**1. Introduction**

Extensive attention has been paid to the formation of deep-water mounds in recent decades [1,2]. The presence of mounds within the strata can cause dome-like bedforms with mounded seismic reflections [3,4]. Various origins of deep-water mounds in debates mainly involved the carbonate reefs [5,6], mud diapirs or mud volcanoes [4,7], deep-water wave sediments [8], sand bars related to differential compaction [9–11], and remnant mounds originated from channel incision [12–15].

In recent years, pervasive mounded seismic reflections were detected in the Miocene Meishan Formation (Fm.) in the Qiongdongnan Basin (QDNB) [13,16]. Numerous models were proposed over the years to interpret their origins but there is no unified conclusion [4,5,14–18]. A widely accepted view in prior studies was that the middle Miocene was the dominant reef-building period in the northern South China Sea, and the mounded reflections were then thought to be the carbonate reefs [5,16,19]. Nevertheless, recent drilling revealed that some mounds were mainly composed of mud-rich lithology rather than reefs [18,20]. Channel incision has also been considered the possible controlling factor in the formation of the Miocene mounds in the study area [4,15]. However, most of the

**Citation:** Xu, L.; Shi, W.; Wang, R.; Ren, J.; He, Y.; Du, H.; Zuo, T.; Huang, J.; Dong, Y. New Insights into the Genetic Mechanism of the Miocene Mounded Stratigraphy in the Qiongdongnan Basin, Northern South China Sea. *Energies* **2022**, *15*, 9478. https://doi.org/10.3390/ en15249478

Academic Editor: Dameng Liu

Received: 16 November 2022 Accepted: 12 December 2022 Published: 14 December 2022

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**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

mounds trend roughly parallel with the inferred strike of the slope, which contradicts the principle that remnant mounds generated by the incision have their axes pointing downslope in most situations [14,16,21]. Additionally, these mounds were interpreted as sediment waves generated by bottom currents, but lacked the overwhelming proof supporting the existence of the bottom currents at that time [13]. Therefore, the models developed previously might not be readily applicable to the study area, and other mechanisms are required to explain the formation of mounds. It is worth noting that much of the topographic relief can appear in the structurally disturbed strata [3,22]. For the QDNB, an important tectonic transformation occurred at the turn of the middle and late Miocene, accompanied by intense tectonic activation corresponding to the time equal to the top of the Meishan Fm. [23–25]. Whether the formation of the mounds within the uppermost layer of the middle Miocene is related to such tectonic change has not been noticed previously.

In this study, we applied 2D and 3D seismic data to describe the characteristics of the mounds within the uppermost layer of the Miocene Meishan Fm. Combined with the tectonic settings, a novel model was developed to explain the formation process of the mounds. This model accentuates the decisive role played by tectonic activities in the creation of the mounds. The research results may offer a new idea in the interpretation of similar geological phenomena in other areas around the world.

### **2. Geological Setting**

The QDNB is located at the west of the NE-trending extensional system in the northern South China Sea [26–29] and comprises the Northern Depression, Northern Uplift, Central Depression, and Southern Uplift from the north to south [30–32] (Figure 1). The Central Depression is located in the deep-water area, including the Ledong, Lingshui, Songnan, Ganquan, Beijiao, Baodao, and Changchang Sags, as well as the Lingnan and Songnan highs [33,34]. The water depths vary from 500 to 1500 m, with the maximum depth reaching 2500 m [35]. The tectonic evolution of the basin is consistent with a typical passive margin containing rifting and thermal subsidence. The unconformity of T6 that formed at ~21 Ma divided the Cenozoic strata of the basin into the syn-rift and post-rift layers. Faults were extremely developed in the syn-rift stage while seldom active in the post-rift stage [13,27]. Since the late Miocene, tectonic subsidence accelerated, accompanied by intense reactivation of faults in the eastern basin [23,24,36]. Correspondingly, the water depth of the basin increased [16,37]. In addition, since the cessation of submarine expansion (~16 Ma), magma has been widely active in the South China Sea and its adjacent areas [25,38]. There is a high heat flow zone in the Baodao to Changchang Sags, which was closely related to the thermal events involving massive magmatic intrusions and eruptions from the Miocene to Pliocene [37].

The main sequence boundaries of the basin including Tg, T8, T7, T6, T5, T4, T3, and T2 divided the Cenozoic strata into Lingtou (E2l), Yacheng (E3y), Lingshui (E3l), Sanya (N1s), Meishan (N1m), Huangliu (N1h), Yinggehai (N2y) and Ledong (Ql) Fms. (Figure 2). The depositional environment transformed from a coast and shallow sea to a semi-deep and deep sea from the middle to late Miocene [4,18]. The lower member of the Meishan Fm. is composed of mudstones, sandstones, and calcareous sandstones; its upper member mainly consists of mudstones mixed with thin argillaceous siltstones [15,20,39]. The lower member of the Huangliu Fm. is dominantly fine sandstones interbedded with thin mudstones and its upper member primarily comprised sandy limestones and fine sandstones [15]. A large submarine canyon (i.e., Central Canyon) was developed in the late Miocene, with an 'S'-shaped axis parallel to the shelf break of the basin [18]. The mounded stratigraphy within the Miocene Meishan Fm. is restricted to the Southern Slope (between the Central Depression and Southern Uplift) which has the topography dipping from SE to NW, and is bounded by the Central Canyon to the north and the Xisha Islands to the south [5,18].

**Figure 1.** Tectonic units of the Qiongdongnan Basin (modified from [30,31]). The Qiongdongnan basin is divided into the eastern and western basin according to the direction change of the basin axis. Seamounts composed of basaltic volcanic rocks developed in the south eastern uplifts and eastern sags. NDB = Northern Depression Belt. NUB = Northern Uplift Belt. CDB = Central Depression Belt. SUB = Southern Uplift Belt. YCU = Yacheng Uplift. STU = Songtao Uplift. BJU = Beijiao Uplift. YNH = Yanan High. LSH = Lingshui High. LNH = Lingnan High. SNH = Songnan High. YNS = Yanan Sag. YBS = Yabei Sag. SXS = Songxi Sag. SDS = Songdong Sag. LDS = Ledong Sag. LSS = Lingshui Sag. BJS = Beijiao Sag. SNS = Songnan Sag. BDS = Baodao Sag. CCS = Changchang Sag. GQS = Ganquan Sag. HGS = Huangguang Sag.

**Figure 2.** Generalized stratigraphic column of the Qiongdongnan Basin (modified from [28,29]).

### **3. Data and Methods**

The 2D and 3D seismic data used in this study were acquired over the past several years by Guangzhou Marine Geological Survey (GMGS). The G Gun II type air-gun sources were employed to acquire the seismic lines [40]. The seismic streamer used the Seal 24-digit cable, with a submerged depth of 8 m, and the receiver streamer had 240 traces and 60-fold coverage [41]. The 5700 km of 2D seismic lines covering the QDNB have a dominant frequency of 30 HZ on average, with a vertical resolution of 20 m and a trace interval of 6.25 m. In particular, new multi-channel 3D seismic volumes acquired in 2018 cover an area of ~800 km2 located in the Lingnan High, with the dominant frequency ranging from 30 to 70 Hz. The sampling interval for the 3D seismic data is 1 ms, with a bin size of 3.125 m × 18.75 m. The seismic data were processed by the Institute of Processing in the GMGS using the GeoCluster (a product of CGG®) processing system. The processing procedures including data input, trace editing, static correction, prestack noise attenuation, amplitude compensation, prestack deconvolution, CMP sorting, velocity analysis, dynamic correction, residual static correction, dip moveout (DMO) correction, prestack time migration, quality control in processing, poststack noise attenuation, and poststack time migration have been described by Wang et al. (2010) and Zhang (2020) [41,42].

The interpretation of seismic data was carried out by the Geoframe® software (a product of Schlumberger®) to construct the seismic stratigraphic framework. The seismic data were zero-phased and displayed normal polarity, indicating a positive event on the seismic profiles which is shown as a red reflection [25]. The identification of seismic facies differences and contact relationships between strata supported the tracking of sequence boundaries [43]. Eight main seismic sequence boundaries including Tg, T8, T7, T6, T5, T4, T3, and T2 were identified (Figures 3–5). Faults can be identified in seismic profiles in the form of the offset of seismic events or zones of poor seismic signal across which reflectors are offset [3,44]. Fault interpretation was conducted by adopting appropriate geometric and kinematic models, e.g., the listric normal fault, domino-type fault, and flower structure [45]. Based on this, the seismic interpretation emphasized describing the geometric characteristics of the mounds within the uppermost layer of the Meishan Fm. The width and height of the mounds and their distribution range were determined based on the 2D seismic profiles. In addition, the isopach map of the Huangliu Fm., prepared based on seismic surfaces T3 and T4, was used to recover the paleogeomorphology corresponding to the end of the Meishan deposition. Moreover, the seismic attribute map of the curvature was extracted by the Geoframe® to reveal the plan-view characters of the mounded topography. Curvature calculates the bending degree of the stratum, which can effectively reflect geomorphic features such as valleys, ridges, and domes [46,47].

To determine the tectonic histories, backstripping was employed to reconstruct the amount and rate of tectonic subsidence in different stages [48,49]. Back-stripping employs the tectonic subsidence equation presented by Steckler and Watts (1978) [50]. The method is based on the crustal isostatic principle to backstrip the present stratigraphy layer by layer and to obtain the true basement subsidence caused by the tectonic driving forces [48]. Tectonic subsidence reconstruction was performed by dividing and dating the sequence boundary of the seismic profiles. The ages of the sequence boundary are shown in Figure 2. In the process, the seismic sequence boundaries were time-depth conversed by using the formula provided by the GMGS. There is a decrease in the porosity of sediment with an increase in overlying strata thickness during the compaction process [49]. To remove the effect of compaction, the original amount of subsidence in each stratum can be recovered by the relationship between porosity and depth that fits an exponential function to recover the original thicknesses of strata [51]. Additionally, considering that the depositional thickness is not equivalent to the subsidence when the sedimentary interface remains below the water surface, the accurate paleo-water depths and eustatic variations were taken into consideration [48,52]. The paleowater depth data were collected from the previous research results of Zhai et al. (2013) and Zuo et al. (2022) (Table 1) [32,53]. The eustatic variations are shown in Figure 2.

**Figure 3.** (**A**,**B**) Uninterpreted and interpreted seismic section traversing the Lingshui Sag, showing the stratigraphic and structural characteristics (for location, see Figure 1). (**C**–**E**) Seismic profiles and their interpretations showing the mounded topography at the top of Meishan Fm (for locations, see Figure 3A). W = width; H = height; TWT = two-way traveltime.

**Figure 4.** (**A**,**B**) Uninterpreted and interpreted seismic section traversing the Beijiao Sag, showing the stratigraphic and structural characteristics (for location, see Figure 1). (**C**–**E**) Seismic profiles and their interpretations showing the mounded topography at the top of Meishan Fm (for locations, see Figure 4A). W = width; H = height; TWT = two-way traveltime.

**Figure 5.** (**A**,**B**) Uninterpreted and interpreted seismic section traversing the Baodao Sag, showing the stratigraphic and structural characteristics (for location, see Figure 1). (**C**–**E**) Seismic profiles and their interpretations showing the mounded topography at the top of Meishan Fm (for locations, see Figure 5A). W = width; H = height; TWT = two-way traveltime.

**Table 1.** Reference value of paleo heat flow and water depth during different periods (referenced from [32,53]). HF = Heat flow; PWD = Paleowater depth. HF1, HF2, and PWD1 apply to the northern slope; HF3, HF4, and PWD2 apply to the central depression; HF5, HF6, and PWD3 apply to the southern uplift.

### **4. Results**

### *4.1. Seismic Stratigraphy*

The seismic reflector T4 corresponds to the regional unconformity which represented the Dongsha movement in the South China Sea [16]. In the Southern Slope, the reflector T4 truncated the underlying strata and was onlapped by overlying sediments [4,15], as shown in Figures 3–5. The underlying Meishan Fm. can be divided into upper and lower members by an obvious interface. The upper member is characterized by strong-moderate amplitudes, moderate frequency, and mounded reflections, and the lower member shows subparallel sheet-shaped reflections with moderate-strong amplitudes and moderate frequency (Figures 3–5). The overlying Huangliu Fm. is dominated by moderate amplitude, moderate-weak frequency, and parallel-subparallel reflections (Figures 3–5). The Huangliu Fm. gradually thins onto the southern margin of the basin. A large submarine canyon (Central Canyon) was developed in the post-rift sequence of the QDNB, which is distributed in the Central Depression from west to east (Figures 3–6). The large magmatic body between Songnan and Baodao Sags divides the canyon into two sections, the west section trending NE and the east section trending nearly EW (Figure 6).

**Figure 6.** Paleogeomorphology at the beginning of the deposition of the Huangliu Fm., showing the directions of the greatest slope in the southern area. The red dashed line indicates the range of the mounds. LSS = Lingshui Sag. BJS = Beijiao Sag. SNS = Songnan Sag. BDS = Baodao Sag. CCS = Changchang Sag. LNH = Lingnan High. SNH = Songnan High. BJU = Beijiao Uplift.

### *4.2. Characteristics of Mounded Stratigraphy*

The NW–SE oriented seismic profiles show that the top of the Meishan Fm. is characterized by the elevations alternating with 'V'-shaped troughs, displaying undulated morphologies (Figures 3–5). The elevations tend to be present as lenticular seismic reflectors that are thickest in the middle part and thin toward both wings, showing dome-like bedforms, which are common not only in the QDNB but also in the Pearl River Basin in the northern South China Sea [5,16,18]. Similar elevations were described as 'mounds' previously, and strata characterized by the presence of mounds are commonly said to have 'mounded topography' [3,18]. The mounded stratigraphy was constrained between the T4 and the boundary of the upper and lower member of the Meishan Fm. (i.e., T5) (Figures 3–5). The mounds distributed in the Lingnan High have heights varying from 70 to 90 m, with the widths ranging from 0.9 to 1.7 km (Figure 3C–E). The heights of a single mound in the Beijiao area vary from 90 to 125 m, and their average width is greater than 1.5 km (Figure 4C–E). The mounds in the south of the Baodao Sag have heights of about 110~210 m, with widths ranging from 1.0 to 2.4 km (Figure 5C–E). On the whole, the scale of the single mound in the eastern area seems larger. The internal reflectors of the mounds show strong-moderate amplitudes and moderate frequency, which are characterized by obvious fold structures and disturbed bedding (Figures 3–5). The seismic reflections within the troughs vary greatly in different areas, displaying strong-moderate amplitudes and moderate frequency in the Lingnan High (Figures 3C–E and 7B,C), and moderateweak amplitudes and low frequency in the Beijiao area and the south of the Baodao Sag (Figures 4 and 5). The reflector T4 commonly truncated the flanks of the mounds and was

onlapped, filled, and leveled by subsequent seismic strata corresponding to the Huangliu Fm. (Figures 3–5). Spatially, the mounds were most developed in the middle of the Southern Slope and disappeared in the Central Depression and South Uplift (Figures 3–6). The mounded stratigraphy covers an area restricted to the east of the Huaguang Sag, west of the Changchang Sag, north of the Beijiao Uplift, and south of the Central Canyon (Figure 6). Additionally, the curvature attribute map calculated for the top of the Meishan Fm. shows that the mounded topography is characterized by coupled elongated ridges and gullies, with most of their axes predominantly oriented SWW–NEE and SW-NE (Figure 7A). These elongated ridges and gullies show a subparallel configuration with a few intersections.

**Figure 7.** (**A**) Characteristics of mounded topography revealed by curvature analysis based on 3D seismic data (See Figure 6 for the location of the 3D survey). The mounded topography is characterized by the alternating distribution of nearly EW-trending elongate troughs and ridges. (**B**,**C**) The top of the Miocene Meishan Formation has a mounded topography characterized by the mounds alternating with troughs (for location, see Figure 7A). TWT = two-way traveltime.

### *4.3. Tectonic Subsidence*

The balanced cross-sections were created by using the backstripping technique to determine the tectonic subsidence in different stages [48,49]. The result shows that the sedimentary centers were controlled by the boundary faults in the Paleogene, during which the sedimentary thickness and subsidence rate in the depression centers are larger than those in the uplift belts (Figures 8 and 9). The Eocene is relatively thin and the subsidence rate is low. The sedimentary thickness and subsidence rate in the early Oligocene significantly increased. The sedimentary thickness in the late Oligocene is relatively thick while the subsidence rate decreased. The faults were almost inactive when the basin entered the post-rift stage and its evolution was mainly controlled by thermal subsidence (Figure 8). During the depositional period of Sanya and Meishan Fms., the sedimentary thickness is relatively thin and the subsidence rate was extremely low, with an average value of less than 150 m/myr (Figure 9). In addition, there was little difference in tectonic subsidence between the Central Depression and the Southern Slope. During the deposition of the Huangliu Fm., the sedimentary thickness increased slightly and the subsidence rate in the Central Depression was ~200 m/myr and gradually decreased southward (Figure 9). During the depositional period of the Yinggehai Fm., sedimentary thickness and subsidence increased sharply, with a maximum cumulative rate approaching ~1100 m/myr in the Lingshui Sag and ~1600 m/myr in the Baodao Sag (Figures 8 and 9). The difference in subsidence between the Central Depression and the Southern Slope and Southern Uplift became more obvious. During the deposition of the Ledong Fm., the deposition thickness was still large, and the Baodao and Lingshui Sags had a subsidence rate of ~800 m/myr and ~950 m/myr, respectively (Figure 9). At the same time, the subsidence of the Southern Uplift was much less than that of the Central Depression. Overall, the most obvious feature of the basin is that since 10.5 Ma, the subsidence began to accelerate, showing higher subsidence in the depressions and lower subsidence in the Southern Uplift.

**Figure 8.** (**A**,**B**) Balanced cross-sections created based on the two profiles traversing the Lingshui and the Baodao Sag, respectively (for location, see Figure 1).

**Figure 9.** (**A**,**B**) Subsidence curves created based on the two sections traversing the Lingshui and the Baodao Sags, respectively (for location, see Figure 1). The subsidence rate was low in the period of the Sanya and Meishan deposition, then increased slightly during the period of the Huangliu Deposition, and increased sharply from the period of the Yinggehai Deposition. Moreover, the subsidence rate of the depressions is higher than that of the Southern Uplift after the period of the Huangliu Deposition. N1s = Sanya Fm., N1m = Meishan Fm.; N1h = Huangliu Fm.; N2y1 = Lower Yinggehai Fm.; N2y2 = Upper Yinggehai Fm.; Ql = Ledong Fm. Ma = Megaannus.

### **5. Discussion**

The mounded topography in the study area was previously supposed to be the result of the incision of bottom currents or channels [14,15]. The main evidence supporting this view is that some troughs between the mounds are characterized by high amplitude reflections marking the sand-prone lithologies which may be a clue to the incision [4,14,15], as shown in Figures 3C–E and 7B,C. However, quite a few troughs distributed over a wider area are characterized by weak amplitudes, probably marking the bathyal–abyssal deposits [5,18] (Figures 4C and 5C). Additionally, the internal reflectors within most of the mounds have folded seismic patterns, which might be related to other forces rather than the incision (Figures 3–5). Moreover, paleogeomorphology indicated that the seabed over the Southern Slope roughly inclined toward NNW after the deposition of the Meishan Fm (Figure 6). If the troughs were indeed derived from the incision, their axes should have tended to the downdip of slope (NNW) in most situations [21]. However, it is not consistent with the result shown in Figure 7, with most of the troughs tending to be parallel to the strike of the slope (SWW–NEE and SW-NE). These doubts implied that the origin of the mounded topography cannot be simply explained solely by incision. In the examples from the Gulf of Mexico, the Brazilian margin, and the Central North Sea, the undulated morphologies can appear over tectonically active slopes [3,21,22,54–57]. Similar geological phenomena were observed at the seabed of the Shenhu Sea (Figure 10A) [40] and the south of the QDNB (Figure 10B), featured by seemingly mounded topography related to the disturbance of strata by detachment faults.  Such a process can be triggered by rapid deposition, earthquakes, seafloor

steepening, and excess pore pressure [58,60]. These studies provided an important insight into discovering the origin of a mounded topography in the study area.

**Figure 10.** (**A**,**B**) Seismic profile and its geological interpretation showing the seemingly mounded topography on the seabed caused by submarine landslides in the Shenhu Sea in the northern South China Sea (profile quoted from [40]). (**C**,**D**) Seismic profile and its interpretation showing the seemingly mounded topography on the seabed in the Southern Slope (for location, see Figure 1). DS = detachment surface; DF = detachment fault; DFT = downfaulted trough; TWT = two-way traveltime.

In this study, the mounded features were interpreted to result from the gravity gliding that was induced by tectonic activities. Firstly, detailed examinations of seismic data revealed that the uppermost layer of the Meishan Fm. was dismembered into a series of moderately deformed blocks by a number of faults with listric geometries which ceased downward to a unified surface (Figure 11A–C). The blocks resting upon the fault planes have shown clockwise rotation, with their internal beds perpendicular to the concave upward fault planes (Figure 11A–C). Secondly, soft-sediment deformation associated with gravity gliding might have occurred in the mounds (blocks) with their internal reflections showing convex-up fold structures and disturbed bedding (Figures 3–5 and 11A–C) [61]. Such phenomenon can be related to the rollover anticlines unique to the listric growth faults or associated with the local compressive stresses pervasive in slide blocks which cause internal beds to buckle [22,62,63]. These features are consistent with the gravity slide tectonics shown in some important examples documented previously [3,21,22,54–57]. It can be inferred that, after the end of Meishan deposition, the uppermost unconsolidated deposits composed of mudstones mixed with thin argillaceous siltstones glided along an underlying shear plane which is probably the top of deep lithified strata [3,15,20,21,39]. Finally, the unbalanced subsidence corresponding to the time equal to the top of the Meishan Fm. was likely to trigger the gravity gliding of sediments which created the mounds. Specifically, the subsidence of the basin shows a decreasing trend from the Central Depression to the southern margin since 10.5 Ma, which immediately steepened the Southern Slope with an NNW inclination (Figures 6 and 9). Studies indicated that the occurrence of a steepening slope induced by the basement-driven differential subsidence was an important aspect of creating sufficient driving forces to drive the gravity gliding [3]. Some scholars suggested that the differential subsidence triggered an intense erosion of the turbidity currents, which created the embryo of the Central Canyon in the late Miocene [64–68]. Therefore, it can be inferred that the differential subsidence across the

Southern Slope since 10.5 Ma might have generated sufficient forces to drive the gravity gliding that created the mounds.

**Figure 11.** (**A**) Uninterpreted seismic profiles, (**B**) interpretations, and (**C**) their geological models showing the formation of the mounded stratigraphy (for locations, see Figure 1).  DS = detachment surface; DF = detachment fault; DFT = downfaulted trough; TWT = two-way traveltime.

Further analysis indicated a time–space coupling relationship between the formation of mounds and the tectonic events including accelerated subsidence, magmatic activity, and fault reactivation. The accelerated subsidence in the post-rift stage has been observed in many rifted basins, which was considered to be related to the deep thermal anomaly [23,69–71]. Detailed examination of seismic data revealed a large number of magmatic intrusions distributed near the deeply rooted faults (Figure 12B). These faults likely extend deeply into magma chambers beneath the Central Depression to provide primary pathways for magma migration [25]. Studies indicated that massive magmas invading up

to the cold upper crust through the faults might contribute to the decay of a deep thermal source and the cooling of the asthenosphere, which would cause rapid subsidence [72–74]. The samples from adjacent areas indicated that the magmatism typically occurred in the Miocene and more recently [25,37]. Therefore, the accelerated subsidence since 10.5 Ma was likely related to the magmatic activities. In addition, such subsidence showed a higher rate at the crustal thinning zone beneath the Central Depression and decreased to the north and south of the basin (Figure 9). Under the influence of differential subsidence, the stratum of the basin was folded into a syncline, which induced extensional strain at the flanks of the syncline [74] (Figure 13A). Many Neogene faults extended upward to the interface T4 (Figure 12C,D), indicating that their formation age dated 10.5 Ma. It can be inferred the extensional strain induced by differential subsidence was accommodated by the generation of faults in the deep rigid layers, as well as the gravity slide tectonics in the shallow soft layers (Figures 12D and 13A) [75]. Although it is a speculation, local seismic disturbance caused by magmatic activity and fault reactivation might also have triggered slope instability and gravitational sliding [57,60,76–79].

**Figure 12.** (**A**) Seismic profile and (**B**) its interpretation showing the magmatic intrusions associated with the deeply rooted faults (for location, see Figure 1). (**C**,**D**) Seismic profile and its interpretation show the dense post-rift faults developed in the eastern depression (for location, see Figure 12A). TWT = two-way traveltime.

**Figure 13.** (**A**) Model to explain the formation of mounded morphologies in the study area of the Qiongdongnan Basin. Escape of massive magmas through the faults contributed to the cooling of the hot mantle material beneath the crustal thinning zone, resulting in quicker subsidence in the overlying Central Depression. The differential subsidence caused the gravitational gliding of the uppermost layers and the generation of faults in the deep rigid layers. The downfaulted troughs steered the gravity flows along their axes. (**B**–**E**) Diagrams illustrating the geological processes responsible for the creation of mounded stratigraphy.

Here, the processes responsible for the formation of mounded stratigraphy are summarized. Firstly, differential subsidence associated with magmatic activities steepened the slope at the end of the Meishan deposition, leading to the gravity gliding of the uppermost unconsolidated layer along a detachment surface (Figure 13B,C). Such a process generated a series of listric detachment faults with numerous tilted fault blocks resting on their fault planes (Figure 13C). The arcuate fault planes and the flanks of blocks together formed the undulated topography. Studies indicated that the denudation of some structural highs

in the southern margin at the turn of the middle and late Miocene generated sedimentary sources, which were transported farther into the basin by gravity flows [15]. Then, there might have been some downfaulted troughs steering the gravity flows along their axes, with the unloading of sand-rich deposits at the bottom (Figure 13D). Deposition of other troughs without passing of gravity flows was predominantly from the succeeding bathyal–abyssal muds (Figure 13D). Finally, the Huangliu Fm. onlapped onto and leveled the mounded topography with its final shape adjusted by compaction (Figure 13E). The results of this study do not deny the existence of the erosion of gravity flows, which is also one of the processes that enhanced the relief amplitude of the mounded geometries. It is worthwhile to mention that gravity gliding derived from differential subsidence is decisive for the creation of mounded topography, while erosion and other processes are considered to be of secondary importance and will embellish such topography rather than create it. The differential subsidence associated with magmatic activities led to the development of mounds, which in turn became important clues implying revolutionary changes in tectonic movement that took place at the time equivalent to T4.

### **6. Conclusions**

Detailed examination of seismic data revealed a unique mounded topography corresponding to the top of the Meishan Fm. in the Southern Slope of the QDNB. Such topography is characterized by the mounds alternating with 'V'-shaped troughs, which display elongated ridges flanked by similar gullies trending roughly parallel with the strike of the slope (SWW–NEE and SW-NE). The height of the mounds varies from about 70~210 m, and they are about 0.9~2.4 km in width. The internal reflectors within the mounds were truncated by the reflector T4 which is in turn overlain by seismic strata corresponding to the Huangliu Fm. Since the late Miocene (ca. 10.5 Ma), under the influence of magmatism, rapid subsidence occurred, which was manifested by the decreasing of subsidence from the center to the south of the depression. Such differential subsidence induced fault reactivation and steepened the slope. These tectonic events triggered the gliding of the uppermost deposits, which generated a series of listric detachment faults that ceased downwards a unified detachment surface. The top of tilted fault blocks that were constrained by these faults formed the rudiment of mounded topography. The downfaulted troughs steered the gravity flows and leveled by the lag deposits or bathyal–abyssal muds. The genetic model of the mounds established in this study accentuates the decisive contribution of tectonic activities to the creation of the mounded topography.

**Author Contributions:** Methodology, L.X. and T.Z.; investigation, L.X. and J.R.; formal analysis, L.X., J.R. and H.D.; writing—original draft preparation, L.X.; supervision, W.S., R.W. and Y.H.; conceptualization, R.W.; writing—review and editing, R.W.; software, Y.H., H.D., J.H. and Y.D.; funding acquisition, R.W. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research was funded by the National Natural Science Foundation of China (No. 42202121).

**Data Availability Statement:** The data relevant with this study can be accessed by contacting the corresponding author.

**Acknowledgments:** This study was financially supported by the National Natural Science Foundation of China (No. 42202121). The data acquired in the research process is primarily attributed to Guangzhou Marine Geological Survey, Guangzhou. Thanks to the editor and reviewers for the suggestions and other assistance in improving this manuscript.

**Conflicts of Interest:** The authors declare no conflict of interest.

### **References**


*Editorial* **Sausages: Nutrition, Safety, Processing and Quality Improvement**

**Javier Carballo 1,2**

Sausages are one of the oldest processed foods known to man. Several hundreds of varieties of sausages are produced worldwide with outstanding social and economic relevance. Each local variety within each sausage type (raw, scalded, cooked, or raw and fermented/ripened) reflects the availability of raw materials, the climate conditions of each geographical environment, the cultural and religious conditionings, and the ancestral manufacture knowledge transmitted through generations.

It is evident and expected that the different local varieties of sausages and the art of making them were perfected over centuries through the experience and the successes/failures in the production processes of the different generations.

However, similar to the manufacturing of other foods and to other production processes in general, the scientific knowledge of the physical, chemical and biological events that take place during the production processes and that are responsible for the nutritional value, sensory characteristics, and chemical and microbiological safety of the final products is relatively recent and, as in other cases, is based on the previous advances of basic disciplines such as chemistry and biology. Ultimately, it is the scientific knowledge of these events that allows them to be controlled and directed and to achieve sensory and nutritional excellence in the finished products.

Without disregarding specific works carried out in other countries, the dawn of scientific knowledge of sausage manufacturing was located in Germany during the central decades of the last 20th century. A good part of the scientific knowledge generated from the study of German local sausage varieties is collected in manuals [1,2] that are now timeless classics and an indisputable reference in the scientific literature of this field. These manuals also contain tips and indications for making sausages of high and constant quality, avoiding the most common defects and manufacturing accidents.

Among all the sausage types, the manufacture of dry-fermented sausages has special complexity, considering that the organoleptic characteristics of these products are the result of a series of modifications of the raw materials and ingredients promoted by the meat tissue enzymes and the microorganisms present, interacting with each other, and that these activities are modulated by the ingredients (salt, species, etc.) and the environmental conditions during the ripening process. As they do not receive heat treatment, they are also the sausages that present the greatest microbiological risks. The greatest research effort in this field has been devoted to the study of this type of sausages. After a series of pioneering studies that were duly reviewed by Lücke [3], starting in the 1980s of the last century studies of biochemical and microbiological characterization of the different local varieties of dry-fermented sausages multiplied. The results of all these studies, carried out mainly on local varieties of Italian, French, Spanish, Greek and Portuguese sausages obtained through spontaneous fermentation, coincide in pointing out the constancy, but uneven intensity, of the glycolytic, proteolytic, lipolytic and oxidation processes that take place in the different varieties of sausages during maturation and the role in these processes of the enzymes of muscle and fat and of the microorganisms.

Regarding the results of the studies on the microbiological characteristics of these local sausage varieties, the lactic acid bacteria and the microorganisms belonging to the

**Citation:** Carballo, J. Sausages: Nutrition, Safety, Processing and Quality Improvement. *Foods* **2021**, *10*, 890. https://doi.org/10.3390/foods 10040890

Received: 28 March 2021 Accepted: 15 April 2021 Published: 19 April 2021

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2021 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

*Staphylococcaceae* and *Micrococcaceae* families were revealed as the majority microbial flora with some participation of yeast and surface moulds in concrete varieties. Lactic acid bacteria develops rapidly during the fermentation of raw-cured sausages, reaching counts of 108–109 c.f.u./g, which remain practically stable until the end of the drying/ripening stage. The participation of this microbial group is decisive for the assurance of the hygienic/sanitary quality of the sausage, as they are responsible for the production of organic acids (lactic and acetic) and the reduction of the pH values. This decrease in pH inhibits the development of spoiling bacteria, accelerates the dehydration process of the product by reducing the water holding capacity of proteins, influences color formation and stability, and contributes to the aroma and flavor of sausages, especially those of short maturation. In addition, they can produce bacteriocins, protein compounds that also contribute to its antimicrobial activity, facilitating its implantation and inhibiting the development of unwanted microorganisms. The lipolytic activity of lactic acid bacteria is considered weak, but not so its proteolytic activity, which has been studied and demonstrated especially in different *Lactobacillus* species.

Due to their greater resistance to salt and their lower oxygen demand, staphylococci largely prevail over micrococci in this type of meat product. Staphylococci reach counts of around 107 c.f.u./g. The growth of these microorganisms is inhibited by the reduction of the pH values, so that only in the case of sausages prepared with high nitrate and low carbohydrate concentrations these microorganisms can become the main microbiota outperforming lactic acid bacteria. The role of staphylococci in the manufacturing processes of meat products is mainly focused on three metabolic activities: (i) nitrate and nitrite reductase activities that make it possible to develop the typical red color in these products, as the nitric oxide formed reacts with the myoglobin and yields nitrosylmyoglobin, pink in color, (ii) catalase activity that degrades the peroxides accumulated in the sausages during the fermentation and that could have negative effects by oxidizing the iron and the cured color, also favoring lipid oxidation reactions, and (iii) proteolytic and lipolytic activities as they have numerous lipases and proteases that favors the triglyceride breakdown, and the formation of peptides, amino acids and other compounds, being all of them the origin of volatile compounds significantly affecting the aroma of the product.

Molds are aerobic micro-organisms, so their growth is fundamentally superficial, reaching in some sausage varieties counts of 105–107 c.f.u./cm2. The presence of a surface microbiota in sausages carries a series of desirable effects, prevents the formation of a superficial crust favoring homogeneous dehydration of the product, avoids rancidity by protecting the sausage from the pro-oxidant effect of light, and contributes to the development of the characteristic aroma and flavor due to the lipolytic and proteolytic capacity of some mould strains. The yeast population in raw-cured sausages has been scarcely studied because its low proportion compared to the bacterial microbiota led to the undervaluation of his role by many authors. Yeasts are found in fermented sausages at levels varying from 103 c.f.u./g to 105 c.f.u./g throughout the manufacturing process. The yeasts contribute to the stabilization of the color of the sausage by displacing oxygen and degrading peroxides due to its catalase activity. Furthermore, their proteolytic and lipolytic activities contribute to the development of the characteristic flavor and aroma of each product.

In the last decades, from each of these microbial groups, isolates were taken from the most common dry-fermented sausage varieties and identified using both classical and molecular methods. With some minor differences among sausage varieties, the microbial profile of the sausages obtained by spontaneous fermentations is quite consistent regardless of the types and regions of origin. Among the lactic acid bacteria, although other genera such as *Leuconostoc*, *Carnobacterium*, *Pediococcus* and *Enterococcus* have been described, the lactobacilli and above all the homofermentative lactobacilli are the main group, being *Lactobacillus sakei*, *L. curvatus*, *L. plantarum* and *L. alimentarius* in this order the main species isolated. *Lactobacillus sakei* seems to be the better adapted species to the ecosystem represented by the dry-fermented sausages and to its special environmental conditions. Among the isolates of staphylococci identified, *Staphylococcus xylosus* largely predominated followed by other species such as *S. carnosus*, *S. equorum*, *S. epidermidis*, *S. saprophyticus*, *S. lentus* and *S. sciuri*. Among the molds present in the meat and meat products, species of the genera *Mucor*, *Rhizopus*, *Aspergillus* and *Penicillium* have been described as dominant, being *P. nalgiovense* and, to a lesser extent, *P. chrysogenum* the main *Penicillium* species. *Debaryomyces hansenii* was reported as the main and more consistent species of yeast. It is the majority participation of one or the other of these microbial species together with the particular application of some processes such as smoking or the addition of specific spices and additives that configures the particularities that give personality to each of the sausages from the different countries and regions.

When raw-cured sausages are manufactured in the traditional way, without the addition of starter cultures, the prevailing environmental conditions in the sausage favor the selective growth of already adapted microbiota. As a way to ensure that this desired microbiota is present, a practice used for many years consisted of inoculating a portion of previously fermented meat to the fresh mix, with which products of greater consistency and stability are obtained. Jensen and Paddock [4] were the first authors to investigate the possibility of using a *Lactobacillus* strain in the production of raw-cured sausages, arousing the interest of other researchers, both Europeans as well as Americans, who began a more in-depth study of the starter cultures and their application to the meat industry.

The starter cultures are added to the mix in order to adequately control the fermentation and maturation processes of raw-cured sausages in such a way as to standardize the process and the quality of the end products. This is possible because the metabolic activities that the starter cultures develop during the processing of meat products and having an effect on various quality factors. The added microorganisms establish themselves as the predominant microbiota, directing fermentation and excluding the undesirable microbiota, thus reducing hygienic risks and accidents of manufacturing due to deficiencies of microbial origin. Furthermore, due to their fermentative, proteolytic and lipolytic activities, they improve the nutritional and sensory qualities of the product, while improving the speed and homogeneity of drying, which is a technological advantage. Nevertheless, commercial starter cultures must meet a number of safety requirements and must have technological competitiveness and economic viability so that their application generates the benefits expected. With regard to safety, microorganisms used as starters must not possess neither toxic nor pathogenic activity and the preparations must be free of any type of polluting, biological or chemical. With regard to technological functions, microorganisms inoculated should predominate over the spontaneous microbiota of the meat mass and develop their metabolic activity. Finally, in terms of economic aspects, the use of the starter cultures must be economically viable and easy to handle. In addition, the storage of frozen of lyophilized cultures should not affect the properties of the strain or cause losses from their activity.

The first starter culture with application in the meat industry that appeared on the market was a strain of *Pediococcus cerevisiae* [5], later classified as *Pediococcus acidilactici*, which was marketed by the Merck company in the U.S.A. in 1957 for the production of summer sausages and spreadable sausages. Almost at the same time, in Germany in 1961 it was commercialized a strain of *Micrococcus* (*Micrococcus* M53) [6] supplied by the Rudolf Müller company, and in 1966 a starter culture appeared for the first time, combining *Lactobacillus plantarum* with a strain of *Micrococcus* [7]. However, the widespread use of starter cultures in the meat industry did not begin to develop until the 1980s, mainly due to the fact that it is possible to obtain dry-fermented sausages of excellent quality without the addition of them [8]. The use of starter cultures, generally composed by a lactic acid bacteria (mainly a *Lactobacillus* strain and a coagulase-negative staphylococci (CNS), is a common and effective practice in the manufacture of fermented sausages in order to improve the color and flavor development, ensure safety and extend shelf-life.

The use of starter cultures and its effect on the microbiological, physicochemical and safety attributes of the different local varieties of dry-fermented sausages was one of the most recurrent research topic in the last decades. However, the use of a commercial nonautochthonous starter culture could have a negative impact on the sensory characteristics of the sausages, resulting in losses of the particularly desirable organoleptic properties that characterize each sausage type. Therefore, the development of specific starter cultures composed by strains isolated from spontaneous non-controlled elaborations of the corresponding type of sausage and adequately characterized in their metabolic performances has aroused the interest of researchers.

Currently the lines of research in relation to the use of starter cultures in the meat industry have been expanded in their objectives. Different authors have tried the addition of proteases and lipases in order to promote the development of the aroma and accelerate the processes of maturation in raw-cured sausages. Finally, another current line of research is on the use of probiotic lactic acid bacteria as starter cultures in raw-cured sausages, thus obtaining functional foods.

The safety of the sausages has also been the subject of abundant studies in recent decades. The microbiological hazards, mainly represented by foodborne pathogens such as *Listeria monocytogenes*, *Staphylococcus aureus*, *Escherichia coli*, *Salmonella* spp., *Yersinia enterocolitica*, and even less frequent pathogenic agents such as *Mycobacterium avium* subsp. *paratuberculosis*, *Aeromonas* spp., or hepatitis E virus, have been appropriately identified in sausages with different biochemical and technological features. In the same way, the chemical hazards, mainly biogenic amines, nitrosamines, mycotoxins, and polycyclic aromatic hydrocarbons in the particular case of smoked sausages, have been duly characterized. Measures of control and prevention of both microbiological and chemical hazards have been developed and essayed. The use of starter cultures appropriately selected can be a solution for most of these hazards.

In recent times, consumers are increasingly concerned about the relationship between health and diet, and they demand foods that are not harmful to their health and, ideally, even that protect and improve it. In this sense, there are concerns about the excessive salt content and the quantity and quality of fat in the diet and its proven relationship with some cardiovascular diseases and certain types of cancer. Traditional sausages are characterized by high salt and fat contents that are necessary to maintain their typical sensory attributes. In such scenario, the reduction of NaCl and/or its partial replacement with other salts, mainly KCl, CaCl2, MgCl2, and/or sodium ascorbate, was essayed obtaining final products having acceptable organoleptic characteristics.

Regarding the modification of the lipid fraction in sausages, the first strategies was the reduction of the fat content and/or the replacement with non-lipid substitutes. This task has not been easy because fat highly contributes to the texture, flavor and mouthfeel of these meat products.  In cooked meat products, some ingredients such as proteins, carbohydrates and fat-based substitutes were essayed with generally satisfactory results, especially when carbohydrates were used as fat replacers. In raw fermented sausages, the use of inulin or several other dietary fibres from fruits or cereals as fat replacers gave satisfactory results on texture and sensory properties. The use of dietary fibres as fat replacers has an added health benefit because increased proportions of fibre in the diet has been proven to reduce the risk of colon cancer, cardiovascular disease, obesity and several other disorders.

In addition to the amount of fat in the diet, the fatty acid profile of the ingested fat has a proven impact on consumer health. The formulation of the sausages has not remained unaffected by this concern. In addition to the attempt to modify the composition of animal fat used as raw material, especially through diet modifications but also by genetic selection, several studies have tried to modify the fatty acid profile of sausages by substituting animal fat by vegetable oils, mainly olive oil, or their corresponding oleogels.

The articles included in the present Special Issue show important and interesting advances and new approaches in most of the research fields mentioned.

As indicated, the study of the microbial communities of the dry-fermented sausages has been one of the most important research topics in recent years. The investigation on the microbial species diversity in fermented sausages is not only important to study the relationship between microbial species, physicochemical features and organoleptic characteristics and to gain control over quality development. It is also appropriate to better understand the link between microbial communities, specific technological features, breeding systems, geographical regions and the differential attributes that gives personality to the finished products. Comi et al. [9] studied the variability of the lactic acid bacteria in fermented sausages due to different pork breeds, breeding systems and production technology. They applied a semi-quantitative molecular method to study the alternation of the different species over time and their concentration ratios. The results of a cluster analysis in this article provide evidence of a plant-and breed-specific ecology of lactic acid bacteria. The authors have also observed that the breeding system can influence the presence of certain LAB species in the sausages.

The use of culture-independent methods presents clear advantages compared to classical methods when it comes to having a real vision of the species present and acting in a sausage throughout its production, and for this reason they have become the methods of choice in recent years. However, many of these methods still have limitations such as a taxonomic resolution not entirely satisfactory. In this context, Van Reckem et al. [10] studied the application of a previously developed high-throughput amplicon sequencing method targeting the 16S rRNA and *tuf* genes to characterize the bacterial communities of 15 fermented meats from 5 European countries. The authors also tried to associate the microbial communities of the different products with their physicochemical features and geographical origin. The obtained data broadened the view on the microbial communities associated with the products analyzed, revealing the presence of subdominant microbial species, particularly coagulase-negative *Staphylococcal* species, underreported in previous studies. On the other hand, the particular composition of the microbial communities could be linked to the special features of the particular products, mainly pH values, salt content and geographical origin.

The inclusion of a concrete microbial strain as starter culture in a fermented product requires a previous exhaustive study of its metabolic abilities in the most diverse possible environmental conditions and also in the presence of the most different substrates. All this is necessary to know what its viability and its performances are and what we can expect from that particular strain when we add it. *Lactobacillus sakei* is widely used as starter culture in fermented sausages due to its outstanding adaptation to meat environments and its ability to maintain high viability thanks to the possession of secondary pathways that are activated when hexoses are deplected. Barbieri et al. [11] studied the metabolism of *Lactobacillus sakei* Chr82, a commercial strain, in the presence of different concentrations of fermentable sugars. They inoculated this strain in a defined medium with glucose or ribose as the only carbon source, both at optimal or reduced concentrations, in order to evaluate its different metabolic and physiological responses to different growth conditions. The results evidenced different growth performances, physiological states of the cells and amino acid consumptions in relation to the carbon source and carbohydrate levels.

The probiotic bacteria have a renewed interest at the present time, given the accumulated evidence on the importance of the human intestinal microbiota on the health derived from its functionality and its interaction with the physiology of other organs, particularly skin and brain. Fermented sausages can be a good carrier for the probiotic lactic acid bacteria, and at the same time that a functional food is elaborated, the metabolic characteristics of the added strains can be exploited, making them act as starter cultures. With this aim, the use of probiotic strains as starter cultures needs a previous study on their technological characteristics to take advantage of their beneficial activities and avoid their undesirable effects on the quality and safety of sausages. Agüero et al. [12] evaluated the in vitro technological and safety characteristics in eight LAB strains having proved probiotic activity. They reported that some of them are good candidates for use as starter

cultures in fermented sausages because their metabolic performances including antimicrobial activity against some of the most known pathogens. One concrete strain, *Lactobacillus rhamnosus* Lr-32, was the most promising among the tested strains but further studies are needed to check and endorse its behavior in a meat matrix.

In local varieties of fermented sausages having a strong personality and with defined and loyal markets, the use of autochthonous starter cultures is the most appropriate way to obtain manufactured products that are uniform, of high and constant quality and that retain the differentiated attributes of their homonyms artisanally obtained through spontaneous fermentations. Rodríguez-González et al. [13] studied the effect of the addition of two different autochthonous starter cultures including one strain of *Lactobacillus sakei* and one of *Staphylococcus equorum* or *Staphylococcus saprophyticus* on the biochemical changes occurring during the manufacture of Galician chorizo sausage, the most popular traditional meat product in the NW Spain. Along the manufacture of three independent batches made with each of the two starter cultures, they studied the changes in proximate composition, pH, Aw, color parameters, nitrogen fractions, free amino acids, biogenic amines, fat parameters, and free fatty acids. The two starter cultures showed good performances and seem to be suitable for increasing the quality and safety of this type of sausage.

Chemical hazards are the subject of special attention in ongoing investigations. Smoking is a process commonly applied to certain sausage types. In the past, it was applied mainly to aid in the preservation of the products due to the antimicrobial or antioxidant activity of some of the components of the smoke, and also due to a certain degree of surface dehydration that took place during the process and that contributes to the inhibition of microbial growth. At present, it is maintained as a hedonic agent, by giving the products a desirable and characteristic color, flavor and aroma. However, some of the components of smoke belonging to the family of polycyclic aromatic hydrocarbons (PAHs) are potential carcinogens and pose a chemical risk to be controlled during sausage manufacture. Usually, controlling the smoking temperature is key to limiting the deposition of PAHs during the process, but in the artisanal traditional smoking processes other strategies to achieve this end should be adopted. In the present Special Issue, Fraqueza et al. [14] make an interesting contribution in this area trying to optimize the smoking process of traditional dry-cured meat products to minimize the presence of PAHs. In this work, dry-cured sausages were submitted to four three different treatments: (i) without smoking, (ii) 20 h effective smoking, (iii) 60 h effective smoking, and (iv) effective smoking until reaching weight losses of 38–40%. The total PAHs content was generally low and did not differ significantly among the four different smoking regimes. The PAH4 (sum of four different polycyclic aromatic hydrocarbons: benzo[*a*]anthracene, chrysene, benzo[*b*]fluoranthene, and benzo[*a*]pyrene) and the benzo[*a*]pyrene contents were below the stablished legal limits in all the analyzed sausages.

The partial or total replacement of the traditional ingredients in sausages with unconventional raw materials allows the obtaining of novel and varied products capable of satisfying the needs of people who have consumption choices limited by cultural conditions, religious beliefs, personal convictions or health reasons. However, the incorporation of these new ingredients leads to the appearance of technological problems in manufacturing and also of organoleptic deficiencies in the final products that must be solved.

Within this research topic, Cullere et al. [15] studied the effect of two different fat inclusion levels, NaCl contents and LAB starter cultures on the weight loss and nutritional characteristics of an Italian-type ostrich salami. Among other results, authors observed that the lowest fat and highest NaCl level provided the greatest cumulative weight loss throughout manufacturing, but by reducing the NaCl level the weight loss was retarded without affecting the nutritional composition of the final sausage. The authors concluded that it is possible to obtain a salami from ostrich meat with lower salt and fat contents, while maintaining a satisfactory quality of the final product.

 Microwave-assisted extraction allows the obtaining of mango peel pectin with improved properties compared to that obtained using the conventional extraction method. Quality attributes (color, texture, and sensory characteristics) of experimental sausages were assessed and compared to those manufactured using the control formula without fat replacement. The authors concluded that the substitution of 5% of fat with pectin in the Chinese sausage could enhance color while conserve the physical qualities and sensory attributes. Therefore, mango peel pectin can be utilized in the low-fat Chinese sausage formulation as a novel fat replacer.

Vargas-Ramella et al. [17] studied the effect of partial (50%) replacement of the animal fat with healthy oils (olive, canola, and soy oil emulsions immobilized in Prosella gel) on the physicochemical attributes, texture, fatty acid profile and volatile compounds of dry-fermented deer sausage. Reformulated sausages were darker, harder, and with higher pH values than control sausages made using only animal fat. Use of soy and canola oils increased the polyunsaturated fatty acid and the w-3 fatty acid contents while decreased the w-6/w-3 ratios and the saturated fatty acid contents, thus allowing the obtaining the best nutritional properties. Regarding the effect on the volatile compounds, the animal fat replacement increased the content of the total and most of the individual volatile compounds. However, the control samples presented equal or higher contents of volatile compounds derived from the lipid oxidation processes than the reformulated sausages. Sausages reformulated with vegetable oils showed higher consumer acceptance than control sausages. In conclusion, replacement of animal fat with vegetable oils, particularly soy oil, could be an excellent strategy to elaborate healthy fermented sausages.

The use of non-meat ingredients in high percentages in sausages with the aim of obtaining healthier products may affect the microbial growth and chemical stability during storage and therefore the shelf-life of the novel sausages. Preservatives should be added in order to improve the shelf-life and safety, but consumers interested in healthier meats request at the same time products without synthetic additives. The search and the essay of natural substitutes for synthetic additives is consequently a challenge for researchers. Ranucci et al. [18] studied the effects of different concentrations of a commercial mix of extracts of pomegranate and citrus on the growth of spoilage microorganisms and on the oxidation during storage in vacuum-packaged cooked sausages made from pork meat, emmer wheat, almond and hazelnut. The authors reported that the use of the mix, particularly at a concentration of 10 g/1000 g delayed the pH decrease and the lipid oxidation processes during storage. The mix also lowered the maximum growth rate of total viable bacteria, lactic acid bacteria, and psychrotrophs. The sensory analysis carried out by sausage consumers showed an increase in the shelf-life of 6 and 16 days for the sausages made by the addition of 5‰ and 10‰ of the extract mix, respectively.

This Special Issue ends with an interesting review made by Martuscelli et al. [19]. Some religious convictions and beliefs and the restrictions imposed on the food to the practitioners entail limitations on the raw materials to be used in the manufacture of meat products (animal species and the ways in which they are slaughtered), and in processing conditions. Various scientific studies were conducted until now on ritual slaughtering practices and manufacturing of meat products for Jewish and Muslim religious communities. On the other hand, the authenticity and traceability of meat is one of the priorities of halal food certification systems in order to prevent fraudulent practices motivated by both ¯ economic and technological reasons. In their article, Martuscelli et al. [19] reviewed studies conducted on the safety, quality and analytical authentication of halal meat products, ¯ with particular attention on salami. The authors discussed the halal meat products and ¯ regulations in Europe, halal salami processing (hal ¯ al raw material, preservatives, use of ¯ spices and/or plant extracts, casings, sensory profile and the hazard represented by the biogenic amines), food safety in halal assurance, and analytical authentication of hal ¯ al¯ meat, salami and other meat products.

Study of the sausages is an exciting task that still offers many possibilities and motivations for researchers. Given the economic importance of sausages, the complexity and

variety of the physical, chemical and microbiological processes that take place during their production that make them surprising and captivating for scientists, and the fact that many of them are deeply rooted in culture and in the heritage of various countries and geographical areas, it is certain that these products will continue to be a source of attention for scientific researchers in the future.

Some sausage varieties are still hardly known in terms of their microbiological and biochemical features, or their production processes are insufficiently standardized. In other cases, there are safety or quality concerns that must be solved so that these sausages can be enjoyed to the fullest of their potential. The improvement of the sensory quality and/or the adaptation of their sensory and nutritional properties to the changes in consumer preferences and requirements, all without sacrificing the personality and differential attributes of each sausage variety, is in all cases a permanent challenge. For all these reasons, further studies and research are essential to improve and continue enjoying these privileged foods.

**Funding:** The author acknowledges the Xunta de Galicia, Spain (The Regional Government) the financial support through the CITACA Strategic Partnership (grant number ED431E 2018/07).

**Conflicts of Interest:** The author declares no conflict of interest.

#### **References**

*Article*


**ADVANCES IN SELECTED PLANT PHYSIOLOGY ASPECTS**

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**Predicting Cognitive Decline in Alzheimer's Disease (AD): The Role of Clinical, Cognitive Characteristics and Biomarkers**

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First published in Croatia, 2012 by INTECH d.o.o. eBook (PDF) Published by IN TECH d.o.o. Place and year of publication of eBook (PDF): Rijeka, 2019. IntechOpen is the global imprint of IN TECH d.o.o. Printed in Croatia

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Chemical Biology Edited by Deniz Ekinci

p. cm. ISBN 978-953-51-0049-2 eBook (PDF) ISBN 978-953-51-5204-0