Ice Fishing

Freshly caught fish are one of life’s primeval pleasures. For most inland consumers, however, fish must be preserved before it can be served. It might not be an obvious question, but how is preserving done? And could it be done better?

I fly too frequently, and have left flotsam and jetsam in many countries. Jetsam (items too heavy, bulky or illegal to carry onto the jet) include dull coffee table books given to me as unwanted corporate gifts, bottles of ill-favoured local liqueurs, a clip of 9mm hollow point and, on one tragic occasion, a bone-in Jamon Iberico ham.

In the small hours I worry more about flotsam. Lost shirts, half-remembered shoes, faded group photographs, discontinued bank notes from nations which no longer exist …

Last week I stumbled across a drift of flotsam I had forgotten in a disused office in a small town in a nameless country I last visited 4 years ago. An extra-wide checkered and zippered laundry bag contained a Westin hotel towel (sorry), a kilt in Hogg tartan I am entitled to wear from my father’s family, a hideous silk necktie suitable only for S&M or suicide, and 5 bottles of vintage Balance oil.

As the office was not air-conditioned, the oil had been subjected to 4 winters and summers with temperatures oscillating between 0 and 25 degrees Celsius. For Americans, that is 30 to 80 degrees Fahrenheit.

Having recently watched an episode of Eating History (1), a TV show of sorts featuring two self-publicists who eat expired food, I wondered. The use-by date on the labels clearly stated 02.2020, putting the bottles 4 years and 4 months beyond the pale. Fish oil has a shelf life of 2 years at best, if shielded from heat and light (2). What would the contents taste like?

Anyone who has inadvertently consumed rancid fish oil will take that Proustian sub-madeleine moment to the grave. Mis-quoting Marcel, slightly, “No sooner had the liquid touched my palate than a shudder ran through me and I stopped, intent upon the extraordinary thing that was happening to me”.

I opened a bottle, and sniffed. Nothing. I took a sip, a mouthful, and could not detect any rancidity at all. I continue to drink it on a daily basis.

If you ever left a bottle of mainstream fish oil behind, even in the refrigerator, you know how quickly this stuff goes bad, and how bad it goes. Something about the Balance oil was off, but it was not the oil. And I immediately knew why.

In 2015 I wrote the first paper (3) which outlined the hypothesis that oily fish comprised more than just fish oil, and that the therapeutic effects of a fish (or whale) based diet were due to a combination of the well-known omega 3 PUFA’s and the then less familiar phlorotannins.

To recap, the phlorotannins are marine polyphenols produced by the same cold-water algae, single-cell species and macroalgae / seaweeds, that produce the omega-3 PUFA’s which percolate up through the marine food webs. These fatty acids are fragile molecules, and are very prone to oxidation; EPA has 5 double bonds and DHA has 6.

They do not oxidise inside the algae, however, nor in the food webs up to and including the apex predators, because they are protected by the lipophile and amphiphile phlorotannins that are produced by those same algae (3). The omega 3’s bind to the phlorotannins and are chaperoned by them until an apex predator such as your grandmother consumes a dish of rollmops, and in this way gains dual and highly effective anti-inflammatory therapeutic benefits.

Most and perhaps all life forms in the cold-water marine ecosystem gain similar benefits from the phlorotannins.

Brown and many red and green marine algae depend on the phlorotannins they produce to survive. Algae are exposed to diverse and demanding environmental conditions which cause substantial oxidative and other stresses (4), imperiling the delicate internal membranes of their chloroplasts which are replete with 3-PUFA’s (5). The fact that algae do not self-combust is due to their portfolio of antioxidants, among which the phlorotannins and fucoidans are key players (6, 7).

One step up the trophic ladder is the krill. The ability of many krill species to grow and breed depends on the phlorotannins and omega-3 PUFA’s they ingest as they browse the algae (8).

Progressively higher trophic levels are broadly occupied by fish that eat krill, fish that eat fish and mammals that eat fish; and phlorotannins appear to be good for all of us.

Fish are prone to oxidative and therefore inflammatory stress and disease caused by insults ranging from ammonia nitrogen, the most prevalent environmental limiting factor in aquaculture (9) and a major complication of agricultural run-off (10), to heavy metal pollutants (11), pesticides (12), microplastics (13) and social deprivation (14).

Yes, social deprivation.

Most fish are social creatures and prefer to live in schools and shoals. When isolated, psychological stress causes cortisol release, insulin resistance and increased oxidative and chronic inflammatory stress in the affected animals (14, 15), likely shortening their lifespan. These chemical shifts, which we also experience when stressed, are linked to aggressive behaviour in fish (16) and fisherfolk (17) alike, in yet another reminder of the commonality of life.

Polyphenols such as the phlorotannins reduce oxidative and chronic inflammatory stress (ie 18-21) via metabolic mechanisms which occur in all animals (22), so it is not surprising that many species of fish do better in life when given algae in their feed (23-27).

They do better after death too. Since the phlorotannins were first found to be very good at preventing fish oil from becoming rancid (28), they have increasingly been used by the fish industry to preserve harvested whole fish, fish fillets and food products enriched with fish oil (29, 30).

Top seat at the cold-water trophic table is traditionally occupied by the Inuit. These folk are considered to have significantly larger amounts of brown adipose tissue than others (31), in what is clearly an adaption to low temperatures. Exercise and cold exposure up-regulate brown fat (31, 32), so there is likely a lifestyle component. There appear to be longer-term genetic factors too, involving one or more mutations that may date back to the Denisovans (33).

But there is more. By a remarkable coincidence, high levels of phlorotannins in the traditional Inuit diet conveniently assist the browning of white adipose tissue (34)! Other polyphenols have already been shown to up-regulate the gene ADRB1 (35), which turns white fat to brown (36), and I suspect that phlorotannins do exactly the same thing.

Mysterious ways … And there is still more.

The traditional Inuit diet is crammed with EPA and DHA. They contain in their tissues high levels of those polyunsaturated molecules (37), which, in life forms other than Inuit and herring, confer unhealthy levels of oxidative and cytotoxic stress (38-41). In humans, mainstream fish oil products stripped of their polyphenols, and which therefore produce significant amounts of cytotoxic and arrhythmogenic oxidation breakdown products in vivo, appear to raise the risk of atrial fibrillation (40-42).

The Inuit are not known for their high incidence of atrial disease, presumably because the phlorotannins they co-ingest together with their PUFA’s prevent the formation of harmful omega 3 peroxidation products in their bodies. The lipophile and amphiphile polyphenols they eat keep them from going rancid, just as they kept my superannuated bottles of Balance oil sweet.

Some supporting evidence. After consuming the out-of-date oil for 120 days, a Balance test confirmed that my 6:3 ratio remains at 2.5 and my omega-3 index at 9%.

I maintain that omega-3’s without the right polyphenol chaperones are ineffective at best, toxic at worst (38, 41, 42) and should be avoided. They are like a fish without a bicycle (43). The omega-3’s and the polyphenols work together, and should always be taken together.

Finally, back to preservation.

The biggest problem with frozen fish and other foods is that the freezing process, even flash freezing, produces ice crystals larger than the internal structures of a cell. These are therefore ruptured during freezing process, so when frozen food is thawed there is a characteristic loss of texture and to some extent taste. This is of course made worse by freezer burn.

The problem is elegantly solved by next-gen acoustic freezing (44).

As the temperature in an acoustic freezer falls the food is bathed in specially tuned high energy sound waves that keep water molecules in motion, thus preventing the growth of large ice crystals. Intracellular structures are relatively unscathed, so that when acoustically frozen fish, shrimp and strawberries are thawed, I cannot tell them from fresh.

Cool, futuristic stuff. For a glimpse into the future of food, visit https://5mingourmet.com/.

End-note. We’re getting closer to whole-human reversible cryopreservation, which will likely require acoustic freezing plus the usual cryoprotectants (45). Significant technical problems remain; one might, for example, wake up with Paris Hilton (46).

Disclaimer: Drinking superannuated oil is a personal choice, not a general recommendation.

Next week: shed your skin

References

1. https://play.history.com/shows/eating-history
2. Mozuraityte R, Kristinova V, Standal IB, Carvajal AK, Aursand M. Oxidative Stability and Shelf Life of Fish oil. Chapter 5 in Oxidative Stability and Shelf Life of Foods Containing Oils and Fats. 2016, AOCDS Press, Pages 209-231
3. Clayton PR, Ladi S. From alga to omega; have we reached peak (fish) oil? J R Soc Med. 2015 Sep;108(9):351-7. 
4. Dykens JA, Schick JM, Benoit C, Buettner GR, Winston GW. Oxygen Radical Production in the Sea Anemone Anthopleura Elegantissima and Its Endosymbiotic Algae. J Exp Biol (1992). 168 (1), 219–241.
5. Sukenik A, Zmora O, Carmeli Y. Biochemical quality of marine unicellular algae with special emphasis on lipid composition. II. Nannochloropsis sp.Aquaculture (1993). 117 (3-4), 313-326
6. https://drpaulclayton.eu/blog/kelp-wanted/
7. Kubanek J, Lester SE, Fenical W, Hay ME. Ambiguous role of phlorotannins as chemical defenses in the brown alga Fucus vesiculosus. (2004). Mar Ecol Prog Ser (277), 79-93
8. Phang SJ, The HX, Looi ML, Arumagam B, Fauzi MhB, Rani U. Phlorotannins from brown algae: a review on their antioxidant mechanisms and applications in oxidative-stress mediated diseases. (2023) J Appl Physiol (35), 867-892
9. Chang ZW, Chiang PC, Cheng W, Chang CC. Impact of ammonia exposure on coagulation in white shrimp, Litopenaeus vannamei. Ecotoxicol. Environ. Saf. 2015;118:98–102.
10. Eddy FB. Ammonia in estuaries and effects on fish. J. Fish Biol. 2005;67:1495–1513.
11. Kumar M, Singh S, Jain A, Yadav S, Dubey A, Trivedi SP. A review on heavy metal-induced toxicity in fishes: Bioaccumulation, antioxidant defense system, histopathological manifestations, and transcriptional profiling of genes. J Trace Elem Med Biol. 2024 May;83:127377. 
12. Slaninova A, Smutna M, Modra H, Svobodova Z. A review: oxidative stress in fish induced by pesticides. Neuro Endocrinol Lett. 2009;30 Suppl 1:2-12. 
13. Kim JH, Yu YB, Choi JH. Toxic effects on bioaccumulation, hematological parameters, oxidative stress, immune responses and neurotoxicity in fish exposed to microplastics: A review. J Hazard Mater. 2021 Jul 5;413:125423. 
14. Schumann S, Mozzi G, Piva E, Devigili A, Negrato E, Marion A, Bertotto D, Santovito G. Social buffering of oxidative stress and cortisol in an endemic cyprinid fish. Sci Rep. 2023 Nov 23;13(1):20579. 
15. Dai C, Zheng J, Qi L, Deng P, Wu M, Li L, Yuan J. Chronic stress boosts systemic inflammation and compromises antiviral innate immunity in Carassius gibel. Front Immunol. 2023 Feb 6;14:1105156.
16. Fialkowski R, Aufdemberge P, Wright V, Dijkstra P. Radical change: Temporal patterns of oxidative stress during social ascent in a dominance hierarchy. Behav. Ecol. Sociobiol. 2021;75:43.
17. Kowal M, Zelazniewiscz A, Nowak-Kornicka J, Groyecka-Bernard A, Pawlowski B, Sorokowski P. Self-reported aggression is related to oxidative stress in men and women. (2024). Europ J Personality. https://doi.org/10.1177/08902070241233027
18. Hussain T, Tan B, Yin Y, Blachier F, Tossou MC, Rahu N. Oxidative Stress and Inflammation: What Polyphenols Can Do for Us? Oxid Med Cell Longev. 2016;2016:7432797.
19. Mitjavila MT, Moreno JJ. The effects of polyphenols on oxidative stress and the arachidonic acid cascade. Implications for the prevention/treatment of high prevalence diseases. Biochem Pharmacol. 2012 Nov 1;84(9):1113-22.
20. Satoh K-i, Nakagawa H, Kasahara S. Effect of Ulva Meal Supplementation on Disease Resistance of Red Sea Bream. Nippon Suisan Gakkai Shi. 1987;53(7):1115–20.
21. Catarino MD, Amarante SJ, Mateus N, Silva AMS, Cardoso SM. Brown Algae Phlorotannins: A Marine Alternative to Break the Oxidative Stress, Inflammation and Cancer Network. Foods. 2021 Jun 25;10(7):1478
22. https://drpaulclayton.eu/blog/sea-horses/
23. Wassef E, El-sayed AM, Kandeel KM, EM S. Evaluation of pterocladia (Rhodophyta) and Ulva (Chlorophyta) meals as additives to gilthead seabream Sparus aurata diets. Egypt J of Aquatic Research. 2005;31:321–32.
24. Nakagawa H, Nematipour G, Yamamoto M. Optimum Level of Ulva Meal Diet Supplement to Minimize Weight Loss During Wintering in Black Sea Bream Acanthopagrus schlegeli (Bleeker). Asian Fish Soc. 1993;6:139–48.
25. Valente LMP, Gouveia A, Rema P, Matos J, Gomes EF, Pinto IS. Evaluation of three seaweeds Gracilaria bursa-pastoris, Ulva rigida and Gracilaria cornea as dietary ingredients in European sea bass (Dicentrarchus labrax) juveniles. Aquaculture. 2006;252(1):85–91. 
26. Mustafa MG, Nakagawa H. A review: Dietary benefits of algae as an additive in fish feed. Isr J Aquacult-Bamid. 1995;47:155–62.
27. Mukherjee P, Pal R. Algae as antioxidants and effective fish feed. African J Fisheries Sci 9(2), 001-006. Sept ’21.
28. Xiaojun Y, Li X, Zhou C, Xiao F. Prevention of fish oil rancidity by phlorotannins from Sargassum kjellmanianum. Journal of Applied Phycology (1996). 8(3):201-203
29. Jónsdóttir1 R, Hermund DB, Jacobsen C, Kristinsson HG. THE USE OF NATURAL ANTIOXIDANTS IN OMEGA-3 RICH FOOD PRODUCTS. https://www.matis.is/media/utgafa/veggspjold/The-use-of-Natural-Antioxidants-in-Omega-3….pdf
30. Yu S, Duan M, Sun J, Jiang H, Zhao J, Tong C, Pang J, Wu C. Immobilization of phlorotannins on nanochitin: A novel biopreservative for refrigerated sea bass (Lateolabrax japonicus) fillets. Int J Biol Macromol. 2022 Mar 1;200:626-634.
31. Andersen S, Kleinschmidt K, Hvingel B, Laurbeg P. Thyroid hyperactivity with high thyroglobulin in serum despite sufficient iodine intake in chronic cold adaptation in an Arctic Inuit hunter population. Eur J Endocrinol. 2012;166:433–40.
32. Coolbaugh CL, Damon BM, Bush EC, Welch EB, Towse TF. Cold exposure induces dynamic, heterogeneous alterations in human brown adipose tissue lipid content. Sci Rep. 2019 Sep 19;9(1):13600.
33. Fumagalli M, Moltke I, Grarup N, Racimo F, Bjerregaard P, Jørgensen ME, Korneliussen TS, Gerbault P, Skotte L, Linneberg A, Christensen C, Brandslund I, Jørgensen T, Huerta-Sánchez E, Schmidt EB, Pedersen O, Hansen T, Albrechtsen A, Nielsen R. Greenlandic Inuit show genetic signatures of diet and climate adaptation. Science. 2015 Sep 18;349(6254):1343-7.
34. Chen L, Liu R, He X, Pei S, Li D. Effects of brown seaweed polyphenols, a class of phlorotannins, on metabolic disorders via regulation of fat function. Food Funct. 2021 Mar 21;12(6):2378-2388. 
35. Lu C, Zhu W, Shen CL, Gao W. Green tea polyphenols reduce body weight in rats by modulating obesity-related genes. PloS one. 2012;7:e38332
36. Li L, Feldman BJ. White adipocytes in subcutaneous fat depots require KLF15 for maintenance in preclinical models. J Clin Invest. 2024 Jul 1;134(13):e172360. 
37. Bang HO, Dyerberg J, Nielsen AB. Plasma lipid and lipoprotein pattern in Greenlandic West-coast Eskimos. Lancet. 1971 Jun 5;1(7710):1143-5.
38.  Tsuduki T, Honma T, Nakagawa K, Ikeda I, Miyazawa T. Long-term intake of fish oil increases oxidative stress and decreases lifespan in senescence-accelerated mice. Nutrition. 2011 Mar;27(3):334-7.
39. Larsson K, Cavonius L, Alminger M, Undeland, I. Oxidation of cod liver oil during gastrointestinal in vitro digestion. Journal of Agricultural and Food Chemistry, 2012, 60(30), 7556-7564.
40. Larsson K, Harrysson H, Havenaar R, Alminger M, Undeland I. Formation of malondialdehyde (MDA), 4-hydroxy-2-hexenal (HHE) and 4- hydroxy-2-nonenal (HNE) in fish and fish oil during dynamic gastrointestinal in vitro digestion. Food & Function. 2016, 7(2), 1176 ñ
41. https://drpaulclayton.eu/blog/thanks-for-all-the-fish/
42. Chen G, Qian ZM, Zhang J, Zhang S, Zhang Z, Vaughn MG, Aaron HE, Wang C, Lip GY, Lin H. Regular use of fish oil supplements and course of cardiovascular diseases: prospective cohort study. BMJ Med. 2024 May 21;3(1):e000451. 
43. Yes, I do know that this is the opposite of the original meaning of the phrase. Thank you for noticing.
44. Yu H, Mei J, Xie J. New ultrasonic assisted technology of freezing, cooling and thawing in solid food processing: A review. Ultrason Sonochem. 2022 Nov;90:106185. 
45. Whaley D, Damyar K, Witek RP, Mendoza A, Alexander M, Lakey JR. Cryopreservation: An Overview of Principles and Cell-Specific Considerations. Cell Transplant. 2021 Jan-Dec;30:963689721999617.
46. https://www.youtube.com/watch?v=wBK7cvSJdps