Benefits and harms of mammographic breast cancer screening [4].
\r\n\t
",isbn:"978-1-83969-561-2",printIsbn:"978-1-83969-560-5",pdfIsbn:"978-1-83969-562-9",doi:null,price:0,priceEur:0,priceUsd:0,slug:null,numberOfPages:0,isOpenForSubmission:!0,hash:"65f2a1fef9c804c29b18ef3ac4a35066",bookSignature:"Dr. Luis Loures",publishedDate:null,coverURL:"https://cdn.intechopen.com/books/images_new/10756.jpg",keywords:"Urban Processes, Urban Patterns, Redevelopment Strategies, Landscape, Land Transformation, Urban Models, Urban Evolution, Urban Organisation, Legislation, Sustainable Development, Green Infrastructure, Regional Planning",numberOfDownloads:null,numberOfWosCitations:0,numberOfCrossrefCitations:null,numberOfDimensionsCitations:null,numberOfTotalCitations:null,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"February 23rd 2021",dateEndSecondStepPublish:"March 22nd 2021",dateEndThirdStepPublish:"May 21st 2021",dateEndFourthStepPublish:"August 9th 2021",dateEndFifthStepPublish:"October 8th 2021",remainingDaysToSecondStep:"14 days",secondStepPassed:!1,currentStepOfPublishingProcess:2,editedByType:null,kuFlag:!1,biosketch:"Dr. Loures has worked on pioneering research on circular planning applied to post-industrial landscape redevelopment. Since he graduated he has published several peer-reviewed papers at the national and international levels and he has been a guest researcher and lecturer both at Michigan State University (USA) and at the University of Toronto (Canada) where he has developed part of his Ph.D. research with the Financial support from the Portuguese Foundation for Science and Technology (Ph.D. grant).",coeditorOneBiosketch:null,coeditorTwoBiosketch:null,coeditorThreeBiosketch:null,coeditorFourBiosketch:null,coeditorFiveBiosketch:null,editors:[{id:"108118",title:"Dr.",name:"Luis",middleName:null,surname:"Loures",slug:"luis-loures",fullName:"Luis Loures",profilePictureURL:"https://mts.intechopen.com/storage/users/108118/images/system/108118.png",biography:"Luís Loures is a Landscape Architect and Agronomic Engineer, Vice-President of the Polytechnic Institute of Portalegre, who holds a Ph.D. in Planning and a Post-Doc in Agronomy. Since he graduated, he has published several peer reviewed papers at the national and international levels and he has been a guest researcher and lecturer both at Michigan State University (USA), and at University of Toronto (Canada) where he has developed part of his Ph.D. research with the Financial support from the Portuguese Foundation for Science and Technology (Ph.D. grant).\nDuring his academic career he had taught in several courses in different Universities around the world, mainly regarding the fields of landscape architecture, urban and environmental planning and sustainability. Currently, he is a researcher both at VALORIZA - Research Centre for Endogenous Resource Valorization – Polytechnic Institute of Portalegre, and the CinTurs - Research Centre for Tourism, Sustainability and Well-being, University of Algarve where he is a researcher on several financed research projects focusing several different investigation domains such as urban planning, landscape reclamation and urban redevelopment, and the use of urban planning as a tool for achieving sustainable development.",institutionString:"Polytechnic Institute of Portalegre",position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"8",totalChapterViews:"0",totalEditedBooks:"2",institution:{name:"Polytechnic Institute of Portalegre",institutionURL:null,country:{name:"Portugal"}}}],coeditorOne:null,coeditorTwo:null,coeditorThree:null,coeditorFour:null,coeditorFive:null,topics:[{id:"10",title:"Earth and Planetary Sciences",slug:"earth-and-planetary-sciences"}],chapters:null,productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"},personalPublishingAssistant:{id:"205697",firstName:"Kristina",lastName:"Kardum Cvitan",middleName:null,title:"Ms.",imageUrl:"https://mts.intechopen.com/storage/users/205697/images/5186_n.jpg",email:"kristina.k@intechopen.com",biography:"As an Author Service Manager my responsibilities include monitoring and facilitating all publishing activities for authors and editors. 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Venkateswarlu",coverURL:"https://cdn.intechopen.com/books/images_new/371.jpg",editedByType:"Edited by",editors:[{id:"58592",title:"Dr.",name:"Arun",surname:"Shanker",slug:"arun-shanker",fullName:"Arun Shanker"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"878",title:"Phytochemicals",subtitle:"A Global Perspective of Their Role in Nutrition and Health",isOpenForSubmission:!1,hash:"ec77671f63975ef2d16192897deb6835",slug:"phytochemicals-a-global-perspective-of-their-role-in-nutrition-and-health",bookSignature:"Venketeshwer Rao",coverURL:"https://cdn.intechopen.com/books/images_new/878.jpg",editedByType:"Edited by",editors:[{id:"82663",title:"Dr.",name:"Venketeshwer",surname:"Rao",slug:"venketeshwer-rao",fullName:"Venketeshwer Rao"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"4816",title:"Face Recognition",subtitle:null,isOpenForSubmission:!1,hash:"146063b5359146b7718ea86bad47c8eb",slug:"face_recognition",bookSignature:"Kresimir Delac and Mislav Grgic",coverURL:"https://cdn.intechopen.com/books/images_new/4816.jpg",editedByType:"Edited by",editors:[{id:"528",title:"Dr.",name:"Kresimir",surname:"Delac",slug:"kresimir-delac",fullName:"Kresimir Delac"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}}]},chapter:{item:{type:"chapter",id:"58715",title:"Adjusting Bioactive Functions of Dairy Products via Processing",doi:"10.5772/intechopen.72927",slug:"adjusting-bioactive-functions-of-dairy-products-via-processing",body:'Dairy products are appreciated for their high nutritional value [1]. Not only the high contents of protein, vitamins, and minerals determine the positive health effect of dairy products. Hidden components called bioactive peptides, encrypted in parent milk proteins, exhibit special functions that might influence our well-being. So far peptides with antihypertensive, anti-oxidative, anti-thrombotic, anticancer, immune-modulatory, antimicrobial, cholesterol-lowering, antidiabetic, mineral-binding, opioid and satiety properties were identified. These peptides occur directly in the dairy products after processing and are resistant to digestion enzymes or they are encrypted in dairy proteins and get released during digestion. Interestingly, the processing method of the dairy products can influence the number and sequence of the resulting peptides after digestion and therefore also the content of bioactive peptides. Heat treatment, chemical and biochemical, and physical treatment can influence the bioactive functionality transmitted by the selected dairy product. In the future, it might be possible to target a wished bioactive function via processing. This book chapter just deals with the effects exhibited by bioactive peptides. However, also other milk components are affected by processing and can exhibit bioactive functions, e.g. effects on the lipids, minerals, and vitamins. Furthermore, the addition of certain bioactive ingredients to dairy products is also not discussed in this chapter. The focus is given to the possible effects transmitted via bioactive peptides and the effect of processing on the peptide profile.
The health potential of dairy protein is not only originating from the unique amino acid composition and their great bioavailability (Figure 1). Especially the high content of essential amino acids and their fast release as free amino acids during digestion [2], plus the high content of certain vitamins and minerals is important for the high nutritional value of bovine milk. However, there is a more hidden health potential of dairy products that is displayed by bioactive peptides. Bioactive peptides contain usually 3–20 amino acid residues and their composition and sequence determine their activity. They are encrypted in the primary sequence of proteins and get released via three different ways [3]:
Hydrolysis by digestive enzymes
Hydrolysis by proteolytic microorganisms
Action of proteolytic enzymes derived from microorganisms or plants
Illustration of milk protein degradation by lactic acid bacteria (LAB) and during digestion via digestive enzyme action resulting in bioactive peptides.
These are the ways to produce bioactive peptides that can be afterwards purified and used as ingredients for manufacturers of functional foods. However, also the more natural way of processing via hydrolysis by proteolytic microorganisms can be an approach to enrich a specific bioactive function in a product. Bioactive peptides have been discovered not only in dairy products, but also in meat, eggs, fish, and other marine organisms and also in plant sources like certain grains, legumes, pulses, and oilseeds [4, 5, 6].
The production of bioactive peptides for use as additives can be done by enzymatic hydrolysis or microbial fermentation [7]. Enzymatic hydrolysis applies digestion enzymes. Mostly trypsin, a pancreatic proteinase is used, but also chymotrypsin, pepsin thermolysin, pancreatin, elastase, carboxypeptidase or a proline-specific endopeptidase can deliver bioactive peptides. Additionally, proteases from bacteria, fungi, and plants also showed interesting properties [7]. Microbial fermentation uses bacteria or yeast that exhibit proteolytic activity to generate peptides. They are grown and added in their exponential phase to the protein of interest. The degree of hydrolysis is then dependent on the strain and its proteolytic activity. In both ways, a purification of the peptides is necessary. This can be for example reached by centrifugation methods, freeze drying, desalting, and membrane filtration techniques [8]. Examples are the production of caseinophosphopeptides from α-s-casein with an immobilized trypsin in a fluidized bed bioreactor [9] and a combination of diafiltration and anion-exchange chromatography [10]. The peptide additives can be added to a product of interest to generate a functional food. For this purpose, also the stability of the peptides with regard to pH, temperature, and food matrix has to be considered. Furthermore, the more natural way to enhance dairy products with bioactive peptides is to directly add a bacterial culture to the dairy product and generate a fermented product containing bioactive peptides. This is the general processing method applied already for each fermented dairy product. If protein is not taken out, all dairy products result in a high quantity of bioactive peptides that might be absorbed in the small intestine. For the functionality of these peptides, the selection of bacteria strains is important to aim for a specific bioactive function via processing (see Section 3).
The possible, so far detected, functionalities of bioactive peptides are summarized in Figure 2.
Possible functionalities of bioactive peptides.
Antihypertensive peptides can inhibit the angiotensin I-converting enzyme (ACE) (EC 3.4.15.1;ACE) that is involved in blood pressure regulation. ACE increases the blood pressure by converting angiotensin I into the vasoconstrictor angiotensin II and additionally degrades vasodilative bradykinin. ACE-inhibitory peptides were detected in different food proteins like bovine casein and human casein, whey protein, zein, gelatin, yeast, and corn [11]. The most ACE-inhibitory peptide in studies of [28], had an IC50 value of 77 μM and was originating from α-lactalbumin with the peptide sequence α-lactalbumin f(104–108). Different studies showed the bioavailability of the ACE-inhibitory peptides Ile-Pro-Pro and Val-Pro-Pro in humans [12, 13]. These two tripeptides are the ones that are studied the most and show the highest evidence for their bioefficacy.
Anti-oxidative peptides help against the oxidative damage caused by reactive oxygen species. The amino acids cysteine, lysine, histidine, methionine, tryptophan, and tyrosine can act as radical scavengers [14]. Therefore, they act as potential antioxidants.
The formation of blood clots can be reduced by antithrombotic peptides. Especially known is the glycomacropeptide (GMP) originating from kappa-casein after enzymatic milk coagulation. GMP can inhibit the aggregation of blood platelets and binding of the human fibrinogen gamma-chain to platelet surface fibrinogen receptors [15]. Also, the absorption into the plasma could be observed in humans for 2 anti-thrombotic peptides [16].
Anticancer peptides can inhibit cancer cell growth. In vitro experiments with HL-60 human leukemia cells showed for example, that after skimmed milk digestion with a proteolytic enzyme from yeast Saccharomyces cerevisiae apoptosis can be induced [17].
Immune-modulatory peptides are mostly found in dairy products. Enzymatic hydrolysis resulted in a number of biologically active peptides that can influence immune cells and release specific signals [18]. Some peptides can stimulate or inhibit immune responses and their positive health effects have been investigated mostly in vitro. These assays are performed with immune cells and target for example proliferation, phagocytosis, differentiation, and cytokine production. A survey of these assays can be found in the review of Maestri et al. [6]. The immunomodulatory potential of peptides originating from whey protein is discussed in the study of Gauthier et al. [19]. Interestingly, there are some in vivo studies that have demonstrated promising results. Otani et al. showed for example that feeding mice a dietary casein phosphopeptide influenced the level of serum IgA and intestinal antigen-specific IgA [20]. The exact mechanism of the action exhibited by immune-modulatory peptides still has to be determined.
Peptides that inhibit dipeptidyl peptidase 4 (DPP-IV, EC 3.4.14.5) are known as satiety increasing peptides. DPP-IV degrades the satiety regulating glucagon-like-peptide 1 [21]. Kopf-Bolanz et al, monitored the fates of specific peptides with known satiety increasing action. They compared different dairy products and found the relative abundance of three potent DPP-IV inhibitory peptides deriving from β-casein. The best source for these peptides was Gruyere cheese. Two other peptides deriving from α-S1-casein were not detectable anymore after the pancreatic phase of the digestion [22]. Tryptophan seems to be an important amino acid in peptides that exhibit a DPP-IV inhibitory potential [23]. Three dipeptides containing tryptophan Trp-Arg, Trp-Lys, and Trp-Leu with half maximum inhibitory concentrations (IC50) < 45 μM could be detected in a study of Nongonierma and Fitzgerald that are potent inhibitors of DPP-IV [24].
Another interesting peptide that has an influence on satiety is the glycomacropeptide (GMP) resulting from cheese production. It has demonstrated in several animals and human studies that it can stimulate the release of cholecystokinin and promote satiety. However, further studies would be necessary to demonstrate a clear bioefficacy [25, 26]. Peptides that increase the satiety are also known as anti-obesity peptides [27].
Peptides that have an affinity for the opioid receptor are categorized in this group. There are receptors that are responsible for specific physiological effects like emotional behavior and food intake. Opioid peptides have the same N-terminal sequence Tyr-Gly-Gly-Phe. There are also atypical opioid peptides with the ending of Tyr-X-Phe or Tyr-X1-X2-Phe. A tyrosine residue at the N-terminal and another aromatic amino acid at the third or fourth position are specific binding motifs of the opioid receptor. The first food-derived opioid peptides were β-casomorphins. Also, casoxins, lactorphins, and exorphins can bind to opioid receptors [28]. So far, a weak opioid activity for α-lactorphin (α-lactalbumin f(50–53)) and β-lactorphin (β-lactoglobulin f(102–105)) was detected in guinea pigs [11], but human data are still missing. Concentrations released from in vivo digestion of milk are quite low. The total amount of α-lactorphin and β-lactorphin in 1 L of bovine milk would be 32 mg (64 μmol), respectively 90 mg (162 μmol), but it might be difficult to obtain a full release of the possible peptide during in vivo digestion. It is so far not clear whether they can get liberated by in vivo digestion at all, but it was demonstrated that casomorphins are liberated in vivo [11].
Diabetes is treated by synthetic antidiabetic drugs that can result in side effects like hypoglycemia or weight gain [8]. To overcome this issue, the application of antidiabetic peptides originating from food sources might be a solution. Antidiabetic peptides could be for example detected in sheep milk [29].
Mineral-binding phosphopeptides can carry different minerals by forming soluble organophosphate salts [30]. Caseinophosphopeptides (CPP) can increase calcium absorption by limiting calcium precipitation in the ileum. Caseins are phosphorylated in the mammary gland at primary sequences rich in serine and glutamic acid forming triplet regions SerP-SerP-SerP-Glu-Glu that occur in α-S1-casein (66–70), α-S2-casein (8–12), (56–60), (129–133) and β-casein (15–19). The presence of CPPs has been shown in vivo. Several animal studies have demonstrated the effect of CPP to enhance calcium bioavailability. In contrast, convincing results from human are still missing [31]. A human study with CPP-enriched preparations (containing candidate functional food ingredients) on calcium absorption from a calcium lactate drink showed no significant results [32]. Another interesting peptide is lactoferricin consisting of 25 amino acid residues. The molecule is folded into two globular units, each capable of binding one ferric (Fe3+) ion [33].
So far mainly peptides derived from soy proteins have been shown to suppress cholesterol in the blood. Some can for example target the cholesterol receptor or suppress the presence of LDL. Important for the functions are mainly the hydrophobic residues [34]. A novel peptide (Ile-Ile-Ala-Glu-Lys) from a trypsin-treated hydrolysate of β-lactoglobulin showed a hypocholesterolemic effect in an animal study [35].
Peptides that induce for example the lysis of bacterial membranes are antimicrobial peptides. They could be detected in α-lactalbumin, β-lactoglobulin, all casein fractions, and lactoferrin [36].
The safety and toxicity of bioactive peptides has to be considered. Different studies demonstrated that casein hydrolysates and Val-Pro-Pro from powdered fermented milk did not show any toxicological potential [37, 38, 39]. Processing can lead to Maillard reaction and result in the production of allergenic compounds [40]. Processing changes the protein structure and might influence the protein degradation and therefore also the response of the immune system. Therefore, it is important to determine the allergic potential that can arise from bioactive peptides. If fermentation takes place, for example, de novo peptides might originate and their allergenic potential has to be determined. First, a comparison with already known allergenic sequences can be done, followed by laboratory tests. The problem is that allergenic sequences can occur over the whole dairy protein sequences, and there can be rare cases that people are allergic to a new peptide sequence arising from fermentation. However so far, mostly positive reports about the effect of fermentation are published [41, 42]. It is also important to mention that these functionalities were observed to a great extent with in vitro methods. Only very few human studies have demonstrated an effect of bioactive peptides in vivo.
To exhibit really a bioactive function in vivo, the peptides must be released during digestion from their originating protein or if they are already in the product as such, they have to be resistant to digestion enzymes. During digestion, the proteins get denatured by gastric acidification and subsequently degraded by pepsin and pancreatic peptidases like trypsin into peptides and amino acids. Furthermore, the final actions of the enzymes at the brush-border membrane in the small intestine have to be taken into account. There are peptidases that cleave amino acids or dipeptides from the N- or C-terminal of the interior bond of the oligopeptides. The mean size of the peptides in the jejunum considering the action of aminopeptidases and dipeptidases from the enterocytes is 3–6 amino acids. Di- and tripeptides can be transported actively by the peptide transporter PEPT1 [43]. Longer peptides can probably get absorbed ether via paracellular or transcellular pathways. The possible transport of a heptapeptide was shown using a cell culture model [44]. In the blood, the peptides must be able to reach their target site in the peripheral organs. In a human study of van Platerink et al., 17 ACE-inhibiting peptides with 5–6 amino acids length could be detected in the blood after consumption of drinks enriched with those peptides [13]. The first proof that the tripeptide Ile-Pro-Pro does not undergo intestinal degradation and can reach the circulation intact was shown from Foltz et al. [12]. Another human study showed the presence of a longer peptide after soybean consumption in the blood [45]. At the target cells, it is assumed that peptides can internalize via endocytosis and get digested in the lysosome. Peptides that do not enter target cells can accumulate in the liver and kidney and can be detected in urine or bile [6]. There is still the need to demonstrate a clear bioefficacy of the peptides and confirm the positive health effects in human studies. In the future possibly health claims for certain bioactive peptides could be developed. So far Japan declared certain antihypertensive peptides such as Val-Pro-Pro, Ile-Pro-Pro, Val-Tyr, and Cys-Pro-Pro as Food of Specific Health Use (FOSHU). In contrast, the European Food and Drug Association (EFSA) did not authorize any claims regarding the effect of bioactive peptides in foods yet [46].
Experiments concerning bioactive peptides are mainly done in vitro. Most of the time, a dairy product is inserted into an in vitro digestion model that mimics human digestion.
There are numerous in vitro digestion models that can be applied. It is important that a model close to human physiology and validated is applied. Recently, a harmonized digestion model was established during the COST digestion action. This model is very physiological and might be used for mimicking digestion [47]. The resulting peptides generated during the digestion process can be detected by peptidomic methods. Analytics of bioactive peptides aim toward three main directions [48]:
Tracing the pathways of formation of bioactive peptides from the parent proteins
Identifying the biological properties
Improving the “positive” properties discovered in natural peptides by design of synthetic structural analogues or peptide mimetics
Peptidomics is the comprehensive qualitative and quantitative analysis of all peptides in a biological sample. In earlier days, protein digestion could be followed by HPLC or Edman sequencing [49]. Nowadays, MS-based techniques such as Liquid chromatography coupled to mass spectrometry (LC-MS) can be applied [22, 50]. Peptidomics of food hydrolysates, for example, led to the discovery of the exact sites of rennet cleavage on kappa-casein or the cleavage sites produced by bacteria during cheese ripening [49]. The detailed human study of Boutrou et al. was identified in the jejuna effluents of healthy adults, after consumption of 30 g milk casein and whey proteins, 356 and 146 peptides [50]. The in vitro model developed by Minekus et al., almost resulted in similar peptides [47]. The different analytical approaches that can be applied are summarized in the review of Dallas et al. [49]. Technology allows the prediction of the peptide sequence and can generate a peptide fingerprint. The peptides can be then compared to the known bioactive peptides from the literature in various databases. An example is the milk bioactive peptide database by Nielsen et al. [51]. This database comprises information on bioactive peptides from across hundreds of original research articles and is available to the public. Furthermore, whole in silico strategies for bioactive function generation including computational modeling might be applied, that still have limitations, but might be used in the future for the design of new products.
Dairy products are processed by the application of different physical and chemical methods. These methods change the protein structure irreversible or reversible depending on the impact of the treatment. The protein can be mainly denatured, hydrolysed, or glycosylated. This structural change can influence the access of the digestion enzymes to the protein and therefore changes the action of the digestion enzymes. An impact on the peptide profile that is generated before absorption into the blood takes place is the result. It is necessary to determine which processing methods and which processing variables are necessary to be able to reach or maintain a specific bioactivity.
Thermal processing is an important step to improve the microbial quality of milk. Additionally, enzyme activities are inactivated and some physicochemical changes can occur that might support processing. The nutritional value is greatly affected by thermal processing. Denaturation, β-elimination, racemization, or iso-peptide bond formation can occur that influence the nutritional value [52]. Denaturation is influenced by pH, protein concentration, ionic environment, genetic variant, and presence of ligands [53]. Heating might even particularly destroy tryptophan, can convert Arginine into citrulline and ornithine, can deamidate glutamine and asparagine, and desulphur cysteine and cysteine. Resulting end products might be lanthionine, lysine-alanine, iso-peptides and ornitho-alanine [52]. The digestibility of whey proteins increases after thermal treatment because the sites for enzymatic hydrolysis are easier to reach for the digestive enzymes. However, strong denaturation reduces digestibility [54]. Kopf-Bolanz et al. showed that heat treatment of dairy products led to an increased number of β-lactoglobulin peptides after in vitro digestion [22]. There is a greater susceptibility to hydrolysis following heat treatment [55]. Regarding the antidiabetic action of casein, there was a significant reduction observed after boiling compared to the raw casein [29]. The denaturation of whey protein via thermal processing led to an increase in the antibacterial activity of α-lactalbumin [56] and lysozyme [57]. The antioxidant action of whey proteins can be maintained by low-temperature processing. This results in high levels of specific dipeptides that can promote the synthesis of the antioxidant glutathione [58]. Extrusion cooking might also affect protein digestibility shown for example in a study of Onwulata et al. [59]. Data on the effect of ohmic heating are rare. Depending on the used temperatures, similar effects like with application of other heating methods might be expected [52]. It was also shown that spray drying or freeze drying did not exhibit negative effects on the immunomodulatory activity of a whey protein hydrolysate. The study also used whey protein concentrate (WPC) and sodium alginate as carriers for encapsulation to reduce bitter taste and resistance to hygroscopicity. They showed that spray drying of whey protein concentrate hydrolysate with the proper carriers did not affect the immunomodulatory activity and might therefore widen its application in food systems [60].
Hydrolysis by acid is applied which is known to improve their protein digestibility. It is used for example for enteral and hypoallergenic infant nutrition. For Mozzarella, the type of acid used is important for the protein yield obtained in the pre-cheeses [61] and might therefore also affect the profile of bioactive peptides. Treatment with alkali for hydrolysis is rarely applied in the food industry. It would result in racemization and loss of protein digestibility [62].
Fermented dairy products like yoghurt and cheese result in a high number of bioactive peptides produced by the lactic acid bacteria. Especially the type of the starter culture, type of probiotic bacteria, and the fermentation parameters play an important role for the bioactive effect that the product might have. Furthermore, only via this way de novo peptides can be generated that do not occur after digestion of milk as such. Streptococcus thermophilus and Lactobacillus bulgaricus possess bacterial activity against Streptococci in vivo that probably derives from the antimicrobial peptides that they produce during fermentation [63]. It is very promising to test different lactic acid bacteria strains for their effect on a bioactive function. One study of Gobbetti et al. showed that a fermentation with L. delbrueckii ssp. Bulgaricus SS1 versus a fermentation with Lactobacillus lactis subspecies cremoris FT4 resulted in a higher ACE-inhibitory activity [64]. The most investigated ACE-inhibitory peptides were obtained after fermentations with L. helveticus and L. helveticus CP790. Also, the Finnish milk product Evolus contained L. helveticus LBK-16H strain as a starter and they all contained the tripeptide IPP and exerted a hypertensive effect [65, 66, 67]. Another study demonstrated the effect of the time of cheese ripening on the ACE-inhibitory activity. Cheese was produced with a mixture of 12 different strains and showed an increase of the inhibitory effect during ripening as long as a certain level of proteolysis was not exceeded [68]. In 10 Swiss cheese types, the ACE-inhibiting peptides V-P-P and I-P-P were quantified. They detected contents of 19.1 mg/kg to 182.2 mg/kg depending on the cheese type that shows the huge effect of different processing ways probably via different lactic acid bacteria [69]. Also, the application of new techniques like next-generation sequencing that reveals the whole genome of bacteria strains might help to select promising strains with specific protease expressions. It was also demonstrated that fermentation reduced the allergenic potential of α-lactalbumin and β-lactoglobulin [41, 42]. The peptides that result after fermentation and enzyme hydrolysis might remain susceptible to further hydrolysis as long as the process goes on. This might lead to a decrease of bioactive function of these peptides. More important is also the stability of the generated peptides. They might be degraded by the digestive enzymes and result in zero activity in the body. The stability versus the action of gastric and pancreatic enzymes has to be tested beforehand. Another problematic point is that the microbial fermentations have to be reproducible [8]. Fermentation with known and established lactic acid bacteria cultures is a great strategy to enrich certain bioactive peptides with a special functionality. This would be a possibility to enhance a bioactive function in a natural way with a minimal processing approach that meets the interests of the consumer. The functionality and bioavailability of bioactive peptides generated via fermentation has to be more clarified.
The use of milk-clotting enzymes and digestive enzymes to produce bioactive peptides is another processing approach. However, most of the resulting peptides had a bitter taste [7]. Membrane-separation technique is applied to enrich peptides with a specific molecular weight [3]. It was also shown that hydrolysed infant formulas show a different peptide profile compared to the standard formulas assuming that infants fed hydrolysed formulas might obtain bioactive peptides that promote other bioactive functions than the ones provided by the standard formulas [70].
Homogenization applies pressure (14–18 MPa) and shear stress that alter the protein structure and improve the digestibility [52]. Use of ultra-high pressure homogenization with pressure around 400 MPa results in more severe protein denaturation [71]. Application of high hydrostatic pressure processing increased digestibility of β-lactoglobulin with pepsin with increasing pressures (400–800 MPa) [72]. Penas et al. also combined high hydrostatic pressure processing with selected food-grade proteases and demonstrated a reduction in antigenicity of the whey protein hydrolysates that can be used as ingredients of hypoallergenic infant formulae [73]. Ultrasound treatment is a non-conventional processing technique that can denature α-lactalbumin and β-lactoglobulin. In whole milk compared to skim milk, the denaturation was stronger and heat addition even increased this effect [74]. A very soft technology is membrane filtration that enables to separate proteins in their native state. This technology only enables a fractionation of different milk components and does not alter the protein structure as such, and it only influences the milk composition.
Not only processing can influence the profile of bioactive peptides. Also, other external factors can influence protein digestion and therefore the bioavailability and generation of bioactive peptides. It is important to consider the effect of the food matrix and meal composition on digestion. For example, the addition of inulin to the dairy product can influence digestion and peptide bioavailability [75]. Also, proteins can form complexes with polyphenols, etc. that could lower protein bioavailability [76]. Furthermore, internal factors can influence the peptide profile. Children and the elderly have different enzyme activities and therefore the digestion enzymes will act slightly different and change the peptide profile [77, 78]. Genetic variations in people for example enzyme deficiencies or changes in the composition of the digestion juices due to different transporter expression can have an impact. The action of digestion enzymes depends on daytime, age and on Helicobacter pylori infection [79]. Also for a lot of other special physiological states, certain diseases and so on, the enzyme activity is affected and might therefore result in a different bioactive peptide bioavailability. It is very important to consider all the factors that can affect peptide bioavailability in the target group of the product.
An enrichment of peptides that can inhibit DPP-IV could result in increasing satiety after consumption of a dairy product. The most promising approach to steer the peptide profile of the product is via fermentation with lactic acid bacteria. It would be promising to test different starter bacteria with different protease activities. Differences in their proteolytic action result in different peptide profiles. Then, an in vitro digestion model might be applied that is mimicking the digestion physiology of the target group. Next step would be peptide profiling and alignment of the results with already known sequences of DPP-IV inhibitory peptides. Furthermore, the inhibitory effect could be also tested using directly an enzyme assay. It is important to consider also all the other processing parameters that can affect protein digestion. Finally, the bioactive effect has to be confirmed in humans that represent the target group of the product (Figure 3).
Targeting bioactive function in product development.
After ingestion of food containing protein, a peptide pattern is generated that probably contains bioactive sequences and is present in the jejunum before absorption takes place. Especially for dairy products, many different bioactive peptides could be identified that might be very interesting for the development of products with a specific functionality. The peptide patterns are strongly influenced by processing. Thermal treatments are used in general to ensure the microbial quality of dairy proteins. They exhibit a great influence on the protein structure for example by protein unfolding. Easier access is then given to the digestion enzymes and the resulting peptide profile is changed. Highly interesting is the fermentation of dairy products with different lactic acid bacteria strains. Certain strains have different protease activities and increase for example the number of antihypertensive peptides resulting after digestion. The angiotensin-converting enzyme inhibition is the most studied functionality and there are reports that could detect bioavailable peptides in the blood. The peptide concentrations reached for example in cheeses are promising to exhibit a bioactive function. Chemical and physical approaches can also influence the protein structure and therefore the protein digestion. The impact of new processing techniques on protein digestion should be always monitored. For the adjustment of a specific bioactive function in a product, an example approach is mentioned. However, it will always also depend on other factors whether the wished functionality is really reached or not. External factors like the meal composition and internal factors like age or genetic preconditions can also have an impact and have to be considered. Furthermore, for safety reasons, there is the small chance that generated de-novo peptides might act as epitopes for rare cases of cow milk allergy. However so far, fermentation with established lactic acid bacteria strains seems to reduce the allergenic potential of dairy products in general. In the future, it is necessary to perform well designed human studies that ensure a bioactive effect and allow the admission of health claims.
According to data from the World Health Organization (WHO), the number of deaths due to cancer will increase up to 45% between 2008 and 2030 and 70% of those deaths will occur in developing countries [1]. To try and change this scenario, the WHO recommends the implementation of cancer control programs that must include cost-effective measures on healthy life style, vaccination programs and screening programs [2]. A screening program consists in a set of coordinated actions with the objective of reducing cancer mortality through early stage diagnosis in an asymptomatic population, with adequate referral to diagnostic and treatment facilities. These programs have four main components: the definition and recruitment of the target population, adequate offer of diagnostic tests with quality assurance, guaranteed offer of follow up exams and biopsies to confirm findings from the initial diagnostic tests, and referral to treatment facilities and timely navigation through the health system [3]. Although screening programs present the potential benefit of reducing mortality, they are not risk-free. The main risks of such a program are the false-positive and false-negative results, and also the occurrence of over diagnosis. All these can lead to clinical and psychological repercussions and, also, to the increase in the health care system expenditure. To address this issue, the Public Health Agency of Canada performed a study to estimate the harms of the local breast cancer-screening program in 7 years, according to age, and the main results can be seen in Table 1 [4].
Age Range | 40–49 years old | 50 to 59 years old | 60 to 69 years old | 70 to 74 years old |
---|---|---|---|---|
Screening strategy | Annual mammogram | Mammogram every two years | Mammogram every two years | Mammogram every two years |
Women that will not have cancer | 993 | 988 | 979 | 968 |
Women that will have cancer | 7 | 12 | 21 | 32 |
Unnecessary biopsies | 43 | 37 | 35 | 30 |
False-positive results | 294 | 294 | 256 | 219 |
Overdiagnosis | 3 | 3 | No reliable data | No reliable data |
Deaths prevented by screening | <1 | 1 | 1 | 2 |
Number needed to screen to prevent one cancer-related death | 1724 | 1333 | 1087 | 645 |
Benefits and harms of mammographic breast cancer screening [4].
In this text, we will use Brazil as a model to discuss screening programs in the developing countries. In the Brazilian setting, breast cancer is the most frequent type of cancer, responsible for 16,724 deaths in 2017 and with an estimate of 66,280 new cases in 2020 [5]. This scenario, however, has some peculiarities when compared to developed countries in the North America or Europe; 41.1% of all cases in Brazil happen in women younger than 50 years old and the majority of the operable cases is diagnosed in locally advanced stages, being 53.3% of the cases in stage II and 23.2% in stage III [6]. These characteristics are not typical of a country with a well-established breast cancer-screening program. The strategy adopted in Brazil states that women over 50 should get a mammogram every two years between 50 and 69 years old [7]. However, due to the early age of diagnosis that we observe in this developing country, we can argue that more than 40% of the diagnosed women are not eligible to the screening program in the first place. Moreover, the late presentation at diagnosis raises the hypothesis that the current screening program is not effective or that the patients do not have proper access to it. Added to that, the mortality due to breast cancer in Brazil has been increasing in the last decades [8]. All these issues taken together generate an ethical dilemma to be explored, once the investment of public resources in an ineffective program impacts negatively the whole society. This way, more effective resources reallocation strategies should be implemented to address this dilemma.
In this chapter we will discuss the breast cancer screening programs in developing countries and the main evidence regarding the barriers in the access to the healthcare system. Beyond that, we will address the main ethical questions related to breast cancer screening from the Rawls’s distributive justice [9] perspective, from the utilitarianism concepts [10, 11] and from the principles of autonomy and non-maleficence. Lastly, we will propose the support to an alternative approach to breast cancer in developing countries, maximizing the cost–benefit ratio in the use of public resources.
The U.S. Preventive Services Task Force (USPSTF) is an independent volunteer panel of American experts that develops recommendations regarding the efficacy of preventive services to asymptomatic patients. These recommendations are based on both benefits and harms that programs might cause, without consideration to the cost of the intervention. Current data about mammographic screening are solid regarding the benefits of this strategy when used in women over 50 years old and the USPSTF recommends a mammogram every two years, in women between 50 and 74; however, this same agency does not consider that there is enough evidence to support mammographic screening from 40 to 49 years old in asymptomatic patients without increased risk to breast cancer [12]. This recommendation is due to the fact that screening in this age range results in a smaller number of prevented deaths when compared to more advanced ages; also leads to a larger number of unnecessary biopsies; and to the possibility of psychological problems, like anxiety, because of the large number of false-positive results. While mammographic screening of 10,000 asymptomatic women between 50 and 59 years old can prevent 8 breast cancer deaths, the same strategy adopted in asymptomatic women between 40 and 49 years old would prevent only 3 breast cancer deaths [13, 14]. Another harm associated with mammographic screening of an asymptomatic population considered by the USPSTF when issuing their recommendation is the occurrence of over diagnosis. Although it is extremely complex to calculate the proportion of diagnosed cases that would never evolve to cancer, the best estimates from randomized clinical trials suggest the occurrence of over diagnosis in 20% of the cases due to mammographic screening [15].
Another agency that carefully evaluated the cost–benefit ratio of mammographic screening in asymptomatic women between 40 and 49 years old was the Ontario Health Technology Advisory Committee through a systematic review of the literature [16]. This work included an evaluation of the USPSTF report [17], the Canadian Preventive Services Task Force (CPSTF) report [18], a Cochrane systematic review [19], five health technology assessments and eight randomized clinical trials [20, 21, 22, 23, 24, 25, 26, 27] with the objective to assess the reduction of the breast cancer mortality in this age range attributable to mammographic screening. This agency reached a similar conclusion as the USPSTF that the mammographic screening in an asymptomatic population between 40 and 49 years old is not effective in reducing breast cancer mortality and that the harms associated with this intervention, like exposure to radiation, high rate of false-negatives leading to delays in diagnosis and high rate of false-positives with associated psychological harmful effects should not be overlooked.
The Brazilian College of Radiology (BCR) and Brazilian Society of Mastology (BSM) however issued a different recommendation, based on different published articles of international literature and methodologically inferior to the ones evaluated and with a clear selection bias [25, 28, 29]. In these studies, it was demonstrated a breast cancer mortality reduction between 18% and 38% in the studied populations. The main point to justify the recommendation of mammographic screening for asymptomatic women between 40 and 49 years old is to emphasize that in this developing country there is a higher proportion of breast cancer patients in this age range when compared to developed countries [30]. Despite the fact that it is a recommendation for Brazil, it did not include a single Brazilian study in the analysis. This scenario is repeated throughout Latin America as it has been shown in a report by The Economist Intelligence unit. Cancer care registries are lacking in Latin America due to insufficient coverage of the population and also due to low quality [31]. Without local high-quality data, it is impossible to perform local health technology assessments and the decision-making process is jeopardized.
Carefully considering the recommendations of these three different countries with very diverse populations, we can conclude that although mammographic screening in women between 40 and 49 provide a modest benefit in reducing breast cancer mortality, the occurrence of adverse effects is more pronounced.
We can also note that the BCR and BSM adopt a paternalistic approach, reflecting the principle of beneficence. In the meantime, the USPSTF and the CPSTF advocate that the screening decision should be shared with the patient. This way, patients that are more risk averse could opt out of the screening program and patients that value more the potential benefits could opt in, following the principles of non-maleficence and autonomy. However, what we must ask is whether it is possible to convey important information regarding the risks associated with a screening program in a clear and, more important, neutral manner. In this sense, it is of utmost importance that the autonomy principle is respected and that patients are not manipulated to undergo tests or treatments which they do not agree with, due to the use of biased information.
Addressing this issue, Biddle introduced the concept of epistemic risk, defined as the risk of error that comes up at any moment in the process of knowledge production [32]. These errors can happen because of biases during the data collection step and also because of decisions made in scenarios of uncertainty. These decisions reflect the set of values of the involved researchers and have consequences to human health and to the definition of public policies. Rudner agrees with this argument and suggests that it’s impossible to prove any hypothesis with full certainty, as there is always a possibility of error. This way, researchers must judge what is the necessary amount of data to accept or reject a hypothesis and this judgment depends on the set of values of the researcher and on the importance of the consequences an error can lead to [33]. Pramesh et al. discuss such a conflict in depth when they justify the necessity of a randomized clinical trial to prove a hypothesis raised by a cross-sectional study, as they believe the data gathered in the latter is not sufficient to support the decision-making process [34].
The reasoning to support a mammographic screening program for asymptomatic women below the age of 50 is not free of the risk of epistemic risks. One kind of epistemic risk associated with to mammographic screening is the inductive risk, defined as the risk of incorrectly accept or reject a hypothesis based on the available evidence [35]. Breast surgeons must accept or reject that a patient has a disease, frequently a ductal carcinoma in situ (DCIS), that will evolve causing symptoms and death based on evidence that does not guarantee the veracity of this hypothesis. That happens mostly because of the lack of evidence to predict which cases of DCIS will evolve to become invasive carcinomas. Another epistemic risk, the one in the gathering of data of breast biopsies, occurs in the evaluation of the differential diagnosis between atypical hyperplasia and DCIS. While the first ones are treated with a small surgical procedure, the latter requires surgical excision followed by radiation therapy and, in some cases, endocrine therapy for 5 years. This way, an error committed by the pathologist might lead to an enormous impact in the treatment of the patients. As pathologists have different formations and different experience backgrounds, and as the biopsy evaluation is a subjective process, this is an epistemic risk that is hard to be assessed. In order to try and decrease the odds of such an error is the development of image analyses software. Mercan et al. evaluated 240 breast biopsies comparing the performance of three experienced pathologists and an automated image analysis method. In this study, the automated method performed better than the pathologists in differentiating atypical hyperplasia and DCIS, becoming a promising alternative for the near future [36]. As we saw in these two examples, the information conveyed to the patients eligible to screening are not obtained in the absence of the researchers personal judgment and values. Thus, more than just respecting the autonomy principle in the shared decision-making process, healthcare workers must convey not only the necessary information but also their values and personal beliefs used by them to define their diagnostic and therapeutic decisions. As long as there is ambiguity in the results of mammographic screening studies in asymptomatic women below the age of 50, the priority should be debating the advantages and disadvantages of this strategy, instead of discrediting their opponents [37].
In Brazil, as in many developing countries, there is no public policy to the implementation of an organized mammographic screening program. As mentioned previously, there is a recommendation from the Brazilian National Cancer Institute (INCA) for mammogram every two years for women between 50 and 69 years old [7] and the main medical societies recommend an annual mammogram for women starting at 40 years of age [30].
This difference in recommendations happens due to complex interactions between the country’s decision makers’ interests, beliefs, perspectives and personal values. In the present scenario, with this disparity of recommendations, patients present late stage diagnosis, worse than the ones observed in Norway before the implementation of the local mammographic screening program (Table 2) [38].
Stage | Brazil (n = 22,527) | Norway (n = 26,883) |
---|---|---|
I | 21.3% | 48.5% |
II | 35.2% | 38.5% |
III | 25.2% | 5.3% |
IV | 8.9% | 6.5% |
Unknown | 1.6% | — |
Prevalence of breast cancer according to stage in the state of São Paulo between 2000 and 2017, and in Norway before the implementation of mammographic screening.
Adapted from Tiezzi et al. [38].
To evaluate the necessity to expand the INCA’s recommendation to other age ranges, Brito et al. analyzed all breast cancer cases, all DCIS cases and all breast cancer related deaths in the city of Aracaju between 1998 and 2014, dividing pages according to age groups [39]. The breast cancer incidence trends remained stable over the studied period across all age groups. Both incidence and cancer-specific mortality in that municipality were similar to the ones observed in countries with the same human development index. The authors concluded that, as these rates remained stable in all age groups, including the ones in which screening is recommended, the investment of public resources to screen women below the age of 50 or over the age of 69 is not justifiable.
A broader study by Rodrigues et al. evaluated retrospective data regarding mammograms between 2008 and 2016 in the public health system [40]. Around nineteen million mammograms were performed in this period with an increase in coverage of 14.5% annually between 2008 and 2012 followed by a stable period between 2012 and 2017. The population coverage of mammogram varied in the period from 14.4% to 24.2% of the target population. This number is far from the 70% coverage recommended by the WHO, necessary to effectively reduce breast cancer-specific mortality [41]. Rodrigues et al. also evaluated the number of mammogram machines available in the country, their geographical distribution and the total number of exams performed in 2016 [42]. In this study, it was demonstrated that Brazil has 4628 machines with a capacity of 14,279,654 exams per year. In 2016, however, only 4,073,079 exams were performed, 29% of the total capacity, displaying a clear under-use of the available infrastructure. The low coverage of the target population with the stable trend in the past few years associated with the under-use of the available infrastructure raises the hypothesis of the existence of barriers to access to the healthcare system.
The Barretos Cancer Hospital adopted an alternative to improve the coverage of the screening program with the use of mobile mammogram machines in trucks reaching 108 municipalities in the northeastern region of São Paulo, targeting women between 40 and 69 years old. Greenwald et al. evaluated the efficacy of this initiative from 2010 to 2015 [43] and, in this period, 122,634 women were evaluated with a coverage of 54.8% of the target population, referral of 12.25% of these women were referred for additional exams with a cancer detection rate of 3,63/1000 women. 92.51% of the referrals to treatment centers were successfully accepted. The results obtained by this program are very promising, showing the potential to be expanded to other regions and other countries.
Brazil is a developing country with a population of 209.3 million inhabitants with enormous social and economical disparities between its 5 regions [44]. Moreover, there are also inequalities in the distribution of human resources and health infrastructure with a significant variation in the number of hospital beds and physicians dedicated to oncological patients leading to significant differences in health outcomes [8]. Another source of outcome variability is the duality of access to the healthcare system. Every Brazilian citizen has unrestricted access to the public health system (PHS) and the richer portion of the population also has access to private healthcare providers through out-of-pocket direct expending or through healthcare insurance companies. This duality of the system is perverse in a way that it perpetuates the idea that a small portion of the population has access to state-of-the-art diagnostic and treatment facilities while the majority of the population, around 71%, depends exclusively on the PHS with all its limitations. When comparing this two scenarios, we observe a striking difference in the initial stage of the breast cancer patients; the majority of the patients seen in the private setting is diagnosed with early stage tumors, whereas the majority of patients that depend on the PHS is diagnosed with locally advanced tumors [45], a clear indication that difficulties to access the healthcare system are the main obstacles to early detection. 37% of the breast cancer cases diagnosed in the PHS are stage III or IV while in the private sector this number falls to 16.2% [46]. These data are corroborated by national studies that showed intervals of 75 to 185 days between initial symptom presentation and initial biopsy [45] and a median interval of 113.4 days between indication and initiation of radiation therapy [47]. For comparison purposes, patients seen in the private setting can have diagnostic tests and start treatment in less than 30 days.
To identify the main barriers to access to the PHS, Vieira et al. conducted a systematic review of the literature identifying 30 publications on this topic [48]. In a general analysis, it has been identified an underuse of mammogram machines on the north and northeast regions of the country and a mammogram coverage of only 35% of the Brazilian women, most of them in the private setting. The main issues related with not having a mammogram performed are non-white ethnicity, low educational level, low familiar income and not having health insurance. Another interesting finding of this study is that normally the treatment of breast cancer is performed in big cities and patients end up traveling more than 100 miles from their residences to the hospitals [49]. Even before the start of treatment, patients have to face delays of more than 60 days in 36.9% of the cases, because of inefficient referral and navigation. The main issues related with delays in the initiation of treatment were non-white ethnicity, not having a partner, low educational level, early stage breast cancer and dependence of the PHS [50]. Exclusive dependence on the PHS and non-white ethnicity were also associated with higher breast cancer-specific mortality [51].
Considering the inefficacy of the screening programs in developing countries and the lack of solid evidence supporting screening of asymptomatic women below the age of 50 years old, we recommend resources reallocation to improve access to the healthcare system and the implementation of a fast track between diagnostic and treatment facilities to symptomatic patients, based on the hierarchical flow proposed by Migowski et al. (Figure 1) [52]. This algorithm proposes three different actions: educational activities in primary care facilities to raise awareness regarding breast cancer and also the potential benefits and harms of mammographic screening; to offer the option of screening mammogram to asymptomatic women aged 50 to 69 during their visit to the primary healthcare provider; and to promote priority access to symptomatic patients, without the need of prior scheduling, in which the ones with suspicious lesions will be referred to diagnostic facilities. This recommendation is supported by Rawls’ two principles of justice [9]. The first principle governs that all persons have equal rights and freedoms. The second principle governs that the adoption of policies that generate social or economical inequalities is only acceptable if it favors the least advantaged portion of society. The promotion of educational activities proposed by Migowski et al. [52] is supported by Rawls’ first principle since it standardizes the access to a basic right, education. The second part of the recommendation is justified by Rawls’ second principle of justice. The adoption of a fast track to symptomatic patients, removing the need of a prior appointment or referral, promotes the reallocation of public resources to remove barriers in the access to care, reducing delays in diagnosis and treatment and, therefore, reducing inequalities in favor of the least advantaged part of the population that relies solely in the public health system. Although the recommendation favors a part of the population, it does not violate individual rights, as asymptomatic patients will still have access to screening mammogram in their routine visits to their primary healthcare providers. Moreover, the proposed recommendation promotes equal access to breast cancer diagnosis and treatment as it removes the age boundaries, starting to provide care to women below the age of 50 years old, an age range responsible for a large amount of new cases in developing countries and that were not previously included in the past recommendation [6].
Hierarchical flow to promote early diagnosis and treatment of breast cancer. Adapted from Migowski et al. [52].
Let us consider for a moment a hypothetical scenario in which the healthcare system works perfectly without any access barriers. Even in this setting, mammographic screening as it is currently suggested would not be ideal in developing countries. The current evidence that recommends mammographic screening is not unanimous and large randomized clinical trials did not show a robust mortality reduction attributable to it [13, 53]. Moreover, even if these studies showed a significant mortality reduction attributable to screening mammogram, their results would hardly be applicable to the developing countries’ realities. Those studies were conducted in countries with high human development index (HDI) and in the context of organized screening. Brazil and most developing countries have lower HDIs and promote opportunistic screening due to the weak organizational structure of the healthcare system. This way, the international studies that assessed the effectiveness of mammographic screening lack the necessary external validity to be applied in developing countries. A recent article published by Vale et al. suggested, that the opportunistic screening program employed in the state of São Paulo, Brazil, promoted an increase in early stage diagnosis without, however, presenting data regarding mortality reduction [54]. Without data showing mortality reduction attributable to the screening program it is impossible to conclude whether this model is effective or not. Adding up to that data we have some concerning facts associated with screening women between the age of 40 and 49; we observe that less than one death from breast cancer is avoided for every one thousand screening mammograms performed; two hundred and ninety-four false-positive results (Table 1) generate additional diagnostic procedures leading to economical impact to the health system and also physical and psychological impacts to the patients. Based on everything that was exposed in this paragraph, we can conclude is not adequate from Bentham’s and Mill’s utilitarianism perspective [10, 11].
In this context, with the shortage of resources to invest in an organized mammographic screening program and without solid data to justify its implementation, can we accept a sub-optimal program? On the one hand, the inexistence of a screening program can lead to the increase in the number of cases diagnosed in late stages, for which the treatment options might be inaccessible and, sometimes, ineffective. On the other hand, developing countries, such as Brazil, sometimes lack the necessary infrastructure to perform timely screening mammograms to the whole eligible population and the consequent breast biopsies of lesions identified through screening [55]. In order to consider a screening program adequate, it must be acceptable, accessible, and sustainable, it must promote equity and it must be economically efficient to the target population [56]. As it has been demonstrated in this chapter, the Brazilian mammographic screening program is not accessible, since the coverage does not reach 30% of the target population [42]. This program is not sustainable either since there is a huge delay between the identification of an abnormal mammogram and the necessary biopsy to confirm the diagnostic. Due to the incapacity to adequately follow-up and refer patients with abnormal findings, the risk of a false-positive result must be considered clinically and ethically relevant. Finally, it’s been demonstrated that mammographic screening in developing countries is not cost-effective when compared to the alternative of treating patients with palpable initial lesions [57, 58]. Contemplating all these issues, Sedhom et al. argued that clinical examination of the breast with fast referral to avoid delays in diagnosis and treatment, although not a screening program, must be considered a more pragmatic and adequate choice than screening mammogram in developing countries [59].
When weighing the benefits and harms of a mammographic screening program in a developing country, in a context where breast cancer-specific mortality has been increasing in the past few decades, it is extremely hard to justify increasing the age range to women aged 40 to 49 years old from an utilitarian perspective, since the amount of resources to establish and make the system work adequately is prohibitive. An alternative strategy that promotes easy access and fast referral of symptomatic patients, relegating a secondary role to mammographic screening, favors a larger and more vulnerable part of the population that depends solely on the PHS. This reallocation of resources to favor the least advantaged members of society is not only ethically justifiable but also a way of promoting social justice.
Rodrigo Goncalves has received consultation fees from EMS Pharmaceuticals in 2019 and 2020 and from Novartis in 2019, not related to the topics of this chapter.
The remaining authors do not have any conflicts of interest to disclose.
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