thesis on yogurt

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• J Food Sci Technol
• v.55(5); 2018 May

Effect of culture levels, ultrafiltered retentate addition, total solid levels and heat treatments on quality improvement of buffalo milk plain set yoghurt

Vijesh yadav.

Room No: 145, By-Products Lab, Dairy Technology Division, ICAR-National Dairy Research Institute, Karnal, Haryana 132001 India

Vijay Kumar Gupta

Ganga sahay meena, associated data.

Studied the effect of culture (2, 2.5 and 3%), ultrafiltered (UF) retentate addition (0, 11, 18%), total milk solids (13, 13.50, 14%) and heat treatments (80 and 85 °C/30 min) on the change in pH and titratable acidity (TA), sensory scores and rheological parameters of yoghurt. With 3% culture levels, the required TA (0.90% LA) was achieved in minimum 6 h incubation. With an increase in UF retentate addition, there was observed a highly significant decrease in overall acceptability, body and texture and colour and appearance scores, but there was highly significant increase in rheological parameters of yoghurt samples. Yoghurt made from even 13.75% total solids containing nil UF retentate was observed to be sufficiently firm by the sensory panel. Most of the sensory attributes of yoghurt made with 13.50% total solids were significantly better than yoghurt prepared with either 13 or 14% total solids. Standardised milk heated to 85 °C/30 min resulted in significantly better overall acceptability in yoghurt. Overall acceptability of optimised yoghurt was significantly better than a branded market sample. UF retentate addition adversely affected yoghurt quality, whereas optimization of culture levels, totals milk solids and others process parameters noticeably improved the quality of plain set yoghurt with a shelf life of 15 days at 4 °C.

Electronic supplementary material

The online version of this article (10.1007/s13197-018-3076-3) contains supplementary material, which is available to authorized users.

Introduction

Yoghurt has been defined as the coagulated product obtained from the mixture of pasteurised milks (skim, concentrated, boiled) and cream by lactic acid fermentation through the action of Lactobacillus bulgaricus and Steptococcus thermophiles provided that its titrable acidity (TA) as lactic acid (LA) shall not be less than 0.85% and not more than 1.2%. The health benefits of yoghurt as the fermented product are well documented. Prajapati and Sreeja ( 2013 ) reported that yoghurt is generally made from cow milk with adjusted total solids (TS) in the range of 14–16% by inoculating with the mixture of Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus thermophilus and incubating at 42 °C to achieve the desired acidity. It contains typical acetaldehyde flavor.

Because of higher fat, lactose, protein (particularly caseins) and minerals (calcium, magnesium and inorganic phosphate), buffalo milk yoghurt possesses superior body and texture than cow milk yoghurt (Ahmad et al. 2008 ). The rate of acid production, extent of proteolysis and flavour (acetaldehyde) development by lactic cultures in buffalo milk yoghurt was also higher (Khanna and Singh 1979 ). Different yoghurt variants based on texture (liquid, set and stirred curd), flavour (natural or plain, fruit, cereal, chocolate) and fat contents (normal, reduced and fat-free) are available in the market. However, yoghurt possesses its own set of problems related to colour and appearance (lumpiness, free whey, a typical colour, colour leaching, lack or excess of fruits in case of fruit yoghurt); flavour (high acetaldehyde, bitter, cooked, low and high acid, foreign, metallic, oxidized, unclean and rancid); body and texture (free whey, gel like or too firm, weak, shrunken, grainy and ropy body) as indicated by several researchers. Consumers are now becoming even more discerning and demands products with improved sensory attributes, enriched with nutrients and manufactured from natural components with simple and clear labels. This leads to development of different types of dahi (Indian yoghurt) and yoghurts such as dietary fiber (soy, oat and inulin) enriched yoghurt (Raju and Pal 2014 ); low-fat set-type yoghurt (Pakseresht et al. 2017 ); flaxseed oil and flour incorporated fruit yoghurt (Kumar et al. 2017 ); low phenylalanine yoghurt (Goldar et al. 2016 ); Bambara groundnut ( Vigna subterranea ) and soybeans ( Glycine max ) based yoghurt (Falade et al. 2015 ); yoghurt containing candied chestnut (Sakin-Yilmazer et al. 2014 ); omega-3 fatty acids fortified Indian yoghurt (Goyal et al. 2016 ); β-glucan fortified dahi (Bhaskar et al. 2017 ) etc.

Sensory attributes and rheological properties of fermented milk products are mainly governed by their total solids content. Meena et al. ( 2015 ) successfully improved the quality of buffalo milk plain dahi employing ultrafiltration (UF). This also resulted in quality improvement and increased nutritive value of yoghurt due to concentration of protein, calcium and phosphorus in retentate. Higher casein contents in UF retentate have been related to the reinforcement of the protein matrix density that leads to improved water holding capacity of the yoghurt gel (Sodini et al. 2004 ). Thus, it is believed that higher protein content results in better overall quality of the curd. Heat treatment of milk is vital for elimination of growth inhibitors and denaturation of serum proteins as it affects texture, microstructure, and rheology of yoghurt. Homogenization of standardised milk is an inevitable step in the yoghurt manufacturer to improve its consistency and whiteness; reduce whey syneresis and prevent fat separation during fermentation and storage. Therefore, to reduce or eliminate the common defects encountered in conventional yoghurt, optimisation of culture levels, milk solid levels maintained by the addition of different ingredients, time–temperature combination of applied heat treatments and UF retentate addition becomes mandatory.

Considering all these points the quality of buffalo milk plain yoghurt was improved through the optimization of heat treatment, milk solids and culture levels; and the changes in its sensory attributes and rheological parameters during refrigerated storage at 4 °C were studied.

Materials and methods

Milk and skimmed milk powder (smp).

The fresh buffalo milk of Murrah breed was procured from Livestock Research Center of National Dairy Research Institute, Karnal; separated at 45 ± 2 °C in a cream separator (Make: Chadha Electro Industries, Delhi; Capacity of 110 L/h) to obtain fresh skim milk (< 0.5% fat) and cream of 65–70% fat.

Fresh buffalo skim milk had 9.98 ± 0.08, 0.26 ± 0.03, 3.80 ± 0.02, 0.79 ± 0.01; 6.60 ± 0.01 and 0.165 ± 0.03% TS, fat, protein, ash contents, pH and TA (% LA) values, respectively. The SMP was procured from M/s Modern Dairies Ltd., Karnal. As per the manufacturer, this SMP was produced from mixed milk and was medium heat treated.

Propagation of yoghurt culture and estimation of lactic acid bacteria counts

Good quality yoghurt of reputed brand containing mixed culture of S. thermophilus and L. bulgaricus was used as yoghurt culture. This culture was propagated in sterilized skimmed milk with 1.5% culture inoculation in a laminar air flow chamber, followed by incubation (45 ± 2 °C/6 h) and refrigerated storage at 4 °C.

Total counts of lactic acid bacteria were estimated in the yoghurt samples by using the yeast extract lactose agar medium adopting the method reported by Sivakumar and Kalaiarasu ( 2010 ).

Packaging materials

Yoghurt samples were packed and stored in 100 mL polystyrene cups sourced from the Experimental Dairy of the institute.

Ultrafiltration

Buffalo skim milk was indirectly flash heat treated to 80 °C, cooled (~ 50 °C) and concentrated in a pilot scale ultrafiltration plant (Make: Tech-Sep France; Module type: tubular; Membrane material, area and cutoff: ZrO 2 , 1.68 m 2 and 50,000 kDa) equipped with balance tank (200 L) and flow meters to 3.87 concentration factor (CF) also called folds. The CF was calculated by weighing the quantity of permeate removed from the skim milk. During operation of UF plant, inlet pressure, outlet pressure and transmembrane pressure (TMP) were kept constant to 4.6, 3.6 and 1 kg/cm 2 , respectively during entire UF operation (Meena et al. 2016 ).

Standardisation, homogenization and heat treatment of buffalo milk and preparation of different yoghurt samples

The selection of culture and TS levels, retentate addition and heat treatments were carried out on the basis of their effect on TA, pH, sensory scores and rheological parameters of yoghurt samples. Buffalo milk was first standardized to 3.25% fat and 13.70–13.80% TS contents with the addition of SMP and cream; homogenized at 2500/500 psi pressures in 1st and 2nd stage at 65–70 °C; heat treated at 85 °C for 30 min; cooled and inoculated with 2, 2.5 and 3% culture levels for the selection of culture level. Similarly, fat and TS levels were also adjusted in buffalo milk containing 0, 11 and 18% 3.87-folds UF retentate with the addition of SMP, cream and water.

For studying the effect of different total solids levels, buffalo milk was standardised to 3.25% fat and 13–14% TS levels with cream and SMP addition and inoculated with the pre-selected culture level. For the studying the effect of heat treatment, standardised milk containing 3.25% fat and earlier selected TS level was individually heat treated for 30 min at 80 and 85 °C followed by its inoculation with pre-selected culture level.

A standardised method for the preparation of optimised yoghurt was developed using the selected levels of culture, TS and heat treatment as shown in Supplementary Fig. 5a. Sensory quality attributes of optimised yoghurt were also compared with a fresh market sample of a reputed brand. The effect of storage period on quality attributes of optimised yoghurt was studied at 4 ± 1 °C.

Thus, milk samples containing different levels of total solids (maintained with or without the addition of UF retentate), subjected to different heat treatments were homogenized, inoculated with yoghurt culture and filled into pre-sterilized polystyrene cups (100 mL), incubated at 42 °C till required minimum TA (0.90% LA) was achieved. Thereafter, without disturbing, these cups containing plain set yoghurt were instantly transferred to refrigerated storage (4 ± 1 °C). All the trails were conducted in triplicate.

Compositional analysis, whey syneresis and textural analysis

The TS, fat, protein, lactose, ash, pH and TA (% LA) values of buffalo skim milk, UF retentate and yoghurt samples were determined in triplicate using standard methods as reported by Meena et al. ( 2015 ) for plain dahi . Moreover, determination of spontaneous whey syneresis and texture analysis of undisturbed plain set yoghurt samples were conducted adopting the procedure reported by Meena et al. ( 2015 ).

Sensory evaluation

A panel of six discriminative and trained judges consisting the faculty of Dairy Technology Division of the institute, performed the sensory evaluation. Yoghurt samples were randomly taken out from the refrigerator (4 ± 1 °C), tempered to 20 °C and then served to judges for sensory evaluation. The samples were evaluated on 100 point score card suggested for yoghurt by Ranganadham and Gupta ( 1987 ). This score card contains maximum 45, 30, 10, 10, 5 marks for flavour, body and texture, acidity, colour and appearance and container and closure, respectively.

Storage study

Samples of optimised yoghurt were filled in 100 mL polystyrene cups and fitted with the cover and investigated for its storage quality during refrigerated storage at 4 ± 1 °C at a constant interval of 3 days up to 18 days.

Statistical analysis

Results obtained in this investigation were subjected to analysis of variance using a complete randomized design and randomized block design as reported by Snedecor and Cochran ( 1968 ). Mean values of two different samples were compared with each other using t test. Mean ± Standard Error (S.E.) were also calculated, wherever required.

Results and discussion

Chemical composition of buffalo skim milk and uf retentate.

The percent TS, fat, protein, lactose and ash in 3.87-fold UF retentate were 22.17 ± 0.61, 0.97 ± 0.18, 14.21 ± 0.67, 4.48 ± 0.08, 2.20 ± 0.04, respectively. The constituents of buffalo skim milk were at par with the earlier reported values by Patel and Mistry ( 1997 ). UF concentration of skim milk markedly increased the constituents in retentate except lactose. Such decrease in lactose with subsequent increase in other milk constituents in retentate have also been reported by Patel and Mistry ( 1997 ) during UF concentration of buffalo skim milk to 1.33, 2.0, 2.85 and 4.34 folds.

Selection of yoghurt culture levels

Yoghurt samples prepared with 2, 2.5 and 3% yoghurt culture levels took 7, 6.5 and 6 h, respectively for achieving the required minimum TA of 0.90% LA. As expected, with increased culture addition, highly significant increase ( p  < 0.01) in the rate of TA development and the decrease in pH of yoghurt were observed. Atta et al. ( 2009 ) had also observed a similar increase in TA and decrease in pH with higher culture addition. At 3% yoghurt culture addition, minimum required TA (0.90% LA) was achieved in least time (6 h). Decreased incubation time leads to reduced cost of yoghurt production. Highly significant increase ( p  < 0.01) in body and texture and overall acceptability scores were observed with an increase in culture levels, but no significant difference was observed in flavour, acidity and colour and appearance scores because of the approximately similar acidity of all yoghurt samples. Whey syneresis was absent in these samples. Moreover, rheological parameters of these samples were statistically at par with each other. Therefore, based on minimum incubation period (i.e. 6 h) required to achieve minimum TA (0.90% LA) and better sensory scores of yoghurt, the addition of 3% yoghurt culture was selected for the further study.

Selection of UF retentate addition

The chemical composition of the yoghurt samples prepared with the addition of different amounts of UF retentate in milk, inoculated with 3% yoghurt culture, are presented in Table  1 . The fat, TS contents and pH values were almost similar in all yoghurt samples. With higher UF retentate addition, protein and ash contents of yoghurt samples increased, but lactose contents decreased progressively. More UF retentate addition in milk leads to highly significant decrease ( p  < 0.01) in the rate of TA development and also decreased pH during incubation. The yoghurt samples prepared with 0, 11 and 18% addition of UF retentate took 6, 6.5 and 7 h, respectively for achieving 0.9% LA TA. This was accorded to higher buffering capacity of the added UF retentate as its high protein contents resisted the change in TA or pH than control milk. Mistry and Kosikowski ( 1986 ) also observed such increase in protein content and buffering capacity of UF retentates with the progression of UF process. Higher buffering capacity of UF retentate requires longer incubation time to attain the desired pH than normal milk and this phenomenon could easily explain that why higher incubation time was taken by retentate added samples to achieve the same TA level. Christopherson and Zottola ( 1989 ) also reported fast rate of drop in pH in skim milk than UF retentate.

Table 1

Chemical composition of yoghurt samples prepared from the milk of different total solids and with the addition of different amounts of 3.87-fold UF retentate

Mean ± S.E. (n = 3)

Highly significant ( p  < 0.01) decrease in body and texture, colour and appearance and overall acceptability scores of yoghurt prepared with 11 and 18% addition of UF retentate were observed compared to yoghurt made without retentate addition. Slight whey syneresis was observed in yoghurt samples prepared from milk containing 18% UF retentate and the same might be responsible for lower colour and appearance scores. Further, this yoghurt contain higher protein content that resulted in much dry, extra firm and lack of smoothness in its texture that also decreased its body and texture and overall acceptability scores. Abrahamsen and Holmen ( 1980 ) also reported that yoghurt manufactured from UF retentate added milk exhibited higher viscosity and firmer (too dry and pudding like) texture, because of its higher protein content. Such changes also underline the lack of proper texture in terms of lower sensory scores of yoghurt prepared from 18% UF retentate added milk in this study. However, acidity and flavour scores of all yoghurt samples were statistically at par with each other.

In comparison to yoghurt made from normal milk, highly significant increase ( p  < 0.01) in rheological parameters of yoghurt samples prepared from different UF retentate added milks were observed as shown in Table  2 . A little whey syneresis (0.30 mL) was only observed in yoghurt manufactured from 18% retentate added milk, which may be due to its longer incubation period. Garg and Jain ( 1980 ) reported that rheological parameters of curd such as hardness and adhesiveness increased with increase in its protein content. Thus, yoghurt prepared from normal milk (without retentate addition) was considered of better quality by judges based on its sensory attributes. Even a little extra firmness was reported by judges in this yoghurt also, so a need was felt here to optimize TS level in standardized milk in order to produce buffalo milk based plain yoghurt with better sensory attributes and rheological parameters.

Table 2

Effect of retentate addition, TS levels and heat treatments on rheological attributes of different yoghurt samples

Firm . Firmness, Stick . Stickiness, WOS Work of shear, WOA work of adhesion

# Mean values (n = 3), *Significant at p  < 0.01, NA not applicable

Selection of total solid levels

The chemical composition of yoghurt samples produced from normal buffalo milk with different TS levels are shown in Table  1 . It was observed that protein content increased progressively in yoghurt samples with the increase in their TS levels.

The rate of TA development and decrease in pH during the incubation period in yoghurt samples prepared with normal buffalo milk with different TS levels were statistically at par with each other. Flavour, body and texture, colour and appearance, and overall acceptability scores of yoghurt prepared with 13.50% TS were highly significantly ( p  < 0.01) better than that of yoghurt prepared with 13 and 14% TS levels. However, body and texture, colour and appearance and overall acceptability scores of yoghurt prepared with 13% TS containing milk were lower because of its weak body and visible whey syneresis in this sample only. On the other side, body and texture and overall acceptability scores of yoghurt prepared from milk containing 14% TS decreased due to its higher firmness as pointed by the sensory panel. These findings are in good agreement with that reported by Mohammeed et al. ( 2004 ); Sodini et al. ( 2004 ) who have underlined that higher TS levels are responsible for increased oral viscosity or perceived thickness, decreased whey syneresis and better texture acceptability of yoghurt samples over lower TS containing samples. Further, with increase in TS levels, significant increase ( p  < 0.01) in firmness, stickiness, work of shear and work of adhesion were observed in yoghurt samples (Table  2 ). The yoghurt sample prepared from standardized milk containing 13.50% TS fetched maximum scores. Increase in TS levels have been reported to decrease the whey syneresis with higher water holding capacity and gel firmness in yoghurt (Shaker et al. 2000 ). Harwalkar and Kalab ( 1986 ) reported that 10–20% increase in TS levels increased yoghurt firmness by 2–3 folds. Because of this reasons, rheological parameters of yoghurt prepared with 13.50% TS were observed significantly ( p  < 0.01) better than that prepared with either 13 or 14% TS levels. Thus, based on better sensory scores and rheological parameters, yoghurt prepared with 13.50% TS was observed to be of the optimum quality.

Selection of heat treatments

The rate of TA development and decrease in pH of yoghurt samples prepared employing different heat treatments (80 °C/30 min and 85 °C/30 min) were statistically at par with each other. In studied temperature range, increase in heating temperature significantly improved ( p  < 0.01) the body and texture and overall acceptability scores, but no-statistical difference was observed in other sensory attributes of yoghurt samples. Body and texture and overall acceptability scores of yoghurt made from high heat treated (85 °C/30 min) milk were significantly higher ( p  < 0.01) than the yoghurt produced from low heat treated (80 °C/30 min) milk as maximum hydration of the protein occurs when milk is heated at 85 °C for 30 min. Lee and Lucey ( 2003 ) reported that ‘in-mouth’ and ‘in-cup viscosities’ of yoghurt made from milk heated at 85 °C were increased by 4–8 times than yoghurt made from milk heated at 75 °C, because of the presence of more cross-linked and branched protein structure (fine structure) with small pores in the high heat treated milk (> 80 °C) than large protein clusters (coarse structure) present in low heat treated milk. Lucey et al. ( 1998 ) also reported that heating of milk (≥ 80 °C/15 min) resulted in significantly increased denaturation of β-lactoglobulin than milk heated at 75 °C/15 min. Firmness, stickiness, work of shear and work of adhesion of yoghurt samples were significantly ( p  < 0.01) increased with increase in heating temperature (Table  2 ). However, whey syneresis was not observed in yoghurt samples prepared from different heat treatments. Dannenberg and Kessler ( 1988 ) reported that the extent of whey protein denaturation in milk during heating had significant impact on viscosity and firmness of acid gel and the same increases with increase in heating temperature (Lee and Lucey 2006 ). Results obtained in this study are similar to that reported by Abd El-Khair ( 2009 ) who emphasized that even at a same protein level, due to difference in the extent of whey protein denaturation, yoghurts made from high heated milk had higher firmness than that produced from low heat treated milk. Thus, based on better sensory scores and rheological parameters of yoghurt, heat treatment of 85 °C/30 min was selected and further used to produce optimized yoghurt sample.

Comparison of sensory quality of optimized yoghurt vis â vis market sample

Optimized yoghurt sample was produced adopting the process shown in Fig.  1 . The comparison of sensory scores of optimized yoghurt and a reputed market sample revealed that body and texture, acidity and overall acceptability scores of optimized yoghurt were significantly ( p  < 0.01) better than market sample, while other sensory attributes showed no-statistical difference. Optimized yoghurt had 13.57% TS, 3.25% fat, 4.15% protein, 5.03% lactose, 0.83% ash (Table  1 ) and met FSSAI ( 2011 ) standards in terms of its chemical composition. Firmness, stickiness, work of shear and work of adhesion of optimized fresh yoghurt were 3.075 N, − 0.508 N, 85.352 N s and − 3.377 N s, respectively. Optimized set plain yoghurt had the firm body and smooth texture without any whey syneresis compared to 0.6 mL whey syneresis in the market sample. Optimized yoghurt was highly preferred over market sample by the sensory panel.

Standardized process for the production of optimized yoghurt

Storage studies: effect of storage period on the sensory quality and microbial counts of optimized yoghurt

The changes occurred in TA and pH values, sensory attributes and rheological parameters of optimized yoghurt indicated that with advancement of the storage period, significant increase ( p  < 0.01) in TA and significant decrease ( p  < 0.01) in pH values of optimized yoghurt were observed. The TA and pH values of yoghurt samples at zero day (fresh) and after 18 days storage were 0.94% LA, 4.33 and 1.20% LA, 1.20% LA, respectively. This might be attributed to TA development by yoghurt culture in yoghurt during storage was continued even at 4 ± 1 °C, but with the lower rate of acid production. These changes in TA and pH values in yoghurt during storage were in good agreement with that previously reported by Atta et al. ( 2009 ); Obi et al. ( 2010 ). Highly Significant decrease ( p  < 0.01) in all sensory scores of yoghurt particularly between 15th to 18th day of storage were observed, that might be due to increase in TA that resulted in visible whey syneresis in yoghurt samples on the 18th day of storage. Rheological parameters of yoghurt increased highly significantly ( p  < 0.01) during first 15 days of storage followed by a steep deterioration from 15th to 18th day of storage (Table  3 ) that could be related to change in pH of yoghurt samples. Similar changes were also observed in firmness and stickiness of yoghurt samples during storage by Köse and Ocak ( 2011 ). Salvador and Fiszman ( 2004 ) reported increased whey syneresis and firmness in whole and skimmed milk yoghurts over storage period.

Table 3

Effect of storage period on rheological parameters of optimized yoghurt

Mean values (n = 3)

Lactic acid bacteria (LAB) counts of yoghurt steeply decreased from the initial value of 9.67 to 7.85 cfu/g on the 18th day of storage. Obi et al. ( 2010 ) also observed a decrease in the total viable count in yoghurt throughout the storage. On the basis of sensory scores, rheological parameters and TA (1.21% LA), the shelf life of optimised yoghurt was observed to be of 15 days at refrigerated storage.

This study was aimed to improve the quality of plain set yoghurt by optimizing different culture levels, amount of retentate addition, TS levels and heat treatments. The desired acidity in yoghurt was achieved in least 6 h with 3% culture addition. Addition of 11 and 18% 3.87 fold UF retentate in milk resulted in slower TA development, because of increased protein content and buffering capacity and had detrimental effect on sensory attributes because of increased firmness in yoghurt samples. The overall quality of yoghurt prepared with 13.50% TS was significantly better than that prepared with 13 and 14% TS levels. Body and texture and overall acceptability scores of yoghurt prepared with heat treatment of 85 °C/30 min were significantly better than the yoghurt prepared at 80 °C/30 min because of more whey protein denaturation that leads to firm body and smooth texture in yoghurt via optimal cross linking, interaction and hydration of proteins. Optimized yoghurt met FSSAI ( 2011 ) standards and possessed firm body and smooth texture with no whey syneresis compared to 0.60 mL whey syneresis in a branded market sample. The shelf life of optimized yoghurt was observed to be 15 days at 4 ± 1 °C. This investigation has established that common quality defects of conventional yoghurt can be eliminated through the proper selection of total milk solids, process parameters and culture levels and collectively these are capable to improve the quality of plain set yoghurt.

Below is the link to the electronic supplementary material.

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A comprehensive review on yogurt syneresis: effect of processing conditions and added additives

• Review Article
• Published: 12 April 2022
• Volume 60 , pages 1656–1665, ( 2023 )

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• Masoumeh Arab 1 ,
• Mojtaba Yousefi 2 ,
• Elham Khanniri 3 ,
• Masoumeh Azari 3 ,
• Vahid Ghasemzadeh-Mohammadi   ORCID: orcid.org/0000-0002-1858-3297 4 &
• Neda Mollakhalili-Meybodi 1  

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Yogurt, produced by the lactic fermentation of milk base, is an important dairy product worldwide. One of the essential sensory properties of yogurt is the texture, and some textural defects such as weak gel firmness and syneresis likely occur in various types of yogurts, affecting consumer acceptance. In this regard, various strategies such as enrichment of milk-based with different additives and ingredients such as protein-based components (skimmed milk powder (SMP), whey protein-based powders (WP), casein-based powders (CP), and suitable stabilizers, as well as modification of processing conditions (homogenization, fermentation, and cooling), can be applied in order to reduce syneresis. The most effective proteins and stabilizers in syneresis reduction are CP and gelatin, respectively. Furthermore, yogurt's water holding capacity and syneresis can be affected by the type of starter cultures, the protolithic activity, production of extracellular polysaccharides, and inoculation rate. Moreover, optimizing the heat treatment process (85 °C/30 min and 95 °C/5 min), homogenization (single or dual-stage), incubation temperature (around 40 °C), and two-step cooling process can decrease yogurt syneresis. This review is aimed to investigate the effect of fortification of the milk base with various additives and optimization of process conditions on improving texture and preventing syneresis in yogurt.

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Abbreviations.

Skimmed milk powder

Whey powder

Whey protein concentrates

Whey protein isolate

Whey protein hydrolysate

Carboxymethyl cellulose

Locust bean gum

Exopolysaccharides

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Support for this study provided by Shahid Sadoughi University of medical sciences is gratefully acknowledged.

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Masoumeh Arab & Neda Mollakhalili-Meybodi

Food Safety Research Center (Salt), Semnan University of Medical Sciences, Semnan, Iran

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Student Research Committee, Department of Food Technology, Faculty of Nutrition Sciences and Food Technology/National Nutrition and Food Technology Research Institute, Shahid Beheshti University of Medical Sciences, Tehran, Iran

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MA and NM designed the study. MY, VQ and NM collected the data. EK and MA wrote the initial draft. MY, MA and VQ revised the initial draft and finally all the autohrs approved the final version of manuscript for the submission.

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Arab, M., Yousefi, M., Khanniri, E. et al. A comprehensive review on yogurt syneresis: effect of processing conditions and added additives. J Food Sci Technol 60 , 1656–1665 (2023). https://doi.org/10.1007/s13197-022-05403-6

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Yogurt, cultured fermented milk, and health: a systematic review

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Dennis A Savaiano, Robert W Hutkins, Yogurt, cultured fermented milk, and health: a systematic review, Nutrition Reviews , Volume 79, Issue 5, May 2021, Pages 599–614, https://doi.org/10.1093/nutrit/nuaa013

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Consumption of yogurt and other fermented products is associated with improved health outcomes. Although dairy consumption is included in most dietary guidelines, there have been few specific recommendations for yogurt and cultured dairy products. A qualitative systematic review was conducted to determine the effect of consumption of fermented milk products on gastrointestinal and cardiovascular health, cancer risk, weight management, diabetes and metabolic health, and bone density using PRISMA guidelines. English language papers in PubMed were searched, with no date restrictions. In total, 1057 abstracts were screened, of which 602 were excluded owing to lack of appropriate controls, potential biases, and experimental design issues. The remaining 455 papers were independently reviewed by both authors and 108 studies were included in the final review. The authors met regularly to concur, through consensus, on relevance, methods, findings, quality, and conclusions. The included studies were published between 1979 and 2017. From the 108 included studies, 76 reported a favorable outcome of fermented milks on health and 67 of these were considered to be positive or neutral quality according to the Academy of Nutrition and Dietetics’ Quality Criteria Checklist. Of the 32 remaining studies, the study outcomes were either not significant (28) or unfavorable (4), and most studies (18) were of neutral quality. A causal relationship exists between lactose digestion and tolerance and yogurt consumption, and consistent associations exist between fermented milk consumption and reduced risk of breast and colorectal cancer and type 2 diabetes, improved weight maintenance, and improved cardiovascular, bone, and gastrointestinal health. Further, an association exists between prostate cancer occurrence and dairy product consumption in general, with no difference between fermented and unfermented products. This article argues that yogurt and other fermented milk products provide favorable health outcomes beyond the milk from which these products are made and that consumption of these products should be encouraged as part of national dietary guidelines.

Systematic review registration:   PROSPERO registration no. CRD42017068953.

Fermented dairy foods and beverages were among the first “processed” food products consumed by humans and have been utilized for centuries as a method of food preservation. 1 Today, fermented foods are generally defined as “foods or beverages manufactured through controlled microbial growth and enzymatic conversion of major and minor food components.” 1 Fermented (or cultured) milks, in particular, are made by the addition of suitable bacteria to usually heat-treated animal milk, followed by incubation to reduce the pH, with or without coagulation pretreatment. The most common examples of fermented milks are yogurt, cultured cream and buttermilk, and kefir, although many variations of these products exist based on historical practices, geography, and type of milk. Nonetheless, yogurt is generally defined as a cultured milk product made using Streptococcus thermophilus and Lactobacillus delbrueckii subsp bulgaricus. 2 In most regions, the microbes must be alive and abundant (containing at least 10 7 cfu/g). Again, depending on region, additional microbes that belong to the genera Lactobacillus and Bifidobacterium are also added to provide health benefits, and these so-called probiotic or bio-yogurts now account for much of the yogurt market. 3

Decades of research suggests that consumption of fermented foods, especially fermented milk products, is associated with improved health outcomes. Although milk and dairy products are included in nearly every national dietary guideline, only a few of these specifically recommend fermented foods. 4–6 Recently, several researchers have proposed that sufficient evidence now exists to consider yogurt and other fermented dairy products that contain live bacteria when developing dietary strategies for improving health. 6–9

The human gastrointestinal (GI) tract is colonized by a diverse and complex population of more than a trillion microbes. The gut microbiota performs many critical functions, including protecting the host against potential pathogens, extracting nutrients from dietary constituents, and modulating digestive and immune homeostasis. 10 Although it is well established that the adult human microbiome is relatively stable, 11 , 12 antibiotics, diet, disease, hygiene, and other factors can disturb the composition and function of this ecosystem. 13 Both the microbes associated with the manufacture of fermented foods, as well as microbes added as probiotics, may influence not only the gut microbiota but also other physiological functions. Some of the microbes found in fermented dairy foods have been shown to survive digestion, and reach the distal GI tract. 1 , 14–16 However, survival of the 2 species used in the manufacture of yogurt beyond the proximal GI tract is less clear. 17–19

Lactic acid bacteria are the major microbes used in yogurt and dairy fermentations, although a diverse range of other organisms are used in other fermentation processes. Among the lactic acid bacteria, Lactobacillus , Streptococcus , Lactococcus , and Leuconostoc are most frequently found in fermented dairy foods, either as starter cultures or as naturally occurring members of the raw material. However, some fermented foods, especially yogurt and other fermented milk products, may also contain added probiotic species of Bifidobacterium and Lactobacillus . Probiotics are currently defined “as live microorganisms that, when administered in adequate amounts, confer a health benefit on the host.” 20

The role of fermented milk products on human health has been the subject of extensive research, including epidemiological, observational, and clinical studies. The purpose of the present study was to perform a systematic review of the published literature to evaluate the effect of fermented milk consumption on specific critical health outcomes, including GI health and disease, cardiovascular health and disease, cancer risk, weight management, diabetes and metabolic health, and bone density.

Eligibility criteria

The protocol for this systematic review was registered with PROSPERO (registration no. CRD42017068953). A systematic computerized search was performed and optimized using the PubMed database to identify studies published from its inception to 2017. The search strategy was limited to articles written in English language only. The search terms included “yogurt,” “kefir,” and “other fermented milks” as the subjects of interest, as well as search terms related to aligned health outcomes, including, but not limited to, “digestive health,” “obesity,” “cardiovascular disease,” and “bone density.” Included were all interventional and observational studies conducted among children aged over 2 years and adults without age restriction that reported one or more health outcomes associated with yogurt or fermented milk consumption. These health outcomes included GI and cardiovascular health, cancer risk, weight management, diabetes and metabolic health, and bone density. No restrictions were placed upon the geographic location of studies or the date of publication. Systematic or narrative reviews, conference or dissertation abstracts, and general information articles were excluded. Study selection was completed using the steps outlined in the Academy of Nutrition and Dietetics’ Evidence Analysis Manual , which uses the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analysis) model ( Figure  S1 ; please see the Supporting Information online ). The eligibility criteria are described in Table 1 , using the PICOS (population, intervention, comparison, outcome, and study design) format as well as the search terms described in Figure 1 . Restrictions were placed on age to exclude studies that exclusively evaluated children aged under 2 years. The outcomes were based on the systematic review protocols of the Nutrition Evidence Library, which has historically been used in the United States to develop the Dietary Guidelines for Americans. Only peer-reviewed published journals were considered. Randomized controlled trials, randomized crossover trials, cohort studies, case-control studies, and cross-sectional studies were eligible for inclusion if a fermented milk product was the dietary component under study.

Search terms and strategy.

PICOS criteria for inclusion and exclusion of studies

The title, abstract, and keywords of identified records were initially screened for the health outcomes of interest. Only human studies using fermented milk products were included. Clinical trials with nonbovine milk, milk that had not undergone fermentation, and acidified milk as the test product were excluded. Clinical trials with milk and acidified milk used as the comparator/control were included. Full texts were obtained for all relevant studies.

Data were extracted and entered into a data extraction form, which included population characteristics and follow-up period, dietary assessment and endpoints, summary of results, and outcomes.

The quality of the studies, which reflected risk of bias, was assessed independently by both authors using the Quality Criteria Checklist in the Nutrition Evidence Library of the Academy of Nutrition and Dietetics, based on the Agency for Healthcare Research and Quality domains for research studies. 21 The latter is used by the Academy of Nutrition and Dietetics when conducting systematic reviews for its Evidence Analysis Library. The Quality Criteria Checklist was used to assess the methodological quality of individual studies using 10 criteria. These criteria were designed specifically to assess the validity of the research design, and included the following questions: (1) Is there a clearly specified research question? (2) Was the selection of subjects free from bias? (3) Were study groups comparable? (4) Was the method of handling withdrawals described? (5) Was blinding used to prevent bias? (6) Was the intervention described in detail? (7) Were outcomes clearly defined and the measures valid and reliable? (8) Was the statistical analysis appropriate for the study design and outcome? (9) Were conclusions supported by results? (10) Is a bias due to the study’s funding or sponsorship unlikely? These criteria are derived from the quality constructs and domains identified by the Agency for Healthcare Research and Quality report on Systems to Rate the Strength of Scientific Evidence. Based on meeting the criteria cited in the Quality Criteria Checklist for each area, studies were designated as positive, neutral, or negative quality. If the answers to validity questions 2, 3, 6, and 7 were rated with a “Yes” by both authors/reviewers, along with at least one additional “Yes”, then the study was rated as “positive quality.” If the answers to validity questions 2, 3, 6, and 7 were rated as “No” by both authors/reviewers, then the study was rated as “neutral quality.” If most (6 or more) of the answers to the questions were rated “No,” the report was designated as a “negative quality” study. Any discrepancies between the 2 reviewers were resolved by discussion. A third reviewer was not necessary to resolve discrepancies. The results of the search process are described below.

The search criteria returned a total of 1057 citations. After abstract review and full-text review, 108 studies ( Figure 2 ) were included in the final review, as follows: 31 randomized controlled trials (RCTs), 15 randomized crossover trials (RCOTs), 6 case-control (CC) studies, 16 cross-sectional (CS) studies, 1 nonrandomized controlled trial, and 39 cohort studies. Of the 108 studies, 76 showed a favorable outcome of fermented milk products on health. Twenty-eight studies showed no significant effect on health (depending on whether the study was an RCT, epidemiological, or observational). A neutral outcome or no significant effect on health was not a negative effect. Rather, intervention caused no response. In 4 studies, unfavorable outcomes (associations with disease) were reported; these were cohort studies.

Flow diagram of the literature search process .

Thirty-eight of the 108 included studies were rated as positive quality according to the Quality Criteria Checklist, and 24 of those 38 positive-quality studies reported a favorable outcome of fermented milk products on health. Fourteen of the 38 positive-quality studies reported no significant effect. None of the positive-quality studies reported an unfavorable outcome of fermented milk products on health. Of the remaining 70 studies, 67 were rated as neutral quality, and 14 reported a favorable outcome. Below we present the specific results for each of the health outcomes reviewed.

GI health and disease

Included were 26 studies evaluating the impact of yogurt and cultured fermented milk on GI health and disease 22–47 ; 16 were RCTs, 22–27 , 29 , 32 , 35 , 37 , 39 , 42–44 , 46 , 47 8 were RCOTs, 30 , 31 , 33 , 34 , 36 , 38 , 40 , 41 1 was a nonrandomized controlled trial, 45 and 1 was a CS study. 28 Twenty 22–24 , 27–36 , 38–41 , 45–47 of the 26 studies showed a favorable outcome for GI health with yogurt or fermented milk consumption, and 6 studies 25 , 26 , 37 , 42–44 showed no effect. Based on the quality criteria (see Methods section), 19 studies 23–26 , 30–38 , 40 , 42–44 , 46 , 47 of the 26 studies were considered positive quality (see summary in Table 2 ). Among these, 11 studies 23–26 , 32 , 35 , 37 , 42–44 , 46 evaluated GI symptoms including bloating, gas and abdominal discomfort, diarrhea, and constipation following consumption of fermented milk products. Another 7 studies 30 , 31 , 33 , 34 , 36 , 38 , 40 measured lactose digestion and tolerance, and 1 study 47 measured colonic permeability. Yogurt was the fermented product evaluated in 19 22– 26 , 29 , 31–33 , 36–44 , 46 of the 26 studies, whereas 7 studies 27 , 28 , 30 , 34 , 35 , 45 , 47 evaluated kefir or other cultured milk products.

Summary of studies

Abbreviations : CC, case-control (study); CH, cohort (study); CS, cross-sectional (study); NRCT, nonrandomized controlled trial; RCOT, randomized crossover trial; RCT, randomized controlled trial.

Lactose digestion and tolerance

Seven positive-quality RCTs demonstrated that yogurt or kefir with live, active cultures significantly enhanced lactose digestion and reduced symptoms of intolerance in lactose maldigesters. 30 , 31 , 33 , 34 , 36 , 38 , 40 Studies included subjects ranging in age from 7 months to 53 years and compared consumption of yogurt with consumption of low-fat or whole milk, acidophilus milk, buttermilk, or lactose in water. Consumption of yogurt improved lactose digestion, as indicated by a reduction in breath hydrogen, and improved tolerance as measured by self-reported symptoms. Hertzler and Clancy 30 fed yogurts and kefir to lactose maldigesters, and both products improved lactose digestion and reduced symptoms of intolerance compared with milk. Kolars et al 31 fed yogurt, lactose-free milk, and milk to maldigesters and showed that yogurt improved lactose digestion and tolerance. They also reported the presence of active microbial beta-galactosidase in the intestinal contents of subjects.

Martini et al 33 compared lactose digestion and tolerance after feeding flavored and frozen yogurts, ice cream, and ice milks. Lactose digestion was improved significantly only with fresh yogurt, which was also the only product that did not cause GI symptoms among the subjects. Martini et al 34 compared yogurts made with different strains of L delbrueckii subsp bulgaricus and S thermophilus along with milk fermented with single strains of L delbrueckii subsp bulgaricus, S thermophilus, Lactobacillus acidophilus , and Bifidobacterium bifidus . The improvement in lactose digestion varied. The milk fermented with B bifidus only marginally improved lactose digestion, whereas milk fermented with S thermophilus and L   delbrueckii subsp bulgaricus (ie, yogurt bacteria) resulted in significant improvements. Onwulata et al 36 found that yogurt was better tolerated than milk treated with commercial lactase. However, pasteurization of yogurt eliminated the enhanced digestion of lactose. 40 Rosado et al 38 fed both lactose-containing and lactose-hydrolyzed yogurt to maldigesters and reported both similarly improved lactose digestion. Finally, Savaiano et al 40 compared lactose digestion from yogurt, pasteurized yogurt, sweet (nonfermented) acidophilus milk (homogenized, pasteurized milk inoculated with L. acidophilus NCFM strain), and cultured milk (buttermilk). Only fresh yogurt significantly improved lactose digestion and tolerance. In one neutral-quality study, Shermak et al 41 also demonstrated improved lactose digestion from, and tolerance to, yogurt.

Diarrhea and constipation

Ten studies evaluated the effects of fermented milk products on diarrhea and/or constipation. 22 , 24–28 , 35 , 44–46 Included were 6 positive-quality studies, 24–26 , 35 , 44 , 46 3 neutral-quality studies, 22 , 27 , 45 and one negative-quality study. 28 In one of the positive-quality studies, Boudraa et al 24 reported improvement in outcomes associated with diarrhea, while in another positive-quality study Yang et al 46 reported improvement in constipation outcomes following consumption of fermented milk. A third study by Nagata et al 35 reported improvements in both. Three positive-quality studies – conducted by Boudraa et al, 25 Conway et al, 26 and Tabbers et al 44 – reported no improvement relative to milk controls.

Among the neutral- and negative-quality studies, Agarwal et al, 22 de Vrese et al, 27 Glibowski and Turczyn, 28 and Van den Nieuwboer et al 45 all reported improved treatment or reduced incidence of diarrhea with fermented milks. Agarwal et al 22 fed milk fermented with Lactobacillus casei to patients in a clinical setting, comparing diarrheal outcomes with patients fed Indian dahi (curd) and ultra-heated yogurt. Diarrhea was significantly improved in the hospital, but not in the community setting with L casei milk, perhaps because of patient compliance. de Vrese et al 27 reported improved treatment of antibiotic-related diarrhea with fermented milk in patients with Helicobacter pylori , and Van den Nieuwboer et al 45 reported improved bowel habits (reduced frequency and severity of diarrhea and constipation) with a probiotic fermented milk among elderly patients in a nursing home. Finally, Glibowski and Turczyn 28 found an inverse correlation between fermented milk consumption and problems with bowel evacuation and diarrhea.

Miscellaneous GI symptoms

In one neutral-quality study, Guyonnet et al 29 fed yogurt with added Bifidobacterium lactis to 371 adults with self-reported digestive symptoms and found improvement in symptoms compared with a nonfermented milk. Marteau et al 32 fed the same yogurt with added B lactis and a nonfermented control milk product to a similar population in a positive-quality study, reporting improvements in GI well-being and digestive symptoms when pooling data from the study by Guyonnet et al 29 with their own. Composite scores of digestive symptoms (combining the Bristol scale and the Food Benefits Assessment questionnaire), but not GI well-being, were improved in the Marteau et al 32 study population.

Irritable bowel syndrome

Five positive-quality studies evaluated the potential for fermented milk products to improve symptoms in patients with irritable bowel syndrome (IBS). 23 , 37 , 42 , 43 , 47 Agrawal et al 23 fed a fermented B bifidus milk to IBS patients and reported reduced stomach distension and an acceleration of orocecal and colonic transit, as well as reduced symptoms, compared with a nonfermented milk product. Zeng et al 47 fed IBS patients a probiotic fermented milk containing S thermophilus , L delbrueckii subsp bulgaricus , L acidophilus , and Bifidobacterium longum and reported a reduction in colonic permeability and a favorable effect on mean global IBS scores as compared with an unfermented milk control in a 4-week study. In contrast, Roberts et al 37 reported no improvement in IBS symptoms with fermented probiotic milks. Simren et al 42 reported an initial favorable effect, which was matched by the control at 8 weeks. Similarly, Sondergaard et al 43 reported improvement in IBS symptoms in both the fermented milk and control groups after 8 weeks.

Cardiovascular health and disease

Twenty-eight included studies evaluated the impact of yogurt and fermented milk on cardiovascular health and disease. 48–75 Eight studies 49 , 52 , 58 , 60 , 66 , 69 , 72 , 73 were of positive quality, 19 studies 48 , 50 , 53–57 , 59 , 62–65 , 67 , 68 , 70 , 71 , 74 , 75 were neutral quality, and 1 study 51 was negative quality. Seven studies were RCTs, 49 , 50 , 60 , 61 , 69 , 72 , 73 5 were RCOTs, 52–56 , 58 , 66 11 were cohort studies, 50 , 54 , 55 , 59 , 62–64 , 67 , 68 , 71 , 74 1 was a CC study, 75 and 4 were CS studies. 48 , 53 , 65 , 70 The studies assessed the effect of fermented milk products on cardiovascular disease and cardiovascular markers, coronary heart disease risk factors, metabolic syndrome, risk of stroke, and heart health–related risk factors, including low-density lipoprotein (LDL) cholesterol, triglycerides, and blood pressure (BP). Twenty-one studies 48 , 50 , 51 , 53–57 , 59 , 62–70 , 72–74 evaluated yogurt as the fermented product used, and 7 studies 49 , 52 , 58 , 60 , 61 , 71 , 75 evaluated fermented milk, not classified as yogurt per United States and European standards. Of the 28 studies, 16 studies 49–51 , 53 , 54 , 56–62 , 65 , 71 , 74 , 75 demonstrated a favorable outcome for yogurt and fermented milk on cardiovascular outcomes, and 11 studies 48 , 52 , 55 , 64 , 66–70 , 72 , 73 demonstrated no significant effect. One study, a well-controlled (>26 000 participants) large prospective cohort of high-risk Finnish male smokers, 63 reported an association between yogurt consumption and increased risk of subarachnoid hemorrhage, but not between yogurt consumption and cerebral infarction or intracerebral hemorrhage. However, no association was found for sour-milk consumption. The authors suggested that other factors in cream – in particular, conjugated linoleic acid – may have accounted for this result.

Hypertension

Four positive-quality RCTs examined the effect of fermented milk products on hypertension and BP. 58 , 60 , 72 , 73 Inoue et al 58 fed either a placebo (n = 15) or milk fermented with L casei strain Shirota and Lactococcus lactis YIT 2027 (n = 20) to mildly hypertensive men and women in an RCT. These strains, in concert, were shown to produce aminobutyric acid at 10–12 mg/100 mL during the fermentation. Significant decreases were observed for diastolic BP and systolic BP within 2 or 4 weeks, respectively, and for mean BP at 4 weeks between baseline and treatment for subjects consuming the fermented milk product. All 3 measures remained lower throughout the 12-week intake period. For the subjects consuming the fermented milk product, significant differences between treatment and placebo were observed in systolic BP after 4 and 12 weeks (13.4 ± 4.1 and 17.4 ± 4.3 mmHg, respectively).

Jauhiainen et al 60 conducted an RCT with hypertensive adults who consumed a fermented milk product containing bioactive peptides resulting from fermentation with Lactobacillus helveticus strain LBK-16H. Compared with the placebo group, subjects in the fermented milk group experienced significant decreases in systolic and diastolic BP (4.1 and 1.8 mmHg, respectively).

In another RCT, Usinger et al 72 fed milk fermented with an angiotensin-converting enzyme–inhibitory peptide-producing strain of L. helveticus to 94 prehypertensive and borderline hypertensive subjects. Daily consumption of either 150 mL or 300 mL of the fermented milk did not influence BP compared with the placebo. However, at the higher feeding level, within-group reductions in BP were observed. Thus, the authors concluded that consumption of 300 mL fermented milk containing bioactive peptides may have a modest effect on BP. In a companion study (Usinger et al), 73 angiotensin-converting enzyme–inhibitory activity in these subjects was measured; however, the fermented milk product did not reduce angiotensin-converting enzyme activity.

Neutral-quality studies evaluating the effect of fermented milk on BP generally showed a favorable effect. 61 , 74 In the Kawase et al 61 study, systolic BP was lowered significantly (by about 5 mmHg) after 8 weeks of consumption of fermented milk containing L casei and S thermophilus . Results from a cohort study of 2636 men and women aged 28–62 years (part of the Framingham Heart Study) showed that yogurt consumption for >15 years was associated with lower risk of hypertension. 74 After adjusting for demographic and lifestyle factors (including overall diet quality, total energy intake, metabolic factors, and medication use), consumption of one additional serving/wk of yogurt correlated with a 6% reduction in risk of developing incident hypertension. Masala et al 65 found an inverse association between yogurt consumption and systolic BP in a CS study of adults, aged 18–25 years. The authors concluded that the results support the beneficial effect of selected dairy products (milk and yogurt) but also cautioned that the effect could be interpreted as yogurt being an indicator of an overall ‘health-conscious’ attitude of the subjects. Hutt et al 57 investigated the effect of consuming a probiotic cheese or yogurt, compared with a control without the additional probiotic strain, on BP in healthy adults. The main effect of the consumption of probiotic cheese and yogurt was a modest, but statistically significant, decrease in diastolic BP, while consuming probiotic cheese was also linked to a significant reduction in systolic BP.

Blood lipids

Three positive-quality studies evaluated the effect of fermented milk products on blood lipids. 49 , 66 , 69 In one RCT, Agerbaek et al 49 reported that milk fermented with S thermophilus and Enterococcus faecium lowered LDL 10% from baseline in 58 Danish adult men, all 44 years old. After 6 weeks of consuming a fermented milk product, total and LDL cholesterol were reduced as compared with placebo. Total cholesterol was reduced by 0.37 mmol/L vs 0.02 mmol/L for the chemically acidified milk used as the control ( P  < 0.01). Richelsen et al 69 fed of identical composition fermented milk and acidified milk control to 87 healthy adults – male and female, aged 50–70 years, with normal cholesterol levels. After 1 month, total and LDL cholesterol were significantly reduced in the fermented milk group compared with the control. Maximum reduction occurred at 3 months (LDL −0.32 mmol/L). Interestingly, however, the placebo group also showed a gradual reduction in LDL cholesterol over the 6-month duration of the study. Thus, although both groups showed a similar reduction in total and LDL cholesterol at the end of the study (6 mo), no statistically significant response for the intervention compared with the placebo was observed. Men and women responded similarly to the intervention. The authors concluded that milk may have a hypocholesterolemic effect but they did not provide an explanation for the more rapid response to fermented milk. Another positive-quality RCT was reported by Massey. 66 Female college students consumed 480 mL of 2% fat yogurt for 4 weeks, then no yogurt for 4 weeks, in a crossover trial. Yogurt consumption had no effect on total cholesterol, triglycerides, high-density lipoproteins, or distribution of lipoprotein fractions.

Several neutral-quality studies supported the finding that fermented milks are hypocholesterolemic. Kawase et al 61 conducted an RCT with 20 men aged 30–51 years with elevated total cholesterol and found that consuming 200 mL of fermented milk twice a day for 8 weeks resulted in an increase in high-density lipoproteins. Subjects in 2 RCTs by Hepner et al 56 of adults aged 21–55 years, who consumed either pasteurized or nonpasteurized yoghurt for 12 weeks, experienced reductions of 5% and 10% in total cholesterol, respectively. As both pasteurized and nonpasteurized yogurt resulted in lowering of serum cholesterol levels, it was suggested that a milk component may have contributed to the cholesterol-lowering effect. Kawase et al 61 conducted an RCT involving 20 men and women aged 30–51 years and found that consuming fermented milk for 8 weeks resulted in a decrease in triglycerides.

Four studies found no significant association between cardiovascular risk factors and consumption of yogurt or fermented or sour milk. 64 , 66 , 72 , 73 Likewise, no consistent associations were found between intakes of total milk, low-fat milk, fermented milk products, cheese, or yogurt, and stroke incidence, stroke mortality, or coronary heart disease incidence or coronary heart disease mortality in a subset of subjects in the Rotterdam cohort study. 68

Collectively, the published reports suggest that the hypertension-lowering effects of fermented milk products may depend on the specific bacteria used during fermentation. Additional positive-quality studies comparing the effects of specific strains on BP are needed. Several neutral-quality studies support the hypocholesterolemic effect of fermented milks.

Cancer risk

Seventeen studies – 1 positive quality and 16 neutral quality – evaluated the effect of yogurt and cultured fermented milk on colorectal, breast, and prostate cancer risk or biomarkers. 76–92 Of these, 1 study 78 was an RCT, 11 were cohort studies, 76 , 79–85 , 87 , 91 , 92 and the remaining 5 were CC studies. 77 , 86 , 88–90 Yogurt was evaluated in 13 76 , 80 , 82–88 of the 17 studies and 4 81 , 89–92 evaluated fermented milk not classified as yogurt. The one positive-quality study was an RCT 78 in which the authors assessed cell-mediated immune function (lymphocyte proliferation assays) as a proxy for cancer protection. No differences were observed in immune function between young women (n = 13) who consumed 2 cups of yogurt per day for 3 months and young women who did not consume yogurt (n = 12). The authors related immune function measurements to risk of breast cancer. Nine studies 77 , 84–87 , 89–92 out of 17 showed a favorable outcome for yogurt and fermented milk on cancer outcomes, 5 studies 76 , 78–81 demonstrated no significant effect, and 3 studies 82 , 83 , 88 demonstrated an unfavorable outcome.

Colorectal cancer

Seven neutral-quality studies assessed yogurt or buttermilk consumption and risk of colorectal cancer or colon cancer risk factors. 77 , 79 , 81 , 84 , 85 , 87 , 88 Using cohort data based on the European Prospective Investigation into Cancer and Nutrition (EPIC) study, Pala et al 85 reported that yogurt consumption was inversely associated with colorectal cancer risk, when comparing highest to lowest intakes based on a prospective study of 45 241 volunteers and 289 diagnosed cases of colorectal cancer. Murphy et al 84 extended these findings using EPIC data and observed an inverse relationship between yogurt consumption and colon cancer occurrence, based on 477 122 volunteers and 4513 cases of colorectal cancer. This relationship was also true for milk in multivariable models but weakened to nonsignificant in linear models. Further, Kampman et al 81 found that yogurt and buttermilk separately exhibited a weak inverse relationship with colorectal cancer in highest vs lowest intake groups in a cohort study of more than 3000 elderly men and women. The authors concluded that intake of fermented dairy products was not significantly associated with colorectal cancer risk in this population. Similarly, in a cohort study, Dik et al 79 found no association between historical prediagnosis intake of yogurt (highest vs lowest quartiles) and diagnosed colon cancer, and colorectal cancer-specific or all-cause death, using EPIC data with 3859 cases of colorectal cancer.

Boutron et al 77 and Senesse et al 87 published CS studies that revealed an inverse association between large-adenoma diagnosis and yogurt consumption. In the Boutron study, 77 the association differed by sex. In men, only the highest level of intake was associated with a reduced risk, whereas in women a reduced risk was observed among those who consumed vs those who did not consume yogurt. In another CS report, 88 investigators found that consumption of labaneh, but not yogurt, was associated with an increased risk of colorectal cancer. Labaneh is a strained yogurt made from whole milk that contains 10% fat, and the authors suggested the saturated fat may account for the increased risk.

Breast cancer

Three neutral-quality CC studies 86 , 89 , 90 and 3 cohort studies 76 , 91 , 92 examined associations between consumption of fermented milk products and breast cancer risk. In a CC study in the Netherlands with 133 incident breast cancer cases and 289 controls, van’t Veer et al 89 found that yogurt and buttermilk consumption was associated with a decreased risk of breast cancer with an odds ratio of 0.63/g. However, milk consumption did not result in a similar correlation. In a later study, Van’t Veer et al 90 expanded this cohort to 168 breast cancer cases and 548 controls, and observed that combining factors relating to low fat, high fiber, and high consumption of fermented milk products resulted in an odds ratio of 0.33. Ronco et al, 86 in a CC study involving 111 breast cancer diagnoses and 222 frequency-matched controls, found a significant inverse association between consumption of skim-milk yogurt/total yogurt and breast cancer in a dose-response pattern. In the Malmö Diet and Cancer cohort of 17 000 women, Wirfalt et al 91 found consumption of fermented milk products, including yogurt (<0.5%–7% fat), was associated with a decreased risk of breast cancer (hazard ratio = 0.89). In a follow-up study, Wirfalt et al 92 observed that consumption of milk fat contained within fermented milk products was also associated with a decreased risk of breast cancer. In contrast, in a cohort study involving 9039 females, Berkey et al 76 found the risk for benign breast disease in girls consuming 1+ cup/d of yogurt was below that of smaller-intake categories.

Prostate cancer

Two neutral-quality cohort studies found association between yogurt consumption and increased risk of prostate cancer when comparing highest to lowest consumption. 82 , 83 As part of the French SU.VI.MAX (Supplementation en Vitamines et Minéraux Antioxydants) study, dietary intakes of 2776 men, 69 of whom were diagnosed with prostate cancer, were analyzed. The association between yogurt intake and increased prostate cancer risk was found to be similar to that between all dairy foods and prostate cancer. The authors attributed their findings to a relationship between calcium intake and prostate cancer risk. Kurahashi et al 83 evaluated prostate cancer risk among 43 435 Japanese men aged 45–64 years. During the 7.5-year duration of the study, 329 men were diagnosed with prostate cancer. The relative risk of diagnosis in the highest consumption quartile was 1.52 – similar to that for other milk products.

Additional positive-quality studies are needed to determine whether yogurt or its microbial components can influence the risk, development, or treatment of cancers. The evidence suggests a favorable relationship between fermented milk consumption and reduction of risk for breast and colon cancer. It appears that the risk for prostate cancer from fermented dairy foods may not be different than the risk from dairy foods in general, but again, further studies are needed.

Weight and body composition

Twenty-two included studies examined the relationship between consumption of yogurt and cultured fermented milk and weight and body composition 70 , 93–113 ; 5 were RCTs, 96 , 107 , 108 , 112 , 113 9 were cohort studies, 94 , 100–102 , 104 , 106 , 109–111 and 8 were CS studies. 70 , 81 , 93–95 , 97–99 , 105 Six studies 96 , 97 , 107 , 108 , 112 , 113 were positive quality and focused on body composition, weight loss, obesity, and muscle soreness. The remaining 16 studies 70 , 98–106 , 109–111 were neutral quality. In 21 of the 22 studies, 93–95 , 97–113 subjects were fed yogurt, and in the remaining study 96 they were fed kefir. Eighteen of the 22 studies 94–107 , 109–111 , 113 reported a favorable outcome for weight control or positive body composition effect, and 4 studies 70 , 93 , 108 , 112 reported no effect.

The 6 positive-quality studies comprised 5 RCTs 96 , 107 , 108 , 112 , 113 and one CS study. 97 Three of the positive-quality RCTs evaluated body composition changes with yogurt consumption; in one trial subjects were fed bifidobacteria-fermented milk, while in another they were fed kefir. Fathi et al 96 observed improved body composition and greater weight loss with kefir or milk. In another study, Takahashi et al 107 fed a bifidobacteria-fermented milk to mildly overweight Japanese subjects. The control was an acidified milk control, matched for nutrient composition, skim-milk powder, and calories. Visceral fat was reduced with the fermented milk, and fecal bifidobacteria were increased, suggesting a microbiome effect. Body weight, BMI, and waist-to-hip ratio did not change. Thomas et al 108 evaluated yogurt, as compared with an isoenergetic sucrose beverage, on postexercise changes in body composition. No significant group differences were observed. Similarly, White et al 112 found no improvement in body composition with yogurt feeding during a resistance training program. Zemel et al 113 fed yogurt to obese subjects as part of a 2-arm dietary restriction protocol. The rate of fat loss increased, and lean mass was spared, with yogurt, vs a lower-calcium control matched for macronutrients and fiber. Finally, in a CS study of adolescent European and Australian populations, Huybrechts et al 97 found that a dietary pattern associated with greater incidence of overweight and obesity, as measured by BMI, was characterized, in part, by a low intake of yogurt.

There were 15 neutral-quality studies. 70 , 93–95 , 98–106 , 109 , 111 Of these, 13 demonstrated significant correlations or associations between yogurt consumption and less obesity, lower body weight, lower adiposity, or reduced weight gain over time in both CS and cohort studies.

In summary, of the 7 positive-quality studies, only one showed a weight-loss difference (Zemel et al 2005). 113 Five showed no difference in weight loss. One was correlative and one showed a change in visceral fat, suggesting a microbiome role of Bifidobacterium animalis subsp lactis. 107 Most of the neutral-quality studies showed correlations between yogurt consumption and weight control. Performing RCTs with a focus on weight control is particularly problematic, based on the likely long duration of the necessary intervention and multiple external variables that are difficult, if not impossible, to control. The available studies on fermented dairy foods and body weight demonstrated a strong correlation between fermented milk consumption and weight control. Such effects could be modulated by changes in the microbiome as suggested by Takahashi et al. 107

Diabetes risk and metabolic syndrome

Diabetes risk..

Nine studies evaluating the impact of yogurt and cultured fermented milk on diabetes risk were included in this review 114–122 ; 1 study was an RCT, 117 2 were RCOTs, 116 , 118 1 was a CS study, 122 and 5 were cohort studies. 114 , 115 , 119–121 The studies assessed the impact of fermented milk products on type 2 diabetes (T2D) risk, glycemia, satiety, glucose metabolism, and insulin resistance. Seven studies 114–116 , 119–122 used yogurt as the fermented product being tested and the other 2 studies 117–118 used a fermented milk and a probiotic fermented milk. Of the 9 studies, 114–120 , 122 8 reported a favorable outcome of yogurt or fermented milk on diabetes outcomes, and 1 study reported no consistent relationship between yogurt consumption and incident diabetes. 121

The 2 positive-quality studies were conducted by Diaz-Lopez et al 115 and El Khoury et al. 116 The former was an RCOT (20 healthy males) with nonfat plain and sweetened yogurts and skim milk among the treatments. 116 The results showed improved efficacy of insulin action of yogurt and skim-milk treatments that was independent of their protein-to-carbohydrate ratios and physical form. In a CS study, Diaz-Lopez et al 115 followed 3454 nondiabetic elderly subjects in a Mediterranean population and reported an inverse relationship between T2D cases and total low-fat dairy and yogurt consumption. Three neutral-quality studies 114 , 119 , 120 reported a significant association between consumption of either yogurt or fermented milk and decreased risk of T2D, and 2 neutral-quality studies 121 , 122 reported an association between yogurt consumption, lower levels of glucose, lower levels of insulin, and less insulin resistance. One neutral-quality study reported a nonsignificant outcome on the effect on diabetes risk with consumption of fermented milk products, Soedamah-Muthu et al 121 evaluated the intake of fermented milk products in a subpopulation from the Whitehall II study and found it to be inversely associated with overall mortality, but not with diabetes. Overall, these studies indicate a significant correlation between fermented milk consumption and reduced risk for T2D.

Metabolic syndrome.

Four neutral-quality studies specifically evaluated metabolic syndrome. As part of the PREDIMED (Prevención con Dieta Mediterránea) cohort study, Babio et al 50 found that among 1868 men and women aged 55–80 years, consumption of both low-fat and high-fat yogurt was associated with a decreased risk for metabolic syndrome (MetS). In a CS study using NHANES (National Health and Nutrition Examination Survey) data, Beydoun et al 53 showed a significant inverse relationship between yogurt consumption and MetS. As part of the Tehran Lipid and Glucose cohort study, Cheraghi et al 54 found that for every serving of yogurt consumed per day (equivalent to 200 g), the incidence of MetS decreased by 57% – a finding that was modest, but significant. One component of the 5 MetS criteria, central adiposity, was found to be significantly inversely associated with high yogurt consumption. Kim and Kim 62 reported that for a cohort of 5510 men and women aged 40–69 years, consumption of 4 or more servings of yogurt per week was associated with a decreased risk for MetS. Among a cohort of 664 men and women aged 18–55 years, Cormier et al 94 reported that yogurt consumption led to an improved cardiometabolic risk profile.

Overall, studies suggest yogurt consumption is strongly associated with risk reduction of metabolic syndrome and diabetes.

Bone health

Seven included studies evaluated the impact of yogurt and cultured fermented milk on bone health 123–129 ; 1 study was an RCT, 124 3 were cohort studies, 125–127 and 3 were CS studies. 123 , 128 , 129 The studies assessed the effect of fermented milk products on growth, bone density, risk of dental caries, and risk of hip fracture. All of the studies evaluated yogurt consumption or yogurt feeding (and one of these used laban, a liquid-type yogurt). Five of the studies 123–125 , 128 , 129 reported a favorable outcome of yogurt consumption, and 2 studies 126 , 127 reported a neutral outcome.

Only one study, conducted by He et al, 124 was positive quality; the other 6 studies 123 , 125–129 were neutral quality. In the He et al 124 study, the diets of preschool children in Beijing suburbs were supplemented with 125 g/d of yogurt for 9 months (vs no supplementation). The treatment group reported improved nutrient intake, lower incidence of respiratory infections and diarrhea, greater height and weight gain, and greater bone mineral density.

In a CS study of an Iranian female adult population, AlQuaiz et al 123 found an increased risk for low bone mineral density among those who did not drink laban (yogurt drink). As part of the Framingham Offspring cohort study, Sahni et al 125 found an association between yogurt consumption and increased bone density. No other dairy groups showed an association. Greater intakes of milk and yogurt (>1 serving/wk) also lowered risk for hip fracture by 20% in older adults, compared with those with a low intake of these dairy foods. 126 Further, as part of the Framingham original cohort study, Sahni et al 127 found less bone loss over a 4-year period among those taking vitamin D supplements, who were also medium-to-high consumers of a combination of milk, yogurt, and cheese.

Additionally, in a CS study by Uenishi and Nakamura, 128 after adjusting for exercise frequency, weight, gender, age, and area of residence, regression analyses indicated that milk and yogurt intake among a population of teenagers (aged 15–18 y) were independently associated with the osteo-sono assessment index, a standard measurement of bone mineral density, while cheese intake was not.

Overall, the studies confirm the positive effect of the high nutrient content of yogurt on bone health.

Conclusions that may be drawn from this systematic review are that (1) a causal relationship exists between lactose digestion and tolerance and yogurt consumption, and (2) consistent associations exist between fermented milk consumption and reduced risk of breast and colorectal cancer, T2D, improved weight maintenance, and improved cardiovascular, bone, and GI health. Further, an association exists between prostate cancer and dairy product consumption in general, with no difference between fermented and unfermented products.

There exist several possible mechanisms for these findings. During fermentation, metabolic activity of microorganisms can alter the nutritive and bioactive properties of dairy products. Thus, health-promoting properties of fermented milk products may be due, in part, to the biosynthesis or release of bioactive compounds resulting from the fermentation process, 130 including bioactive peptides with antihypertensive, antimicrobial, antioxidative, and immune-modulatory activities. 131 Lactic acid bacteria may also produce bacteriocins, biogenic amines, and exopolysaccharides. 132 , 133 Conjugated linoleic acid, which has demonstrated anti-inflammatory, anti-atherogenic, and antioxidant properties, is naturally present in milk fat and may increase during fermentation. 1 The B vitamins folate, riboflavin, and B12 can be synthesized by fermentation-associated bacteria in dairy foods, thereby increasing the nutritive content and providing additional health benefits. 134–136

The strongest evidence supporting the health benefits of fermented foods is for their ability to improve lactose digestion and tolerance. Multiple RCTs support this function and the physiological role of the beta-galactosidase enzyme produced by yogurt bacteria for in vivo hydrolysis of lactose during GI transit, resulting in improved lactose digestion and tolerance.

An important potential confounding factor in cohort and other correlation-based studies is that individuals with a propensity toward healthy diets may simply consume more fermented foods. Thus, it is critical that, when feasible, controlled and blinded studies be conducted with populations matched for age, gender, socioeconomic status, education, and other factors that may influence food consumption behavior. Although the limitations of observational studies are well known (including potential for bias and lack of causation), 137 they can still provide valuable suggestions for improving public health. 138–140

Further, dairy foods contain high levels of several essential nutrients, including high-quality protein, calcium, potassium, phosphorus, and vitamins A, D, B12, riboflavin, and niacin. Hence, distinguishing the health benefits of fermented vs nonfermented milk products is often difficult. Many of the studies cited in this review used milk products as controls. Thus, these studies are able to distinguish the specific effect of fermentation. In contrast, other studies utilized nonmilk controls, cannot distinguish between nutrient content and fermentation factors influencing the results.

In a review of dietary recommendation in 13 European Union member states, none mentioned yogurt as an alternative for people with lactose intolerance, despite an approved function claim in the European Union for live cultures in yogurt or fermented milk to aid with lactose digestion. 141 Further, only 5 European Union member states currently have national nutrition guidelines or recommendations that include yogurt with live bacteria. 142 Nonetheless, there appears to be emerging interest in including fermented foods as part of dietary guidelines. 4 , 16 , 133 , 142–144 While the US dietary guidelines, as well as national recommendations from other countries, recommend the consumption of yogurt for its nutrient content, specific comments on fermented milk products are rare. Evidence described in this review suggests such recommendations are warranted.

Thank you to the Danone North America staff, including Kristie Leigh and Miguel Freitas, for assistance in carrying out the PRISMA protocol and for editorial support. Authors R.W.H. and D.A.S. contributed equally to this manuscript. Both authors reviewed publications according to the PRISMA protocol and wrote and edited the manuscript. They are solely responsible for its content.

Funding . This work was supported by Danone North America Public Benefit Company (White Plains, NY). Danone North America did not provide concept, design, or approval of this manuscript.

Declaration of interests . D.A.S. serves on the Danone North America Nutrition Advisory Board and is Chair of the Ritter Pharmaceuticals Medical Advisory Board. R.W.H. is a consultant to Danone North America.

Supporting Information

The following Supporting Information is available through the online version of this article at the publisher’s website.

Appendix S1 PRISMA checklist

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• dairy products
• health outcomes

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• Nutritional Medicine
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Review on Set Yogurt Production Process

• October 2020
• Conference: Dairy Product

• Addis Ababa Institute of Technology

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