Introduction

This study was prompted by an observed case in which a planned cesarean section on a French Bulldog resulted in the delivery of 3 healthy neonates. The resuscitated neonates were placed in an incubator set at 32.2 °C, with oxygen set to deliver 1 L/min (Puppywarmer Pro Series Transport Incubator 325X450X350a; Warmer3 LLC). All 3 puppies were dead within 40 minutes. The temperature in the incubator was > 42.8 °C according to a transrectal digital thermometer reading on a deceased neonate, although the incubator thermostat (TS) read 29.4 °C.¹

Veterinarians and breeders rely on warming devices, including incubators, to maintain proper environmental temperatures for neonates. Neonates of many species, including dogs and cats, are poikilothermic, which means their body temperature is heavily influenced by their environment.^2,3 They have minimal ability to generate heat, except through nonshivering thermogenesis from ingestion of colostrum.⁴ Due to their small size and consequent greater ratio of surface area to volume, core body temperature in canine neonates responds rapidly to the environment and they can quickly become hypothermic or hyperthermic.^5,6 Neonatal puppies begin to exhibit shivering thermogenesis between 6 and 8 days⁷ but do not achieve complete thermoregulatory ability until 18 days of age.⁸ Maintaining the appropriate core body temperature is key in supporting early neonatal life, and alterations in temperature are an important cause of neonatal mortality. Neonates have limited physical capacity to move away from or toward heat sources, so care must be taken to ensure that their environment is maintained within an appropriate thermal range. Core temperatures below 35.0 °C lead to bradycardia, dyspnea, loss of suckle reflex, hypoglycemia, gastrointestinal ileus, and multiple organ failure^4,9; temperatures above 41.1 °C lead to pulmonary edema, petechial and ecchymotic hemorrhage in multiple organs, and death.^10,11

We used 5 different neonatal incubator models designed for use with dogs and cats to determine how closely their set temperatures matched actual temperatures. We used independent tools (eg, thermocouple [TC] and infrared [IR] temperature sensors) to monitor microenvironmental temperatures within neonatal incubators and compare them to the set TS temperature. On the basis of our findings, we provide recommendations to veterinarians and breeders on how to use and monitor neonatal incubators.

Methods

Five incubators were set up (May 25, 2022) in the same facility and tested without replication (of the time/intended temperature/incubator combinations within temperature-measuring device); the following incubators at each time and temperature were measured one after the other as quickly as possible: incubator 1 (Puppywarmer Pro Series Transport Incubator, 330 × 457 × 330 mm), incubator 2 (Puppywarmer Incubator, 457 × 610 × 559 mm), incubator 3 (Puppywarmer Pro Series Incubator, 549 × 549 × 549 mm), incubator 4 (Curadle MX B60 N Pet Brooder; Autoelex Co Ltd), and incubator 5 (Curadle MX B90 N Pet Brooder). Incubator 1 was the same incubator from the case earlier described.¹ Ambient temperature was 22 °C, and relative room humidity was 60%. Humidity was not determined in each incubator. Incubators 1 through 3 all had a rubber mat as the substrate designed to absorb radiant heat from the unit at the top of the incubator. Incubators 4 and 5 had a hard plastic bottom and relied on warm air blown into the unit with a fan. Each TS on the respective incubators was set to 29.4 °C, and singular temperature readings were recorded at 10, 20, and 30 minutes using 3 different methods in quick succession: the built-in TS, a TC (Conformité Européenne and Restriction of Hazardous Substances certified), and an IR temperature sensor (ThermoWorks). Each instrument provided a digital readout for which no interpretation was needed. For each temperature measurement, the incubator door was opened for no longer than 10 seconds at a time when acquiring readings. The TC was placed approximately 2.5 cm above the surface of the incubator, near the center of each respective unit. The IR was aimed through the open door and held approximately 30 cm from the center of the floor of each incubator. After 30 minutes, the incubator TSs were increased to 35.0 °C and temperature readings were repeated in the same manner as the previous temperature setting. These 2 temperature settings were chosen as the common upper and lower settings typically used in our clinic. During the entire trial, for all incubator models, oxygen concentrators (Puppywarmer 2L Pro Series Oxygen Concentrator for incubators 1 through 3; Phillips Respironics EverFlo for incubators 4 and 5) were set to deliver oxygen at 1 L/min and oxygen tubes were connected as per manufacturer recommendations (ie, positioned on the floor of the Puppywarmer models).

Results

Readings from the TS remained within ± 2 °C of the then-current target temperature in each incubator on all measurements. Three of 5 (60%; 95% CI, 17% to 93%) incubators had IR and TC temperature readings that varied > ± 2 °C from the TS temperature (Figures 1–3). In 1 instance, the IR temperature was approximately 20 °C higher than that of the TS. Incubators’ 4 and 5 IR and TC readings did not vary ± 2 °C from the TS readings (Figures 4 and 5).

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Temperatures in veterinary neonatal incubator 1 (Puppywarmer Pro Series Transport Incubator; Warmer3 LLC) as measured with the incubators’ built-in thermostats (TS; circles), a thermocouple (TC; squares) measuring air temperature 2.5 cm above the substrate, and an infrared sensor (IR; triangles) measuring substrate temperatures at the center of each incubator at 10, 20, 30, 40, 50, 60, and 70 minutes after starting from room temperature in a study conducted on May 25, 2022. The dotted line tracks the temperature set on the built-in TS, while the TS target was 29.4 °C for the first 30 minutes and 35 °C for the final 40 minutes. The solid line indicates 41.1 °C, above which rapid organ failure occurs due to hyperthermia.

Citation: Journal of the American Veterinary Medical Association 262, 1; 10.2460/javma.23.07.0382

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Temperatures in veterinary neonatal incubator 2 (Puppywarmer Incubator; Warmer3 LLC). See Figure 1 for methods and key.

Citation: Journal of the American Veterinary Medical Association 262, 1; 10.2460/javma.23.07.0382

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Temperatures in veterinary neonatal incubator 3 (Puppywarmer Pro Series Incubator; Warmer3 LLC). See Figure 1 for methods and key.

Citation: Journal of the American Veterinary Medical Association 262, 1; 10.2460/javma.23.07.0382

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Temperatures in veterinary neonatal incubator 4 (MX B60 N Pet Brooder; Curadle/Autoelex Co Ltd). See Figure 1 for methods and key.

Citation: Journal of the American Veterinary Medical Association 262, 1; 10.2460/javma.23.07.0382

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Temperatures in veterinary neonatal incubator 5 (MX B90 N Pet Brooder; Curadle/Autoelex Co Ltd). See Figure 1 for methods and key.

Citation: Journal of the American Veterinary Medical Association 262, 1; 10.2460/javma.23.07.0382

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Discussion

This report documents discordant temperature measurements from the set point on neonatal incubator TSs. Some recorded temperatures were 20 °C greater than the set temperature. The incubators in this study were all designed specifically for use with puppies and all set at temperatures below target core body temperatures for dogs. Our follow-up comparative trial confirmed the tendency of some models to heat well beyond the set temperature. The temperatures achieved in these incubators were far above those compatible with healthy organ function and pose a serious risk to neonatal puppies. It is recommended that veterinarians and caregivers use independent, supplemental tools such as TC and IR to monitor incubator temperatures.

Methods used to maintain appropriate environmental temperature include surfaces warmed with electricity or water, warmed air, and radiant heaters. Commercial incubators might use any of these methods. Whatever method is chosen, checks and balances should be in place independent of the primary device to ensure that the environmental temperature is in the desired range.

Thermocouples are metallic and rely on conduction for temperature measurement. They are regarded as effective for monitoring surface temperatures and so must be in direct contact with the surface in question.¹² The unit used in this study had a certificate of conformance indicating accuracy of 0.4 °C at both 0 and 100 °C. The sensor was placed approximately 2.5 cm above the substrate and would in this way reflect air temperatures, not surface temperatures. Infrared sensors are useful for rapidly detecting the differing temperatures from adjacent areas. The unit used in this study had a certificate of conformance indicating accuracy between 1.0 and 1.5 °C at temperatures between 0 and 100 °C, respectively. As such, it is important to be careful regarding where they are focused. In this study, the sensor was focused on the substrate and therefore should have reflected local surface temperatures.

Surfaces will differ in temperature on the basis of how they are being heated and may not reflect the actual body temperature of the neonates. Rectal temperature most accurately reflects core body temperature of a neonatal animal.^4,13 Given their small size, care must be taken not to cause irritation from frequent monitoring. We recommend rotating the neonates when monitoring a litter transrectally and trying to sample neonates from the warmest and/or coolest areas of the nesting box or incubator, depending on subsequent readings and visual assessments. Alternatively, IR sensors may also be used to measure neonatal temperature. They should have a strict standard operating procedure, and their accuracy should be verified with measurements taken by rectal thermometers.

In addition to checking all new equipment for proper function prior to use with live animals, the first author’s clinical practice has adopted preventive measures for monitoring neonatal temperatures following cesarean sections. These include the following:

1. 1.Incubator temperature is measured every 15 minutes using 2 independent methods:
   1. a.Thermocouple with the wire placed alongside the neonates.
   2. b.Infrared temperature monitor aimed at the neonatal thorax.
2. 2.Rectal temperature is monitored every 15 minutes from one of the neonates (rotated to a different neonate every measurement) for the first hour.
3. 3.Visual assessment of neonatal breathing pattern and activity level every 15 minutes.

Monitoring in this manner has allowed us to identify concerning temperature fluctuations in other incubators, thereby allowing intervention to prevent potential further hyperthermic events. We continue to use our increased monitoring protocols as a safety measure and recommend this as an appropriate standard of care for veterinarians performing cesarean sections and offering neonatal care.

Disclosures

The authors have nothing to disclose. No AI-assisted technologies were used in the generation of this manuscript.

Funding

The authors have nothing to disclose.