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Journal of Perinatology (2009), 112 r 2009 Nature Publishing Group All rights reserved.

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Neonatal hypothermia in low resource settings: a review

V Kumar1,2, JC Shearer1, A Kumar2 and GL Darmstadt1
Department of International Health, International Center for Advancing Neonatal Health, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, USA and 2Clinical Epidemiology Unit, King Georges Medical University, Lucknow, Uttar Pradesh, India Introduction If a denition of life were required, it must be most clearly on that capacity, by which the animal preserves its proper heat under the various degrees of temperature of the medium in which it livesy a few degrees of increase or diminution of the heat of the system, produces disease and death said James Currie some two centuries ago, recognizing the central importance of temperature regulation in health.1 Although folklore associated with increased temperature or fever has been recorded throughout history across virtually every culture and civilization, a recognition of hypothermia and its clinical signicance, particularly for newborn health is a relatively recent advance.1,2 Moreover, progress toward thermal care of newborns in developed countries has far outstripped knowledge and practice in developing country settings, where 99% of global neonatal deaths occur.3,4 Hypothermia during the newborn period is widely regarded as a major contributory cause of signicant morbidity in developing countries and, at its extreme, mortality.5 High prevalence of hypothermia has been reported from countries with the highest burden of neonatal mortality, where hypothermia is increasingly gaining attention and signicance as a critical intervention for newborn survival. The World Health Organization (WHO) adopted thermal control among the essential components of newborn care.6 However, the context, paradigms and risk factors for thermal care within these low resource settings differ markedly from high-income countries, which has important implications for design and delivery of thermal care interventions. The objective of this review is to describe the epidemiology of neonatal hypothermia in low resource, high neonatal mortality settings, its pathophysiology, biological risk factors, risks associated with domiciliary care and thermometry. We also review strategies for prevention and management of hypothermia and discuss directions for future research.

Background: Hypothermia is increasingly recognized as a major cause of neonatal morbidity and mortality in resource poor settings. High prevalence of hypothermia has been reported widely from warmer high mortality regions of Africa and South Asia. The World Health Organization recognizes newborn thermal care as a critical and essential component of essential newborn care; however, hypothermia continues to remain under-documented, under-recognized and under-managed.

Objective: This review aims to provide a thorough patho-physioepidemiological discussion of neonatal hypothermia applied to local risk factors within the developing country context with particular emphasis on prevention, recognition and management. Method: All available published literature on neonatal hypothermia relevant to resource poor settings were reviewed. Studies from the developing country settings were primarily reviewed for epidemiology, domiciliary risk factors as well as potential interventions for thermal care. Result and Discussion: Functional integrity and efciency of biological systems is critically dependent on an optimal and very narrow range of core body temperature. Risk factors for neonatal hypothermia differ markedly within low resource settings. A combination of physiological, behavioral and environmental factors universally put all newborns, irrespective of birth weight, at risk of hypothermia. The knowledge decit along the continuum from health providers to primary care givers has sustained the silent epidemic of hypothermia. The challenges of recognition, understanding of local risk factors and communication have meant a lack of informed thermal care for newborns. Simple, feasible interventions exist, but need to be applied, based on local risk factors that disrupt the warm chain. Further research is needed to document local risk factors, develop better techniques for recognition, evaluation of thermal care within essential newborn care and communication strategies for program effectiveness. Journal of Perinatology advance online publication, 22 January 2009; doi:10.1038/jp.2008.233 Keywords: hypothermia; skin-to-skin care; warm chain; community; newborn; neonatal health
Correspondence: Dr GL Darmstadt, Integrated Health Solutions Development, Global Health Program, Bill and Melinda Gates Foundation, PO Box 23350, Seattle, WA 98102, USA. E-mail: gdarmsta@jhsph.edu Received 27 July 2007; revised 18 December 2008; accepted 19 December 2008

Methods This review aimed to consider all available published literature on neonatal hypothermia relevant to low resource settings. The studies

Neonatal hypothermia V Kumar et al

included in the review consisted of studies from developed country settings, particularly those that were pertinent to the discussion of the pathophysiology of neonatal hypothermia and potential implications for developing countries. Studies from developing country settings were primarily reviewed for epidemiology, domiciliary risk factors as well as potential interventions for thermal care. The principal electronic reference libraries searched were PubMed, Embase, Popline, Cochrane Reference Libraries and Google Scholar. The search strategies included keywords, combinations, MeSH and snowball searching for related articles. The search terms used included neonatal hypothermia, developing country, interventions, community among others. Pertinent books, monographs and reports were accessed.

Fetal thermoregulation and transition in newborns To appreciate the thermoregulatory challenge that newborns face immediately after birth, it is important to understand the transition in thermoregulation from fetus to newborn. The fetus is a metabolically active organism whose temperature closely follows maternal temperature, forming a heat clamp, and remains 0.5 1C higher.2729 This heat clamp creates a steady state and provides the fetus with a thermostable environment.30 Although the fetus develops in a warm and thermostable environment, its basal heat production (kcal kg1) is about twice that of adult levels.30 After birth, thermal exchange with the environment occurs along a temperature gradient from the interior of the body to the body surface to the surrounding air. When the rate of heat loss exceeds the rate of heat production, body temperature falls.31 Heat loss in newborns Body heat is exchanged (loss and gain) with the environment through conduction, convection, radiation and evaporation (Table 1). The exchange is modulated by ambient temperature, humidity, wind, solar exposure, sky and ground radiation, posture, clothing and so on. The limitations of thermoregulatory control are due to inherent capacity to generate heat and to environmental factors limiting heat transfer and heat exchange.1 Heat loss from the newborn is mainly due to evaporation of amniotic uid from the babys body. However, loss of body heat also occurs by conduction if the baby is placed naked on a cold surface (for example, a table, weighing scale or cold mattress); by convection if the naked newborn is exposed to cooler surrounding air; and by radiation from the baby to cooler objects in the vicinity (for example, a cold wall or a window), even if the baby is not actually touching them. Heat loss increases with air movement, and a baby risks getting cold even at a room temperature of 30 1C (86 1F) if there is a draft.32 At birth, the newly born infant is suddenly exposed to a wet and cold environment and responds by increasing heat production and attempts to conserve heat by cutaneous vasoconstriction. These responses begin within a matter of minutes and can persist for many hours.33 In the absence of thermal protection, the newborn may lose considerable heat, resulting in a drop of the infants body temperature at a rate of 0.2 to 1.0 1C min1. Within the rst minutes following birth, skin temperature of the baby typically falls by 3 to 4 1C.26,34 In fact, a naked baby exposed to an environmental temperature of 23 1C (73.4 1F) at birth suffers the same rate of heat loss as does a naked adult at 0 1C (32 1F).32 Practices such as leaving the baby unattended, delayed drying and wrapping, and bathing immediately after birth, subject the baby to additional risk of hypothermia. Newborns in general and preterm infants in particular are prone to excessive heat loss because they have a relatively large surface area in relation to body mass; the surface-to-mass ratio is

Denition Neonatal hypothermia is dened as an abnormal thermal state in which the newborns body temperature drops below 36.5 1C (97.7 1F). Progressive reduction in body temperature leads to adverse clinical effects ranging from mild metabolic stress to death. In 1997, WHO categorized hypothermia into three stages based on core temperature, prognoses and action required:7  Cold stress: 36.0 to 36.4 1C (96.8 to 97.5 1F); cause for concernFwarm the baby and seek to identify cause(s).  Moderate hypothermia: 32.0 to 35.9 1C (89.6 to 96.6 1F); dangerFimmediate warming of the baby is needed.  Severe hypothermia: <32.0 1C (<89.6 1F); outlook is graveFskilled care is urgently needed. Of the 20 studies reviewed for denition of hypothermia, only 7 applied the WHO criteria, 9 used <36.0 1C, 2 used <35.5 1C and 3 used <35.0 1C as cutoffs for hypothermia.3,825 Uniform adoption and application of the standard WHO denition is fundamental to coordinated advancements in detection and management, but hypothermia continues to be variably dened, leading to under-recognition and under-reporting, and inadvertent denial of care to those who are misclassied but in need of care.

Pathophysiology of neonatal hypothermia Functional integrity and efciency of biological systems is critically dependent on an optimal range of core body temperature. With a variance of <0.3%, body temperature is one of the least variable and most vital factor of the internal environment of homeotherms, including humans.26 As noted by Currie, homeotherms must orchestrate a ne balance between heat production and heat dissipation such that heat loss or gain from the environment is precisely regulated and body temperature is maintained within the optimal range for efcient metabolism, growth and survival.1,26
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3 Table 1 Sources of heat loss and methods of prevention

Source of heat loss Evaporation: the change in state from liquid to gas, using energy from Evaporation of amniotic uid from the newborn skin Evaporation of amniotic uids while the newborn is being resuscitated Evaporation of water after a bath Evaporation of water from the skin, after diffusing through the epidermis (transepidermal water loss) Method of prevention heat Wipe and dry the newborn immediately after delivery Perform resuscitation under a radiant warmer, or on a heated water-lled mattress Delay bathing; dry and wrap immediately after bathing Apply plastic wraps or bags, apply topical agents (that is, sunower oil, aquaphor)

Conduction: the transfer of heat between two objects in contact, from the warmer to the cooler object Infant is placed on a cold surface (that is, weighing scale, Keep the infant wrapped when not in skin-to-skin position; place a warmed blanket between exam table) the baby and cold surface; delay weighing and other non-essential examinations Newborn is placed on the oor or other surface beside the Teach families and traditional birth attendants that the newborn should be placed mother until the placenta is delivered skin-to-skin with the mother after delivery (following immediate drying) Convection: the transfer of heat by air currents that move across the exposed skin of the newborn Newborn is exposed to air current from a draft, fan and so on Limit fans in delivery and nursery rooms; encourage home births to occur in rooms that are free of drafts; keep the newborn in skin-to-skin position Radiation: the transfer of heat from the newborn to another colder object, even if there is no contact between the two Cold objects in the room transfer heat away from the infant Repair drafty windows and walls in the home or hospital; in the home, heat the delivery room with a re

particularly high in low birth weight (LBW) infants compared with normal birth weight newborns. Premature infants fare worse because of truncated substrate deposition in the last trimester of pregnancy, thus limiting the insulation provided by subcutaneous fat. Preterm babies have consistently higher insensible heat losses35,36 compared with term babies as a result of high water loss from the skin.37,38 These losses are particularly high in babies <33 weeks gestational age during the rst few days of life due to their thin, poorly keratinized stratum corneum, which offers low resistance to the diffusion of water.39 Asphyxiated babies are also at increased risk of profound drop in body temperature immediately after birth.31 Metabolism and heat production in newborns Metabolic processes, including non-shivering thermogenesis, serve as the principal source of body heat in newborns. The resting metabolic rate of the newborn baby increases from a typical range of 35 to 40 kcal kg1 day1 on day 1 to values of 40 to 60 kcal kg1 day1 during the later neonatal period, reaching adult values by about 6 months of age.31 Heat production per unit body surface area is lower in preterm infants, particularly below 28 weeks of gestation. Metabolic rates depend not only on postnatal and gestational age, but also on birth weight and size for gestation.4042 Babies who are small for gestational age tend to have higher thermogenesis than gestationally immature babies of similar birth weight.43 Other factors increase metabolic rate in newborns, including ingestion of food, particularly colostrum, increased activity, cold

exposure and being awake.32,44 Infection can increase the risk of hypothermia by increasing the catabolic state and disturbing normal temperature control.45 Factors that reduce metabolic rate are illness, particularly with hypoxia or asphyxia, starvation and deep sleep.46 Applying these principles to the developing country context, LBW babies (15.5% of all newborns worldwide and 30% in South Asia) are at increased risk of hypothermia, and in combination with the practice of discarding colostrum and delayed breastfeeding,47 the magnitude of risk expands to become almost universal.47,48 Thermal regulation and ambient conditions The newborn baby has immature thermoregulatory controls during the early neonatal period, which resemble a poikilotherm or at best a partial homeotherm.26 Thus, control of body temperature can be achieved only over a narrow range of ambient conditions without external inputs of heat or aids to heat preservation. In the unclothed resting adult, the lower limit of the thermoneutral zone is 26 to 28 1C at 50% relative humidity; however, in the naked full-term newborn infant, it is much higher at 32 to 35 1C. In small, premature infants (for example, 1 kg), the lower limit of the thermoneutral zone may be as high as 35 1C.49 This difference assumes signicance, because it shows that environmental temperature conditions that do not require any thermoregulatory effort in the adult may seriously overtax the metabolic thermoregulatory system of the newborn. The average ambient temperature within regions with the highest rates of neonatal mortality in South Asia and sub-Saharan Africa is 20 to 30 1C with
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wide seasonal and diurnal variation. This has implications for the majority of deliveries within developing countries that take place at home or in facilities with inadequate heating capacities, where low ambient temperatures rapidly overwhelm the newborn. On the other hand, practices such as immediate drying, wiping, swaddling, wrapping with warm blankets and skin-to-skin contact (STSC) reduce heat loss (and in the case of STSC, provide conductive heat gain) during the critical rst few hours.31 Pathophysiological effects Thermoregulation is multisystem, multiorgan dependent, and hypothermia impacts them all with pathophysiological manifestations proportionate to the degree of hypothermia.1,32 As a rst line of defense, heat loss is minimized by peripheral vasoconstriction, an effect which is most pronounced in the extremities. Peripheral vasoconstriction leads to acrocyanosis, cool extremities and decreased peripheral perfusion.32 The skin of hypothermic newborns is often cold to the touch, and will feel strikingly cold in severe cases (<28 1C). Facial erythema or redness may give the false impression of vitality. The second line of defense in newborns is non-shivering thermogenesis associated with metabolism of brown adipose tissue. Lack of shivering contributes to lack of recognition of newborn hypothermia by minimally trained health workers and families. Further, even nonshivering thermogenesis is impaired in the newborn for the rst 12 h of life and in infants who are ill, hypoxic or experienced asphyxia at birth.32 Signs of hypothermia are listed in Panel 1, and overlap signicantly with those of septicemia.32 Hypothermia beyond the rst day of life often indicates infection, particularly septicemia,32,50,51 and the WHO recommends that all hypothermic infants be assessed for infection.8 Conversely, hypothermia has been posited to predispose infants to infection due to lethargy, leading to aspiration pneumonia.50,51 Central nervous system depression also results in bradycardia, apnea and poor feeding.1,32 The consequences of increased metabolism during hypothermia include hypoglycemia, hypoxia and metabolic acidosis.1,31 Behaviorally, cold infants will initially become more agitated, sleep less and lie in a exed posture to reduce skin exposure to the air.7,31 These infants may appear dead, and anecdotal reports from the developing world state that severely hypothermic infants have been left for dead, to later recover.7 Although all of these symptoms may not be present during cold stress or mild hypothermia, they will become apparent as the severity of the condition increases.1 In severe cases, associated ndings and sequelae include cold panniculitis, sclerema neonatorum and subcutaneous fat necrosis.52 Cold panniculitis presents with circumscribed red lesions on the skin of infants and children who have been exposed to cold. These lesions disappear on their own after a period of weeks or months.53 Sclerema neonatorum, a generalized waxy hardening of the skin, has been
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associated with hypothermia, and is considered a sign of severe underlying morbidity, including sepsis, cardiopulmonary disease, diarrhea or dehydration.52,53 A report from China documented an incidence of sclerema of 6.7% among all infants born in the cold season in six middle-income rural and urban counties.54 The case fatality rate reported for sclerema neonatorum is >50%.53 Subcutaneous fat necrosis is associated with cold stress, although its exact etiology is unclear.53,55 A benign disease with an excellent prognosis consists of localized indurations of fat necrosis distributed most commonly on the cheeks, back, buttocks, arms and/or thighs.53 Incidence The incidence of hypothermia has been estimated both among hospital and home-born newborns in low resource settings (Table 2) in South Asia, including Bangladesh, India, Pakistan, Bhutan and Nepal, as well as in other tropical climates in developing countries. For example, in Nepal, 85% of newborns in a maternity hospital had a temperature <36 1C within 2 h of birth.16 In Ethiopia,56 Zambia57 and Zimbabwe,17 one-half to two-thirds of newborns evaluated were hypothermic. The incidence of primary hypothermiaFan independent morbidity that presents as a result of cold stressFis high immediately following birth in hospital settings.1114,16,20,5860 Few studies have addressed aspects surrounding the birth and postpartum care that can put the newborn at risk for hypothermia.9,16,57,61 In one village-based study in India, 11% of 189 neonates were found to be hypothermic (<35.6 1C) based on a single temperature reading taken within the rst 24 h after birth. Only 58% of newborns were wiped soon after delivery, the head was covered in 59% in winter and 11% in summer, no baby was kept skin-to-skin, and the room temperature was <24 1C in 41% of households.9 If the WHO denition of hypothermia was applied (that is, <36.5 1C), the incidence of hypothermia in the study conducted by Kumar and Aggarwal9 could well go up to 38% in home-delivered babies. This is corroborated by a more recent community-based study in Shivgarh, rural India, where the prevalence of hypothermia (<36.5 1C) was high in both LBW (49%) and normal birth weight (43%) infants. In the rst data of its kind, the study also found that among hypothermic newborns, 42% of their mothers had a lower temperature, emphasizing the overwhelming nature of the cold ambient temperature and lack of resources available to combat the cold.3 In Gadchiroli, India, body temperatures were recorded in the home throughout the neonatal period, and 80% of hypothermia cases (axillary temperature <35 1C) occurred on the rst day.8 Among infants who are diagnosed with hypothermia in the days or weeks following birth, their hypothermia is often secondary, that is, a symptom of sepsis or other infection.8,17 19

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5 Table 2 Incidence of hypothermia in developing country settings

Population Type of data Home Location Sample size 763 Denition Measurements (time and frequency) Temperature measured on days 1, 2, 3, 5, 7, 15, 21, 28 Prevalence/ incidence 17% Comments Reference

All newborns

Central India

Skin temperature <35 1C Axillary <36.5 1C Axillary <36.5 1C Axillary <35 1C Rectal <36.5 1C Rectal <36.5 1C Rectal <35.5 1C Axillary <36 1C Rectal <36 1C Axillary <36 1C Rectal <36 1C

Independent morbidity 13.9%; as part of sepsis, incidence 3.1%

Bang et al.8

All newborns All newborns All newborns

Home Home Hospital

Haryana, India North India Shimla, North India Uganda

189 1732 2063

Within 24 h after birth One measurement (mean 17.1 h after birth) Measurement within 24 h of birth and each day following until discharge 10, 30, 60, 90 min postpartum

11.1% 45% 2.9% Cutoff is low

Kumar and Aggarwal9 Darmstadt et al.3 Kaushik et al.10

All newborns



All newborns Uncomplicated newborns Uncomplicated newborns Uncomplicated newborns Sick newborns

Hospital Hospital (nursery) Hospital Hospital Hospital (Neonatal unit) Hospital (Neonatal Intensive Care Unit, NICU) Hospital (NICU) Hospital (neonatal care unit)

Iran Nepal

940 31

After birth (mean 20 min) Longitudinal measurements (mean of 5.6 measurements per infant) On rst day of life (mean 7 h) At 2 h after birth Measured on admission to neonatal unit and every 4 h following On admission

29, 82, 83 and 79 % at each time point 53.3% 81%

All consecutive deliveries

Byaruhanga et al.


Nayeri and Nili12 Anderson et al.13

Nepal Nepal Harare, Zimbabwe Zambia

76 500 313

63% 85% 51.4%

Winter; healthy, term newborns only Winter; nursery

Bolam et al.14 Johanson et al.16 Kambarami et al.17

Sick newborns



Warm season; all infants were born outside the hospital

Christensson et al.18

Sick newborns Sick newborns

Brazil Turkey

320 60

Axillary <36.5 1C Rectal <36 1C

On admission to NICU On admission to neonatal care unit

31.6% 88%

Warm season; referral hospital LBW; transport was implicated in rate

da Mota Silveira et al.19 Sarman et al.20

Seasonality Seasonal variation in ambient temperature leads to variation in the incidence of hypothermia. A study in northern India reported a 70% incidence of hypothermia among newborns during January to March, 20% during April to June, 32% in July to September and 55% in October to December. Seasonal hypothermia rates were not signicantly different for LBW compared with normal weight infants in warmer months, but signicant differences were found during the colder months.3 Bang et al.8 reported similar variations from central India (21.5% incidence in the winter versus 13.8% in summer using a denition of hypothermia as <35 1C). In the

northern Indian state of Haryana, newborns born at home had an incidence of hypothermia of 19.1% in the winter months, but only 3.1% in the summer. However, in the summer, 36.8% of newborns were hyperthermic.9 Risk factors for hypothermia in resource-poor settings There are several socioeconomic, cultural and systemic factors that characterize newborn care in resource-poor settings that potentially expose newborns to a higher risk of hypothermia, even in warm climates (Table 3).
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6 Table 3 Risk factors for hypothermia

Risk Description

Physiological risks Low birth weight (LBW) Association between rectal temperature and birth weight was recorded among newborns in West Africa (r 0.48, P<0.01).62 and preterm Christensson et al.18 reported a statistically signicant association between admission weight and rectal temperature of newborns. In Tanzania, the odds ratio of hypothermia among LBW newborns was 11.0, compared with normal weight newborns.63 Environmental and behavioral risks Delivery room is Among home deliveries in Nepal, only 16% of households reported heating the place of delivery throughout the labor and delivery process.64 not warmed Delivery room is cooled In Haryana, India, fans were used to cool delivery space used for summer home births in 49.5% of 189 births.9 Newborns born into an air-conditioned delivery room in Malaysia had a mean body temperature of 36.5 1C at birth, versus 37.7 1C for newborns born into a non-air-conditioned room.65 Newborn is not dried or In Himachal Pradesh, India, 28.7% of babies were wiped at birth.61 wrapped immediately In Zambia, the practice reported by women and midwives was to care for the baby only after the placenta was delivered.66 In a study of 5411 home births in Nepal, 4% were wrapped within 5 min of birth.64 Newborn is bathed soon In Uganda, bathing is perceived locally to clean the newborn of dirty skin, and more recently to protect against the vertical after birth transmission of HIV.11 In a randomized controlled trial of early bathing in Uganda, those newborns who were bathed 1 h after birth had an odds ratio of 3.88 (95% condence interval: 2.186.91) of being hypothermic 30 min after bathing.58 In Bangladesh, the newborn is bathed daily, and exposed to the outside air before bathing.67 In an India study, newborns were bathed as often as three times per day.61 In Zambia, mother and newborn are bathed together soon after birth.66 In Nepal, where bathing is nearly universal, a study of 5411 newborns documented that 92% were bathed within an hour of birth.64 Oil massage Oil massage of the newborn is common throughout South Asian and Middle Eastern countries, and mustard oil is used most commonly.68 Newborns are unwrapped to facilitate the oil application.61,67,68 Mustard oil, when applied to a mouse model, was a statistically signicant contributor to transepidermal water loss, causing deterioration of skin barrier function.69 Postpartum connement As observed in Bangladesh, mothers and their newborn sleep for several days (for example, 79 days in Bangladesh) in the place of birth as opposed to the bedroom or family bed, potentially exposing the newborn to cold.9 Transport Travel between the delivery and newborn ward resulted in a 5 1C core-skin temperature gap in newborns in Nepal.14 The risk of death among hypothermic newborns in an urban Indian hospital was highly correlated with the length of time it took to transfer and admit the newborn from the delivery ward to the neonatal intensive care unit.70 Silveira et al.71 recommend in utero transport whenever possible, encouraging women to deliver in a hospital to reduce the possibility of a post-labor transport if the baby requires extra care after birth. When hospital fees were introduced into Nigeria in the early 1980s, an increased rate of home deliveries among women who could no longer afford hospital care in one region caused a signicant increase in hypothermia among infants who required post-delivery transport to the hospital.72

Incidence of LBW More than 20 million infants worldwide, representing 16% of all liveborn infants, are born with LBW, 96% of them in developing countries.48 These rates are likely to underestimate the true magnitude of the problem, as more than half of infants in the developing world are not weighed. The incidence of LBW in many developing countries is as high as 30% or more.48,73 Additionally, in these settings, birth weight is not perceived to be an important determinant of newborn health, therefore LBW babies may not receive appropriate care, thus aggravating the risk.74
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Risk factors related to domiciliary care Approximately half of women in low- and middle-income countries deliver at home, with most deliveries conducted by traditional birth attendants and relatives.75 Lack of awareness regarding hypothermia is conspicuous from the absence of vernacular equivalents for the term.3,76 Caregivers have limited understanding of the special thermal care needs of the newborn, and often perceive newborn thermal care requirements as similar to those of adults. Many practices adopted during delivery and the early neonatal period inadvertently expose the newborn to higher risk of

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hypothermia, thus compounding the baseline risk already present due to inherent physiological susceptibility during this period. Delivery and immediate newborn care. The delivery room, which later serves as the postnatal connement room,67 is usually an unused and secluded portion of the home with inadequate arrangements to ensure warmth and prevent drafts of air. In South Asia, the room is often plastered with fresh cow dung or clay, which cools it further. As the risk to the mothers life is perceived to be higher, it is a common practice to focus attention primarily on the mother until the delivery of the placenta, while the newborn is left unattended, sometimes on the ground, leading to prolonged exposure.67,77 Immediate drying and wrapping of the baby is not a common practice,67,66,77 and leads to further heat loss. Early bathing is common, sometimes with vigorous scrubbing of the skin to remove the vernix, especially when local knowledge dictates that the vernix is a dirty or polluting substance.47,78 Early bathing can increase the risk of hypothermia, despite the use of warm water and STSC.58 Forceful removal of vernix disrupts the skin barrier, and leads to skin cooling due to increased transepidermal water loss through the compromised skin barrier.79 Postnatal connement. Postnatal connement is a common practice in most parts of South Asia and sub-Saharan Africa to seclude the mother from the newborn during the period of ritual pollution, to promote bonding between the mother and baby, and to protect the newborn against malec inuences such as the evil eye and evil spirits.67 Connement is observed for varying lengths of time across different cultures, often for the rst 40 days and is most stringent during the early neonatal period.67 It takes the following forms: (1) minimizing movement outside the home and contact with male members of the household; and (2) sleeping where birth took place on a temporary bed on the oor, rather than in the mothers bedroom. Temporary arrangements for sleeping with limited insulation pose an additional risk for hypothermia. The room is often inadequately lit, which makes it difcult to spot danger signs. Moreover, the practice of connement is a signicant barrier to access to health care. Massage. Oil massage is a routine newborn care practice in much of South Asia and sub-Saharan Africa as a local strategy for maintaining health,68 including thermal protection. However, newborns are unwrapped and exposed to the environment during massage. Mustard oil, which is the most commonly used oil in South Asia, has been shown to damage skin barrier function, leading to increased transepidermal loss of water and heat.68,69,80 Although massage with certain emollients may be benecial,5,81,82 frequent and prolonged environmental exposure during massage could result in cold stress. Thus, care needs to be taken to limit exposure during the massage process.

Breastfeeding. Delaying initiation of breastfeeding for 2 to 3 days and discarding of the colostrum is common practice in many communities in low resource settings.47,83 In addition to sacricing the stimulation to metabolism that comes from breastfeeding, delayed breastfeeding signicantly reduces skin contact with the mother and further increases the risk of hypothermia. Risk during transport Transport of the newborn is a signicant source of cold exposure. Evidence from studies on neonatal transport between wards within hospitals suggests that even in such controlled settings, risk of hypothermia during transport is high.14,70 It is a common observation in developing countries that preterm and high-risk infants are referred soon after birth, rather than in utero.73 This practice further aggravates the risk of cold exposure among rural populations who live far from health centers and have limited access to modern transportation. Care in health facilities Studies on the knowledge and practices of health professionals in low resource settings regarding thermal control of newborns revealed widespread prevalence of several high-risk practices in health facilities: inadequate warmth in delivery rooms, improper or delayed drying and wrapping of the newborn, bathing immediately after birth, reduced and delayed contact with the mother and delayed initiation of breastfeeding.57,84,85 Health providers had insufcient knowledge regarding the physiology of thermoregulation in newborns, methods of correct measurement of temperature, denition of neonatal hypothermia, prevention and management of hypothermia and its associated risks.84,85 Moreover, correct knowledge did not always translate into practice or institutional policies.85 Arrangements for management of hypothermic and LBW babies were either absent or inadequate.73 Electricity supply problems were common, and incubators, even if present, were dysfunctional.16

Recognition of hypothermia Measurement and detection The folklore of fever transcends across civilizations and cultures, and has been well documented throughout history with its etymological roots in the ancient language of Latin.1 Such recognition seems to have eluded hypothermia and still continues to do so. A possible explanation could lie in the superior ability of human touch to detect fever compared with hypothermia.86 Until the development of the clinical thermometer, human touch remained the only mode of thermometry and still continues to play an important role in temperature detection throughout the world. Palpation. The WHO suggests using a combination of two-site palpation (foot and abdomen) to detect cold stress and hypothermia. However, this was not found to be reliable by studies
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8 Table 4 Hypothermia detection: touch and liquid crystal thermometry

Technique Location Sample size Denition of hypothermia Axillary <36 1C Skin <36.5 1C Axillary <36.5 1C Axillary <36.5 1C Rectal <35.5 1C Axillary <36 1C Axillary <35 1C Results Reference

Foot palpation by hospital health workers Palpation of forehead, abdomen and foot by pediatricians Touch of abdomen by mothers and community health workers (CHWs) Touch of abdomen and soles of feet by a eld supervisor ThermoSpot on axilla ThermoSpot on axilla and abdomen ThermoSpot on abdomen

Nepalese hospital Indian hospital Rural India Rural India Malawian hospital Zimbabwean hospital Indian urban slum

250 50 189 500 10 (100 paired measurements) 313 (2787 paired measurements) 32 (180 paired measurements)

Sensitivity 1142%; Specicity 93100% Sensitivity 96% (forehead), 83% (abdomen), 98% (foot); specicity not reported Sensitivity 25% (mothers) and 34% (CHWs); specicity 97% (mothers) and 96% (CHWs) Sensitivity 74% Specicity 96.7% Sensitivity 100%; specicity 99% Sensitivity 19%; specicity 100% Sensitivity 88%; specicity 97%

Bolam et al.14 Singh et al.21 Kumar et al.22 Agarwal et al.25 Kennedy et al.23 Kambarami et al.17 Green et al.24

conducted by Ellis and co-workers14 and others who found that the use of touch led to underestimation of neonatal hypothermia (Table 4).22,25 WHO recommends the use of a low-reading mercury-in-glass thermometer, but it is fragile and difcult to obtain in many parts of the world. In settings where thermometers are not readily available, further studies are needed to explore reliable approaches for detection through palpation as well as application of modern technology such as the ThermoSpot device (TALC, St Albans, Hertfordshire, UK). Liquid crystal thermometryFThermoSpot. Use of the simple and feasible ThermoSpot device has been successfully tested in hospital and community settings (Table 4). This device, about the size of a small coin, is a one-use, adhesive, 12-mm liquid crystal temperature dot that is placed on the newborns skin, typically just medial to and above the axilla. It turns green if the newborn is normothermic, but shows black if the infant is hypothermic.25 As seen in Table 4, compared with the gold-standard test, the most accurate results with use of this device were obtained when the case denition of hypothermia was lowered (in one case to <35 1C), thus increasing specicity. Nonetheless, this technology has potentially important application for community and home births. It is simple, safe, provides continuous temperature monitoring and can be used even by unlettered caregivers. Data on impact of the device on care practices in rural India is forthcoming.87 Another variant of liquid crystal thermometry is in the form of a calibrated reusable strip that allows visual recognition of temperature in 1 1C gradations between 30 and 41 1C.73 Prevention and management of hypothermia Many of the warming technologies that are routinely used in highresource settings, including incubators, cannot be feasibly adapted
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to settings that are without reliable infrastructure or power sources. Prevention and management of hypothermia in low resource settings must focus on simple and effective interventions combined with behavior change and training. Practical guides, including Save the Childrens Care of the Newborn,88 the WHO MotherBaby Package6 and the WHO Thermal Protection of the Newborn32 provide recommendations to all levels of the health system and its providers. Various interventions for prevention and management of hypothermia have been tested in community as well as hospital settings, and have added to the existing evidence base.3,5,8,8994 Warm chain The warm chain32 is a set of 10 interlinked procedures to be taken at birth and during the following few hours and days to prevent hypothermia by minimizing heat loss in all newborns. Failure to implement any one of these procedures will break the chain and put the newborn baby at risk of hypothermia. The 10 steps of the warm chain are as follows: (1) warm delivery room, (2) immediate drying, (3) skin-to-skin contact, (4) breastfeeding, (5) bathing and weighing postponed, (6) appropriate clothing/ bedding, (7) mother and baby together, (8) warm transportation, (9) warm resuscitation and (10) training and awareness raising. Some of these and other evidence-based practices for prevention and management of hypothermia are described below.

Proper wiping and wrapping. Immediately following birth, newborns must be carefully wiped, dried and covered to prevent heat loss through evaporation of the amniotic uid.6,18 Proper wiping and drying was found to prevent signicant drops in temperature in the rst 2 h after birth.57 Head caps, especially woolen ones, are recommended for all babies, and the infant should be dressed and wrapped warmly when not in the

Neonatal hypothermia V Kumar et al

skin-to-skin position.95 The newborn should be properly wrapped,88 and tight swaddling is not recommended due to possible adverse effects.96 Skin-to-skin care. Skin-to-skin care has shown promising results for prevention and management of hypothermia for both low and normal birth weight babies in hospital as well as community settings. Kangaroo Mother Care refers to the technique of prolonged, continuous STSC between mothers and their LBW infants in the hospital and after discharge.97 The practice of Kangaroo Mother Care in hospitalized LBW infants has been associated with a number of benets, and is now considered to be at least as good as standard care with incubators.89,91 Besides improved thermoregulation of the newborn, other potential benets include improved maternalinfant bonding, more rapid transition to physiological stability following birth, reduced crying and longer periods of alertness, improved breastfeeding and growth, reduced incidence of serious bacterial infections and earlier discharge from hospital.5 STSC was shown to be at least as effective as incubator care for the management of hypothermia in normal birth weight neonates in hospital settings.90 Encouraging results from hospitalbased studies have led to the introduction of variants of Kangaroo Mother Care in community settings with widespread acceptance.3,94 In a community-based study of STSC in rural India, the practice was introduced as a universal strategy for all newborns regardless of birth weight, with multiple benets and no reported adverse effects.3 STSC is also recommended during postnatal transport.93 Breastfeeding. In addition to the heat exchange between newborn and mother, and provision of calories from fat,98 the process of suckling, which occurs with greater frequency in breastfed as compared with bottle-fed newborns, increases energy expenditure, stimulating basal metabolic activity and thus aiding thermoregulation.98,99 Breastfeeding also prevents bacterial infection,98 thereby preventing a common cause of secondary hypothermia. Synthetic external insulation Various synthetic wraps, bags, boxes and covers have been found to prevent heat loss in the newborn, and are particularly effective when used immediately after delivery. A Cochrane review of polyethylene and polyurethane bags and wraps showed that they resulted in signicantly lower rates of hypothermia among infants <32 weeks gestation.79,100 Many of these bags and plastic sheets are locally available at low cost in low resource settings. Topical agents and oil massage The application of topical agents, including parafn39,69 petrolatum, mineral oil and lanolin,69 or corn,77 sunower, sesame or safower oil,69,79,80,101 have been shown to reduce transepidermal water loss and as well as loss of heat. This is especially relevant for preterm newborns with an immature skin

barrier. Vegetable oils can potentially augment nutrition and possibly aid in skin barrier development by the transcutaneous uptake of lipids.69,79,80,101 Randomized trials among neonates are few, but Fernandez et al.101 in India showed that corn oil improved thermoregulation of infants. Although hypothermia was not a primary outcome in a study of sunower seed oil massage in Egypt, the application improved skin condition among preterm infants.81 In mouse models, sunower seed oil and Aquaphor accelerated barrier recovery and prevented transepidermal water loss as compared with controls.69 In the same study, mustard, soybean and olive oils delayed barrier recovery, and mustard oil was shown to damage epidermal cellular structure and barrier function. Mustard oil, which is widely used in South Asia for newborn and infant massage, is also easily adulterated to include toxic compounds.69 In randomized, controlled trials in hospitals in Egypt and Bangladesh, sunower seed oil applications reduced the incidence of neonatal sepsis by about 40 to 50%,5,81 and in Bangladesh they reduced the risk of mortality by 26%.82 Thus, evidence exists to promote the use of this highly cost effective intervention102 in hospitalized, preterm infants <33 weeks gestational age in low resource settings. However, further research is needed on the impact of this intervention in all newborns (that is, both term and preterm infants) in the hospital, and no data exist on the impact of this intervention in community settings. Promotion of this intervention should include education for the community and health providers on maintenance of the warm chain and preservation of vernix during massage.

Conclusion and further research Neonatal hypothermia has been documented (Panel 1) throughout the developing world, and is an important source of neonatal

Panel 1 Summary points

Denition: Neonatal hypothermia is dened as axillary temperature <36.5 1C.7 Risk factors Physiological: Preterm; low birthweight; septicemia.7,45,51 Environmental: Ambient temperature <32 1C (or 2528 1C if the newborn will be immediately dried and placed skin-to-skin)7; Drafty environment, including the use of fans or open windows in the delivery room.65 Behavioral: Absence of immediate drying and wrapping;20,85 bathing soon after birth;9,61,64,66,68 mustard oil massage;68,80 delayed or prolonged transport of the newborn.70 72 Signs/Symptoms: Lethargy, poor feeding, weak cry, reduced movements, peripheral edema and swelling of limb tissues, skin cold to touch.7 Prevention and Management: Behaviors and appropriate technology that maintain the appropriate thermal environment and prevent heat loss, including STSC and breastfeeding,60,90,99 radiant warmers and incubators (in areas of consistent electricity),20 heated water-lled mattresses,20 plastic wraps and bags,79,100 and topical agents (including oil massage).39,69,79,80,101

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morbidity; the contribution of hypothermia to neonatal mortality is poorly understood. For most newborns, hypothermia can be easily and affordably prevented. Increased knowledge among hospital and community providers, as well as families, could greatly impact the current incidence and case fatality of hypothermia. Promotion of immediate drying and wrapping of the newborn, as well as universal STSC could prevent a majority of the incident cases among newborns. With adequate prevention, management will be required less, and associated conditions can be avoided. Researchers studying hypothermia and its interventions should be encouraged to use the same case denitions for hypothermia, including temperature cutoff and place and mode of temperature measurement (Panel 2). This will enable simplied comparison of epidemiology and intervention effectiveness between studies. There is currently no accepted verbal autopsy denition for hypothermia, and thus, its contribution to neonatal mortality remains obscure. Future qualitative research is also needed at the community level on local knowledge and perceptions of cold in the newborn, including the connotations surrounding the local terms for cold. This eld of knowledge includes the Ayurvedic, Chinese and humoral concepts of hot and cold, which informs many health-related behaviors in societies throughout the world. Research is also needed to evaluate the effectiveness of communitybased interventions at preventing and managing hypothermia, including STSC and behavior change management. Investments in training at the clinic or hospital level are urgently needed. Further exploration of gaps in knowledge and practice may signal the need for enhanced training of auxiliary health-care workers in facility-based settings. Finally, education of parents can help increase demand for adequate and timely thermal protection in hospitals at birth. Under the prevailing conditions, the risks and consequences of hypothermia are considerable. Attention of researchers, funding agencies and development organizations to the issue of hypothermia is immediately sought to promote locally acceptable and affordable solutions for prevention and management of neonatal hypothermia.

This study was supported by The Ofce of Health, Infectious Diseases and Nutrition, Global Health Bureau, United States Agency for International Development (USAID) under the terms of Award GHS-A-00-03-00019-00, Global Research Activity Cooperative Agreement with the Johns Hopkins Bloomberg School of Public Health; the USAID India (New Delhi) Mission; and the Saving Newborn Lives program of Save the Children-US, through a grant from the Bill and Melinda Gates Foundation.

1 Blatteis CM. Physiology and Pathophysiology of Temperature Regulation: World Scientic, Singapore, 1998. 2 Committee HAA. Committee Report: American Pediatrics: milestones at the Millennium. Pediatrics 2001; 107: 14821491. 3 Darmstadt GL, Kumar V, Yadav R, Singh V, Singh P, Mohanty S et al. Introduction of community-based skin-to-skin care in rural Uttar Pradesh, India. J Perinatol 2006; 26(10): 597604. 4 Lawn JE, Cousens S, Zupan J. 4 million neonatal deaths: when? Where? Why? Lancet 2005; 365(9462): 891900. 5 Darmstadt GL, Bhutta ZA, Cousens S, Adam T, Walker N, de Bernis L. Evidence-based, cost-effective interventions: how many newborn babies can we save? Lancet 2005; 365(9463): 977988. 6 World Health Organization. Mother-baby Package: Implementing Safe Motherhood in Countries. World Health Organization: Geneva, 1994. 7 WHO. Thermal Control of the Newborn: a Practical Guide. Maternal and Safe Motherhood Programme, Division of Family Health: Geneva, Switzerland, 1993. 8 Bang AT, Reddy HM, Deshmukh MD, Baitule SB, Bang RA. Neonatal and infant mortality in the ten years (1993 to 2003) of the Gadchiroli eld trial: effect of home-based neonatal care. J Perinatol 2005; 25(Suppl 1): S92S107. 9 Kumar R, Aggarwal AK. Body temperatures of home delivered newborns in north India. Trop Doct 1998; 28(3): 134136. 10 Kaushik SL, Grover N, Parmar VR, Kaushik R, Gupta AK. Hypothermia in newborns at Shimla. Indian Pediatr 1998; 35(7): 652656. 11 Byaruhanga R, Bergstrom A, Okong P. Neonatal hypothermia in Uganda: prevalence and risk factors. J Trop Pediatr 2005; 51(4): 212215. 12 Nayeri F, Nili F. Hypothermia at birth and its associated complications in newborns: a follow up study. Iranian J Publ Health 2006; 35(1): 4852. 13 Anderson S, Shakya KN, Shrestha LN, Costello AM. Hypoglycaemia: a common problem among uncomplicated newborn infants in Nepal. J Trop Pediatr 1993; 39(5): 273277. 14 Bolam A, Manandhar DS, Shrestha P, Ellis M, Costello AM. The effects of postnatal health education for mothers on infant care and family planning practices in Nepal: a randomised controlled trial. BMJ 1998; 316(7134): 805811. 15 Jalil F. Perinatal health in Pakistan: a review of the current situation. Acta Paediatr 2004; 93(10): 12731279. 16 Johanson RB, Malla DS, Tuladhar C, Amatya M, Spencer SA, Rolfe P. A survey of technology and temperature control on a neonatal unit in Kathmandu, Nepal. J Trop Pediatr 2001; 39(1): 410. 17 Kambarami RA, Mutambirwa J, Maramba PP. Caregivers perceptions and experiences of kangaroo care in a developing country. Trop Doct 2002; 32(3): 131133. 18 Christensson K, Bhat GJ, Eriksson B, Shilalukey-Ngoma MP, Sterky G. The effect of routine hospital care on the health of hypothermic newborn infants in Zambia. J Trop Pediatr 1995; 41(4): 210214. 19 da Mota Silveira SM, Goncalves de Mello MJ, de Arruda Vidal S, de Frias PG, Cattaneo A. Hypothermia on admission: a risk factor for death in newborns referred to the Pernambuco Institute of Mother and Child Health. J Trop Pediatr 2003; 49(2): 115120.

Panel 2 Research and policy priorities


Consider the inclusion of hypothermia as a cause of death in verbal autopsy instruments. Augment current qualitative and anthropological research surrounding the local understandings of cold, hypothermia and other related topics. Evaluate current and future community-based interventions that include thermal care components. Invest heavily in training all levels of health workers to prevent and manage hypothermia, with a focus on the immediate thermal care of a newborn.

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