Influence of malocclusion and orthodontic treatment in the masticatory efficiency of patients with craniofacial disorders

Abstract

This study evaluates masticatory efficiency in orthodontic patients with craniofacial disorders compared to controls without, considering the effect of an orthodontic appliance and malocclusion. A total of 119 participants (7–21 years), divided into a craniofacial disorder and control group (n = 42 and n = 77; mean age 13.5 ± 5.2 and 14.2 ± 3.3 years) were included. Masticatory efficiency was evaluated using a standard food model test, where masticated test food bodies were analyzed, and parameters like particle number (n) and area (mm²) were recorded. This study newly introduced the masticatory efficiency index (MEI), which encompasses the above terms (number and area), with a high MEI being an indicator of high masticatory ability. Younger orthodontic patients with a craniofacial disorder had a significantly decreased MEI (0.50 ± 0.25 n/mm²) compared to patients without (1.10 ± 0.48 n/mm²; p = 0.02). The presence of a crossbite significantly decreased masticatory efficiency, particularly in craniofacial disorder patients (0.69 ± 1.44 n/mm²) versus controls (0.89 ± 1.00 n/mm², p = 0.04). As treatment progressed with age and fixed appliances, mastication group differences became non-significant, suggesting that patients with a craniofacial disorder were catching up to healthy controls in the rehabilitation of their masticatory function. Considering an early diagnosis of malocclusion during orthodontic therapy in combination with speech therapy can avoid negative malocclusion effects with growth, caused by muscle imbalances.

Graphical abstract

Highlights

• •First study implementing the Masticatory Efficiency Index (MEI).
• •Craniofacial disorders decrease masticatory efficiency and therefore the MEI.
• •Crossbite malocclusion affects MEI more in craniofacial disorders than in controls.
• •Orthodontic treatment progress increases MEI in craniofacial disorders.
• •Rehabilitation of craniofacial disorders led to catching up to healthy controls.

1. Introduction

Among different orthodontic patients, those with craniofacial disorders (CD) pose the greatest treatment challenge. With a prevalence of 1:600 [1], cleft lip and/or palate (CL/P) is among the most common CD. It can manifest in different cleft formations: right or left-sided unilateral CL/P, bilateral CL/P, cleft lip with or without alveolus (CL), and isolated cleft palate (CP). The latter is also associated with another CD, Robin sequence (RS), where CP is found in 80–90% of patients (prevalence 12/100.000) [2], and which also comprises mandibular retrognathia, glossoptosis, and upper airway obstruction [3]. Orthodontic patients with CD have special dentoskeletal growth patterns. Patients with CL/P show asymmetric growth and maxillary hypoplasia, resulting from the cleft segmentation of the maxilla and post-operative scar formation [[4], [5], [6]]. Instead, RS patients show a bimaxillary retrognathia with steep mandibular planes and an enlarged gonial angle with a shorter ramus, which results in a skeletal class II configuration [[7], [8], [9], [10], [11]]. Moreover, the extraoral picture shows a more convex profile with a deficit in the lower facial proportions, because the soft tissue cannot mask the presence of RS [12]. These patterns cause an imbalance and disruption of the dentoskeletal system, leading to severe physical and functional difficulties in daily life, involving e.g. mastication function and speech development [13,14].

The term masticatory efficiency is commonly used to describe the number of masticatory cycles required to reduce ingested food to swallowable pieces, whereas masticatory performance refers to the particle size distribution of food chewed after a standardized number of cycles [[15], [16], [17]]. For masticatory efficiency evaluation, the “sieve method” is one of the most common techniques, based on the collection and assessment of particles from previously masticated food [[18], [19], [20], [21], [22], [23], [24]]. Mastication is affected, among others, by the occurrence of malocclusion, skeletal configuration, consistency of food, and number of functional teeth. Several studies reported that patients with malocclusion have a reduced masticatory ability [[25], [26], [27], [28]]. A suitable milling of food is indispensable for an appropriate functioning of the gastrointestinal system [29]. Dysfunctional deglutition, i.e., insufficiently milled particles, is known to increase the risk of gastric diseases [30]. Patients with malocclusion were found to overestimate their masticatory capacity, when in reality they need longer chewing cycles to obtain the same results as their healthy peers and are unaware of swallowing larger food particles [17]. This could be a result of patients associating the orthodontic treatment of their malocclusion more strongly with a perceived esthetic outcome than with any masticatory benefit [31].

Given that the stomatognathic system is affected by the occurrence of a CD, mastication is also expected to be affected. While an esthetic outcome is the main factor for seeking orthodontic treatment, subjects with malocclusion may also complain about functional problems [26]. Mastication problems were mentioned in a European survey among CL/P patients as a frequent complication [32]. The influence of diverse aspects like malocclusion on masticatory efficiency has been extensively described in healthy subjects [16,27,33,34], while little is known about it in patients with CD. A previous study evaluated parameters like type of CD, cleft formation, chewing side, dentition stage, age, and sex, where an influence of all these parameters on masticatory efficiency was found in CD patients [35]. However, it is also possible that a reduction in mastication efficiency is not only associated with the presence of CD, but rather due to malocclusion in combination with orthodontic treatment. This could not only influence CD orthodontic patients, but also healthy subjects, and thus, comparing these groups may be relevant so that a deeper comprehension of the actual influence of an underlying CD on mastication can be reached. Authors are unaware of studies evaluating malocclusion in relation to orthodontic treatment comparing CD patients with healthy controls.

Thus, this study aims to evaluate the influence of malocclusion, as well as the employed orthodontic appliance, on masticatory efficiency in patients with CD and healthy controls, using a standard food model test, based on the following null hypotheses.

• •Age does not affect the masticatory efficiency of CD patients and healthy subjects.
• •Employed orthodontic appliances (fixed or removable) do not affect the masticatory efficiency.
• •Malocclusion does not affect masticatory efficiency.

2. Results

The descriptive participant sample evaluation is shown in Table 1. During a recruitment period of eight months, a total of 140 children fulfilled inclusion criteria. Of these, 21 could not be included, due to restrictions imposed by the COVID-19 pandemic, poor compliance (e.g. missing appointments), or no interest in participating in the study. This yielded a final study sample of 119 children, divided into 42 participants with CD and 77 controls (C). The CD group included 4 RS and 38 CL/P patients. The latter were further classified depending on their cleft formation and location. The mean age of participants was 14.3 years (range 7–21) in CD patients and 13.5 years (range 7–21) in the control group. The sex ratio was equally distributed in the control group, whereas there were more males in the CD group.

Table 1.

Descriptive participant sample evaluation (n and percentage [%]) according to age, sex, craniofacial malformation, cleft location, skeletal class, Angle classification malocclusion, crossbite, orthodontic appliance, and speech therapy. Abbreviations: CD = craniofacial disorder; SD = standard deviation; RS = Robin sequence; CL/P = cleft lip and/or palate; CP = cleft palate; CL = cleft lip and alveolus.

Sex	CD group		Control group			CD group		Control group
	n	%	n	%	Orthodontic appliance	n	%	n	%
Male	25	59.52	36	46.75	Fixed	21	50.00	42	54.55
Female	17	40.48	41	53.25	Removable	21	50.00	35	45.46
Craniofacial malformation	n	%	n	%	Angle class malocclusion	n	%	n	%
RS	4	9.52			Right side
CL/P	32	76.20			Class I	20	47.62	42	54.54
CP	4	9.52			Class II	10	23.80	25	32.47
CL	2	4.76			Class III	12	28.57	10	12.98
Cleft location	n	%	n	%	Left side
Unilateral	26	81.25			Class I	19	45.24	34	44.16
→Left	18	56.25			Class II	11	26.19	33	42.86
→Right	8	25.00			Class III	12	28.40	10	12.99
Bilateral	6	18.75
Skeletal class	n	%	n	%	Crossbite	n	%	n	%
Class I	6	14.29	32	41.56	Posterior	3	7.14	2	2.60
Class II	13	30.95	34	44.16	Anterior	8	19.05	2	2.60
Class III	23	54.76	11	14.29	Circular	3	7.14	1	1.30
					Non	28	66.67	72	93.51
Speech therapy	n	%	n	%	Age
Yes	40	95.24	7	9.09	7–12 years	20	47.63	22	28.57
No	2	4.76	70	90.91	13–21 years	22	52.38	55	71.43

The most common CD was CL/P, with a left unilateral CL/P being twice as common as a right or bilateral CL/P. An equal number of isolated CP and RS patients were evaluated, whereas the smallest subgroup formed those with CL. The occurrence of a crossbite, as well as a higher skeletal class and Angle malocclusion, were more frequent in the CD group (Table 1). Among the employed orthodontic appliances, fixed and removable ones were equally distributed across groups, while fixed appliances were slightly more prominent in C (Table 1). Whereas almost all CD patients were receiving speech therapy in combination with orthodontic treatment, only seven healthy participants were attending such therapy.

When considering the employed orthodontic appliance (Table 2), removable appliances were mostly used for younger patients in both groups. Among fixed appliances, maxillary expansion and multibracket appliances were employed, with the latter being the most common. Some patients also had a combination of both appliances at enrollment. In further assessments, these appliances were summarized as fixed appliances.

Table 2.

Participant sample (n) and age (years) distribution for the employed orthodontic appliance type for the participants with and without a craniofacial disorder (CD). Abbreviations: SD = standard deviation; Min = minimum; Max = maximum.

Orthodontic appliance		CD group				Control group
		n	Age (years)			n	Age (years)
			Mean ± SD	Min	Max		Mean ± SD	Min	Max
Removable		21	11.19 ± 3.27	7	19	35	13.06 ± 3.80	7	21
Fixed	Maxillary expansion	3	15.67 ± 1.53	14	17	1	14.00 ± 0.00	14	14
	Multibracket	16	15.00 ± 2.86	10	21	39	15.49 ± 2.26	12	21
	Combination of both	2	12.50 ± 3.53	10	15	2	14.15 ± 0.50	14	15

Controls showed a higher MEI compared to the CD group (MEI_CD = 0.82 ± 1.15; MEI_C = 1.50 ± 2.25), but this was not statistically significant (p = 0.06). Older patients (13–21 years) with or without CD showed a higher MEI compared to younger ones (7–12 years) (MEI_{CD_young} = 0.50 ± 0.25 n/mm²; MEI_{CD_old} = 1.12 ± 0.24 n/mm²; p = 0.22; MEI_{C_young} = 1.10 ± 0.48 n/mm²; MEI_{C_old} = 1.63 ± 0.30 n/mm²; p = 0.62), but again this difference was not statistically significant. Within the younger patient group, those with CD had a significantly lower masticatory efficiency than the control group (p = 0.02).

Patients with CD employing a fixed orthodontic appliance had no significantly better masticatory efficiency than those with removable devices (p = 0.42) (Fig. 1). Similar results were found in the control group (p = 0.30). There were no significant differences between both groups for removable (p = 0.29) and fixed (p = 0.20) appliances, but orthodontic patients without CD showed better masticatory efficiency within each type of appliance (Fig. 1).

Fig. 1.

Age group (left) and employed appliance (right) effect on the Masticatory Efficiency Index (MEI) (n/mm²) results of craniofacial disorder (CD) (n = 42) and control (C) groups (n = 77). Age groups comprised of two groups: 7–12 years and 13–21 years. All nine chewing cycles were considered for the MEI evaluation. Groups were compared by the Kruskal Wallis test, and those revealing a statistically significant difference were denoted by (*) (p < 0.05).

To obtain a better understanding of the role of malocclusion, both dental and skeletal malocclusion were evaluated, including the occurrence and type of crossbite, skeletal, and Angle classification type.

Concerning the occurrence of a crossbite, this study found this to be significantly reduced for all obtained parameters in patients with CD, while the control group was not affected. However, it must be noted that this group comprised only 5 children (Table 3, Fig. 2).

Table 3.

Influence of crossbite malocclusion on masticatory efficiency in CD (n = 42) and control (n = 77) groups, concerning the total test (all nine chewing cycles). Mean and standard deviations of particle number (PN) (n), area (A) (mm²) and Masticatory Efficiency Index (MEI) (n/mm²) were given. Statistical significance was considered at p < 0.05 and denoted with (*).

	Crossbite				No crossbite
	Count	PN (n)	A (mm2)	MEI (n/mm2)	Count	PN (n)	A (mm2)	MEI (n/mm2)
CD group	14	49.29 ±64.38	258.27 ±150.37	0.69 ±1.44	28	68.00 ±48.90	160.23 ±103.60	0.89 ±1.00
Control	5	91.40 ±65.37	141.39 ±122.47	1.40 ±1.34	72	84.13 ±74.34	147.22 ±106.93	1.49 ±2.30
P-value		0.13	0.13	0.13		0.54	0.41	0.49

Fig. 2.

Influence of a crossbite malocclusion on the masticatory Efficiency Index (MEI) (n/mm²) results of craniofacial disorder (CD) (n = 42) and control (C) groups (n = 77). Groups were compared by the Kruskal-Wallis test, and those revealing a statistically significant difference were denoted by (*) (p < 0.05).

Concerning skeletal class malocclusion, patients with CD showed an amplified masticatory efficiency with an increase in skeletal class (Table 4, Fig. 3), but differences were not significant. In contrast, the MEI in skeletal class II in CD was significantly decreased, compared to C (p = 0.04) (Fig. 2).

Table 4.

Influence of the skeletal class malocclusions on masticatory efficiency of craniofacial disorder (CD) patients (n = 42) and the control group (n = 77) concerning the total test (all nine chewing cycles). Mean and standard deviations of particle number (PN) (n), area (A) (mm²), and Masticatory Efficiency Index (MEI) (n/mm²) were given. Statistical significance was considered at p < 0.05 and denoted with (*).

Skeletal class	Class I			Class II			Class III
	PN (n)	A (mm2)	MEI (n/mm2)	PN (n)	A (mm2)	MEI (n/mm2)	PN (n)	A (mm2)	MEI (n/mm2)
CD group	54.33 ±51.65	176.78 ±113.24	0.63 ±1.00	60.31 ±49.62	185.18 ±101.58	0.72 ±1.02	64.52 ±58.89	201.48 ±147.93	1.29 ±1.27
Control	86.00 ±87.44	169.98 ±117.68	1.70 ±2.70	92.00 ±64.82	118.02 ±90.78	1.53 ±1.85	57.63 ±49.08	169.49 ±109.62	0.70 ±0.10
P-value	0.59	0.65	0.59	0.08	0.02*	0.04*	0.88	0.88	0.83

Fig. 3.

Skeletal class malocclusion effect on the Masticatory Efficiency Index (MEI) (n/mm²) results of craniofacial disorder (CD) (n = 42) and control group (C) (n = 77) differed by the skeletal class malocclusion (considering all nine chewing cycles). Groups were compared by the Wilcoxon test, and those revealing a statistically significant difference were denoted by (*) (p < 0.05).

Concerning Angle classification malocclusion, patients with and without CD showed the best values for class I, and lowest for class III (Table 5, Fig. 4). No statistical difference between classes within one group was observed. Additionally, the CD and control groups had no statistically significant difference in any value recorded for each class (Table 5).

Table 5.

Masticatory efficiency comparing patients with craniofacial disorders (CD) (n = 42) and controls (n = 77) regarding the left and right-sided sagittal malocclusion classifications class I, II, and III according to E.H. Angle [66] considering all nine chewing cycles. Mean and standard deviations of particle number (n), area (mm²), and Masticatory Efficiency Index (MEI) (n/mm²) were given for different Angle class situations. Statistical significance was considered at p < 0.05 and denoted with (*).

Angle class - Right side
Class I				Class II			Class III
	PN (n)	A (mm2)	MEI (n/mm2)	PN (n)	A (mm2)	MEI (n/mm2)	PN (n)	A (mm2)	MEI (n/mm2)
CD group	61.95 ±53.04	181.57 ±112.74	0.84 ±1.13	64.50 ±41.64	164.40 ±112.87	0.75 ±0.71	59.17 ±67.75	235.57 ±160.89	0.85 ±1.52
Control	82.40 ±78.52	156.12 ±110.33	1.52 ±2.54	94.44 ±70.41	122.37 ±96.28	1.60 ±2.04	69.20 ±60.45	169.06 ±118.76	1.02 ±1.32
P-value	0.43	0.37	0.44	0.26	0.21	0.25	0.43	0.34	0.37
Angle class - Left side
	Class I			Class II			Class III
	PN (n)	A (mm2)	MEI (n/mm2)	PN (n)	A (mm2)	MEI (n/mm2)	PN (n)	A(mm2)	MEI (n/mm2)
CD group	66.42 ±51.99	166.89 ±107.44	0.90 ±1.13	60.09 ±42.12	173.00 ±110.82	0.68 ±0.71	55.92 ±69.05	252.35 ±160.45	0.83 ±1.53
Control	94.06 ±83.30	146.92 ±114.24	1.82 ±2.75	82.97 ±68.18	138.12 ±99.21	1.36 ±1.90	57.80 ±49.00	175.34 ±113.40	0.76 ±1.06
P-value	0.39	0.35	0.38	0.36	0.28	0.33	0.39	0.34	0.34

Fig. 4.

Masticatory Efficiency Index (MEI) (n/mm2) results for the craniofacial disorder (CD) (n = 42) and control (C) groups (n = 77) regarding the malocclusion parameter according to Angle class I, II, and III [66] on the right side (left) and on the left side (right) in the overall test (all nine chewing cycles). There was no statistically significant difference between groups as determined by the Wilcoxon test (p < 0.05).

The influence of the employed chewing side (right, left side, or bilateral chewing cycle only) and sample body hardness (hard, medium, or soft only) was evaluated for the different malocclusion types. Those that yielded statistically significant differences are only resumed in Table 6. The type of orthodontic appliance and the Angle malocclusion showed the least effect on masticatory efficiency, followed by the skeletal malocclusion types. For the latter, there were significant differences between skeletal class III and II concerning the control group, regarding the particle number in medium hardness leveled test bodies (p = 0.04), and the area in bilateral chewing (p = 0.04) and medium hardness level (p = 0.03). In particular, the presence of a crossbite influenced masticatory efficiency significantly in patients with CD. CD patients with no crossbite could chew the test bodies into significantly more particles (p = 0.04) and with a smaller area (p = 0.04) on the left chewing side. No significant differences were found in the control group. Comparing both groups without a crossbite, there was a significant result of the area on the left chewing side, showing better results in the control group. Patients without a CD showed a significantly higher MEI chewing hard-leveled test bodies and chewing on the left side.

Table 6.

Influence of employed chewing side (right, left side, bilateral), sample body hardness (hard, medium, soft), and malocclusion types in the craniofacial disorder (CD) (n = 42) and control (C) groups (n = 77) regarding the number of particle (PN) (n) and Area (A) (mm²) and Masticatory Efficiency Index (MEI) (n/mm²). Masticatory efficiency of the different groups was compared by the Kruskal-Wallis and Wilcoxon test, and only those revealing a statistically significant difference (*p < 0.05) were resumed here. Abbreviation: SD = standard deviation.

	Median	Mean	SD	P-value
PN (n) in C group chewing medium level
Skeletal class II	27.00	30.18	27.34	0.04*
Skeletal class III	16.00	16.82	12.85
A (mm2) in C group chewing bilateral
Skeletal class II	89.61	114.88	88.01	0.04*
Skeletal class III	137.15	184.94	133.79
A (mm2) in C group chewing medium level
Skeletal class II	88.73	125.66	101.54	0.03*
Skeletal class III	134.4	192.14	124.72
PN (n) in CD group chewing left side
No crossbite	20.00	22.48	16.81	0.04*
Crossbite	5.00	16	22.04
PN (n) in CD group chewing bilateral
No crossbite	24.00	24.78	16.48	0.02*
Crossbite	9.00	16.33	21.05
PN (n) in CD group chewing hard level
No crossbite	14.00	24.44	19.15	0.02*
Crossbite	6.00	15.80	21.63
A (mm2) in CD group chewing left side
No crossbite	126.50	178.73	133.06	0.04*
Crossbite	149.75	281.41	155.55
A (mm2) in CD group chewing bilateral side
No crossbite	99.85	147.22	109.33	0.01*
Crossbite	290.82	266.76	146.55
A (mm2) in CD group chewing medium level
No Crossbite	153.10	168.46	125.25	0.02*
Crossbite	344.52	283.71	160.81
A (mm2) in CD group chewing hard level
No Crossbite	134.07	218.12	157.47	0.04*
Crossbite	80.25	117.69	97.62
MEI (n/mm2) in between groups chewing hard level
CD group	0.89	0.24	0.38	0.04*
C group	0.18	0.55	0.92
MEI (n/mm2) in between groups chewing left side
CD group	0.09	0.27	0.40	0.01*
C group	0.19	0.56	0.79

3. Discussion

This study aimed to ascertain whether the type of employed orthodontic appliance and the presence of malocclusion might influence the masticatory efficiency of orthodontic patients with CD compared to healthy controls. It also aimed to see whether there is a difference between orthodontic patients with and without CD. High masticatory efficiency implies that the food can be ground to a higher number and smaller particle size, with less effort, positively affecting quality of life [27].

This is the first study using the MEI to summarize the obtained values of particle number and area of the masticated food samples. The statistical evaluation and subsequent interpretation of these two aspects were found to be challenging in the study by Schmidt et al. [35]. This term was introduced to enhance the ease of evaluating results, as well as to improve their feasibility and comparability. Despite the integration of this new evaluation tool, both studies demonstrated a similar masticatory efficiency. In Schmidt's study [34], the masticatory ability was also decreased in CD patients, showing a significantly higher particle area. Nonetheless, concluding the results of both studies they revealed still a knowledge gap and further the arrival of new, more complicated findings in patients with CD compared to healthy ones. This may lead to future research.

Concerning the effect of age on mastication, the MEI of younger orthodontic patients with CD showed a significantly decreased masticatory ability compared to those without, which is in contrast to Schmidt et al., where differences were significant only for older CD subjects [35]. Thus, it can be assumed that by merging both parameters into one index, the significance of one parameter does not influence that of the index overall. Nonetheless, both studies showed that at the beginning of orthodontic treatment, younger CD patients have a decreased masticatory efficiency than those without CD. As treatment progresses, the mastication difference between orthodontic patients with and without a CD becomes non-significant, suggesting that patients with CD are catching up with their masticatory ability, as already shown by Schmidt et al. [35]. Thus, the first null hypothesis can at least in part be confirmed.

Both patient groups had a better masticatory ability with fixed orthodontic appliances, but as this difference was not significant, the second null hypothesis cannot be confirmed. Regarding further alignment of the dental arches with fixed appliances provides a higher number and area of occlusal contact, which benefits the masticatory efficiency [26]. Most studies report on the benefit of masticatory efficiency after, not during, orthodontic treatment, so there is little data on this issue [36]. Studies suggest that the improved masticatory efficiency just reflects general development and thus, the dental maturation in growing individuals is independent of the employed orthodontic treatment [17,33,35,37]. This goes in line with the results of this study. Thus, concluding that over the orthodontic treatment period, the rehabilitation process is beneficial for patients with CD, who get used to the orthodontic appliances and know how to include them in everyday life.

The presence of a crossbite malocclusion reduced the masticatory efficiency the most in both groups, particularly in patients with CD. Thus, the third null hypothesis was accepted. In a study by Cassi et al. the masticatory pattern of CL/P with crossbite was compared to a sex-matched control group without crossbite (n = 18, mean age 7 years); finding that no statistically significant difference existed between both, which does not go in line with the current study [38]. Besides, the study of Cassi et al. showed that CL/P patients had an irregular masticatory function with increased reverse chewing cycles on the crossbite side [38]. Others found that children with CL/P (n = 50, mean age 21 years) also had a class I occlusion [39], but their masseter muscle activity remained unaffected, and the temporal muscle had an increased EMG potential with unilateral posterior crossbites. These outcomes could explain that CD patients with a skeletal class III configuration showed the best chewing results. Especially patients with CL/P can compensate for this through higher muscle activity and different movement patterns. This compensation could describe the already mentioned improvement in mastication in older CD patients. In growing patients, this could involve a structural adaptation of the whole stomatologic system, potentially resulting in a comprehensive pathological masticatory process and having a negative impact on quality of life [40,41].

The relationship between malocclusion and masticatory function is yet unclear. Corruccini suggested that the occurrence of malocclusions results from an insufficient growth of the jaws due to an insufficiently hard diet which provides too little incentive to chew food properly [42]. Experimental studies suggest that both dietary consistency and masticatory activity influence the masticatory muscles [[43], [44], [45]], aspects of bone growth [43,44,46], and craniofacial morphology [[47], [48], [49], [50], [51], [52], [53], [54], [55], [56]]. After the introduction of the functional matrix hypothesis, it was understood that bone growth occurs as an adaptation to functional stimuli [57], such as in the process of mastication [58]. This means that organisms can adapt to an external influence, known as phenotypic plasticity, to increasing their chances of survival [58], with malocclusion being a physiological condition originating from the environment or functional stimuli early after birth. In the present study (Table 1), the occurrence of malocclusion was more prominent in the CD group, affected by the extension of the cleft, endogenous teeth, and surgical procedures. Feeding is especially challenging for patients with CD, while breastfeeding is hardly possible. The latter is known to play an important functional role in the development of the oral cavity [59]. These early functional imbalances and defects in anatomical structures might pose negative effects on the development of the masticatory process. Rhythmic movements like mastication are mostly (pre-)programmed in the brain but are continuously updated by new experiences, as well as resulting protective reflexes [60]. Thus, negative oral experiences and the cleft defect might further alter this mastication pattern. In this scenario, early logopedic intervention and adhesion to routine logopedic training, as well as the use of a drinking plate for the proper placement of the tongue for feeding, are paramount. Not only is speech therapy necessary to address speech difficulties [65–69] but also to correct and retrain the associated abnormal myofunctional patterns, as well as to improve orofacial muscles to create normal occlusal relationships, proper mastication patterns and to make the patient more confident with these processes [61,62]. Ultimately, speech therapy should address the disadvantages imposed by the CD in early life, improving the overall oral health and mastication efficiency.

Several limitations merit attention. Firstly, challenges arose due to the limited prevalence of CD and specific inclusion criteria for orthodontic treatment, resulting in constraints on the sample size. This limitation necessitated the use of descriptive statistics rather than more robust analyses in certain cases. While acknowledging the potential benefits of a larger sample size for increased statistical robustness, the rarity of the condition presented challenges in achieving this goal. The inclusion of a broader age range, influenced by the rarity of these conditions, may have introduced bias, especially considering the immature fine motor control in young children with primary dentition, evolving with permanent dentition [64]. Despite the limited prevalence, this study boasts one of the largest sample sizes yet reported for masticatory efficiency in studies on CD patients [35]. Additionally, all participants underwent consistent treatment approaches, minimizing potential statistical biases.

Another limitation lies in orthodontic treatment's known to reduce masticatory ability, potentially causing discomfort during chewing [35,63]. This factor could have adversely affected the masticatory efficiency results in the control group. For a more meaningful comparison, future studies should exclusively involve healthy participants without orthodontic treatment. Moreover, the study had a relatively broad age range. Finally, the disruption caused by the COVID-19 pandemic affected appointment regularity and participant recruitment, leading to a reduced sample size in the current study.

Considering the absence of similar studies evaluating masticatory efficiency in patients with CD while considering the impact of an orthodontic appliance and malocclusion, and in light of the limitations and findings of Schmidt et al. [35], there is a compelling need for future research. Such studies should include a third group of patients without orthodontic treatment needs, broaden the participant sample, and adopt a longitudinal design. The implementation of the MEI proved valuable in comparing diverse patient samples, consolidating masticatory efficiency into a single parameter that enhances both comparability and result interpretation. Consequently, the present study advocates for the continued use of MEI in future research.

3.1. Conclusion

Within the limitations of this study, the following can be concluded.

• •Younger orthodontic CD patients have a significantly decreased masticatory efficiency compared to patients without CD.
• •As the treatment progresses with fixed appliances, the mastication difference becomes not significant, which could be an indicator of patients with CD catching up with the masticatory ability of healthy orthodontic patients and suggesting a positive effect from their rehabilitation therapy.
• •Crossbite malocclusion decreases masticatory efficiency and affects the development of the stomatological system negatively in both groups, particularly in CD.
• •The newly introduced MEI, implemented as a standardized tool, proved beneficial for masticatory data evaluation, facilitating enhanced data exchange and comparisons across research.

The results highlighted a knowledge gap in the current literature regarding the masticatory efficiency of patients with CD, emphasizing the importance of future research to capitalize on opportunities for advancement. The early malocclusion recognition and treatment are of great importance for the rehabilitation of these patients. For that, functional orthodontic approaches should be considered in combination with intensive speech therapy to address malocclusions, given that the latter are caused by a deficit growth and an imbalance of the facial muscles.

4. Materials and methods

As the present study is a follow-up to that of Schmidt et al. [35], the same methods were employed, but now with a focus on masticatory efficiency evaluation influenced by malocclusion and orthodontic treatment. It was approved by the institutional ethics committee of Tübingen University Hospital (approval number: 188/2019BO1) in accordance with the Declaration of Helsinki. In addition, written and informed consent was obtained from all subjects and/or their legal guardians, who were informed about the nature of the study and invited to participate with their child during routine follow-up visits. All research was performed by relevant guidelines and regulations.

4.1. Participants

These have already been described in detail in a previous study [35]. In short, subjects aged 7–21 years were divided into a CD and a healthy control group, with a further age-based division into 7–12 and 13–21 years being chosen because permanent dentition is completed by that age and an age-related change in mastication can be expected [64].

4.2. Standardized food model test

Evaluations were performed using the automated food model test Occlusal Systems CHEW (Orehab minds GmbH, Stuttgart, Germany), following the methodology proposed by Slavicek et al. [65]. Test food samples comprise of eatable gelatins (Gelatin SPM 5765, Biogel AG, Luzern, Switzerland) that were prepared in three different hardness grades by modifying the gelatin:water ratio and distinguished by diverse colors (green as soft = 15.5 g/mass, yellow as medium = 23 g/mass, red as hard = 31 g/mass). These aimed to stimulate the mass of conventional food, while being identically shaped (cylindrical ø = 2 cm, h = 1 cm) and flavored.

A standard procedure was employed to gather the data, so that participants masticated the test samples in as many parts as possible while avoiding swallowing. Different chewing cycle variations were considered, where sample hardness (only hard, only medium, only soft) and chewing protocol (only right side, only left side, bilaterally only) were modified. In this way, all patients underwent nine cycles, each lasting 30 s. Masticated food was gathered into a sieve, rinsed with cold water and distributed on the test plate. The nine test plates were positioned within the standardized photographic unit (CHEW Box) to capture essential images. These images were then submitted for evaluation by DRS CHEW (Digital Reporting Services), an internet server-based program developed by Orehab Minds GmbH (Stuttgart, Germany). Not offered as a stand-alone version to the public, this program oversees the image recognition process. Through this system, both particle count (n) and particle area (mm²) are automatically computed, and the results are subsequently integrated into a comprehensive output report.

For the general masticatory efficiency results, all nine chewing cycles were considered. A high masticatory efficiency is denoted as that containing a high particle number alongside a small area. Given that the term is expressed by two different factors, i.e. particle number and area, for comparison purposes an index called Masticatory Efficiency Index (MEI) was implemented, which was defined as $MEI\left(\frac{n}{{mm}^2}\right)=\frac{PN}{A}$, with PN being the particle number and A the area. In this way, higher MEI denoted higher masticatory efficiency.

4.3. Skeletal and dental malocclusion

The intraoral picture of the dental malocclusion in both sagittal and transversal dimensions was assessed chairside during the examinations of this study. The sagittal relationship of the permanent first molar on the left and right side was evaluated using the classification of E.H. Angle [66], where a class I occlusion is defined as the mesiobuccal cusp of the maxillary first molar aligning with the buccal groove of the mandibular first permanent molar. Additionally, the transversal relationship of the anterior and posterior teeth was examined to asses crossbite. For the skeletal malocclusion, lateral cephalometric radiographs were taken from the clinical record to determine the severity of the malocclusion, as these show the skeletal sagittal relationship of the jaws about the skull base. These were analyzed according to the Hasund method [67]. Ultimately, the attendance of patients to speech therapy was recorded.

4.4. Statistical analyses

Patient data were pseudonymized upon collection from the clinical records. Statistical evaluation and descriptive statistics were carried out using JMP (Version 15.2.0, SAS Institute Inc., Cary, USA). Descriptive statistics included the mean and standard deviation (SD) of each sample. In the case of non-normal distribution, Kruskal-Wallis and Wilcoxon tests were performed (α = 0.05). A p-value <0.05 was considered statistically significant.

5. Ethics statement

This study was reviewed and approved by the institutional ethics committee of Tübingen University Hospital, with the approval number: 188/2019BO1. All participants or their legal guardians provided informed consent to participate in the study.

Data availability statement

Data will be made available on reasonable request. Therefore, please contact the corresponding author: christina.weismann@med.uni-tuebingen.de.

CRediT authorship contribution statement

Christina Weismann: Writing – original draft, Visualization, Supervision, Methodology, Investigation, Formal analysis, Data curation, Conceptualization. Maria Schmidt: Writing – review & editing, Visualization, Investigation, Formal analysis, Data curation. Josephine Effert: Writing – review & editing, Validation, Investigation, Data curation. Gregor Slavicek: Writing – review & editing, Project administration, Methodology, Formal analysis, Conceptualization. Florian Slavicek: Software, Methodology, Formal analysis, Conceptualization. Matthias C. Schulz: Writing – review & editing, Validation, Supervision. Christian F. Poets: Writing – review & editing, Visualization, Validation, Supervision, Data curation. Bernd Koos: Writing – review & editing, Supervision, Resources, Project administration, Conceptualization. Maite Aretxabaleta: Writing – original draft, Visualization, Supervision, Project administration, Investigation, Formal analysis, Data curation, Conceptualization.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.