Because sutures are not always discernible for Wetzelielloideae, this cannot be proven for many Wetzelielloideae specimens.

Therefore, we are sceptical about the validity of this fundamental assumption underlying the taxonomic revisions of Wetzelielloideae.

We have concerns that the drastic revisions of the primary criteria for taxonomic classification as proposed by Williams et al. ( 2015) do not reflect phylogenetic significance.

Regardless of our concerns, the revision of taxonomic concepts to accommodate just one subfamily seems an illogical step if the taxonomic concepts applied towards the other dinoflagellate cyst groups remain the same.


The validity of the proposed taxonomic definitions in the subdivision of Wetzelielloideae does not allow for plasticity in archaeopyle type within otherwise morphologically similar dinoflagellate cysts.

This leads to taxonomic separation of – apart from the type of archaeopyle – morphologically indistinguishable species (Plate 1).

However, many other dinoflagellate cyst taxa are characterised by variability in archaeopyle type, and the level of detachment of the operculum is permitted within a genus, and even within species definitions.


For instance, Dissiliodinium and Durotrigia (Bailey 1987; Feist-Burkhardt et al. 2001) [4][5] have a variable archaeopyle consisting of one to five precingular plates; Lingulodinium machaerophorum (Wall 1967) [6] and Diphyes (Goodman & Witmer 1985) [7] have either a 3’ precingular or a tA apical archaeopyle; Florentinia (e.g. Sluijs & Brinkhuis 2009) [8] varies its archaeopyle involving from tA to tA3P; Schematophora (Bijl et al. 2013b) [9] has various levels of detachment of the apical series; species of Spinidinium and Vozzhennikovia (Sluijs et al. 2009) [10] involve either one (2A) or all three anterior intercalary plates in the archaeopyle; and Phthanoperidinium (Islam 1982) [11] varies its archaeopyle by occasionally including the 4’’ plate to the otherwise 2A archaeopyle.

Notably, many Protoperidinium species (e.g. Harland 1982) [3] vary in outline and type of the 2A archaeopyle.


For these genera, taxonomic concepts at genus and species levels are not primarily set on archaeopyle type but, rather, on wall morphology, ornamentation and process distribution.

We indeed observe variability in the type of archaeopyle in many Wetzelielloideae, even within the same samples, for example in specimens of Apectodinium in the original description (see examples in Plate 1).

Scanning electron microscope images of a specimen of Apectodinium hyperacanthum (Bijl et al., 2013b, plate VII, figure n) [9] show a clear angular, rectangular archaeopyle but with an adnate anterior end.

These two characteristics together are not compatible with the proposed taxonomic concept of Williams et al. ( 2015) for Apectodinium hyperacanthum, which should have a detached operculum.


If we followed the taxonomic concepts proposed, we should erect a new genus and new species for the specimen illustrated by Bijl et al. ( 2013) [9].

However, based on wall ornament, this specimen is clearly a species of Apectodinium in its original taxonomic concept.

The proposed taxonomic revision of Williams et al. ( 2015) would place the specimens exhibiting adnate soleiform archaeopyles within Wetzeliella, while based on all the other morphological features, they have close affinities to Apectodinium, which it restricts to equiepeliform archaeopyles.


In our view, the adnate soleiform versus free epeliform archaeopyles both occur within a complex of Wetzelielloidae that are similar in many more morphological characteristics than they differ, which is why in the original concept all of these were grouped into Apectodinium.


The original taxonomic concept of Wetzelielloideae is very practical for most of the species.

Applying the new taxonomic concept to the latter leads to many discussions, confusion, and unnecessary and unwanted taxonomic splitting.

Taxonomic uncertainty in the original concepts of Wetzelielloideae occurs predominantly at the species level and only very rarely at the generic level.


For instance, in many cases (sub-optimal preservation, overload of amorphous organic matter, clumping, over-oxidation), the – in our view – subtle differences in outline and ornament between Charlesdowniea columna and Charlesdowniea coleothrypta make it difficult to separate them from one another in the original taxonomic framework.

However, Williams et al. ( 2015) considered these two species to be within two different genera, as they have noted slight differences in archaeopyle type.


This proposed taxonomic revision does not at all alleviate the difficulty in deciding to which of the two species a specimen belongs.

In fact it complicates the situation because, in the new taxonomic concept, the generic classification is compromised if the archaeopyle type is not clearly discernible.

We argue that because the two species share so many morphological features, it is most practical to at least retain these species in the same genus.

Williams et al. ( 2015) broke with this basic principle of hierarchy in morphological variation for the Wetzelielloideae, which is a profound concern for the field of dinoflagellate cyst palaeontology.


We therefore find that the proposed revision leads to unnecessary speciation of dinoflagellate cyst taxa that are highly similar (if not identical) in cyst outline and wall ornamentation, but only vary slightly, if at all (see examples above), in archaeopyle type.

We now observe very chaotic, inconsistent genus and species concepts, in which cysts with the same wall features are placed in different genera just because of a slight, often non-diagnostic difference in archaeopyle type.


Central to the taxonomic definitions proposed by Williams et al. ( 2015) is the type of archaeopyle.

In practice, however, this particular morphological feature is not easily assessed using transmissed light microscopy, particularly in Wetzelliellioideae.

This is because the archaeopyle can be poorly visible in many specimens for numerous factors including poor contrast between the archaeopyle and the translucent wall; specimens are often sub-ideally oriented on the microscope slide, lack parasutural/penitabular ornamentation, and in some instances bear numerous processes that may obscure the visibility of the archaeopyle (e.g. Sluijs & Brinkhuis 2009 plate 1, figures I, J; Bijl et al. 2013, plate I, figures e, j) [8][9].

Finally, some specimens (may) have partially adnate opercula (see examples in Plate 2), to say nothing of specimens that have not hatched.


The orientation of the cyst relative to the plane of view poses a serious limitation on the practicality of the proposed taxonomic criteria underlying the revision.

In the paper by Williams et al. ( 2015), this problem was illustrated in figures 15 and 16 of plate 1, and figures 15 and 16 of plate 2.

Two seemingly similar specimens with identical cyst outline and wall ornament were illustrated.

However, Williams et al. ( 2015) placed these two specimens into two different genera because they deduced a difference in archaeopyle type.

According to Williams et al. ( 2015) the specimen illustrated in plate 1 has an equiepeliform archaeopyle, and, according to their scheme, is to be placed in Sophismatia, while the specimen illustrated in plate 2 exhibits a hyperepeliform archaeopyle and is therefore to be assigned to another genus, i.e. Sagenodinium.

However, the specimen in plate 1 is oriented in oblique polar view, while the specimen in plate 2 is photographed in equatorial view.

The oblique polar view results in an underestimation of the height of the archaeopyle relative to its width, giving the impression of an equiepeliform archaeopyle.

This example also supports the inference that two cysts that are as similar as these two specimens should be assigned to the same species, or at least the same genus, based on outline and ornamentation, even if the archaeopyles differ slightly (see Section 2.2).


The practical application of taxonomic concepts should be reconsidered when generic assignment is easily influenced by analytical issues, such as the angle of view.

Even more crucially, taxa with identical cyst outline and wall ornamentation, such as the above examples, cannot be classified to the genus level if the archaeopyle type cannot be determined, which is often the case in Wetzelielloideae.

Our example given here clearly points to the ambiguity induced by the taxonomic concepts proposed.


Williams et al. ( 2015) argued that some species within Wetzeliella (notably W. articulata) have a generic species definition and as such have a long stratigraphical range.

The proposed revision aims to add more stratigraphical importance to such long-ranging species.

Interestingly, even after the proposed taxonomic revision, Wetzeliella articulata remains a species with a rather broad taxonomic description and a long stratigraphical range.


There are, however, numerous examples where species within the Wetzelielloideae, well defined within the original taxonomic framework, represent clear, unambiguous stratigraphical markers, such as; Apectodinium augustum at the Paleocene–Eocene Thermal Maximum (e.g. Sluijs et al. 2007) [12]; Charlesdowniea edwardsii, Dracodinium waipawaense and Wetzeliella samlandica in the early Eocene (Hollis et al. 2009; Hollis et al. 2012; Bijl et al. 2013a, b; Dallanave et al. 2016) [9][13][14][15]; Dracodinium rhomboideum, Dracodinium pachydermum and Charlesdowniea columna in the middle Eocene (Eldrett et al. 2004; Eldrett & Harding 2009; Firth et al. 2013) [16][17][18]; and Wetzeliella gochtii and Rhombodinium perforatum in the Oligocene (e.g. Pross 2001; Fensome et al. 2008; Pross et al. 2010; Sliwinska et al. 2012; Egger et al. in press) [2][19][20][21][22].

Williams et al. ( 2004) published a cornerstone stratigraphical article in which many wetzeliellioid dinoflagellate cyst species are listed as good biostratigraphical markers including Charlesdowniea columna, C. crassiramosa, C. edwardsii, Dracodinium condylos, D. politum, D. varielongitudum, D. waipawaense, Rhombodinium draco, R. perforatum, R. porosum, Wetzeliella gochtii, W. meckelfeldensis and Wilsonidium echinosuturatum [23].


If we accept the proposed taxonomic revisions, the stratigraphical ranges of many of these species may need to be seriously reconsidered and, in the worst case, may become practically useless if we do not allow for some plasticity in archaeopyle type.

The stratigraphical ranges of species with in theory a stable archaeopyle type and morphology will remain unaffected by the taxonomic revision.


However, we cannot be certain that these species really have stable archaeopyle types, as this has never been the primary criterion to distinguish genera or species.

Therefore, it would require a thorough revisiting of the stratigraphical records where species were initially stratigraphically calibrated to verify whether, according to the taxonomic concepts of Williams et al. ( 2015), the stratigraphical calibration of the species is still correct, or whether the species which were initially grouped together now need to be separated based on a different archaeopyle type.


Contrary to Williams et al. ( 2015), we thus see no improvement in the stratigraphical applicability of Wetzelielloideae in the revised taxonomic concepts.


We recognise that dinoflagellate cyst taxonomy is imperfect for all groups, including the Wetzeliellioideae, and that there is a constant need for improvement.

Williams and colleagues are profound experts in this field and their countless high-quality contributions are invaluable.

However, based on the material we have observed, we find the variability and plasticity of cyst-wall and archaeopyle morphology within the Wetzelielloideae equally large, but render the cyst-wall morphology in practice a much more practical criterion for taxonomic differentiation than archaeopyle type, and more in line with that within other families.

The above considerations on the taxonomic revisions proposed by Williams et al. ( 2015) lead us to propose to retain the taxonomic concepts within Wetzeliellioideae that existed prior to their contribution.


The paper by Williams et al. ( 2015) concerning a proposed taxonomic revision of the subfamily Wetzelielloideae has led to a Comment by Bijl et al. ( 2016) that questions the validity of our assumptions regarding recognition of the equiepeliform, latiepeliform, hyperepeliform and soleiform archaeopyle types and their significance at the generic level.

In this response we address the points that they raise, which are: the introduction of taxonomic criteria allegedly not followed in other fossil subfamilies; the erection of too many taxa; the unworkable nature of the proposed classification; and the reduction of stratigraphic applicability of many significant stratigraphic marker species.

We have organized our response under the following topics: pragmatism versus theory; generic criteria: intergroup consistency; the genus Apectodinium and operculum attachment; stratigraphic utility; the number of taxa; and recognition problems.

We also discuss specimens illustrated in the two plates included with the Comment.

The variations in archaeopyle shapes and types of attachment of the operculum (the latter concept has been modified following more recent research) that we have used in part to separate the genera within the Wetzelielloideae have been previously applied to other peridiniaceans subfamilies, most notably the Deflandreoideae.

As with that subfamily, we consider that our focus on archaeopyle shape and operculum attachment for differentiating wetzelielloidean genera introduces an approach that may help refine the stratigraphic ranges of individual species.

While it is a fundamental truth that there are no “correct” taxonomic ideas, we consider that new approaches should be tested with usage over time, not rejected out of hand prior to careful study.

Bijl et al. ( 2016) raise several objections to the new classification of the Wetzelielloideae that was presented in Williams et al. ( 2015), in which we emphasized the primary importance of archaeopyle outline and the secondary importance of wall morphology and ornamentation in distinguishing genera.


The proposed reclassification led to the erection of thirteen genera and three species, a number which could be regarded as intimidating.

In cataloguing their concerns in the abstract, Bijl et al. state that the proposed revision: introduces taxonomic criteria that divert [diverge] drastically from criteria in other dinocyst subfamilies; unnecessarily erects and emends many genera and species; poses serious analytical and practical limitations; leads to profound reduction of the stratigraphic applicability of many marker species.

Although Bijl et al. raise these four concerns in both the abstract and the introduction, they are not clearly organized in section 2 of their main text.

In our response we have decided to follow a format that responds to the points raised above in a more logical fashion, albeit collectively addressing the issues raised.

Bijl et al. ( 2016, p. 2*) entitle their Section 2.1 “Pragmatic versus hypothesized evolutionary lineages”, implying that our proposals are superficially based. But we deliberately did not propose any lineages in our paper and strongly discourage such an approach.

As we suggested, dinocyst species interpreted from the fossil record represent tips of an “evolutionary bush”, and detailed attempts to arrange fossil species into lineages are, in our view, largely meaningless. What we did present (Williams et al. 2015, fig.


6) was an informal cladogram (and labelled as such) speculating on broad relationships among wetzelielloideans and focussing on archaeopyle type (further discussed below).

As is well established and fundamental in the biological literature, cladograms reflect potential relationships, not lineages (Wiley et al. 1991).

(* In writing this response the final pagination for Bijl et al. ’s article was not available to us, so the page numbers we give are for the online version, which has pages numbered 1 to 7.) The cladogram was added late to our paper as an afterthought at the prompting of a reviewer, so our generic classification was not driven by theory as reflected in that diagram.

Indeed, our proposals are based on our long practical experience (Williams and Downie 1966; Damassa 1979; Bujak et al. 1980; Fensome et al. 2009; Weston et al. 2012; Fensome et al., 2016; Nøhr-Hansen et al. in press).


We would be the last to claim that our extensive observations make our taxonomic ideas correct or better than others ― indeed, taxonomy is a subjective discipline and no scheme can be considered “correct”. But our wealth of practical experience undermines the charge that our ideas are based on theory.

Although our proposed classification is founded on many years of incremental observations, the following anecdote helps emphasize the practical nature of our ideas.

One of us spent several years analyzing Late Cretaceous and Cenozoic assemblages from the Scotian Basin, offshore eastern Canada (Fensome et al. 2008, 2009).

Wetzelielloids are relatively common in many assemblages from Paleogene strata in the Scotian Basin, but it was puzzling that specimens with a clearly “popped-out” epeliform archaeopyle like those in Williams and Downie’s (1966) classic wetzelielloid study were rarely if ever observed; all Scotian Basin wetzelielloids showed a soleiform archaeopyle or no clearly evident archaeopyle.

This mystery was dramatically underlined during a visit to view the Williams and Downie holotypes at the Natural History Museum in London; most if not all wetzelielloids in the latter material strikingly had an epeliform archaeopyle.

It turns out that the Early Eocene is mostly missing in the Scotian Basin, probably stripped during the Montagnais impact event some 50 million years ago (Weston et al. 2012; Deptuck and Campbell 2012).

Here then is a “first pass” practical biostratigraphic observation ― wetzelielloids with an epeliform archaeopyle are primarily Early Eocene in age, whereas assemblages dominated by soleiform archaeopyles are of later Eocene and Oligocene age.

Bijl et al. ( 2016, p. 2) are concerned that “drastic revisions of the primary criteria for taxonomic classification … do not reflect phylogenetic significance.”


However, as further discussed below, we do not consider that our revisions are so “drastic”: we just emphasized one factor, the archaeopyle shape, over others.

Fensome et al. ( 1993) recognized that tabulation is a principal criterion in establishing phylogenetically based dinoflagellate taxa ― indeed the primary criterion among dinoflagellate taxa represented in the fossil record.

This tenet is now generally accepted.

The problem among peridinioids is that the tabulation is so stable, with the “standard peridinialean tabulation” among fossil peridiniaceans (in contrast to protoperidiniaceans) varying little from the Late Jurassic to the Miocene (Fensome et al. 1993).

The priority consideration in classifying fossil peridiniaceans has been the archaeopyle ― both in terms of the number and configuration of plates involved and the shape of the second anterior intercalary (2a) plate, as discussed in detail below.

The defining character of the Wetzelielloideae is the presence of a four-sided, or quadra, 2a plate, in contrast to the hexa, or six-sided, 2a plate of “mainstream” peridiniaceans.

To us, the most reasonable basis for generic definitions would be to use aspects of tabulation if possible, to which end we applied the shape of the 2a plate as reflected in the archaeopyle.

Thus, definitions of family, subfamily and genera all have a basis in the tabulation, and within the Wetzelielloideae this follows the precedent applied at least partially in other peridiniacean subfamilies.

We accept that the shape of the wetzelielloidean 2a plate as shown by the archaeopyle may not reflect exactly the shape of the 2a plate in the motile cell (although no such motile cells exist to confirm this).

However, in our experience, the configuration of the archaeopyle in wetzelielloideans correlates more with geological age than does the overall shape of the cyst.


Do Bijl et al. really consider that archaeopyle shape is potentially less reflective of phylogenetic relationships than horn development or ornament? Among fossil dinoflagellates, these features have been shown time and again not to accord with phylogeny.

For example Cornu and Monteil in Monteil (1991) identified four morphological stages, or ecotypes, in the Muderongia-Phoberocysta complex based on variations in horn length, process type, and the distribution of ornament, including the extent to which it reflects tabulation.

They showed that these morphological variations reflect environmental rather than evolutionary factors.

The genera Oligosphaeridium and Hystrichosphaeridium were often considered to be closely allied in early work on fossil dinoflagellate cysts because of their strikingly similar chorate morphology.

But Evitt (1985) convincingly showed by detailed examination of the process arrangement (reflecting tabulation) that the two genera belonged to different fundamental groups of gonyaulacoid cysts, recognized by Fensome et al. ( 1993) as the families Gonyaulacaceae and Goniodomaceae.

These and other examples show that assessing phylogenetic relationships on the basis of superficial shape and wall structure is fraught with problems.

Aspects relating to tabulation have been proven generally not so susceptible to pitfalls of evolutionary convergence.

According to Bijl et al. ( 2016, p. 1), Williams et al. (


2015) introduced “… taxonomic criteria that divert [i.e. diverge] drastically from well-established conventions” and that (p. 4) a “profound concern for the field of dinoflagellate cyst paleontology” is that Williams et al. ( 2015) break with the “basic principle of hierarchy in morphological variation for the Wetzelielloideae ….” What exactly are the “well-established conventions” and the “basic principle of hierarchy in morphological variation” referred to by Bijl et al. from which we have diverged and broken?

To assess this issue, let’s look at the definitions of wetzelielloidean genera as established prior to Williams et al. ( 2015).

The genus Wetzeliella itself was erected by Eisenack (1954, p. 187), who gave the following circumscription: “Shell more or less flattened, rhomboidal to pentagonal or also more or less oval, usually with apical horn, lateral horns on both sides and two antapical horns, all of which can be strongly reduced, without tabulation, almost always ornamented with bristles or spines.

Transverse and longitudinal furrows, respectively, not determinable as flagellar groove (the former perhaps indicated sometimes).

Ellipsoidal capsule present interiorly.

” ( Translation from the German by Stover and Evitt (1978, p.130.) An excystment opening (later termed an archaeopyle) was not recognized in 1954 by Eisenack, an omission remedied by Williams & Downie (1966, p. 182), who stated “Archaeopyle usually present … resulting from loss of plate 2a.

” Gocht (1955) erected Dracodinium and Rhombodinium.


Dracodinium was differentiated from Wetzeliella in lacking an apical horn on the pericyst, although there could be a slight protuberance.

Subsequent authors (e.g. Williams & Downie 1966 by implication and Lentin & Williams 1976) considered Dracodinium to be a taxonomic junior synonym of Wetzeliella. But Costa & Downie (1979) and Lentin & Williams (1989) retained Dracodinium.

Gocht (1955) differentiated Rhombodinium from Wetzeliella on its lack of ornamentation.

Alberti (1961) considered Rhombodinium to be a subgenus of Wetzeliella, but subsequent authors (e.g. Lentin & Williams 1977) retained Rhombodinium at generic rank.

The genus Kisselevia, although originally invalidly proposed (as Kisselovia) by Vozzhennikova (1963), was validated by Vozzhennikova (1967) (see Fensome and Williams 2004 for nomenclatural history).

Vozzhennikova’s (1963) concept appears to have encompassed forms that we would now consider as wetzelielloideans with a smooth or reticulate wall, with or without spinules “in modal connections” (based on translation in Stover and Evitt 1978, p. 110).

Vozzhennikova (1967) restricted Kisselevia to forms with a reticulate or reticulate-spinose wall (based on translation in Stover and Evitt 1978, p. 110–111).

Stover and Evitt (1978, p. 111) stated that “Kisselovia [i.e. Kisselevia] differs from Wetzeliella in having all or some of the intratabular groups of processes covered by pieces of ectophragm whose outlines approximate the shapes of paraplates.

” Stover and Evitt’s concept was thus somewhat different from Vozzhennikova’s, and after restudy of the type, Lentin & Vozzhennikova (1989) restricted the genus to forms with a reticulate periphragm and neither processes nor ectophragm.

For wetzelielloideans with processes connected distally by trabeculae or ectophragm, Lentin & Vozzhennikova proposed the genus Charlesdowniea.

Lentin & Williams (1976) erected Wilsonidium for wetzelielloideans with sutural ornamentation.


In the same year, Costa & Downie (1976) erected Apectodinium as a subgenus of Wetzeliella on the basis of a pericoel that was absent or restricted to the bases of the horns, a thin endophragm, identical periarchaeopyle and endoarchaeopyle, and an overall size less than other taxa within the Wetzeliella group (i.e. the Wetzelielloideae).

Apectodinium was raised to generic rank by Lentin and Williams (1977).

As Apectodinium has a pivotal place in the present discussion, we discuss it further in a separate section below.

The proposal of Gochtodinium by Bujak (1979) is especially significant in that it was the first genus in the group to be based on archaeopyle morphology, in this case a soleiform archaeopyle.

However, Lentin and Vozzhennikova (1989, p. 219) stated that they could not accept a genus based solely on the presence of a soleiform archaeopyle.

Oddly, in inadvertent support of our position, Lentin and Vozzhennikova additionally stated that “… it appears that the presence of a soleiform archaeopyle is an intraspecific variation which may be stratigraphically controlled ….

” Unrecognized at the time is that the type of Wetzeliella, an Oligocene specimen, also has a soleiform archaeopyle (RAF personal observation), and so we also consider Gochtodinium to be a taxonomic junior synonym of Wetzeliella.

In Fensome et al. ( 2009), the present authors erected two genera Talladinium and Axiodinium, based in large part on archaeopyle morphology.

Thus, prior to our 2015 paper, wetzelielloidean genera were based on a variety of criteria, ranging from wall structure to archaeopyle type, but we see no “well-established conventions” or “basic principle of hierarchy in morphological variation”. And what do Bijl et al. ( 2016, p. 1) intend when they recommend that “we propose to retain the generic definitions of Wetzelielloideae that existed prior to the revisions by Williams et al. (


2015) until a revision supported by the community is available”.

Which particular prior definitions do they mean? Presumably they would not accept the new genera (Axiodinium and Talladinium) proposed in Fensome et al. ( 2009).

In a similar vein, Bijl et al. ( 2016, p. 2) state: “Taxonomic definitions at the generic level are made predominantly based on specific morphologic and geometric features (such as cyst outline, cavation, number of wall layers, process outline and distribution, plate and/or sutural ornamentation, etc.), with the archaeopyle type being a consequence of geometry.

Williams et al. ( 2015) broke with this convention because they specifically consider [sic] archaeopyle type to be an indicator for phylogeny.” On the contrary, using archaeopyle morphology to define higher level taxa (i.e. above species) seems to us a well-trodden path among dinoflagellate-cyst taxa.

That archaeopyle morphology had largely not been used to define wetzelielloidean genera would seem more the exception to us.

Tabulation is fundamental to higher-level classification among fossil dinoflagellates, but among forms with a similar overall tabulation, aspects of archaeopyle developments or its reflection in particular plates, has commonly proven critical, as demonstrated in Fensome et al. (


Take, for example, the goniodomacean genera Homotryblium and Hystrichosphaeridium.

If one relied on ornamentation for generic differentiation, species of these two genera would be included in a single genus, with Hystrichosphaeridium being senior.

However, the genera can be distinguished through the development of an apical archaeopyle in Hystrichosphaeridium and an epicystal archaeopyle in Homotryblium.

Consider how much stratigraphic and paleoenvironmental information would be lost if the two genera were not separated (Dybkjaer 2004).

Among the peridiniaceans, genera in the subfamily Deflandreoideae are widely defined by archaeopyle size and shape, a reflection of the nature of the second anterior intercalary (2a) plate.

For example Chatangiella is defined by an omegaform hexa 2a plate, Alterbidinium by an iso-to stenodeltaform 2a, Cerodinium by an iso-deltaform 2a, Deflandrea by a latideltaform 2a, and Lentinia by a very large isodeltaform 2a.

These archaeopyle traits clearly have biostratigraphic, and surely evolutionary, significance.

That the archaeopyle shape consistently reflects geometry is also belied by the fact that some specimens otherwise attributable to Chatangiella (with broad “shoulders”) have a deltaform hexa archaeopyle, not an omegaform one (GLW and RAF unpublished observations).

Bijl et al. ( 2016, p.2) contend that we “applied the basic assumption that the archaeopyle type directly reflects the shape of the plate(s) involved”, citing Harland (1982) as proof of this statement.

However, Harland was studying protoperidinioids, which are notoriously variable in tabulation and archaeopyle development.


While we accept that archaeopyles may not reflect the shape of equivalent plates on the motile stage in some cases, surely the archaeopyle type must to some extent reflect plate dimensions and shape.

For example, it is hard to visualize a latiepeliform archaeopyle representing loss of a plate of identical dimensions to that of a hyperepeliform archaeopyle. And even if, for example, a soleiform archaeopyle does not exactly match the shape of the 2a plate in the motile cell, why could this not be a valid generic and phylogenetic criterion in itself, as its stratigraphic distribution clearly suggests to us that it is? Another argument advanced by Bijl et al. is that the use of the archaeopyle splits otherwise identical taxa.

For example, Bijl et al. ( 2016, p. 2) state that… “subtle differences in outline and ornament between Charlesdowniea columna and Charlesdowniea coleothrypta makes it difficult to separate them from one another ….” In the context of the current discussion, Daniel Michoux (personal communication) has stated that he disagrees with Bijl et al. ’s statement “… referring to the differences in outline and ornament between Charlesdowniea columna and Charlesdowniea coleothrypta as ‘subtle’.

As the author of C. columna, I consider the difference to be perfectly clear and these two species easy to distinguish.

” ( Any future discussion about these two species should also involve the closely similar species Wetzeliella? clathrata, which we consider to have a soleiform archaeopyle.)


In actuality our proposals should simplify differentiation, since the primary distinguishing feature would be recognizing whether the archaeopyle is equiepeliform or latiepeliform or, in the case of Wetzeliella? clathrata, soleiform.

The problem of clearly separating species is widespread among fossil dinoflagellates and is equally true if criteria such as ornamentation, wall structure, pericoel development and the degree of expression of tabulation are involved; all have been used to define wetzelielloidean genera.

Our revised concepts highlight this issue anew, but do not make it a greater or lesser problem in general.

Bijl et al. ( 2016, p. 4) make the sweeping statement: “We now observe very chaotic, inconsistent genus and species concepts, in which species with the same wall features are placed in multiple genera just because of a slight, non-diagnostic difference in archaeopyle type.

” This might be a valid criticism point if both Charlesdowniea (now Piladinium) columna and Charlesdowniea coleothrypta had the same stratigraphic distribution.

However, a single specimen should never be used to determine the age of the assemblage.

In such cases, if most specimens show one type of archaeopyle and its occurrence is consistent with the ranges of other markers in the assemblage, wouldn’t it would be biostratigraphically useful to make the split based on archaeopyle style?

Bijl et al. ( 2016, p. 2) end their section 2.1 with the confusing sentence: “Regardless of our concerns, the revision of taxonomic concepts to accommodate just one subfamily seems an illogical step if the taxonomic concepts applied towards the other dinoflagellate cyst groups remain the same.” Their contention (p. 6) that “… the cyst-wall morphology [is] in practice a much more practical criterion for taxonomic differentiation than archaeopyle type, and more in line with that within other families” is in our experience untrue.


Just as Evitt (1981) famously wrote “… dinoflagellates did it differently …”, so each “group” within the dinoflagellates “did it differently” ― one “size” does not fit all.

( Bijl et al. mix “subfamilies” and “groups” in the quoted sentence; we will use “group” in the sense of any combination of genera that have been identified as constituting a family, subfamily or less formally recognized set of genera with similar morphology … for example, the areoligeraceans Cyclonephelium, Tenua, Cerbia, Circulodinium, Cassidium, Canningia and Canninginopsis could be considered the Cyclonephelium group.) Thus, for a group like the subfamily Palaeoperidinioideae, which expresses an extremely stable standard peridinialean tabulation, genera are defined on the number and arrangement of plates involved in archaeopyle formation.

For example Chichaouadinium is based on the removal of the 2a plate and the incomplete separation of all surrounding plates, whereas Palaeoperidinium is based on the removal of all dorsal plates on the epicyst in a single opercular piece or as a flap adnate at the cingulum.

In the Cyclonephelium group, or indeed the family Areoligeraceae as a whole, not only is the tabulation extremely stable but so too is the nature of the archaeopyle; so for classification we have no choice but to resort to features of the wall structure and ornamentation for generic definitions.

It seems obvious to us that evaluating separate groups on their own internal merits leads to both a more practical generic breakdown and a potentially more phylogenetically meaningful one.

In Williams et al. ( 2015) we defined Apectodinium as wetzelielloidean cysts with an equiepeliform archaeopyle, periphragm and endophragm thin and appressed except sometimes under the horns, and a pericyst with processes that are distally free.

To differentiate circumcavate, thicker-walled forms with an equiepeliform archaeopyle Fensome et al. ( 2009) erected the genus Axiodinium.

Costa and Downie (1976, p. 608) considered Apectodinium to be “related to the original stock from which most other wetzelielloid species derived”.


The genus is an enigma.

As noted by Bijl et al. ( 2016), the archaeopyle of Apectodinium can be variable, sometimes including the 4” plate and also sometimes being adnate.

It is not surprising that if the 4” plate can be involved in archaeopyle formation in Apectodinium, that the operculum could be adnate.

In their critique of Williams et al. ( 2015), Bijl et al. place particular emphasis on Apectodinium, although this genus is atypical of the subfamily as a whole.

The problem is perhaps that Apectodinium, as the probable precursor to other wetzelielloideans, was “experimenting” with the mode of archaeopyle formation.

Similar experimentation is also shown by palaeoperidinioideans in the Albian to early Cenomanian, where otherwise morphologically similar genera such as Luxadinium, Laciniadinium, Ovoidinium and Epelidosphaeridia, show variability in the archaeopyle type and the presence of a free versus attached operculum.

In terms of attached versus free opercula, Williams et al. ( 2015) were incorrect in making the statement that the operculum in equiepeliform, hyperepeliform and latiepeliform archaeopyle types is always unattached.

We now consider the degree of detachment of the operculum is variable, as demonstrated by Iakovleva (2016).


Thus, we accept the modified definitions of the archaeopyle types proposed by Iakovleva, who emphasized that the soleiform type involves an archaeopyle formed by a generally inverted omegaform 2a plate, with the operculum consistently attached anteriorly.

That cysts at various stages of excystment must be preserved explains why in some cysts an archaeopyle does not appear to be present.

There is obviously variability in the outline of the archaeopyle in Apectodinium, which is why we had difficulty in deciding how to fit it into the overall scheme.

The specimens of Apectodinium hyperacanthum illustrated in Bijl et al. with the attached operculum would remain in Apectodinium following the redefinition of the epeliform archaeopyle by Iakovleva (2016).

This emendation is also applicable to the hyperepeliform and the latiepeliform archaeopyle.

But the soleiform archaeopyle is unique, again following Iakovleva’s findings.

One of the main criticisms that Bijl et al. ( 2016, p. 1)) make regarding Williams et al. ( 2015) is that the paper “… unnecessarily erects and emends many new genera and species.

” In fact, we proposed only three new species and did not emend any existing ones, but we acknowledge that 13 new genera is a lot for a single paper.

The logic for creating so many genera was to provide a framework for testing the validity of the model in which we consider archaeopyle type as the first order hierarchical character.


Our approach did not nullify the importance of surface ornamentation at the generic level; we did indeed use ornament type and arrangement, as well as wall structure, as secondary criteria.

Another concern that Bijl et al. ( 2016, p. 4) express is that “The orientation of the cyst relative to the plane of view poses a serious limitation on the practicality of the proposed criteria underlying the revision.

” Well-orientated specimens are a key asset in species assignment, regardless of which morphologic features are diagnostic.

This problem is demonstrated in the two specimens illustrated in Williams et al. ( 2015, pl.

1, fig. 15 and pl. 2, figs. 15–16); following previous criteria used to separate species of the wetzelielloideans, these specimens would be included in the same species, or at least the same genus.

But taking into account the nature of the archeopyle, one specimen is assignable to Sophismatia (pl. 1, figs.15) and the other to Sagenodinium franciscanum (pl.2, fig.15–16).


Orientation to reveal key morphologic features is more of a problem in some fossil dinoflagellate genera than others.

In the wetzelielloideans, the dorso-ventral compression of most specimens determines that when mounted on a slide, they will be orientated predominantly in that plane. If there is some doubt about one specimen, another specimen of the same species can be sought.

Since ages are rarely based on single specimens, this should not pose an insurmountable problem.

Similar problems occur in other dinoflagellate-cyst taxa: witness the difficulty of confirming the identity of species of Batiacasphaera when they are orientated so that the archaeopyle looks precingular.

Recognition of wetzelielloideans that do not appear to have an archaeopyle can be frustrating, but usually a few with some indication of an opening can be found on a slide.

There may be an explanation for this paucity of specimens in some samples that do not appear to have an archaeopyle.

One possibility is that most or all of the specimens possess a soleiform archaeopyle and the operculum has fallen back into place.

Another is that the sea floor in shallow marine paleoenvironments was anoxic, and therefore prevented excystment.

Regarding the specimen illustrated in Williams et al. ( 2015, pl.

1, fig.


2), Bijl et al. ( 2016, p. 4) state that “The oblique polar view results in an underestimation of the height of the archaeopyle relative to its width, giving the impression of an equiepeliform archaeopyle”.

A primary feature of the equiepeliform archaeopyle is that it does not extend into the apical pericoel, unlike the hyperepeliform archaeopyle.

With this specimen, we thought that the archaeopyle did not extend into the apical pericoel, but we could have been wrong in our interpretation.

Observations on other morphologically similar specimens in the same assemblage would solve this riddle.

Bijl et al. ( 2016) also objected to emphasis on archaeopyle type because it is difficult to consistently see the details of this feature.

This can be due to: poor optical contrast; orientation; lack of penitabular or parasutural ornamentation; too many processes; partial adnation; some cysts not having excysted; quality of preservation; and the presence of obscuring debris.

These are universal concerns in studies of all fossil dinoflagellate groups but can usually be overcome with patience in searching for other specimens.

Bijl et al. ( 2016, p. 1) state that our proposals will “... lead to profound reduction of the stratigraphic applicability of many marker species….” Firstly, Bijl et al.


are confusing taxonomy with stratigraphy. And secondly, generic assignments rarely have an impact on stratigraphic ranges of species, with the exception of such species as Wetzeliella articulata, as discussed below. As Williams et al. ( 2015) did not generally modify species or species concepts, nothing has changed to affect stratigraphic ranges of most of the species.

Admittedly, the refinement of generic concepts will make some species more tightly constrained morphologically; for example Wetzeliella articulata should now have a shorter range than previously assessed, but this still has to be tested because the current generally published range is based in part on what we would now consider misidentifications.

We fail to understand why tighter morphological circumscriptions leading to potentially more restricted stratigraphic ranges would be detrimental to biostratigraphy.

The ranges of the bulk of wetzelielloidean species remain the same: no one would argue that, for example, Apectodinium augustum has a well-defined, restricted stratigraphic range (whether as Apectodinium or Axiodinium).

What strikes us most is that the majority of species have not been transferred from their previous generic assignments.

Bijl et al. ( 2006, p. 1) fault Williams et al. ( 2015) for “…not introducing any new stratigraphic markers in replacement.” However, the intent of our paper was not to introduce stratigraphic markers but to present a new taxonomic treatment for the Wetzelielloideae, emphasizing the variations in archaeopyle type.


We understand that it might be considered annoying to have to change generic names for species that are well embedded in zonation schemes. Does this mean that there should be a moratorium on taxonomic treatments of such names? In our view, wetzelielloidean taxonomy prior to our 2015 revision was not serving applications such as biostratigraphy well, and needed an overhaul using the full range of morphological criteria in a coherent and internally consistent scheme.

We continue to think that our scheme, with thoughtful modifications such as those introduced by Iakovleva (2016), will achieve this goal if sincerely tested.

To substantiate some of their points regarding the supposed impracticability of the revisions to the Wetzelielloideae proposed by Williams et al. ( 2015), Bijl et al. ( 2016) include two plates; however, some of the specimens illustrated seem to be of questionable value in making their case.

The specimens illustrated in Bijl et al. ( 2016, pl.

1, figs. 1–3) are all considered to belong to Rhombodinium porosum but apparently show variability in archaeopyle type ranging from “hypersoleiform to ? epeliform”.


The first problem is that Williams et al. ( 2015) used the term equiepeliform archaeopyle rather than epeliform archaeopyle.

The second concern is that both the specimens shown in their plate 1, figures 1–2 have soleiform archaeopyles.

Figure 3 appears to be latiepeliform.

However, it is unusual in that the operculum may still be attached but pushed into the endocyst.

Are these three specimens from the same sample and is there any evidence of reworking?

Their plate 1, figures 4–6 purport to show specimens of Apectodinium that possess an archaeopyle involving the 4” plate as well as the 2a plate.

However, we do not find that plate 1, figures 4 and 5 convincingly show the involvement of the 4” plate.

Moreover, the nature of the archaeopyle of the specimen illustrated in plate 1, figure 6 is difficult to determine.

Plate 1, figures 7 and 8 are specimens of Wetzeliella symmetrica, the former with a soleiform and the latter with a “(slightly?) hypersoleiform archaeopyle” respectively.

We consider that figure 8 shows a specimen with a soleiform archaeopyle.


But regardless, it seems to be splitting hairs to regard it as “(slightly?) hypersoleiform”.

Figure 9 does not show a specimen with a posteriorly attached operculum but rather one with an anteriorly attached operculum.

Bijl et al. ( 2016) assign the specimens illustrated in plate 1, figures 10 and 11 to Rhombodinium draco, but state (in the caption, p. 3) that they “should be considered a (new?) species of Rhadinodinium according to Williams et al. ( 2015)” and that the “archaeopyle [in their figure 10] shows clear signs of rupture of the (likely) once soleiform archaeopyle.

When it becomes questionable whether an operculum is secondarily ruptured or primarily attached/detached, speciation on a genus level becomes impossible if too much emphasis is given to the archaeopyle type for classification”.

First of all the authors are implying that one has to confirm the archaeopyle type in every specimen seen.

Secondly, many genera among fossil dinoflagellates rely on recognition of the archaeopyle before they can be identified: examples are Hystrichosphaeridium and Homotryblium, Exochosphaeridium and Pervosphaeridium, and Spinidinium and Chichaouadinium. And some genera are difficult to name unless you have an apical or lateral orientation; an example is Batiacasphaera, which in most views, as noted previously, looks as though it has a precingular archaeopyle.

In their plate 2, Bijl et al.


illustrate specimens “that do not clearly show an archaeopyle type and, therefore, are impossible to classify on the genus level using the proposed taxonomic concepts of Williams et al. ( 2015).” Again, how many times do you clearly discern an archaeopyle in a single specimen, even though it may be the key to its classification?

The archaeopyle may not be developed because there was no excystment or it may be difficult to determine the type because of the orientation of the specimen, or because the operculum is partially attached (as highlighted by Iakovleva 2016) and has fallen back into place.

Their plate 2, figures 1 and 2 are identified as Apectodinium homomorphum.

This species tends to be common to abundant in samples, so determination of archaeopyle type should not pose a problem. And under light microscopy, the thin-walled endocyst and its adherence to the pericyst, except where underlying the horns, would immediately reveal its identity.

We agree that, as illustrated, plate 2, figure 3 is impossible to speciate, although Bijl et al. label it as Apectodinium homomorphum.

As we have stated above, this species is common in some assemblages, especially around the Paleocene–Eocene boundary, so finding specimens that show an archaeopyle should not be difficult in a productive sample.

We think that the specimens illustrated in figures 4 and 5 have soleiform archaeopyles, but the quality of the illustrations precludes positive confirmation.

Other specimens in the sample would probably provide the needed evidence.


The operculum is not posteriorly attached, as it should never be in this category Following Williams et al. ( 2015), we would include the specimen illustrated in Bijl et al. ’s plate 2, figure 6 in Vallodinium, even though the operculum is still in place: that is because the 2a plate in this specimen is clearly equiepeliform.

As Iakovleva (2016) has demonstrated, the operculum can be attached in the equiepeliform group.

The archaeopyle of the specimen illustrated in plate 2, figures 7–9 and identified as Wetzeliella symmetrica looks latiepeliform.

That being so, the specimen should not be in situ in the Oligocene and thus may be reworked.

We wonder if there are any other specimens with similar morphology in the sample.

One wonders how many palynologists would agree with the assignment of the specimens illustrated in plate 2, figures 4–5, 7–10 to Wetzeliella symmetrica.

Enhancing the stratigraphic and paleoenvironmental value of fossils are major goals of paleontologists, and most accept that taxonomy should be supportive of those pursuits while at the same time reflecting phylogenetic relationships insofar as possible.

To achieve such a meaningful and internally coherent subdivision of a group (e.g. subfamily) a consistent hierarchy of factors is required, as is the need for flexibility of criteria between groups.

That said, taxonomy should never be considered “written in stone”; taxonomy is a subjective pursuit, and no individual practitioner is obliged to follow the schemes proposed by colleagues (in contrast to nomenclature, which has definite rules that must be followed).

Thus, Bijl et al. (


2016) are free to use whatever taxonomic scheme they prefer. What is apparent and disappointing to us is that they wrote their paper opposing our long-considered ideas without trying them out ― a few months is obviously not enough time to test what we agree is a new approach to the wetzelielloidean taxonomy.

Moreover, they imply that they are speaking for a broader community, writing (p. 1) that “… we propose to retain the generic definitions of Wetzelielloideae that existed prior to the revisions by Williams et al. ( 2015), until a revision supported by the community is available” [underline added here].

Who would be a member of the community that would give approval to any future taxonomic proposals for the Wetzelielloideae and what are the necessary qualifications for membership of said community? Of course it is the most fundamental tenet of science that ideas be reviewed, debated, and if necessary rejected. But in our view, taxonomic ideas need to be properly tested over time; and new ideas should be encouraged, regardless of whether or not they are eventually followed.


Diabetes is a major cause of morbidity and mortality in the United States. It is the seventh leading cause of death (Aubert, Herman, Waters, Moore, Sutton, Peterson et al., 1998), and the cost of medical care is $100 billion annually (Caravalho & Saylor, 2000).

Approximately 15 million adults are living with diabetes, and the prevalence rates have continued to escalate over the past decade, with racial/ethnic minority populations suffering a disproportionate burden of disease (McBean, Li, Gilbertson, & Collins, 2004).

African-Americans are twice as likely to be diagnosed with diabetes than whites, and are more likely to have poorly controlled diabetes and diabetic complications such as blindness, end-stage renal disease and limb amputation (Bonds, Zaccaro, Karter, Selby, Saad, & Goff, 2003; Gary, McGuire, McCauley, & Brancati, 2004; Harris, 2001).

African-Americans are also more likely to have uncontrolled co-morbid conditions such as hypertension and hyperlipidemia, which increases the complexity of disease management (Brancati, Kao, Folsom, Watson, & Szklo, 2000; Heisler, Smith, Hayward, Krein, & Kerr, 2003; Jha, Varosy, Kanaya, Hunninghake, Hlatky, Waters et al., 2003; Nelson, Norris, & Mangione, 2002).


Positive patient-provider relationships can facilitate diabetes management and potentially reduce diabetes disparities (Greenfield, Kaplan, Ware, Yano, & Frank, 1988; Stewart, 1995).

Persons with diabetes who participate in shared decision-making (where patients actively participate in healthcare discussions and decisions with their physicians) have greater diabetes self-efficacy, participate more in diabetes self-management, and are more likely to adhere to plans of care (Benbassat, Pilpel, & Tidhar, 1998).


Shared decision-making (SDM) has been positively associated with improved diabetes control, enhanced preventive care utilization, lowered blood pressure, fewer hospitalizations, and increased patient satisfaction (Adams, Smith, & Ruffin, 2001; Greenfield, Kaplan, & Ware, 1985; Greenfield, Kaplan, Ware et al., 1988; Lerman, Brody, Caputo, Smith, Lazaro, & Wolfson, 1990; Stewart, Brown, Donner, McWhinney, Oates, Weston et al., 2000).


In its report Crossing the Quality Chasm, the Institute of Medicine stressed the importance of patients having "the education and support they require to make decisions and participate in their own care" (Richardson, Berwick, Bisgard, Bristow, Buck, Cassel et al., 2001).

Since then, SDM has been increasingly advocated by healthcare providers and organizations (Davidson, Powers, Hedayat, Tieszen, Kon, Shepard et al., 2007; Larson, Fihn, Kirk, Levinson, Loge, Reynolds et al., 2004; Michel & Moss, 2005; Richardson, Berwick, Bisgard et al., 2001; Sheridan, Harris, & Woolf, 2004; van der Weijden, van Veenendaal, & Timmermans, 2007).


Unfortunately, results from previous studies show that racial/ethnic minority patients are more likely to experience barriers to communication in patient/physician communication (e.g. shared decision making) as compared to white patients.

For example, African-Americans are more likely to rate their physicians as less participatory than whites, even when controlling for socioeconomic status and duration of the patient-provider relationship (Cooper-Patrick, Gallo, Soc Sci Med.

Author manuscript; available in PMC 2011 July 1.

Manuscript Gonzales, Vu, Powe, Nelson et al., 1999).

Analyses of audio-taped clinic visits document that African-Americans experience shorter outpatient visits and less positive clinical encounters with white physicians including less respect, responsiveness and listening than their white patient peers (Cooper, Roter, Johnson, Ford, Steinwachs, & Powe, 2003; Johnson, Roter, Powe, & Cooper, 2004; Levinson, Hudak, Feldman, Frankel, Kuby, Bereknyei et al., 2008; Oliver, Goodwin, Gotler, Gregory, & Stange, 2001).


Yet, studies examining patients' perceptions of how race affects shared decision-making are limited.

Research in fields outside of medicine suggests that race plays a significant role in communication patterns and interpersonal interactions between African-Americans and whites, particularly in situations of perceived power differences, such as interactions with law enforcement (e.g. police officers, judges, lawyers), commercial retail (e.g. store clerks and restaurant staff) and financial agents (e.g. bank tellers, loan officers) (Gamble, 1997; Purdie-Vaughns, Steele, Davies, Ditlmann, & Crosby, 2008).

Thus, it is likely that a similar paradigm exists for African-Americans' perceptions about communication patterns with physicians.

Jacobs et al. explored physician trust among African-Americans, and noted that trusting relationships were important to some aspects of patient communication, including openness and honesty with one's physician, and decisions to follow treatment recommendations (Jacobs, Rolle, Ferrans, Whitaker, & Warnecke, 2006).


There is also an extensive literature about African-Americans' perceptions about their treatment within healthcare settings, including issues of disrespect and discrimination (Blandhard & Lurie, 2004).

African-Americans are more likely to report experiencing racial discrimination within healthcare than other racial/ethnic groups, with reports ranging from 13-69% in comparison to 1-2% of whites (Ren, Amick, & Williams, 1999; Bird & Bogart, 2001).

Perceived discrimination in healthcare is positively correlated with poor health including depression, self-rated health, days spent unwell in bed, and hypertension (Krieger & Stephen, 1996; Ren, Amick, & Williams, 1999; Bird, Bogart, & Delahanty, 2004).

Self-reports of discrimination have been associated with delays in prescription medication utilization and medical testing/treatment, indicating that such experiences represent an additional barrier to accessing healthcare (Bird, Bogart, & Delahanty, 2004; Van Houtven, Voils, Oddone, Weinfurt, Friedman, Schulman et al., 2005).


This study utilized qualitative methodologies to examine the perceptions of African-American patients with diabetes about the influence of race on patient/physician communication and shared decision-making.

This investigation was guided by SDM models that contain 3 domains (Charles, Gafni, & Whelan, 1997; Peek, Quinn, Gorawara-Bhat, Odoms-Young, Wilson, & Chin, 2008):


1. Information-sharing: The bidirectional exchange of information between patients and their physicians about symptoms, diagnoses and lifestyle issues relevant to choosing a treatment plan.

Patients feel empowered to "tell their story" and have their concerns validated, and physicians provide information using "layman's terms" and in ways that promote patient understanding.


2. Deliberation/Physician recommendation: Physician recommendations for treatment plans are grounded in full disclosure of all treatment options.

Ideally, patient preferences for treatment are elicited and discussed.


Decision-making: Patients and physicians arrive at a treatment plan.

The process has been conceptualized as a joint endeavor that results in mutual agreement about the plan of care.

However, some patients who want a shared role in decision-making may exercise their decisions behaviorally (i.e. adhering or non-adhering to physician recommendations).


This study suggests that race-related barriers may exist to shared decision-making between African-American patients and their physicians.

Finding innovative ways to address such communication barriers and enhance SDM among African-Americans is an important area of research. Because barriers to shared decision-making may exist for patients and providers alike (Peek, Wilson, Gorawara-Bhat, Odoms-Young, Quinn, & Chin, 2009), communication strategies should be developed for both groups.

Extending cultural competency training and general communication training for physicians to address potential race-related barriers to SDM has the potential to enhance shared decision-making among African-Americans.

While patient communication interventions can be effective, only one study has examined the efficacy of such an intervention among African-Americans and it had no demonstrable effect (although it increased patient communication among whites), a finding the authors attribute to the intervention's lack of cultural appropriateness (Greenfield, Kaplan, Ware, Yano, & Frank, 1988; Post, Cegala, & Marinelli, 2001).

Systematic reviews and meta-analyses of diabetes interventions indicate that culturally-tailoring interventions and incorporating behavioral and pyschosocial strategies (versus information transfer alone) have the potential for greater effectiveness (Peek, Cargill, & Huang, 2007; Peyrot, 1999; Anderson, Funnell, Butler, Arnold, Fitzgerald, & Feste, 1995; Brown, 1999).

A recent study reported an increase in diabetes self- efficacy among Hispanic Americans when family members were used to support communication efforts with physicians (Coffman, 2008).

Thus, culturally-tailored communication training for patients may be an effective strategy for increasing SDM among African-Americans with diabetes, particularly if it incorporates patient beliefs and cultural norms, and addresses potential issues of internalized racism.


The methods for this qualitative study have been described in detail elsewhere (Peek, Quinn, Gorawara-Bhat et al., 2008), but are summarized here.

We used a phenomenologic research method that included in-depth, individual semi-structured interviews (n=24) and 5 focus groups (n=27) among African-Americans with diabetes.

Consistent with guidelines of qualitative methodology, we conducted data collection and analysis simultaneously, and continued enrollment until theme saturation was met (Glaser & Strauss, 1967).

A moderator/interviewer experienced in discussing health topics and interpersonal communication was matched to patients on race/ethnicity (Anderson, Barr, Edwards, Funnell, Fitzgerald, & Wisdom, 1996; Jackson, 1991).

Each focus group consisted of 5-6 people and lasted approximately 90 minutes.

Individual interviews lasted approximately 60 minutes.


After receiving approval from our institution's research ethics committee (the Institutional Review Board), study participants were recruited using criterion sampling (Patton, 2002).

Eligible patients included African-Americans with diabetes, ≥ 21 years old who had an established relationship with an attending primary care physician at an academic practice in Chicago, Illinois.

Patients were randomly identified and up to three attempts were made to contact them via telephone.

In addition, culturally-appropriate, low-literacy recruitment materials advertising the study were posted in the clinic waiting room and examination rooms.

Study participants received a $15 gift card to a local grocery store as an incentive.

Patient sociodemographic and clinical information was collected via self-administered surveys immediately prior to the interviews, and was collected anonymously in the focus groups.

Interviews were conducted between September 2006 and February 2007 (response rate of study participation invitations: 67%) and focus groups were conducted between January 2007 and March 2007 (response rate: 57%).


Topic guides were created with the goal of exploring the following: patient definitions and perceptions of shared decision-making, barriers and facilitators of SDM, and the perceived influence of race/culture on SDM.

The guides were informed by constructs of the Charles SDM model (Charles, Gafni, & Whelan, 1997, 1999; Montori, Gafni, & Charles, 2006), the Theory of Planned Behavior (Ajzen, 1991) and the Ecological Model (McLeroy, Bibeau, Steckler, & Glanz, 1988), pilot-tested, and modified in an iterative way.


The guide consisted of a list of open-ended questions and follow-up probes.

Queries about race began with the question 'Do you think that race affects people's relationships with their doctors?' and followed with probes such as 'How exactly might race affect the relationship?' and 'Do you think it matters if the doctor is black or not?' We also asked for situational examples (i.e. 'Can you tell me a situation where race played a role [either good or bad] in communicating with the doctor?'), comparative impressions (e.g. 'Do you think it's easier, harder, or the same for blacks to talk with their doctors compared to whites?' and 'Do you think that doctors treat African-American patients, in general, the same, better, or worse than white patients?'), and SDM barriers and facilitators (e.g. What suggestions would you give to African-Americans who are having trouble 'speaking up' to their doctors?).


Individual interviews and focus groups were audio-taped, transcribed verbatim and imported into Atlas.ti 4.2 software.

A team of five investigators with experience in medicine, public health, and psychology independently reviewed and coded the first transcript, met to discuss codes, and created uniform coding guidelines.

Subsequently, each transcript was independently coded by two randomly assigned reviewers who then met to discuss coding and address discrepancies.

Remaining differences were resolved by the entire group.

A codebook was developed using an iterative process where modifications were made to the codes, themes, and concepts that arose from new transcripts (Morgan, 1997).

The focus groups were subsequently coded in a similar fashion and analyzed separately from the in-depth interviews for additional codes and themes.

Related themes from the analysis were used to develop a conceptual model for understanding the relationship between race and shared decision-making.


The majority of study participants were female (82%) and approximately half were 40 to 65 years old (Table).

Sixty percent of study participants had completed at least "some college", nearly half the study participants were retired and approximately half had private insurance.

No statistically significant demographic differences existed between participants in the in- depth interviews and the focus groups, although participants in the in-depth interviews tended to be older (mean age 66 years vs. 59 years).

The average duration of diabetes was 14 years.


Participants had a variety of views regarding the perceived relevance of race to shared decision- making and the attributed source of potential race-related communication problems (i.e. patient, physician or socioeconomic).

However, dominant themes and patterns emerged within each interview type (in-depth interviews or focus groups) about race and SDM.

Whereas the majority of the in-depth interview participants reported that race did not play an important role in patient/provider communication, participants in the focus groups perceived race as a significant factor in such communication.

Detailed themes that emerged using each methodology are discussed below.


Relevance of Race-The majority of participants in the in-depth interviews (85%) reported that race did not influence patient/provider communication or shared decision-making.

Many participants framed their comments in terms of what should occur in an ideal relationship between patients and their physicians, rather than what actually does occur.


"They are doctors… if they are doctors to take care or soothe whatever the problem is, then it doesn't make a difference who [the patient] is-black or white." ( 80 year old woman with 3 co-morbid illnesses)


None of the participants reported personally experiencing discrimination or other negative race-related encounters, although most acknowledged that they had "heard about such things", either through their own social networks or "the media".


Participants described race-related issues that may affect patient and physician communicating patterns, and be a barrier to active patient involvement in shared decision-making.

Although a range of viewpoints were expressed in both focus groups and in-depth interviews, different themes predominated in these two settings.

Within the in-depth interviews, patients were more likely to report that race does not influence patient/provider communication, and among those stating that race may affect communication, patient factors (e.g. limited health knowledge, "bad attitudes" and internalized racism) were thought to be barriers to SDM.

No one reported experiencing negative race-related communication encounters or discrimination (although many reported hearing about such occurrences), and most believed that their self-efficacy and communication style accounted for their success at shared decision-making.


In contrast, the majority of patients in the focus groups indicated that race does influence patient/physician communication and shared decision-making, and primarily described physician factors (e.g. discrimination and cultural discordance) as the origin of communication disparities.

Within every focus group, participants discussed negative communication encounters between white physicians and themselves, family members and/or close friends that they attributed to race.


The reasons for the difference in the predominance of themes between the focus groups and the in-depth interviews are unclear, but likely reflect an array of complex sociopolitical and interpersonal dynamics.

First, the differential dynamics of one-on-one versus group encounters could have played a significant role (Lewin & Gullickson, 1997).

Despite the use of a race- concordant interviewer and assurances of confidentiality, participants in the in-depth interviews may have felt uncomfortable discussing topics potentially portraying their physician unfavorably, particularly with a researcher affiliated with the health system in which they received their care.

In such settings, participants may have felt more compelled to conform to societal norms about patient perceptions of care (Ajzen & Fishbein, 1980).

In contrast, focus group participants may have felt more anonymous and more empowered, within a group of persons with similar backgrounds, to speak more openly about healthcare experiences, particularly after someone else had "normalized" and validated perceptions of discrimination within the group (Kitzinger, 1994; Morgan, 1995).


Second, our findings may be interpreted in light of Attribution Theory, wherein people explain, or attribute, their own and others' behaviors in ways that help maintain a positive self-image (Bem, 1972).

Persons who have negative experiences are likely to assign external causation (i.e. environmental factors), and persons with positive experiences are likely to assign an internal causation (i.e. personal attributes) (Bem, 1972; Jones & Davis, 1965; Kelley, 1967).

We found that persons who denied having negative communication experiences usually attributed their successful interactions to their own self-efficacy, and often attributed negative communication encounters of others to patient-related factors.

Similarly, persons who reported negative race-related communication experiences (all of which were reported within focus groups) were usually persons who attributed communication disparities externally to physician-related factors such as discrimination.

This external attribution may have been reinforced by group dynamics wherein group norms prohibit the attribution of responsibility to a given member of the group.


Finally, differences in ages between interview and focus group participants may partially explain our findings.

Participants in the focus groups were somewhat younger than those in the in-depth interviews.

Previous studies have shown that African- Americans that grew up during the civil rights era have more racial centrality/group identification than African- Americans born prior to World War II (Jackson, 1987).

Researchers have shown that racial centrality/group identification is positively associated with reports of perceived discrimination, and thus, generational differences may account for some of the higher reporting of negative communication experiences and discrimination within the focus groups (Sellers & Shelton, 2003).


Regardless of the reasons for the differential predominance of themes between the focus groups and the in-depth interviews, our participants identified a range of patient and physician-related factors that may lower the quality of patient/physician communication and be a barrier to shared decision-making between African-American patients and their physicians.

Many participants perceived these race-related communication barriers as being rooted in issues of discrimination, cultural discordance and internalized racism.


In order to fully understand the relationship between race and shared decision-making, it is important to place it within the larger context of race and health within the U.S. Jones developed a framework for understanding how race and racism contribute to health disparities (Jones, 2000).

This framework consists of three levels of racism-institutionalized, personally- mediated, and internalized racism (Jones, 2000).

Institutionalized racism, defined as "differential access to the goods, service and opportunities of society by race" (Jones, 2000), has had manifestations within the field of medicine that include unethical experimentation (Gamble, 1997; Washington, 2006), disparities in healthcare (Hasnain-Wynia, Baker, Nerenz, Feinglass, Beal, Landrum et al., 2007; Schneider, Zaslavsky, & Epstein, 2002; Smedley, Stith, & Nelson, 2002), and unequal access to resources such as health insurance (Doty & Holmgren, 2004; Shi, 2001).

Institutionalized racism affects African-Americans' expectations about the quality of care they will receive from clinicians and health systems (Boulware, Cooper, Ratner, LaVeist, & Powe, 2003; Jacobs, Rolle, Ferrans et al., 2006).

Participants in this study noted It is the other two levels of racism- personally-mediated and internalized- that are particularly relevant to the findings in this study.

Internalized racism, defined as "acceptance by members of the stigmatized race of negative messages about their own abilities and intrinsic worth" (Jones, 2000) was reflected in the in-depth individual interviews, where participants perceived that deficient characteristics of other African-Americans (e.g. not "speaking well" or having limited health knowledge) were the reason for communication disparities and less shared decision-making between African-American patients and their physicians.


In contrast to the in-depth interviews, within the focus groups, personally-mediated racism, defined as "prejudice [differential assumptions about the abilities, motives and intentions of others according to their race] and discrimination [differential actions towards others according to their race]" (Jones, 2000), was a prominent theme, and participants disproportionately attributed communication disparities to physician-related factors such as discrimination.

A growing body of literature documents the use of negative stereotypes about African-American patients by physicians and healthcare disparities that may result from such implicit bias (Bogart, Kelly, Catz, & Sosman, 2000; Finucane & Carrese, 1990; Green, Carney, Pallin, Ngo, Raymond, Iezzoni et al., 2007; Rathore, Lenert, Weinfurt, Tinoco, Taleghani, Harless et al., 2000; van Ryn & Burke, 2000; van Ryn, Hanan, Burke, & Besculides, 1999), and the clinical encounter may create conditions that heighten the use of stereotypes and unconscious bias.

Situations with time pressure, high cognitive demand, limited resources and uncertainty (all found in clinical settings) increase the likelihood of using cognitive shortcuts (e.g. stereotypes) to make decisions (Hamilton, 1981).

The most potent forms of discrimination currently experienced by African-Americans are the subtle and unconscious forms of discrimination experienced regularly (Banks, Kohn-Wood, & Spencer, 2006; Harrell, 2000).


We found that participants primarily discussed race-related communication problems within the context of white physicians, although racially unmatched relationships with foreign-born Asian and Indian physicians were reported as particularly problematic.

No one in our study reported race-related communication barriers (e.g. discrimination) from African-American physicians.

This is an important finding because there is literature suggesting that African- Americans may anticipate and/or report discrimination from same-race physicians in addition to different-race physicians (LaVeist, Rolley, & Diala, 2003; Malat & Hamilton, 2006).

Thus, the lingering vestiges of racism-institutional, internalized and personally-mediated- on both African-Americans and whites, both patients and physicians, may have the potential to influence patient/physician communication and shared decision-making.


Within each SDM domain (information-sharing, deliberation/physician recommendations, and decision- making), participants identified areas in which race may have a negative influence.

Within the information-sharing domain (where patients and physicians discuss symptoms, diagnoses and lifestyle issues), participants felt that African-American patients may be less likely to share information with their providers, particularly about health behaviors and medication usage, and physicians may be less likely to share information with their African- American patients, including important information about patient's illnesses and the results of diagnostic tests.

Participants also noted that physicians may be less likely to actively and patiently listen to African-American patients in comparison to whites.


Our findings are particularly important in light of a previous paper where we reported that information-sharing may be the most important SDM domain to African-Americans, and that the need to "tell their story and be heard" is a crucial experience for this population (Peek, Quinn, Gorawara-Bhat et al., 2008).


This commentary briefly explores the conceptual issues that underlie studies of race and racism in health care.

First, what do we mean by racism in the contemporary medical context?

Second, is there a model of racism that can encompass the range of what is referred to as racism? That is, is it possible to conceptualise everything that is meant by racism, from features of interpersonal communication to population-level inequalities, in a single model? In their article “Race and Shared Decision-Making: Perspectives of African-Americans with Diabetes” Peek et al. ( 2010) explore how patients’ perceptions of race may influence decision-making in a medical context [1].

A model of shared decision-making (‘Information-sharing, Deliberation or Physician recommendation and Decision-making’) is posited as an intervention capable of reducing disparities in disease outcome.

Racialised inequalities in rates of diabetes diagnosis, complication, disease management and quality of outcome are well documented and require urgent remedial attention.

Previous research has shown that methods of shared decision-making do not work as well with minority ethnic patients as with majority ethnic patients [2][3].


Peek et al. explore how Black people in the US with diabetes view the role of race in decision-making about medical care with their doctors, using a combination of in-depth interviews and focus groups.

None of the 24 people who were interviewed reported experiencing any ‘discrimination or other race-related encounters’ and most of them said that race did not play an important role in patient-provider communication [1].

By contrast, in the focus groups people were willing to discuss ‘negative communication encounters between White physicians and themselves, family members and/or close friends that they attributed to race’.

In particular, ‘cultural discordance’ was discussed, whereby White doctors failed to appreciate Black patients’ ways of being and talking.

This failure of communication with White doctors was compared with more satisfactory encounters with African American doctors.

Peek et al. state that in every focus group participants discussed racism at three levels: institutionalized, personally-mediated, and internalized racism [1].

Institutional racism, which the authors see as the least relevant for their study, is defined as ‘differential access to goods and services’ [1].

This definition of institutional racism is problematic because it is subject to what Miles (1989) called ‘conceptual inflation’ [6].

If inequality in access is assumed to be caused by racism, the effects of other forms of discrimination (sexism or class prejudice) are conflated.

If inequality in outcome is an adequate indicator of the operation of racism, we remain ignorant about how it operates.

Where racialised inequality can be measured in health care settings institutional racism is increasingly put forward as a cause.

Since it is rarely defined in detail, the term institutional racism is increasingly employed as a description of inequality that has no clear cause.

One rationale for using the term institutional racism without adequate theoretical justification is to keep the prospect of racism in service provision on the public agenda.

However, without credible models of its operation institutional racism will lose analytic purchase and come to be seen as irrelevant.


Peek et al. ( 2010) suggest that ‘personally-mediated’ and ‘internalized racism’ are more relevant to their findings than institutional racism [1].

A ‘cultural discordance’ whereby Black patients feel that their concerns are not taken seriously by White doctors and a reluctance on the part of Black people to speak up in front of White professionals are encompassed under these headings.

Neither of these features (or failures) of communication constitutes racism in the sense of being discrimination based on a view of humanity as hierarchically divided into differentially valued races.

It is hard to see how the subtle nature of unsatisfactory communication with White doctors, reported by Black people with diabetes, relates to the entrenched racialised inequalities in diabetes outcomes with which the paper by Peek and colleagues opens.

In the study, not only was the dissatisfactory communication reported to be subtle, but discussion of any issues around race was confined to the focus groups, being largely absent from the semi-structured interviews.

The researchers employed ‘race-concordant’ interviewers: one-to-one interviewing is often presented as the best way to develop rapport and generate insight [1].

Nonetheless in this case, it did not generate insights around racism.

Even in the focus groups, where, as Peek et al. describe, there are various reasons why people might be more willing to discuss racism, the talk apparently related more to other people’s experiences than to discussants’ first person encounters.

People at risk of suffering the effects of racism may not wish to discuss it as relevant to their own experience of illness for various reasons and may prefer to emphasize their effective resistance to racism [5].


The relative absence of any talk about racism in this study, the subtle nature of the ‘cultural discordance’ described, stands in contrast with the stark racialised health inequalities around the experience of diabetes and health care for the disease.

The apparent mismatch between the robustly demonstrable population inequities and the difficulties around interpersonal communication with health care staff where discrimination is difficult to measure, should prompt some serious questions.

In particular, how can the conceptual models that link communication around health care to population health outcomes offer causative mechanisms?

Peek et al. ( 2010) suggest that improving the quality of communication between Black patients and White health care staff could be a means of addressing racialised inequity at the population level: how can we envisage or imagine this working? As detailed in Peek and colleagues’ paper, we know that Black patients feel disrespect in the medical encounter to a greater extent than White patients [1].

The paper expands on how Black patients’ dissatisfaction with medical communication might be a matter of racism.

In the stressful conditions of the clinical encounter ‘cognitive shortcuts’ such as stereotypes may be used to facilitate decision-making.

We know from research on medical consultations that patients with educational and class backgrounds most similar to their physicians tend to get the best quality service [10].

Can poorer quality of medical consultations account for poorer health outcomes? Probably not in and of itself, but in the context of long-term socio-economic racialised disadvantage, it is likely to have an effect.

The mechanisms that account for health inequalities that characterize unequal societies [8] may well be responsible for racialised inequalities too.

If a person’s sense of being supported by relationships with others (rather than oppressed by them) is good for health over the life course, then racism would damage health over a life time.

Peek et al. concludes that: all aspects of shared decision-making information-sharing, deliberation/physician recommendations, and decision-making have the potential to be negatively influenced by race, through mechanisms of cultural discordance, patient beliefs arising from internalized racism, unconscious stereotyping/bias (personally-mediated racism).

Such influences serve to exacerbate the inherent power imbalance that exists between patients and their physicians [1].


This paragraph describes aspects of communication that can be seen as racism and as a solution, the authors recommend extending ‘cultural competency training and general communication training for physicians to address potential race-related barriers’ [1].

The communication problems identified include Black patients’ own internalized racism and unconscious racism from physicians, as well as cultural discordance and yet the solution is seen entirely in terms of physician education around race.

This raises some questions: how can physician education address unconscious racism? Should ‘internalized racism’ be tackled through education and if so, whose education? This is familiar but nonetheless paradoxical territory to anyone interested in racism in health care settings: stark racialised inequalities, a sense among patients and their families that racism is relevant to their experience of health care services together with sparse evidence of the occurrence of overt racism.

The great difficulty in identifying specific behaviours, procedures or speech as racist is not surprising given that the public expression of racism is both illegal and largely unacceptable.

The existence of subtle racism has been described by researchers of education [4] and the law [7], but is less well discussed in health research (but see [9]).

How can we, in studies of health and illness, understand the subtle communication problems between White doctors and Black patients alongside entrenched racialised inequalities (in evidence even after controlling for socio-economic status) which have persisted across generations?

Hypothesizing mechanisms that include the micro-processes of interactions between patients and professionals and the macro-processes of population-level inequalities is a missing step in our reasoning at present.

The process of constructing these models is hindered by the ambiguities around what we mean by ‘racism’.


Black patients who encounter disrespect from health care professionals are not explicitly being told that they are an unworthy group because of their skin colour.

The understated nature of the disrespect puts it on a par with the disrespect of other marginalized or stigmatised groups.

However, this disrespect, albeit subtle, must be interpreted in the cultural and social context where Blackness has been denigrated and disparaged both interpersonally and institutionally over time.

The disrespect that has been found in the health care system cannot be interpreted as causing the population-level inequalities, but can be seen as evidence that ‘race’ exists as a category of meaning at the micro- as well as the macro-level.

The re-conceptualisation of racism so it can be operationalised constructively and fairly is a key task for research in this field.

Recasting ideas around racism in a way that is useful for the 21st century represents an urgent and difficult challenge.

The urgency comes from the rootedness of concepts of racism in 19th and 20th century ideas which inform their meaning for both recipients and perpetrators of racism.

Disrespect from White professionals is interpreted in the light of racism that was institutionalized in the twentieth century, but is now illegal.

Historical context is crucial for understanding the experience and perpetuation of racist inequality, but there is also a need to examine how racism works now.

Physicians who contribute to cultural discordance with Black patients are not 19th century-style racists and doubtless know that racism is wrong.

The health-damaging effects of 21st century subtle racism differ dramatically from the operation of 19th century institutionalized segregationist racism.

It is unclear whether training in ‘cultural competency’ is the best means of addressing contemporary racism.

The suggestion that some racist effects take place unconsciously also raises problems for education as the key response to contemporary racism.

How can the further education and training of health care professionals, recommended by Peek et al. ( 2010), work at the level of the unconscious? Are we to consider interventions that tap into our subliminal prejudice? Is this realistic or constructive?

Racism is illegal, but if we are capable of being racist unconsciously, how can it be regulated? If we agree with this paper that some racism in operation is internalized, do Black as well as White health care professionals require their subconscious re-training?

Sociological approaches to racism in health care settings should offer some leads in how best to tackle this problem.

However, our theoretical conceptualisation of racism lacks subtlety.

We have perhaps failed to attend to Miles’s suggestion that we demonstrate the determinate influence of racism through appropriate historical work [6].

While the interpersonal nature of racism has been studied, its sociological and its social nature has not been adequately addressed.

In health care settings we do not have the appropriate empirical or theoretical material to be able to give a convincing account of how subtle racism at the interpersonal level joins up with population-level inequalities.

The painful politics of racism has made this examination difficult: the extremity of racist abuses in the past can distract from sober reflection on the social meaning of contemporary racism.

However, a failure to update our thinking has risks for physicians and patients alike.

Racism is a shared system of knowledge which informs individual beliefs, but also cultural, political, economic and institutional aspects of our social system.

As long as we see the solution to racism lying only in educating the individual, we fail to address the complexity of racism and risk alienating patients and physicians alike.


Bradby’s (2010) critique of our paper ‘Race and Shared Decision-Making: Perspectives of African-Americans with Diabetes’ (Peek at al., 2010) highlights important questions about racism, patient/provider communication and U.S. health disparities.

We address her concerns through the following questions: 1) How can we best conceptualize racism in healthcare? 2) Is there evidence for racism in the current U.S. healthcare system?, 3) How can we disentangle racial discrimination from discrimination based on other social factors?, 4) Is there evidence and/or theoretical model(s) that link institutional racism to population-level health disparities?, 5) Is there evidence and/or theoretical model(s) that link the patient/provider relationship and communication disparities to population-level health disparities?, and 6) Are there potentially effective solutions to address institutional racism, particularly unconscious provider bias?


How can we best conceptualize racism in healthcare?


The Institute of Medicine (IOM), in its landmark report Unequal Treatment: Confronting Racial and Ethnic Disparities in Health Care, identified two causes of healthcare disparities: healthcare systems and discrimination at the patient/provider level (defined as ‘biases, prejudices, stereotyping, and uncertainty in clinical communication and decision-making’) [1].


Within this context, one can consider theoretical models to further define racism and discrimination within healthcare.

We used Camara Jones’ framework because of its widespread use and because it was developed to highlight how racism can lead to health disparities [2].


Jones describes three levels of racism: institutionalized racism, personally-mediated racism and internalized racism.

Institutionalized racism, defined as differential access to goods, services, and opportunities by race, includes differential access to health insurance, which study participants described as a contributing factor to communication disparities between African-Americans and their physicians.


It is important to note that institutional racism does not require personal bias commonly associated with term ‘racism.

’ This type of racism, termed personally-mediated racism, is defined as prejudice (differential assumptions about the abilities, motives, and intentions of others according to their race) and discrimination (differential actions toward others according to their race) [2].


Prejudice and discrimination may manifest as disrespect, poor service and failure to communicate options [2], all of which our study participants described in their experiences within the U.S. healthcare system.


They attributed differential physician assumptions (e.g. “maybe they assumed that she would not understand”) and behaviors (e.g. “they just talk right at the patient because they are black”) specifically to being African-American, indicating participants’ perceived influence of race on patient/physician encounters.


There are two important points to underscore about personally mediated racism.

First, it may occur subconsciously.

Well-meaning individuals may harbor assumptions about people that reflect societal norms.

According to social science theory, everyone uses the strategy of social categorization (e.g. by race or gender) in an attempt to understand, predict and control one’s environment and process new information [3, 4].

Unfortunately, this process can lead to exaggeration of negative inter-group differences (stereotypes) and an over-generalization of them (bias/prejudice) [4, 5].

Second, although discrimination may be subconscious, its impact is powerful.

Racism need not take overt forms of slavery or segregation to have a significant effect.

In fact, the most potent forms of discrimination that African-Americans currently experience are subtle forms experienced chronically [6].


Finally, Jones defines internalized racism as the acceptance by members of stigmatized races of negative messages about their abilities and intrinsic worth [2].

Internalized racism can have many manifestations, including helplessness, self-devaluation, and limiting one’s right to self-determination and self-expression [2].

Our participants reported a decreased ability of African-Americans to question their treatment and speak up to their physicians, and also described devaluing characteristics (e.g. poor physical presentation, not “speaking well”) as potential causes of communication disparities.


The above literature defining racism in healthcare provides a strong theoretical framework for understanding its contribution to health disparities, and corroborates the findings of our study.


Is there evidence for racism in the current U.S. healthcare system?


Indeed, there is evidence that racism exists within the U.S. healthcare system (institutional racism) and among healthcare providers (personally-mediated racism).

The IOM report Unequal Treatment reviewed the disparities literature and concluded that an important contributor to racial disparities in health status is the difference in the quality of medical care given to racial/ethnic minorities [1].

For example, among diabetes patients, African-Americans are less likely to receive influenza vaccinations, have glycosylated hemoglobin (HbA1c) testing or cholesterol testing [7].


Healthcare providers may harbor racial biases (personally mediated racism), and may be at increased risk of using stereotypes as cognitive short-cuts because of clinical encounter characteristics (time pressure, high cognitive demand, limited resources and uncertainty) [3].

There is evidence that physicians hold stereotypes based on patient characteristics (e.g. race), which may influence their interpretation of patient behaviors and symptoms, and consequently their clinical decisions [8, 9].

For example, one study found that physicians were more likely, after controlling for confounding variables, to rate their African-American patients as less educated, less intelligent, more likely to abuse drugs and alcohol, and less likely to adhere to treatment regimens [10].

Green et al. ( 2007) documented the association between implicit physician bias and racial disparities in treatment recommendations for acute myocardial infarctions [11].


While there is no consensus on how to best measure healthcare discrimination [12], most researchers rely upon patient reports of perceived discrimination--a strategy with inherent advantages and disadvantages.

While perceptions may be misinterpreted, they do reflect patients’ personal experiences and how they are internalized, which may be important to how discrimination affects health (see discussion below).

This may be particularly true for patients who lived through U.S. segregation, as their historical healthcare experiences undoubtedly shaped how they currently experience healthcare encounters.

In our study, all but three participants were born before the 1964 Civil Rights Act outlawing U.S. segregation.


There is growing evidence that minorities perceive healthcare discrimination and that such perceptions are associated with important outcomes, such as less preventive healthcare (e.g. cancer screening, dyslipidemia screening, and influenza vaccinations) [13, 14], prescription medication utilization and medical testing/treatment [15].

Among diabetes patients, perceived healthcare discrimination is associated with lower quality physician interactions, and worse diabetes care and outcomes [16, 17, 14].


The above evidence compels us to conclude that racism is embedded within the U.S. healthcare system, at both institutional and personally mediated levels.


How do we disentangle racial discrimination from discrimination based on other social factors?


Racial disparities in healthcare (institutional racism) persist after adjusting for other sociodemographic variables such as gender and class [1].

There has been less research separating personally-mediated racism from other forms of discrimination.

However, in several studies, healthcare discrimination attributed to race (vs. other social factors) was reported most commonly among minorities and associated with worse care and outcomes [14, 17, 18].

For example, in a study of discrimination and diabetes management, perceived racial discrimination was associated with a 50% lower probability of three aspects of diabetes care, while perceived gender discrimination was associated with a 22% lower probability of one aspect of care [17].