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Development of the Upper Lip

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Development of the Upper Lip ORIGINAL ARTICLE Development of the Upper Lip Craig W. Senders, MD; Erik C. Peterson; Andrew G. Hendrickx, PhD; Mark A. Cukierski, PhD Objectives: To affirm and reanalyze George L. Streeter’s sal, medial nasal, and maxillary prominences form the “merging theory” of upper-lip development in primates by nose. There is fusion of the maxillary prominence with observing progressive embryologic stages in facial devel- the medial nasal prominence. This fusion has not been opment using scanning electron microscopy (SEM) and to previously described. This has resulted in a modifica- further understand upper-lip development. tion of the current theory of upper-lip development into one we refer to as the “dynamic fusion theory.” Design: The study was conducted at the California Re- gional Primate Research Center, Davis. Twenty primate em- Conclusions: The dynamic fusion theory explains the bryos (Macaca fascicularis) and 2 fetuses were examined merging process of the mesenchymal and ecotodermal with SEM. The development of the frontonasal promi- layers of the facial prominences that contribute to the up- nence, maxillary prominence, medial nasal prominence, and per-lip formation. The dynamic fusion theory of facial lateral nasal prominence were sequentially observed. The prominence movement details the interaction between contribution of these prominences to the formation of the epithelial layers: both epithelial layers must fuse prop- upper lip and nose were carefully analyzed. erly to avoid cleft-lip deformities. Results: The maxillary prominence and medial nasal prominence form the upper lip, whereas the lateral na- Arch Facial Plast Surg. 2003;5:16-25 UR QUEST for knowledge created 3-dimensional reconstructions by and understanding has a best-fit method. His 3-dimensional re- led to an exploration of constructions of the face are remarkable, the embryologic develop- especially when one considers that his ment of the upper lip. The work was done without the assistance of Olate Franklin P. Mall ignited the flame by computer-aided digital analysis. founding the department of embryology at Our work used scanning electron mi- the Carnegie Institution of Washington, croscopy (SEM), which has the advantage Washington, DC, which today contains one of allowing a full analysis of facial develop- of the most well-respected human em- ment at greater resolution of surface struc- bryo collections. He bequeathed the col- tures. A primate model was used because lection to the late George L. Streeter, MD, of the lack of human embryonic tissue. All who devoted his life to studying the devel- embryos were used in multiple research opment of the embryo.1 It is the great work projects. Although Streeter’s work is re- of Streeter, who discovered and devel- markable, SEM analyses were used to con- oped many of the insights into embryo- firm and alter certain aspects of his work. logic staging and development, that stands as the foundation for many of today’s in- METHODS quiries. Facial development has always been difficult to study because of the translu- Adult female cynomolgus monkeys (Macaca fas- cency of the embryo and limited visualiza- cicularis) were housed individually in alumi- tion caused by the head-flexed position of num cages at the California Regional Primate Re- search Center, Davis, and maintained in embryos. accordance with standards established by the From the University of Streeter explored new techniques to Federal Animal Welfare Act and the Institute for 1 California, Davis. Dr Cukierski overcome obstacles. He studied embry- Laboratory Animal Resources. Animal rooms is now with Merck Research onic histologic sections and used these were maintained on a 12-hour light-dark cycle Laboratories, West Point, Pa. sections as a framework. Streeter hand- (lighted from 7 AM to 7 PM) with a year-round (REPRINTED) ARCH FACIAL PLAST SURG/ VOL 5, JAN/FEB 2003 WWW.ARCHFACIAL.COM 16 ©2003 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 temperature of approximately 22°C and 60% relative humidity. Monkeys were fed twice daily with Purina Monkey Chow (15% Table 1. Catalog of the Embryos Analyzed protein) (Ralston Purina Company, St Louis, Mo), and water was According to Stage Distribution, Estimated Age, provided ad libitum by automatic Lixit devices (Lixit Animal Care and Crown-to-Rump Lengths Products, Napa, Calif). Menstruation was detected by visual ex- amination of the external genitalia or by detection of blood on a Stage Estimated Age, d Crown-to-Rump Length, mm cotton tip swab after insertion into the vaginal canal. Females were 12 28 6 mated by natural insemination by housing with a single fertile 13 26 7 male for approximately 2 hours every other day over a 5-day pe- 14 29 7 riod at midcycle. The middle of the mating period was desig- 16 31 10 nated as day 0 of pregnancy. Pregnancy was confirmed by posi- 16 35 9 tive radioreceptor assay tests for chorionic gonadotropin in serum.2 16 32 10 16 31 10 Embryos were removed by hysterotomy, placed in phosphate- 16 32 11 buffered saline, and dissected free of the placenta and develop- 17 37 12 mental adnexa. The embryos were fixed by immersion in 2% glu- 17 33 13 taraldehyde, 2% paraformaldehyde in 0.1M cacodylate, or 17 32 12 phosphate buffer at pH 7.3 and then measured and photo- 17 36 12 graphed intact. The Carnegie system for staging human em- 18 38 16 1 18 35 16 bryos was used to stage the embryos externally, and subsequent 21 40 20 histologic analysis of several internal organs was used for con- 20 39 20 firming of stage.3 The fixed heads were removed using a razor 20 39 21 blade and stored in refrigerated buffer until processing. Other in- 21 41 19 vestigators used other tissues. The tissues were dehydrated in 21 42 19 graded series of ethanol and critical-point dried using liquid car- 23 46 26 Fetus 52 33 bon dioxide as a transition fluid. The dried specimens were Fetus 52 Unmeasurable mounted on stubs with double-stick tape or conducting silver paint and coated with palladium gold in a Denton Vacuum evaporator (Moorestown, NJ) or sputter-coated with gold in a Polaron E51 coater (Ladd/Polaron, Williston, Vt). The specimens were exam- tral surface of the stomodeum, which is still dispropor- ined in an ETEC Autoscan U-1 (Applied Materials, Santa Clara, tionate to the size of the corpus but has become smaller Calif) or an ISA SS60 (ISA Inc, Louisville, Ky) scanning electron with the merging of the mandibular prominences. microscope. After photographing the heads intact, we made fur- ther dissections (using microdissecting knives) on the dried speci- EARLY STAGE 16 mens. The heads were then recoated and examined as above. A total of 22 specimens ranging from stage 12 to fetus were exam- A major advance in stage 16 (Figure 3) is the appear- ined (staged according to Hendrickx,4 O’Rahilly,5 and Wilson 6 ance of the nasal pits, which appear to end blindly and are et al )(Table 1). located more medially than their precursors, the nasal plac- odes. The nasal pits begin as rounded spheres and de- RESULTS velop into “comma” shapes, pointing slightly laterally by late stage 16. The maxillary prominence is well devel- STAGE 12 oped, much like the lateral and medial nasal promi- nences. As the maxillary prominence develops toward the Figure 1 shows the 3 prominences of stage 12, the fron- median plane, the caudal portion of the frontonasal groove tonasal, maxillary, and mandibular (see Table 2). The starts to move cranially. The lateral and medial nasal promi- frontonasal prominence forms the forehead and the ros- nences are well developed and easily distinquished cau- tral boundary of the stomodeum (primitive mouth). The dally, but the separation is ill-defined cranially. The me- mandibular prominence forms the caudal boundary of the dial nasal and maxillary prominences merging caudally primitive mouth. The maxillary prominence is ventral to form the paired labial furrows, which are located lateral the developing eye. The mandibular arch has a median to the frontonasal groove along the upper lip. The man- groove (mandibular groove), which separates the devel- dibular groove remains prominent. Lingual swellings are oping branchial arches. The nasal placodes are barely dis- very evident just lateral to the mandibular groove. The me- cernible. The mandible is separated by the stomodeum, dian mandibular groove continues to become shallower. which is disproportionate to the size of the corpus. The nasolacrimal groove is very distinct. The lateral and medial nasal prominences and the maxillary prominence STAGES 13 AND 14 are merging at the nasal sill. The lateral and medial nasal prominences form the nasal sill, whereas the maxillary The nasal placodes have become more pronounced in prominence supports the nasal sill caudally. The stomo- stages 13 and 14 (Figure 2) and have moved slightly deum is still elongated across the corpus but is achieving medially from their stage-12 positions. The maxillary na- a more distinct shape with medial movement of the max- sal prominence and lateral nasal prominence have be- illary prominences. come visible and are positioned more medially. The max- illary prominence is more distinct. The nasolacrimal LATE STAGE 16 groove is visible separating the maxillary and the lateral nasal prominences. The mandibular groove has become Small bridges of epithelial tissue span the nasal sill re- shallower. The frontonasal groove is located on the ven- gion between the lateral and medial nasal maxillary promi- (REPRINTED) ARCH FACIAL PLAST SURG/ VOL 5, JAN/FEB 2003 WWW.ARCHFACIAL.COM 17 ©2003 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/26/2021 A B Figure 1. Scanning electron microscopic views of stage 12 Macaca fascicularis embryo.
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