A Common Marmoset Model of Mother-Infant Intervention for Breastfeeding Disorders in the Presence of Paternal Inhibition and Maternal Neglect

Mayuko Yoda; Yoshimasa Kamei; Hayato Sakurai; Hiroko Kakei; Ting Tao; Hideo Yamanouchi; Tetsuya Kunikata; Masanori Hariyama; Ricki Colman; Mamiko Koshiba

doi:10.3791/64232

Behavior

A Common Marmoset Model of Mother-Infant Intervention for Breastfeeding Disorders in the Presence of Paternal Inhibition and Maternal Neglect

Published: September 22, 2023 doi: 10.3791/64232

Mayuko Yoda^1,2, Yoshimasa Kamei³, Hayato Sakurai⁴, Hiroko Kakei⁴, Ting Tao^1,2,4, Hideo Yamanouchi⁴, Tetsuya Kunikata⁴, Masanori Hariyama⁵, Ricki Colman⁶, Mamiko Koshiba^1,4,5

¹Graduate School of Sciences and Technology for Innovation, Yamaguchi University, ²Faculty of Health Sciences and Nursing, Juntendo University, ³Obstetrician, Medical Department, Saitama Medical University, ⁴Department of Pediatrics, Saitama Medical University, ⁵Graduate School of Information Sciences, Tohoku University, ⁶Department of Cell and Regenerative Biology and Wisconsin National Primate Research Center, University of Wisconsin, Madison

Summary

Here, we present a nonhuman primate model of mother-infant intervention for breastfeeding disorders in the presence of paternal inhibition and maternal neglect. The mate model video complements education to support primate and human caregivers with respect to infants with breastfeeding problems such as pain.

Abstract

Parents' psychological stress during the perinatal and neonatal periods continues to increase in an environment of declining birthrates, aging populations, and shrinking family sizes. The increase in child abuse and neglect cases, most likely by inexperienced and insufficiently knowledgeable parents, necessitates education on childcare and intervention techniques in nursing and midwifery training. In particular, attachment formation early in life between mother and infant is crucial. To accurately teach sensitive and comprehensive information on intervention techniques for mother-child attachment formation, realistic videos, and educational materials are necessary. Although pseudoeducational materials are available, they might be limited in explaining complex realism, particularly to support breastfeeding that involves both parents and child and that encourages interaction between the two.

In a previous study in a common marmoset (Callithrix jacchus) model, we experimentally controlled infant feeding and nurturing through 24 h of constant sensing and collected 1 month of quantitative data on psychological indices that possibly translated to psychological development. Age-dependent dynamic visualization of these data by multivariate analyses inferred causal relationships between early parental feeding and psychobiological rhythm formation. In the same primate model, we identified a spontaneous case of breastfeeding failure in which the father inhibited his neonatal infant's feeding and the mother appeared to abandon nurturing, leading to clinically significant weight loss in the infant.

Thus, we explored intervention techniques to promote mother-infant interaction. The mother was trained to allow the infant to spontaneously explore her breast. Initially, the mother refused to display the feeding pose potentially due to pain associated with breast engorgement. Massage was used to soften the breast and feeding was reintroduced. We hypothesize that activation of instinctive attachment formation mechanisms by encouraging spontaneity in each parent and child is the key to successful feeding intervention.

Introduction

The perinatal and neonatal periods are often stressful for parents. This is a particular problem in countries like Japan, where direct exposure to child rearing is limited given the countries' low birthrate, aging population, and tendency to live in nuclear families. This situation is exacerbated by a lack of institutionally supported education regarding child rearing¹. Against the background of this limited experience and the social problems associated with poverty, for instance, in younger couples, there is a high risk of postnatal growth failure related to breastfeeding issues in the presence of stress-related abuse and neglect by parents².

The establishment of breastfeeding by mothers separated from their infants after delivery is crucial for attachment formation and "the comparison between breastfeeding and formula feeding shows that the former has an effect on the development of rich emotions in newborns," suggesting a strong causal relationship between breastfeeding and attachment formation³. However, to improve early breastfeeding success and postnatal growth and development if there are medical problems in the infant or mother, it is often necessary to separate the infant from the mother to allow appropriate nutritional management of the newborn. Following the stabilization of the newborn, mothers must be provided guidance and support to successfully establish breastfeeding. Fathers, intimate partners, and other support individuals should be included in this instruction to learn how to nurture their child and provide appropriate support for breastfeeding⁴. Most of the available literature (e.g., "Environment and Nursing Intervention from Immediately After Delivery to Establishment of Breastfeeding") focuses mainly on interventions and support for mothers⁵. It is expected to be better taught to midwifery and nursing students' awareness and specific intervention skills to support breastfeeding that involves both the parents and child and that encourages interaction between the two.

Previously, we developed the common marmoset (Callithrix jacchus) as a small nonhuman primate model to explore the psychobiological basis of perinatal and neonatal interventions⁶. We designed a system that uses social scene-dependent changes⁷^,⁸^,⁹ and biomolecular activities¹⁰^,¹¹^,¹² to quantitatively identify developmental changes in the control of sensory (visual, auditory, tactile, olfactory) perception in different environments. Using principal component analysis (PCA), we were able to extract multiple explanatory behavioral factors, which allowed us to reproduce the complex neural network responsible for social psychological function in these animals. The results of this Behavior Output analysis for Quantitative Emotional state Translation (BOUQUET) method suggested that social interaction between adult males and females could be visualized quantitatively based on familiarity-dependent features in the same evaluation system¹¹. We hypothesized that differences in common marmoset behavior reflect each individual's psychocognitive learning in the past.

In this study, we compared animals in three conditions: siblings in a social environment where children interacted with each other, a single child that only experienced social interactions with their parent, and a situation similar to human foster care in which young were separated from any genetic family members. The BOUQUET analysis revealed quantitative differences in the time course of social response behavior development between groups, indicating that familial interactions (i.e., parents and siblings) during development influence the formation of social psychological functions¹³. In addition, we analyzed psychosocial development from postnatal day 15 to day 45 in marmosets using continuous infrared imaging in a situation replicating foster care in which formula was provided by the research staff. Data, including body surface temperatures, activity, and location preference, suggested the existence of unique age-dependent patterns. Further analysis indicated that experience during initial feeding periods may have significantly influenced behavioral rhythms after 1 month of development¹⁴. Circadian rhythms and their disruption are known to be closely related to mental functions that are required for human adaptability to an increasingly complex society, and their formation is influenced by early childhood experiences.

This report follows previous findings¹¹^,¹³^,¹⁴ to explore the feasibility of intervening in a case of breastfeeding failure in a common marmoset family displaying abuse-like behavior by the father and neglect-like behavior by the mother. While marmosets generally produce multizygotic multiples and are known for their communal raising of the offspring by not only the mother but also with the cooperation of the father and older siblings, this primate model involved a nuclear family, parents, and their only offspring, which aimed to mimic the current state of the human social condition. The first-time common marmoset parents exhibited disinhibited behavior followed by cessation of breastfeeding and infant abandonment, leading to the infant failing to thrive. The intervention and recovery process in this case of attachment dysfunction in a social feeding primate model was assessed through video records. The symptoms and treatment effects are indicated by an increase or decrease in body weight relative to the survival limit, referring to previously published criteria¹⁵^,¹⁶. The larger goal of this study is to determine the efficacy of human clinical interventions for the education of mothers and fathers who implement breastfeeding and the midwives who support them. Although the abandonment of vulnerable offspring with some problems by natural selection might be categorized as normal behavior for common marmosets, this clinical model aims to explore human evolutionary strategies of supporting health and well-being for the dignity of all life.

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Protocol

This study protocol was approved by the Institutional Animal Care and Use Committee of Saitama Medical University (2476).

1. Animals

House a pair of parents with their first-time infants of common marmosets (Callithrix jacchus) who have no experience raising any infants in a light-sealed incubated cage sized according to their welfare guidelines, maintaining constant temperature (25-30 °C), and a 12 h light/dark cycle). Set light intensity per cage at 750-930 lx during the light period and 0 lx during the dark period. Ensure that the parents are healthy with respect to feeding and cleaning.

2. The diagnosis of underweight and parental infant-rearing abnormality

Refer to the general diagnosis and intervention flows visualized in Figure 1 (A: Infant, B: Mother). When the infant is found to be underweight, choose intervention methods for the infant based on the presence or absence of five infant behaviors (crying, clinging to mother, head control, routing reflex, sucking) and for the mother based on the presence or absence of five maternal behaviors (the will to feed, breast enlargement, infant's sucking acceptance, milk secretion, and pain expression).
NOTE: Take care throughout to not cross-contaminate the animals' scent.

3. Animal characteristics

Gestational age at birth
1. Make a note of the common marmoset's full-term gestation period of approximately 140-150 days. This compares to the human standard full term ¹⁷.
Birth and developmental weight
1. Age and sex definition
  1. As a day-old notation, define birthdays as postnatal day 0 (PD 0). Define the sex of the infant by examination of external genitalia.
2. Identification of congenital malformations or diseases
  1. Examine the infant to identify any congenital malformations or diseases, paying particular attention to those that might cause feeding difficulties (e.g., cleft palate).
3. Body weight measurement
  1. Weigh the infant daily using a scale with 0.1 g increments to check their feeding volume. Prepare a clean plastic box or bowl lined with soft tissue paper to hold the infant and maintain its body temperature during weighing. Tare the prepared box or bowl on the scale, place the infant in the prepared container, and record the body weight. Weigh daily at approximately the same time to compare with the standard ¹⁵^,¹⁶.
4. Body weight gain graph
  1. Visualize a graph of body weight gain per day. The weight at birth and on the second day is expected to be more than 27 g and to then increase by approximately 1 g per day according to the colony records of neonatal infants' weight required for survival (Figure 2).
5. Assessment of milk intake volume
  1. Assess milk intake volume by weighing the infant both before and after feeding. However, be aware that separating the infant from the parent for weighing may itself cause stress and interfere with nurturing behavior. If normal breastfeeding and growth are expected, reduce weight measurements to once daily for the first week.
6. Crown, rump, and length measurement (CRL)
  1. Measure CRL by laying the infant flat in the prone position against a ruler and determining the length from the top of the head to the base of the tail (Supplemental Figure S1).
Breastfeeding behavior of the infant
1. Confirm that the infant is performing four behavioral patterns (Figure 1A).
  1. Determine whether the infant is clinging to the mother's body sufficiently.
  2. Observe whether the infant's head is bent forward to the mother's body by its own whole body muscle tension.
  3. Note whether the infant explores and reaches the mother's nipple by itself as a human sucking "routing" reflex with some parental help.
  4. Vocalizing a phee call¹¹^,¹² loudly when separated from its parents.
Mother's breastfeeding behavior and function
1. Confirm these behavior patterns and functions in the mother (Figure 1B).
  1. Confirm the mother's cooperative acceptance of the newborn for breastfeeding.
  2. Confirm that when the mother's breast becomes taut, the mother encourages the infant to suckle, and then the breast becomes less taut and the teat protrudes.
  3. Support the mother's breastmilk secretion by pressing the breast side with the fingers (Figure 3A). Check that the breast tension is not too hard and is without engorgement.
    NOTE: Wear soft and thick cowhide gloves to prevent the mother from biting and hold the mother using the nondominant hand.
  4. Observe the mother's expression and look for signs of pain as the cause of her refusal of the infant suckling.
Father's parenting behavior
1. Observe the father's parenting behavior. Observe whether the father is carrying the infant excessively and interfering with nursing. The father's assistance to carry the infants is usually limited.
Intervention targeting both the mother and infant to reestablish spontaneous breastfeeding
1. When an underweight infant ( less than 27 g ) is found, observe the family relationship and search for any abnormal parental infant-rearing behavior. Potential parental abnormal behaviors pose a high risk of harming the infant or interfering with feeding (abuse) or abandonment of feeding (neglect).
2. When the infant is too weak to explore or cling to the mother and initiate nursing by itself, separate it from the mother and give it a minimal amount of formula (e.g., 0.5 mL of Lebens Haihai, Wakodo at two-thirds concentration) by oral syringe, as needed based on body weight (Figure 1A,B).
3. As the first intervention step aimed at the mother, soften the hardened nipple area by pressing and massaging in three steps from the areola base toward the nipple between fingers to open the milk duct (Figure 3B). Exude milk slightly from the teat for the odor to encourage the infant to explore.
4. Next, hold the mother's body softly and lay the infant near the mother's breast to encourage it to search for the mother's nipple (Figure 1C). Guide the mother to raise her arms to improve nipple access for the infant. After the infant finds the nipple, continue the breast massage to assist with milk secretion. Confirm that the mother's breast is relieved of pressure, likely relieving the pain and the teat is protruding.
5. During the intervention, provide occasional handling and build rapport with the family.
6. Repeat this intervention one or more times per day until the mother voluntarily allows feeding and the infant learns to suck spontaneously. When the infant's feeding is inhibited by the father, remove the father from the family until the infant's development improves.

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Representative Results

Diagnosis of underweight and parental infant-rearing abnormality
A pair of five-year-old common marmosets (Callithrix jacchus) obtained from a colony at Saitama Medical University gave birth to their first set of offspring (twins) overnight in May 2019. This was a spontaneous vaginal birth. Only one of the offspring (a male) was found alive and embracing the mother's body. Another sibling was found dead, the birth weight (less than 25 g) and sex unclear, multiple hours after death. The presence or absence of milk ingestion behavior between the mother and offspring was unknown at the first perinatal check.

The infant was weighed daily at approximately the same time. The delivery day weight was 26 g, lower than the standard¹⁵^,¹⁶. The colony records of neonatal infants' weight for survival have a minimum weight of 27 g (Figure 2). The CRL was 9 cm. The father was frequently observed to be persistently licking the infant since day 1. Such paternal behavior has never been identified in our common marmoset colonies. By day 2, the infant lost weight (Figure 4, PD2(1), reaching the lowest weight 23 to 24 g recorded in our breeding history (the previous minimal record; 27 g), and did not appear to be initiating nursing. The infant did not appear to have the strength to initiate and maintain spontaneous suckling behavior.

Because of the condition of the infant, we searched for any evidence of abnormal parental rearing behavior in the recorded video. The father also showed strange behavior In addition to persistent licking, he appeared to be encouraging the infant to suckle his breast (see the accompanying video). The mother sometimes approached the father to touch the infant; however, the father appeared to brush the mother away, causing breastfeeding failure-milk duct closure and breast tautening followed by the mother's refusal to allow the infant to suckle because of pain. The mother's breast enlargement appeared painful and she seemed unwilling to be suckled, translating to "abandonment". This abnormal parental behavior was defined as "abuse" or "abandonment", behaviors that prevented the infant from feeding spontaneously. It was determined that intensive care was required.

Combination of formula and breast milk
Thus, the first feeding intervention (0.5 mL of formula by syringe) occurred at 10:30 h on postnatal day 2 (PD2) (Figure 4A). Fortunately, before further intervention, it was confirmed that the infant maintained both the routing reflex (one of the most important neural functions at this neonatal stage) and the ability to cry loudly, producing the typical "Phee call"¹¹^,¹²^,¹³. Two additional formula feedings were added at 12:30 h and 17:30 h during Day 2, resulting in a weight increase of 1 g to a body weight of 25 g.

Guided clinical care: voluntary participation in breastfeeding by mother and infant
On Day 2, breastfeeding intervention began. The mother was hand-held and her engorged breast was digitally massaged by the interventionist (Figure 4B). Next, the infant was placed on the mother's body and encouraged to spontaneously search for the nipple (Figure 4C). The mother maintained a tentative pose and showed limited resistance. The interventionist guided the mother to raise her arms to improve nipple access. During this process, the infant was confirmed to be feeding continuously. The mother showed some reluctance when the infant began suckling, likely due to the pain associated with breast engorgement. As nursing progressed, the breast seemed to soften, likely relieving the pain.

At 11:30 h on Day 3, the father was holding the infant again, impeding the infant's access to the mother for breastfeeding. At this time, the infant's weight had decreased to 23 g, requiring further intervention as follows. The father was separated from the family, and the infant was syringe-fed 0.8 mL of formula and encouraged to breastfeed. At 13:30 h and 16:30 h, a combination of 0.9 mL of formula and breastfeeding occurred. At 18:30 h, the infant weighed 25g and both mother and child seemed to be well accustomed to the breastfeeding support (Figure 4). Formula supplementation was discontinued at this point to avoid overfeeding. Body weight increased to 26.8 g on Day 4 and 28 g on Day 5. With repeated breast massage and encouragement of the infant's active exploration, the infant quickly learned to breastfeed and showed steady weight gain (Figure 4, postnatal day (PD) 12). In addition, the mother began to facilitate breastfeeding by actively raising her arms (Figure 4D).

Figure 1: Two diagnostic and intervention flowcharts on common marmoset infant-mother breastfeeding. (A) Infant; (B) mother. Please click here to view a larger version of this figure.

Figure 2: Weight comparison with the averages and standard errors of developmental increase and the minimal record of 27 g for survival in our colony. Dark gray dots and lines: Body weight averages and standard errors in 10 neonatal infants. Red line: This study case of maldevelopment in a neonatal infant. Please click here to view a larger version of this figure.

Figure 3: Mother's breast massage to support milk secretion by opening the milk duct and secreting milk. (A) Side pressure (blue arrow) for breast milk secretion. (B) Three steps of fingers' pinch from the base of areolas toward nipples to open the milk ducts.*Note that the hand approaching directions are different between A and B. Please click here to view a larger version of this figure.

Figure 4: Diagnosis of underweight, less than the minimal record for survival. The infant's weight records from postnatal day (PD) 2 (required intervention for survival) to 12 (the standard increase, approximately 1 g per day) indicate the developmental conditions before and after three types of interventions A, B, and C with the goal behavioral example D. (A) Formula supplementation by syringe. (B) Softening the breast and exuding milk from the teat. (C) Holding the mother and laying the infant to explore the nipple. (D) The mother's cooperative posture during breastfeeding with the infant. Please click here to view a larger version of this figure.

Supplemental Figure S1: Crown, rump, length measurement of the infant marmoset. Please click here to download this File.

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Discussion

Parental care of infants in diverse species requires mutual physiological and psychological considerations⁷^,⁹^,¹⁰^,¹²^,¹³^,¹⁴^,¹⁸^,¹⁹^,²⁰^,²¹^,²²^,²³^,²⁴. The condition of the inexperienced parents might simulate the condition of human parents with childcare in the modern environment of declining birth rates and nuclear families. Therefore, this protocol was aimed at a comparative primatological examination of the risks and intervention, although only one empirical example was presented. We clinically intervened to support the establishment of breastfeeding in first-time marmoset parents with a newborn that was not appropriately gaining weight. In this pair, the father's behavior toward the infant and mother likely prevented appropriate breastfeeding, leading to the infant's weight loss.

The intervention consisted of separating the father from the mother and infant, softening the mother's breast by massage, and encouraging the infant to explore the breast. When the infant reached the nipple and latched on, further massage activated feeding. Formula was syringe-fed to supplement nutrition, leading to weight gain. The series of interventions were repeated to encourage the infant to explore the breast, which eventually led to successful voluntary sucking and attachment between the mother and infant. The repeated intervention steps guided the gradual development of cooperation between the mother and infant in spontaneous feeding behavior. This success confirms the existence of a mechanism for social bond formation related to feeding and other nurturing behaviors as we predicted in our previous study using BOUQUET, an analytical method for detailed and comprehensive interspecies behavioral and physiological structure visualization¹⁴. In addition, this study suggests that spontaneous interaction between mother and infant may be important in the evaluation of breastfeeding disorders.

During formula feeding, the infant continued to vocalize with "phee" calls, loud, long calls that last several seconds²⁵. Our previous studies have quantitatively confirmed that the "phee" call becomes less frequent as marmosets progress from juvenile to young adult stages¹³. The "phee" call is a form of social communication exchanged between individuals separated by distance²⁶^,²⁷. It may also be used as a communication medium for neonates with their nonverbal caregivers. Since "phee" calls were not inhibited in this study, even when the infant was significantly underweight, they may be necessary for the success of the intervention. The presence and frequency of "phee" calls could perhaps be used as an indicator of improvement when implementing feeding interventions such as the human infant's cry¹³.

In this case, we could induce the marmoset mother and infant to learn appropriate feeding behaviors. In humans, inducing improvement in the psychological state of mothers who refuse to raise their children would be challenging because forcing mothers to interact with their offspring is not possible. Therefore, the most important finding from this case study is that the best approach to intervening in breastfeeding failure may be to support mother-infant attachment formation²²^,²³. In this process, the most important factor may be the newborn's spontaneous nipple exploration²⁹. An important step may also be the availability of sufficient nutrition (as provided here through formula supplementation) to support biological growth and completion of the neural circuitry related to the reward system allowing the infant to search for and reach the nipple on its own following visual and olfactory clues⁸^,²².

As a possible assumption, the infant itself might be abnormal and was not providing adequate cues that would elicit parental care. To improve early breastfeeding success and postnatal growth and development, if there are medical problems in the infant or mother, it is often necessary to separate the infant from the mother to allow appropriate nutritional management of the newborn. Following the stabilization of the newborn, mothers must be provided guidance and support to successfully establish breastfeeding. This common marmoset rare model around family social problems must contribute to reminding us of a certain human strategy in developmental psychiatry. While the number of abuse cases is increasing in Japan, the percentage of fathers encouraged to take parental leave and actively enjoy child rearing has been steadily increasing³⁰, and the Common Marmoset's parenting may come close as a model. A marmoset father holding an infant is not an abnormal behavior, although this case seemed so because the father kept licking the infant's face strongly and excessively. As another assumption, it might be possible that the mother was rejecting this infant and did not want to nurse it because of breast pain³¹. This protocol must suggest an example of intervention for such problems in humans. Because the claims in this paper are derived from the observations of only one case of a single-family unit, with a single infant in the multiparous species³² being different from humans, further studies are required to compare such results with observations in humans.

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Disclosures

The authors declare no conflicts of interest, financial or otherwise.

Acknowledgments

We thank all members of the experimental animal department of Saitama Medical University. We appreciate Yamaguchi University and Tohoku University for their research support. This study was supported by JSPS KAKENHI Grant Numbers JP 16K10106, 17K18648, and 19K08305.

Materials

Name	Company	Catalog Number	Comments
			Specification
Common Marmoset			Self Breeding
			Mother 5 year-old Number: 1
			Father 5 year-old Number: 1
			infant 0-13 day-old Number: 1
Formula Milk			Lebens Haihai, Wakodo Number: 1
			distilled water
Plastic glove			powder-free
Syringe			1 mL Number: 1
Video Cemera			Sony Handycam Number: 1
			iPhone camera Number: 1
Weight Scale			0.1 g increment Number: 1

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Behavior