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Review

Heat Inactivation of Influenza Viruses—Analysis of Published Data and Estimations for Required Decimal Reduction Times for Different Temperatures and Media

by
Martin Hessling
*,
Nicole Fehler
,
Anna-Maria Gierke
,
Ben Sicks
and
Petra Vatter
Institute of Medical Engineering and Mechatronics, Ulm University of Applied Sciences, Albert-Einstein-Allee 55, D-89081 Ulm, Germany
*
Author to whom correspondence should be addressed.
Microbiol. Res. 2022, 13(4), 853-871; https://doi.org/10.3390/microbiolres13040060
Submission received: 15 September 2022 / Revised: 14 October 2022 / Accepted: 17 October 2022 / Published: 20 October 2022
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Abstract

:
(1) Background: Influenza is a viral infection that has claimed many millions of lives over the past 100 years, and there is always a risk that a new influenza virus will emerge and cause another pandemic. One way to reduce such a potential new influenza virus will be heat inactivation. The question in this study is how much the heat sensitivities of previous influenza viruses differ. If they are very similar, it is expected that a new influenza virus can be inactivated with the same heat parameters as previous influenza viruses. (2) Methods: Through a literature search, published heat inactivation results are compiled and analyzed using Arrhenius models and regression equations for decimal reduction times for different temperatures and media determined. (3) Results: There are about 50 studies on heat inactivation of human and avian influenza viruses so far, showing large differences in heat sensitivity of influenza viruses in different media. However, within a single medium the differences between viruses are rather small. (4) Conclusions: At a temperature of 60 °C, previous influenza viruses can be reduced by 4 or more orders of magnitude within approximately 30 min in almost all media, and this is likely to be true for a potential new influenza virus. Further studies, especially on human influenza viruses, would be desirable.

1. Introduction

The coronavirus pandemic, which began back in 2019, is still ongoing in 2022, and the number of new COVID-19 (Coronavirus Disease 2019) infections worldwide is currently around 1 million per day [1]. Most of this transmission is airborne. Surfaces and other potential carriers seem to play a minor role [2,3,4].
Influenza is an infection that has many similarities with COVID. The source of severe respiratory illnesses in humans, which can occur in a pandemic, is also an enveloped RNA virus that can also be transmitted via air. Unlike coronaviruses, however, influenza viruses can remain infectious for prolonged periods on surfaces, in liquids, or on other fomites [5,6,7].
The triggers of human influenza infections are influenza viruses of types A and B, with type A appearing in the form of many subtypes that are distinguished on the basis of their surface proteins hemagglutinin (H1 to H18) and neuraminidase (N1 to N11). For example, the trigger of the largest influenza pandemic to date, the Spanish flu of 1918, with its estimated 50 million deaths, was an influenza A virus of the subtype H1N1 [8]. All subsequent influenza pandemics have also been caused by influenza A viruses [8]. Such a pandemic can be caused by humanity coming into contact for the first time with a new influenza A virus subtype for which no immunity exists in the population. Such a new subtype may appear, for example, when an influenza virus jumps from an animal to a human host. In the past, poultry and pigs have been particularly relevant in this regard, with water fowl considered the natural reservoir of influenza viruses [8,9].
In case of detected influenza infections in humans or animals—it is tried to stop the spread of the virus. For this purpose, it is necessary to inactivate influenza viruses on various fomites. These could be liquids like water, surfaces and animal foodstuffs.
Chemical disinfection and UV radiation are common and effective disinfection techniques, but they cannot always be applied or, in the case of UV radiation for example, may not reach the viruses. Heat inactivation is another well-known disinfection approach that also works in bulk materials. In this process, heat inactivates mainly the relevant viral proteins [10].
There are already some published studies that clearly demonstrate the effect of heat on influenza viruses [11,12,13,14,15,16,17]. However, so far, mostly only individual influenza A virus subtypes have been investigated for some contaminated media like phosphate buffered saline (PBS), animal food or filtering facepiece material [18,19,20,21,22]. It would be desirable to be able to make general statements on the temperature sensitivity of all influenza viruses in all relevant media. In case of the emergence of a new pandemic influenza virus, simple heat inactivation protocol suggestions would be already available.
Therefore, in the study presented here, published heat inactivation data for influenza viruses are collected and analyzed to estimate necessary heat application durations for 90% reduction, the so-called decimal reduction time or D value, for different temperatures and media. As a mathematical basis, it is assumed that virus inactivation follows at least approximately an exponential course:
c ( t ) = 10 − k ( T )   t
c(t) is the concentration of non-inactivated viruses at time t and k(T) is the inactivation rate at temperature T (in Kelvin). In this representation, the reciprocal of the inactivation rate k(T) is equal to the necessary decimal reduction time D(T) for a 90% inactivation:
D ( T ) = 1 k ( T )  
In order to compare virus data for different temperatures, a simple model is also applied for the temperature dependence of the inactivation rate, in which it is assumed that the inactivation rate depends exponentially on the temperature T:
        k ( T ) = 10 − a T + b
→   D ( T ) = 10   a T − b
            →   log ( D ( T ) ) = a   1 T − b  
with the temperature-independent parameters a and b. In this representation, the logarithm (base 10) of D(T) is a linear function of 1/T.
This approach is the so-called Arrhenius model, which was proposed by Hiatt 1964 [23], among others, and has been successfully applied for a variety of virus inactivation analyses, e.g. influenza viruses [12,24] and also many other viruses [25,26,27,28,29,30,31].

2. Materials and Methods

Pubmed and Google Scholar were searched for various combinations of the terms: “influenza”, “flu”, “heat”, “disinfection”, “inactivation”, “reduction” and “sterilization”. Matching publications were examined to determine if they could also be included in this study. In addition, the suitability of all recent publications that cited the previously found sources was reviewed.
When assessing the suitability of studies, only those that addressed the effect of heat of ≥40 °C were included. Studies involving lower temperatures or the simultaneous application of other potentially inactivating measures were not considered. Because high and low pH values can also have an inactivating effect, only studies with mean pH values between 5.5 and 8.5 were included.
The quantitative data required for this analysis were often not directly provided in the retrieved publications. In such cases, it was attempted to determine quantitative values from graphs or tables. For example, in tables of infected or dead chicken embryos, the values for EID50 (embryo infectious dose 50) or ELD50 (embryo lethal dose 50) were determined analogously to the procedure of Reed and Muench [32]. In some cases, the contaminated medium was not explicitly named. In that case, it was assumed that the medium in which the viruses were propagated was also used for the inactivation experiments.
The parameters for the Arrhenius model discussed above were then determined for each medium separately, using linear regression and D(T) was plotted as a linear function of 1/T in each case. With the help of the determined temperature dependence of D(T) for the different contaminated media, expected decimal reduction times for different potential inactivation temperatures are calculated at the end.

3. Results

In total, about 50 publications on heat inactivation were retrieved, the oldest of which is almost 75 years old [11]. The overview of all inactivation data found is given in Table 1. In all cases, influenza virus reduction by the application of heat was observed, but in some cases quantitative analysis was impossible. This was the case, for example, when the temperature changed over the observation period or a virus concentration was below the detection limit after heat application. Where possible, the inactivation duration D for 90% inactivation for the respective virus at the specified temperature is given in Table 1. The publication by Chu mentioned above [11] is the only evaluable study on heat inactivation of influenza B viruses. Otherwise, the results are exclusively for influenza A viruses.
Figure 1 gives an overview of the correlation between 1/T and log(D(T)) for all influenza inactivation results in liquids except liquid animal foods or waste. Log(D(T)) = 0 indicates a decimal reduction time of 1 min, log(D(T)) = 1 is 10 min, and log(D(T)) = −1 represents 0.1 min. Also revealed is the result of a linear regression for D(T). The high scattering or deviation of the individual results from the regression curve is also represented in the relatively low square of the regression coefficient R2. For the corresponding Dlin regress(T) from linear regression holds:
D l i n   r e g r e s s ( T ) = 10 3812.6   K T − 10.995
Due to the scatter of the data, the most often investigated liquids PBS (phosphate buffered saline), allantoic fluid and cell culture medium were also analyzed separately. Figure 2 reveals all results of evaluable inactivation experiments from Figure 1, which were performed in PBS. These are data from Chmielewski et al. [18] for one low pathogenic avian influenza virus subtype (LPAI) and one high pathogenic avian influenza virus subtype (HPAI). Within the limits of their scattering, the values for the two virus subtypes are relatively close to each other and, because of the small data base, no reliable conclusions can be drawn about differences between these viruses. For Dlin regress(T) the derived formula from the linear regression is:
D l i n   r e g r e s s ( T ) = 10 18183   K T − 54.596
All results of evaluable inactivation experiments from Figure 1, which were performed in allantoic fluid are presented in Figure 3. Data exist for various influenza A virus subtypes and even for influenza B, but due to the small data base and the scatter of the individual values, no reliable conclusion can be drawn about differences in the temperature sensitivity of these influenza viruses. Based on data of all viruses in Figure 3 the decimal reduction time Dlin regress(T) is:
D l i n   r e g r e s s ( T ) = 10 8962.1   K T − 26.512
Figure 4 shows the results from evaluable inactivation experiments performed in cell culture media. Again, data exist for different influenza A virus subtypes (H1N1 and H7N7), but because the very limited database and different employed cell culture media, no meaningful conclusions can be reached about susceptibility differences between the different influenza viruses. Based on data of all viruses in Figure 4 the decimal reduction time Dlin regress(T) is:
D l i n   r e g r e s s ( T ) = 10 2267.5   K T − 6.517
The correlation between 1/T and log(D(T)) for all influenza inactivation results on surfaces is presented in Figure 5. For the corresponding Dlin regress(T) from the linear regression is:
D l i n   r e g r e s s ( T ) = 10 6726.1   K T − 19.279
Many published studies deal with the inactivation of influenza viruses in products or waste from the poultry industry. For example, Figure 6 presents the correlation between 1/T and log(D(T)) for all influenza inactivation results in chicken meat. Figure 6 also includes the result of a linear regression for the decimal reduction time Dlin regress(T):
D l i n   r e g r e s s ( T ) = 10 14699   K T − 44.152
Figure 7 shows the corresponding correlation for homogenized whole egg and the decimal reduction time Dlin regress(T) is:
D l i n   r e g r e s s ( T ) = 10 32006   K T − 96.587
The published inactivation data for dried egg white can be viewed in Figure 8. For the decimal reduction time Dlin regress(T) applies here:
D l i n   r e g r e s s ( T ) = 10 9786.4   K T − 26.674
For plain, salted, sweetened, or fortified egg yolk, the inactivation results published to date can be found in Figure 9, and linear regression of all data yields the following equation for the decimal reduction time Dlin regress(T):
D l i n   r e g r e s s ( T ) = 10 13098   K T − 39.814
Inactivation results also exist for fat-free eggs and egg replacements and are depicted in Figure 10, along with the regression line for the decimal reduction time Dlin regress(T):
D l i n   r e g r e s s ( T ) = 10 29081   K T − 87.814
In the event of an influenza outbreak, waste products must also be contaminated. Investigation results for manure and litter can be found in Figure 11. For the decimal reduction time Dlin regress(T) applies:
D l i n   r e g r e s s ( T ) = 10 17227   K T − 51.567
Applying the equations just determined for the decimal reduction times for the various contaminated media, the decimal reduction times for various temperatures were calculated and presented in Table 2.

4. Discussion

Despite the seemingly large number of individual results, the scope of the data is scarce because the individual results differ not only in temperature, but also in the medium and virus subtype examined. This prevents a more comprehensive investigation for differences between virus subtypes or even for possible differences between avian and human influenza viruses, which could be caused by the different body temperatures with 37 °C for humans and 40–42 °C for birds [9,71].
The small number of available data is also evident, for example, in the investigations in liquid egg white (Figure 8) and compost. For each only 4 and 5 data points, respectively, are available for only two different temperatures. For some of the investigated media, R2 of the regression curve is only between 0.4 and 0.6, which means that only 40% to 60% of the observed variation of the measured values can be explained by the model (regression curve). It should be noted that the residual variations of 60–40% are probably at least partially due to statistical biological scatter. Additionally, some of the figures display results of different working groups with different equipment and laboratory procedures. E.g., there may be differences in the precision (and speed) with which these different groups were able to adjust and measure the temperature of their virus samples, which would also contribute to the data scattering and a lower R2.
Inactivation of influenza viruses at comparatively low temperatures starting at about 50 °C is nevertheless clearly evident, but there are major differences with respect to the contaminated media. In particular, in dried egg white, the virus is relatively stable even at high temperatures. For all other media examined, the decimal reduction time from 60 °C is less than 10 min. It should be mentioned that so far, there is no published investigation or even hypothesis on the reason for this obvious dependence of the influenza virus heat stability on the medium.
Antiviral measures officially require a virus reduction of at least 4 powers of ten [72,73]. Under the assumption made above of exponential virus inactivation, an inactivation time of 4 decimal reduction times is necessary for this. With the exception of the dried egg white, such a 99.99% reduction could be accomplished at 60 °C in approximately about half an hour or even faster in almost all media.
These estimates are based on the Arrhenius model and the limited available data. The latter is rather unexpected, since influenza is an infection that typically causes about 500,000 deaths annually [74] and even more in pandemics, up to the estimated 50 million deaths that fell victim to the Spanish flu [75,76]. That is significantly more victims than in the current coronavirus pandemic and yet there are not more studies. In fact, the last and only study of influenza B virus heat inactivation is even 75 years old and there is also only one quantitative investigation on heat inactivation of influenza A in PBS performed by Swayne and colleagues, who have even generated about half of all single results in this study.
Investigations that are more current are largely concerned with avian influenza viruses. The background does not always seem to be the threat influenza poses to humans, but at least also economic interests of the poultry industry. This is an understandable and comprehensible motivation, but especially against the background of the coronavirus pandemic and the experiences from the influenza pandemics of the last 100 years, one should not wait with further influenza inactivation studies until the next influenza pandemic arrives, which can come at any time [77].

5. Conclusions

It seems that even moderate temperatures around 60 °C, which are well below the 121 °C sterilization temperature commonly used in many areas, are sufficient for influenza virus inactivation within about half an hour. However, the differences in various contaminated media are very large and, at least in dried egg white, influenza viruses are very temperature stable.
Because of the limited data available, it is difficult to determine how large the differences in heat sensitivity are between different influenza virus (sub-)types, or whether there are also relatively heat insensitive influenza viruses and thus whether a future, emerging influenza virus may also be relatively heat stable. Further investigations—prior to the next influenza pandemic—seem reasonable.

Funding

This research received no external funding.

Conflicts of Interest

The authors declare no conflict of interest.

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Microbiolres 13 00060 g001 550
Figure 1. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in liquids other than animal foods or waste along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
Figure 1. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in liquids other than animal foods or waste along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
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Figure 2. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in PBS along with the linear regression curve and for better understanding, D(T) is also given on the right Y-axis in a logarithmic scale. (LPAI: low pathogenic avian influenza, HPAI: high pathogenic avian influenza).
Figure 2. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in PBS along with the linear regression curve and for better understanding, D(T) is also given on the right Y-axis in a logarithmic scale. (LPAI: low pathogenic avian influenza, HPAI: high pathogenic avian influenza).
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Figure 3. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in allantoic fluid along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
Figure 3. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in allantoic fluid along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
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Figure 4. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in cell culture medium along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
Figure 4. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in cell culture medium along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
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Figure 5. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data on surfaces along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
Figure 5. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data on surfaces along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
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Figure 6. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in chicken meat along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
Figure 6. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in chicken meat along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
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Figure 7. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in homogenized whole egg along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
Figure 7. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in homogenized whole egg along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
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Figure 8. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in dried egg white along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
Figure 8. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in dried egg white along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
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Figure 9. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in plain, sugared, salted and fortified egg yolk along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
Figure 9. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in plain, sugared, salted and fortified egg yolk along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
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Figure 10. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in in fat free egg and egg substitutes along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
Figure 10. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in in fat free egg and egg substitutes along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
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Figure 11. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in manure, litter and feces along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
Figure 11. Correlation between 1/T and log(D(T)) for all published influenza virus thermal inactivation data in manure, litter and feces along with the linear regression curve. For better understanding, D(T) is also given on the right Y-axis in a logarithmic scale.
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Table
Table 1. Overview of published influenza virus thermal inactivation experiments with virus (sub-type), medium and determined decimal reduction time D(T). (* experiments were not included in the quantitative analysis. PBS: phosphate buffered saline, MEM: minimal essential medium, DMEM: Dulbecco’s Modified Eagle’s Medium, RH: relative humidity).
Table 1. Overview of published influenza virus thermal inactivation experiments with virus (sub-type), medium and determined decimal reduction time D(T). (* experiments were not included in the quantitative analysis. PBS: phosphate buffered saline, MEM: minimal essential medium, DMEM: Dulbecco’s Modified Eagle’s Medium, RH: relative humidity).
VirusTemperature [°C]D [min]Sample MediumRemarkReference
in PBS
H1N1, A/Puerto Rico/8/34, human56 PBSsuccessful inactivation but no quantification possible *[33]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)5512.0PBS [18]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)574.80PBS [18]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)582.30PBS [18]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)591.30PBS [18]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)611.00PBS [18]
H7N1, A, avian (HPAI)70<1.05PBSlower detection limit reached; no quantification possible *[34]
H7N1, A, avian (HPAI)100<1.53PBSlower detection limit reached; no quantification possible *[34]
H7N2, A/chicken/New York/13142/94, avian (LPAI)5321.7PBS [18]
H7N2, A/chicken/New York/13142/94, avian (LPAI)552.80PBS [18]
H7N2, A/chicken/New York/13142/94, avian (LPAI)572.30PBS [18]
H7N2, A/chicken/New York/13142/94, avian (LPAI)581.20PBS [18]
H7N2, A/chicken/New York/13142/94, avian (LPAI)591.10PBS [18]
H7N2, A/chicken/New York/13142/94, avian (LPAI)610.80PBS [18]
H9N2, A, avian (LPAI)60 PBSsuccessful inactivation but no quantification possible *[35]
in allantoic fluid
H1N1, A/California/07/2009, human5038.46allantoic fluid (assumed) [36]
H1N1, A/Beijing/HZ01/2013, human5025.00allantoic fluid (assumed) [36]
H1N1, A/Puerto Rico/8/34, human5027.78allantoic fluid (assumed) [36]
H1N1, A/Texas/1/85, human542.31allantoic fluid (assumed) [37]
A/Mel (prob. H1N1, A/Melbourne/35), human56 allantoic fluidsuccessful inactivation but no quantification possible *[38]
A/WSN (prob. H1N1, A/WSN/33), human56 allantoic fluidsuccessful inactivation but no quantification possible *[38]
H3N2, A/Aichi/2/84, human564.40allantoic fluid [12]
H5N1, A/chicken/Chonburi/Thailand/CU-7/04, avian556.74allantoic fluid (assumed) [39]
H5N1, A/chicken/Chonburi/Thailand/CU-7/04, avian606.29allantoic fluid (assumed) [39]
H5N1, A/chicken/NakornPatom/Thailand/CU-K2/2004605.15allantoic fluid (assumed) [39]
H5N1, A/chicken/NakornPatom/Thailand/CU-K2/2004, avian652.34allantoic fluid (assumed) [39]
H5N1, A/chicken/Ratchaburi/Thailand/CU-68/04, avian554.55allantoic fluid (assumed) [39]
H5N1, A/chicken/Ratchaburi/Thailand/CU-68/04, avian601.89allantoic fluid (assumed) [39]
fowl plaque virus (probably H5N1, A/turkey/Ontario/6213/1966), avian563.57allantoic fluid [40]
H7N9, A/Anhui/1/2013, avian561.69allantoic fluid [17]
H7N9, A/Anhui/1/2013, avian650.97allantoic fluid [17]
H7N9, A/Shanghai/1/2013, avian561.95allantoic fluid [17]
H7N9, A/Shanghai/1/2013, avian650.97allantoic fluid [17]
H7N9, A/Anhui/1/2013, (human)5045.45allantoic fluid (assumed) [36]
H9N2, A/chicken/Nanjing/1/2013, avian5026.32allantoic fluid (assumed) [36]
H9N2, A/turkey/Wisconsin/1966, avian56<81.8allantoic fluidlower detection limit reached; no quantification possible *[41]
different influenza A strains54 allantoic fluid/PBSsuccessful inactivation but no quantification possible *[42]
B/Lee, human5015.00allantoic fluidrough estimation[11]
B/Lee, human527.50allantoic fluidrough estimation[11]
B/Lee, human543.75allantoic fluidrough estimation[11]
in cell culture medium
H1N1, A/Netherlands/266/2008, human5613.10DMEM [43]
H1N1, A/Netherlands/266/2008, human730.53DMEM [43]
H1N1, A/NWS/33 (ATCC VR-219), human700.82DMEM [14]
H1N1, A/NWS/33 (ATCC VR-219), human800.73DMEM [14]
H1N1, A/NWS/33 (ATCC VR-219), human90<0.162DMEMlower detection limit reached; no quantification possible *[14]
H1N1, A/Puerto Rico/8/34, human703.33MEM droplets [16]
H1N1, A/Puerto Rico/8/34, human801.23MEM droplets [16]
H1N1, A/Puerto Rico/8/34, human900.69MEM droplets [16]
H1N1, A/Puerto Rico/8/34, human1000.50MEM droplets [16]
H1N1, A/Puerto Rico/8/34, human1100.25MEM droplets [16]
H1N1, A/SW/Sk/02, swine55 MEMsuccessful inactivation but no quantification possible *[44]
H3N2, A/Bangkok/1/1979/, human4532894.74DMEM (assumed)results orders of magnitude above typical results; not included in analysis *[45]
H3N2, A/Bangkok/1/1979/, human5013419.22DMEM (assumed)results orders of magnitude above typical results; not included in analysis *[45]
H3N2, A/Bangkok/1/1979/, human559661.84DMEM (assumed)results orders of magnitude above typical results; not included in analysis *[45]
H3N2, A/Bangkok/1/1979/, human603344.48DMEM (assumed)results orders of magnitude above typical results; not included in analysis *[45]
H3N2, A/Wisconsin/67/2005, human70 DMEMsuccessful inactivation but no quantification possible *[46]
H7N3, A/Mallard/NL/12/00, avian (LPAI)70 DMEMsuccessful inactivation but no quantification possible *[46]
H7N7, A/FPV/Bratislava/79, avian508.33MEM [15]
H7N7, A/FPV/Bratislava/79, avian553.70MEM [15]
H7N7, A/FPV/Bratislava/79, avian580.75MEM [15]
H7N7, A/FPV/Bratislava/79, avian600.53MEM [15]
H7N7, A/FPV/Bratislava/79, avian630.38MEM [15]
in other liquids
H1N1, A/NWS/33, human586.71liquid (blood plasma) [47]
H5N1, A/NIBRG-14, human58 liquid (blood plasma)successful inactivation but no quantification possible *[48]
H5N1, A, avian (HPAI)56 peptone watersuccessful inactivation but no quantification possible *[49]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)56 different mediasuccessful inactivation but no quantification possible *[50]
H5N9, A/turkey/Wisconsin/68, avian (LPAI)56 different mediasuccessful inactivation but no quantification possible *[50]
H7N3, A, avian56 peptone watersuccessful inactivation but no quantification possible *[51]
H9N2, A/turkey/Wisconsin/66, avian (LPAI)56 different mediasuccessful inactivation but no quantification possible *[50]
on surfaces
H1N1, A/Puerto Rico/8/34, human5516.67stainless steel (surface) RH 25% [52]
H1N1, A/Puerto Rico/8/34, human555.17stainless steel (surface) RH 50% [52]
H1N1, A/Puerto Rico/8/34, human55<3.41stainless steel (surface) RH 75%successful inactivation but no quantification possible *[52]
H1N1, A/Puerto Rico/8/34, human6012.50stainless steel (surface) RH 25% [52]
H1N1, A/Puerto Rico/8/34, human603.66stainless steel (surface) RH 50% [52]
H1N1, A/Puerto Rico/8/34, human60<2.88stainless steel (surface) RH 75%successful inactivation but no quantification possible *[52]
H1N1, A/Puerto Rico/8/34, human658.33stainless steel (surface) RH 25% [52]
H1N1, A/Puerto Rico/8/34, human65<2.94stainless steel (surface) RH 50%successful inactivation but no quantification possible *[52]
H1N1, A/Puerto Rico/8/34, human65<6.12different filtering facepiece materials (RH 85%)lower detection limit reached; no quantification possible *[22]
H1N1, A/WSN/331050.02surface (steel, polypropylen, cotton) [53]
H3N2, A/Wisconsin/67/2005 (recombinant), human (?)727.50droplets on filter material [54]
H3N2, A/Wisconsin/67/2005 (recombinant), human (?)82<6.98droplets on filter materialsuccessful inactivation but no quantification possible *[54]
H3N2, A/recombinant strain, human (?)81<7.7towel/filtering facepiece materiallower detection limit reached; no quantification possible *[55]
H5N1, A, avian (LPAI)65<4.316 different filtering facepiece materials (RH > 60%)lower detection limit reached; no quantification possible *[56]
in chicken meat
H5N1, A/chicken/Korea/ES/2003, avian (HPAI)573.98chicken thigh meat [57]
H5N1, A/chicken/Korea/ES/2003, avian (HPAI)574.48chicken breast meat [57]
H5N1, A/chicken/Korea/ES/2003, avian (HPAI)582.17chicken thigh meat [57]
H5N1, A/chicken/Korea/ES/2003, avian (HPAI)582.56chicken breast meat [57]
H5N1, A/chicken/Korea/ES/2003, avian (HPAI)591.35chicken thigh meat [57]
H5N1, A/chicken/Korea/ES/2003, avian (HPAI)591.27chicken breast meat [57]
H5N1, A/chicken/Korea/ES/2003, avian (HPAI)600.99chicken thigh meat [57]
H5N1, A/chicken/Korea/ES/2003, avian (HPAI)601.18chicken breast meat [57]
H5N1, A/chicken/Korea/ES/2003, avian (HPAI)610.48chicken thigh meat [57]
H5N1, A/chicken/Korea/ES/2003, avian (HPAI)610.57chicken breast meat [57]
H5N1, A/chicken/Korea/ES/2003, avian (HPAI)572.31breast meat [58]
H5N1, A/chicken/Korea/ES/2003, avian (HPAI)30-70 thigh and breast meatsuccessful inactivation but no quantification possible *[59]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)572.92breast meat [58]
H5N2, A/chicken/Texas/298313/2004, avian (LPAI)572.39breast meat [58]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)574.46chicken meat [58]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)582.36chicken meat [58]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)591.36chicken meat [58]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)601.06chicken meat [58]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)610.39chicken meat [58]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)65 thigh and breast meatsuccessful inactivation but no quantification possible *[59]
H7N7, A/FPV/Bratislava/79, avian5010.71chicken meat suspension [15]
H7N7, A/FPV/Bratislava/79, avian553.33chicken meat suspension [15]
H7N7, A/FPV/Bratislava/79, avian581.30chicken meat suspension [15]
H7N7, A/FPV/Bratislava/79, avian600.48chicken meat suspension [15]
H7N7, A/FPV/Bratislava/79, avian630.32chicken meat suspension [15]
in egg products
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)5510.73homogenized whole egg [21]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)574.48homogenized whole egg [21]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)590.37homogenized whole egg [21]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)600.56homogenized whole egg [19]
H7N2, A/chicken/New York/13142-5/94, avian (LPAI)556.69homogenized whole egg [21]
H7N2, A/chicken/New York/13142-5/94, avian (LPAI)572.25homogenized whole egg [21]
H7N2, A/chicken/New York/13142-5/94, avian (LPAI)590.36homogenized whole egg [21]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)554.28liquid egg white [21]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)570.38liquid egg white [21]
H7N2, A/chicken/New York/13142-5/94, avian (LPAI)556.60liquid egg white [21]
H7N2, A/chicken/New York/13142-5/94, avian (LPAI)570.36liquid egg white [21]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)553168.00dried egg white [21]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)572016.00dried egg white [21]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)591872.00dried egg white [21]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)611440.00dried egg white [21]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)63288.00dried egg white [21]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)54.4400.60dried egg white [60]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)60160.70dried egg white [60]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)65.5109.40dried egg white [60]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)71.143.70dried egg white [60]
H7N2, A/chicken/New York/13142-5/94, avian (LPAI)55720.00dried egg white [21]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)62.20.05sugared egg yolk [19]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)63.30.02sugared egg yolk [19]
H7N2, A/chicken/New York/13142/94, avian (LPAI)561.10sugared egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)570.53sugared egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)580.44sugared egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)590.39sugared egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)600.33sugared egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)610.31sugared egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)62.20.23sugared egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)63.30.13sugared egg yolk [20]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)61.10.23fortified egg yolk [19]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)62.20.14fortified egg yolk [19]
H7N2, A/chicken/New York/13142/94, avian (LPAI)570.91fortified egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)580.61fortified egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)590.47fortified egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)600.38fortified egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)61.10.13fortified egg yolk [20]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)550.34salted egg yolk [21]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)62.20.06salted egg yolk [19]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)63.30.04salted egg yolk [19]
H7N2, A/chicken/New York/13142/94, avian (LPAI)580.86salted egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)590.66salted egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)600.60salted egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)610.58salted egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)62.20.50salted egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)63.30.38salted egg yolk [20]
H7N2, A/chicken/New York/13142-5/94, avian (LPAI)550.68salted egg yolk [21]
H7N2, A/chicken/New York/13142-5/94, avian (LPAI)570.37salted egg yolk [21]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)600.06plain egg yolk [19]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)61.10.03plain egg yolk [19]
H7N2, A/chicken/New York/13142/94, avian (LPAI)571.52plain egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)581.32plain egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)591.28plain egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)600.73plain egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)61.10.67plain egg yolk [20]
H7N2, A/chicken/New York/13142/94, avian (LPAI)620.59plain egg yolk [20]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)5518.60fat free egg product [61]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)568.50fat free egg product [61]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)56.73.60fat free egg product [61]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)572.50fat free egg product [61]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)57.71.10fat free egg product [61]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)580.40fat free egg product [61]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)590.40fat free egg product [61]
H7N2, A/chicken/New York/13142/94, avian (LPAI)552.90fat free egg product [61]
H7N2, A/chicken/New York/13142/94, avian (LPAI)56.71.00fat free egg product [61]
H7N2, A/chicken/New York/13142/94, avian (LPAI)570.80fat free egg product [61]
H7N2, A/chicken/New York/13142/94, avian (LPAI)57.70.72fat free egg product [61]
H7N2, A/chicken/New York/13142/94, avian (LPAI)580.60fat free egg product [61]
H7N2, A/chicken/New York/13142/94, avian (LPAI)590.50fat free egg product [61]
H7N2, A/chicken/New York/13142/94, avian (LPAI)610.40fat free egg product [61]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)56.75.60egg substitute [19]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)57.72.30egg substitute [19]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)590.75egg substitute [19]
in waste
H5N1, A/Thai field strain, avian40 chicken manuresuccessful inactivation but no quantification possible *[62]
H5N1, A/chicken/Sikkim/151466/2008, avian (HPAI)421363.64dry poultry faeces [63]
H5N1, A/chicken/Sikkim/151466/2008, avian (HPAI)421333.33wet poultry faeces [63]
H5N1, rgA/gyrfalcon/WA/41088/2014xPR8, avian (LPAI)43.3 littersuccessful inactivation but no quantification possible *[64]
H5N1, A/duck/Egypt/VRLCU-R28/2012, avian (HPAI)56 littersuccessful inactivation but no quantification possible *[65]
H7N1, A/turkey/Italy/4580/1999, avian (HPAI)43.3 littersuccessful inactivation but no quantification possible *[64]
H7N2, A/chicken/PA/3972-1/97, avian565.15chicken manure [66]
H7N2, A/chicken/PA/3972-1/97, avian600.61chicken manure [66]
H7N2, A/chicken/PA/3972-2/97, avian568.06chicken manure [66]
H7N2, A/chicken/PA/3972-2/97, avian601.48chicken manure [66]
H7N2, A/chicken/PA/3779-1/97, avian568.06chicken manure [66]
H7N2, A/chicken/PA/3779-1/97, avian601.48chicken manure [66]
H7N2, A/chicken/PA/3779-2/97, avian568.63chicken manure [66]
H7N2, A/chicken/PA/3779-2/97, avian601.79chicken manure [66]
swine influenza5029.41liquid manure [13]
swine influenza5511.76liquid manure [13]
H5N2, A/chicken/Pennsylvania/1370/83, avian (HPAI)>40 compostsuccessful inactivation but no quantification possible *[67]
H6N2, A/turkey/Mass/3740/6550–65 compost (different consistence)successful inactivation but no quantification possible *[68]
H7N1, A/turkey/Italy/1387/00, avian (HPAI)458.33compost [69]
H7N1, A/turkey/Italy/1387/00, avian (HPAI)454.20compost (different consistence) [70]
H7N1, A/turkey/Italy/1387/00, avian (HPAI)457.20compost (different consistence) [70]
H7N1, A/turkey/Italy/1387/00, avian (HPAI)552.40compost (different consistence) [70]
H7N1, A/turkey/Italy/1387/00, avian (HPAI)552.50compost (different consistence) [70]
Table
Table 2. Expected decimal reduction times in minutes for different temperatures and media, determined using the previously determined equations for decimal reduction times.
Table 2. Expected decimal reduction times in minutes for different temperatures and media, determined using the previously determined equations for decimal reduction times.
MediumTemperature [°C]
50556065707580
“all liquids”6.44.32.851.931.320.910.64
PBS49.96.91.020.1580.0260.0050.001
allantoic fluid17.26.52.521.0070.4140.1740.075
cell culture medium3.22.51.961.5541.2410.9970.806
surfaces35.116.98.314.1752.1411.1190.596
chicken meat22.74.60.980.2170.0500.0120.003
homog. whole egg318.39.80.340.0130.001<0.001<0.001
dried egg white42121454518190.572.0728.0411.21
egg yolk5.51.30.330.0870.0240.0070.002
fat free egg166.07.00.330.0170.001<0.001<0.001
manure/litter58.59.01.470.2510.0450.0090.002
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Hessling, M.; Fehler, N.; Gierke, A.-M.; Sicks, B.; Vatter, P. Heat Inactivation of Influenza Viruses—Analysis of Published Data and Estimations for Required Decimal Reduction Times for Different Temperatures and Media. Microbiol. Res. 2022, 13, 853-871. https://doi.org/10.3390/microbiolres13040060

AMA Style

Hessling M, Fehler N, Gierke A-M, Sicks B, Vatter P. Heat Inactivation of Influenza Viruses—Analysis of Published Data and Estimations for Required Decimal Reduction Times for Different Temperatures and Media. Microbiology Research. 2022; 13(4):853-871. https://doi.org/10.3390/microbiolres13040060

Chicago/Turabian Style

Hessling, Martin, Nicole Fehler, Anna-Maria Gierke, Ben Sicks, and Petra Vatter. 2022. "Heat Inactivation of Influenza Viruses—Analysis of Published Data and Estimations for Required Decimal Reduction Times for Different Temperatures and Media" Microbiology Research 13, no. 4: 853-871. https://doi.org/10.3390/microbiolres13040060

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