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Subjects with colour vision deficiency in the community: what do primary care physicians need to know?

Subjects with colour vision deficiency in the community: what do primary care physicians need to... Background: Congenital colour vision deficiency (CVD) has a prevalence of 8% for men and 0.4% for women. Amongst people born with normal colour vision, the acquired form of CVD can also affect them at later stages of their lives due to disease or exposure to toxin. Most CVD persons have difficulties dealing with colours in everyday life and at work, but these problems are under-reported due to a lack of its awareness in the general population. This literature review seeks to present findings of studies and reports on the impact of CVD on the affected persons chronologically through different stages of their lives and their coping measures. Methods: Scientific publications and corresponding references relating to how CVD affects individuals were searched, identified and retrieved from PubMed, National University of Singapore and Cochrane electronic databases. Books that were not available electronically were manually searched. Paramedical literature was also included through online searches using Google and Google Scholar. Inclusion criteria were English-based studies pertaining to effects of CVD on everyday life and respective coping measures, including experimental, observational studies, symposium proceedings and systematic review. There was no timeframe restriction for these publications. Articles using anecdotal evidence were excluded with the exception of those used to describe the effects of CVD on play age and school age. Our literature search found 136 articles, 60 of which were used in this review based on the respective selection criteria. Results: CVD affects many aspects of life from childhood to adulthood. The implications extend across play, sports, driving, education, occupation, discrimination, and health and safety issues. Awareness of CVD helps to identify and develop corresponding coping strategies. Conclusions: More work needs to be done in raising awareness of CVD and its implications, as well as implementing measures to overcome these difficulties. Keywords: Colour vision deficiency, Activities of daily living, Coping measures Background cones is abnormal – protanomaly involves reduced sensi- Individuals with normal colour vision (NCV) have three tivity to red, deuteranomaly involves reduced sensitivity to types of specialised cells, known as cones, in their retina to green and tritanomaly involves reduced sensitivity to blue. help them to perceive red, green and blue colours. People Dichromacy occurs when a person only has two retinal with abnormal cones will perceive colours differently. There cones that are able to perceive colour, resulting in the total are several types of such colour vision deficiency (CVD). absence of one colour. There are three types of dichro- Anomalous trichromacy occurs when one of the three macy – protanopia, deuteranopia, and tritanopia. Congenital CVD has a prevalence of 8% for men and 0.4% for women [1]. In Singapore, a study done on 1249 * Correspondence: tan.ngiap.chuan@singhealth.com.sg Research Department, SingHealth Polyclinics Head Office, 167 Jalan Bukit children aged 13–15 years using the Ishihara 24-plate Merah, Connection One Tower 5, #15-10, Singapore 150167, Singapore 3 edition book found 5.3% of boys and 0.2% of girls to be DUKE-NUS Graduate Medical School, 8 College Rd, Singapore 169857, colour blind [2]. All people with CVD, except for a few Singapore Full list of author information is available at the end of the article © 2014 Chan et al. ; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 2 of 10 http://www.apfmj.com/content/13/1/10 mildly affected deuteranomals, report that they encoun- timeframe indicated as some studies done on CVD de- ter problems with colour perception in everyday life and cades ago have implications that remain pertinent today. at work [3]. Yet, there have been few studies systematic- The exclusion criteria used were non-English articles ally documenting the personal difficulties that CVD per- and non-human studies. Articles using anecdotal evi- sons experience in their daily lives [4]. There seems to dence were also excluded with the exception of those be a lack of awareness for the implications of CVD in used to describe the effects of CVD on play age and the general population [1,5]. Furthermore, CVD can de- school age due to the paucity of primary sources of evi- velop later in life due to development of disease or ex- dence for these stages of life. Eligibility assessment was posure to toxins such as chemicals or drugs which affect performed by two unblinded reviewers. Disagreements the retinal cellular structure and function [6-9]. Known between reviewers were resolved by consensus. as acquired colour vision impairment (ACVI), the preva- The literature search on electronic databases provided lence of CVD, inclusive of both the congenital and ac- a total of 118 citations. Additional 18 records were iden- quired forms, is expected to increase globally with the tified through hand searches, reference lists and search increasing population. Therefore, this article presents a engines on the World Wide Web. After adjusting for du- review of current literature, comprising scientific studies plicates, 124 remained. Of these, 52 were excluded as and paramedical reports of the effects of CVD on indi- they were not within the scope of the review, their full viduals through their different stages of life. This would text was not available or not translated into English. The better help those afflicted with CVD to identify the do- full texts of the remaining 72 citations were examined in mains of difficulties in daily living and to determine pos- detail. It appeared that 12 did not meet the inclusion cri- sible strategies to cope with their predicaments. teria as they were not relevant to the topics of discussion. Eventually, 60 records met the inclusion and exclusion cri- Methods teria and were used in this review. Of these 60, 46 were Data sources identified via electronic databases while 14 were identified Studies on how CVD affects well-being were identified from alternative sources as mentioned earlier. The selec- from multiple sources. The following electronic data- tion of studies is summarised in Figure 1 below. bases were searched: PubMed database, National Univer- Each article was evaluated using the PICOS framework sity of Singapore (NUS) database and Cochrane database (population, interventions, comparator, outcome and of systematic reviews. Search terms included ‘colour vi- study design). sion deficiency’, ‘colour vision impairment’, ‘colour blind- ness’, ‘well-being’, ‘quality of life’, ‘everyday life’, ‘everyday Limitations tasks’, ‘discrimination’, ‘handicap’, ‘education’, ‘driving’, ‘acci- No review protocol was used hence there may be bias dents’, ‘occupation’, ‘aviation’, ‘maps’. The last search was incurred in review methods in the post hoc decisions. performed on 22 May 2013. The references within the Publication bias and outcome reporting bias have been retrieved articles found were also searched. Additionally, well documented and may overestimate the effects of electronic journals in the field of CVD that were avail- CVD in the included studies [10,11]. able online were searched. Books that were not available electronically were hand searched for relevant studies. Results We also used the proceedings of the eleventh and thir- The impact of CVD on affected persons will be pre- teenth Symposiums of the International Research Group sented chronologically from childhood at play and in on Colour Vision Deficiencies, held in Sydney (1991) schools, young adulthood, working life to late adulthood. and France (1995) respectively. Paramedical literature Figure 2 summarises the impact of CVD on affected in- was included through online searches on the World dividuals at different stages of their life. Wide Web, using search engines such as Google and Google Scholar. All literature found was added to End- Play age Note X6 digital library. A child engages play and learning during childhood. They are often exposed to colourful objects such as toys Study selection and accessories during these activities. A child with deu- Inclusion criteria were articles available in English lan- teranomaly, the commonest form of colour-blindness, will guage, studies pertaining to effects of CVD on everyday be able to accurately name only four colours within a box life and specific populations (for example, pilots). These of 24 coloured pencils. Nevertheless, they will probably be publications consist of experimental, observational stud- able to guess more [12]. Consequently, parents of CVD ies, symposium proceedings and systemic review. No re- children often reported that their children were mis- strictions on the years of study/follow-up, publication taken as slow learners or ridiculed in preschool for mixing status or publication date were imposed. There was no colours up and colouring objects wrongly [13,14]. Such Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 3 of 10 http://www.apfmj.com/content/13/1/10 Records were identified through Additional records were identified database searching (n = 118) through other sources (n = 18) 12 duplicate records were removed . (n = 12) Records were screened. Records were excluded. (n = 124) (n = 52) Full-text articles were Full-text articles were assessed for eligibility excluded, with reasons (n = 72) (n = 12) Studies were included in qualitative synthesis (n = 60) Figure 1 Flow diagram of study selection. Figure 2 Summary of activities that can be affected by CVD across various stages of life. Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 4 of 10 http://www.apfmj.com/content/13/1/10 Table 1 Common difficulties faced by CVD students in mistakes may cause embarrassment to the child and lead academic subjects to significant consequences such as school refusal or social Subject Areas of difficulties withdrawal. Other learning difficulties include inability to accurately Art Unable to appreciate how colours are used describe things around them, failure to follow instructions Use of wrong colours when painting relating to colour and to read coloured printing against a Chemistry Unable to read litmus paper accurately coloured background [12]. This will translate into prac- Unable to tell the colours of different chemical solutions in tical problems such as difficulty completing workbook quantitative analysis tasks relating to colour, and even cheating in tests because May be unable to identify metals by colour of flame the child is unable to tell the questions written in coloured produced when a metal is burnt ink or chalk on the board [14]. Biology Unable to accurately read stained slides under microscope In Parten’s classification of stages of play, activities May not be able to identify species of plants such as associative and cooperative play, which involves May not be able to accurately carry out dissections interpersonal interactions, are critical stages of social de- May have difficulty understanding coloured diagrams in velopment. However, CVD children may face difficulties textbooks when playing with others because they cannot differenti- Physics Will have difficulty with coloured wiring and use of prisms ate between different teams distinguished by coloured tags, nor recognise coloured pieces in board games [14]. Maths Unable to read pie charts and graphs In the area of personal safety, CVD children may get Data from Dutton F [13], Waggoner TL [14], Sullivan K [15], Albany-Ward K [16], Spalding JAB [17]. lost more easily if given directions using coloured ob- jects as signs [14]. CVD children may also be fussy about eating certain food, for example, vegetables, because they intelligence scores and elementary school achievement perceive these foods in unpalatable colours [12]. The ef- [18]. A literature review conducted in 1992 reported that fect on the choice of food should not be overlooked in a studies attempting to relate CVD to learning difficulty were phase whereby proper nutrition is important for the equivocal in their outcome [19]. A subsequent study in child’s growth. 1998 showed significantly lower general academic scores among 82 children with CVD as compared to 82 children School age with NCV, matched by age and class [20]. In contrast, a Most children with CVD are unaware of their condition, 2004 cohort study on 499 CVD children found that CVD with many only realising so when they are in secondary did not cause significantly lower scores in mathematics school [12]. Steward and Cole in their study showed that and reading at 7 years and 16 years of age respectively, 49% of dichromats and 8% of anomalous trichromats be- even after adjusting for birth-weight, social class at birth, came aware of their CVD in primary school, with a fur- family size, and parental education [21]. Furthermore, the ther 22% of dichromats and 28% of anomalous trichromats highest educational qualification was not significantly asso- in secondary school [4]. They also showed that 71% of di- ciated with colour vision status [21]. Another 2004 ques- chromats and 27% of anomalous trichromats began to sus- tionnaire survey showed no significant difference in the pect having CVD after they encountered difficulties with disciplines studied between NCV and CVD persons, but colour [4]. However, 77% and 94% respectively had a clear CVD interviewees tended towards technical studies (30%, diagnosis of CVD only after formal colour vision testing as opposed to 18% of NCV subjects), and less of them [4]. Upon diagnosis, they often retrospectively recall the undertook tertiary education in university (68.9%, as op- difficulties they faced with discriminating colours in earlier posed to 79.9% of NCV subjects) [22]. life [4]. CVD-related difficulties during the schooling years are CVD students struggle in a variety of subjects, espe- common and are observed in a variety of sports. In an cially the sciences. Sullivan (2011) noted that CVD chil- Australian study on 102 CVD subjects, one in four re- dren tend to lag behind in many subjects where colour ported difficulties with sporting activities [4]. Confusion is used as a teaching tool, including mathematics, sci- arises due to inability of CVD players to differentiate their ence, geography, reading, sport and food technology team members from the opponents wearing coloured uni- [12]. The common difficulties faced by CVD students in forms. Theformeralsotendto loseorangegolf balls in the academic subjects are summarised in Table 1 [13-17]. grass, and mistake red for brown snooker balls [4,12,23]. Nonetheless, studies which aimed to determine the impact of CVD on academic achievement showed con- Young adulthood during military service flicting outcomes, possibly due to differences in study Colour vision is involved in a variety of military activities designs. A 1969 case control study showed no signifi- and training. Certain vocations in the air-force, navy and cance difference between NCV and CVD children in infantry require normal colour vision [23,24]. Those Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 5 of 10 http://www.apfmj.com/content/13/1/10 commonly affected are military personnel in the aviation appears the same to a CVD user as it does to one with and maritime divisions of the defence force. NCV [32]. Although map reading among CVD users has In aviation, a Farnsworth lantern test is routinely used not been studied extensively, it was found that readers with to screen colour vision and involves identification of a CVD made more errors naming the boundary lines on pair of lights consisting of combinations of red, green or multi-coloured terrain maps [33]. Another study showed white. The Precision Approach Path Indicator (PAPI) that only a small percentage of CVD readers could name signal system tells pilots whether their aircraft is above, the colours of a weather radar display without error [34]. below, or on the correct approach path for landing. It CVD persons are slower and less successful in search tasks, displays four signal lights that can be red or white. A when colour is the primary attribute of the target object, or case–control study was performed on 52 CVD subjects if colour is used to organize visual displays [3,35]. and 52 subjects with NCV in 2008: amongst CVD sub- jects who passed the Farnsworth lantern, they made sig- Middle to late adulthood nificantly more errors naming PAPI signals than NCV Activities of daily living subjects and 80% of them made more errors than the Nearly 90% of dichromats and up to two-thirds of anom- worst performing NCV subject [25]. Another study showed alous trichromats reported difficulties with everyday tasks that CVD observers made significantly more errors and that involve colour [4]. Tables 2 and 3 show the difficulties were slower in completing tasks requiring processing of reported by persons with CVD, and the difficulties sub- colour coded electronic flight information [26]. analysed within each subtype of CVD [4,22]. The Holmes–Wright lantern type A (H-W A) is an oc- Even amongst NCV individuals during the early part of cupational colour vision test used by the UK Civil Aviation life, they can develop CVD as they age. Acquired CVD or Authority (CAA) and approved by Joint Aviation Require- ACVI can occur due to age-related crystalline changes in ments (JAR) to select aircrew. The Commission Inter- lens, age-related maculopathy and conditions such as dia- nationale d’Eclairage (CIE) recommends that the Falant betes, glaucoma and optic neuritis. They can also be pass criteria be used with all approved lanterns. However, a caused by medications such as digoxin, sildenafil, chloro- 2008 study showed that this investigation and selection cri- quine and ethambutol. ACVI are often tritan (blue-yellow) teriausedbythe UK CAA andCIE do notidentifyindivid- in nature. Tritan defects cannot be detected using the uals with superior colour discrimination ability and lack Ishihara chart. Instead, the Hardy, Rand and Rittler plates internal consistency [27]. There is thus no evidence to sug- may be more useful as tritan plates are also included and gest that successful CVD applicants have significantly bet- the severity of the defects can be graded [6]. Alternatively, ter colour discrimination ability than CVD people who fail. the Farnsworth D15 test may be used [6]. The selection process is therefore potentially unfair to CVD persons applying for aviation positions. Driving and accidents In navy, CVD persons have difficulty recognising red- Safe driving requires the driver to recognise colour-coded green-white maritime signals. The Holmes-Wright Type traffic lights and road signage. A case control study B lantern is the standard colour vision test used by the showed that both CVD and NCV subjects who were quali- Board of Trade in maritime industry [28]. A 1983 study fied to drive were in similar proportions (83.4% and 83.8% that validated the Holmes-Wright Type B lantern test as Table 2 Difficulties in everyday life reported by 151 CVD a discriminating test showed that all CVD persons failed, subjects and 302 NCV subjects except for a few mild deuteranomals [28]. This correlates Difficulties associated with % of CVD % of NCV Significance with other studies which also showed that all CVD per- observers observers (p value) sons, except for a few mild deuteranomals, make errors Clothing colours 23.8 1.0 <0.0001 recognising maritime signals [29,30]. Furthermore, the Workplace/hobbies colours eg. 13.2 1.0 <0.0001 rate of errors increases with decreasing signal illumin- pie charts ance [29,30]. Both protanopes and protanomals have sig- Natural colours 40.4 1.0 <0.0001 nificantly reduced visual range for red signals [29,31]. Colours relating to cooking s eg. 31.7 8.6 <0.0001 Kinney, Paulson and Beare showed that only 40% of deu- Identification of cooked versus tans and 14% of protans performed as well as their raw meat worse performing NCV subjects [29]. It is largely ac- Sports colours eg. shirts of 21.2 1.3 <0.0001 cepted that normal colour vision is essential for safe players maritime navigation. Skin colours 3.3 1.7 0.0007 Inherited CVD is marked by a difficulty in discerning red Television colours setting 6.0 0.7 0.0002 from green, while acquired CVD leads to decreased ability Data from Tagarelli et al. [22] (Statistical significance of differences were to distinguish blue from green. CVD persons struggle with calculated using the chi-square test or Fisher exact test, two-tailed significance reading coloured maps, although a monochromatic map level 0.05). Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 6 of 10 http://www.apfmj.com/content/13/1/10 Table 3 Percentage of subjects with different types of CVD reporting difficulty in everyday tasks Difficulties associated with Dichromats (%) Anomalous trichromats (%) Protans (%) Deutans (%) NCV (%) (n = 37) (n = 65) (n = 36) (n = 66) (n = 102) Clothing/goods colours 86 66 78 71 0 Workplace/hobbies colours 68 23 50 33 0 Plant/flower identification 57 18 44 26 0 Ripeness of fruits and vegetables 41 22 31 27 0 Cooked versus raw meat 35 17 33 20 0 Sports colours 32 18 19 23 0 Adjust television colour settings 27 18 28 18 2 Skin colours eg. sunburn, rashes 27 11 17 17 0 Previously taken wrong medication due to colour 03 3 1 0 difficulties Data from Steward and Cole [4]. respectively) [22]. However, regular use of a car was sig- In terms of accident rates, studies reported that CVD nificantly less common among CVD subjects than NCV drivers did not have more road traffic accidents than subjects [22]. NCV drivers [21,22,36,42]. However, protans showed Reading road traffic signals tend to be less difficult for significantly more rear end collisions and accidents by CVD observers compared to maritime, aviation and rail overlooking red rear, stop and warning lights than colour signals because the former is viewed from much shorter normal [36]. Rear end collisions seemed more prevalent distances. Furthermore, they are assisted by cues such as amongst protans because the red lights of the rear end position of traffic lights, relative brightness and move- appeared dimmer to them, resulting in delayed percep- ment of other traffic [3,4,36]. Nevertheless, experimental tion in poorly illuminated areas. Deutans caused more studies have shown that people with CVD make more accidents than NCV drivers at traffic light controlled in- errors recognizing the colours of road traffic signals than tersections, although this was not statistically significant those with normal vision [37,38]. Deuteranopes have sig- [36]. A case control study also showed that there was no nificantly reduced ability to notice red, orange and green increased risk of unintentional workplace injuries amongst colour-coded traffic control devices compared to NCV CVD subjects [21]. subjects [39]. Protans are known to have reduced visual range for red signals compared to NCV observers [36,40]. Restriction of career options and workplace discrimination About 18-20% of anomalous trichromats and 50-60% of Individuals with CVD appeared to have restricted career dichromats admitted to difficulty recognizing road traffic options. A 1971 study found that only 214 out of 569 CVD signals while 10-15% of protans admitted to difficulty see- subjects made suitable choices of career [43]. Table 4 shows ing red signal lights [4,23,41]. careers and occupations known to be affected by CVD Atchison DA et al. showed that response times and error [23,24]. The Commission Internationale de L’Éclairage rec- rates for recognising red and yellow lights were increased ommends that normal colour vision be a prerequisite for in CVD subjects compared to NCV subjects [38]. On the pilots of scheduled passenger aircraft, especially large air- contrary, Tagarelli et al. showed there were no differences craft, and is mandatory for other commercial pilots to pass between the two groups in identifying the colours of traffic a lantern test and should not have a protan (red-deficient) light signals. However, when the relative positions of the colour vision deficiency [44]. traffic lights were changed, more CVD subjects had diffi- According to Birch, coloured signals may be preferred to culty identifying the colours than NCV subjects but the dif- short wavelength radio for communication in the armed ference was not statistically significant [22]. forces because radio signals can be intercepted [23]. Hence, Significantly higher proportion of CVD subjects pre- vocations such as signals personnel and again aircraft pilots ferred daytime driving over night-time driving compared will be unsuitable for individuals with CVD. to NCV subjects [22]. This could be due to difficulty iden- In the railway industry, train drivers and other rail tifying the reflectors on the road and identifying the lights workers must be able to recognize red, yellow and green of the car ahead at night [22]. Confusion of traffic lights signals at distances up to 1 km, sometimes under condi- and street lights was also noted in one-third of CVD tions of poor visibility due to fog or rain. Hovis JK and drivers [4]. The detection of dashboard warning lights Oliphant D reported that 97% of individuals with CVD (which are often red) was significantly more difficult for failed a lantern test (CNLAN) that was found to provide a protans than deutans (17% versus 3% respectively) [4]. reasonable functional assessment of colour discrimination Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 7 of 10 http://www.apfmj.com/content/13/1/10 Table 4 Career and occupations known to apply a colour Even among healthcare professionals, CVD can be dis- vision standard advantageous to doctors and dentists. Difficulties faced NORMAL COLOUR VISION Commercial airline pilots, air traffic by CVD doctors and medical students are summarised controllers, technical and in Table 5 [5,17]. maintenance staff at airports, CVD doctors tend to avoid the following specialties aircraft pilots and engineers in the armed services, naval officers, where normal colour vision is important: histopathology, submarine personnel, masters and microbiology, haematology, dermatology, ophthalmol- watchkeepers on merchant marine ogy, surgery, anaesthesia (uses differently coloured gas vessels, customs and excise officers, train drivers, railway tanks) [17]. A 1990 case control study showed that CVD engineers and maintenance staff; dentists made significantly more errors in the hue and workers in industrial colour quality chroma aspects of shade selection, hence affecting their assurance and colour matching, workers in fine art reproduction ability to select prosthetic teeth to match natural teeth and photography, some electrical [50]. Hue is the quality that distinguishes one family of and electronic engineers colours from another based on their different wave- COLOUR VISION STANDARD Fire fighters, police officers, some lengths in the visible spectrum. Chroma is the satur- APPLIED BUT ACCEPTS SOME WITH electrical and electronic engineers, ation, intensity, or strength of the hue. SLIGHT CVD some ranks in the armed services, hospital laboratory technicians, Nearly one-quarter of CVD subjects reported having merchant seamen colour difficulties in previous jobs, as well as being pre- OCCUPATIONS WHERE CVD IS A Art teaching, bacteriology, botany, cluded from an occupation because of their CVD [4]. DISADVANTAGE AND COLOUR chemistry, interior design, Steward and Cole showed that 43% of dichromats and VISION STANDARD MAY APPLY histopathology, horticulture, geology, diamond grading, 29% of anomalous trichromats reported their CVD had metallurgy affected their choice of career [4]. 46% of dichromats Data from Birch J [23] and Health Promotion Board of Singapore [24]. and 15% of anomalous trichomats also reported colour difficulties with everyday work, and this was statistically significant when compared with NCV subjects [4]. for the rail industry [45]. Vingrys AJ and Cole BL, in their However, a 2004 questionnaire survey revealed that literature review to determine whether colour vision stan- CVD people had little difficulty in maintaining perman- dards were justified for the transport industry, found that ent employment [22]. Nonetheless, they were more likely CVD observers made more errors and had significantly to hold subordinate jobs, for example, as agents, clerks slower reaction times in recognising coloured signal lights or servants, whereas NCV subjects preferred autono- [46]. It concluded that there was sufficient evidence to war- mous activities, such as commercial and trade work [22]. rant retention of colour vision standards in transport in- A subsequent study in 2005 also revealed that there was dustries where the highest standards of safety are expected. no significant difference between proportion of CVD Severe CVD is generally unacceptable in the police force. Conflict of evidence regarding identification of clothing or Table 5 Difficulties faced by CVD doctors and medical vehicles or items using colours at the scene of crime may students interfere with jurisdiction in criminal or forensic cases [23]. No. Difficulties faced by CVD doctors and medical students CVD applicants can be recruited as fire fighters if they 1 Body colour changes: pallor, cyanosis, jaundice pass the Ishihara’s test. Should they fail this colour vision 2 Skin rashes, erythema and lymphangitis test, they would have to undertake the Farnsworth-Munsell 3 Blood and urine test strips Standard D15 test (FMD-15) [47-49]. Protans are not ac- cepted in the fire brigade because of their reduced visibility 4 Ophthalmology: disc pallor, diabetic changes, haemorrhage versus pigmentation, glaucoma, haemorrhage in anterior chamber, Kayser of red signs and traffic signals. In addition, oxygen (black) Fleischer rings and acetylene (maroon) gas cylinders are similar in shape 5 Body products: blood versus bile in urine, faeces, sputum, vomit and might be confused due to this CVD [49]. Other critical 6 Otoscopy: inflamed drum, wax versus blood tasks which require colour discrimination among the fire- fighters include interpretation of computer displays in com- 7 Microscopy munications units, assessment of gas level in gas detectors, 8 Mouth and throat conditions useofindicator papers, identificationof zoneoffireon 9 Ishihara test giving building evacuation and fault indicator panels, deduction of 10 Chemistry end-points the burning substance based on the colour of the smoke 11 Tissue identification in surgery and flames and distinction of hydraulic and pressure hoses, 12 Gangrene and sores fire extinguishers, gas cylinders, pipes, ducts, and triage labels [47]. Data from Spalding [5,17]. Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 8 of 10 http://www.apfmj.com/content/13/1/10 Table 6 Recommendations for colour-coded designs and NCV people in the major occupational groups ex- cept for transport operations, aircraft and ship officers, No. Recommendations for colour-coded designs electrical and electronic engineering, as well as fibre and 1 Avoid specific colours if no redundancy is possible textile processing [51]. 2 Include redundancy, especially lightness difference, whenever possible Health-related activities 3 Segment areas of colour which might otherwise be confused The effect of colour on appetite is important because poor 4 Avoid dark red or green text on a black background growth and malnutrition due to poor oral intake, can 5 Enhance colour conspicuity such as using white or yellow for affect the young and old respectively. Colour perception objects which have to be seen in poor illumination or at night of food can adversely affect the appetite and taste percep- 6 Avoid glare tion of CVD people. A food study in 1978 demonstrated Data from Birch [23]. that addition of red dye to fruit flavoured beverages in- creased the perceived sweetness by 5-10%, while an addition of blue dye to cherry or strawberry flavoured bev- for congenital red-green colour blindness in children and erages decreased sourness and fruit flavour by 20% [52]. should be made routine in schools. Currently, vision Colours are often used to differentiate the different screening in schools in Singapore only includes visual acu- types of oral medications. Steward and Cole reported ity and stereopsis [54-56]. that some CVD subjects in their study had previously Nevertheless, screening for acquired CVD (ACVI) is taken the wrong medications due to difficulties with challenging as they do not follow the well-defined pat- colour [4]. Depending on what medication was taken, terns of congenital CVD and may be difficult to classify the adverse outcomes could range from insignificant to [6,57]. Currently, there is a paucity of primary studies to fatal. Patients who habitually mix their medications evaluate the costs and benefits of mass screening for ac- without the external packaging in the same pill storage quired CVD, although some preliminary studies show compartment would be more prone to such hazards. that doing so may help detect diabetic retinopathy and CVD may also affect the interpretation of coloured primary open angle glaucoma earlier [8,58,59-62]. dipstick results used in healthcare [5,17,53]. A case–con- Once CVD has been detected via screening, measures trol study involving patients who had ACVI due to dia- must be taken to help the afflicted overcome their difficul- betic retinopathy showed that diabetics made significantly ties with colour discrimination.Thisisespeciallyimportant more errors in interpreting urinary glucose dipstick results as 46% of dichromats and 15% of anomalous trichomats than non-diabetic controls [53]. This would make moni- reported colour difficulties with everyday work [4]. Means toring of glycemic control more difficult, although moni- of overcoming occupational colour deficiencies used in- toring is more commonly done via serum glucose today. clude asking others, using instruments, keeping objects of With increasing age and concurrent rising incidence of different colours in separate places and avoiding colour malignancies, detecting and awareness of colour-related tasks [4]. A 2001 study showed that the use of tinted con- signs and symptoms become important for susceptible indi- tact lenses in CVD subjects significantly reduced error viduals. Nonetheless, Spalding (1995) and Spalding (2004) rates on the Ishihara and Farnsworth Munsell D-15 test mentioned difficulties in detecting hemoptysis, hematem- [62]. This may provide some assistance in colour-related esis, hematuria and bloody stools reported by these affected Table 7 Steps for improving the classroom for CVD individuals [5,17]. Detecting these presenting symptoms children early would allow earlier diagnosis and treatment of No. Steps for improving the classroom for CVD children any underlying sinister conditions, such as lung cancer, 1 Label felt tips, paints, pencils etc. upper gastrointestinal bleeds, bladder cancer and colo- 2 Colour-code boxes of toys, art materials and books rectal cancer. 3 Check computer-based teaching aids, web pages, computer settings Discussion 4 Use strong contrast on white or chalkboards. CVD is currently under-diagnosed as there is no struc- tured screening in various parts of the world. Screening 5 Use patterns and labels rather than colours for maps, pie charts, diagrams for CVD is important so that appropriate career advice can be given to these individuals, especially during the 6 In sports and games, ensure that children can see who is on his or her ‘team’ period when they are receiving their education [43]. This 7 Group and label beads, bricks and colouring material according to would require detection of CVD through screening using colour pseudoisochromatic tests, and then determining the type 8 Organise ‘buddies’ for science experiments, art projects etc. and severity via spectral and hue discrimination tests re- spectively. The Ishihara chart would be ideal for screening Data from Albany-Ward K [16]. Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 9 of 10 http://www.apfmj.com/content/13/1/10 tasks. Tables 6 and 7 show recommendations for colour- 11. Dwan K, Altman DG, Arnaiz JA, Bloom J, Chan AW, Cronin E, Decullier E, Easterbrook PJ, Von Elm E, Gamble C, Ghersi D, Ioannidis JP, Simes J, coded designs made by Birch and simple steps for improv- Williamson PR: Systematic Review of the Empirical Evidence of Study ing the classroom made by Albany-Ward K, the founder of Publication Bias and Outcome Reporting Bias. PLoS One 2008, the Colour Blind Awareness organisation [16,23]. 3(8):e3081. 12. Sullivan K: Colour-blind children. Special Educ Needs 2011, 12:21–23. 13. About Color Blindness (Color Vision Deficiency): Life's minor frustrations Conclusions (and occasional dangers) for the color blind. In [http://www.toledo-bend. com/colorblind/aboutCB.asp] CVD people face a wide range of difficulties in everyday 14. Testing Color Vision: Frequently Asked Questions. In [http:// life, especially for the dichromats. Many people are not colorvisiontesting.com/color7.htm] aware of their CVD until they face difficulties differenti- 15. Sullivan K: The colour conundrum. In SecEd, Volume 15; 2011. 16. Albany-Ward K: Why colour really does matter. In Prep School, Volume 15; ating colours or after they have undertaken colour vision 2011:36–37. testing. Screening for CVD is one possible intervention 17. Spalding JAB: Doctors with inherited colour vision deficiency: their and should be carried out early in life. Increasing the difficulties in clinical work. In Colour Vision Deficiencies XIII. Volume 59. Edited by Cavonius CR. The Netherlands: Springer Netherlands; 1997:483–489. awareness of CVD and its impact at the various stages 18. Mandola J: The role of color vision anomalies in elementary school of life will prompt the affected individuals to take on ap- achievement. J Sch Health 1969, 39(9):633–636. propriate measures to ensure that CVD does not become 19. Wilkinson WK: The cognitive and social-emotional correlates of color deficiency in children: a literature review and analysis. Adolescence 1992, their handicap. 27(107):603–611. 20. Grassivaro Gallo P, Panza M, Viviani F, Lantieri PB: Congenital dyschromatopsia Abbreviations and school achievement. Percept Mot Skills 1998, 86(2):563–569. NCV: Normal colour vision; CVD: Colour vision deficiency; ACVI: Acquired 21. Cumberland P, Rahi JS, Peckham CS: Impact of congenital colour vision colour vision impairment. deficiency on education and unintentional injuries: findings from the 1958 British birth cohort. BMJ 2004, 329(7474):1074–1075. Competing interests 22. Tagarelli A, Piro A, Tagarelli G, Lantieri PB, Risso D, Olivieri RL: Colour The authors declare that they have no competing interest. blindness in everyday life and car driving. Acta Ophthalmol Scand 2004, 82(4):436–442. 23. Birch J: Diagnosis of defective colour vision: Butterworth-Heinemann; 2001. Authors’ contributions 24. Colour Vision Deficiency: Health Promotion Board; 2001. TNC conceived the study. CV and GS conducted the literature review and drafted the article. TNC reviewed the drafts of the article. All authors read 25. Cole BL, Maddocks JD: Color vision testing by Farnsworth lantern and and approved the final manuscript. ability to identify approach-path signal colors. Aviat Space Environ Med 2008, 79(6):585–590. Author details 26. Macdonald WA, Cole BL: Evaluating the role of colour in a flight Ministry of Health Holdings Pte Ltd, 1 Maritime Square, #11-25, Harbour information cockpit display. Ergonomics 1988, 31(1):13–37. Front Centre, Singapore 099253, Singapore. Research Department, 27. Birch J: Performance of colour-deficient people on the Holmes-Wright SingHealth Polyclinics Head Office, 167 Jalan Bukit Merah, Connection One lantern (type A): consistency of occupational colour vision standards in Tower 5, #15-10, Singapore 150167, Singapore. DUKE-NUS Graduate Medical aviation. Ophthalmic Physiol Opt 2008, 28(3):253–258. School, 8 College Rd, Singapore 169857, Singapore. 28. Vingrys AJ, Cole BL: Validation of the Holmes - Wright lanterns for testing colour vision. Ophthalmic Physiol Opt 1983, 3(2):137–152. Received: 15 August 2013 Accepted: 19 September 2014 29. Kinney JA, Paulson HM, Beare AN: The ability of color defectives to judge signal lights at sea. J Opt Soc Am 1979, 69(1):106–110. 30. Vingrys A, Cole B: The ability of colour defective observers to recognise an optimised set of red, green and white signal lights. In Colour Vision References Deficiencies XI. Volume, Volume 56. Edited by Drum B. The Netherlands: 1. Spalding JA: Colour vision deficiency in the medical profession. Br J Gen Springer Netherlands; 1993:87–95. Pract 1999, 49(443):469–475. 31. Huang M, Bullough J, Boyce P, Bierman A: Detection and Identification of 2. Chia A, Gazzard G, Tong L, Zhang X, Sim E-L, Fong A, Saw SM: Red-green Light-Emitting Diode Traffic Signals by Protan Observers. Transport Res colour blindness in Singaporean children. Clin Experiment Ophthalmol Rec 2003, 1844(1):52–58. 1844. 2008, 36(5):464–467. 32. Culp G: Increasing Accessibility for Map Readers with Acquired and 3. Cole BL: The handicap of abnormal colour vision. Clin Exp Optom 2004, Inherited Colour Vision Deficiencies: A Re-Colouring Algorithm for Maps. 87(4–5):258–275. Cartogr J 2012, 49(4):302–311. 4. Steward JM, Cole BL: What do color vision defectives say about everyday 33. Kuyk TK, Veres JG, Lahey MA, Clark DJ: Ability of deutan color defectives to tasks? Optom Vis Sci 1989, 66(5):288–295. perform simulated air traffic control tasks. Am J Optom Physiol Opt 1987, 5. Spalding JAB: Confessions of a colour blind physician. Clin Exp Optom 64(1):2–10. 2004, 87(4–5):344–349. 34. Mertens HW, Milburn NJ: Performance of color-dependent air traffic 6. Formankiewicz M: Acquired colour vision deficiencies. In Optometry Today, control tasks as a function of color vision deficiency. Aviat Space Environ Volume 49. ; 2009:37+. Med 1996, 67(10):919–927. 7. Lawrenson JG, Kelly C, Lawrenson AL, Birch J: Acquired colour vision 35. Cole BL, Lian KY: Search for coloured objects in natural surroundings by deficiency in patients receiving digoxin maintenance therapy. Br J people with abnormal colour vision. Clin Exp Optom 2006, 89(3):144–149. Ophthalmol 2002, 86(11):1259–1261. 36. Verriest G, Neubauer O, Marre M, Uvijls A: New investigations concerning 8. Papaconstantinou D, Georgalas I, Kalantzis G, Karmiris E, Koutsandrea C, the relationships between congenital colour vision defects and road Diagourtas A, Ladas I, Georgopoulos G: Acquired color vision and visual traffic security. Int Ophthalmol 1980, 2(2):87–99. field defects in patients with ocular hypertension and early glaucoma. 37. Nathan J, Henry GH, Cole BL: Recognition of colored road traffic light Clin Ophthalmol 2009, 3:251–257. signals by normal and color-vision-defective observers. J Opt Soc Am 9. Pinckers A, Marré M: Basic phenomena in acquired colour vision 1964, 54(8):1041–1045. deficiency. Doc Ophthalmol 1983, 55(3):251–271. 10. Chan A, Hróbjartsson A, Haahr MT, Gøtzsche PC, Altman DG: Empirical 38. Atchison DA, Pedersen CA, Dain SJ, Wood JM: Traffic signal color recognition evidence for selective reporting of outcomes in randomized trials: is a problem for both protan and deutan color-vision deficients. Hum Comparison of protocols to published articles. JAMA 2004, 291(20):2457–2465. Factors 2003, 45(3):495–503. Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 10 of 10 http://www.apfmj.com/content/13/1/10 39. O'Brien KA, Cole BL, Maddocks JD, Forbes AB: Color and defective color vision as factors in the conspicuity of signs and signals. Hum Factors 2002, 44(4):665–675. 40. Cole BL: Protan colour vision deficiency and road accidents. Clin Exp Optom 2002, 85(4):246–253. 41. Cole BL, Maddocks JD: Defective colour vision is a risk factor in driving. In Colour Vision Deficiencies XIII, Volume 59. Edited by Cavonius CR. The Netherlands: Springer Netherlands; 1997:471–481. 42. Norman LG: Medical aspects of road safety. Lancet 1960, 1(7133):1039–1045. 43. Taylor WO: Effects on employment of defects in colour vision. Br J Ophthalmol 1971, 55(11):753–760. 44. Illumination ICo: Technical Report: International Recommendations for Colour Vision Requirements for Transport. Vienna, Austria: CIE Central Bureau; 2001. 45. Hovis JK, Oliphant D: A lantern color vision test for the rail industry. Am J Ind Med 2000, 38(6):681–696. 46. Vingrys AJ, Cole BL: Are colour vision standards justified for the transport industry? Ophthalmic Physiol Opt 1988, 8(3):257–274. 47. Dain SJ, Hughes LE: Survey of the Colour Vision Demands in Fire-Fighting. Oxford, United Kingdom: Oxford University Press; 2003. 48. Margrain T, Birch J: A suitable study to evaluate colour vision requirements for firefighters? Occup Med 1994, 44(5):257–258. 49. Margrain TH, Birch J, Owen CG: Colour vision requirements of firefighter. Occup Med (Lond) 1996, 46(2):114–124. 50. Davison SP, Myslinski NR: Shade selection by color vision-defective dental personnel. J Prosthet Dent 1990, 63(1):97–101. 51. Cumberland P, Rahi JS, Peckham CS: Impact of congenital colour vision defects on occupation. Arch Dis Child 2005, 90(9):906–908. 52. Kostyla AS, Clydesdale FM: The psychophysical relationships between color and flavor. CRC Crit Rev Food Sci Nutr 1978, 10(3):303–321. 53. Bresnick Gh GAPMKK: Urinary glucose testing inaccuracies among diabetic patients: Effect of acquired color vision deficiency caused by diabetic retinopathy. Arch Ophthalmol 1984, 102(10):1489–1496. 54. Vision Screening for Pre-School. [http://www.hpb.gov.sg/HOPPortal/health- article/520] 55. Health Screening for Primary School. [http://www.hpb.gov.sg/HOPPortal/ health-article/632] 56. Health Screening for Secondary School. [http://www.hpb.gov.sg/ HOPPortal/health-article/690] 57. Hong S: Types of acquired color-vision defects. AMA Arch Ophthalmol 1957, 58(4):505–509. 58. Roy Ms GRDPMJ: Color vision defects in early diabetic retinopathy. Arch Ophthalmol 1986, 104(2):225–228. 59. Fong DS, Barton FB, Bresnick GH: Impaired color vision associated with diabetic retinopathy: Early Treatment Diabetic Retinopathy Study Report No. 15. Am J Ophthalmol 1999, 128(5):612–617. 60. Rodgers M, Hodges R, Hawkins J, Hollingworth W, Duffy S, McKibbin M, Mansfield M, Harbord R, Sterne J, Glasziou P, Whiting P, Westwood M: Colour vision testing for diabetic retinopathy: a systematic review of diagnostic accuracy and economic evaluation. Health Technol Assess (Winchester, England) 2009, 13(60):1–160. 61. Pacheco-Cutillas M, Edgar DF, Sahraie A: Acquired colour vision defects in glaucoma—their detection and clinical significance. Br J Ophthalmol 1999, 83(12):1396–1402. 62. Swarbrick HA, Nguyen P, Nguyen T, Pham P: The ChromaGen contact lens system: colour vision test results and subjective responses. Ophthalmic Physiol Opt 2001, 21(3):182–196. doi:10.1186/s12930-014-0010-3 Submit your next manuscript to BioMed Central Cite this article as: Chan et al.: Subjects with colour vision deficiency in and take full advantage of: the community: what do primary care physicians need to know? Asia Pacific Family Medicine 2014 13:10. • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Asia Pacific Family Medicine Springer Journals

Subjects with colour vision deficiency in the community: what do primary care physicians need to know?

Chan, Xin; Goh, Shi; Tan, Ngiap
Asia Pacific Family Medicine , Volume 13 (1) – Oct 9, 2014
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Copyright © 2014 by Chan et al. ; licensee BioMed Central Ltd.
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Medicine & Public Health; General Practice / Family Medicine; Primary Care Medicine
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Abstract

Background: Congenital colour vision deficiency (CVD) has a prevalence of 8% for men and 0.4% for women. Amongst people born with normal colour vision, the acquired form of CVD can also affect them at later stages of their lives due to disease or exposure to toxin. Most CVD persons have difficulties dealing with colours in everyday life and at work, but these problems are under-reported due to a lack of its awareness in the general population. This literature review seeks to present findings of studies and reports on the impact of CVD on the affected persons chronologically through different stages of their lives and their coping measures. Methods: Scientific publications and corresponding references relating to how CVD affects individuals were searched, identified and retrieved from PubMed, National University of Singapore and Cochrane electronic databases. Books that were not available electronically were manually searched. Paramedical literature was also included through online searches using Google and Google Scholar. Inclusion criteria were English-based studies pertaining to effects of CVD on everyday life and respective coping measures, including experimental, observational studies, symposium proceedings and systematic review. There was no timeframe restriction for these publications. Articles using anecdotal evidence were excluded with the exception of those used to describe the effects of CVD on play age and school age. Our literature search found 136 articles, 60 of which were used in this review based on the respective selection criteria. Results: CVD affects many aspects of life from childhood to adulthood. The implications extend across play, sports, driving, education, occupation, discrimination, and health and safety issues. Awareness of CVD helps to identify and develop corresponding coping strategies. Conclusions: More work needs to be done in raising awareness of CVD and its implications, as well as implementing measures to overcome these difficulties. Keywords: Colour vision deficiency, Activities of daily living, Coping measures Background cones is abnormal – protanomaly involves reduced sensi- Individuals with normal colour vision (NCV) have three tivity to red, deuteranomaly involves reduced sensitivity to types of specialised cells, known as cones, in their retina to green and tritanomaly involves reduced sensitivity to blue. help them to perceive red, green and blue colours. People Dichromacy occurs when a person only has two retinal with abnormal cones will perceive colours differently. There cones that are able to perceive colour, resulting in the total are several types of such colour vision deficiency (CVD). absence of one colour. There are three types of dichro- Anomalous trichromacy occurs when one of the three macy – protanopia, deuteranopia, and tritanopia. Congenital CVD has a prevalence of 8% for men and 0.4% for women [1]. In Singapore, a study done on 1249 * Correspondence: tan.ngiap.chuan@singhealth.com.sg Research Department, SingHealth Polyclinics Head Office, 167 Jalan Bukit children aged 13–15 years using the Ishihara 24-plate Merah, Connection One Tower 5, #15-10, Singapore 150167, Singapore 3 edition book found 5.3% of boys and 0.2% of girls to be DUKE-NUS Graduate Medical School, 8 College Rd, Singapore 169857, colour blind [2]. All people with CVD, except for a few Singapore Full list of author information is available at the end of the article © 2014 Chan et al. ; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 2 of 10 http://www.apfmj.com/content/13/1/10 mildly affected deuteranomals, report that they encoun- timeframe indicated as some studies done on CVD de- ter problems with colour perception in everyday life and cades ago have implications that remain pertinent today. at work [3]. Yet, there have been few studies systematic- The exclusion criteria used were non-English articles ally documenting the personal difficulties that CVD per- and non-human studies. Articles using anecdotal evi- sons experience in their daily lives [4]. There seems to dence were also excluded with the exception of those be a lack of awareness for the implications of CVD in used to describe the effects of CVD on play age and the general population [1,5]. Furthermore, CVD can de- school age due to the paucity of primary sources of evi- velop later in life due to development of disease or ex- dence for these stages of life. Eligibility assessment was posure to toxins such as chemicals or drugs which affect performed by two unblinded reviewers. Disagreements the retinal cellular structure and function [6-9]. Known between reviewers were resolved by consensus. as acquired colour vision impairment (ACVI), the preva- The literature search on electronic databases provided lence of CVD, inclusive of both the congenital and ac- a total of 118 citations. Additional 18 records were iden- quired forms, is expected to increase globally with the tified through hand searches, reference lists and search increasing population. Therefore, this article presents a engines on the World Wide Web. After adjusting for du- review of current literature, comprising scientific studies plicates, 124 remained. Of these, 52 were excluded as and paramedical reports of the effects of CVD on indi- they were not within the scope of the review, their full viduals through their different stages of life. This would text was not available or not translated into English. The better help those afflicted with CVD to identify the do- full texts of the remaining 72 citations were examined in mains of difficulties in daily living and to determine pos- detail. It appeared that 12 did not meet the inclusion cri- sible strategies to cope with their predicaments. teria as they were not relevant to the topics of discussion. Eventually, 60 records met the inclusion and exclusion cri- Methods teria and were used in this review. Of these 60, 46 were Data sources identified via electronic databases while 14 were identified Studies on how CVD affects well-being were identified from alternative sources as mentioned earlier. The selec- from multiple sources. The following electronic data- tion of studies is summarised in Figure 1 below. bases were searched: PubMed database, National Univer- Each article was evaluated using the PICOS framework sity of Singapore (NUS) database and Cochrane database (population, interventions, comparator, outcome and of systematic reviews. Search terms included ‘colour vi- study design). sion deficiency’, ‘colour vision impairment’, ‘colour blind- ness’, ‘well-being’, ‘quality of life’, ‘everyday life’, ‘everyday Limitations tasks’, ‘discrimination’, ‘handicap’, ‘education’, ‘driving’, ‘acci- No review protocol was used hence there may be bias dents’, ‘occupation’, ‘aviation’, ‘maps’. The last search was incurred in review methods in the post hoc decisions. performed on 22 May 2013. The references within the Publication bias and outcome reporting bias have been retrieved articles found were also searched. Additionally, well documented and may overestimate the effects of electronic journals in the field of CVD that were avail- CVD in the included studies [10,11]. able online were searched. Books that were not available electronically were hand searched for relevant studies. Results We also used the proceedings of the eleventh and thir- The impact of CVD on affected persons will be pre- teenth Symposiums of the International Research Group sented chronologically from childhood at play and in on Colour Vision Deficiencies, held in Sydney (1991) schools, young adulthood, working life to late adulthood. and France (1995) respectively. Paramedical literature Figure 2 summarises the impact of CVD on affected in- was included through online searches on the World dividuals at different stages of their life. Wide Web, using search engines such as Google and Google Scholar. All literature found was added to End- Play age Note X6 digital library. A child engages play and learning during childhood. They are often exposed to colourful objects such as toys Study selection and accessories during these activities. A child with deu- Inclusion criteria were articles available in English lan- teranomaly, the commonest form of colour-blindness, will guage, studies pertaining to effects of CVD on everyday be able to accurately name only four colours within a box life and specific populations (for example, pilots). These of 24 coloured pencils. Nevertheless, they will probably be publications consist of experimental, observational stud- able to guess more [12]. Consequently, parents of CVD ies, symposium proceedings and systemic review. No re- children often reported that their children were mis- strictions on the years of study/follow-up, publication taken as slow learners or ridiculed in preschool for mixing status or publication date were imposed. There was no colours up and colouring objects wrongly [13,14]. Such Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 3 of 10 http://www.apfmj.com/content/13/1/10 Records were identified through Additional records were identified database searching (n = 118) through other sources (n = 18) 12 duplicate records were removed . (n = 12) Records were screened. Records were excluded. (n = 124) (n = 52) Full-text articles were Full-text articles were assessed for eligibility excluded, with reasons (n = 72) (n = 12) Studies were included in qualitative synthesis (n = 60) Figure 1 Flow diagram of study selection. Figure 2 Summary of activities that can be affected by CVD across various stages of life. Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 4 of 10 http://www.apfmj.com/content/13/1/10 Table 1 Common difficulties faced by CVD students in mistakes may cause embarrassment to the child and lead academic subjects to significant consequences such as school refusal or social Subject Areas of difficulties withdrawal. Other learning difficulties include inability to accurately Art Unable to appreciate how colours are used describe things around them, failure to follow instructions Use of wrong colours when painting relating to colour and to read coloured printing against a Chemistry Unable to read litmus paper accurately coloured background [12]. This will translate into prac- Unable to tell the colours of different chemical solutions in tical problems such as difficulty completing workbook quantitative analysis tasks relating to colour, and even cheating in tests because May be unable to identify metals by colour of flame the child is unable to tell the questions written in coloured produced when a metal is burnt ink or chalk on the board [14]. Biology Unable to accurately read stained slides under microscope In Parten’s classification of stages of play, activities May not be able to identify species of plants such as associative and cooperative play, which involves May not be able to accurately carry out dissections interpersonal interactions, are critical stages of social de- May have difficulty understanding coloured diagrams in velopment. However, CVD children may face difficulties textbooks when playing with others because they cannot differenti- Physics Will have difficulty with coloured wiring and use of prisms ate between different teams distinguished by coloured tags, nor recognise coloured pieces in board games [14]. Maths Unable to read pie charts and graphs In the area of personal safety, CVD children may get Data from Dutton F [13], Waggoner TL [14], Sullivan K [15], Albany-Ward K [16], Spalding JAB [17]. lost more easily if given directions using coloured ob- jects as signs [14]. CVD children may also be fussy about eating certain food, for example, vegetables, because they intelligence scores and elementary school achievement perceive these foods in unpalatable colours [12]. The ef- [18]. A literature review conducted in 1992 reported that fect on the choice of food should not be overlooked in a studies attempting to relate CVD to learning difficulty were phase whereby proper nutrition is important for the equivocal in their outcome [19]. A subsequent study in child’s growth. 1998 showed significantly lower general academic scores among 82 children with CVD as compared to 82 children School age with NCV, matched by age and class [20]. In contrast, a Most children with CVD are unaware of their condition, 2004 cohort study on 499 CVD children found that CVD with many only realising so when they are in secondary did not cause significantly lower scores in mathematics school [12]. Steward and Cole in their study showed that and reading at 7 years and 16 years of age respectively, 49% of dichromats and 8% of anomalous trichromats be- even after adjusting for birth-weight, social class at birth, came aware of their CVD in primary school, with a fur- family size, and parental education [21]. Furthermore, the ther 22% of dichromats and 28% of anomalous trichromats highest educational qualification was not significantly asso- in secondary school [4]. They also showed that 71% of di- ciated with colour vision status [21]. Another 2004 ques- chromats and 27% of anomalous trichromats began to sus- tionnaire survey showed no significant difference in the pect having CVD after they encountered difficulties with disciplines studied between NCV and CVD persons, but colour [4]. However, 77% and 94% respectively had a clear CVD interviewees tended towards technical studies (30%, diagnosis of CVD only after formal colour vision testing as opposed to 18% of NCV subjects), and less of them [4]. Upon diagnosis, they often retrospectively recall the undertook tertiary education in university (68.9%, as op- difficulties they faced with discriminating colours in earlier posed to 79.9% of NCV subjects) [22]. life [4]. CVD-related difficulties during the schooling years are CVD students struggle in a variety of subjects, espe- common and are observed in a variety of sports. In an cially the sciences. Sullivan (2011) noted that CVD chil- Australian study on 102 CVD subjects, one in four re- dren tend to lag behind in many subjects where colour ported difficulties with sporting activities [4]. Confusion is used as a teaching tool, including mathematics, sci- arises due to inability of CVD players to differentiate their ence, geography, reading, sport and food technology team members from the opponents wearing coloured uni- [12]. The common difficulties faced by CVD students in forms. Theformeralsotendto loseorangegolf balls in the academic subjects are summarised in Table 1 [13-17]. grass, and mistake red for brown snooker balls [4,12,23]. Nonetheless, studies which aimed to determine the impact of CVD on academic achievement showed con- Young adulthood during military service flicting outcomes, possibly due to differences in study Colour vision is involved in a variety of military activities designs. A 1969 case control study showed no signifi- and training. Certain vocations in the air-force, navy and cance difference between NCV and CVD children in infantry require normal colour vision [23,24]. Those Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 5 of 10 http://www.apfmj.com/content/13/1/10 commonly affected are military personnel in the aviation appears the same to a CVD user as it does to one with and maritime divisions of the defence force. NCV [32]. Although map reading among CVD users has In aviation, a Farnsworth lantern test is routinely used not been studied extensively, it was found that readers with to screen colour vision and involves identification of a CVD made more errors naming the boundary lines on pair of lights consisting of combinations of red, green or multi-coloured terrain maps [33]. Another study showed white. The Precision Approach Path Indicator (PAPI) that only a small percentage of CVD readers could name signal system tells pilots whether their aircraft is above, the colours of a weather radar display without error [34]. below, or on the correct approach path for landing. It CVD persons are slower and less successful in search tasks, displays four signal lights that can be red or white. A when colour is the primary attribute of the target object, or case–control study was performed on 52 CVD subjects if colour is used to organize visual displays [3,35]. and 52 subjects with NCV in 2008: amongst CVD sub- jects who passed the Farnsworth lantern, they made sig- Middle to late adulthood nificantly more errors naming PAPI signals than NCV Activities of daily living subjects and 80% of them made more errors than the Nearly 90% of dichromats and up to two-thirds of anom- worst performing NCV subject [25]. Another study showed alous trichromats reported difficulties with everyday tasks that CVD observers made significantly more errors and that involve colour [4]. Tables 2 and 3 show the difficulties were slower in completing tasks requiring processing of reported by persons with CVD, and the difficulties sub- colour coded electronic flight information [26]. analysed within each subtype of CVD [4,22]. The Holmes–Wright lantern type A (H-W A) is an oc- Even amongst NCV individuals during the early part of cupational colour vision test used by the UK Civil Aviation life, they can develop CVD as they age. Acquired CVD or Authority (CAA) and approved by Joint Aviation Require- ACVI can occur due to age-related crystalline changes in ments (JAR) to select aircrew. The Commission Inter- lens, age-related maculopathy and conditions such as dia- nationale d’Eclairage (CIE) recommends that the Falant betes, glaucoma and optic neuritis. They can also be pass criteria be used with all approved lanterns. However, a caused by medications such as digoxin, sildenafil, chloro- 2008 study showed that this investigation and selection cri- quine and ethambutol. ACVI are often tritan (blue-yellow) teriausedbythe UK CAA andCIE do notidentifyindivid- in nature. Tritan defects cannot be detected using the uals with superior colour discrimination ability and lack Ishihara chart. Instead, the Hardy, Rand and Rittler plates internal consistency [27]. There is thus no evidence to sug- may be more useful as tritan plates are also included and gest that successful CVD applicants have significantly bet- the severity of the defects can be graded [6]. Alternatively, ter colour discrimination ability than CVD people who fail. the Farnsworth D15 test may be used [6]. The selection process is therefore potentially unfair to CVD persons applying for aviation positions. Driving and accidents In navy, CVD persons have difficulty recognising red- Safe driving requires the driver to recognise colour-coded green-white maritime signals. The Holmes-Wright Type traffic lights and road signage. A case control study B lantern is the standard colour vision test used by the showed that both CVD and NCV subjects who were quali- Board of Trade in maritime industry [28]. A 1983 study fied to drive were in similar proportions (83.4% and 83.8% that validated the Holmes-Wright Type B lantern test as Table 2 Difficulties in everyday life reported by 151 CVD a discriminating test showed that all CVD persons failed, subjects and 302 NCV subjects except for a few mild deuteranomals [28]. This correlates Difficulties associated with % of CVD % of NCV Significance with other studies which also showed that all CVD per- observers observers (p value) sons, except for a few mild deuteranomals, make errors Clothing colours 23.8 1.0 <0.0001 recognising maritime signals [29,30]. Furthermore, the Workplace/hobbies colours eg. 13.2 1.0 <0.0001 rate of errors increases with decreasing signal illumin- pie charts ance [29,30]. Both protanopes and protanomals have sig- Natural colours 40.4 1.0 <0.0001 nificantly reduced visual range for red signals [29,31]. Colours relating to cooking s eg. 31.7 8.6 <0.0001 Kinney, Paulson and Beare showed that only 40% of deu- Identification of cooked versus tans and 14% of protans performed as well as their raw meat worse performing NCV subjects [29]. It is largely ac- Sports colours eg. shirts of 21.2 1.3 <0.0001 cepted that normal colour vision is essential for safe players maritime navigation. Skin colours 3.3 1.7 0.0007 Inherited CVD is marked by a difficulty in discerning red Television colours setting 6.0 0.7 0.0002 from green, while acquired CVD leads to decreased ability Data from Tagarelli et al. [22] (Statistical significance of differences were to distinguish blue from green. CVD persons struggle with calculated using the chi-square test or Fisher exact test, two-tailed significance reading coloured maps, although a monochromatic map level 0.05). Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 6 of 10 http://www.apfmj.com/content/13/1/10 Table 3 Percentage of subjects with different types of CVD reporting difficulty in everyday tasks Difficulties associated with Dichromats (%) Anomalous trichromats (%) Protans (%) Deutans (%) NCV (%) (n = 37) (n = 65) (n = 36) (n = 66) (n = 102) Clothing/goods colours 86 66 78 71 0 Workplace/hobbies colours 68 23 50 33 0 Plant/flower identification 57 18 44 26 0 Ripeness of fruits and vegetables 41 22 31 27 0 Cooked versus raw meat 35 17 33 20 0 Sports colours 32 18 19 23 0 Adjust television colour settings 27 18 28 18 2 Skin colours eg. sunburn, rashes 27 11 17 17 0 Previously taken wrong medication due to colour 03 3 1 0 difficulties Data from Steward and Cole [4]. respectively) [22]. However, regular use of a car was sig- In terms of accident rates, studies reported that CVD nificantly less common among CVD subjects than NCV drivers did not have more road traffic accidents than subjects [22]. NCV drivers [21,22,36,42]. However, protans showed Reading road traffic signals tend to be less difficult for significantly more rear end collisions and accidents by CVD observers compared to maritime, aviation and rail overlooking red rear, stop and warning lights than colour signals because the former is viewed from much shorter normal [36]. Rear end collisions seemed more prevalent distances. Furthermore, they are assisted by cues such as amongst protans because the red lights of the rear end position of traffic lights, relative brightness and move- appeared dimmer to them, resulting in delayed percep- ment of other traffic [3,4,36]. Nevertheless, experimental tion in poorly illuminated areas. Deutans caused more studies have shown that people with CVD make more accidents than NCV drivers at traffic light controlled in- errors recognizing the colours of road traffic signals than tersections, although this was not statistically significant those with normal vision [37,38]. Deuteranopes have sig- [36]. A case control study also showed that there was no nificantly reduced ability to notice red, orange and green increased risk of unintentional workplace injuries amongst colour-coded traffic control devices compared to NCV CVD subjects [21]. subjects [39]. Protans are known to have reduced visual range for red signals compared to NCV observers [36,40]. Restriction of career options and workplace discrimination About 18-20% of anomalous trichromats and 50-60% of Individuals with CVD appeared to have restricted career dichromats admitted to difficulty recognizing road traffic options. A 1971 study found that only 214 out of 569 CVD signals while 10-15% of protans admitted to difficulty see- subjects made suitable choices of career [43]. Table 4 shows ing red signal lights [4,23,41]. careers and occupations known to be affected by CVD Atchison DA et al. showed that response times and error [23,24]. The Commission Internationale de L’Éclairage rec- rates for recognising red and yellow lights were increased ommends that normal colour vision be a prerequisite for in CVD subjects compared to NCV subjects [38]. On the pilots of scheduled passenger aircraft, especially large air- contrary, Tagarelli et al. showed there were no differences craft, and is mandatory for other commercial pilots to pass between the two groups in identifying the colours of traffic a lantern test and should not have a protan (red-deficient) light signals. However, when the relative positions of the colour vision deficiency [44]. traffic lights were changed, more CVD subjects had diffi- According to Birch, coloured signals may be preferred to culty identifying the colours than NCV subjects but the dif- short wavelength radio for communication in the armed ference was not statistically significant [22]. forces because radio signals can be intercepted [23]. Hence, Significantly higher proportion of CVD subjects pre- vocations such as signals personnel and again aircraft pilots ferred daytime driving over night-time driving compared will be unsuitable for individuals with CVD. to NCV subjects [22]. This could be due to difficulty iden- In the railway industry, train drivers and other rail tifying the reflectors on the road and identifying the lights workers must be able to recognize red, yellow and green of the car ahead at night [22]. Confusion of traffic lights signals at distances up to 1 km, sometimes under condi- and street lights was also noted in one-third of CVD tions of poor visibility due to fog or rain. Hovis JK and drivers [4]. The detection of dashboard warning lights Oliphant D reported that 97% of individuals with CVD (which are often red) was significantly more difficult for failed a lantern test (CNLAN) that was found to provide a protans than deutans (17% versus 3% respectively) [4]. reasonable functional assessment of colour discrimination Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 7 of 10 http://www.apfmj.com/content/13/1/10 Table 4 Career and occupations known to apply a colour Even among healthcare professionals, CVD can be dis- vision standard advantageous to doctors and dentists. Difficulties faced NORMAL COLOUR VISION Commercial airline pilots, air traffic by CVD doctors and medical students are summarised controllers, technical and in Table 5 [5,17]. maintenance staff at airports, CVD doctors tend to avoid the following specialties aircraft pilots and engineers in the armed services, naval officers, where normal colour vision is important: histopathology, submarine personnel, masters and microbiology, haematology, dermatology, ophthalmol- watchkeepers on merchant marine ogy, surgery, anaesthesia (uses differently coloured gas vessels, customs and excise officers, train drivers, railway tanks) [17]. A 1990 case control study showed that CVD engineers and maintenance staff; dentists made significantly more errors in the hue and workers in industrial colour quality chroma aspects of shade selection, hence affecting their assurance and colour matching, workers in fine art reproduction ability to select prosthetic teeth to match natural teeth and photography, some electrical [50]. Hue is the quality that distinguishes one family of and electronic engineers colours from another based on their different wave- COLOUR VISION STANDARD Fire fighters, police officers, some lengths in the visible spectrum. Chroma is the satur- APPLIED BUT ACCEPTS SOME WITH electrical and electronic engineers, ation, intensity, or strength of the hue. SLIGHT CVD some ranks in the armed services, hospital laboratory technicians, Nearly one-quarter of CVD subjects reported having merchant seamen colour difficulties in previous jobs, as well as being pre- OCCUPATIONS WHERE CVD IS A Art teaching, bacteriology, botany, cluded from an occupation because of their CVD [4]. DISADVANTAGE AND COLOUR chemistry, interior design, Steward and Cole showed that 43% of dichromats and VISION STANDARD MAY APPLY histopathology, horticulture, geology, diamond grading, 29% of anomalous trichromats reported their CVD had metallurgy affected their choice of career [4]. 46% of dichromats Data from Birch J [23] and Health Promotion Board of Singapore [24]. and 15% of anomalous trichomats also reported colour difficulties with everyday work, and this was statistically significant when compared with NCV subjects [4]. for the rail industry [45]. Vingrys AJ and Cole BL, in their However, a 2004 questionnaire survey revealed that literature review to determine whether colour vision stan- CVD people had little difficulty in maintaining perman- dards were justified for the transport industry, found that ent employment [22]. Nonetheless, they were more likely CVD observers made more errors and had significantly to hold subordinate jobs, for example, as agents, clerks slower reaction times in recognising coloured signal lights or servants, whereas NCV subjects preferred autono- [46]. It concluded that there was sufficient evidence to war- mous activities, such as commercial and trade work [22]. rant retention of colour vision standards in transport in- A subsequent study in 2005 also revealed that there was dustries where the highest standards of safety are expected. no significant difference between proportion of CVD Severe CVD is generally unacceptable in the police force. Conflict of evidence regarding identification of clothing or Table 5 Difficulties faced by CVD doctors and medical vehicles or items using colours at the scene of crime may students interfere with jurisdiction in criminal or forensic cases [23]. No. Difficulties faced by CVD doctors and medical students CVD applicants can be recruited as fire fighters if they 1 Body colour changes: pallor, cyanosis, jaundice pass the Ishihara’s test. Should they fail this colour vision 2 Skin rashes, erythema and lymphangitis test, they would have to undertake the Farnsworth-Munsell 3 Blood and urine test strips Standard D15 test (FMD-15) [47-49]. Protans are not ac- cepted in the fire brigade because of their reduced visibility 4 Ophthalmology: disc pallor, diabetic changes, haemorrhage versus pigmentation, glaucoma, haemorrhage in anterior chamber, Kayser of red signs and traffic signals. In addition, oxygen (black) Fleischer rings and acetylene (maroon) gas cylinders are similar in shape 5 Body products: blood versus bile in urine, faeces, sputum, vomit and might be confused due to this CVD [49]. Other critical 6 Otoscopy: inflamed drum, wax versus blood tasks which require colour discrimination among the fire- fighters include interpretation of computer displays in com- 7 Microscopy munications units, assessment of gas level in gas detectors, 8 Mouth and throat conditions useofindicator papers, identificationof zoneoffireon 9 Ishihara test giving building evacuation and fault indicator panels, deduction of 10 Chemistry end-points the burning substance based on the colour of the smoke 11 Tissue identification in surgery and flames and distinction of hydraulic and pressure hoses, 12 Gangrene and sores fire extinguishers, gas cylinders, pipes, ducts, and triage labels [47]. Data from Spalding [5,17]. Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 8 of 10 http://www.apfmj.com/content/13/1/10 Table 6 Recommendations for colour-coded designs and NCV people in the major occupational groups ex- cept for transport operations, aircraft and ship officers, No. Recommendations for colour-coded designs electrical and electronic engineering, as well as fibre and 1 Avoid specific colours if no redundancy is possible textile processing [51]. 2 Include redundancy, especially lightness difference, whenever possible Health-related activities 3 Segment areas of colour which might otherwise be confused The effect of colour on appetite is important because poor 4 Avoid dark red or green text on a black background growth and malnutrition due to poor oral intake, can 5 Enhance colour conspicuity such as using white or yellow for affect the young and old respectively. Colour perception objects which have to be seen in poor illumination or at night of food can adversely affect the appetite and taste percep- 6 Avoid glare tion of CVD people. A food study in 1978 demonstrated Data from Birch [23]. that addition of red dye to fruit flavoured beverages in- creased the perceived sweetness by 5-10%, while an addition of blue dye to cherry or strawberry flavoured bev- for congenital red-green colour blindness in children and erages decreased sourness and fruit flavour by 20% [52]. should be made routine in schools. Currently, vision Colours are often used to differentiate the different screening in schools in Singapore only includes visual acu- types of oral medications. Steward and Cole reported ity and stereopsis [54-56]. that some CVD subjects in their study had previously Nevertheless, screening for acquired CVD (ACVI) is taken the wrong medications due to difficulties with challenging as they do not follow the well-defined pat- colour [4]. Depending on what medication was taken, terns of congenital CVD and may be difficult to classify the adverse outcomes could range from insignificant to [6,57]. Currently, there is a paucity of primary studies to fatal. Patients who habitually mix their medications evaluate the costs and benefits of mass screening for ac- without the external packaging in the same pill storage quired CVD, although some preliminary studies show compartment would be more prone to such hazards. that doing so may help detect diabetic retinopathy and CVD may also affect the interpretation of coloured primary open angle glaucoma earlier [8,58,59-62]. dipstick results used in healthcare [5,17,53]. A case–con- Once CVD has been detected via screening, measures trol study involving patients who had ACVI due to dia- must be taken to help the afflicted overcome their difficul- betic retinopathy showed that diabetics made significantly ties with colour discrimination.Thisisespeciallyimportant more errors in interpreting urinary glucose dipstick results as 46% of dichromats and 15% of anomalous trichomats than non-diabetic controls [53]. This would make moni- reported colour difficulties with everyday work [4]. Means toring of glycemic control more difficult, although moni- of overcoming occupational colour deficiencies used in- toring is more commonly done via serum glucose today. clude asking others, using instruments, keeping objects of With increasing age and concurrent rising incidence of different colours in separate places and avoiding colour malignancies, detecting and awareness of colour-related tasks [4]. A 2001 study showed that the use of tinted con- signs and symptoms become important for susceptible indi- tact lenses in CVD subjects significantly reduced error viduals. Nonetheless, Spalding (1995) and Spalding (2004) rates on the Ishihara and Farnsworth Munsell D-15 test mentioned difficulties in detecting hemoptysis, hematem- [62]. This may provide some assistance in colour-related esis, hematuria and bloody stools reported by these affected Table 7 Steps for improving the classroom for CVD individuals [5,17]. Detecting these presenting symptoms children early would allow earlier diagnosis and treatment of No. Steps for improving the classroom for CVD children any underlying sinister conditions, such as lung cancer, 1 Label felt tips, paints, pencils etc. upper gastrointestinal bleeds, bladder cancer and colo- 2 Colour-code boxes of toys, art materials and books rectal cancer. 3 Check computer-based teaching aids, web pages, computer settings Discussion 4 Use strong contrast on white or chalkboards. CVD is currently under-diagnosed as there is no struc- tured screening in various parts of the world. Screening 5 Use patterns and labels rather than colours for maps, pie charts, diagrams for CVD is important so that appropriate career advice can be given to these individuals, especially during the 6 In sports and games, ensure that children can see who is on his or her ‘team’ period when they are receiving their education [43]. This 7 Group and label beads, bricks and colouring material according to would require detection of CVD through screening using colour pseudoisochromatic tests, and then determining the type 8 Organise ‘buddies’ for science experiments, art projects etc. and severity via spectral and hue discrimination tests re- spectively. The Ishihara chart would be ideal for screening Data from Albany-Ward K [16]. Chan et al. Asia Pacific Family Medicine 2014, 13:10 Page 9 of 10 http://www.apfmj.com/content/13/1/10 tasks. Tables 6 and 7 show recommendations for colour- 11. Dwan K, Altman DG, Arnaiz JA, Bloom J, Chan AW, Cronin E, Decullier E, Easterbrook PJ, Von Elm E, Gamble C, Ghersi D, Ioannidis JP, Simes J, coded designs made by Birch and simple steps for improv- Williamson PR: Systematic Review of the Empirical Evidence of Study ing the classroom made by Albany-Ward K, the founder of Publication Bias and Outcome Reporting Bias. 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Ophthalmic Physiol Opt 2001, 21(3):182–196. doi:10.1186/s12930-014-0010-3 Submit your next manuscript to BioMed Central Cite this article as: Chan et al.: Subjects with colour vision deficiency in and take full advantage of: the community: what do primary care physicians need to know? Asia Pacific Family Medicine 2014 13:10. • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit

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