Fluid milk shelf life – from hours to months
Petr Dejmek
Dept of Food Technology, Engineering and Nutrition, Lund University,
Box 124, S-221 00, Lund, Sweden
Tel +46 46 2229810, fax +46 46 2224622, mail Petr.Dejmek@food.lth.se
Abstract
The development of shelf life of liquid milk and the scientific background of the problem and the technical solutions utilized are followed in a historical perspective. It is concluded that the general increase in affluence of the society and the general improvement of the engineering competence contributed most to the observed increase of fluid milk shelf life.
At a first glance, one can be overwhelmed by the spectacular increase of the shelf life of fluid milk. Sixty years ago, a substantial part of fluid milk was distributed, even in the developed countries, in bulk to retailers and sold over the counter. Such milk had a shelf life of hours and would be boiled in the household to keep until the evening, or overnight. Currently shelf life is counted in weeks and months, Fig 1. The problems caused by short shelf life are since long forgotten by the consumers , and freshness rather than functionality seems to be gaining prominence, so that the average shelf life on the market might be decreasing again.
Milk at ambient temperatures is a selective substrate for lactic acid bacteria and these are always present in the environment. Thus milk sours “spontaneously” and the presence of lactic acid effectively limits the growth of other organisms, apart from some yeasts. No

common seriously pathogenic organisms thrive in sour milk. In the Nordic countries, skim milk would be collected throughout the summer season in a large vessel and kept for use over winter - the Icelandic skyr is a vestige of this traditional milk storage system. While the nutritional value of milk was kept intact, the taste was not to everybody’s liking. This is graphically depicted in an Icelandic tale from the Middle Ages, Egil Skallagrimsons saga.
Egil, a famous Icelandic poet and warrior, came uninvited to a Swedish farm, and was treated with milk. Hungry, he gorged himself, but when he later found out that there was meat to be had, he nearly killed the unfortunate farmer
Today fermented milks are considered a product completely separate from liquid milk, and from consumer perspective, detectable taste or structure changes to milk limit its shelf life.
These are most often caused by the metabolites of growing microorganisms. Nonbacterial changes in the chemistry of milk are mostly caused by oxidation or indigenous enzymes of milk. Physical instability presents an interesting development. As long as milk fat was a most cherished milk component, creaming was not a limitation to shelf life. It was actively promoted, and a large body of research was generated in the search of a thick and distinct creamline. Nowadays, creaming is barely tolerated. Sediment, on the other hand has always been a shelf life limiting product fault.
Apart from the changes observable by the consumer, shelf life may be limited by legislation.
Many countries impose, in addition to health related criteria, arbitrary limits on some aspect of milk microflora, typically a maximum CFU count using some officially promulgated procedure.

The current view of milk shelf life can be summarized as follows (Walstra, Wouters and
Geurts, 2006):
Pasteurized milk can be spoiled by psychrotrophic recontamination, or if that is largely avoided, by pasteurization surviving spores. Its maximum shelf life will depend on the temperature in the storage chain, from a few days where storage temperatures of 12°C are legal, to beyond three and up to six weeks at temperatures close to milk freezing point. The shelf life of sterilized milk is less clearly defined, as no easily detectable bacterial growth occurs. Taste deterioration is governed again by storage temperature, being 3 to 6 months in ambient temperature in moderate climates, and by the presence of heat treatment surviving lytic bacterial enzymes. After monthlong storage at moderate temperatures UHT milk may gel as a late effect of proteolytic activity Some formation of a bottom sediment occurs. Oxidation is usually avoided, but Maillard reactions may become prominent at tropical storage temperatures.
The early scientific understanding of milk shelf life
As so often in food science, practical solutions are often found to problems for which causes are not understood. Famously, canning, invented by Nicholas Appert in 1804, produced long life food, even if Appert the whole of his life firmly believed that it was the exclusion of air that caused the success of his method. Similarly in milk. It was found that evaporation concentrated canned milk will keep well. Gail Borden, with only one year of formal schooling, experimented with ways to concentrate and can milk, obtained US patent for his vacuum evaporation of milk in 1856 (Borden 1856), and went on to become a household name. In his patent application , Borden mentions that “scalding milk to improve its preservative qualities has long been known”. The Swiss pediatrician Henri Nestle

independently experimented with ways of providing safe food for infants, and his factory for condensed milk in Cham started in 1866.
Bacteria as a cause of milk souring was proposed as early as 1844. Nevertheless, in the early days of scientific inquiry into milk, the attribution of milk souring to microorganisms was for a long time in doubt. Due to the almost unavoidable contamination of milk with lactic bacteria, it was believed that souring of milk is a milk inherent reaction, similar to fruit ripening, in
Borden’s words “ milk is a living fluid, and as soon as drawn from the cow begins to die, change and decompose”. It was only when Joseph Lister about 1874 succeeded in drawing sterile milk from the udder and isolated “Bacterium Lactis” (Lactococcus lactis subsp lactis) 1 that the argument was finally settled (Ford, 1928).
Louis Pasteur is usually credited for the general idea of microorganisms as the cause of spoilage, and the use of moderately high temperatures for the inactivation of microorganisms, based on his research on spoilage of wine around 1860-1865 (P.F.F,.1898). There is no known evidence that Pasteur applied his method to milk The use of Pasteur’s name could have originated as a marketing gimmick to capitalize on Pasteur’s fame. The first mention of pasteurization in English is rather late, 1886, in The Times.
In the later part of the nineteenth century tremendous progress was achieved in general, medical and even dairy bacteriology. The basic science based strategies to increase milk shelf life – to avoid contamination, to inactivate, to keep temperatures low - were well established long before the turn of the 20 th century. The existence of spores was also known by then, and it was well known that temperatures above atmospheric boiling point of water are needed to inactivate them, as seen in a few sentences from a lecture reported in Science 1890, Fig 2.

Even the the basic chemistry of non-bacterial milk deterioration had proceeded fairly far by then. In 1897 Russel and Babcock (of Babcock test fame) found that noncontaminated milk contains an enzyme which degrades caseins, this proteolytic milk indigenous enzyme was named “galactase”. Encyclopedia Britannica 1911. Similarly an indigenous lipase was demonstrated by Moro in 1902. Even oxidation was studied, and the effect of light as a prooxidant was shown by Hanuš in 1899. Further development occurred in the thirties. Heat stability of milk lipase was studied by Nair, 1930. The effect of milk fat globule membrane damage on lipolysis was determined by Dorner and Widmer in 1931, the effect of copper and iron on autoxidation by Guthrie et al in 1931, and the effect of deareation by Dahle and
Palmer in 1937. The basic mechanism of the chain reaction in autooxidation was explained in
1943 by Farmer and Sutton, and the prooxidant role of riboflavin by Patton and Josephson in
1953. (Josephson 1954)
.
History of milk heat treatment
Heat treatment is the basis, or an important part, of all current shelf life improving methods.
Commercial heat treatment of liquid milk is well over 100 years old. In Paris, heat treated milk was apparently sold in 1875 (Jensen, 1950).
Before the advent of refrigeration and mechanized transport, the market for liquid milk was limited to farms in the immediate neighborhood of cities. Milk was used primarily for butter production, and skim milk returned to farms as feed. It was the shelf life improvement of this milk by heating (from 12 to 36h at room temperature, according to a Danish experimental dairy report from 1883) that gave impetus to the fast spread of pasteurization in Europe. Only

later the health implications (for the health of the cow herd, not the consumer!) were understood.
Some European countries legislated obligatory heat treatment of milk used for calf feeding, to contain bovine tuberculosis (Germany 1894, Denmark 1898). The commercial advantage of increased shelf life at a small increase of handling costs then led to a rapid introduction of milk heat treatment in the cities of Europe. In Sweden 60% of dairies delivered pasteurized milk in 1896. The adoption of heat treatment in USA was much slower, and highly controversial, with only 25% of dairies pasteurizing in 1905. There was a widely held belief that treating milk was unnatural and destroyed some of its essential “goodness” and unheated
“certified milk” produced under official supervision and inspection a better alternative.
Sterilized milk was produced commercially in the Netherlands already in 1889, and in
Germany and Britain in 1894 and was popular with the customers despite its significantly different appearance and taste (Davies, 1950).
Process and equipment for milk treatment
A profusion of heat treatment equipment was developed and used, a plethora of heating times and temperature combinations existed. Continuous heaters appeared as early as 1882, in connection with continuous centrifugation, but the distribution of residence times was poorly understood and controlled. Gradually, in the early twentieth century, continuous systems lost favor and batchwise heating and heating of retail containers became the rule, as a consequence of public health concerns about the reliability of the operation of continuous

systems. Public authorities intervened to impose obligatory rules for times, temperatures and processing conditions. Later, the pendulum swung, first towards a semi-continuous, so called
“holder” pasteurization. In true batch pasteurizer, the milk was heated and cooled in a vat. In holder pasteurizer, milk was continuously heated and pumped to a vat, and after specified holding time, typically 30 minutes, pumped out and cooled. The acceptance of true continuous pasteurization, “High Temperature Short Time”, HTST despite its much lower costs varied between countries, in Great Britain continuous pasteurization remained illegal until 1941 (Davies, 1950).
In most countries, multiple pasteurization of milk for public consumption is not allowed. A subpasteurization treatment, thermizaton at 65
C
for 20s ahead of the final thermal treatment had been introduced by Stadhouders in 1962 and caused an average shelf life increase of a few days . In 1970 Martin and Blackwood found that thermization led to partial spore germination (Blackwood and Martin 1972).
Already the very early milk treatment equipment could be surprisingly modern. So in 1912
Tödt’s Momentanerhitzer, Fig 3, which let milk under pressure pass a narrow channel, heated from both sides with steam, could achieve 130-140C with a residence time of 5-30 sec. In the same year, Lobeck’s Biorizer, Fig 4, sprayed milk into a steam filled chamber. Several designs of double tube heat exchangers for milk, Fig 5, were developed in the early 20 th century (Stassano, Montana, Nielsen) and heat regeneration was widely used in them, in particular as the energy costs increased during the first world war (Weigmann, 1932). In 1923
Seligman’s APV, Aluminium Plant and Vessel Company introduced the plate heat exchanger but seemed to meet skepsis from health authorities - in Denmark, while in common use for other duties in dairies, plate heat exchangers were permitted for consumer milk pasteurization

first in 1939 (Jensen, 1950). The basic design of Gaulin’s high pressure homogenizer of 1904 survived with small changes until today. It’s adoption to treat milk before in bottle sterilization was described (Davies, 1950) as a heaven-sent improvement which eliminated
“the objectionable glue-like gelatinous mass of butterfat on the neck of the bottle”. The patent application for injection heating followed by flash cooling was filed in 1924 (Grinrod
1929). Wonderful Heath Robinson machines for automatic temperature control (boiling alcohol displacing mercury and the weight of mercury switching a valve) were invented at the turn of the century, however, automatic temperature control began to be generally used in the early 30ies. Stainless steel was introduced in plate heat exchangers just before the second world war, and the material began to be widely used in dairies first after the war, in neutral
Sweden with its own steel industry somewhat earlier.
Apart from the classical heating methods, ohmic heating achieved limited success in some markets, and ohmic milk heaters are still being produced. The argument for ohmic heaters is based on the fact that there need not be any surface hotter than the nominal heating temperature.
Microwave heating was attempted in an ingenious concept by a Swedish startup company,
AlfaStar (1986-1996). It tried to use microwave heating of filled and sealed milk packages, and to compensate for the poor penetration depth of microwaves, the packages were flattened for the treatment and later folded back to rectangular shape. However, the attempt failed, it is unclear whether for technical or commercial reasons.
UHT

While milk pasteurization and its equipment have not seen a major change during the last fifty years, there has been a significant development in the production of sterile milk. It was for a long time fairly obvious that inactivation of spores has a steeper dependence on temperature than the taste affecting chemical reactions in milk, and thus that a high temperature, short time treatment would be beneficial. The technical difficulty of reliably achieving a defined residence time shorter than a few second led to an “optimal” temperature range around 140
C
.
This approach received the name Ultra High Temperature treatment, UHT, in an analogy to the HTST flow pasteurization. The problem of UHT was that with hot filling, the packages could not be cooled fast enough, and with cold filling, the sterility could not be guaranteed.
In the current perspective, UHT milk is the obvious flag-bearer of the long shelf life milk concept. A kind of UHT product existed since at least 1951, when preheated milk was filled in cans and sterilized by the Dole process at 220
C
for 45s , but the origins of UHT are traditionally connected with the Uperization process developed by Sulzer Brothers and Alpura
( later taken over by APV) and the TetraPak sterile carton filler which went commercial at
Verbandsmolkerei in Bern, Switzerland in 1961 (Burton H 1967a, b).
From what has been shown earlier it should be clear that the high temperature heating process and the equipment to perform it was just another step in the evolution of more sophisticated and better controlled heat processing lines. Such lines had been commonly used to pretreat milk destined for in bottle or in can sterilization, in fact the Bern plant was originally built with a can filler and a Dole can sterilizing process. All other major equipment manufacturers developed their own variants of the UHT processing line within a few years, either of the same direct steam injection type (Cherry Burrell, Alfa Laval), of steam infusion type, akin to the above mentioned Biorizer (Laguillharre, Breil&Martel, Paasch&Silkeborg,

DASI), or with indirect heating (Alfa Laval, APV, Cherry-Burrell, Ahlborn, Sordi, Storck ),
Anonymous 1967, Burton 1967c,d,e,f,g, Krebs 1975 .
In the same way, filler designs had gradually evolved towards more reliable hygienic standards by painstaking focus on detail, be it foaming in the filler, cleanability of the enclosure, overpressure, cleaning procedures and so on. If a single breakthrough should be singled out in UHT milk development, it would probably be the use of hydrogen peroxide to achieve a reliable sterility of the packaging material in the TetraPak aseptic filler which remained the dominant aseptic filler for a long time. The basic concept of wetting the packaging material with a hydrogen peroxide solution and drying it off again remains the dominant sterilization technique for packages which are not sterile produced onsite.
Plastic based sterile packaging appeared first with Prepack’s plastic pouch in 1964 and some ten years later with Formseal’s deep drawn cup and Remy’s blow moulded bottle. The light and oxygen barrier properties of the plastic packages have only slowly improved to match the five-ply sterile carton which, in contrast to the carton used for pasteurized milk, from the very beginning included the impermeable aluminium layer.
The need for longer shelf life of milk was not acutely felt in the US, with its much better developed refrigeration system and common 3 week shelf life of pasteurized milk,. It took twenty years before the first commercial UHT plant appeared. There is a surprising analogy with the slow acceptance of pasteurization.
With the microbial growth eliminated, there was a renewed surge of interest in the reasons why UHT milk would not keep indefinitely. Heat stable bacterial proteases were identified by
Mayerhofer, Marshall, White, & Lu, (1973) and heat stable lipases by Driessen &

Stadhouders,1974. A new indigenous proteolytic enzyme,Cathepsin D, was identified by
Kaminogawa&Yamauchi 1972 and the role of plasmin, plasminogen, and their inhibitor/activator systems clarified in the early 80ies (Grufferty&Fox,1988, Kelly &
McSweeney, 2003).
The gelation of UHT mik on prolonged storage at moderate ambient temperature was ascribed to plasmin, (De Koning, Kaper, Rollema & Driessen 1985), but the cause of the variation in sediment formation has yet not been conclusively determined.
Further technical developments appeared in the specific configuration of the final heating device and in the choice and detail of package and enclosure sterilizing, but these have much less effect on shelf life than the time temperature profile chosen, and the storage temperature .From the technical point of view, there is no principal difference between a UHT plant and a plant designed for the production of extended shelf life milk (Rysstad & Kolstad
2006).
Nonthermal methods of bacteria inactivation
Numerous nonthermal ways of containing the microbially caused deterioration of milk have been invented and sometimes also applied. Many chemical disinfectants were developed for medical use in late nineteenth century, and practically all of them have also been tested in milk
Formaldehyde was an early favourite. In USA, Britain and Germany it was sold, mixed with sugar, as a branded milk preserving additive, “freezine” “milk sweet” and played a role of an alternative in USA in the heated discussion on pasteurization. Hydrogen peroxide was

proposed and investigated by Schrodt 1883, and was temporarily allowed for use in dairies in
Germany during the first world war. In general, German law forbade all disinfectants in milk as early as 1879, (Weigman 1932), but in US, hydrogen peroxide (followed by catalase continues to be an allowed additive for cheese milk. In renewed interest for highly reactive species, hydrogen peroxide, this time in conjunction with the lactoperoxidase thiocyanate briefly occurred in the 1970ies, Björck, Rosén, Marshall & Reiter 1975. The effects of carbon dioxide on bacteria was studied already by Pasteur, according to an extensive review of its effects (Valley 1928), and proposals to utilize carbon dioxide, attractive not least because it is a natural constituent of fresh milk, reappear every now and than in different guises, and remain an active area of research, most recently as supercritical carbon dioxide, Werner and
Hotchkiss 2006.
High pressure treatment of milk, currently another popular research topic, could recently celebrate a centenary of the original work of Hite,1899. Hite had succeded in prolonging milk shelf life, but the technical difficulties of obtaining the necessary pressures caused that his work was largely forgotten and only reappeared when Japanese researchers teamed up with heavy industry who had the necessary engineering knowhow. Obviously much more is now known about the mechanism of action of high pressure. A few selected applications of high pressure in foods have been a commercial success, among them avocado paste and raw ham, and some dairy applications, e.g. to eliminate yeasts in fermented products, show promise, but in liquid milk the high resistance of spores is a problem.
Radiation of all varieties was a common research topic until later part of the twentieth century, from the work on UV radiation by Ayers in 1910 to post-atomic bomb interest in beta radiation, Brasch 1947. Radiation has been a favoured option for food sterilization by many

for a long time, the German Federal Research Centre for Nutrition and Food in Karlsruhe keeps an updated bibliography of its literature with over 16000 documents at the latest count, but few milk producers would dream of touching the subject. That apart, gamma radiation at spore affecting intensity produces such unacceptable taste that it hardly has been considered as an option, and even UV light is likely to suffer from the same limitation. Intense visible light has been promoted as bactericide, but there is little evidence that it has any other effects than its thermal energy content and its UV-light admixture.
Electric field gradients which cause a potential difference of a few volts across a cell can permeabilize the cell membrane and cause cell death, even for potentials of short duration.
The phenomenon has been much studied since the seventies, Zimmerman, Pilwat & Riemann,
1974 and provides the basis of Dunn & Pearlmann 1897 patent. Just how the permeabilization happens is still not properly understood, Teissie, Golzio & Rols(2005) For use in liquid milk, the high voltage apparatus cost, and the poor effect on spores are the problem.
The removal of bacteria
In contrast to work on bacterial inactivation, surprisingly little has been done in dairy research on bacterial separation with the goal of improving shelf life. Currently, two methods are in commercial use, centrifugation and microfiltration. None of them achieves the count reductions obtainable by pasteurization. For this reason, they are combined with a pasteurization, and their shelf-life improving effect depends on the spore count of the raw milk.
A common problem of both filtration and centrifugation based methods is that they only can treat skim milk. For fat-containing milk the spores in the cream fraction need to be handled by

other methods. A considerable ingenuity has been shown by the companies involved in the configuration of their systems to minimize product losses and heat induced flavors, but some type of an UHT-like treatment is a necessity.
High speed Sharpless centrifuge has been the standard method of recovery for bacteria in bioengineering for almost a century, but given the size considerations and the relatively high density of casein micelles it appeared unlikely that a significant effect in milk could be achieved. The original work was performed in the fifties (Simonart and de Beer, 1953,
Simonart 1962) with the aim of improving milk quality, but it was the specific needs of cheesemaking which led to the eventual adoption of the centrifugation based methods for milk shelf life improvement.
In cheesemaking, spores of Clostridium species can lead to so called late blowing , a serious problem where cheeses during maturation become inflated. The problem was traditionally solved by addition of nitrite to cheese milk, but when public health concerns about nitirite conversion to nitrosamines appeared, an alternative was sought. Heat treatment sufficient to destroy spores is not an alternative, because of the effect on rennettability and cheese quality in general. Spores are rather dense, and therefore centrifugal separation was attempted and proved fairly successful. It was introduced under the trade name bactofugation in the sixties.
The effect of centrifugation on the reduction of microorganisms is rather limited, a few orders of magnitude, but the remaining bacteria can be handled by pasteurization type heat treatment. As an application for improving liquid milk shelf life, centrifugation appeared in the late eighties, and the shelf life increases were not dramatic.
Sterile filtration using dead.end microfilters has been a staple laboratory procedure since the commercial production of filters by Sartorius started in 1927, The smallest bacteria are

several tenths of micrometer in diameter, and thus a nominal pore size of 0.2 micrometer is needed to exclude bacteria completely. However, as anyone with a standard 0.2 micron syringe filter will quickly find out, it is not possible to sterile filter any significant amount of milk. The problem is based on the fact that at least a portion of casein micelles is fairly large, in the same order of magnitude as the filter pore size. Even if the micelles are smaller than the pores, they are sterically excluded from the space close to the pore wall, and milk serum can thus pass the pores faster than the micelles. Therefore casein micelles are concentrated at the entrance to the pore, and will eventually clog it. This is a general phenomenon, (often called concentration polarization) and it hindered the commercial use of filtration techniques for the separation of submicrometer particles until the advent of cross flow techniques. In cross flow filtration, a very large circulation rate tangential to the surface of the filter sweeps away the accumulated material from the pore entrance..
The surprising (van der Horst and Hanemaaijer 1990) findings that in cross flow filtration, realistic separation of bacteria and spores from milk could be achieved seems to have first been made during investigations aimed at assessing microfiltration as an alternative to centrifugal separation of fat at Alfa Laval in the early eighties (Holm, Malmberg and
Svensson 1989). Commercialization of the finding required a considerable effort, not least because of poor reliability and cleanability of polymeric microfiltration membranes and could only be completed after the commercialization of ceramic microfilters, a completely unrelated development, originally a byproduct of the French nuclear research. The first commercial plant producing extended shelf life milk based on microfiltration, at Ault Foods, only came onstream in 1997.
Conclusion

On the relevant, i.e. relative scale, the shelf life improvement of two orders of magnitude, from hours to weeks, is extremely impressive. It has been achieved by milk pasteurization, avoidance of initial contamination and recontamination and by maintenance of the cold chain
Without denigrating the excellent research in applied dairy science it appears that the general affluence of the western societies, which allowed refrigerated distribution and home refrigerators, the small gradual improvements of the technical implementation of milk processing, and focus on attention to detail along the whole chain, from cleaning of the cow’s teats to formal quality control procedures in dairies have contributed more than any research result.
Similarly, the success of UHT treatment and the centrifugation and microfiltration based extended shelf life methods seems to be more a result of improved overall engineering design and capability than of basic new insights and flashes of genius.
Outlook
In comparison to other aspects of milk shelf life, relatively little attention seems to have been paid to sterile extraction of milk and the maintenance of carbon dioxide/oxygen status of raw milk.
Given the explosive growth of biological sciences, it would be surprising if a more complete understanding of the biology of spore germination would not lead to new methods of reliably inducing germination, and thus make sporicidal treatments superfluous.
In the very long perspective, even affinity based separations of pathogens and product spoiling enzymes might become a technically and commercially viable alternative..
In the near perspective, a better understanding of the casein micelle might make it possible to manipulate the micelle size on the technical scale and thereby improve the efficiency of

bacteria separating methods. Centrifugation efficiency is also likely to be improved by the detailed CFD simulations of centrifuge flow patterns which are now feasible.
Acknowledgements
The author, not a shelf life specialist, can not claim to stand on the shoulders of giants.
Perhaps peering between the legs of a crowd is a more fitting description. Far from being a review, this a personal view based on idiosyncratic reading of mostly secondary and tertiary sources and informal contacts within the dairy world during thirty years. Help from Bozena
Malmgren, fellow researcher and TetraPak UHT specialist, Lars Ljung of TetraPak, with a vivid interest in dairy history, and from professor Pieter Walstra is gratefully acknowledged.
As the Chinese saying has it, the merits, if any, of this work should be attributed to the sources, the faults and errors are entirely mine.

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Legends to Figures
Fig 1 Liquid milk shelf life in USA and Europe
Fig 2 Fragments of text from Conn, H.W. 1890 The fermentations of milk and their prevention. Science 17(432) 272-274
Fig 3 Tödt’s Momentanerhitzer, 1912, an early steam heated thin channel heater, (from
Wiegand, 1932).
Fig 4 Lobeck’s Biorizer, 1912, an early steam infusion heater, (from Wiegand, 1932)
Fig 5 Double tube heat exchanger, from the 1925 product catalogue of Aktiebolaget Separator
(later Alfa Laval)

Fig1
ESL
EU
ESL USA
ESL Special
Products USA
Standard pasteurised
EU
Standard pasteurised
USA
UHT

Fig 2

Fig 3

Fig 4
Fig 5