77/153	87/17±90/139	70/17±73/155

Table 4

ANCOVA of post-test scores of SBP and DBP, SaO2 percentage and heart rate in the studied groups.
Variable statistical indicator		Freedom degree	Mean squares	F	ANCOVA significance	Effective rate
SBP(mm Hg)	Pretest	1	99/3921	31/219	00/0>	02/0
SBP(mm Hg)	Group membership	2	18/13	73/0	48/0 P=	02/0
SaO2(%)	Pretest	1	52/2496	16/51	01/0>	02/0
SaO2(%)	Group membership	2	71/45	16/0	34/0 P=	02/0
DBP (mm Hg)	Pretest	1	56/1080	04/19	001/0>	40/0
DBP (mm Hg)	Group membership	2	74/94	67/1	19/0 P=	40/0
Heart rate	Pretest	1	83/14185	33/124	001/0>	10/0
Heart rate	Group membership	2	46/532	66/4	01/0 P=	10/0

As shown in table 3, by eliminating the effect of the pretest variable, there is no significant difference between the estimated means of SBP (p=0.48), DBP (p=0.34) and SaO2 percentage scores (p=0.19) in terms of group membership.

Therefore, the effect of the intervention on SBP, DBP and SaO2 percentage was statistically ineffective (Table 4).

However, by eliminating the effect of the pretest variable, no significant difference was found between the estimated means of heart rate scores in terms of group membership. It could be concluded that the heart rate decreased in MBMO group compared to control and another mother's BMO groups.

PIPP score

In assessing the effect of MBMO on the mean scores, the PIPP in preterm infants admitted to the hospital was analyzed after the intervention using ANOVA test so that the group had a significant effect on the PIPP (P<0.001). In evaluating the means, it was found that the mean pain was 6.60±1.35, 10.07±2.03 and 11.43±1.97 in MBMO, another mother’s BMO and control groups, respectively. Hence, the results of post-hoc Tukey's test suggested that the difference was significant in all three groups.

The findings from the present study demonstrated that the MBMO decreased the behavioral responses to pain caused by HBV in preterm infants and reduced heart rate in MBMO group rather than another mother’s and control groups, but was ineffective on other physiological indicators such as SBP, DBP and SaO2 percentage.

Zhang et al. (2018) conducted a systematic review study to investigate the analgesic effects of BMO on infants. Their meta-analysis results demonstrated that the heart rate changes and SaO2 percentage during and after the procedure were lower in MBMO group than in control group at the time of pain sampling (17) which are consistent with the finding of the current study, except for SaO2 percentage. Stimulation with MBMO has a soothing effect on the behavioral responses to pain and reduces infant’s pain.

This odor stimulation can restore the memory associated with the calm that the infant enjoys mother's presence, and thus alleviate the behavioral reactions caused by pain.

In the ongoing study, the mean score of PIPP was lower in the group receiving BMO than the other two groups. The results of Sajjadi et al. (2016) illustrated that the mean scores of PIPP had a significant difference in MBMO group compared to control group. Moreover, a significant difference was found in the means of heart rate and SaO2 percentage after intervention.

Their results are similar to those of the present study, except for percentage decrease in SaO2. This difference in SaO2 percentage may be due to the different types of pulse oximeter (in their study, purchased from Poyandegan Rah Salamat Company and in our study, purchased from Saadat Company).

Jebreili et al. (2014) expressed that there was a statistically significant difference between mean scores of PIPP in the MBMO group compared to control group during and after blood sampling. The use of MBMO has a reducing effect on pain control in painful treatments such as intravenous blood sampling (8), which are in line with the ongoing study.

Alemdar et al. (2017) conducted a study on the effect of mother’s BMO, amniotic fluid odor and body odor on physiological and behavioral responses to heel stick pain in preterm infants admitted to the NICU in Girsan, Turkey.

They expressed that there was no statistically significant difference between groups in terms of physiological and behavioral responses to pain such as heart rate, duration of crying and pain level. Only in the amniotic fluid odor group, the SaO2 percentage was slightly different (15), which are inconsistent with the results of the present study. One of the possible reasons for this discrepancy is the difference between both studies in terms of methodology and intervention type.

In above study, 5 cc of mother’s breast milk was poured on a sponge and placed five centimeters away from the neonate's nose for fifteen minutes before and after the intervention, while in our study, 2 cc of mother’s breast milk was poured on a cotton swab and placed three centimeters away from the infant's nose. This process in the current study started 3 min before vaccination and continued until the vaccination was completed.

In the ongoing study, the heart rate was significantly lower in MBMO group than in control group, but other physiological indicators such as blood pressure and oxygen saturation percentage had no difference.

Aziznejad et al. (2013) evaluated the physiological indicators and concluded that there was a statistically significant difference only in the respiration rate between sucrose and control groups immediately after the intervention, but there was no significant difference between four groups in other variables (crying duration, heart rate and SaO2 percentage).

They suggested that sucrose solution declined the pain severity and respiration rate (immediately after the intervention) in infants (18). Therefore, like our study, the maternal breast milk intervention was ineffective on the SaO2 percentage in their study.

The MBMO decreases the behavioral responses to HBV pain and heart rate compared to another mother’s BMO and control groups, while is ineffective on other physiological indicators including SBP, DBP and SaO2 percentage in preterm infants. Hence, when the mother is not present on the hospitalized neonate’s bed, the MBMO can be used as a familiar smell to manage the preterm infant’s pain before performing invasive procedures such as vaccination.

Individual differences in the response to infant pain can be influential.

ANOVA: Analysis of Variance; MBMO: Maternal Breast Milk Odor ; BMO: Another Mother’s Breast Milk Odor ; HBV: Hepatitis B Vaccine ; HR: Heart Rate ; NICU: Neonatal Intensive Care Unit; PIPP: Premature Infant Pain Profile ; SBP: Systolic Blood Pressure ; DBP: Diastolic Blood Pressure ; SaO2 : Arterial Oxygen Saturation

Ethics approval and consent to participate

The study protocol was approved by the Ethics Committee of the Ethics Committees of Babol University of Medical Sciences (IR.MUBABOL.REC.1397.253). The trial is registered in the IRCT20190220042771N1 after participation in the study, written informed consent was obtained from each child’s primary guardian.

Consent for publication

The article does not contain any individual’s details and consent for publication is not applicable.

Availability of data and materials

The datasets generated and analyzed during the current study are not publicly available due to an agreement with the participants on the confidentiality of the data but are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding

This research received a grant from Babol University of Medical Sciences (Grant number: 258-9706616). The Babol university of Medical Sciences did not have any role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.

Authors’ contributions

ASA Study conception/design, carried out the analysis, interpretation of the data and drafting the manuscript. PA First supervisor the study, Study conception/design, analysis, drafting of manuscript, critical revisions for important intellectual content, Administrative/ technical/ material support, Final revision. ZAR critically revised and checked closely the proposal, the analysis and interpretation of the data and design the article. HGA performed the data analysis and ZV contributed the data collection. All authors read and approved the final manuscript.

Acknowledgements

The authors would like to thank the Research Deputy of Babol University of Medical Sciences, authorities and colleagues of the Neonatal intensive care unit of Babol Rouhani Hospital as well as the infants’ parents who helped us in this research.

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The Effect of Inhaling Mother’s Breast Milk Odor on the Behavioral Responses to Pain Caused by Hepatitis B Vaccine in Preterm Infants: A Randomized Clinical Trial

Status:

Journal Publication

Version 1

Abstract

Figures

Background

Methods

Design

Setting and sample

Data collection and processing

Pain measurement

Ethical consideration

Results

Study subjects

PIPP score

Discussion

Conclusion

Limitations

Abbreviations

Declarations

Ethics approval and consent to participate

Consent for publication

Availability of data and materials

Competing interests

Funding

Authors’ contributions

Acknowledgements

References

Supplementary Files

Status:

Journal Publication

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