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Abstract

Objectives

The aim of this study was to compare the characteristics of fresh and stored feline red blood cells (RBCs) after passage through an 18 μm microaggregate filter.

Methods

Nine cats were recruited for a single blood donation using an open collection system. A simulated transfusion using a syringe driver and microaggregate filter was performed over 2 h with half the blood on the day of donation and the other half after 35 days of storage. Differences in haematological parameters, haemolysis percentage and osmotic fragility (OF) were compared on the day of donation pre-filter passage (D0–) vs day of donation post-filter (D0+) or day 35 storage pre-filter (D35–) and post-filter (D35+). Blood was cultured at D0+ and D35+.

Results

There were no statistically significant differences in the D0– vs D0+ comparisons. There were statistically significant (P <0.05) increases in haemolysis percentage, red cell distribution width (RDW) percentage and mean OF, and decreases in packed cell volume (PCV), RBC count, haemoglobin and haematocrit for D0– vs D35–. The same was found for D0– vs D35+ with the addition of a significant increase in mean cell haemoglobin (MCH). For D35– vs D35+ only MCH significantly increased. At day 35, 6/9 units had haemolysis percentages that exceeded 1%. This increased to 8/9 of stored units post-filter passage. All blood units cultured negative.

Conclusions and relevance

Fresh RBCs exhibited no in vitro evidence of injury following passage through an 18 μm microaggregate filter. Increased MCH was observed in the stored blood and may represent haemolysis induced by the filter. All other changes can be explained by storage lesion rather than filter passage. The findings highlight the importance of blood banking quality controls and the need for further research to assess the effects of transfusion technique, specifically filter passage, on storage lesion-affected feline blood.

Keywords

Erythrocytes storage lesion micropore filters blood transfusion erythrocyte indices haemolysis osmotic fragility in vitro techniques syringes

Introduction

Blood transfusions are essential to feline emergency and critical care medicine. While a few commercial blood banks exist, many practitioners worldwide collect blood in-house.¹ Accessibility to suitable donors can be challenging, and the storage of feline blood is controversial.^2,3 Consequently, feline blood donations are often performed on demand for immediate transfusion to the recipient.

Storage of blood is advantageous, allowing collection from donors in a controlled environment and immediate access to blood products for recipients. There are few studies reporting on the ideal storage time of feline blood.^2–7 Official feline blood banking standards have not been established, with current recommendations to determine blood ‘shelf life’ extrapolated from human guidelines.^3–5 The US Food and Drug Administration (FDA) human blood banking regulations stipulate a minimum of 75% 24 h post-transfusion red blood cell (RBC) survival in the recipient’s circulation⁸ and a maximum of 1% haemolysis after 42 days of storage.⁹ Using biotinylating cell-labelling techniques, 85% RBC survival 24 h post-transfusion has been demonstrated for feline whole blood (FWB) stored in citrate dextrose adenosine phosphate 1 (CPDA-1) for 35 days.⁶

Collectively termed the ‘storage lesion’, the progressive biochemical and biomechanical RBC changes that occur during storage may have implications for RBC survival and viability post-transfusion.^10,11 Alterations to RBC membrane integrity and shape lead to reduced cell deformability and oxygen-carrying capacity and increased haemolysis.^4,10,12 Biochemical, haematological and morphological features of storage lesion have been documented in feline blood.^{3–5,11,13–17} Both unchanged³ and significantly increased¹⁷ mean osmotic fragility (MOF) and varying levels of haemolysis have been reported.^3–5

Cat transfusions are typically delivered via syringe driver¹ and 18 μm microaggregate filter.^18,19 This technique has been demonstrated to cause no significant in vivo loss of RBCs compared with the traditional gravity-dependent delivery methods in cats.²⁰ Notably, in this study blood was stored for <12 h prior to transfusion.²⁰

To date, there have been no studies assessing the effects of filter passage on stored feline RBCs. The objective of this study was to determine whether passage through a microaggregate filter damages feline RBCs as indicated by increased haemolysis percentage, MOF or haematological derangements, and if these effects are compounded in blood that has been stored for 35 days.

Materials and methods

Blood donors and sampling protocol

Nine domestic cats between 1 and 9 years of age with a minimum lean body weight of 4.5 kg were recruited. Cats were in good health based on history, physical examination and results of screening tests including complete blood count (CBC), serum biochemistry, feline immunodeficiency virus and feline leukaemia virus tests (Witness FIV/FeLV; Zoetis Animal Health) and echocardiogram. Informed consent was obtained from each owner, and the study protocol was approved by the University of Sydney Animal Ethics Committee (project number: 2018/1358).

Prior to donation, 6/9 cats received between 50 and 100 mg of oral gabapentin. For blood donation, cats were sedated with intramuscular and/or intravenous injection(s) of 0.19–0.25 mg/kg midazolam, 0.15–0.2 mg/kg butorphanol and 3.75–8.3 mg/kg ketamine. An intravenous catheter was placed, and mask oxygen provided. Additional sedation with alfaxalone was used for 3/9 cats. Cats were monitored with electrocardiography, pulse oximetry and oscillometric blood pressure. Full vitals and anaesthetic depth were assessed every 5 mins until cats regained consciousness. Cats were placed in lateral recumbency and the neck clipped of fur followed by surgical skin preparation. An open collection system consisting of a 21 G butterfly needle attached to a three-way stopcock, 50 ml syringe containing CPDA-1 in a 1:7 ratio to the intended blood volume and 100 ml blood storage bag (Animal Blood Banking International) was used to collect blood via jugular venepuncture. A maximum of 10 ml/kg of blood was collected per cat. Half the blood was partitioned into the storage bag via the three-way stopcock. The extension line was stripped of blood and sealed with metal clips. Blood units were stored upright in a dedicated refrigerator at +4°C for 35 days. A maximum of three cats donated blood on any 1 day.

Simulated transfusion and blood culture

Blood sampling was performed at four time points: the day of donation, pre-filter passage (D0–); the day of donation, post-filter passage (D0+); after 35 days of storage, pre-filter passage (D35–); and after 35 days of storage, post-filter passage (D35+). On the day of donation, half the blood was reserved in the collection syringe for immediate sampling and simulated transfusion. The syringe was disconnected from the three-way stopcock and 4 ml of blood transferred to EDTA and plain tubes. The syringe was then connected to a micro-bore extension set and 18 μm microaggregate filter (Hemo-nate; Utah Medical Products) and loaded into a syringe driver (Perfusor Space Syringe Infusion Pump; B Braun Vet Care). Blood was ‘transfused’ over a 2 h period. The initial 10 ml was inoculated into a blood culture bottle (Oxoid Signal Blood Culture bottle; Thermo Fisher Scientific) for anaerobic and aerobic culture with the final 4 ml reserved post-filter passage for analysis. Blood culture bottles were incubated at 37°C ± 1°C in both aerobic and anaerobic conditions with daily inspection for 5 days for signs of bacterial growth. After 35 days of storage, blood reserved in the storage bags was aseptically drawn into a syringe via a spike (Swan-lock take set; Codan US). Blood collection for analysis and simulated transfusion as described above was performed (D35– and D35+).

Haematology and haemolysis

Haematology was performed at each time point within 6 h of sample collection using an automated haematology machine (Sysmex XN 1000RF Vet Analyser; Roche Diagnostics). Parameters measured included RBC count, haemoglobin (Hb), haematocrit (HCT), mean cell volume (MCV), mean cell Hb (MCH), mean cell Hb concentration (MCHC) and red blood cell distribution width (RDW). A manual packed cell volume (PCV) was performed and used to calculate MCH and MCHC.

As previously described in cats, Hb was determined using a specific analyser (Hb 201 + System; HemoCue) with daily calibration using a 120 g/l standard.²¹ Plasma was obtained by centrifuging (Orbital 360; Clements) 1 ml of anticoagulated blood at 1200 g for 15 mins. Supernatant Hb was determined by a spectrophotometer (Plasma/Low Hb; HemoCue) for determination of low Hb levels. This analyser was calibrated each day of use with 1.0 g/l and 5.0 g/l controls. Percentage haemolysis was calculated using the formula:

\begin{array}{l} H a e m o l y s i s (%) = S u p e r n a t a n t H b (g / l) \times \\ (100 - P C V) / T o t a l H b (g / l) .^{5} \end{array}

Osmotic fragility testing

Osmotic fragility (OF) testing was performed using 360 μl of blood reserved from each time point based on methods previously described.^3,22,23 A stock solution of 10% phosphate buffered saline with pH 7.4 was diluted with distilled water to create a 1% NaCl solution. Using this solution and distilled water, 18 test tubes were prepared with NaCl concentrations ranging from 0.9% to 0.0% NaCl in 0.05% increments. To each tube, 20 μl of blood was added and mixed by inversion. Samples were incubated at 22°C for 45 mins then centrifuged (Centrifuge 5810R; Eppendorf AG) at 2000 g for 10 mins. The optical density of each supernatant was determined spectrophotometrically (Tecan M1000 Pro plate reader; Tecan Austria) at a wavelength of 540 nm. Distilled water was used as a blank. Percentage of haemolysis for each dilution was calculated based on the distilled water sample representing complete RBC lysis. OF curves were plotted, and the MOF values were determined from the curves as the concentration of NaCl at which 50% haemolysis occurred.

Statistical analysis

Data were grouped according to storage time and filter passage. All data were assessed for normality using a Shapiro–Wilk test and statistical analysis performed using commercially available software (SPSS Statistics, Version 24; IBM). The Wilcoxon signed ranks test was used to compare differences in the ranks of haematological parameters, percentage haemolysis and OF for D0– vs D0+, D0– vs D35–, D0- vs D35+ and D35– vs D35+. Statistical significance was determined using a z-statistic applied to sum of ranks, and differences were considered statistically significant when P <0.05.

Results

Haematological parameters, haemolysis percentage and MOF

Results are reported in Table 1.

Table 1

Effect of storage and microaggregate filter passage on haematological parameters, including mean osmotic fragility (MOF) and haemolysis percentage in nine feline whole blood units

Parameter	Day	Filter passage	Median	Range
				Minimum	Maximum
PCV (%)	0	Pre-filter	27^a	20	31
		Post-filter	24^a	19	32
	35	Pre-filter	22^b	15	27
		Post-filter	22^b	13	25
HCT (%)	0	Pre-filter	0.27^a	0.2	0.36
		Post-filter	0.24^a	0.18	0.33
	35	Pre-filter	0.23^b	0.17	0.29
		Post-filter	0.22^b	0.14	0.28
RBC count (×10¹²/l)	0	Pre-filter	6.45^a	4.29	8.51
		Post-filter	6.08^a	4.56	8.78
	35	Pre-filter	5.95^b	3.67	7.31
		Post-filter	6.01^b	3.4	6.84
Hb (g/l) Benchtop analyser	0	Pre-filter	93^a	66	114
		Post-filter	90^a	68	114
	35	Pre-filter	86^b	55	96
		Post-filter	71^b	62	107
Hb (g/l) Diagnostic laboratory	0	Pre-filter	95^a	66	120
		Post-filter	87^a	62	115
	35	Pre-filter	87^b	57	98
		Post-filter	86^b	52	95
MCV (fl)	0	Pre-filter	40.5^a	35.9	45.9
		Post-filter	40.2^a	35.5	42.7
	35	Pre-filter	39.2^a	33.2	42.5
		Post-filter	38.2^a	33.6	45.5
MCH (pg)	0	Pre-filter	14.1^a	12.3	15.4
		Post-filter	14^a	12.2	15.6
	35	Pre-filter	14.2^a	12.4	15.5
		Post-filter	14.4^b	12.5	15.7
MCHC (g/l)	0	Pre-filter	354^a	335	387
		Post-filter	351^a	326	376
	35	Pre-filter	364^a	348	414
		Post-filter	376^a	337	413
RDW (%)	0	Pre-filter	15.5^a	13.2	21.5
		Post-filter	15.7^a	13.2	21.2
	35	Pre-filter	20.4^b	17.6	22
		Post-filter	19.9^b	17.8	22.4
Haemolysis (%)	0	Pre-filter	0.23^a	0.12	0.29
		Post-filter	0.17^a	0.08	0.36
	35	Pre-filter	1.31^b	0.81	1.85
		Post-filter	1.48^b	0.84	2.07
MOF (NaCl %)	0	Pre-filter	0.54^a	0.48	0.55
		Post-filter	0.53^a	0.47	0.55
	35	Pre-filter	0.58^b	0.53	0.63
		Post-filter	0.59^b	0.53	0.64

Only comparisons involving day 0 pre-filter samples are represented. Superscript letters that are different when compared with day 0 pre-filter samples within each category indicate significant differences (P <0.05) using the Wilcoxon signed-rank test

Mean cell volume (MCV) and mean cell haemoglobin concentration (MCHC) are calculated from manual packed cell volume (PCV) and reference laboratory haemoglobin, and not the haematocrit (HCT) value

Haemolysis % was calculated from the equation found in the methods using the Hb 201 total haemoglobin measurement

RBC = red blood cell; Hb = haemoglobin; MCH = mean cell Hb; RDW = red cell distribution width

There were no significant differences (P >0.05) in any parameter pre- (D0–) and post-filter (D0+) passage on the day of blood collection. Comparing D0– and D35– there were statistically significant increases in percentage haemolysis (Z = −2.803, P = 0.005), RDW (Z = −2.67, P = 0.008) and MOF (Z = −2.701, P = 0.007), and decreases in PCV (Z = −2.536, P = 0.011), RBC count (Z = −2.547, P = 0.011), haemoglobin (benchtop analyser) (Z = −2.49, P = 0.013), haemoglobin (diagnostic laboratory) (Z = −2.552, P = 0.011) and haematocrit (Z = −2.49, P = 0.013). The same significant increases and decreases were found when comparing D0– and D35+, with the addition of a statistically significant increase in MCH (Z = −1.481, P = 0.016). Comparing D35– and D35+, the only significant change was an increase in MCH (Z = −1.994, P = 0.046).

Microbiological analysis

Bacteria were not cultured aerobically or anaerobically from any of the units at either D0+ or D35+.

Discussion

This study is the first to examine in vitro markers of quality in fresh and stored FWB that has been passed through a microaggregate filter. Presumably, stored RBCs affected by the storage lesion are less deformable and more at risk of damage when travelling through micropores. However, the results of this study indicated that most changes could be attributed to the storage lesion. Increased MCH was the only statistically significant change that could be ascribed to an effect of filter passage. The haematological changes and notably significant increase in haemolysis percentage observed at day 35 of storage may have clinical implications for blood recipients and blood banking quality control programmes.

Designed to remove microaggregates of cell debris, platelets, white blood cells and fibrin that accumulate during blood storage,^24,25 the specific filter used in this study is recommended for feline blood transfusions.^18,19 While clinical use has been validated in a feline RBC survival study,²⁰ a similar study in dogs identified significant in vivo loss of RBCs within 24 h of transfusion via syringe pump and microaggregate filter.²⁶ Shearing stress and mechanical trauma from filter passage were suggested as mechanisms for early RBC clearance by the recipients’ reticuloendothelial system.²⁶ Interestingly, the authors found no significant changes to RBC count, plasma Hb or OF in fresh blood transfused via gravity, pump or syringe pump with microaggregate filter.²⁶ Similarly, no significant changes to CBC variables, OF or RBC morphology were reported in a recent study evaluating effect of syringe driver and microaggregate filter passage on fresh canine whole blood (WB).²⁷ While the species and study methodologies differ, the results are in line with the present study, demonstrating a lack of microaggregate filter-induced in vitro damage to fresh blood.

PCV, RBC count, Hb and HCT all decreased significantly during storage. While not reported in stored FWB,^3,4,16 a decrease in PCV during storage of feline packed RBCs (PRBCs) has been described.⁵ The PCV of canine and human stored PRBCs generally increases with storage owing to increased RBC membrane permeability and subsequent intracellular water influx and cell swelling.^28–30 It has been theorised that feline RBCs are resistant to swelling owing to their specific surface area-to-volume ratios and possibly reduced OF, compared with canine RBCs.⁵ This is supported by the lack of significant end storage MCV change in this study.

Studies of canine PRBCs^31–33 report significant PCV decreases with storage, ascribed to RBC sedimentation in the primary collection bag prior to transfer to satellite bags for storage. The authors believe this may have played a role in the changes to PCV, RBC count, Hb and HCT noted in this study. Settling of the RBCs dependent to the plasma was noted in the syringes during the simulated transfusion. Decreased RBC count and HCT or PCV and an increase in MCH and MCHC are also well described secondary to in vitro haemolysis in human^34,35 and canine³⁶ blood. While statistical significance was not reached, the observed increase in MCHC during storage supports this theory. It is likely that a combination of species-specific RBC factors, including blood collection and handling technique, contributed to the observed changes.

MCH only significantly changed in comparisons involving the filter passage of stored blood. In both the D0– vs D35+ and D35– vs D35+ comparisons MCH increased. MCH is the average mass of Hb per RBC and is calculated from Hb and RBC count or (as used in this study) PCV.³⁵ Total Hb measurements were performed by methodologies that lyse RBCs, therefore not discriminating intracellular from free Hb. Consequently, increased MCH may occur as a result of in vitro haemolysis where PCV is decreased and Hb concentration remains stable,³⁵ or as is theorised in this case, decreased comparatively less than the PCV. The significant decreases in RBCs and PCV and increase in haemolysis percentage in the D0– vs D35+ comparison supports this theory. MCH was the only parameter to significantly change in the stored blood pre- and post-filter comparison. Filter passage-enhanced in vitro haemolysis where the threshold of change for the other indicators of haemolysis did not reach statistical significance may also explain this finding.

MOF significantly increased by the end of storage, a finding replicated with or without filter passage. Storage-related increases in MOF have been reported in feline PRBCs collected via vascular access ports (VAPs), with the increase in RBC fragility attributed to VAP-induced membrane damage.¹⁷ Increased MOF has also been documented in stored human WB³⁷ and PRBCs,^12,38 and stored canine PRBCs.³¹ Changes to MOF are not a uniformly reported feature of storage lesion, with some human blood storage studies^39–41 and a recent study of stored FWB collected by a novel closed collection system³ demonstrating no statistically significant MOF increase.

Stored human RBCs shed membrane microvesicles, leading to irreversible alterations to their shape and the formation of sphero-echinocytes and spherocytes that have less ability to withstand increased osmotic stress.¹² Increases in echinocyte number,^3,4,16 spherocytes and lysed RBCs¹⁶ have been identified in FWB stored for 35 days. RBC membrane alteration during storage likely caused the increase in MOF observed in this study, with the significant end storage RDW increase supporting RBC anisocytosis and morphological variation.⁴² While increased MOF and haemolysis percentage failed to reach statistical significance in the pre- and post-filter comparison at day 35, the overall increase in haemolysis suggests that filter passage-induced injury may be amplified in storage lesion-affected RBCs. The clinical implications of transfusing stored feline blood with increased OF is unknown and may affect the longevity of transfused RBCs in the recipient.

Haemolysis percentage significantly increased from the day of collection compared with D35. In line with recently published studies investigating haemolysis percentage in stored FWB, no sample had a haemolysis percentage that exceeded 1% at the point of collection (D0)^3–5 or after filter passage on D0. By D35, two-thirds (n = 6/9) of the blood units’ haemolysis percentage exceeded the FDA limit of 1%. This increase was statistically significant for both D0 vs D35 pre- and post-filter comparisons. This finding is similar to a recent study where mean haemolysis percentage in FWB units exceeded 1% by 21 days of storage.⁴ Another study of feline PRBCs documented a mean haemolysis percentage of >1% in 13.8% of units stored for longer than 28 days. In contrast, a study of eight FWB units retained a haemolysis percentage <1% at the end of 35 days of storage.³ The comparatively lower mean haemolysis at all times points in that study may have been a consequence of reduced shear stress associated with using a novel closed system and smaller 20 ml aspiration syringes for blood collection.³ Although not statistically significant when compared with D35 pre-filter samples, 8/9 (89%) units had >1% haemolysis post-filter passage at D35. A recent canine study found no significant increase in haemolysis percentage in PRBCs stored for <14 days after passage through an 18 µm filter at maximal manual infusion rates.⁴³

The clinical significance of transfusing blood with >1% haemolysis has not been established in cats. Free haemoglobin induces oxidative stress, with potentially detrimental effects to renal, myocardial and vascular systems.^44,45 Transfusion of haemolysed blood carries an increased risk of adverse transfusion reactions and in dogs, has resulted in death.⁴⁶ The findings in the present study highlight the importance of blood banking quality controls and the need for further research to clarify the consequences of syringe pump infusion and filter passage on storage lesion-affected feline blood.

This study had a number of limitations. It is likely the small number of blood units evaluated made some statistical comparisons underpowered. RBC morphological analysis was not performed, limiting further interpretation of some haematological alterations. Five samples on the day of collection and three samples at D35 had a haemolysis percentage that decreased between pre- and post-filter passage analysis. Similar results have been found in humans²⁵ and dogs,⁴³ and the reasons for this are unclear. Proposed mechanisms include the settling of blood during the transfusion and/or partial filter occlusion, leading to inconsistencies in HCT/PCV and plasma Hb results.²⁵ Haemolysis percentage was derived from haemoglobin concentrations measured via automated analysers rather than gold-standard reference methods. While designed for very low-level plasma haemoglobin readings, the plasma/low haemoglobin system demonstrates non-linearity for haemoglobin readings between 0 and 0.3 g/l. The inability to distinguish between very low-level haemoglobin values may have affected the accuracy of some haemolysis calculations.

Conclusions

FWB undergoes haematological changes, including increased haemolysis percentage and increased MOF, with storage. While the significant MCH increases suggest enhanced in vitro haemolysis in stored blood due to microaggregate filter passage, the difference in haemolysis percentage was ultimately not statistically significant in the comparison assessing isolated filter passage effect on stored blood. In vivo studies are required to understand if haematological derangements associated with the storage lesion and potentially enhanced by transfusion and filter passage-associated shear stress translate to reduced RBC viability within recipient circulation.

Footnotes

Acknowledgements

The authors thank Dr Michael Ward for his assistance with the statistical analysis.

Accepted: 16 March 2021

Author note

This research was presented as an abstract at the Australian and New Zealand College of Veterinary Science (ANZCVS) Emergency and Critical Care (ECC) Chapter Online Scientific Series and Abstract Forum 2020.

Conflict of interest

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

Funding

This work was supported by the June Rose Bullock Bequest 2018; Sydney School of Veterinary Science Small Research Grant from Bequests.

Ethical approval

This work involved the use of non-experimental animals only (including owned or unowned animals and data from prospective or retrospective studies). Established internationally high standards (‘best practice’) of individual veterinary clinical patient care were followed. Ethical approval from a committee, while not necessarily required, was nonetheless obtained, as stated in the manuscript.

Informed consent

Informed consent (either verbal or written) was obtained from the owner or legal custodian of all animal(s) described in this work (either experimental or non-experimental animals) for the procedure(s) undertaken (either prospective or retrospective studies). No animals or humans are identifiable within this publication, and therefore additional informed consent for publication was not required.

ORCID iD

Sophia A Morse

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Effect of microaggregate filter passage on feline whole blood stored for 35 days

Abstract

Objectives

Methods

Results

Conclusions and relevance

Keywords

Introduction

Materials and methods

Blood donors and sampling protocol

Simulated transfusion and blood culture

Haematology and haemolysis

Osmotic fragility testing

Statistical analysis

Results

Haematological parameters, haemolysis percentage and MOF

Microbiological analysis

Discussion

Conclusions

Footnotes

Acknowledgements

Author note

Conflict of interest

Funding

Ethical approval

Informed consent

ORCID iD

References