Abstract

Non-human vertebrate blood is commonly collected and assayed for a variety of applications, including veterinary diagnostics and physiological research. Small, often non-lethal samples enable the assessment and monitoring of the physiological state and health of the individual. Traditionally, studies that rely on blood physiology have focused on captive animals or, in studies conducted in remote settings, have required the preservation and transport of samples for later analysis. In either situation, large, laboratory-bound equipment and traditional assays and analytical protocols are required. The use of point-of-care (POC) devices to measure various secondary blood physiological parameters, such as metabolites, blood gases and ions, has become increasingly popular recently, due to immediate results and their portability, which allows the freedom to study organisms in the wild. Here, we review the current uses of POC devices and their applicability to basic and applied studies on a variety of non-domesticated species. We located 79 individual studies that focused on non-domesticated vertebrates, including validation and application of POC tools. Studies focused on a wide spectrum of taxa, including mammals, birds and herptiles, although the majority of studies focused on fish, and typical variables measured included blood glucose, lactate and pH. We found that calibrations for species-specific blood physiology values are necessary, because ranges can vary within and among taxa and are sometimes outside the measurable range of the devices. In addition, although POC devices are portable and robust, most require durable cases, they are seldom waterproof/water-resistant, and factors such as humidity and temperature can affect the performance of the device. Overall, most studies concluded that POC devices are suitable alternatives to traditional laboratory devices and eliminate the need for transport of samples; however, there is a need for greater emphasis on rigorous calibration and validation of these units and appreciation of their limitations.

Introduction

Blood has been collected from non-human vertebrates for decades to obtain information about organismal physiology, health and condition. Blood is an essential and specialized bodily fluid that delivers necessary nutrients and transports metabolic waste products away from the tissues (Ku, 1997). As a result of its multi-faceted role in supporting organismal life, measurements of the chemical and haematological structure of blood can yield important information, often from a relatively small, non-lethal sample (Rogers and Booth, 2004; Cooke et al., 2005; Wimsatt et al., 2005). Veterinarians and animal health specialists routinely collect blood to evaluate the condition and health of animals (Schalm et al., 1975; Archer and Jeffcott, 1977; Thrall et al., 2012). Today, reference values for a range of species, including domestic and exotic vertebrates, are available to inform veterinary practice and enable health monitoring (see Thrall et al., 2012). Comparative physiologists (see Prosser, 1973) collect and study blood from a variety of model vertebrates in an attempt to understand organismal functions, such as osmoregulation (Beadle, 1957), cardiorespiratory capacity (White, 1978) and the evolutionary basis for, and ecological consequences of, intra- and inter-specific variation (Garland and Adolph, 1991; Garland and Carter, 1994; Spicer and Gaston, 1999). Likewise, much work has been devoted to understanding animal–environment interactions, such as effects of thermal extremes (di Prisco, 1997), living at high altitude (Hall et al., 1936) and seasonal influences on blood physiology (Erickson and Youatt, 1961).

Animal physiologists interested in understanding the consequences of a variety of stressors, such as climate change (Helmuth, 2009) and human disturbance (Busch and Hayward, 2009), also rely on markers in vertebrate blood to identify mechanisms of action, detect thresholds and predict consequences in the growing field of conservation physiology (Wikelski and Cooke, 2006; Cooke and O'Connor, 2010; Cooke et al., 2013). Traditionally, these applications required holding animals in captivity; however, a movement of veterinary practices towards conservation and wildlife surveillance (see Meffe, 1999; Deem et al., 2001) has led to the reinvigoration of comparative physiology, with a focus on the ecological and evolutionary processes in a diversity of non-domesticated taxa (Feder and Block, 1991; Mangum and Hochachka, 1998; Denver et al., 2009; Romero and Wikelski, 2010). This progression has led to the application of physiological approaches needed to understand and solve conservation problems (Cooke and O'Connor, 2010). Fortunately, the ‘field physiology toolbox’ has been expanding rapidly, enabling researchers to study physiological attributes, including blood physiology, outside of the laboratory and even in remote locations (Costa and Sinervo, 2004).

The ability to measure blood physiology repeatedly and accurately has relied historically on large, laboratory-bound equipment and/or complicated and time-consuming assays. While many of these traditional methods are widely accepted and still employed in laboratory/captive settings, they require field biologists to preserve and transport samples for later analysis or to focus on other observable measures, such as behaviour, instead of using physiological measures (St-Louis, 2000). Moreover, certain measurements, such as blood acid–base properties, require immediate reading for maximal accuracy, which is not possible in instances where remotely collected blood is transported back to a laboratory setting. Modern advancements in portable metering or point-of-care (POC) devices have the potential to allow biologists to move towards direct field analysis rather than laboratory-based analysis of samples. Originating in human medicine and later progressing into veterinary science, these devices have shown potential in field biology for a variety of taxa (e.g. Cooke et al., 2008; Atkins et al., 2010; Gallagher et al., 2010; Peiró et al., 2010; Gubala et al., 2012; Sampson et al., 2012).

For field biologists, the usefulness of POC devices is largely tied to their portability, allowing the device to be transported in situ with the researcher and study organism for nearly immediate sampling and results (Morgan and Iwama, 1997; Cooke et al., 2008). This early insight provided by POC devices has a range of advantages, including the option to modify a protocol on site, which is useful because pilot testing is often not possible in field studies. In addition, immediate analysis of samples can minimize the potential loss of samples by breakage, transportation and/or degradation (Clark et al., 2011). However, issues may arise when POC devices are applied more broadly, both in terms of environmental conditions and taxonomic group (Costa and Sinervo, 2004). To be functional broadly in field environments, POC devices must compensate for fluctuations in background humidity and temperature as well as account for the physiological differences between relatively stable homeotherms (for which most POC devices are initially calibrated) and heterothermic models that vary along with their external conditions (Costa and Sinervo, 2004; Gallagher et al., 2010; Mecozzi et al., 2010). Physiological conditions and species-specific differences may further complicate the reliability of POC devices, leading to inaccurate and/or imprecise results; as such, the development of species-specific blood physiology ranges may be necessary. Although there are obvious drawbacks to the use of POC devices in the field on non-domesticated and less studied organisms, the ease of use and portability of these devices may largely outweigh the disadvantages. In addition, owing to the affordability of POC devices, the growing number of validation studies on non-domesticated species and the continuing technological advances (e.g. more parameters, greater portability), these devices are likely to play an integral role in modern biology for basic and applied studies.

In this review, we have collected and synthesized information from a number of studies that have used portable POC devices to measure blood physiology parameters from non-domesticated vertebrate animals. Although POC devices vary in size, our review was limited to ‘easily portable’ POC devices due to their increased applicability to field biology. We defined ‘easily portable’ as any device <5 kg that was powered by a self-contained battery and did not require external electricity or compressed gas canisters. We assumed, based on those criteria, that devices could be carried easily by backpack, horseback, small aeroplane, canoe, etc. to remote areas. The objectives of this review were as follows: (i) to examine the current uses of POC devices in medical and veterinary science; (ii) to summarize the calibration and application of POC devices for use on non-domesticated vertebrate taxa (fish, reptiles, birds and mammals); (iii) to identify the limitations of such devices; and (iv) to consider potential future uses of POC devices.

History of point-of-care device development

In the past two decades, POC devices have revolutionized at-home patient care and emergency diagnostic capability by enabling paramedics, healthcare professionals and even patients to measure biochemical markers rapidly and accurately. The use of POC devices in humans was first recorded in 1994, and by 2009 25% of tests were being performed at the site of care (Plebani, 2009). Based on their success and convenience, the use of POC devices has been projected to increase by 12% per year (Plebani, 2009).

These devices can and have been used in various settings, including management and treatment of disease symptoms in the home and in paramedic care (i.e. ambulance), as well as use in field diagnostics (Plebani, 2009; Cima, 2011). Perhaps the most widespread application of such POC devices is for diabetic monitoring of blood glucose, with many variants available for purchase from pharmacies, which have been integrated into day-to-day management of insulin levels by millions of people around the world (Klonoff, 2005). Furthermore, POC devices have been integrated into emergency departments; for example, some units can measure biochemical markers for patients with acute chest pains suggestive of myocardial injury to provide a rapid, whole-blood analysis in 20 min (Apple et al., 2000). Ideally, these devices should help to reduce turnover time for patients in hospitals and, by doing so, enable better utilization of resources, reduce time to discharge and ensure better patient management (Altinier et al., 2001). Not only will the technology of POC devices reduce healthcare costs in North America but, owing to the portability of these devices, it also has the potential to allow the distribution of this healthcare across the world and into less developed regions (Cima, 2011). Human uses have been expanded further to include the monitoring of performance athletes (e.g. lactate levels) and, indeed, some POC devices have been developed for that explicit purpose (e.g. Lactate Pro; Pyne et al., 2000).

Since the introduction of POC devices in the medical field, veterinary science has adopted their use in clinics to monitor the health of animals (Allen and Holm, 2008). As a result of their origins in human medicine (Acierno et al., 2007), quality control is necessary because of the many physiological and biochemical differences across taxa (Allen and Holm, 2008); however, there are a growing number of such devices designed specifically for domesticated animals (e.g. Gluco Pet). Testing the precision of a POC device, or validation, is done by comparing animal- and parameter-specific values with those obtained from a ‘gold standard’ bench-top analyser or laboratory assays (e.g. Clark et al., 2008). The process of validation of POC devices is ongoing, as new devices and biomarkers used to assess animal health are constantly emerging. This task has proved to be even more complex because a specific range of measured values for a particular parameter may vary in its concordance with a bench-top analyser (e.g. POC values may agree better with laboratory-based values inside but not outside of a specific range; Hollis et al., 2008).

Once validated for a certain animal-specific physiological parameter, POC devices have been shown to improve the efficiency of establishing both a diagnosis and a prognosis for that animal (Acierno et al., 2007). Point-of-care devices allow for easy and early identification of sick animals and do not require specialized laboratory personnel (Steinmetz et al., 2007). For example, blood lactate as a measure of tissue hypoxia in sick animals can be measured quickly and accurately with a POC device using a small volume of blood (Mizock and Falk, 1992). Due to the low cost associated with the use of POC testing, many private animal owners, in particular horse owners, use these devices for establishing treatment action, because this early information can be used to determine whether additional, more expensive testing or treatment is necessary (Delesalle et al., 2007). In addition, as new biomarkers are discovered, the hope is that new POC devices will also emerge, benefitting not only veterinary medicine, but also other fields, such as conservation and field physiology.

General approach

We examined various studies that used POC devices on a range of non-domesticated vertebrate taxa. Despite the prominent use and origins of POC devices in emergency patient care and veterinary medicine of domesticated animals (e.g. horses, dogs, cats, mice), we excluded all such studies herein, given our focus on wild, traditionally non-domesticated animals. In some cases, it was unclear whether animals (mostly fish; e.g. Gomes et al., 2006a, b; Trushenski et al., 2010) in captivity were wild or captive bred, so we relied on our best judgement. We did encounter several studies that used POC devices with invertebrates (e.g. Allender et al., 2010; Butcher et al., 2012), but focused solely on vertebrates, given that invertebrate blood physiology is less well studied. As noted above, we included only studies that used devices considered to be ‘easily portable’. In addition, we excluded all portable devices that were not electronic (e.g. refractometers for plasma protein) or that simply separated blood constituents [e.g. manual or electronic centrifuges for quantifying haematocrit (Hct)].

Primary literature searches were conducted between 15 September and 18 November 2012. Relevant papers were found by searching a variety of academic journal databases (e.g. Web of Science, Scopus) and Internet search engines (e.g. Google Scholar) with relevant search terms (e.g. ‘point-of-care analyser’, ‘portable clinical analyser’, ‘glucose meter’), as well as identifying citations by other papers. To identify papers that fitted our criteria, we reviewed the study design to determine whether a POC device was used. We then extracted key information and populated a database with predetermined headings, such as species, parameters tested, POC device used, type of study and limits. Studies were classified either as validations, which compared the POC devices with traditional laboratory analysis, or as applications, which used POC devices to measure blood chemistry for either basic or applied research. In some studies, POC devices were used for both validation and application purposes, and such studies were therefore classified accordingly as both.

Characteristics and trends in point-of-care device literature

General characteristics

The literature search yielded 79 studies involving the use of POC devices in a variety of non-domesticated vertebrate species. The use of POC devices in ecology and conservation is a relatively novel concept, because the majority of published articles have appeared within the last decade and range from 1995 to the present. We collected articles from various journals (n = 42), which included a wide variety of themes, such as veterinary medicine, disease, toxicology, conservation, physiology and food science. Of the 79 peer-reviewed studies, 8.9% (n = 7) of articles were published in Fisheries Research, while 7.6% (n = 6) of articles were published in Comparative Biochemistry and Physiology Part A. Validation studies comprised 17.7% (n = 14) of papers, from which applications studies accounted for 78.5% (n = 62) of the total. Only 3.8% (n = 3) of studies combined both validation and application.

Taxonomic patterns

We retrieved papers from four different taxonomic vertebrate groups, namely fish, birds, reptiles and mammals. Due to the large number of fish studies and the associated physiological differences between teleost and cartilaginous fishes, we separated all Chondrichthyes-based studies into a separate group. Teleost fish were the most-studied taxa, accounting for more than half of the total number of articles (n = 48; 60.8%). Studies focusing on Chondrichthyes accounted for 15.2% (n = 12) of all studies, while mammals, reptiles and birds accounted for 11.4% (n = 9), 8.9% (n = 7) and 3.8% (n = 3), respectively. Atlantic salmon (Salmo salar) was the most-studied species (8.9%; n = 7), while studies focused on smallmouth bass (Micropterus dolomieu) and Atlantic cod (Gadus morhua) were the second and third most-studied organisms, with 7.6% (n = 6) and 6.3% (n = 5), respectively.

Point-of-care device tools and parameters tested

In total, studies used 20 different POC devices that fit the ‘easily portable’ definition (see Introduction). Although we found several studies using the VetScan analyser, which is considered a POC device by the authors of those papers, it did not fit our definition of ‘easily portable’ and was therefore excluded. The i-STAT hand-held blood analyser was the device most used (53.2%; n = 42), followed by the Lactate Pro lactate meter and Accu-chek glucometer, which were used in 27.8% (n = 22) and 24.1% (n = 19) of assessed studies, respectively (Table 1). In addition, glucometers were the most diverse POC device, with nine different models being used. The majority of devices used (85%; n = 17) measured only one parameter, such as the Lactate Pro, while the i-STAT analyser was the most used device that was capable of analysing more than one blood parameter. Finally, the majority of studies used whole blood, rather than plasma, when using the POC devices (94.9%; n = 75).

Table 1:

List of most common point-of-care devices used in studies analysed (note that not all data are available due to products being discontinued)

Device Company Parameters tested Additional cartridges/strips Type of blood required Amount of blood required (μl) Battery required Range (mmol/l unless otherwise stated) Dimensions (length × width × height; mm) Weight (g) Current validations Temperature range (°C) Humidity range (relative humidity unless stated) 
Accu-chek Advantage Roche Diagnostics/Boehringer Mannheim Glucose Yes; Accu-chuk strips Whole 0.6 One 3 V lithium battery 0.6–33.3 84 × 53 × 21 60 No 10–40 10–90% 
IQ Prestige Home Diagnostics Inc. Glucose Yes; Prestige IQ strips Whole One AAA 1.5 V alkaline battery 1.4–33.3 70 × 102 × 20 102 Burdick et al. (2012), mammal 15–37 Any non-condensing atmosphere 
Ascensia Elite Bayer Corporation Glucose Yes; Ascensia Elite Test strips Whole One 3 V lithium battery 1.1–33.3 81 × 51 × 14 50 No 10–40 20–80% 
ExacTech Abbott Point of Care Glucose Yes; ExacTech strips Whole 10 Not available Not available 93 × 55 × 10 43 No Not available Not available 
Freestyle Freedom Lite Abbott Point of Care Glucose Yes; Freestyle Freedom Lite strips Whole 0.3 One 3 V lithium battery 1.1–27.9 8.38 × 5.08 × 1.3 42.35 Wells and Pankhurst (1999), fish 4–40 5–90% non-condensing 
Glucometer Elite Bayer Corporation Glucose Yes; Glucometer Elite strips Whole Two 3 V lithium batteries 1.1–33.3 97.8 × 56 × 14.5 60 No 10–40 20–80% 
Sure Step Life Scan/Johnson and Johnson Glucose Yes; Sure Step strips Whole Three AA 1.5 V alkaline batteries 0–500 mg/dl 89 × 61 × 20 107.7 Lieske et al. (2002), birds 10–35 10–90% 
One Touch Ultra Life Scan/Johnson and Johnson Glucose Yes; One Touch Ultra strips Whole One 3 V lithium battery 1.1–33.3 79 × 57 × 23 42 No 6–44 10–90% 
Precision QID Medisense Glucose Yes; MicroFlo Plus strips Whole 3.5 Non-replaceable 1.1–33.3 97 × 48 × 15 39 No 4–30 Not available 
Accusport Analyser Boehringer Mannheim Lactate Yes; Lactate Test strips Whole 10–20 Three 1.5 V AAA batteries 0.8–22 115 × 62 × 18.5 100 Wells and Pankhurst (1999), fish 5–35 10–90% 
Accutrend Roche Diagnostics Lactate Yes; Lactate Test strips Whole 20–25 Three 1.5 V AAA batteries 0.8–22 115 × 62 × 18.5 100 No 5–35 10–90% 
Lactate Pro Arkray KDK Lactate Yes; Lactate Pro Strips Whole Two 3 V lithium batteries 0.8–23.3 83.8 × 55 × 14.5 50 No 10–40 20–80% 
HemoCue Hemocue 201+ Haemoglobin Yes; meseauring cuvette Non-specific Non-specific Four AA batteries 0–256 g/l 160 × 85 × 43 350 Clark et al. (2008) Not available Not available 
BMS Hemoglo-binometer BMS Haemoglobin Yes Non-specific Non specific Two size ‘C’ batteries 4–20 g/dl 170 × 70 × 40 Not available Iwama et al. (1995) 10–40 Not available 
IQ128 Elite IQ Scientific Instruments Inc. pH No Non-specific Non-specific Two 3 V lithium batteries pH 2–12 152.4 × 78.57 × 16.38 450 Brown et al. (2008), fish 5–40 Not available 
WTW pH Meter pH330 Hoskin Scientific Ltd pH No Non-specific Non-specific Four AA batteries −2.00 to 19.99 pH units 172 × 80 × 37 300 No −5 to 105 Not available 
SevenGo Pro Mettler Toledo pH and ion No Non-specific Non-specific Four AA batteries −2.00 to 19.99 pH units 220 × 90 × 45 325 No 0–40 0–85% 
IRMA True Point International Technidyne Corporation Various; lactate, glucose, pH, variety of ions Yes; various cartridges depending on parameters to be tested Whole blood or plasma 125–500 One 7.2 V battery Various ranges depending on parameters 292.1 × 211.3 × 127 2381 No 12–30 0–80% non-condensing 
i-STAT Abbott Point of Care Various; lactate, glucose, pH, variety of ions Yes; various cartridges depending on parameters to be tested Non-specific Non-specific Two 9 V lithium batteries Various ranges depending on parameters 209 × 64 × 52 520 No 16–30 0–90% 
Ames Mini-lab Miles Canada Inc. Various Not available Not available Not available Not available Not available Not available Not available Iwama et al. (1995) Not available Not available 
Device Company Parameters tested Additional cartridges/strips Type of blood required Amount of blood required (μl) Battery required Range (mmol/l unless otherwise stated) Dimensions (length × width × height; mm) Weight (g) Current validations Temperature range (°C) Humidity range (relative humidity unless stated) 
Accu-chek Advantage Roche Diagnostics/Boehringer Mannheim Glucose Yes; Accu-chuk strips Whole 0.6 One 3 V lithium battery 0.6–33.3 84 × 53 × 21 60 No 10–40 10–90% 
IQ Prestige Home Diagnostics Inc. Glucose Yes; Prestige IQ strips Whole One AAA 1.5 V alkaline battery 1.4–33.3 70 × 102 × 20 102 Burdick et al. (2012), mammal 15–37 Any non-condensing atmosphere 
Ascensia Elite Bayer Corporation Glucose Yes; Ascensia Elite Test strips Whole One 3 V lithium battery 1.1–33.3 81 × 51 × 14 50 No 10–40 20–80% 
ExacTech Abbott Point of Care Glucose Yes; ExacTech strips Whole 10 Not available Not available 93 × 55 × 10 43 No Not available Not available 
Freestyle Freedom Lite Abbott Point of Care Glucose Yes; Freestyle Freedom Lite strips Whole 0.3 One 3 V lithium battery 1.1–27.9 8.38 × 5.08 × 1.3 42.35 Wells and Pankhurst (1999), fish 4–40 5–90% non-condensing 
Glucometer Elite Bayer Corporation Glucose Yes; Glucometer Elite strips Whole Two 3 V lithium batteries 1.1–33.3 97.8 × 56 × 14.5 60 No 10–40 20–80% 
Sure Step Life Scan/Johnson and Johnson Glucose Yes; Sure Step strips Whole Three AA 1.5 V alkaline batteries 0–500 mg/dl 89 × 61 × 20 107.7 Lieske et al. (2002), birds 10–35 10–90% 
One Touch Ultra Life Scan/Johnson and Johnson Glucose Yes; One Touch Ultra strips Whole One 3 V lithium battery 1.1–33.3 79 × 57 × 23 42 No 6–44 10–90% 
Precision QID Medisense Glucose Yes; MicroFlo Plus strips Whole 3.5 Non-replaceable 1.1–33.3 97 × 48 × 15 39 No 4–30 Not available 
Accusport Analyser Boehringer Mannheim Lactate Yes; Lactate Test strips Whole 10–20 Three 1.5 V AAA batteries 0.8–22 115 × 62 × 18.5 100 Wells and Pankhurst (1999), fish 5–35 10–90% 
Accutrend Roche Diagnostics Lactate Yes; Lactate Test strips Whole 20–25 Three 1.5 V AAA batteries 0.8–22 115 × 62 × 18.5 100 No 5–35 10–90% 
Lactate Pro Arkray KDK Lactate Yes; Lactate Pro Strips Whole Two 3 V lithium batteries 0.8–23.3 83.8 × 55 × 14.5 50 No 10–40 20–80% 
HemoCue Hemocue 201+ Haemoglobin Yes; meseauring cuvette Non-specific Non-specific Four AA batteries 0–256 g/l 160 × 85 × 43 350 Clark et al. (2008) Not available Not available 
BMS Hemoglo-binometer BMS Haemoglobin Yes Non-specific Non specific Two size ‘C’ batteries 4–20 g/dl 170 × 70 × 40 Not available Iwama et al. (1995) 10–40 Not available 
IQ128 Elite IQ Scientific Instruments Inc. pH No Non-specific Non-specific Two 3 V lithium batteries pH 2–12 152.4 × 78.57 × 16.38 450 Brown et al. (2008), fish 5–40 Not available 
WTW pH Meter pH330 Hoskin Scientific Ltd pH No Non-specific Non-specific Four AA batteries −2.00 to 19.99 pH units 172 × 80 × 37 300 No −5 to 105 Not available 
SevenGo Pro Mettler Toledo pH and ion No Non-specific Non-specific Four AA batteries −2.00 to 19.99 pH units 220 × 90 × 45 325 No 0–40 0–85% 
IRMA True Point International Technidyne Corporation Various; lactate, glucose, pH, variety of ions Yes; various cartridges depending on parameters to be tested Whole blood or plasma 125–500 One 7.2 V battery Various ranges depending on parameters 292.1 × 211.3 × 127 2381 No 12–30 0–80% non-condensing 
i-STAT Abbott Point of Care Various; lactate, glucose, pH, variety of ions Yes; various cartridges depending on parameters to be tested Non-specific Non-specific Two 9 V lithium batteries Various ranges depending on parameters 209 × 64 × 52 520 No 16–30 0–90% 
Ames Mini-lab Miles Canada Inc. Various Not available Not available Not available Not available Not available Not available Not available Iwama et al. (1995) Not available Not available 

Summary of taxon-specific validation and application studies

Chondrichthyes

Validation studies

Only two studies were found that assessed the accuracy of POC devices with Chondrichthyes species. Both validation studies compared laboratory-based equipment with POC devices using linear regressions (Table 2). Gallagher et al. (2010) used the i-STAT analyser to measure acid–base parameters and/or a lone metabolite (lactate) in the whole blood of three different Chondrichthyes species. The i-STAT analyser was determined to be acceptable for the measurement of pH, partial pressure of oxygen (pO2) and carbon dioxide (pCO2) with temperature correction, as well as lactate, but given that derived correction factors varied by species and only a lone temperature point was examined, the authors cautioned against broad applicability across taxa and temperatures without further testing (Gallagher et al., 2010). Awruch et al. (2011) determined that the use of the Lactate Pro was acceptable for measuring lactate, using a single species (i.e. Galeorhinus galeus), despite the fact that the device consistently overestimated lactate concentrations in whole blood relative to plasma. Further research is suggested into this lack of consistency between blood and plasma lactate values (Awruch et al., 2011). While not a validation relative to traditional instrumentation, a third study found compatibility in side-by-side acid–base values between two POC instruments (i-STAT analyser vs. IRMA TruPoint analyser) when reading whole blood from minimally stressed chondrichthyans (Mandelman and Skomal, 2009). While more work is needed in parameters beyond acid–base, initial studies signify that POC devices can be acceptable tools for blood parameter readings in Chondrichthyes.

Table 2:

The point-of-care (POC) device validation studies used in this study, grouped by class

Citation Species Temperature (°C) POC device used Standard method Analyte measured Comparison with POC reading Acceptable comparison 
Awruch et al. (2011) Shark (Galeorhinus galeusNot available Lactate Pro Enzymatic kit/spectrophotometer Lactate Similar Yes 
Gallagher et al. (2010) Sharks (Carcharhinus plumbeus, Mustelus canis25 i-STAT (CG4+) Blood gas analyser (thermostatted) pH Similar Yes 
    Blood gas analyser (thermostatted) pO2 Similar Yes 
    Blood gas analyser (thermostatted) pCO2 Similar Yes 
    Laboratory lactate and glucose analyser Lactate Similar Yes 
Brown et al. (2008) Bony fish (Gadus morhuaNot available Lactate Pro Enzymatic kit/spectrophotometer Lactate Similar Yes 
Clark et al. (2008) Bony fish (Oncorhynchus nerka, Oncorhynchus tshawytscha, Thunnus orientalis, Scomber japonicusNot available HemoCue Drabkin method Haemoglobin Higher Somewhat 
Cooke et al. (2008) Bony fish (Albula vulpes21–25 i-STAT (E3+) Laboratory chemistry analyser Na+ Higher Yes 
     K+ Lower Yes 
     Cl Lower Somewhat 
    Centrifuge Haematocrit Variable Yes 
   Accu-Chek Advantage Laboratory chemistry analyser Glucose Similar Yes 
DiMaggio et al. (2010) Bony fish (Fundulus seminolisNot available i-STAT (E3+) Centrifuge Haematocrit Lower No 
    Flame photometer Na+ Lower No 
    Flame photometer K+ Lower No 
    Chloridometer Cl Higher No 
Evans et al. (2003) Bony fish (Oreochromis niloticus25–28 One Touch Ultra Laboratory colorimetric method Glucose Lower Yes 
Harrenstien et al. (2005) Bony fish (Sebastes melanops, Sebastes mystinus11.5 i-STAT (EC8+) Laboratory chemistry analyser Na+ Lower Somewhat 
    Laboratory chemistry analyser K+ Similar No 
    Laboratory chemistry analyser Cl Variable No 
    Laboratory chemistry analyser BUN Lower Somewhat 
    Laboratory chemistry analyser Glucose Similar No 
    Laboratory chemistry analyser Haemoglobin Lower Somewhat 
    Blood gas analyser pH Lower Somewhat 
    Blood gas analyser pCO2 Higher Somewhat 
    Blood gas analyser TCO2 Lower No 
    Blood gas analyser HCO3 Lower No 
    Blood gas analyser Base excess Lower No 
Iwama et al. (1995) Bony fish (Salmo salarNot available ExacTech Laboratory assay kit Glucose Similar Yes 
   BMS Hemoglobinometer Laboratory assay kit Haemoglobin Similar Yes 
   Ames minilab Laboratory assay kit Glucose, haemoglobin Similar Yes 
Serra-Llinares et al. (2012) Bony fish (Gadus morhuaLactate Pro Reference values Lactate Similar Yes 
Wells and Pankhurst (1999) Bony fish (Oncorhynchus mykiss14–40 Accuchek Advantage Hexokinase method Glucose Lower Somewhat 
   Accusport Enzymatic kit/spectrophotometer Lactate Lower Somewhat 
McCain et al. (2010) Reptiles (Pogona vitticeps, Tiliqua gigas, Geochelone platynota, Geochelone elegans, Boa constrictor, Pituophis melanoleucusNot available i-STAT (6+) Laboratory chemistry analyser Na+ Similar Somewhat 
     K+ Similar Somewhat 
     Cl Similar Somewhat 
     Glucose Similar Somewhat 
Wolf et al. (2008) Reptile (Caretta caretta, Chelonia mydas, Lepidochelys kempii18.9–27.2 i-STAT (EC8+) Centrifuge Haematocrit Lower Somewhat 
    Laboratory chemistry analyser Na+ Similar Somewhat 
    Laboratory chemistry analyser K+ Similar Somewhat 
    Laboratory chemistry analyser Cl Lower Somewhat 
    Laboratory chemistry analyser Glucose Lower Somewhat 
    Laboratory chemistry analyser BUN Higher Somewhat 
Lieske et al. (2002) Bird (Cerorhinca monocerataNot available Accu-Chek Advantage Reagent strips Glucose Similar Yes 
   Precision QID Reagent strips Glucose Similar Yes 
   Glucometer Elite Reagent strips Glucose Similar Yes 
   Sure Step Reagent strips Glucose Similar Yes 
Burdick et al. (2012) Mammal (Odocoileus virginianusNot available IQ Prestige Smart Laboratory/portable chemistry analyser Glucose Variable No 
   Prestige Smart Laboratory/portable chemistry analyser Glucose Variable No 
Hopper and Cray (2007) Mammal (Macaca fasicularisNot available i-STAT (EC8+) Centrifuge Haematocrit Lower Somewhat 
    Laboratory chemistry analyser Na+ Higher Somewhat 
    Laboratory chemistry analyser K+ Similar Somewhat 
    Laboratory chemistry analyser Cl Higher Somewhat 
    Laboratory chemistry analyser BUN Higher Somewhat 
    Laboratory chemistry analyser Glucose Lower Somewhat 
    Laboratory chemistry analyser Haemoglobin Higher Somewhat 
    Laboratory chemistry analyser TCO2 Higher Yes 
Larsen et al. (2002) Mammal (Mirounga angustirostrisNot available i-STAT (6+) Laboratory chemistry analyser Na+ Lower No 
    Laboratory chemistry analyser K+ Similar Yes 
    Laboratory chemistry analyser Cl Higher Somewhat 
    Laboratory chemistry analyser BUN Similar Yes 
    Laboratory chemistry analyser Glucose Lower Somewhat 
    Centrifuge Haematocrit Similar Yes 
Citation Species Temperature (°C) POC device used Standard method Analyte measured Comparison with POC reading Acceptable comparison 
Awruch et al. (2011) Shark (Galeorhinus galeusNot available Lactate Pro Enzymatic kit/spectrophotometer Lactate Similar Yes 
Gallagher et al. (2010) Sharks (Carcharhinus plumbeus, Mustelus canis25 i-STAT (CG4+) Blood gas analyser (thermostatted) pH Similar Yes 
    Blood gas analyser (thermostatted) pO2 Similar Yes 
    Blood gas analyser (thermostatted) pCO2 Similar Yes 
    Laboratory lactate and glucose analyser Lactate Similar Yes 
Brown et al. (2008) Bony fish (Gadus morhuaNot available Lactate Pro Enzymatic kit/spectrophotometer Lactate Similar Yes 
Clark et al. (2008) Bony fish (Oncorhynchus nerka, Oncorhynchus tshawytscha, Thunnus orientalis, Scomber japonicusNot available HemoCue Drabkin method Haemoglobin Higher Somewhat 
Cooke et al. (2008) Bony fish (Albula vulpes21–25 i-STAT (E3+) Laboratory chemistry analyser Na+ Higher Yes 
     K+ Lower Yes 
     Cl Lower Somewhat 
    Centrifuge Haematocrit Variable Yes 
   Accu-Chek Advantage Laboratory chemistry analyser Glucose Similar Yes 
DiMaggio et al. (2010) Bony fish (Fundulus seminolisNot available i-STAT (E3+) Centrifuge Haematocrit Lower No 
    Flame photometer Na+ Lower No 
    Flame photometer K+ Lower No 
    Chloridometer Cl Higher No 
Evans et al. (2003) Bony fish (Oreochromis niloticus25–28 One Touch Ultra Laboratory colorimetric method Glucose Lower Yes 
Harrenstien et al. (2005) Bony fish (Sebastes melanops, Sebastes mystinus11.5 i-STAT (EC8+) Laboratory chemistry analyser Na+ Lower Somewhat 
    Laboratory chemistry analyser K+ Similar No 
    Laboratory chemistry analyser Cl Variable No 
    Laboratory chemistry analyser BUN Lower Somewhat 
    Laboratory chemistry analyser Glucose Similar No 
    Laboratory chemistry analyser Haemoglobin Lower Somewhat 
    Blood gas analyser pH Lower Somewhat 
    Blood gas analyser pCO2 Higher Somewhat 
    Blood gas analyser TCO2 Lower No 
    Blood gas analyser HCO3 Lower No 
    Blood gas analyser Base excess Lower No 
Iwama et al. (1995) Bony fish (Salmo salarNot available ExacTech Laboratory assay kit Glucose Similar Yes 
   BMS Hemoglobinometer Laboratory assay kit Haemoglobin Similar Yes 
   Ames minilab Laboratory assay kit Glucose, haemoglobin Similar Yes 
Serra-Llinares et al. (2012) Bony fish (Gadus morhuaLactate Pro Reference values Lactate Similar Yes 
Wells and Pankhurst (1999) Bony fish (Oncorhynchus mykiss14–40 Accuchek Advantage Hexokinase method Glucose Lower Somewhat 
   Accusport Enzymatic kit/spectrophotometer Lactate Lower Somewhat 
McCain et al. (2010) Reptiles (Pogona vitticeps, Tiliqua gigas, Geochelone platynota, Geochelone elegans, Boa constrictor, Pituophis melanoleucusNot available i-STAT (6+) Laboratory chemistry analyser Na+ Similar Somewhat 
     K+ Similar Somewhat 
     Cl Similar Somewhat 
     Glucose Similar Somewhat 
Wolf et al. (2008) Reptile (Caretta caretta, Chelonia mydas, Lepidochelys kempii18.9–27.2 i-STAT (EC8+) Centrifuge Haematocrit Lower Somewhat 
    Laboratory chemistry analyser Na+ Similar Somewhat 
    Laboratory chemistry analyser K+ Similar Somewhat 
    Laboratory chemistry analyser Cl Lower Somewhat 
    Laboratory chemistry analyser Glucose Lower Somewhat 
    Laboratory chemistry analyser BUN Higher Somewhat 
Lieske et al. (2002) Bird (Cerorhinca monocerataNot available Accu-Chek Advantage Reagent strips Glucose Similar Yes 
   Precision QID Reagent strips Glucose Similar Yes 
   Glucometer Elite Reagent strips Glucose Similar Yes 
   Sure Step Reagent strips Glucose Similar Yes 
Burdick et al. (2012) Mammal (Odocoileus virginianusNot available IQ Prestige Smart Laboratory/portable chemistry analyser Glucose Variable No 
   Prestige Smart Laboratory/portable chemistry analyser Glucose Variable No 
Hopper and Cray (2007) Mammal (Macaca fasicularisNot available i-STAT (EC8+) Centrifuge Haematocrit Lower Somewhat 
    Laboratory chemistry analyser Na+ Higher Somewhat 
    Laboratory chemistry analyser K+ Similar Somewhat 
    Laboratory chemistry analyser Cl Higher Somewhat 
    Laboratory chemistry analyser BUN Higher Somewhat 
    Laboratory chemistry analyser Glucose Lower Somewhat 
    Laboratory chemistry analyser Haemoglobin Higher Somewhat 
    Laboratory chemistry analyser TCO2 Higher Yes 
Larsen et al. (2002) Mammal (Mirounga angustirostrisNot available i-STAT (6+) Laboratory chemistry analyser Na+ Lower No 
    Laboratory chemistry analyser K+ Similar Yes 
    Laboratory chemistry analyser Cl Higher Somewhat 
    Laboratory chemistry analyser BUN Similar Yes 
    Laboratory chemistry analyser Glucose Lower Somewhat 
    Centrifuge Haematocrit Similar Yes 

Na+, sodium; K+, potassium; Cl, chloride; BUN, blood urea nitrogen; TCO2, total carbon dioxide; pCO2, partial pressure of carbon dioxide; HCO3, bicarbonate; pO2, oxygen partial pressure. For each species and analyte, the POC and standard (control) device are presented together with the relative comparison between the two. Where possible, the relevant body/experimental temperatures are presented. The distilled opinions presented by the authors of each study are also presented, but case-by-case caveats are not reported here. Many papers with ‘acceptable’ comparisons argue the need for corrective calculations or find these devices acceptable for relative rather than absolute measurement of an analyte.

Application studies

As a result of their frequency of capture in commercial fisheries as bycatch and target species, many application studies of chondrichthyans have focused on the physiological consequences related to acute capture stress. The physiological effects of otter trawl capture in spiny dogfish was a reoccurring topic, presented by Mandelman and Farrington (2007a, b) as a duo of papers, which assessed pH, pO2 and pCO2 values in relationship to various aspects of capture (e.g. transport, captivity; Mandelman and Farrington, 2007b). Researchers have compared pH values generated with POC devices for Chondrichthyes captured by long-line (Mandelman and Skomal, 2009; Brooks et al., 2011; Hyatt et al., 2012), rod and reel (Brill et al., 2008) and gillnet (Frick et al., 2012; Hyatt et al., 2012). Additional physiological parameters associated with aerial exposure and seasonality (Cicia et al., 2012), tonic immobility (Brooks et al., 2011) and reference ranges of wild and captive individuals (Naples et al., 2012) have been studied. Most of these studies were conducted in the field, although four studies (Brill et al., 2008; Brooks et al., 2011; Cicia et al., 2012; Naples et al., 2012) were conducted fully or partly in a laboratory setting. A total of four POC devices were used to assess blood physiology in various Chondrichthyes species. The i-STAT analyser, a multi-parameter POC device, was the most commonly used device, while two single-parameter devices (Accu-chek glucometer and Lactate Pro lactate meter) were both used in more than one study. Numerous blood parameters were measured, with pH, lactate and pCO2 being the most commonly studied variables as indicators of acute stress.

Teleost fish

Validation studies

Point-of-care devices have been used widely in teleost fishes. The accuracy of these devices has been validated by nine studies in teleosts, where POC devices were statistically compared with laboratory-based equipment (Table 2). The i-STAT analyser has been validated for use in bonefish (Albula vulpes; Cooke et al., 2008) and Seminole killifish (Fundulus seminoles; DiMaggio et al., 2010) as well as two species of rockfish (Sebastes melanops and Sebastes mystinus; Harrenstien et al., 2005). Cooke et al. (2008) validated the i-STAT analyser for chloride (Cl), sodium (Na+), potassium (K+) and haematocrit (Hct), and although the POC device and laboratory reference results deviated slightly, they concluded that relative differences could be determined accurately for bonefish. This differed from a study by DiMaggio et al. (2010), where the same blood parameters were assessed by the i-STAT, but the device was determined to be unsuitable for assessment in Seminole killifish, largely due to issues with blood clotting. In a third study on two species of rockfish by Harrenstien et al. (2005), the i-STAT was validated for pH, pCO2, Na+, urea nitrogen, Hct and haemoglobin (Hb); however, it was found to be unsuitable for glucose (due to a wide reference range), total CO2, bicarbonate (HCO3) and K+ (due to unknown factors or device inconsistency), as well as Cl (and therefore anion gap; as these values were outside the measurable range of the device). The Ames Minilab and ExacTech glucose meter has also been validated for use in rainbow trout (Oncorhynchus mykiss) and Atlantic salmon for analysis of glucose and Hb but not erythrocyte number (Iwama et al., 1995). Minilab erythrocyte number measurements were thought to have varied from laboratory reference values due to physiological differences in human and teleost red blood cells, because this device was originally calibrated for use on human samples (Iwama et al., 1995). Generally, these studies suggest that the i-STAT, Minilab analyser and ExacTech glucose meter are useful in the measurement of blood parameters in teleost fish; however, species-specific validation is necessary for these devices because they were originally designed for use on mammals.

Glucose has also been validated for measurement by multiple versions of the Accu-chek, Freestyle Freedom Lite and the OneTouch Ultra glucose meter. Two other studies determined that glucose could be measured by the Accu-chek glucose meter in bonefish (Cooke et al., 2008) and rainbow trout (Wells and Pankhurst, 1999). One further study validated the use of the OneTouch Ultra glucose meter in Nile tilapia (Oreochromis niloticus; Evans et al., 2003). Overall, these studies suggested that relative rather than absolute values should be represented, because these devices tended to underestimate glucose values compared with laboratory reference values.

Two lactate POC devices, the Accusport and Lactate Pro lactate analysers, have been validated for use in teleost fishes. The Accusport (Wells and Pankhurst, 1999) lactate meter underestimated lactate levels compared with laboratory reference values in rainbow trout; similar to glucose, it was suggested that relative rather than absolute values should be represented. Alternatively, Brown et al. (2008) found that the Lactate Pro meter provided more accurate lactate values in Atlantic cod (Gadus morhua), when compared with laboratory reference values; however, resting lactate levels were below the detection limit of this meter. Serra-Llinares et al. (2012) has suggested that the Lactate Pro meter can effectively measure lactate levels from frozen plasma in Atlantic cod (Gadus morhua). These studies suggest that these two POC devices may provide reliable and useful lactate measurements.

Haemoglobin measurements by POC devices have been validated for the BMS Hemoglobinometer and the HemoCue haemoglobin analyser in four Salmonid and two Perciformes species. Iwama et al. (1995) found that the BMS Hemoglobinometer accurately measured Hb levels in two salmonid species; however, readings below 4 g/dl were not possible. Haemoglobin levels were generally overestimated by the HemoCue haemoglobin analyser in comparison to laboratory analysis (Drabkin's method) in two Salmonid and two Perciformes species; however, it was suggested that calibration equations could be applied to the data due to the systematic nature of the overestimation (Clark et al., 2008). Overall, both POC devices may provide valuable Hb measurements, provided they are validated in the species of interest prior to application.

Application studies

Teleosts represent an important group of vertebrates in fisheries and aquaculture; as such, there is a demand for understanding the physiological impacts of these practices on fish. Point-of-care devices provide a convenient method to assess the effects of commercial and recreational fishing on a number of fish species. The effects of catch-and-release angling and barotrauma have been assessed mainly using glucose and lactate levels as indicators of stress, as well as Hct and Hb in smallmouth and largemouth bass (Micropterus salmonides; Gravel and Cooke, 2008; Hanson et al., 2008; White et al., 2008; Nguyen et al., 2009; Thompson et al., 2012), muskellunge (Esox masquinongy; Landsman et al., 2011), northern pike (Esox lucius; Arlinghaus et al., 2009), great barracuda (Sphyraena barracuda; O'Toole et al., 2010), snapper (Pagrus auratus; Wells and Dunphy, 2009) and bonefish (Suski et al., 2007). Henry et al. (2009) quantified the effects of fishing lure retention on smallmouth bass (glucose and lactate), while Roth and Rotabakk (2012) assessed the consequences of commercial and recreational fisheries in saithe (Pollachius virens; multiple parameters).

Field and laboratory-based experiments as well as aquaculture facility practices generally require fish handling. As such, the physiological effects of fish manipulation have been assessed in a number of studies using POC devices. Fish capture, transportation, holding and sedation are some of the common practices involved when researching teleosts. Using bonefish, Murchie et al. (2009) assessed the effect of capture, transport and long-term holding, while Cooke et al. (2008) evaluated the effect of different capture techniques to assess post-capture stress on a number of blood physiology parameters. Moran et al. (2008) assessed the effect of hypercapnic conditions associated with transportation on glucose and lactate levels in yellowtail kingfish (Seriola lalandi). Further studies investigated the physiological effects of sedation on fish. The effects of electrosedation on glucose and lactate levels were examined in grass carp (Ctenopharyngodon idella; Bowzer et al., 2012), hybrid striped bass (Morone chrysops × Morone saxatilis; Trushenski and Bowker, 2012; Trushenski et al., 2012a) and largemouth bass (Trushenski et al., 2012b). Anaesthetics used prior to harvest in channel catfish (Bosworth et al., 2007) have been assessed for various parameters; in addition, the effects of the overall anaesthetic efficiency and how this affects the quality of RNA extracted (Olsvik et al., 2007) have been studied. The post-mortem effects of carbon monoxide (Bjørlykke et al., 2011) and pre-slaughter live-chilling sedation effects (Foss et al., 2012) have been examined in Atlantic salmon. Point-of-care devices have also been used to measure glucose, potassium and sodium in Atlantic salmon fillets to determine retention of the synthetic antioxidant, butylated hydroxyanisole (Petri et al., 2008).

In addition to capture and handling, teleosts are often exposed to a number of other abiotic and biotic stressors. For example, using glucose and/or lactate levels, Bjørn et al. (2001) studied infection of brown trout (Salmo trutta) by salmon lice, Evans et al. (2003) studied sub-lethal dissolved oxygen stress and susceptibility to Streptococcus algalactiae in Nile tilapia, and Breau et al. (2011) studied the effects of increased water temperature on Atlantic salmon. Effects of captive rearing have been studied by looking at the effects of water reuse and stock density on growth rate in juvenile cod (Gadus morhua; Foss et al., 2006) and the interactive effects of ammonia and oxygen on the growth and physiology of juvenile Atlantic cod (Remen et al., 2008). Several additional studies have examined effects of anthropogenically induced stressors, mainly on glucose and lactate levels, but also other blood parameters, including blood gas and ion levels, Hct and Hb levels. The effects of confinement in rainbow trout (Wells and Pankhurst, 1999), as well as pre-slaughter stress and stress assessment in aquaculture facilities in Atlantic cod (Hultmann et al., 2012), have been examined. Surgical techniques and recovery have been examined, specifically focusing on hepatic portal vein cannulation technique in Atlantic salmon (Eliason et al., 2007). In addition, the effect of squeezing to simulate gill net damage in rainbow trout (Kojima et al., 2004) and stress associated with dam-related changes in river flow in mountain whitefish (Prosopium williamsoni; Taylor et al., 2012) have been assessed. Finally, the effects of various toxicants and pollutants on blood parameters have been examined in a cichlid species (Cichlasoma dimerus; Da Cuña et al., 2011), two salmonid species (Meland et al., 2010; Olsvik et al., 2010) and the round goby (Neogobius melanostomus; Marenetette et al., 2012).

The manipulation of teleost physiology is also of particular relevance to investigators interested in understanding the intrinsic principles of physiological processes, as well as the result of these manipulations on physiological processes. Point-of-care devices provide a means to examine such physiological end-points easily. Dey et al. (2010) examined the effect of altering cortisol and androgen levels on glucose levels during the parental care period of smallmouth bass. In addition, Herbert et al. (2002) measured glucose and lactate levels during strenuous exercise in 14 species of tropical reef fish. Laporte and Trushenski (2012) studied the effect of manipulating the composition of aquafeeds on glucose and/or lactate levels in hybrid striped bass. Turbot (Scophthalmus maximus) were used to determine the interaction effects of oxygen saturation on growth and blood physiology (Foss et al., 2007).

Overall, 10 POC devices have been used in applied studies to assess blood physiology parameters in teleost fish; however, not all devices have been validated for use in teleosts. The Accu-chek glucose meter and Lactate Pro were the most widely used POC devices, followed by the i-STAT, Freestyle blood glucose meter, Accutrend and Accusport lactate meters. The use of these POC devices in teleost fish across a wide range of applied studies demonstrates not only their usefulness in field and laboratory-based physiology, but also the need for further species-specific validation of these tools.

Reptiles

Validation studies

Two studies were conducted to validate the use of the i-STAT analyser for various blood parameters on reptiles (Table 2). McCain et al. (2010) concluded that whole-blood readings for Cl, glucose, K+ and Na+ using the i-STAT analyser in various reptiles were not accurate compared with laboratory measurements. Despite its variation from laboratory-based results, McCain et al. (2010) suggested that as a result of consistently biased values, the i-STAT could provide clinical utility if analyser-specific reference intervals were set. Wolf et al. (2008) compared the i-STAT analyser with four other analysers (two laboratory diagnostic methods and two table-top analysers) using whole blood from various sea turtle species [loggerhead turtles (Caretta caretta), green turtles (Chelonia mydas) and Kemp's ridley turtles (Lepidochelys kempii)] for Na+, K+, Cl, glucose, blood urea nitrogen (BUN) and Hct. In most cases, i-STAT readings disagreed with other analysers, except for BUN, which the authors proposed was a result of differences in the mechanisms used to measure the analytes. Given that the use of POC analysers has generated mixed results in reptiles in general, additional research to validate various POC devices in this group is warranted.

Application studies

Five studies have used POC devices to measure blood parameters, such as acid–base properties, in reptiles. The i-STAT analyser was the most frequently used device, with three studies using this tool to assess the health and wellbeing of various sea turtle species. Sea turtles are frequently encountered as bycatch in marine fisheries, and two studies assessed the physiological effects of different capture and handling techniques. Harms et al. (2003) examined the differential effects of trawl vs. pound net in loggerhead sea turtles and Innis et al. (2010) evaluated the physiological status and health of leatherback sea turtles directly captured by hoop net or incidentally entangled in fixed (i.e. stationary) fishing gears. Anderson et al. (2011) also measured blood parameters in green turtles that were cold stunned or hypothermic. In addition, bycatch-related blood physiology was assessed in freshwater fisheries using the Lactate Pro and IQ128 Elite pH meter to evaluate the physiological response to various types of bycatch-reduction devices, using painted turtles (Chrysemys picta; Larocque et al., 2012) as well as eastern musk (Sternotherus odoratus) and northern map turtles (Graptemys geographica; Stoot et al., 2013). Given the recent increase in research effort, the use of POC analysers is becoming a more common mode to evaluate stress and health in both marine and freshwater reptiles.

Birds

Validation studies

Based on our search criteria, only one study has validated the use of POC devices for avian species (Table 2). Lieske et al. (2002) used adult rhinoceros auklets (Cerorhinca monocerata) to assess the accuracy of four POC devices (Accu-chek Advantage, Bayer Glucometer Elite, Precision QID and Sure Step). Based on mean difference and regression models, all devices were deemed reliable and potentially useful for screening in the field, although the four hand-held devices underestimated blood glucose of rhinoceros auklets by an average of 33% compared with reference values (Lieske et al., 2002). Based on ease of use, comparative accuracy, test time, cost and blood volume requirement, the Accu-chek Advantage and Precision QID monitors were the most appropriate POC devices for this avian model, and future research is suggested with known hypoglycaemic avian blood as well as blood from different species to assess overall utility of the devices (Lieske et al., 2002).

Application

Two POC devices have been used in practical applications to measure glucose and numerous other physiological parameters in avian species. Researchers have used the Bayer Glucometer Elite device in the field and laboratory to assess the possible effect of nectar consumption on plasma glucose in various passerine species, including warblers (Cecere et al., 2011), and to determine whether plasma glucose levels were based on circadian rhythm or temperature (Downs et al., 2010). Although not validated for avian species, the i-STAT analyser has been used to analyse blood acid–base, ionic and haematological properties to provide reference data for non-anaesthetized Amazon parrots (Amazona aestiva; Paula et al., 2008).

Mammals

Validation

Our search discovered three studies that have assessed the accuracy of POC devices for use in non-domesticated mammals (Table 2). All but one validation study compared the i-STAT analyser with laboratory-based equipment to measure various blood parameters in three different mammalian species. The i-STAT analyser was determined to be acceptable for the measurement of glucose, BUN, Na+, K+ and total CO2 in cynomolgus macaques (Macaca fasicularis; Hopper and Cray, 2007) and glucose, BUN, Na+, K+, Cl and Hct in elephant seals (Mirounga angustirostris; Larsen et al., 2002). In addition, Burdick et al. (2012) compared laboratory-based equipment (Hitachi 917 chemistry analyser) with the IQ Prestige Smart System Handheld Glucometer and the Prestige Smart System Glucometer for measurement of blood glucose levels in juvenile white-tailed deer (Odocoileus virginianus). Agreement between laboratory-based equipment and the two POC glucometers was poor, thus driving the conclusion that these two POC devices were not appropriate for measurement of blood glucose concentrations in this species.

Applications

Two POC devices, the i-STAT analyser and Accutrend lactate meter, were used to assess blood physiology in various non-domesticated mammal species. Of the six application studies completed to date, all six used the i-STAT, with pH and blood gases being the most commonly measured variables. Application studies examined the physiological effects related to invasive capture techniques in white-tailed deer (Boesch et al., 2011), anaesthetics in polar bears (Ursus maritimus; Cattet et al., 2003), immobilization in Baird's tapirs (Tapirus bairdii; Feorster et al., 2000) and manual restraint as opposed to anaesthetic in the Arabian oryx (Oryx leucoryx; Kilgallon et al., 2008). Application studies also examined the physiological effects related to sleep apnoea in Northern elephant seals (Mirounga angustirostris; Stockard et al., 2007), as well as an assessment and post-release monitoring of mass-stranded dolphins (Sampson et al., 2012).

Limitations across taxonomic groups

General limitations

Of the devices used in this data set, two broad categories of POC devices can be designated: the widely applicable multi-analyte devices (e.g. i-STAT analyser) and the specialized single-analyte devices (e.g. Lactate Pro). The i-STAT analyser is beneficial in that it can be used to test a variety of analytes, but it requires a certain amount of user knowledge and training in order to operate the machine settings, to dispense the sample into the cartridge appropriately and to avoid cartridge errors. These devices require a working knowledge of the device as well as the physiology of the organism but are ideal for obtaining multiple physiological measures from a single sample. Conversely, single-analyte devices, such as the Lactate Pro, are more specialized in scope, function on a limited number of analytes and operate on the submitted blood sample without further input or setting configuration. These devices are typically small, easy to use, relatively inexpensive and ideal if only one blood variable measurement is required.

Physiological limitations

As a result of their origins in medical sciences, POC devices were designed to measure blood parameters of homeothermic mammals, particularly humans. These devices rely on individuals with a body temperature of ∼37°C and non-nucleated blood cells, thus the ability of POC devices to be applied to a broader variety of taxa will have challenges. Consequently, body temperature was a reoccurring caveat across studies of ectotherms using these devices, especially in relationship to temperature-sensitive blood acid–base measurements (Harrenstien et al., 2005; Gallagher et al., 2010; Sampson et al., 2012). Indeed, several studies concluded that there is a need for species-specific temperature corrections for these parameters and emphasized that extrapolation of published temperature corrections from one species to another should be done with caution [e.g. Chondrichthyes (Mandelman and Skomal, 2009; Cicia et al., 2012), teleost fish (Olsvik et al., 2010; Foss et al., 2012), reptiles (Harms et al., 2003; Anderson et al., 2011) and birds (Paula et al., 2008)].

Inaccurate readings can be the result of incorrect measurements. Many devices rely on pre-set ratios to calculate parameters and have species-specific correction values, which differ among species and taxa. For example, the i-STAT analyser was not used to measure base excess and saturated arterial oxygen in sea turtles due to its use of human-specific conversion factors (Harms et al., 2003). Along the same lines, the internal temperature calibration capability for pH and blood gases on the i-STAT analyser is based on mammalian conversion factors, and may thus compromise accuracy of values of those parameters when the conversion tool is employed for ectotherms, such as fish (Mandelman and Skomal, 2009). Glucose monitors have similar issues, because they are designed to measure whole-blood samples but use a correction factor to convert results to plasma glucose concentrations (Kuwa et al., 2001). These devices use human plasma-to-whole-blood corrective values, which can underestimate glucose values in birds (Lieske et al., 2002; Acierno et al., 2008). In addition, this trend for underestimation is also seen in POC lactate measurements in teleost fish (e.g. Wells and Pankhurst, 1999; Venn Beecham et al., 2006).

Whole blood vs. plasma and point-of-care value range restrictions

The input medium is important to consider when using POC devices, where whole blood and plasma are the two most prevalent media used. Whole blood is unmodified (with the potential exception of the addition of an anticoagulant) and is therefore ideal for field studies where processing and storage may be difficult or impossible. Plasma is extracellular fluid retrieved by spinning down whole blood by centrifugation to remove haematocytes. Plasma is often the preferred medium for laboratory studies owing to its higher stability for storage compared with whole blood (Thrall et al., 2012); however, the need for centrifugation can limit feasibility in the field. Although urine may be analysed by POC devices for some analytes, it is not as widely used. For example, urine cannot be tested reliably using the i-STAT analyser (Erickson and Wilding, 1993). Serum can also be used as an input medium, but it has certain advantages and disadvantages similar to plasma (Thrall et al., 2012).

In the studies investigated here, the vast majority assessed whole blood when using a POC device, while some used plasma, particularly those in controlled environments where plasma was often stored and analysed at a later date. Validation studies that measured the difference between whole blood and plasma analyte levels found that the analyte value differed significantly but in a predictable manner, with plasma values typically being higher (Iwama et al., 1995). The persistent differences between plasma- and whole-blood-derived values allow for relative but not direct comparisons, which limits inference across studies (Larsen et al., 2002; Cooke et al., 2008).

As these devices are designed for human blood parameter ranges, their tolerances can often be too restrictive for other taxa and result in error readings [e.g. Chondrichthyes (Awruch et al., 2011; Hyatt et al., 2012; Naples et al., 2012), teleost fish (Harrenstien et al., 2005; Brown et al., 2008), reptiles (Larocque et al., 2012) and birds (Lieske et al., 2002); Fig. 1). For example, many studies that used the i-STAT analyser to assess blood physiology in teleost fish and Chondrichthyes have reported out-of-range readings for various parameters, including Na+ (Olsvik et al., 2007; Suski et al., 2007; Brill et al., 2008) and Cl (Harrenstien et al., 2005; Brill et al., 2008; DiMaggio et al., 2010). In situations when limits are too narrow, dilutions can be used to obtain measurable readings (Suski et al., 2007; Brill et al., 2008); however, this can only be achieved with plasma, creating a problem for any cartridge type (e.g. the EC8+ on the i-STAT) on a multi-analyte device that includes both out-of-range analytes as well as those specific to whole blood for a given species (e.g. certain acid–base and haemotogical parameters). In such instances, the user is unable to obtain value readings for all analytes for that cartridge and must prioritize whether to run the cartridge on whole blood or on extracted and diluted plasma, depending on which analyte(s) is less valuable to lose.

Figure 1:

Whole blood values for select analytes on representative commonly studied species, the rainbow trout (Oncorhynchus mykiss) and the painted turtle (Chrysemys picta). Box plots represent the maximal ranges from the literature and horizontal lines represent the maximal reportable range of the most commonly used point-of-care device in the present study, the i-STAT analyser.

Figure 1:

Whole blood values for select analytes on representative commonly studied species, the rainbow trout (Oncorhynchus mykiss) and the painted turtle (Chrysemys picta). Box plots represent the maximal ranges from the literature and horizontal lines represent the maximal reportable range of the most commonly used point-of-care device in the present study, the i-STAT analyser.

Field and environmental limitations

When conducting fieldwork, researchers may encounter several different environmental conditions that have the potential to interfere with POC device use (Fig. 2). Waterproofing becomes necessary when working with species in aquatic settings to protect devices from potential water damage. Small amounts of water (especially saltwater) within cartridge ports and battery compartments of POC devices can compromise the condition of the unit and damage it. Waterproof cases protect devices from water and general damage during transport, although depending on case size, portability can be reduced. In addition, these cases protect the device only while in transit, and care must be taken during device use to avoid potential submersion. Future steps to develop POC devices that are waterproof and more durable would reduce the need for bulky cases.

Figure 2:

Point-of-care (POC) devices can be used in the field in a variety of situations. (A) Point-of-care glucose meter being set up on a boat (photograph by Lisa Thompson). (B) Protective cases, similar to the one shown, are useful for ensuring that POC devices are not damaged by the elements (photograph by Lisa Thompson). (C) Point-of-care devices, such as this glucose meter, can be used in laboratory trials to obtain immediate results on the condition of the individual (photograph by Petra Szekeres). (D) Some POC devices, such as the i-STAT, can obtain multiple blood parameters to be measured from one sample (photograph by John Mandelman). (E) Point-of-care i-STAT device in use on a boat (photograph by John Mandelman). (F) Point-of-care pH meter in use to examine blood pH in freshwater turtles (photograph by Sarah Larocque).

Figure 2:

Point-of-care (POC) devices can be used in the field in a variety of situations. (A) Point-of-care glucose meter being set up on a boat (photograph by Lisa Thompson). (B) Protective cases, similar to the one shown, are useful for ensuring that POC devices are not damaged by the elements (photograph by Lisa Thompson). (C) Point-of-care devices, such as this glucose meter, can be used in laboratory trials to obtain immediate results on the condition of the individual (photograph by Petra Szekeres). (D) Some POC devices, such as the i-STAT, can obtain multiple blood parameters to be measured from one sample (photograph by John Mandelman). (E) Point-of-care i-STAT device in use on a boat (photograph by John Mandelman). (F) Point-of-care pH meter in use to examine blood pH in freshwater turtles (photograph by Sarah Larocque).

The effects of temperature and atmospheric humidity on the usability and accuracy of POC devices are further potential issues when working in the field. Studies conducted on the use of POC devices in disaster-relief situations have concluded that temperature and humidity can affect glucose test strips, which alters the readings of various glucose monitors (Louie et al., 2000; Nichols, 2011). Many POC devices and their associated cartridges have environmental range limits in which they function optimally, and deviations outside of this range can produce inaccurate readings (Sampson et al., 2012). Functional minima and maxima (e.g. i-STAT analyser has a functional range of 16–30°C; Lactate Pro cannot function properly above 40°C) limit the possible field season in some climates and preclude sampling altogether in some areas (e.g. polar and desert regions). Users are often forced to carry a cooling or heating mechanism to ensure that the POC device is kept within the usable thermal range. In addition, many POC devices use a cartridge or strip that requires storage at specific temperatures (e.g. i-STAT cartridges require refrigeration before use and can be kept at room temperature for only 2 weeks following removal). Furthermore, these devices are affected by extreme humidity conditions, such that most devices operate between 10 and 90% relative humidity (e.g. Lactate Pro and i-STAT operate in the range 20–80 and 0–90% relative humidity, respectively). Overall, field settings can make storage and maintenance of POC devices in varying temperatures and humidities difficult. As such, modifications of POC devices to incorporate a broader thermal and humidity tolerance is needed before these devices can be considered fully effective for studies of species inhabiting a wide range of environments.

Conclusions and future directions

Overall, most POC devices have been found to be suitable alternatives to traditional laboratory-based devices in conservation physiology studies, although they should be used with caution. With continuing technological developments, such devices have the potential to be used more widely in field physiology studies on a variety of taxa. However, the popularity of such devices will depend on technological advances in the usability and reliability of POC devices in the field. Environmental conditions (e.g. temperature and humidity) affect the usability and accuracy of POC devices; as such, POC devices need to be functional broadly in field environments and require improvements or modifications to overcome their functional limitations (temperature range, humidity, storage requirements, maintenance etc.). Technological advances will increase the applicability of POC devices to a variety of species living in different field conditions or in wide demographic ranges. This will ensure that extreme or fluctuating environmental field conditions do not interfere with the use of POC devices by damaging the devices or affecting the accuracy of the results. Partnerships and collaborations between field biologists and manufacturing companies can help to formulate such technological improvements.

In addition to technological advancements of POC devices, there is an increased need for validation studies on non-human and non-domesticated species to confirm the accuracy and reliability of these devices, particularly given the lack of universality in the calibrations of POC devices among species evaluated to date. Therefore, precise calibration and species-specific validation of POC devices are necessary prior to application in a broader range of species (Lieske et al., 2002; DiMaggio et al., 2010; Gallagher et al., 2010). Validation studies should address taxonomic and thermal effects on device precision and accuracy (Cicia et al., 2012). In particular, efforts should be made to garner larger sample sizes to compare with current reference values (Naples et al., 2012). Optimally, a calibration can be established across the broadest possible range of values for a given analyte, in the event of a lack of equivalence or linearity across the full spectrum of readable or biologically/clinically relevant values. Furthermore, biases can occur among taxa, where validation studies tend to be carried out in species or groups that are easy to study or are of economic importance (e.g. Atlantic salmon). The diversity among taxa in terms of habitat ecology and blood physiology points to the need for further investigation into a broader range of organisms, especially non-mammalian taxa. Focusing on representative models within each taxa, validating commonly used devices and assessing blood parameters in natural, free-living animals would be a good starting point. Validations of these devices on ectothermic species should be of high importance due to their physiological differences from endothermic species. In addition, developing a standardized protocol to validate devices, within the taxon level, would be beneficial and aid with the standardization of validations.

With the growing use of POC devices in field-based conservation physiology studies, there is a push towards the streamlined approach that is provided by multi-analyte devices (e.g. i-STAT). The ability to measure multiple blood parameters from a single sample by a single device is ideal for field-based studies, where extensive sample analysis is often difficult. Currently, the majority of the POC devices (e.g. LactatePro and various glucometers) measure one parameter exclusively, which can not only increase the equipment load for field biologists but also the amount of sample required. The development of more multi-analyte devices that are able to measure multiple blood parameters efficiently and accurately across a variety of taxa will increase the use of these devices by field physiologists.

In addition to the current POC devices available, there is the potential to develop devices that could measure blood parameters beyond those that are currently possible, again allowing conservation physiologists the flexibility of on-site sample analysis. Point-of-care devices that would enable direct measurement of primary in addition to secondary stress analytes would allow remote determination of levels now attainable only via more time-consuming processes in the laboratory. The ability to obtain POC measurements of glucocorticoids or other steroids (such as reproductive hormones), among other biomarkers, would be highly valuable for field-based conservation physiology studies.

In conclusion, the use of hand-held and portable POC devices is appealing for field-based conservation physiology studies because they rapidly provide on-site results without the need for sample storage. Overall, there is great potential for the use of POC devices to advance the field of conservation physiology, but continued progress is needed in the areas discussed to increase both the utility of these devices across environments and taxonomic groups and their capacity to obtain additional information on stress levels and health of animals in remote settings. Also needed is a more thorough appreciation of the various limitations associated with POC devices and recognition that although they provide rapid information, they do not replace traditional analytical methods.

Acknowledgements

S.J.C. is supported by the Canada Research Chairs Program and the Natural Sciences and Engineering Research Council of Canada. We thank Nick Lapointe, Jon Midwood and two anonymous referees for providing comments on an earlier version of this manuscript.

References

1
Acierno
MJ
Johnson
ME
Eddleman
LA
Mitchell
MA
(
2008
)
Measuring statistical agreement between four point of care (POC) lactate meters and a laboratory blood analyzer in cats
.
J Feline Med Surg
 
10
:
110
114
.
2
Allen
SE
Holm
JL
(
2008
)
Lactate: physiology and clinical utility
.
J Vet Emerg Crit Care
 
18
:
123
132
.
3
Allender
MC
Schumacher
J
George
R
Milam
J
Odoi
A
(
2010
)
The effects of short- and long-term hypoxia on hemolymph gas values in the American horseshow crab (Limulus polyphemus) using a point-of-care analyzer
.
J Zoo Wildl Med
 
41
:
193
200
.
4
Altinier
S
Zaninotto
M
Mion
M
Carraro
P
Rocco
S
Tosato
F
Plebani
M
(
2001
)
Point-of-care testing of cariac markers: results from an experience in an emergency department
.
Clin Chim Acta
 
311
:
67
72
.
5
Anderson
ET
Harms
CA
Stringer
EM
Cluse
WM
(
2011
)
Evaluation of hematology and serum biochemistry of cold-stunned green sea turtles (Chelonia mydas) in North Carolina, USA
.
J Zoo Wildl Med
 
42
:
247
255
.
6
Apple
FS
Anderson
FP
Collinson
P
Jesse
RL
Kontos
MC
Levitt
MA
Miller
EA
Murakami
MM
(
2000
)
Clinical evaluation of the first medical whole blood, point-of-care testing device for detection of myocardial infarction
.
Clin Chem
 
46
:
1604
1609
.
7
Archer
RK
Jeffcott
LB
(
1977
)
Comparative Clinical Haematology
.
Blackwell Scientific Publications
,
London
, pp
737
.
8
Arlinghaus
R
Klefoth
T
Cooke
SJ
Gingerich
A
Suski
CD
(
2009
)
Physiological and behavioural consequences of catch-and-release angling on northern pike (Esox lucius L.)
.
Fish Res
 
97
:
223
233
.
9
Atkins
A
Jacobson
E
Hernandez
J
Bolten
AB
Lu
X
(
2010
)
Use of a portable point-of-care (Vetscan Vs2) biochemical analyzer for measuring plasma biochemical levels in free-living loggerhead sea turtles (Caretta caretta)
.
J Zoo Wildl Med
 
41
:
585
593
.
10
Awruch
CA
Simpfendorfer
C
Pankhurst
NW
(
2011
)
Evaluation and use of a portable field kit for measuring whole-blood lactate in sharks
.
Mar Freshwater Res
 
62
:
694
699
.
11
Beadle
LC
(
1957
)
Respiration in the African swamp-worm, Alma emini Mich
.
J Exp Biol
 
34
:
1
10
.
12
Bjørlykke
GA
Roth
B
Sørheim
O
Kvammeb
BO
Slinde
E
(
2011
)
The effects of carbon monoxide on Atlantic salmon (Salmo salar L.)
.
Food Chem
 
127
:
1706
1711
.
13
Bjørn
PA
Finstad
B
Kristoffersen
R
(
2001
)
Salmon lice infection of wild sea trout and Arctic char in marine and freshwaters: the effects of salmon farms
.
Aquacult Res
 
32
:
947
962
.
14
Boesch
JM
Boulanger
JR
Curtis
PD
Erb
HN
Ludders
JW
Kraus
MS
Gleed
RD
(
2011
)
Biochemical variables in free-ranging white-tailed deer (Odocoileus virginianus) after chemical immobilization in clover traps or via ground-darting
.
J Zoo Wildl Med
 
42
:
18
28
.
15
Bosworth
BG
Small
BC
Gregory
D
Kim
J
Black
S
Jerrett
A
(
2007
)
Effects of rested-harvest using the anesthetic AQUI-S™ on channel catfish, Ictalurus punctatus, physiology and fillet quality
.
J World Aquac Soc
 
30
:
276
284
.
16
Bowzer
JC
Trushenski
JT
Gause
BR
Bowker
JD
(
2012
)
Efficacy and physiological responses of grass carp to different sedation techniques: II. Effect of pulsed DC electricity voltage and exposure time on sedation and blood chemistry
.
N Am J Aquacult
 
74
:
567
574
.
17
Breau
C
Cunjak
RA
Peake
SJ
(
2011
)
Behaviour during elevated water temperature: can physiology explain movement of juvenile Atlantic salmon to cool water?
J Anim Ecol
 
80
:
844
853
.
18
Brill
R
Bushnell
P
Schroff
S
Seifert
R
Galvin
M
(
2008
)
Effects of anaerobic exercise accompanying catch-and-release fishing on blood-oxygen affinity of the sandbar shark (Carcharhinus plumbeus, Nardo)
.
J Exp Mar Biol Ecol
 
354
:
132
143
.
19
Brooks
EJ
Sloman
KA
Liss
S
Hassan-Hassanein
L
Danylchuk
AJ
Cooke
SJ
Mandelman
JW
Skomal
GB
Sims
DW
Suski
CD
(
2011
)
The stress physiology of extended duration tonic immobility in the juvenile lemon shark, Negaprion brevirostris (Poey 1868)
.
J Exp Mar Biol Ecol
 
409
:
351
360
.
20
Brown
JA
Watson
J
Bourhill
A
Wall
T
(
2008
)
Evaluation and use of the Lactate Pro, a portable lactate meter, in monitoring the physiological well-being of farmed Atlantic cod (Gadus morhua)
.
Aquaculture
 
285
:
135
140
.
21
Burdick
S
Mitchell
MA
Neil
J
Heggem
B
Whittington
J
Acierno
MJ
(
2012
)
Evaluation of two point-of-care meters and a portable chemistry analyzer for measurement of blood glucose concentrations in juvenile white-tailed deer (Odocoileus virginianus)
.
J Am Vet Med Assoc
 
240
:
596
599
.
22
Busch
DS
Hayward
LS
(
2009
)
Stress in a conservation context: a discussion of glucocorticoid actions and how levels change with conservation-relevant variables
.
Biol Conserv
 
142
:
2844
2853
.
23
Butcher
PA
Leland
JC
Broadhurst
MK
Paterson
BD
Mayer
DG
(
2012
)
Giant mud crab (Scylla serrata): relative efficiencies of common baited traps and impacts on discards
.
ICES J Mar Sci
 
69
:
1511
1522
.
24
Cattet
MRL
Caulkett
NA
Lunn
NJ
(
2003
)
Anesthesia of polar bears using xylazine-zolazepam-tiletamine or zolazepam-tiletamine
.
J Wildl Dis
 
39
:
655
664
.
25
Cecere
JG
Spina
F
Jenni-Eiermann
S
Boitani
L
(
2011
)
Nectar: an energy drink used by European songbirds during spring migration
.
J Ornithol
 
152
:
923
931
.
26
Cicia
AM
Schlenker
LS
Sulikowski
JA
Mandelman
JW
(
2012
)
Seasonal variations in the physiological stress responses to discrete bouts of aerial exposure in the little skate, Leucoraja erinacea
.
Comp Biochem Physiol A Mol Integr Physiol
 
162
:
130
138
.
27
Cima
M
(
2011
)
Microsystems technologies for medical applications
.
Annu Rev Chem Biomol Eng
 
2
:
355
378
.
28
Clark
TD
Eliason
EJ
Sandblom
E
Hinch
SG
Farrell
AP
(
2008
)
Calibration of a hand-held haemoglobin analyser for use on fish blood
.
J Fish Biol
 
73
:
2587
2595
.
29
Clark
TD
Donaldson
MR
Drenner
SM
Hinch
SG
Patterson
DA
Hills
J
Ives
V
Carter
JJ
Cooke
SJ
Farrell
AP
(
2011
)
The efficacy of field techniques for obtaining and storing blood samples from fishes
.
J Fish Biol
 
79
:
1322
1333
.
30
Cooke
SJ
O'Connor
CM
(
2010
)
Making conservation physiology relevant to policy makers and conservation practitioners
.
Conserv Lett
 
3
:
159
166
.
31
Cooke
SJ
Crossin
GT
Patterson
DA
English
KK
Hinch
SG
Young
JL
Alexander
RF
Healey
MC
Van Der Kraak
G
Farrell
AP
(
2005
)
Coupling non-invasive physiological assessments with telemetry to understand inter-individual variation in behaviour and survivorship of sockeye salmon: development and validation of a technique
.
J Fish Biol
 
67
:
1342
1358
.
32
Cooke
SJ
Suski
CD
Danylchuk
SE
Danylchuk
AJ
Donaldson
MR
Pullen
C
Bulté
G
O'Toole
A
Murchie
KJ
Koppelman
JB
et al
(
2008
)
Effects of different capture techniques on the physiological condition of bonefish Albula vulpes evaluated using field diagnostic tools
.
J Fish Biol
 
73
:
1351
1375
.
33
Cooke
SJ
Sack
L
Franklin
CE
Farrell
AP
Beardall
J
Wikelski
M
Chown
SL
(
2013
)
Conservation physiology: perspectives on an increasingly integrated and essential science
.
Conserv Physiol
 
1
: .
34
Costa
DP
Sinervo
B
(
2004
)
Field physiology: physiological insights from animals in nature
.
Annu Rev Physiol
 
66
:
209
238
.
35
Da Cuña
RH
Rey Vázquez
G
Piol
MN
Guerrero
NV
Maggese
MC
Lo Nostro
FL
(
2011
)
Assessment of the acute toxicity of the organochloride pesticide endosulfan in Cichlasoma dimerus (Teleostei, Perciformes)
.
Ecotoxicol Environ Saf
 
74
:
1065
1073
.
36
Deem
SL
Karesh
WB
Weisman
W
(
2001
)
Putting theory into practice: wildlife health in conservation
.
Conserv Biol
 
15
:
1224
1233
.
37
Delesalle
C
Dewulf
J
Lefebvre
RA
(
2007
)
Determination of Lactate concentration in blood plasma and peritoneal fluid in horses with colic by an Accusport analyzer
.
J Vet Intern Med
 
21
:
293
301
.
38
Denver
RJ
Hopkins
PM
McCormick
SD
Propper
CR
Riddiford
L
Sower
SA
Wingfield
JC
(
2009
)
Comparative endocrinology in the 21st century
.
Integr Comp Biol
 
49
:
339
348
.
39
Dey
CJ
O'Connor
CM
Gilmour
KM
Van Der Kraak
G
Cooke
SJ
(
2010
)
Behavioral and physiological responses of a wild teleost fish to cortisol and androgen manipulation during parental care
.
Hormones Behav
 
58
:
599
605
.
40
DiMaggio
MA
Ohs
CL
Petty
BD
(
2010
)
Evaluation of a point-of-care-blood analyzer for use in determination of select hematological indices in the Seminole killifish
.
N Am J Aquacult
 
72
:
261
268
.
41
di Prisco
G
(
1997
)
Physiological and biochemical adaptations in fish to a cold marine environment
. In
Battaglia
B
Valencia
J
Walton
DWH
, eds,
Antarctic Communities: Species, Structure and Survival. 6th SCAR Biology Symposium, Venice, Italy, 1996
 .
Cambridge University Press
,
Cambridge
, pp
251
260
.
42
Downs
CT
Wellmann
AE
Brown
M
(
2010
)
Diel variations in plasma glucose concentrations of Malachite Sunbirds Nectarinia famosa
.
J Ornithol
 
151
:
235
239
.
43
Eliason
EJ
Kiessling
A
Karlsson
A
Djordjevic
B
Farrell
AP
(
2007
)
Validation of the hepatic portal vein cannulation techniques using Atlantic salmon Salmo salar L
.
J Fish Biol
 
71
:
290
297
.
44
Erickson
AW
Youatt
WG
(
1961
)
Seasonal variations in the hematology and physiology of black bears
.
J Mammal
 
42
:
198
203
.
45
Erickson
KA
Wilding
P
(
1993
)
Evaluation of a novel point-of-care system, the i-STAT portable clinical analyzer
.
Clin Chem
 
39
:
283
287
.
46
Evans
JJ
Shoemaker
CA
Klesius
PH
(
2003
)
Effects of sublethal dissolved oxygen stress on blood glucose and susceptibility to Streptococcus agalactiae in Nile Tilapia
.
J Aquat Anim Health
 
15
:
202
208
.
47
Feder
ME
Block
BA
(
1991
)
On the future of animal physiological ecology
.
Funct Ecol
 
5
:
136
144
.
48
Feorster
SH
Bailey
JE
Aguilar
R
Loria
DL
Foerster
CR
(
2000
)
Butorphanol/xylazine/ketamine immobilization of free-ranging Baird's tapirs in Costa Rica
.
J Wildl Dis
 
36
:
335
341
.
49
Foss
A
Kristensen
T
Åtland
Å
Hustveit
H
Hovland
H
Øfsti
A
Imsland
AK
(
2006
)
Effects of water reuse and stocking density on water quality, blood physiology and growth rate of juvenile cod (Gadus morhua)
.
Aquaculture
 
256
:
255
263
.
50
Foss
A
Imsland
AK
Roth
B
Schram
E
Stefansson
SO
(
2007
)
Interactive effects of oxygen saturation and ammonia on growth and blood physiology in juvenile turbot
.
Aquaculture
 
271
:
244
251
.
51
Foss
A
Grimsbø
E
Vikingstad
E
Nortvedt
R
Slinde
E
Roth
B
(
2012
)
Live chilling of Atlantic salmon: physiological response to handling and temperature decrease on welfare
.
Fish Physiol Biochem
 
38
:
656
571
.
52
Frick
LH
Walker
TI
Reina
RD
(
2012
)
Immediate and delayed effects of gill-net capture on acid–base balance and intramuscular lactate concentration of gummy sharks, Mustelus antarcticus
.
Comp Biochem Physiol A Mol Integr Physiol
 
162
:
88
93
.
53
Gallagher
AJ
Frick
LH
Bushnell
PG
Brill
RW
Mandelman
JW
(
2010
)
Blood gas, oxygen saturation, pH, and lactate values in Elasmobranch blood measured with a commercially available portable clinical analyzer and standard laboratory instruments
.
J Aquat Anim Health
 
22
:
229
234
.
54
Garland
T
Jr
Adolph
SC
(
1991
)
Physiological differentiation of vertebrate populations
.
Ann Rev Ecol Syst
 
22
:
193
228
.
55
Garland
T
Jr
Carter
PA
(
1994
)
Evolutionary physiology
.
Annu Rev Physiol
 
56
:
579
621
.
56
Gomes
LC
Chagas
EC
Brinn
RP
Roubach
R
Coppati
CE
Baldisserotto
B
(
2006a
)
Use of salt during transportation of air breathing pirarucu juveniles (Arapaima gigas) in plastic bags
.
Aquaculture
 
256
:
521
528
.
57
Gomes
LC
Chagas
EC
Martin-Junior
H
Roubach
R
Ono
EA
Lourenço
JNP
(
2006b
)
Cage culture of tambaqui (Colossoma macropomum) in a central Amazon floodplain lake
.
Aquaculture
 
253
:
374
384
.
58
Gravel
MA
Cooke
SJ
(
2008
)
Severity of barotrauma influences the physiological stats, postrelease behaviour, and fate of tournament-caught smallmouth bass
.
N Am J Fish Manag
 
28
:
607
617
.
59
Gubala
V
Harris
LF
Ricco
AJ
Tan
MX
Williams
DE
(
2012
)
Point of care diagnostics: status and future
.
Anal Chem
 
84
:
487
515
.
60
Hall
FG
Dill
DB
Guzman Barron
ES
(
1936
)
Comparative physiology in high altitudes
.
J Cell Comp Physiol
 
8
:
301
313
.
61
Hanson
KC
Gravel
M-A
Redpath
T
Cooke
SJ
Seipker
MJ
(
2008
)
Latitudinal variation in physiological and behavioral responses of nest-guarding smallmouth bass to common recreational angling practices
.
Trans Am Fish Soc
 
137
:
1558
1566
.
62
Harms
CA
Mallo
KM
Ross
PM
Segars
A
(
2003
)
Venous blood gases and lactates of wild loggerhead sea turtles (Caretta caratta) following two capture techniques
.
J Wildl Dis
 
39
:
366
374
.
63
Harrenstien
LA
Tornquist
SJ
Miller-Morgan
TJ
Fodness
BG
Clifford
KE
(
2005
)
Evaluation of a point-of-care blood analyzer and determination of reference ranges for blood parameters in rockfish
.
J Am Vet Med Assoc
 
226
:
255
265
.
64
Helmuth
B
(
2009
)
From cells to coastlines: how can we use physiology to forecast the impacts of climate change?
J Exp Biol
 
212
:
753
760
.
65
Henry
NA
Cooke
SJ
Hanson
KC
(
2009
)
Evaluation of a point-of-care blood analyzer and determination of reference ranges for blood parameters in rockfish
.
Fish Res
 
100
:
178
182
.
66
Herbert
NA
Wells
RMG
Baldwin
J
(
2002
)
Correlates of choroid rete development with the metabolic potential of various tropical reef fish and the effect of strenuous exercise on visual performance
.
J Exp Mar Biol Ecol
 
275
:
31
46
.
67
Hollis
AR
Dallap Schaer
BL
Boston
RC
Wilkins
PA
(
2008
)
Comparison of the Accu-Chek Aviva point-of-care glucometer with blood gas and laboratory methods of analysis of glucose measurements in equine emergency patients
.
J Vet Int Med
 
22
:
1189
1195
.
68
Hopper
KJ
Cray
C
(
2007
)
Evaluation of a portable clinical analyzer in cynomolgus macaques (Macaca fasicularis)
.
J Am Assoc Lab Ani Sci
 
46
:
53
57
.
69
Hultmann
L
Phu
TM
Tobiassen
T
Aus-Hansen
Ø
Rustad
T
(
2012
)
Effects of pre-slaughter stress on proteolytic enzyme activities and muscle quality of farmed Atlantic cod (Gadus morhua)
.
Food Chem
 
134
:
1399
1408
.
70
Hyatt
MW
Anderson
PA
O'Donnell
PM
Berzins
IK
(
2012
)
Assessment of acid–base derangements among bonnethead (Sphyrna tiburo), bull (Carcharhinus leucas), and lemon (Negaprion brevirostris) sharks from gillnets and longline capture and handling methods
.
Comp Biochem Physiol A Mol Integr Physiol
 
162
:
113
120
.
71
Innis
C
Merigo
C
Dodge
K
Tlusty
M
Dodge
M
Sharp
B
Myers
A
McIntosh
A
Wunn
D
Perkins
C
et al
(
2010
)
Health evaluation of leatherback turtles (Dermochelys coriacea) in the northwest Atlantic during first capture and fisheries gear disentanglement
.
Chelonian Conserv Biol
 
9
:
205
222
.
72
Iwama
GK
Morgan
JD
Barton
BA
(
1995
)
Simple field methods for monitoring stress and general condition of fish
.
Aquacult Res
 
26
:
273
282
.
73
Kilgallon
C
Bailey
T
Arca-Ruibal
B
Misheff
M
O'Donovan
D
(
2008
)
Blood-gas and acid-base parameters in nontranquilized Arabian Oryx (Oryx leucoryx) in the United Arab Erimates
.
J Zoo Wildl Med
 
39
:
6
12
.
74
Klonoff
DC
(
2005
)
Continuous glucose monitoring: roadmap for 21st century diabetes therapy
.
Diabetes Care
 
28
:
1231
1239
.
75
Kojima
T
Ishii
M
Kobayashi
M
Shimizu
M
(
2004
)
Blood parameters and electrocardiogram in squeezed fish simulating the effect of net damage and recovery
.
Fish Sci
 
70
:
860
866
.
76
Ku
DN
(
1997
)
Blood flow in arteries
.
Annu Rev Fluid Mech
 
29
:
399
434
.
77
Kuwa
K
Nakayama
T
Hoshino
T
Tominaga
M
(
2001
)
Relationships of glucose concentrations in capillary whole blood, venous whole blood and venous plasma
.
Clin Chim Acta
 
307
:
187
192
.
78
Landsman
SJ
Wachelkab
HJ
Suski
CD
Cooke
SJ
(
2011
)
Evaluation of the physiology, behaviour, and survival of adult muskellunge (Esox masquinongy) captured and released by specialized anglers
.
Fish Res
 
110
:
377
386
.
79
Laporte
J
Trushenski
JT
(
2012
)
Production performance, stress tolerance and intestinal integrity of sunshine bass fed increasing levels of soybean meal
.
J Anim Physiol Anim Nutr
 
96
:
513
526
.
80
Larocque
SM
Cooke
SJ
Blouin-Demers
G
(
2012
)
A breath of fresh air: avoiding anoxia and mortality of freshwater turtles in fyke nets by the use of floats
.
Aquat Conserv
 
22
:
198
205
.
81
Larsen
RS
Haulena
M
Grindem
CB
Gulland
FMD
(
2002
)
Blood values of juvenile northern elephant seals (Mirounga angustirostris) obtained using a portable clinical analyzer
.
Vet Clin Path
 
31
:
106
110
.
82
Lieske
CL
Ziccardi
MH
Mazet
JAK
Newman
SH
Gardner
IA
(
2002
)
Evaluation of 4 handheld blood glucose monitors for use in seabird rehabilitation
.
J Avian Med Surg
 
164
:
277
285
.
83
Louie
RF
Tang
Z
Shelby
DG
Kost
GJ
(
2000
)
Point-of-care testing: millennium technology for critical care
.
Lab Med
 
31
:
402
408
.
84
McCain
SL
Flatland
B
Schumacher
JP
Clarke
EO
III
Fry
MM
(
2010
)
Comparison of chemistry between 2 portable, commercially available analyzers and a conventional laboratory analyzer in reptiles
.
Vet Clin Path
 
39
:
474
479
.
85
Mandelman
JW
Farrington
MA
(
2007a
)
The estimated short-term discard mortality of a trawled elasmobranch, the spiny dogfish (Squalus acanthias)
.
Fish Res
 
83
:
238
245
.
86
Mandelman
JW
Farrington
MA
(
2007b
)
The physiological status and mortality associated with otter-trawl capture, transport, and captivity of an exploited elasmobranch
,
Squalus acanthias. ICES J Marine Sci
 
64
:
122
130
.
87
Mandelman
JW
Skomal
GB
(
2009
)
Differential sensitivity to capture stress assess by blood acid–base status in five carcharhinid sharks
.
J Comp Physiol B
 
179
:
267
277
.
88
Mangum
CP
Hochachka
PW
(
1998
)
New directions in comparative physiology and biochemistry: mechanisms, adaptations, and evolution
.
Physiol Biochem Zool
 
71
:
471
484
.
89
Marenetette
JR
Tong
S
Balshine
S
(
2012
)
The cortisol stress response in male round goby (Neogobius melanostomus): effects of living in polluted environments
.
Environ Biol Fish
 
96
:
723
733
.
90
Mecozzi
DM
Brock
K
Tran
NK
Hale
KN
Kost
GJ
(
2010
)
Evidence-based point-of-care device design for emergency and disaster care
.
Point Care
 
9
:
65
69
.
91
Meffe
GK
(
1999
)
Conservation medicine
.
Conserv Biol
 
13
:
953
954
.
92
Meland
S
Heier
LS
Salbu
B
Tollefsen
KE
Farmen
E
Rosseland
BO
(
2010
)
Exposure of brown trout (Salmo trutta L.) to tunnel wash water runoff — chemical characterisation and biological impact
.
Sci Total Environ
 
408
:
2646
2656
.
93
Mizock
BA
Falk
JL
(
1992
)
Lactic acidosis in critical illness
.
Crit Care Med
 
20
:
80
93
.
94
Moran
D
Wells
RMG
Pether
SJ
(
2008
)
Low stress response exhibited by juvenile yellowtail kingfish (Seriola lalandi Valenciennes) exposed to hypercapnic conditions associated with transportation
.
Aquacult Res
 
39
:
1399
1407
.
95
Morgan
JD
Iwama
GK
(
1997
)
Measurements of stressed states in the field
. In
Iwama
G
Pickering
A
Sumpter
J
Schreck
C
, eds,
Fish Stress and Health in Aquaculture
 .
Cambridge University Press
,
New York
, pp
247
268
.
96
Murchie
KJ
Danylchuk
SE
Pullen
CE
Brooks
E
Shultz
AD
Suski
CD
Danylchuk
AJ
Cooke
SJ
(
2009
)
Strategies for the capture and transport of bonefish, Albula vulpes, from tidal creeks to a marine research laboratory for long-term holding
.
Aquacult Res
 
40
:
1538
1550
.
97
Naples
LM
Mylniczenko
ND
Zuchariah
TT
Wilborn
RE
Young
FA
(
2012
)
Evaluation of critical care blood analytes assessed with a point-of-care portable blood analyzer in wild and aquarium-housed elasmobranchs and the influence of phlebotomy site on results
.
J Am Vet Med Assoc
 
241
:
117
125
.
98
Nguyen
V
Gravel
M-A
Mapleston
A
Hanson
KC
Cooke
SJ
(
2009
)
The post-release behaviour and fate of tournament-caught smallmouth bass after ‘fizzing’ to alleviate distended swim bladders
.
Fish Res
 
96
:
313
318
.
99
Nichols
JH
(
2011
)
Blood glucose testing in the hospital: error sources and risk management
.
J Diabetes Sci Techol
 
5
:
173
177
.
100
Olsvik
PA
Lie
KK
Hevrøy
EM
(
2007
)
Do anesthetics and sampling strategies affect transcription analysis of fish tissues?
BMC Mol Biol 8: 48
 .
101
Olsvik
PA
Kroglund
F
Finstad
B
Kristensen
T
(
2010
)
Effects of the fungicide azoxystrobin on Atlantic salmon (Salmo salar L.) smolt
.
Ecotoxicol Environ Saf
 
73
:
1852
1861
.
102
O'Toole
AC
Danylchuk
AJ
Suski
CD
Cooke
SJ
(
2010
)
Consequences of catch-and-release angling on the physiological status, injury, and immediate mortality of great barracuda (Sphyraena barracuda) in The Bahamas
.
ICES J Mar Sci
 
67
:
1667
1675
.
103
Paula
VV
Fantoni
DT
Otsuki
DA
Auler
JOC
Jr
(
2008
)
Blood-gas and electrolyte values for Amazon parrots (Amazona aestiva)
.
Pesq Vet Bras
 
28
:
108
112
.
104
Peiró
JR
Borges
AS
Gonçalves
RC
Mendes
LCN
(
2010
)
Evaluation of a portable clinical analyzer for the determination of blood gas partial pressures, electrolyte concentrations, and hematocrit in venous blood samples collected from cattle, horses, and sheep
.
Am J Vet Res
 
71
:
515
521
.
105
Petri
D
Hamre
K
Lundebye
AK
(
2008
)
Retention of the synthetic antioxidant butylated hydroxyanisole in Atlantic salmon (Salmo salar) fillets
.
Aquacult Nutr
 
14
:
453
458
.
106
Plebani
M
(
2009
)
Does POCT reduce the risk of error in laboratory testing?
Clim Chim Acta
 
404
:
59
64
.
107
Prosser
CL
(
1973
)
Comparative Animal Physiology: Sensory, Effector and Integrative Physiology
, Ed
3
.
Saunders
,
Philadelphia, USA
, pp
145
147
.
108
Pyne
BP
Boston
T
Martin
DT
Logan
A
(
2000
)
Evaluation of the Lactate Pro blood analyser
.
Eur J Appl Physiol
 
82
:
112
116
.
109
Remen
M
Imsland
AK
Stefansson
SO
Jonassen
TM
Foss
A
(
2008
)
Interactive effects of ammonia and oxygen on growth and physiological status of juvenile Atlantic cod (Gadus morhua)
.
Aquaculture
 
274
:
292
299
.
110
Rogers
KD
Booth
DT
(
2004
)
A method of sampling blood from Australian freshwater turtles
.
Wildlife Res
 
31
:
93
95
.
111
Romero
LM
Wikelski
M
(
2010
)
Stress physiology as a predictor of survival in Galapagos marine iguanas
.
Proc Biol Sci
 
277
:
3157
3162
.
112
Roth
B
Rotabakk
BT
(
2012
)
Stress associated with commercial longlining and recreational fishing of saithe (Pollachius virens) and the subsequent effect on blood gases and chemistry
.
Fish Res
 
115–116
:
110
114
.
113
St-Louis
P
(
2000
)
Status of point-of-care testing: promise, realities, and possibilities
.
Clin Biochem
 
33
:
427
440
.
114
Sampson
K
Merigo
C
Lagueux
K
Rice
J
Cooper
R
Weber
ES
III
Kass
P
Mandelman
JW
Innis
C
(
2012
)
Clinical assessment and postrelease monitoring of 11 mass stranded dolphins on Cape Cod, Massachusetts
.
Mar Mammal Sci
 
28
:
404
425
.
115
Schalm
OW
Jain
NC
Carroll
EJ
(
1975
)
Veterinary Haematology
, Ed
3
.
Lea and Febiger
,
Philadelphia
.
116
Serra-Llinares
RM
Tveiten
H
Damsgård
B
Aas-Hansen
O
(
2012
)
Evaluation of a fast and simple method for measuring plasma lactate levels in Atlantic cod, Gadus morhua (L.)
.
Intern J Fish Aquacult
 
4
:
217
220
.
117
Spicer
JI
Gaston
KJ
(
1999
)
Physiological Diversity and its Ecological Implications
.
Blackwell Science
,
Oxford, UK
.
118
Steinmetz
HW
Vogt
R
Sabine
K
Riond
B
Hatt
J-M
(
2007
)
Evaluation of the i-STAT portable clinical analyzer in chickens (Gallus gallus)
.
J Vet Diagn Invest
 
19
:
382
388
.
119
Stockard
TK
Levenson
DH
Berg
L
Fransioli
JR
Baranov
EA
Pronganis
PJ
(
2007
)
Blood oxygen depletion during rest-associated apneas of northern elephant seals (Mirounga angustirstris)
.
J Exp Biol
 
210
:
2607
2617
.
120
Stoot
LJ
Cairns
NA
Blouin-Demers
G
Cooke
SJ
(
2013
)
Physiological disturbances and behavioural impairment associated with the incidental capture of freshwater turtles in a commercial fyke-net fishery
.
Endang Species Res
 
21
:
13
23
.
121
Suski
CD
Cooke
SJ
Danylchuk
AJ
O'Connor
CM
Gravel
M-A
Redpath
T
Hanson
KC
Gingerich
AJ
Murchie
K
Danylchuk
SE
et al
(
2007
)
Physiological disturbance and recovery dynamics of bonefish (Albula vulpes), a tropical marine fish, in response to variable exercise and exposure to air
.
Comp Biochem Physiol A Mol Integr Physiol
 
148
:
664
673
.
122
Taylor
MK
Cook
KV
Hasler
CT
Schmidt
DC
Cooke
SJ
(
2012
)
Behaviour and physiology of mountain whitefish (Prosopium williamsoni) relative to short-term changes in river flow
.
Ecol Freshw Fish
 
21
:
495
657
.
123
Thompson
LA
Cooke
SJ
Donaldson
MR
Hanson
KC
Gingerich
A
Klefoth
T
Arlinghaus
R
(
2012
)
Physiology, behaviour, and survival of angled and air-exposed largemouth bass
.
North Am J Fish Manage
 
28
:
1059
1068
.
124
Thrall
MA
Weiser
G
Allison
R
Campbell
TW
(
2012
)
Veterinary Hematology and Clinical Chemistry
.
Wiley-Blackwell
,
Oxford, UK
.
125
Trushenski
JT
Bowker
JD
(
2012
)
Effect of voltage and exposure time on fish response to electrosedation
.
J Fish Wildl Manage
 
3
:
1
12
.
126
Trushenski
JT
Schwarz
M
Takeuchi
R
Delbos
B
Sampaio
LA
(
2010
)
Physiological responses of cobia Rachycentron canadum following exposure to low water and air exposure stress challenges
.
Aquaculture
 
307
:
173
177
.
127
Trushenski
JT
Bowker
JD
Gause
BR
Mulligan
BL
(
2012a
)
Chemical and electrical approaches to sedation of hybrid striped bass: induction, recovery, and physiological responses to sedation
.
Trans Am Fish Soc
 
141
:
455
467
.
128
Trushenski
JT
Bowker
JD
Mulligan
BL
Gause
BR
(
2012b
)
Induction, recovery, and hematological responses of largemouth bass to chemo- and electrosedation
.
N Am J Aquacult
 
74
:
214
223
.
129
Venn Beecham
R
Small
BC
Minchew
CD
(
2006
)
Using portable lactate and glucose meters for catfish research: acceptable alternatives to established laboratory methods?
N Am J Aquacult
 
68
:
291
295
.
130
Wells
RMG
Dunphy
BJ
(
2009
)
Potential impact of metabolic acidosis on the fixed-acid Bohr effect in snapper (Pagrus auratus) following angling stress
.
Comp Biochem Physiol A Mol Integr Physiol
 
154
:
56
60
.
131
Wells
RMG
Pankhurst
NW
(
1999
)
Evaluation of simple instruments for the instruments for the measurement of blood glucose and lactate, and plasma protein as stress indicators in fish
.
J World Aquacult Soc
 
30
:
276
284
.
132
White
AJ
Schreer
JF
Cooke
SJ
(
2008
)
Behavioural and physiological responses of the congeneric largemouth (Micropterus salmoides) and smallmouth bass (M. dolomieu) to various exercise and air exposure durations
.
Fish Res
 
89
:
9
16
.
133
White
FN
(
1978
)
Comparative aspects of vertebrate cardiorespiratory physiology
.
Annu Rev Physiol
 
40
:
471
499
.
134
Wikelski
M
Cooke
SJ
(
2006
)
Conservation physiology
.
Trends Ecol Evol
 
21
:
38
46
.
135
Wimsatt
J
O'Shea
TJ
Ellison
LE
Pearce
RD
Price
VR
(
2005
)
Anesthesia and blood sampling of wild big brown bats (Eptesicus fuscus) with an assessment of impacts on survival
.
J Wildl Dis
 
41
:
87
95
.
136
Wolf
KN
Harms
CA
Beasley
JF
(
2008
)
Evaluation of five clinical chemistry analyzers for use in health assessment in sea turtles
.
J Am Vet Med Assoc
 
233
:
470
475
.

Author notes

Editor: Craig Franklin
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted distribution and reproduction in any medium, provided the original work is properly cited.