A Randomized Controlled Trial: The Effect of Own Mother's Breast Milk Odor and Another Mother's Breast Milk Odor on Pain Level of Newborn Infants

Abstract

Objective:

Our research was conducted empirically to determine whether another mother's breast milk could be used to reduce the pain of newborns who were not able to access their own mother's milk for any reason.

Materials and Methods:

The sample group of the research included 90 newborns [smell of own mother's milk (30), smell of another mother's milk (30), and the control group (30)] hospitalized in the unit. A neonatal information form was used as the data collection tool, the Neonatal Pain, Agitation, and Sedation Scale (N-PASS) was used to assess the newborn's pain, and an evaluation form prepared by the researcher was used to record the findings.

Results:

The group which was exposed to their own mother's milk had a significantly lower N-PASS mean score compared to other groups and the group which was exposed to another mother's milk was observed to have a significantly lower N-PASS mean score compared to the control group (p < 0.05). While the median values for the total time spent crying of the “own mother's milk” group and the “another mother's milk” group were similar; the total time spent crying of the control group had a significantly higher median value.

Conclusion:

Our research determined that, while the most effective method for reducing pain in newborns was the smell of their own mother's breast milk, for newborns who were not able to access their own mother's breast milk, the smell of breast milk from a different mother could also be used.

Introduction

Today, it is known that the neuropsychological bases of pain have developed by the end of the second trimester of pregnancy, and that babies can feel pain.¹ Pain memory develops in the intrauterine period,² and the pain that is experienced in early periods is recorded in operational memory.³ This information indicates that newborns can experience pain as much as other age groups and that pain negatively affects the newborns.⁴

Newborns can experience pain for many reasons, but especially as a result of invasive procedures. Newborns who are placed in a neonatal intensive care unit (NICU) have to go through several invasive procedures for diagnostic and treatment purposes.⁵ This experience of pain affects the baby's behavior, the family-baby interaction, and the baby's adaptation to the extrauterine world; and it can negatively affect the growth of the baby.⁶ It is thus very important to correctly evaluate and control pain. The greatest responsibility in this regard falls to the nurses who spend the most time with the newborns and have the opportunity to constantly monitor them.

Nurses should evaluate the pain in a timely and accurate manner, and use an appropriate approach to try and keep the pain within tolerable limits.⁷ Suitable pharmacological and nonpharmacological methods can be used for pain control. There are many nonpharmacological methods for reducing pain. These include interventions such as kangaroo care,⁸ positioning, pacifiers, breastfeeding,^9–11 oral administration of sweet solutions,¹² and music.¹³ Another effective nonpharmacological method is to use the sense of smell.¹⁴

A baby's sense of smell starts to develop in the intrauterine period. The newborn has developed olfaction by the 26th to 28th week of gestation.¹⁵ Olfaction is one of the most sophisticated senses that enables the creation of an emotional connection between mother and newborn and causes the neonate to show various behavioral reactions.¹⁶

Odors are known to have a pain-relieving effect. This effect is thought to occur through the secretion of neurotransmitters.¹⁷ Newborns can be exposed to a familiar smell, such as their mother's odor, the odor of her breast milk, or of the amniotic fluid,¹⁸ to relieve pain. They can also be given soothing odors such as lavender and vanilla.^18,19 Studies have shown a reduction in spontaneous crying when newborns are exposed to the odor of amniotic fluid²⁰ or another maternal odor.²¹

Studies show that the smell of breast milk reduces pain in the newborn.²² However, there is insufficient information about whether the odor of another mother's breast milk can be used to reduce the stress and pain of a newborn, if the milk from the mother is not available for any reason. For this reason, our study aimed to evaluate the effects of the smell of their own mother's milk and the smell of the breast milk from another mother on the babies' pain levels during venous blood sampling in an NICU.

Hypotheses

H1: The smell of its own mother's breast milk is effective in reducing the pain associated with venous blood sampling in term infants

H2: The smell of another mother's breast milk is effective in reducing the pain associated with venous blood sampling in term infants

H3: Between exposing a baby to the smell of its own mother's milk and exposing it to the smell of another mother's milk during venous blood sampling, no difference in reducing the pain.

H4: Between exposing a baby to the smell of another mother's breast milk and the control group, no difference in reducing the pain associated with venous blood sampling in term infants.

Materials and Methods

Type of study, place, and time

This was an experimental, randomized, controlled study. The study was conducted between August 1 and December 1, 2017 in the NICU of a hospital in Eskisehir, Turkey. This study was approved by the Clinical Research Ethical Committee, and a permit was obtained from the hospital. Only babies from parents who gave informed consent were included in the study.

Research population and sample

The universe of the research was the newborns (N = 184) who were placed in the NICU of a hospital in Eskisehir, between August 1 and December 1, 2017. The sample size was determined through the power of analysis. Using similar studies in the literature,^18,20,21 it was determined that a total of 54 newborns, 18 in each group, were needed to have a power of 0.90 with β = 0.10 and α = 0.05. However, the study went beyond this number and was completed with 90 newborns who met the sampling selection criteria and whose parents had been informed about the study. The power of the study was found to be 0.99 (β = 0.10 and α = 0.05) in the power analysis with 90 newborns at the end of the study.

The study consisted of three groups. These were the group exposed to the odor of their own mother's breast milk (first Group), the group given the odor of another mother's breast milk (second Group), and the control group (third Group). The stratification and blocking methods were used to assign subjects to the groups. Newborns meeting the sample selection criteria were stratified according to week of gestation, and then the infants were assigned to the groups by the lottery method (blocking) by researcher so that each group would have an equal number of infants. Each group had 30 subjects.

The inclusion criteria were as follows: being born at term, having had no analgesics and/or sedatives in the previous 24 hours, having no condition that impeded pain assessment (intracranial hemorrhage, neuromotor developmental failure, etc.), having had no new painful interventions within the previous hour (e.g., blood sampling, aspiration, eye examination, etc.), not using mechanical ventilation, not having had any surgical procedure.

The exclusion criteria were as follows: being premature, having parents who had not agreed that the baby could participate in the research and/or who asked to leave the research while it was ongoing, and having experienced a failure of the initial intervention and subsequently requiring multiple trials.

Data collection tools

To collect data in the study a Neonatal Identification Information Form, Data Evaluation Form, and the Neonatal Pain, Agitation, and Sedation Scale (N-PASS) were used.

Neonatal identification information form

This was a form created by the researcher containing the questions regarding the identification of the newborn.

Data evaluation form

This was a form created by the researcher to evaluate the heart rate, respiratory rate, oxygen saturation, and time spent crying of the newborn before, during, and after blood sampling.

Neonatal pain, agitation, and sedation scale

This scale, which can be used in both term and preterm newborns, was developed by Hummel et al. in 2003 to evaluate acute and/or chronic pain. The scale was adapted to Turkish in 2011 by Acikgoz et al.²³ The Cronbach's alpha internal consistency coefficient was found to be 0.797 for the preprocess and 0.917 for during and after the process. The N-PASS consists of two separate parts measuring the level of the baby's sedation and the level of pain; crying and restlessness, behavior-state, facial expression, hand and foot and body tension, and vital findings. The total pain score is between 0 and +11, and the total sedation score is between 0 and −10. A high score indicates severe pain. The purpose of the treatment is to keep the pain score at 3 or lower.^23–24

Data collection

Ethical considerations

This study was approved by the Clinical Research Ethical Committee, and a permit was obtained from the hospital. Only babies from parents who gave informed consent were included in the study. All protocols conformed to the ethical guidelines of the Declaration of Helsinki 1975.

In a routine clinical procedure, no odor is applied to the newborns. Parents of the newborns involved in the study were informed of the study. Three groups were stated to be in the study. It was explained to all parents that the first group would smell their mother's breast milk, the second group would smell different breast milk, and the third group would not smell any odor. Then, the group in which the babies would be included was specified. Infants of the parents who agreed to participate in the study after the informing process was completed were included in the study.

Application

The newborn identification information form was filled by the researcher with information from the mother and the patient file.

A loose swaddling was applied to the newborns in all groups as a pain control intervention. Before the procedure began, a radiant heater was placed in the baby's NICU and the newborn was then taken to the bed where the procedure was to be performed and monitored for blood sampling. Heart rate, respiratory rate, and oxygen saturation were measured and the N-PASS and pain levels were assessed by two independent people (one being a researcher, the other being a nurse who was not a researcher and who performed the intervention). The relationship between the N-PASS scores independently obtained by the two observers at the end of the study was calculated using the intraclass correlation coefficient (ICC). ICC values were found to be 0.98 before the procedure, 0.99 during, and 0.81 after the procedure. Our study shows that the results obtained by the researcher and the independent observer were consistent.

Procedural steps are shown in Figure 1.

FIG. 1.

Process implementation steps.

Analysis and evaluation of data

The data were analyzed using the IBM SPSS 21 package program (IBM Corp. Released 2012. IBM SPSS Statistics for Windows, Version 21.0. IBM Corp., Armonk, NY) and Minitab 17 (Minitab 17 Statistical Software, 2010. [Computer software]. Minitab, Inc., State College, PA). Normal distribution of quantitative variables was investigated using the Shapiro–Wilk test. The summary representation of the quantitative variables with a normal distribution is given as the mean ± standard deviation, and the nonnormally distributed data are presented as median (Q1–Q3). The Mann–Whitney U test was used to compare the N-PASS scores according to the delivery method and gender. For the comparison of groups that had more than one subcategory one-way ANOVA was used if the distribution of data was normal, and the Kruskal–Wallis Test was used if the data were abnormally distributed. In the one-way ANOVA, multiple comparisons were made with the Tukey's test when the variances were homogeneous. In the Kruskal–Wallis test, paired comparisons were performed using Dunn's Test. The average N-PASS scores, heart rates, respiratory rates, and oxygen saturation values before, during, and after treatment were analyzed using two-way analysis of variance (single factor repeat). Multiple comparisons of group and repeated measurements were made with least significance difference. Qualitative variables in this study were shown as frequency and percentage. The relationship between qualitative variables was examined using the Pearson's chi-square and Pearson's exact chi-square analysis. Results obtained with p < 0.05 were accepted as significant.

Results

There was no statistically significant difference between the three groups in terms of gestation week, gender, pattern of nutrition, postnatal age, first and fifth minute Apgar scores, last feeding time, birth weight, birth height, head circumference, and the current weight of the newborns (Table 1) (p > 0.05). These results indicate that the intervention and control groups were similar in terms of variables.

Table 1.

Intergroup Comparison of the Newborn Identification Features

	Own mother's breast milk odor		Another mother's breast milk odor		Control group		Total
	N	%	N	%	n	%	N	%	Chi-square	p
Gestation week
38–38⁺⁶	10	33.3	10	33.3	10	33.4	30	100.0	0.000	1.000
39–39⁺⁶	10	33.3	10	33.3	10	33.4	30	100.0
40	10	33.3	10	33.3	10	33.4	30	100.0
Gender
Girl	13	31.0	13	31.0	16	38.0	42	100.0	0.804	0.669
Boy	17	35.4	17	35.4	14	29.2	48	100.0	0.804	0.669
Nutrition pattern
Breast milk	4	57.1	0	0	3	42.9	7	100.0	8.208	0.080
Formula	0	0	2	33.3	4	66.7	6	100.0
Breast milk + Formula	26	33.8	28	36.4	23	29.8	77	100.0

	Medyan	Q1–Q3	Medyan	Q1–Q3	Medyan	Q1–Q3	Statistic	p
Postnatal age	3.00	2.00–6.25	2.50	1.00–4.00	3.00	2.00–6.25	4.957	0.084
Apgar score
First minute			9.00	9.00–9.00	9.00	9.00–9.00	3.519	0.172
Fifth minute	10.00	10.00–10.00	10.00	10.00–10.00	10.00	10.00–10.00	0.419	0.811
Last feeding time	75.00	60.00–90.00	60.00	60.00–90.00	90.00	45.00–90.00	1.131	0.568
Birth
Weight	3070.00	2905.00–3168.75	3000.00	2867.50–3366.25	3170.00	2873.75–3486.25	1.631	0.442
Height	49.00	48.00–50.00	48.00	46.75–50.00	48.00	46.00–50.00	0.204	0.903
Head circumference	35.00	34.00–35.00	35.00	33.75–36.00	35.00	33.75–35.00	0.662	0.718
Current weight	2970.00	2770.00–3092.50	2980.00	2857.50–3320.00	3162.00	2848.75–3441.25	4.139	0.126

When the average N-PASS scores during the procedure were examined, It was determined that the average N-PASS score of the “own mother's milk” group was lower than that of both the other groups, and that the average N-PASS score of the “another mother's” milk group was lower than that of the control group. These findings were statistically significant. When the postprocedural N-PASS average scores of the groups were compared, it was found that there was a significant difference between the “own mother's breast milk odor” group and the control group, and between the “another mother's breast milk odor” group and the control group (p < 0.001) (Table 2).

Table 2.

Inter- and Intragroup Comparison of Neonatal Pain, Agitation, Sedation Scale Score Averages Before, During, and After the Procedure

Groups (n = 30)	N-PASS			p
	X ± SS
	Min – Max
	(a) Pre-procedural	(b) During the procedure	(c) Post-procedural
(1) Own Mother's Breast Milk Odor	0.46 ± 0.14	4.40 ± 0.20	1.00 ± 0.19	a-b: <0.001
	0.00–2.00	2.00–7.00	0.00–3.00	b-c: <0.001
	0.00–2.00	2.00–7.00	0.00–3.00	a-c: 0.004
(2) Another Mother's Breast Milk Odor	0.56 ± 0.14	5.10 ± 0.20	1.27 ± 0.19	a-b: <0.001
	0.00–3.00	4.00–8.00	0.00–5.00	b-c: <0.001
	0.00–3.00	4.00–8.00	0.00–5.00	a-c: <0.001
(3) Control group	0.53 ± 0.14	7.83 ± 0.20	2.47 ± 0.19	a-b: <0.001
	0.00–3.00	5.00–9.00	1.00–5.00	b-c: <0.001
	0.00–3.00	5.00–9.00	1.00–5.00	a-c: <0.001
p	1–2: 0.619	1–2: 0.019	1–2: 0.332
	1–3: 0.740	1–3: <0.001	1–3: <0.001
	2–3: 0.868	2–3: <0.001	2–3: <0.001

Bold indicates significant at 0.01 ≤ p < 0.05; highly significant at 0.001 ≤ p < 0.01; very highly significant at p < 0.001.

N-PASS, neonatal pain/agitation sedation scale.

When oxygen saturation levels and average heart rate were examined, it was found that there was a statistically significant difference between the “own mother's breast milk odor” group and the control group, and between the “another mother's breast milk odor” group and the control group (p < 0.05) (Table 3).

Table 3.

Intergroup Comparison of the Heart Rate and Oxygen Saturations of the Newborns During the Procedure

		(1) Own mother's breast milk odor	(2) Another mother's breast milk odor	(3) Control group	p
Heart rate	X± SSMin–Max	153.40 ± 3.10	145.06 ± 3.10	162.96 ± 3.10	1–2: 0.610
					1–3: 0.032
					2–3: <0.001
Oxygen saturations		95.06 ± 0.33	95.00 ± 0.33	93.96 ± 0.33	1–2: 0.887
					1–3: 0.021
					2–3: 0.030

Bold indicates significant at 0.01 ≤ p < 0.05; highly significant at 0.001 ≤ p < 0.01; very highly significant at p < 0.001.

It was determined that there was a significant difference between the groups in terms of the total time spent crying (p < 0.001). The median values of the total time spent crying of the “own mother's breast milk odor” group and the “another mother's breast milk odor” groups were similar. However, the median time spent crying of the control group was found to be higher (Table 4).

Table 4.

Intergroup Comparison of Crying Time of Newborns

	n	Medyan (Q1–Q3)	Statistic^*	p	Multiple comparison
Total crying time (sn) (during the procedure + postprocedural)
(1) Own mother's breast milk odor	30	20.00 (16.75–23.25)	54.096	p < 0.001	1–3: p < 0.001
(1) Own mother's breast milk odor	30	20.00 (16.75–23.25)			2–3: p < 0.001
(2) Another mother's breast milk odor	30	20.00 (15.75–25.00)
(3) Control group	30	45.50 (35.75–55.25)

Bold indicates very highly significant at p < 0.001.

Kruskal Wallis test.

Discussion

Intergroup comparisons revealed that there was no significant difference between the preprocedural N-PASS score averages (p > 0.05) and that the groups were similar. However, when the N-PASS scores during the procedure were evaluated, it was determined that there was a significant difference between the groups (1–2: p = 0.019, 1–3: p < 0.001, 2–3: p < 0.001). It was determined that the N-PASS score of the “own mother's breast milk” group was lower than the control group, and the N-PASS score of the “different mother's breast milk” group was lower than the control group (Table 2). These results were statistically significant. They showed that the most effective method for reducing baby's pain during venous blood sampling was the smell of its own mother's milk, and that the smell of a different mother's milk was significantly more effective than not being exposed to any smell (the control group). When the postprocedural N-PASS scores of the groups were compared, it was found that there was a significant difference between the “own mother's breast milk odor” group and the control group and between the “another mother's breast milk odor” group and the control group (1–3: p < 0.001, 2–3: p < 0.001). This result is also important in that the postpartum baby's pain responses were reduced and/or terminated earlier than in the control group in the “own mother's breast milk odor” and “another mother's breast milk odor” groups.

Studies^16,18,25 have shown that the odor of breast milk has positive effects on the newborns. Doucet et al.,²⁶ in their study of 55 healthy newborns born between the 38th and 42nd gestational week, noted that the smell of breast milk was associated with mouth opening, licking, stimulation of eyes, and decreased and delayed crying in newborns. In another study²⁷ using the smell of breast milk and formula milk during heel lance, the pain scores of newborns who smelled breast milk were significantly lower than the other group. However, in terms of pain-relieving effects of the smell of breast milk from a different mother, only the study of Nishitani et al.²¹ was available in the literature. In this study, 48 healthy term newborns were divided into four groups; an “own mother's breast milk odor” group, a “different mother's breast milk odor” group, a “formula milk” group, and a control group. It was found that the newborns who smelled their own mother's breast milk odor during heel lance had significantly less pain than the newborns in the other groups. No significant difference was found between the other groups. This study is similar to our results in terms of newborns who smell their own mother's milk experiencing less pain. However, in our study, it was determined that there was also a significant difference between the “another mother's breast milk” group and the control group. Newborns smelling the milk of a different mother were found to have less pain than the control group. Contrary to Nishitani's work, studies have shown that the newborns have a significant positive response to different mom's scents²⁷ and familiar smells such as vanilla.^19,28 Nishitani et al. has attributed the reason for this result being different than the other studies to the difference in postnatal ages of the infants. Nishitani et al. suggested that scent-based responses in newborns may include factors associated with both biological and prenatal/postnatal experience. Although our study result is different from Nishitani et al., it is similar to the studies showing that different mom's scent or a different familiar scent (such as vanilla scent) is effective in newborns. Our result is important because it shows that the milk from another mother can be used in newborns whose mother is not present. We can conclude that the N-PASS score of newborns exposed to the smell of another mother's breast milk smell in our study was lower than that of the control group because the newborns responded positively to familiar smells.^18,26–30

In our study, it was found that there was a significant difference (p < 0.05) between the “own mother's milk” and the control group and between the “another mother's milk” group and the control group in terms of the heart rate (beats/min) and oxygen saturation. It was determined that the control group was the group with the highest average heart rate and lowest oxygen saturation. Similarly, different studies^18,26,31,32 suggest that breastfeeding affects neonatal heart rate and oxygen saturation positively during invasive interventions. Another study by Aoyama et al.³⁰ found that the smell of breast milk significantly increased oxygenation saturation in the orbitofrontal region of newborns compared to the group that smelled formula. Although a statistically significant difference in oxygen saturation levels was noted between the study groups, given that the levels were all over 90% its clinical significance remains to be determined.

When the total time spent crying was compared between the groups in our study, there was a significant difference between the “own mother's milk” group and the control group and between the control group and the “another mother's breast milk” group (1–3: p < 0.001; 2–3: p < 0.001). While the median values of the total time spent crying of the “own mother's breast milk” group and the “another mother's breast milk” group were similar, the median value of the total time spent crying of the control group was significantly higher than that of the other groups. It is stated in the literature^21,28 that smelling breast milk affects the time newborns spend crying, which is similar to our results. In another study²⁰ comparing the smell of the mother's milk, the smell of amniotic fluid, and the smell of the mother, there was no significant difference in terms of time spent crying, but it was found that newborns who smelled amniotic fluid cried for less time. In our study, it was determined that there was a significant difference (p < 0.001) between the time spent crying of the newborns in the control group and the newborns in the “another mother's breast milk” group, and that the newborns who smelled a different mother's breast milk cried less than the control group. This also supports the notion that the odor of different mother's milk can be used when taking blood from infants whose mother is not present or available.

Limitations of the study

The study was carried out only during venous blood sampling and with term babies.

In the study, the babies were fed in three different ways (breast milk only, formula milk only, and breast milk + formula milk). This is a limitation. However, comparison between the three groups revealed that they were similar in this respect.

In our study, the last feeding times of newborns were different. However, there was no significant difference between the groups in this regard and the groups were similar (p > 0.05).

Conclusions and Suggestions

This study has shown that the most effective method for reducing pain in newborns is the smell of their own mother's breast milk, but the smell of another mother's breast milk can also be used with newborns whose mother is not present. We thus recommend that the smell of their own mother's breast milk be used with newborns during venous blood withdrawal, or, where the mother is not present, the smell of another mother's breast milk. A further recommendation is that blind studies be conducted using the smells of different mother's breast milk with different interventional procedures and with infants at different gestational weeks.

Footnotes

Disclosure Statement

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding Information

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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